Disease specific modules and hub genes for intervention strategies: A co-expression network based approach for Plasmodium falciparum clinical isolates

Infection, Genetics and Evolution

Volumn 35, Issue , 2015, Pages 96-108

  Subudhi, Amit Kumar ^a   Boopathi, Pon Arunachalam ^a   Pandey, Isha ^a   Kaur, Ramandeep ^a   Middha, Sheetal ^b   Acharya, Jyoti ^b   Kochar, Sanjay K ^b   Kochar, Dhanpat K ^c   Das, Ashis ^a  

^a BIRLA INSTITUTE OF TECHNOLOGY AND SCIENCE   (India)

^b S P MEDICAL COLLEGE   (India)

^c RAJASTHAN UNIVERSITY OF HEALTH SCIENCES   (India)

Author keywords

Complicated malaria; Plasmodium falciparum; Weighted gene co expression network

Indexed keywords

ARTICLE; CATABOLISM; DISEASE SEVERITY; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE MAPPING; MALARIA FALCIPARUM; NONHUMAN; NUCLEOTIDE METABOLISM; OXIDATION REDUCTION REACTION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RESPIRATORY CHAIN; RNA BINDING; BIOLOGY; COMPLICATION; DNA MICROARRAY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; HUMAN; ISOLATION AND PURIFICATION; PARASITOLOGY; PROCEDURES;

PLASMODIUM FALCIPARUM; PROTOZOA;

PROTOZOAL PROTEIN;

COMPUTATIONAL BIOLOGY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; MALARIA, FALCIPARUM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS;

EID: 84938884791     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2015.08.007     Document Type: Article

References (69)

1. Allen R.J., Kirk K. The membrane potential of the intraerythrocytic malaria parasite Plasmodium falciparum. J. Biol. Chem. 2004, 279:11264-11272.
2. Balaji S., Babu M.M., Iyer L.M., Aravind L. Discovery of the principal specific transcription factors of Apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Res. 2005, 33:3994-4006.
3. Beitz E., Pavlovic-Djuranovic S., Yasui M., Agre P., Schultz J.E. Molecular dissection of water and glycerol permeability of the aquaglyceroporin from Plasmodium falciparum by mutational analysis. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:1153-1158.
4. Ben-David E., Shifman S. Networks of neuronal genes affected by common and rare variants in autism spectrum disorders. PLoS Genet. 2012, 8:e1002556.
5. Bozdech Z., Llinas M., Pulliam B.L., Wong E.D., Zhu J., DeRisi J.L. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 2003, 1:E5.
6. Carlson M.R., Zhang B., Fang Z., Mischel P.S., Horvath S., Nelson S.F. Gene connectivity, function, and sequence conservation: predictions from modular yeast co-expression networks. BMC Genomics 2006, 7:40.
7. Daily J.P., Le Roch K.G., Sarr O., Ndiaye D., Lukens A., Zhou Y., Ndir O., Mboup S., Sultan A., Winzeler E.A., Wirth D.F. In vivo transcriptome of Plasmodium falciparum reveals overexpression of transcripts that encode surface proteins. J. Infect. Dis. 2005, 191:1196-1203.
8. Daily J.P., Scanfeld D., Pochet N., Le Roch K., Plouffe D., Kamal M., Sarr O., Mboup S., Ndir O., Wypij D., Levasseur K., Thomas E., Tamayo P., Dong C., Zhou Y., Lander E.S., Ndiaye D., Wirth D., Winzeler E.A., Mesirov J.P., Regev A. Distinct physiological states of Plasmodium falciparum in malaria-infected patients. Nature 2007, 450:1091-1095.
9. Das A., Holloway B., Collins W.E., Shama V.P., Ghosh S.K., Sinha S., Hasnain S.E., Talwar G.P., Lal A.A. Species-specific 18S rRNA gene amplification for the detection of P. falciparum and P. vivax malaria parasites. Mol. Cell. Probes 1995, 9:161-165.
10. Date S.V., Stoeckert C.J. Computational modeling of the Plasmodium falciparum interactome reveals protein function on a genome-wide scale. Genome Res. 2006, 16:542-549.
11. de Jong S., Boks M.P., Fuller T.F., Strengman E., Janson E., de Kovel C.G., Ori A.P., Vi N., Mulder F., Blom J.D., Glenthoj B., Schubart C.D., Cahn W., Kahn R.S., Horvath S., Ophoff R.A. A gene co-expression network in whole blood of schizophrenia patients is independent of antipsychotic-use and enriched for brain-expressed genes. PLoS ONE 2012, 7:e39498.
12. Dumont M.E., Cardillo T.S., Hayes M.K., Sherman F. Role of cytochrome c heme lyase in mitochondrial import and accumulation of cytochrome c in Saccharomyces cerevisiae. Mol. Cell. Biol. 1991, 11:5487-5496.
13. Fang J., Zhou H., Rathore D., Sullivan M., Su X.Z., McCutchan T.F. Ambient glucose concentration and gene expression in Plasmodium falciparum. Mol. Biochem. Parasitol. 2004, 133:125-129.
14. Florens L., Washburn M.P., Raine J.D., Anthony R.M., Grainger M., Haynes J.D., Moch J.K., Muster N., Sacci J.B., Tabb D.L., Witney A.A., Wolters D., Wu Y., Gardner M.J., Holder A.A., Sinden R.E., Yates J.R., Carucci D.J. A proteomic view of the Plasmodium falciparum life cycle. Nature 2002, 419:520-526.
15. Flueck C., Bartfai R., Niederwieser I., Witmer K., Alako B.T., Moes S., Bozdech Z., Jenoe P., Stunnenberg H.G., Voss T.S. A major role for the Plasmodium falciparum ApiAP2 protein PfSIP2 in chromosome end biology. PLoS Pathog. 2010, 6:e1000784.
16. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., Carlton J.M., Pain A., Nelson K.E., Bowman S., Paulsen I.T., James K., Eisen J.A., Rutherford K., Salzberg S.L., Craig A., Kyes S., Chan M.S., Nene V., Shallom S.J., Suh B., Peterson J., Angiuoli S., Pertea M., Allen J., Selengut J., Haft D., Mather M.W., Vaidya A.B., Martin D.M., Fairlamb A.H., Fraunholz M.J., Roos D.S., Ralph S.A., McFadden G.I., Cummings L.M., Subramanian G.M., Mungall C., Venter J.C., Carucci D.J., Hoffman S.L., Newbold C., Davis R.W., Fraser C.M., Barrell B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419:498-511.
17. Gargalovic P.S., Imura M., Zhang B., Gharavi N.M., Clark M.J., Pagnon J., Yang W.P., He A., Truong A., Patel S., Nelson S.F., Horvath S., Berliner J.A., Kirchgessner T.G., Lusis A.J. Identification of inflammatory gene modules based on variations of human endothelial cell responses to oxidized lipids. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:12741-12746.
18. Ghazalpour A., Doss S., Zhang B., Wang S., Plaisier C., Castellanos R., Brozell A., Schadt E.E., Drake T.A., Lusis A.J., Horvath S. Integrating genetic and network analysis to characterize genes related to mouse weight. PLoS Genet. 2006, 2:e130.
19. Ginsburg H. Abundant proton pumping in Plasmodium falciparum, but why?. Trends Parasitol. 2002, 18:483-486.
20. Glick B.S., Rothman J.E. Possible role for fatty acyl-coenzyme A in intracellular protein transport. Nature 1987, 326:309-312.
21. Groot P.H., Scholte H.R., Hulsmann W.C. Fatty acid activation: specificity, localization, and function. Adv. Lipid Res. 1976, 14:75-126.
22. Hansen M., Kun J.F., Schultz J.E., Beitz E. A single, bi-functional aquaglyceroporin in blood-stage Plasmodium falciparum malaria parasites. J. Biol. Chem. 2002, 277:4874-4882.
23. Holm L.M., Jahn T.P., Moller A.L., Schjoerring J.K., Ferri D., Klaerke D.A., Zeuthen T. NH3 and NH4+ permeability in aquaporin-expressing Xenopus oocytes. Pflugers Arch. 2005, 450:415-428.
24. Hu G., Cabrera A., Kono M., Mok S., Chaal B.K., Haase S., Engelberg K., Cheemadan S., Spielmann T., Preiser P.R., Gilberger T.W., Bozdech Z. Transcriptional profiling of growth perturbations of the human malaria parasite Plasmodium falciparum. Nat. Biotechnol. 2010, 28:91-98.
25. Huang da W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37:1-13.
26. da Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
27. Iwanaga S., Kaneko I., Kato T., Yuda M. Identification of an AP2-family protein that is critical for malaria liver stage development. PLoS ONE 2012, 7:e47557.
28. Kafsack B.F., Rovira-Graells N., Clark T.G., Bancells C., Crowley V.M., Campino S.G., Williams A.E., Drought L.G., Kwiatkowski D.P., Baker D.A., Cortes A., Llinas M. A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature 2014, 507:248-252.
29. Kochar D.K., Saxena V., Singh N., Kochar S.K., Kumar S.V., Das A. Plasmodium vivax malaria. Emerg. Infect. Dis. 2005, 11:132-134.
30. Kochar D.K., Tanwar G.S., Khatri P.C., Kochar S.K., Sengar G.S., Gupta A., Kochar A., Middha S., Acharya J., Saxena V., Pakalapati D., Garg S., Das A. Clinical features of children hospitalized with malaria - a study from Bikaner, northwest India. Am. J. Trop. Med. Hyg. 2010, 83:981-989.
31. Krungkrai J., Prapunwattana P., Krungkrai S.R. Ultrastructure and function of mitochondria in gametocytic stage of Plasmodium falciparum. Parasite 2000, 7:19-26.
32. Langfelder P., Horvath S. Eigengene networks for studying the relationships between co-expression modules. BMC Syst. Biol. 2007, 1:54.
33. Langfelder P., Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 2008, 9:559.
34. Lang-Unnasch N., Murphy A.D. Metabolic changes of the malaria parasite during the transition from the human to the mosquito host. Annu. Rev. Microbiol. 1998, 52:561-590.
35. Le Roch K.G., Zhou Y., Blair P.L., Grainger M., Moch J.K., Haynes J.D., De La Vega P., Holder A.A., Batalov S., Carucci D.J., Winzeler E.A. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 2003, 301:1503-1508.
36. LeRoux M., Lakshmanan V., Daily J.P. Plasmodium falciparum biology: analysis of in vitro versus in vivo growth conditions. Trends Parasitol. 2009, 25:474-481.
37. Llinas M., Bozdech Z., Wong E.D., Adai A.T., DeRisi J.L. Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains. Nucleic Acids Res. 2006, 34:1166-1173.
38. Mackinnon M.J., Li J., Mok S., Kortok M.M., Marsh K., Preiser P.R., Bozdech Z. Comparative transcriptional and genomic analysis of Plasmodium falciparum field isolates. PLoS Pathog. 2009, 5:e1000644.
39. Matesanz F., Tellez M., Alcina A. The Plasmodium falciparum fatty acyl-CoA synthetase family (PfACS) and differential stage-specific expression in infected erythrocytes. Mol. Biochem. Parasitol. 2003, 126:109-112.
40. Mi-Ichi F., Kita K., Mitamura T. Intraerythrocytic Plasmodium falciparum utilize a broad range of serum-derived fatty acids with limited modification for their growth. Parasitology 2006, 133:399-410.
41. Miller L.H., Baruch D.I., Marsh K., Doumbo O.K. The pathogenic basis of malaria. Nature 2002, 415:673-679.
42. Miller J.A., Horvath S., Geschwind D.H. Divergence of human and mouse brain transcriptome highlights Alzheimer disease pathways. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:12698-12703.
43. Mitamura T., Hanada K., Ko-Mitamura E.P., Nishijima M., Horii T. Serum factors governing intraerythrocytic development and cell cycle progression of Plasmodium falciparum. Parasitol. Int. 2000, 49:219-229.
44. Moriyama Y., Hayashi M., Yatsushiro S., Yamamoto A. Vacuolar proton pumps in malaria parasite cells. J. Bioenerg. Biomembr. 2003, 35:367-375.
45. Muller S. Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Mol. Microbiol. 2004, 53:1291-1305.
46. Newby Z.E., O'Connell J., Robles-Colmenares Y., Khademi S., Miercke L.J., Stroud R.M. Crystal structure of the aquaglyceroporin PfAQP from the malarial parasite Plasmodium falciparum. Nat. Struct. Mol. Biol. 2008, 15:619-625.
47. Oldham M.C., Horvath S., Geschwind D.H. Conservation and evolution of gene coexpression networks in human and chimpanzee brains. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:17973-17978.
48. Painter H.J., Campbell T.L., Llinas M. The Apicomplexan AP2 family: integral factors regulating Plasmodium development. Mol. Biochem. Parasitol. 2011, 176:1-7.
49. Pakalapati D., Garg S., Middha S., Acharya J., Subudhi A.K., Boopathi A.P., Saxena V., Kochar S.K., Kochar D.K., Das A. Development and evaluation of a 28S rRNA gene-based nested PCR assay for P. falciparum and P. vivax. Pathog. Glob. Health 2013, 107:180-188.
50. Pakalapati D., Garg S., Middha S., Kochar A., Subudhi A.K., Arunachalam B.P., Kochar S.K., Saxena V., Pareek R.P., Acharya J., Kochar D.K., Das A. Comparative evaluation of microscopy, OptiMAL((R)) and 18S rRNA gene based multiplex PCR for detection of Plasmodium falciparum & Plasmodium vivax from field isolates of Bikaner, India. Asian Pac. J. Trop. Med. 2013, 6:346-351.
51. Planche T., Krishna S. Severe malaria: metabolic complications. Curr. Mol. Med. 2006, 6:141-153.
52. Promeneur D., Liu Y., Maciel J., Agre P., King L.S., Kumar N. Aquaglyceroporin PbAQP during intraerythrocytic development of the malaria parasite Plasmodium berghei. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:2211-2216.
53. Saliba K.J., Allen R.J., Zissis S., Bray P.G., Ward S.A., Kirk K. Acidification of the malaria parasite's digestive vacuole by a H+-ATPase and a H+-pyrophosphatase. J. Biol. Chem. 2003, 278:5605-5612.
54. Siau A., Silvie O., Franetich J.F., Yalaoui S., Marinach C., Hannoun L., van Gemert G.J., Luty A.J., Bischoff E., David P.H., Snounou G., Vaquero C., Froissard P., Mazier D. Temperature shift and host cell contact up-regulate sporozoite expression of Plasmodium falciparum genes involved in hepatocyte infection. PLoS Pathog. 2008, 4:e1000121.
55. Subudhi A.K., Boopathi P.A., Garg S., Middha S., Acharya J., Pakalapati D., Saxena V., Aiyaz M., Orekondy H.B., Mugasimangalam R.C., Sirohi P., Kochar S.K., Kochar D.K., Das A. Natural antisense transcripts in Plasmodium falciparum isolates from patients with complicated malaria. Exp. Parasitol. 2014, 141C:39-54.
56. Subudhi A.K., Boopathi P.A., Pandey I., Kohli R., Karwa R., Middha S., Acharya J., Kochar S.K., Kochar D.K., Das A. Plasmodium falciparum complicated malaria: modulation and connectivity between exportome and variant surface antigen gene families. Mol. Biochem. Parasitol. 2015, 201:31-46.
57. Surolia N., Surolia A. Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nat. Med. 2001, 7:167-173.
58. Ta T.H., Hisam S., Lanza M., Jiram A.I., Ismail N., Rubio J.M. First case of a naturally acquired human infection with Plasmodium cynomolgi. Malar. J. 2014, 13:68.
59. Tarun A.S., Peng X., Dumpit R.F., Ogata Y., Silva-Rivera H., Camargo N., Daly T.M., Bergman L.W., Kappe S.H. A combined transcriptome and proteome survey of malaria parasite liver stages. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:305-310.
60. Tewari R., Straschil U., Bateman A., Bohme U., Cherevach I., Gong P., Pain A., Billker O. The systematic functional analysis of Plasmodium protein kinases identifies essential regulators of mosquito transmission. Cell Host Microbe 2010, 8:377-387.
61. World Health O. Severe falciparum malaria. Trans. R. Soc. Trop. Med. Hyg. 2000, 94:1-90.
62. World Helath Organization, 2014. World Malaria Report 2014. Geneva, Switzerland: World Helath Organization. Available at < http://www.who.int/malaria/publications/world_malaria_report_2014/en/.
63. Wuchty S., Ipsaro J.J. A draft of protein interactions in the malaria parasite P. falciparum. J. Proteome Res. 2007, 6:1461-1470.
64. Yatsushiro S., Taniguchi S., Mitamura T., Omote H., Moriyama Y. Proteolipid of vacuolar H(+)-ATPase of Plasmodium falciparum: cDNA cloning, gene organization and complementation of a yeast null mutant. Biochim. Biophys. Acta 2005, 1717:89-96.
65. Ye J., Coulouris G., Zaretskaya I., Cutcutache I., Rozen S., Madden T.L. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 2012, 13:134.
66. Yuda M., Iwanaga S., Shigenobu S., Kato T., Kaneko I. Transcription factor AP2-Sp and its target genes in malarial sporozoites. Mol. Microbiol. 2010, 75:854-863.
67. Zeuthen T., Wu B., Pavlovic-Djuranovic S., Holm L.M., Uzcategui N.L., Duszenko M., Kun J.F., Schultz J.E., Beitz E. Ammonia permeability of the aquaglyceroporins from Plasmodium falciparum, Toxoplasma gondii and Trypanosoma brucei. Mol. Microbiol. 2006, 61:1598-1608.
68. Zhang B., Horvath S. A general framework for weighted gene co-expression network analysis. Stat. Appl. Genet Mol Biol 2005, 4. (Article 17).
69. Zhou Y., Ramachandran V., Kumar K.A., Westenberger S., Refour P., Zhou B., Li F., Young J.A., Chen K., Plouffe D., Henson K., Nussenzweig V., Carlton J., Vinetz J.M., Duraisingh M.T., Winzeler E.A. Evidence-based annotation of the malaria parasite's genome using comparative expression profiling. PLoS ONE 2008, 3:e1570.