Inferring Developmental Stage Composition from Gene Expression in Human Malaria

PLoS Computational Biology

Volumn 9, Issue 12, 2013, Pages

  Joice, Regina ^a   Narasimhan, Vagheesh ^a   Montgomery, Jacqui ^b,c   Sidhu, Amar Bir ^d   Oh, Keunyoung ^a   Meyer, Evan ^a   Pierre Louis, Willythssa ^a   Seydel, Karl ^e,f   Milner, Danny ^a,g   Williamson, Kim ^h   Wiegand, Roger ^d   Ndiaye, Daouda ⁱ   Daily, Johanna ^a,j   Wirth, Dyann ^a,d   Taylor, Terrie ^e,f   Huttenhower, Curtis ^a,d   Marti, Matthias ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b MALAWI LIVERPOOL WELLCOME TRUST CLINICAL RESEARCH PROGRAMME   (Malawi)

^c LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

^f UNIVERSITY OF MALAWI   (Malawi)

^g BRIGHAM AND WOMEN S HOSPITAL   (United States)

^h LOYOLA UNIVERSITY CHICAGO   (United States)

ⁱ UNIVERSITÉ CHEIKH ANTA DIOP   (Senegal)

^j ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DISEASES; DRUG THERAPY; GENE EXPRESSION;

'CURRENT; DEVELOPMENTAL STAGE; EXPRESSION MEASUREMENTS; EXPRESSION PROFILE; GENE SET ENRICHMENT ANALYSIS; GENES EXPRESSION; MALARIA PARASITE; PLASMODIUM FALCIPARUM; QUANTITATIVE RT-PCR; SEXUAL STAGES;

MICROARRAYS;

ALPHA BETA HYDROLASE; ARTEMISININ; BINDING PROTEIN; CONSERVED PLASMODIUM PROTEIN; HYDROLASE; PLASMODIUM EXPORTED PROTEIN; SKELETON BINDING PROTEIN 1; UNCLASSIFIED DRUG;

ADOLESCENT; ARTICLE; ASEXUAL REPRODUCTION; CHILD; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DISEASE TRANSMISSION; FEMALE; GAMETOCYTE; GENE EXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIMIT OF DETECTION; LIPID METABOLISM; MAJOR CLINICAL STUDY; MALARIA; MALE; MICROARRAY ANALYSIS; MITOCHONDRION; NONHUMAN; PARASITEMIA; PLASMODIUM (LIFE CYCLE STAGE); PLASMODIUM FALCIPARUM; QUANTITATIVE ANALYSIS; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BIOLOGICAL MARKERS; GENE EXPRESSION; HUMANS; MALARIA, FALCIPARUM; MODELS, BIOLOGICAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; REAL-TIME POLYMERASE CHAIN REACTION; SELECTION, GENETIC;

EID: 84892741523     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003392     Document Type: Article

References (46)

1. Alonso PL, Brown G, Arevalo-Herrera M, Binka F, Chitnis C, et al. A research agenda to underpin malaria eradication. PLoS Med 8: e1000406.
2. Alano P, (2007) Plasmodium falciparum gametocytes: still many secrets of a hidden life. Mol Microbiol 66: 291-302.
3. Young JA, Fivelman QL, Blair PL, de la Vega P, Le Roch KG, et al. (2005) The Plasmodium falciparum sexual development transcriptome: a microarray analysis using ontology-based pattern identification. Mol Biochem Parasitol 143: 67-79.
4. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, et al. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1: E5.
5. Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, et al. (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301: 1503-1508.
6. Eksi S, Haile Y, Furuya T, Ma L, Su X, et al. (2005) Identification of a subtelomeric gene family expressed during the asexual-sexual stage transition in Plasmodium falciparum. Mol Biochem Parasitol 143: 90-99.
7. Niederwieser I, Felger I, Beck HP, (2000) Plasmodium falciparum: expression of gametocyte-specific genes in monolayer cultures and malaria-positive blood samples. Experimental parasitology 95: 163-169.
8. Schneider P, Schoone G, Schallig H, Verhage D, Telgt D, et al. (2004) Quantification of Plasmodium falciparum gametocytes in differential stages of development by quantitative nucleic acid sequence-based amplification. Mol Biochem Parasitol 137: 35-41.
9. Buates S, Bantuchai S, Sattabongkot J, Han ET, Tsuboi T, et al. Development of a reverse transcription-loop-mediated isothermal amplification (RT-LAMP) for clinical detection of Plasmodium falciparum gametocytes. Parasitol Int 59: 414-420.
10. Clarke J, Seo P, Clarke B, Statistical expression deconvolution from mixed tissue samples. Bioinformatics 26: 1043-1049.
11. Stuart RO, Wachsman W, Berry CC, Wang-Rodriguez J, Wasserman L, et al. (2004) In silico dissection of cell-type-associated patterns of gene expression in prostate cancer. Proc Natl Acad Sci U S A 101: 615-620.
12. Paul RE, Bonnet S, Boudin C, Tchuinkam T, Robert V, (2007) Age-structured gametocyte allocation links immunity to epidemiology in malaria parasites. Malaria journal 6: 123.
13. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature genetics 25: 25-29.
14. Silvestrini F, Lasonder E, Olivieri A, Camarda G, van Schaijk B, et al. (2010) Protein export marks the early phase of gametocytogenesis of the human malaria parasite Plasmodium falciparum. Mol Cell Proteomics 9: 1437-1448.
15. Van Tyne D, Park DJ, Schaffner SF, Neafsey DE, Angelino E, et al. (2011) Identification and Functional Validation of the Novel Antimalarial Resistance Locus PF10_0355 in Plasmodium falciparum. PLoS Genet 7: e1001383.
16. Neafsey DE, Schaffner SF, Volkman SK, Park D, Montgomery P, et al. (2008) Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol 9: R171.
17. Walliker D, Quakyi IA, Wellems TE, McCutchan TF, Szarfman A, et al. (1987) Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236: 1661-1666.
18. Florens L, Washburn MP, Raine JD, Anthony RM, Grainger M, et al. (2002) A proteomic view of the Plasmodium falciparum life cycle. Nature 419: 520-526.
19. Blisnick T, Morales Betoulle ME, Barale JC, Uzureau P, Berry L, et al. (2000) Pfsbp1, a Maurer's cleft Plasmodium falciparum protein, is associated with the erythrocyte skeleton. Mol Biochem Parasitol 111: 107-121.
20. Sargeant TJ, Marti M, Caler E, Carlton JM, Simpson K, et al. (2006) Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol 7: R12.
21. Daily JP, Scanfeld D, Pochet N, Le Roch K, Plouffe D, et al. (2007) Distinct physiological states of Plasmodium falciparum in malaria-infected patients. Nature 450: 1091-1095.
22. Buchholz K, Burke TA, Williamson KC, Wiegand RC, Wirth DF, et al. (2011) A high-throughput screen targeting malaria transmission stages opens new avenues for drug development. J Infect Dis 203: 1445-1453.
23. Milner DA Jr, Pochet N, Krupka M, Williams C, Seydel K, et al. (2012) Transcriptional Profiling of Plasmodium falciparum Parasites from Patients with Severe Malaria Identifies Distinct Low vs. High Parasitemic Clusters. PloS one 7: e40739.
24. Price R, Nosten F, Simpson JA, Luxemburger C, Phaipun L, et al. (1999) Risk factors for gametocyte carriage in uncomplicated falciparum malaria. Am J Trop Med Hyg 60: 1019-1023.
25. Adjalley SH, Johnston GL, Li T, Eastman RT, Ekland EH, et al. (2011) Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Proceedings of the National Academy of Sciences of the United States of America 108: E1214-1223.
26. Booker ML, Bastos CM, Kramer ML, Barker RH Jr, Skerlj R, et al. (2010) Novel inhibitors of Plasmodium falciparum dihydroorotate dehydrogenase with anti-malarial activity in the mouse model. The Journal of biological chemistry 285: 33054-33064.
27. Barker RH Jr, Urgaonkar S, Mazitschek R, Celatka C, Skerlj R, et al. (2011) Aminoindoles, a novel scaffold with potent activity against Plasmodium falciparum. Antimicrobial agents and chemotherapy 55: 2612-2622.
28. Fivelman QL, McRobert L, Sharp S, Taylor CJ, Saeed M, et al. (2007) Improved synchronous production of Plasmodium falciparum gametocytes in vitro. Mol Biochem Parasitol 154: 119-123.
29. Alano P, Roca L, Smith D, Read D, Carter R, et al. (1995) Plasmodium falciparum: parasites defective in early stages of gametocytogenesis. Exp Parasitol 81: 227-235.
30. van Wolfswinkel ME, de Mendonca Melo M, Vliegenthart-Jongbloed K, Koelewijn R, van Hellemond JJ, et al. (2012) The prognostic value of schizontaemia in imported Plasmodium falciparum malaria. Malaria journal 11: 301.
31. Mitri C, Thiery I, Bourgouin C, Paul RE, (2009) Density-dependent impact of the human malaria parasite Plasmodium falciparum gametocyte sex ratio on mosquito infection rates. Proceedings Biological sciences/The Royal Society 276: 3721-3726.
32. Okamoto N, Spurck TP, Goodman CD, McFadden GI, (2009) Apicoplast and mitochondrion in gametocytogenesis of Plasmodium falciparum. Eukaryotic cell 8: 128-132.
33. Schneider P, Bousema T, Omar S, Gouagna L, Sawa P, et al. (2006) (Sub)microscopic Plasmodium falciparum gametocytaemia in Kenyan children after treatment with sulphadoxine-pyrimethamine monotherapy or in combination with artesunate. Int J Parasitol 36: 403-408.
34. Stuart RO, Wachsman W, Berry CC, Wang-Rodriguez J, Wasserman L, et al. (2004) In silico dissection of cell-type-associated patterns of gene expression in prostate cancer. Proceedings of the National Academy of Sciences of the United States of America 101: 615-620.
35. Niederwieser I, Felger I, Beck HP, (2001) Limited polymorphism in Plasmodium falciparum sexual-stage antigens. The American journal of tropical medicine and hygiene 64: 9-11.
36. Taylor TE, Fu WJ, Carr RA, Whitten RO, Mueller JS, et al. (2004) Differentiating the pathologies of cerebral malaria by postmortem parasite counts. Nat Med 10: 143-145.
37. Taylor TE, (2009) Caring for children with cerebral malaria: insights gleaned from 20 years on a research ward in Malawi. Trans R Soc Trop Med Hyg 103 Suppl 1: S6-10.
38. Trager W, Jensen JB, (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
39. Lambros C, Vanderberg JP, (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65: 418-420.
40. Eksi S, Czesny B, van Gemert GJ, Sauerwein RW, Eling W, et al. (2006) Malaria transmission-blocking antigen, Pfs230, mediates human red blood cell binding to exflagellating male parasites and oocyst production. Mol Microbiol 61: 991-998.
41. Eksi S, Williamson KC, (2011) Protein targeting to the parasitophorous vacuole membrane of Plasmodium falciparum. Eukaryotic cell 10: 744-752.
42. Smith JD, Kyes S, Craig AG, Fagan T, Hudson-Taylor D, et al. (1998) Analysis of adhesive domains from the A4VAR Plasmodium falciparum erythrocyte membrane protein-1 identifies a CD36 binding domain. Mol Biochem Parasitol 97: 133-148.
43. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, et al. (2006) GenePattern 2.0. Nat Genet 38: 500-501.
44. Huttenhower C, Schroeder M, Chikina MD, Troyanskaya OG, (2008) The Sleipnir library for computational functional genomics. Bioinformatics 24: 1559-1561.
45. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M, (2010) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic acids research 38: D355-360.
46. Merrick CJ, Huttenhower C, Buckee C, Amambua-Ngwa A, Gomez-Escobar N, et al. (2012) Epigenetic Dysregulation of Virulence Gene Expression in Severe Plasmodium falciparum Malaria. The Journal of infectious diseases 205: 1593-1600.