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Journal articles on the topic 'Gene structure in plasmodia'

Author: Grafiati

Published: 4 June 2021

Last updated: 5 February 2022

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1

Knapp, Bernhard, Erika Hundt, and Hans A. Küpper. "Plasmodium falciparum aldolase: gene structure and localization." Molecular and Biochemical Parasitology 40, no. 1 (April 1990): 1–12. http://dx.doi.org/10.1016/0166-6851(90)90074-v.

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2

Lal, Altaf A., Vidal F. de la Cruz, Gary H. Campbell, Patricia M. Procell, William E. Collins, and Thomas F. McCutchan. "Structure of the circumsporozoite gene of Plasmodium malariae." Molecular and Biochemical Parasitology 30, no. 3 (September 1988): 291–94. http://dx.doi.org/10.1016/0166-6851(88)90099-0.

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3

Lajoie-Mazenc, I., C. Detraves, V. Rotaru, M. Gares, Y. Tollon, C. Jean, M. Julian, M. Wright, and B. Raynaud-Messina. "A single gamma-tubulin gene and mRNA, but two gamma-tubulin polypeptides differing by their binding to the spindle pole organizing centres." Journal of Cell Science 109, no. 10 (October 1, 1996): 2483–92. http://dx.doi.org/10.1242/jcs.109.10.2483.

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Cells of eukaryotic organisms exhibit microtubules with various functions during the different developmental stages. The identification of multiple forms of alpha- and beta-tubulins had raised the question of their possible physiological roles. In the myxomycete Physarum polycephalum a complex polymorphism for alpha- and beta-tubulins has been correlated with a specific developmental expression pattern. Here, we have investigated the potential heterogeneity of gamma-tubulin in this organism. A single gene, with 3 introns and 4 exons, and a single mRNA coding for gamma-tubulin were detected. They coded for a polypeptide of 454 amino acids, with a predicted molecular mass of 50,674, which presented 64–76% identity with other gamma-tubulins. However, immunological studies identified two gamma-tubulin polypeptides, both present in the two developmental stages of the organism, uninucleate amoebae and multinucleate plasmodia. The two gamma-tubulins, called gamma s- and gamma f-tubulin for slow and fast electrophoretic mobility, exhibited apparent molecular masses of 52,000 and 50,000, respectively. They were recognized by two antibodies (R70 and JH46) raised against two distinct conserved sequences of gamma-tubulins. They were present both in the preparations of amoebal centrosomes possessing two centrioles and in the preparations of plasmodial nuclear metaphases devoid of structurally distinct polar structures. These two gamma-tubulins exhibited different sedimentation properties as shown by ultracentrifugation and sedimentation in sucrose gradients. Moreover, gamma s-tubulin was tightly bound to microtubule organizing centers (MTOCs) while gamma f-tubulin was loosely associated with these structures. This first demonstration of the presence of two gamma-tubulins with distinct properties in the same MTOC suggests a more complex physiological role than previously assumed.

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4

Li, Wu-Bo, David J. Bzik, Toshihiro Horii, and Joseph Inselburg. "Structure and expression of the Plasmodium falciparum SERA gene." Molecular and Biochemical Parasitology 33, no. 1 (February 1989): 13–25. http://dx.doi.org/10.1016/0166-6851(89)90037-6.

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5

Robson, Kathryn J. H., and M. W. Jennings. "The structure of the calmodulin gene of Plasmodium falciparum." Molecular and Biochemical Parasitology 46, no. 1 (May 1991): 19–34. http://dx.doi.org/10.1016/0166-6851(91)90195-c.

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6

Nunes, Alvaro, Vandana Thathy, Thomas Bruderer, Ali A. Sultan, Ruth S. Nussenzweig, and Robert Ménard. "Subtle Mutagenesis by Ends-in Recombination in Malaria Parasites." Molecular and Cellular Biology 19, no. 4 (April 1, 1999): 2895–902. http://dx.doi.org/10.1128/mcb.19.4.2895.

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ABSTRACT The recent advent of gene-targeting techniques in malaria (Plasmodium) parasites provides the means for introducing subtle mutations into their genome. Here, we used the TRAPgene of Plasmodium berghei as a target to test whether an ends-in strategy, i.e., targeting plasmids of the insertion type, may be suitable for subtle mutagenesis. We analyzed the recombinant loci generated by insertion of linear plasmids containing either base-pair substitutions, insertions, or deletions in their targeting sequence. We show that plasmid integration occurs via a double-strand gap repair mechanism. Although sequence heterologies located close (less than 450 bp) to the initial double-strand break (DSB) were often lost during plasmid integration, mutations located 600 bp and farther from the DSB were frequently maintained in the recombinant loci. The short lengths of gene conversion tracts associated with plasmid integration intoTRAP suggests that an ends-in strategy may be widely applicable to modify plasmodial genes and perform structure-function analyses of their important products.

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7

Sharma, Yagya D., and Araxie Kilejian. "Structure of the knob protein (KP) gene of Plasmodium falciparum." Molecular and Biochemical Parasitology 26, no. 1-2 (November 1987): 11–16. http://dx.doi.org/10.1016/0166-6851(87)90124-1.

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8

Schwarz, R. T., V. Riveros-Moreno, M. J. Lockyer, S. C. Nicholls, L. S. Davey, Y. Hillman, J. S. Sandhu, R. R. Freeman, and A. A. Holder. "Structural diversity of the major surface antigen of Plasmodium falciparum merozoites." Molecular and Cellular Biology 6, no. 3 (March 1986): 964–68. http://dx.doi.org/10.1128/mcb.6.3.964.

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The structures of the major merozoite surface antigen of Plasmodium falciparum and the gene encoding it were indistinguishable for the Wellcome strain and the Thai clone T9/94 but different for clones T9/96, T9/98, and T9/101. The central portion of the gene is subject to the greatest variation in structure. The protein from all five lines was found to be posttranslationally modified by covalent addition of both carbohydrate and fatty acid.

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9

Schwarz, R. T., V. Riveros-Moreno, M. J. Lockyer, S. C. Nicholls, L. S. Davey, Y. Hillman, J. S. Sandhu, R. R. Freeman, and A. A. Holder. "Structural diversity of the major surface antigen of Plasmodium falciparum merozoites." Molecular and Cellular Biology 6, no. 3 (March 1986): 964–68. http://dx.doi.org/10.1128/mcb.6.3.964-968.1986.

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The structures of the major merozoite surface antigen of Plasmodium falciparum and the gene encoding it were indistinguishable for the Wellcome strain and the Thai clone T9/94 but different for clones T9/96, T9/98, and T9/101. The central portion of the gene is subject to the greatest variation in structure. The protein from all five lines was found to be posttranslationally modified by covalent addition of both carbohydrate and fatty acid.

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10

Tsuboi, Takafumi, Osamu Kaneko, Chiho Eitoku, Nantavadee Suwanabun, Jetsumon Sattabongkot, Joseph M. Vinetz, and Motomi Torii. "Gene structure and ookinete expression of the chitinase genes of Plasmodium vivax and Plasmodium yoelii." Molecular and Biochemical Parasitology 130, no. 1 (August 2003): 51–54. http://dx.doi.org/10.1016/s0166-6851(03)00140-3.

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11

Triglia, T., and A. F. Cowman. "Primary structure and expression of the dihydropteroate synthetase gene of Plasmodium falciparum." Proceedings of the National Academy of Sciences 91, no. 15 (July 19, 1994): 7149–53. http://dx.doi.org/10.1073/pnas.91.15.7149.

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12

Weber, James L., and Wayne T. Hockmeyer. "Structure of the circumsporozoite protein gene in 18 strains of Plasmodium falciparum." Molecular and Biochemical Parasitology 15, no. 3 (June 1985): 305–16. http://dx.doi.org/10.1016/0166-6851(85)90092-1.

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13

Irving, David O., George A. M. Cross, Roslyn Feder, and Michael Wallach. "Structure and organization of the histidine-rich protein gene of Plasmodium lophurae." Molecular and Biochemical Parasitology 18, no. 2 (February 1986): 223–34. http://dx.doi.org/10.1016/0166-6851(86)90040-x.

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14

Harrison, Thomas E., Adam J. Reid, Deirdre Cunningham, Jean Langhorne, and Matthew K. Higgins. "Structure of the Plasmodium-interspersed repeat proteins of the malaria parasite." Proceedings of the National Academy of Sciences 117, no. 50 (November 30, 2020): 32098–104. http://dx.doi.org/10.1073/pnas.2016775117.

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The deadly symptoms of malaria occur as Plasmodium parasites replicate within blood cells. Members of several variant surface protein families are expressed on infected blood cell surfaces. Of these, the largest and most ubiquitous are the Plasmodium-interspersed repeat (PIR) proteins, with more than 1,000 variants in some genomes. Their functions are mysterious, but differential pir gene expression associates with acute or chronic infection in a mouse malaria model. The membership of the PIR superfamily, and whether the family includes Plasmodium falciparum variant surface proteins, such as RIFINs and STEVORs, is controversial. Here we reveal the structure of the extracellular domain of a PIR from Plasmodium chabaudi. We use structure-guided sequence analysis and molecular modeling to show that this fold is found across PIR proteins from mouse- and human-infective malaria parasites. Moreover, we show that RIFINs and STEVORs are not PIRs. This study provides a structure-guided definition of the PIRs and a molecular framework to understand their evolution.

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15

Day, Karen P., Yael Artzy-Randrup, Kathryn E. Tiedje, Virginie Rougeron, Donald S. Chen, Thomas S. Rask, Mary M. Rorick, et al. "Evidence of strain structure in Plasmodium falciparum var gene repertoires in children from Gabon, West Africa." Proceedings of the National Academy of Sciences 114, no. 20 (May 1, 2017): E4103—E4111. http://dx.doi.org/10.1073/pnas.1613018114.

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Existing theory on competition for hosts between pathogen strains has proposed that immune selection can lead to the maintenance of strain structure consisting of discrete, weakly overlapping antigenic repertoires. This prediction of strain theory has conceptual overlap with fundamental ideas in ecology on niche partitioning and limiting similarity between coexisting species in an ecosystem, which oppose the hypothesis of neutral coexistence. For Plasmodium falciparum, strain theory has been specifically proposed in relation to the major surface antigen of the blood stage, known as PfEMP1 and encoded by the multicopy multigene family known as the var genes. Deep sampling of the DBLα domain of var genes in the local population of Bakoumba, West Africa, was completed to define whether patterns of repertoire overlap support a role of immune selection under the opposing force of high outcrossing, a characteristic of areas of intense malaria transmission. Using a 454 high-throughput sequencing protocol, we report extremely high diversity of the DBLα domain and a large parasite population with DBLα repertoires structured into nonrandom patterns of overlap. Such population structure, significant for the high diversity of var genes that compose it at a local level, supports the existence of “strains” characterized by distinct var gene repertoires. Nonneutral, frequency-dependent competition would be at play and could underlie these patterns. With a computational experiment that simulates an intervention similar to mass drug administration, we argue that the observed repertoire structure matters for the antigenic var diversity of the parasite population remaining after intervention.

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16

Abel, Steven, and Karine G. Le Roch. "The role of epigenetics and chromatin structure in transcriptional regulation in malaria parasites." Briefings in Functional Genomics 18, no. 5 (April 26, 2019): 302–13. http://dx.doi.org/10.1093/bfgp/elz005.

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AbstractDue to the unique selective pressures and extreme changes faced by the human malaria parasite Plasmodium falciparum throughout its life cycle, the parasite has evolved distinct features to alter its gene expression patterns. Along with classical gene regulation by transcription factors (TFs), of which only one family, the AP2 TFs, has been described in the parasite genome, a large body of evidence points toward chromatin structure and epigenetic factors mediating the changes in gene expression associated with parasite life cycle stages. These attributes may be critically important for immune evasion, host cell invasion and development of the parasite in its two hosts, the human and the Anopheles vector. Thus, the factors involved in the maintenance and regulation of chromatin and epigenetic features represent potential targets for antimalarial drugs. In this review, we discuss the mechanisms in P. falciparum that regulate chromatin structure, nucleosome landscape, the 3-dimensional structure of the genome and additional distinctive features created by parasite-specific genes and gene families. We review conserved traits of chromatin in eukaryotes in order to highlight what is unique in the parasite.

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17

Uskov, A. N., A. I. Soloviev, V. Yu Kravtsov, R. V. Gudkov, E. V. Kolomoets, and A. E. Levkovskiy. "MOLECULAR-GENETIC MECHANISMS OF PLASMODIUM FALCIPARUM VIRULENCE AND TROPICAL MALARIA PATHOGENESIS." Journal Infectology 10, no. 3 (October 7, 2018): 23–29. http://dx.doi.org/10.22625/2072-6732-2018-10-3-23-29.

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There is introduced the analysis of molecular-genetic mechanisms of tropical malaria pathogenesis and P. falciparum virulence. It is shown, that pathogenesis of tropical malaria is associated with the properties of red blood cells membrane surface (RBCs or erythrocytes) that are infected by P. falciparum. There are «knobs structures» on membrane surface infected RBCs. Knobs structures contains a complex of P. falciparum proteins – PfEMP1 (Plasmodium falciparum erythrocyte membrane protein 1). PfEMP1 is associated with virulence of P. falciparum. Complex PfEMP1 has difficult polymorphous structure. Domains of PfEMP1 are able to associate with different cell receptors. Virulence`s individual components of the main factor are selectively sensitive to different tissues and organs. The severity of the clinical malaria infection course depends on the complex structure PfEMP1 of malaria parasites. Composition of polypeptide PfEMP1 is determined by var-complex. Nowadays there are 60 variants of var-complex. Regulation of gene expression, forming part of the var-complex, is carried out on a molecular-genetic level, cellular level, tissue level. Modern research in this area are aimed to explore genes polymorphism of the virulence`s main factor, to identify mechanism of its differential expression. Search of molecular – genetic markers is relevant to develop methods of gene diagnostic and malaria vaccine.

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18

Triglia, Tony, Hans-Detlev Stahl, Pauline E. Crewther, Anabel Silva, Robin F. Anders, and David J. Kemp. "Structure of a Plasmodium falciparum gene that encodes a glutamic acid-rich protein (GARP)." Molecular and Biochemical Parasitology 31, no. 2 (November 1988): 199–201. http://dx.doi.org/10.1016/0166-6851(88)90170-3.

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19

van Lin, L. H. M. "Interspecies conservation of gene order and intron-exon structure in a genomic locus of high gene density and complexity in Plasmodium." Nucleic Acids Research 29, no. 10 (May 15, 2001): 2059–68. http://dx.doi.org/10.1093/nar/29.10.2059.

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20

Green, Judith L., and Anthony A. Holder. "Structure of the E8 gene encoding a high molecular mass rhoptry protein of Plasmodium yoelii." Molecular and Biochemical Parasitology 110, no. 1 (September 2000): 167–69. http://dx.doi.org/10.1016/s0166-6851(00)00251-6.

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21

Kaneko, Osamu, Jianbing Mu, Takafumi Tsuboi, Xinzhuan Su, and Motomi Torii. "Gene structure and expression of a Plasmodium falciparum 220-kDa protein homologous to the Plasmodium vivax reticulocyte binding proteins." Molecular and Biochemical Parasitology 121, no. 2 (May 2002): 275–78. http://dx.doi.org/10.1016/s0166-6851(02)00042-7.

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22

Ruiz, José L., and Elena Gómez-Díaz. "The second life of Plasmodium in the mosquito host: gene regulation on the move." Briefings in Functional Genomics 18, no. 5 (May 6, 2019): 313–57. http://dx.doi.org/10.1093/bfgp/elz007.

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Abstract Malaria parasites face dynamically changing environments and strong selective constraints within human and mosquito hosts. To survive such hostile and shifting conditions, Plasmodium switches transcriptional programs during development and has evolved mechanisms to adjust its phenotype through heterogeneous patterns of gene expression. In vitro studies on culture-adapted isolates have served to set the link between chromatin structure and functional gene expression. Yet, experimental evidence is limited to certain stages of the parasite in the vertebrate, i.e. blood, while the precise mechanisms underlying the dynamic regulatory landscapes during development and in the adaptation to within-host conditions remain poorly understood. In this review, we discuss available data on transcriptional and epigenetic regulation in Plasmodium mosquito stages in the context of sporogonic development and phenotypic variation, including both bet-hedging and environmentally triggered direct transcriptional responses. With this, we advocate the mosquito offers an in vivo biological model to investigate the regulatory networks, transcription factors and chromatin-modifying enzymes and their modes of interaction with regulatory sequences, which might be responsible for the plasticity of the Plasmodium genome that dictates stage- and cell type-specific blueprints of gene expression.

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23

Murakami, K., K. Tanabe, and S. Takada. "Structure of a Plasmodium yoelii gene-encoded protein homologous to the Ca(2+)-ATPase of rabbit skeletal muscle sarcoplasmic reticulum." Journal of Cell Science 97, no. 3 (November 1, 1990): 487–95. http://dx.doi.org/10.1242/jcs.97.3.487.

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A cation-transporting ATPase gene of Plasmodium yoelii was cloned from the parasite genomic library using an oligonucleotide probe derived from a conserved amino acid sequence of the phosphorylation domain of the aspartyl phosphate family of ATPases. The complete nucleotide sequence was determined and it predicts a 126,717 Mr encoded protein composed of 1115 amino acids. Northern blot analysis revealed that the gene is transcribed during the asexual stages of parasite development. The P. yoelii protein contains functional and structural features common to the family of aspartyl phosphate cation-transporting ATPases. The parasite protein shows the highest overall homology in amino acid sequence (42%) to the Ca2(+)-ATPase of rabbit skeletal muscle sarcoplasmic reticulum. Homologies to other aspartyl phosphate cation-transporting ATPases including a plasma membrane Ca2(+)-ATPase were between 13 and 24%. The structure predicted from a hydropathy plot also shows 10 transmembrane domains, the number and location of which correlated well with the sarcoplasmic reticulum Ca2(+)-ATPase. On the basis of these results, we conclude that the parasite gene encodes an organellar, but not plasma membrane, Ca2(+)-ATPase. The P. yoelii protein, furthermore, contains all six amino acid residues in the transmembrane domains that were recently identified as comprising a high-affinity Ca2(+)-binding site. It follows that organellar Ca2(+)-ATPases of rabbit and Plasmodium conserve functionally important amino acid residues, even though they are remote from each other phylogenetically.

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24

Florent, Isabelle, Betina M. Porcel, Elodie Guillaume, Corinne Da Silva, François Artiguenave, Eric Maréchal, Laurent Bréhélin, et al. "A Plasmodium falciparum FcB1-schizont-EST collection providing clues to schizont specific gene structure and polymorphism." BMC Genomics 10, no. 1 (2009): 235. http://dx.doi.org/10.1186/1471-2164-10-235.

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25

Colomer-Gould, Veronica, and Vincenzo Enea. "Plasmodium yoelii nigeriensis circumsporozoite gene structure and its implications for the evolution of the repeat regions." Molecular and Biochemical Parasitology 43, no. 1 (November 1990): 51–58. http://dx.doi.org/10.1016/0166-6851(90)90129-a.

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26

Otto, Thomas D., Ulrike Böhme, Mandy Sanders, Adam J. Reid, Ellen I. Bruske, Craig W. Duffy, Pete C. Bull, et al. "Long read assemblies of geographically dispersed Plasmodium falciparum isolates reveal highly structured subtelomeres." Wellcome Open Research 3 (May 3, 2018): 52. http://dx.doi.org/10.12688/wellcomeopenres.14571.1.

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Background: Although thousands of clinical isolates of Plasmodium falciparum are being sequenced and analysed by short read technology, the data do not resolve the highly variable subtelomeric regions of the genomes that contain polymorphic gene families involved in immune evasion and pathogenesis. There is also no current standard definition of the boundaries of these variable subtelomeric regions. Methods: Using long-read sequence data (Pacific Biosciences SMRT technology), we assembled and annotated the genomes of 15 P. falciparum isolates, ten of which are newly cultured clinical isolates. We performed comparative analysis of the entire genome with particular emphasis on the subtelomeric regions and the internal var genes clusters. Results: The nearly complete sequence of these 15 isolates has enabled us to define a highly conserved core genome, to delineate the boundaries of the subtelomeric regions, and to compare these across isolates. We found highly structured variable regions in the genome. Some exported gene families purportedly involved in release of merozoites show copy number variation. As an example of ongoing genome evolution, we found a novel CLAG gene in six isolates. We also found a novel gene that was relatively enriched in the South East Asian isolates compared to those from Africa. Conclusions: These 15 manually curated new reference genome sequences with their nearly complete subtelomeric regions and fully assembled genes are an important new resource for the malaria research community. We report the overall conserved structure and pattern of important gene families and the more clearly defined subtelomeric regions.

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27

CHIANG, Peter K., Margaret E. CHAMBERLIN, Diarmuid NICHOLSON, Sandrine SOUBES, Xin-zhuan SU, Gangadharan SUBRAMANIAN, David E. LANAR, et al. "Molecular characterization of Plasmodium falciparum S-adenosylmethionine synthetase." Biochemical Journal 344, no. 2 (November 24, 1999): 571–76. http://dx.doi.org/10.1042/bj3440571.

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S-Adenosylmethionine (AdoMet) synthetase (SAMS: EC 2.5.1.6) catalyses the formation of AdoMet from methionine and ATP. We have cloned a gene for Plasmodium falciparum AdoMet synthetase (PfSAMS) (GenBank accession no. AF097923), consisting of 1209 base pairs with no introns. The gene encodes a polypeptide (PfSAMS) of 402 amino acids with a molecular mass of 44844 Da, and has an overall base composition of 67% A+T. PfSAMS is probably a single copy gene, and was mapped to chromosome 9. The PfSAMS protein is highly homologous to all other SAMS, including a conserved motif for the phosphate-binding P-loop, HGGGAFSGKD, and the signature hexapeptide, GAGDQG. All the active-site amino acids for the binding of ADP, Pi and metal ions are similarly preserved, matching entirely those of human hepatic SAMS and Escherichia coli SAMS. Molecular modelling of PfSAMS guided by the X-ray crystal structure of E. coli SAMS indicates that PfSAMS binds ATP/Mg2+ in a manner similar to that seen in the E. coli SAMS structure. However, the PfSAMS model shows that it can not form tetramers as does E. coli SAMS, and is probably a dimer instead. There was a differential sensitivity towards the inhibition by cycloleucine between the expressed PfSAMS and the human hepatic SAMS with Ki values of 17 and 10 mM, respectively. Based on phylogenetic analysis using protein parsimony and neighbour-joining algorithms, the malarial PfSAMS is closely related to SAMS of other protozoans and plants.

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28

Dessens, Johannes T., Jacqui Mendoza, Charles Claudianos, Joseph M. Vinetz, Emad Khater, Stuart Hassard, Gaya R. Ranawaka, and Robert E. Sinden. "Knockout of the Rodent Malaria Parasite Chitinase PbCHT1 Reduces Infectivity to Mosquitoes." Infection and Immunity 69, no. 6 (June 1, 2001): 4041–47. http://dx.doi.org/10.1128/iai.69.6.4041-4047.2001.

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ABSTRACT During mosquito transmission, malaria ookinetes must cross a chitin-containing structure known as the peritrophic matrix (PM), which surrounds the infected blood meal in the mosquito midgut. In turn, ookinetes produce multiple chitinase activities presumably aimed at disrupting this physical barrier to allow ookinete invasion of the midgut epithelium. Plasmodium chitinase activities are demonstrated targets for human and avian malaria transmission blockade with the chitinase inhibitor allosamidin. Here, we identify and characterize the first chitinase gene of a rodent malaria parasite,Plasmodium berghei. We show that the gene, namedPbCHT1, is a structural ortholog ofPgCHT1 of the avian malaria parasite Plasmodium gallinaceum and a paralog of PfCHT1 of the human malaria parasite Plasmodium falciparum. Targeted disruption of PbCHT1 reduced parasite infectivity inAnopheles stephensi mosquitoes by up to 90%. Reductions in infectivity were also observed in ookinete feeds—an artificial situation where midgut invasion occurs before PM formation—suggesting that PbCHT1 plays a role other than PM disruption. PbCHT1 null mutants had no residual ookinete-derived chitinase activity in vitro, suggesting that P. berghei ookinetes express only one chitinase gene. Moreover, PbCHT1 activity appeared insensitive to allosamidin inhibition, an observation that raises questions about the use of allosamidin and components like it as potential malaria transmission-blocking drugs. Taken together, these findings suggest a fundamental divergence among rodent, avian, and human malaria parasite chitinases, with implications for the evolution ofPlasmodium-mosquito interactions.

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29

Chalvet, Wanda, Jean-François Pouliquen, and Thierry Fandeur. "Structure of the Knob Protein Gene of the Saimiri Monkey-adapted Palo Alto Strain of Plasmodium falciparum." Memórias do Instituto Oswaldo Cruz 93, no. 2 (March 1998): 243–46. http://dx.doi.org/10.1590/s0074-02761998000200021.

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30

Gibson, Helen L., Jeffrey E. Tucker, David C. Kaslow, Antoniana U. Krettli, William E. Collins, Michael C. Kiefer, Ian C. Bathurst, and Philip J. Barr. "Structure and expression of the gene for Pv200, a major blood-stage surface antigen of Plasmodium vivax." Molecular and Biochemical Parasitology 50, no. 2 (February 1992): 325–33. http://dx.doi.org/10.1016/0166-6851(92)90230-h.

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31

Assefa, Samuel, Caeul Lim, Mark D. Preston, Craig W. Duffy, Mridul B. Nair, Sabir A. Adroub, Khamisah A. Kadir, et al. "Population genomic structure and adaptation in the zoonotic malaria parasite Plasmodium knowlesi." Proceedings of the National Academy of Sciences 112, no. 42 (October 5, 2015): 13027–32. http://dx.doi.org/10.1073/pnas.1509534112.

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Malaria cases caused by the zoonotic parasite Plasmodium knowlesi are being increasingly reported throughout Southeast Asia and in travelers returning from the region. To test for evidence of signatures of selection or unusual population structure in this parasite, we surveyed genome sequence diversity in 48 clinical isolates recently sampled from Malaysian Borneo and in five lines maintained in laboratory rhesus macaques after isolation in the 1960s from Peninsular Malaysia and the Philippines. Overall genomewide nucleotide diversity (π = 6.03 × 10−3) was much higher than has been seen in worldwide samples of either of the major endemic malaria parasite species Plasmodium falciparum and Plasmodium vivax. A remarkable substructure is revealed within P. knowlesi, consisting of two major sympatric clusters of the clinical isolates and a third cluster comprising the laboratory isolates. There was deep differentiation between the two clusters of clinical isolates [mean genomewide fixation index (FST) = 0.21, with 9,293 SNPs having fixed differences of FST = 1.0]. This differentiation showed marked heterogeneity across the genome, with mean FST values of different chromosomes ranging from 0.08 to 0.34 and with further significant variation across regions within several chromosomes. Analysis of the largest cluster (cluster 1, 38 isolates) indicated long-term population growth, with negatively skewed allele frequency distributions (genomewide average Tajima’s D = −1.35). Against this background there was evidence of balancing selection on particular genes, including the circumsporozoite protein (csp) gene, which had the top Tajima’s D value (1.57), and scans of haplotype homozygosity implicate several genomic regions as being under recent positive selection.

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32

Pologe, L. G., D. de Bruin, and J. V. Ravetch. "A and T homopolymeric stretches mediate a DNA inversion in Plasmodium falciparum which results in loss of gene expression." Molecular and Cellular Biology 10, no. 6 (June 1990): 3243–46. http://dx.doi.org/10.1128/mcb.10.6.3243.

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Ring-infected erythrocyte surface antigen-negative isolates of Plasmodium falciparum demonstrate a complex DNA rearrangement with inversion of 5' coding sequences, deletion of upstream and flanking sequences, and healing of the truncated chromosome by telomere addition. An inversion intermediate that results in the telomeric gene structure for RESA has been identified in the pathway. This inversion creates a mitotically stable substrate for the sequence-specific addition of telomere repeats at the deletion breakpoint.

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Pologe, L. G., D. de Bruin, and J. V. Ravetch. "A and T homopolymeric stretches mediate a DNA inversion in Plasmodium falciparum which results in loss of gene expression." Molecular and Cellular Biology 10, no. 6 (June 1990): 3243–46. http://dx.doi.org/10.1128/mcb.10.6.3243-3246.1990.

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Ring-infected erythrocyte surface antigen-negative isolates of Plasmodium falciparum demonstrate a complex DNA rearrangement with inversion of 5' coding sequences, deletion of upstream and flanking sequences, and healing of the truncated chromosome by telomere addition. An inversion intermediate that results in the telomeric gene structure for RESA has been identified in the pathway. This inversion creates a mitotically stable substrate for the sequence-specific addition of telomere repeats at the deletion breakpoint.

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Alano, Pietro, Francesco Silvestrini, and Lucia Roca. "Structure and polymorphism of the upstream region of the pfg2725 gene, transcriptionally regulated in gametocytogenesis of Plasmodium falciparum." Molecular and Biochemical Parasitology 79, no. 2 (August 1996): 207–17. http://dx.doi.org/10.1016/0166-6851(96)02663-1.

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Koussis, Konstantinos, Chrislaine Withers-Martinez, David A. Baker, and Michael J. Blackman. "Simultaneous multiple allelic replacement in the malaria parasite enables dissection of PKG function." Life Science Alliance 3, no. 4 (March 16, 2020): e201900626. http://dx.doi.org/10.26508/lsa.201900626.

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Over recent years, a plethora of new genetic tools has transformed conditional engineering of the malaria parasite genome, allowing functional dissection of essential genes in the asexual and sexual blood stages that cause pathology or are required for disease transmission, respectively. Important challenges remain, including the desirability to complement conditional mutants with a correctly regulated second gene copy to confirm that observed phenotypes are due solely to loss of gene function and to analyse structure–function relationships. To meet this challenge, here we combine the dimerisable Cre (DiCre) system with the use of multiple lox sites to simultaneously generate multiple recombination events of the same gene. We focused on the Plasmodium falciparum cGMP-dependent protein kinase (PKG), creating in parallel conditional disruption of the gene plus up to two allelic replacements. We use the approach to demonstrate that PKG has no scaffolding or adaptor role in intraerythrocytic development, acting solely at merozoite egress. We also show that a phosphorylation-deficient PKG is functionally incompetent. Our method provides valuable new tools for analysis of gene function in the malaria parasite.

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Lal, A. A., V. F. de la Cruz, J. A. Welsh, Y. Charoenvit, W. L. Maloy, and T. F. McCutchan. "Structure of the gene encoding the circumsporozoite protein of Plasmodium yoelii. A rodent model for examining antimalarial sporozoite vaccines." Journal of Biological Chemistry 262, no. 7 (March 1987): 2937–40. http://dx.doi.org/10.1016/s0021-9258(18)61449-8.

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Sperança, Márcia A., Rinke Vinkenoog, Maristela Ocampos, Katja Fischer, Chris J. Janse, Andrew P. Waters, and Hernando A. del Portillo. "Primary Structure of the Plasmodium vivax crk2 Gene and Interference of the Yeast Cell Cycle upon Its Conditional Expression." Experimental Parasitology 97, no. 3 (March 2001): 119–28. http://dx.doi.org/10.1006/expr.2001.4596.

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Wang, S., and K. Takeyasu. "Primary structure and evolution of the ATP-binding domains of the P-type ATPases in Tetrahymena thermophila." American Journal of Physiology-Cell Physiology 272, no. 2 (February 1, 1997): C715—C728. http://dx.doi.org/10.1152/ajpcell.1997.272.2.c715.

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The P-type ATPases (e.g., Na+-K+-ATPase and Ca2+-ATPase) occur widely in living cells of fungi, Protozoa, plants, and animals. These ion pumps show a high degree of divergence in their primary structures but share a limited number of common amino acid residues for their ATP-catalytic function. Particularly, the amino acid sequences for the phosphorylation site (DKTGTLT) and the binding site for ATP (and its analogs; GDGVND) are conserved throughout evolution. Using two degenerate oligonucleotides corresponding to these regions, we applied a polymerase chain reaction (PCR) technique to the search for P-type ATPase isoforms, which will provide a clue to the evolutionary mechanisms of ion pumps in Tetrahymena thermophila. A total of 12 distinct P-type ATPase genes were identified. Sequence comparisons revealed that seven of them can be compiled into a multigene family, which is similar to animal Na+-K+- and H+-K+-ATPase genes. One of them is close to the sarco(endo)plasmic reticulum Ca2+-ATPase gene, and the other four share a significant homology with the gene encoding Plasmodium ATPase-1 whose function is unknown. A Northern blot analysis and reverse transcriptase-PCR demonstrated that all identified genes are expressed, but the expression levels vary widely under different culture conditions. A Southern blot analysis after pulse-field gel electrophoresis showed that all of these genes exist in T. thermophila macronuclei. The Na+-K+- and H+-K+-ATPase gene family has a high multiplicity (at least 10 different genes detected on genomic Southern blot analysis) and is distributed on four different macronuclear chromosomes. On the basis of a calculation with the amino acid sequences of the cloned cytoplasmic loop region (between the phosphorylation and the gamma-[4-(N-2-chloroethyl-N-methylamino)]-benzylamido ATP sites), the genes with >80% identity form a cognate linkage group within the same macronuclei chromosome, whereas the genes with <70% identity are separated in different chromosomes. The phylogenetic analysis showed that this multigene family is the result of a series of gene duplications.

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Otto, Thomas D., Sammy A. Assefa, Ulrike Böhme, Mandy J. Sanders, Dominic Kwiatkowski, Matt Berriman, and Chris Newbold. "Evolutionary analysis of the most polymorphic gene family in falciparum malaria." Wellcome Open Research 4 (December 3, 2019): 193. http://dx.doi.org/10.12688/wellcomeopenres.15590.1.

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The var gene family of the human malaria parasite Plasmodium falciparum encode proteins that are crucial determinants of both pathogenesis and immune evasion and are highly polymorphic. Here we have assembled nearly complete var gene repertoires from 2398 field isolates and analysed a normalised set of 714 from across 12 countries. This therefore represents the first large scale attempt to catalogue the worldwide distribution of var gene sequences We confirm the extreme polymorphism of this gene family but also demonstrate an unexpected level of sequence sharing both within and between continents. We show that this is likely due to both the remnants of selective sweeps as well as a worrying degree of recent gene flow across continents with implications for the spread of drug resistance. We also address the evolution of the var repertoire with respect to the ancestral genes within the Laverania and show that diversity generated by recombination is concentrated in a number of hotspots. An analysis of the subdomain structure indicates that some existing definitions may need to be revised From the analysis of this data, we can now understand the way in which the family has evolved and how the diversity is continuously being generated. Finally, we demonstrate that because the genes are distributed across the genome, sequence sharing between genotypes acts as a useful population genetic marker.

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Chang, Sandra P., Kenton J. Kramer, Karen M. Yamaga, Ann Kato, Stephen E. Case, and Wasim A. Siddiqui. "Plasmodium falciparum: Gene structure and hydropathy profile of the major merozoite surface antigen (gp195) of the Uganda-Palo Alto isolate." Experimental Parasitology 67, no. 1 (October 1988): 1–11. http://dx.doi.org/10.1016/0014-4894(88)90002-1.

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Ravindra, Gudihal, and Padmanabhan Balaram. "Plasmodium falciparum triosephosphate isomerase: New insights into an old enzyme." Pure and Applied Chemistry 77, no. 1 (January 1, 2005): 281–89. http://dx.doi.org/10.1351/pac200577010281.

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Triosephosphate isomerase (TIM), a central enzyme in the glycolytic pathway, has been the subject of extensive structural and mechanistic investigations over the past 30 years. The TIM barrel is the prototype of the (β/α)8 barrel fold, which is one of the most extensively used structural motifs in enzymes. Mechanistic studies on TIM from a variety of sources have emphasized the importance of loop 6 dynamics for enzyme activity. Several conserved residues in TIM have been investigated by extensive site-directed mutagenesis of the enzyme from yeast, chicken, and trypanosoma. The cloning and sequencing of the TIM gene from the malarial parasite Plasmodium falciparum in 1993 revealed the unexpected mutation of a hitherto conserved residue serine (S96) to phenylalanine (F96). Subsequent results from the genome sequencing programs of Plasmodium falciparum, Plasmodium vivax, and Plasmodium yoelii confirmed the presence of the S96F mutation in malarial parasites. The crystal structure of PfTIM and several inhibitor complexes, including a high-resolution (1.1 Å) structure of the PfTIM 2-phosphoglycerate complex, revealed that loop 6 had a propensity to remain open, even in several ligand bound structures. Furthermore, both open and closed forms could be characterized for the same complex. Since glycolysis is the primary source of ATP for the malarial parasite during the intraerythrocytic stage, glycolytic enzymes present themselves as potential targets for inhibitors. Two distinct approaches have been explored. The use of dimer interface peptides, which interfere with assembly, has proved promising. Inactivation of the enzyme by modification of a cysteine (C13) residue, which lies close to the active site residue, lysine (K12) is another potential strategy. The differential reactivity, of the four-cysteine residues, at positions 13, 126, 196, and 217 in each subunit has been established using electrospray ionization mass spectrometry. Studies of single tryptophan mutants (W11F and W168F) of PfTIM provide a probe to study folding, stability, and inhibitor interactions.

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Tarr, Sarah J., Chrislaine Withers-Martinez, Helen R. Flynn, Ambrosius P. Snijders, Laura Masino, Konstantinos Koussis, David J. Conway, and Michael J. Blackman. "A malaria parasite subtilisin propeptide-like protein is a potent inhibitor of the egress protease SUB1." Biochemical Journal 477, no. 2 (January 31, 2020): 525–40. http://dx.doi.org/10.1042/bcj20190918.

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Subtilisin-like serine peptidases (subtilases) play important roles in the life cycle of many organisms, including the protozoan parasites that are the causative agent of malaria, Plasmodium spp. As with other peptidases, subtilase proteolytic activity has to be tightly regulated in order to prevent potentially deleterious uncontrolled protein degradation. Maturation of most subtilases requires the presence of an N-terminal propeptide that facilitates folding of the catalytic domain. Following its proteolytic cleavage, the propeptide acts as a transient, tightly bound inhibitor until its eventual complete removal to generate active protease. Here we report the identification of a stand-alone malaria parasite propeptide-like protein, called SUB1-ProM, encoded by a conserved gene that lies in a highly syntenic locus adjacent to three of the four subtilisin-like genes in the Plasmodium genome. Template-based modelling and ab initio structure prediction showed that the SUB1-ProM core structure is most similar to the X-ray crystal structure of the propeptide of SUB1, an essential parasite subtilase that is discharged into the parasitophorous vacuole (PV) to trigger parasite release (egress) from infected host cells. Recombinant Plasmodium falciparum SUB1-ProM was found to be a fast-binding, potent inhibitor of P. falciparum SUB1, but not of the only other essential blood-stage parasite subtilase, SUB2, or of other proteases examined. Mass-spectrometry and immunofluorescence showed that SUB1-ProM is expressed in the PV of blood stage P. falciparum, where it may act as an endogenous inhibitor to regulate SUB1 activity in the parasite.

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Swamy, Lakshmi, Borko Amulic, and Kirk W. Deitsch. "Plasmodium falciparum var Gene Silencing Is Determined by cis DNA Elements That Form Stable and Heritable Interactions." Eukaryotic Cell 10, no. 4 (February 11, 2011): 530–39. http://dx.doi.org/10.1128/ec.00329-10.

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ABSTRACT Antigenic variation in the human malaria parasite Plasmodium falciparum depends on the transcriptional regulation of the var gene family. In each individual parasite, mRNA is expressed exclusively from 1 var gene out of ∼60, while the rest of the genes are transcriptionally silenced. Both modifications to chromatin structure and DNA regulatory elements associated with each var gene have been implicated in the organization and maintenance of the silent state. Whether silencing is established at the level of entire chromosomal regions via heterochromatin spreading or at the level of individual var promoters through the action of a silencing element within each var intron has been debated. Here, we consider both possibilities, using clonal parasite lines carrying chromosomally integrated transgenes. We confirm a previous finding that the loss of an adjacent var intron results in var promoter activation and further show that transcriptional activation of a var promoter within a cluster does not affect the transcriptional activity of neighboring var promoters. Our results provide more evidence for the hypothesis that var genes are primarily silenced at the level of an individual gene, rather than by heterochromatin spreading. We also tested the intrinsic directionality of an intron's silencing effect on upstream or downstream var promoters. We found that an intron is capable of silencing in either direction and that, once established, a var promoter-intron pair is stably maintained through many generations, suggesting a possible role in epigenetic memory. This study provides insights into the regulation of endogenous var gene clusters.

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Kimura, M., Y. Yamaguchi, S. Takada, and K. Tanabe. "Cloning of a Ca(2+)-ATPase gene of Plasmodium falciparum and comparison with vertebrate Ca(2+)-ATPases." Journal of Cell Science 104, no. 4 (April 1, 1993): 1129–36. http://dx.doi.org/10.1242/jcs.104.4.1129.

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A Ca(2+)-ATPase gene was cloned from the genomic libraries of Plasmodium falciparum. From the deduced amino acid sequence of the gene, a 139 kDa protein with a total of 1228 amino acids was predicted. Sequence of a partial cDNA clone of the gene identified two introns near the 3′-end at the regions identical to the regions assumed for the Ca(2+)-ATPase gene of P. yoelii, a rodent malaria species. As compared with a variety of Ca(2+)-ATPases, the P. falciparum Ca(2+)-ATPase had the highest amino acid sequence homology (78%) to the P. yoelii Ca(2+)-ATPase, moderate homology (45-50%) to vertebrate sarcoplasmic/endoplasmic reticulum Ca(2+)-ATPases (SERCAs), and lowest homology (20%) to a plasma membrane Ca(2+)-ATPase. The P. falciparum protein conserved sequences and residues that are important for the function and/or structure of the organellar type Ca(2+)-ATPase, such as high affinity Ca(2+)-binding sites, fluorescein isothiocyanate (FITC)-binding regions, and the phosphorylation site, but the protein did not contain calmodulin-binding regions that occur in the plasma membrane type Ca(2+)-ATPase. Thus we concluded the cloned gene was the organellar type Ca(2+)-ATPase of P. falciparum. In a region between the phosphorylation site and FITC-binding region, the P. falciparum protein was about 200 residues longer than the rabbit SERCA and lacked a sequence that binds to phospholamban, a protein that regulates the activity of the rabbit SERCA.(ABSTRACT TRUNCATED AT 250 WORDS)

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FECCHIO, ALAN, MARCOS ROBALINHO LIMA, MARIA SVENSSON-COELHO, MIGUEL ÂNGELO MARINI, and ROBERT E. RICKLEFS. "Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil." Parasitology 140, no. 2 (September 3, 2012): 181–92. http://dx.doi.org/10.1017/s0031182012001412.

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SUMMARYStudies on avian haemosporidia are on the rise, but we still lack a basic understanding of how ecological and evolutionary factors mold the distributions of haemosporidia among species in the same bird community. We studied the structure and organization of a local avian haemosporidian assemblage (genera Plasmodium and Haemoproteus) in the Cerrado biome of Central Brazil for 5 years. We obtained 790 blood samples from 54 bird species of which 166 (21%) were infected with haemosporidians based on molecular diagnostics. Partial sequences of the parasite cytochrome b gene revealed 18 differentiated avian haemosporidian lineages. We also analysed the relationship of life-history traits (i.e., nesting height, migration status, nest type, sociality, body mass, and embryo development period) of the 14 most abundant bird species with the prevalence of avian haemosporidia. It was found that host species that bred socially presented a higher prevalence of Haemoproteus (Parahaemoproteus) than bird species that bred in pairs. Thus, aspects of host behaviour could be responsible for differential exposure to vectors. The assemblage of avian haemosporidia studied here also confirms a pattern that is emerging in recent studies using molecular markers to identify avian haemosporidians, namely that many lineages are host generalists.

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Paton, Michael G., Guy C. Barker, Hiroyuki Matsuoka, Jai Ramesar, Chris J. Janse, Andy P. Waters, and Robert E. Sinden. "Structure and expression of a post-transcriptionally regulated malaria gene encoding a surface protein from the sexual stages of Plasmodium berghei." Molecular and Biochemical Parasitology 59, no. 2 (June 1993): 263–75. http://dx.doi.org/10.1016/0166-6851(93)90224-l.

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Zakeri, Sedigheh, Hengameh Sadeghi, Akram Abouie Mehrizi, and Navid Dinparast Djadid. "Population genetic structure and polymorphism analysis of gene encoding apical membrane antigen-1 (AMA-1) of Iranian Plasmodium vivax wild isolates." Acta Tropica 126, no. 3 (June 2013): 269–79. http://dx.doi.org/10.1016/j.actatropica.2013.02.017.

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Hernandez-Rivas, R., D. Mattei, Y. Sterkers, D. S. Peterson, T. E. Wellems, and A. Scherf. "Expressed var genes are found in Plasmodium falciparum subtelomeric regions." Molecular and Cellular Biology 17, no. 2 (February 1997): 604–11. http://dx.doi.org/10.1128/mcb.17.2.604.

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The antigenic variation and cytoadherence of Plasmodium falciparum-infected erythrocytes are modulated by a family of variant surface proteins encoded by the var multigene family. The var genes occur on multiple chromosomes, often in clusters, and 50 to 150 genes are estimated to be present in the haploid parasite genome. Transcripts from var genes have been previously mapped to internal chromosome positions, but the generality of such assignments and the expression sites and mechanisms that control switches of var gene expression are still in early stages of investigation. Here we describe investigations of closely related var genes that occur in association with repetitive elements near the telomeres of P. falciparum chromosomes. DNA sequence analysis of one of these genes (FCR3-varT11-1) shows the characteristic two-exon structure encoding expected var features, including three variable Duffy binding-like (DBL) domains, a transmembrane sequence, and a carboxy-terminal segment thought to anchor the protein product in knobs at the surface of the parasitized erythrocyte. FCR3-varT11-1 cross-hybridizes with var genes located close to the telomeres of many other P. falciparum chromosomes, including a transcribed gene (FCR3-varT3-1) in chromosome 3 of the P. falciparum FCR3 line. The relatively high level transcription from this gene shows that the polymorphic chromosome ends of P. falciparum, which have been proposed to be transcriptionally silent, can be active expression sites for var genes. The pattern of the FCR3-varT11-1 and FCR3-varT3-1 genes are variable between different P. falciparum lines, presumably due to DNA rearrangements. Thus, recombination events in subtelomeric DNA may have a role in the expression of novel var forms.

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Gupta, Ashish, Parul Mehra, Abhijeet Deshmukh, Ashraf Dar, Pallabi Mitra, Nilanjan Roy, and Suman Kumar Dhar. "Functional Dissection of the Catalytic Carboxyl-Terminal Domain of Origin Recognition Complex Subunit 1 (PfORC1) of the Human Malaria Parasite Plasmodium falciparum." Eukaryotic Cell 8, no. 9 (July 24, 2009): 1341–51. http://dx.doi.org/10.1128/ec.00170-09.

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ABSTRACT Origin recognition complex subunit 1 (ORC1) is essential for DNA replication in eukaryotes. The deadly human malaria parasite Plasmodium falciparum contains an ORC1/CDC6 homolog with several interesting domains at the catalytic carboxyl-terminal region that include a putative nucleoside triphosphate-binding and hydrolysis domain, a putative PCNA-interacting-protein (PIP) motif, and an extreme C-terminal region that shows poor homology with other ORC1 homologs. Due to the unavailability of a dependable inducible gene expression system, it is difficult to study the structure and function of essential genes in Plasmodium. Using a genetic yeast complementation system and biochemical experiments, here we show that the putative PIP domain in ORC1 that facilitates in vitro physical interaction with PCNA is functional in both yeast (Saccharomyces cerevisiae) and Plasmodium in vivo, confirming its essential biological role in eukaryotes. Furthermore, despite having less sequence homology, the extreme C-terminal region can be swapped between S. cerevisiae and P. falciparum and it binds to DNA directly, suggesting a conserved role of this region in DNA replication. These results not only provide us a useful system to study the function of the essential genes in Plasmodium, they help us to identify the previously undiscovered unique features of replication proteins in general.

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Ghedira, Kais, Yosr Hamdi, Abir El Béji, and Houcemeddine Othman. "An Integrative Computational Approach for the Prediction of Human-Plasmodium Protein-Protein Interactions." BioMed Research International 2020 (December 19, 2020): 1–11. http://dx.doi.org/10.1155/2020/2082540.

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Host-pathogen molecular cross-talks are critical in determining the pathophysiology of a specific infection. Most of these cross-talks are mediated via protein-protein interactions between the host and the pathogen (HP-PPI). Thus, it is essential to know how some pathogens interact with their hosts to understand the mechanism of infections. Malaria is a life-threatening disease caused by an obligate intracellular parasite belonging to the Plasmodium genus, of which P. falciparum is the most prevalent. Several previous studies predicted human-plasmodium protein-protein interactions using computational methods have demonstrated their utility, accuracy, and efficiency to identify the interacting partners and therefore complementing experimental efforts to characterize host-pathogen interaction networks. To predict potential putative HP-PPIs, we use an integrative computational approach based on the combination of multiple OMICS-based methods including human red blood cells (RBC) and Plasmodium falciparum 3D7 strain expressed proteins, domain-domain based PPI, similarity of gene ontology terms, structure similarity method homology identification, and machine learning prediction. Our results reported a set of 716 protein interactions involving 302 human proteins and 130 Plasmodium proteins. This work provides a list of potential human-Plasmodium interacting proteins. These findings will contribute to better understand the mechanisms underlying the molecular determinism of malaria disease and potentially to identify candidate pharmacological targets.

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