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Systems biomedical analysis of Schistosoma japonicum |
| Ze-Guang HAN MD, |
| Shanghai-MOST Key Laboratory
for Disease and Health Genomics, Chinese National Human Genome Center
at Shanghai, Shanghai 201203, China；Rui-Jin Hospital, Shanghai
Jiao Tong University School of Medicine, Shanghai 200025, China; |
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Abstract Human schistosomiasis, caused mainly by three principal species including Schistosoma japonicum, S. mansoni, and S. hematobium, remains a major public health concern worldwide. S. japonicum is prevalent in southern China, being a major disease risk for 66 million people. The blood fluke has a complex life cycle for survival: as a free-living form in fresh water and as a parasite in the snail intermediate and vertebrate definitive hosts. Systems-based biomedical analyses, including genomic, transcriptomic, proteomic and metabonomic approaches, have been performed on the schistosome. These comprehensive investigations have not only characterized the genomic features but also chartered gene and protein expression profiles across genders and developmental stages. The integration of the huge information will lay a global and solid foundation for the molecular architecture of the biology, pathogenesis, and host-parasite interactions of the human blood fluke, which will facilitate the development of a new antischistosomal vaccine and drugs as well as diagnostic markers for the treatment and control of schistosomiasis.
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| Keywords
Schistosoma japonicum
systems biomedical analysis
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Issue Date: 05 June 2010
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Engels D, Chitsulo L, Montresor A, Savioli L. The global epidemiological situation of schistosomiasisand new approaches to control and research. Acta Trop, 2002, 82(2): 139―146
doi: 10.1016/S0001-706X(02)00045-1
|
|
Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet, 2006, 368(9541): 1106―1118
doi: 10.1016/S0140-6736(06)69440-3
|
|
Haas W, Diekhoff D, Koch K, Schmalfuss G, Loy C. Schistosomamansoni cercariae: stimulation of acetabular gland secretion is adaptedto the chemical composition of mammalian skin. J Parasitol, 1997, 83(6): 1079―1085
doi: 10.2307/3284366
|
|
Haas W, Schmitt R. Characterizationof chemical stimuli for the penetration of Schistosoma mansoni cercariae.I. Effective substances, host specificity. Z Parasitenkd, 1982, 66(3): 293―307
doi: 10.1007/BF00925346
|
|
Abath F G C, Morais C N L, Montenegro C E L, Wynn T A, Montenegro S M L. Immunopathogenic mechanisms in schistosomiasis: What can be learntfrom human studies? Trends Parasitol, 2006, 22(2): 85―91
doi: 10.1016/j.pt.2005.12.004
|
|
Amiri P, Locksley R M, Parslow T G, Sadick M, Rector E, Ritter D, McKerrow J H. Tumor necrosis factor alpha restores granulomas and inducesparasite egg-laying in schistosome-infected SCID mice. Nature, 1992, 356(6370): 604―607
doi: 10.1038/356604a0
|
|
Davies S J, Grogan J L, Blank R B, Lim K C, Locksley R M, McKerrow J H. Modulation of blood flukedevelopment in the liver by hepatic CD4+ lymphocytes. Science, 2001, 294(5545): 1358―1361
doi: 10.1126/science.1064462
|
|
de Mendonça R L, Escrivá H, Bouton D, Laudet V, Pierce R J. Hormones and nuclear receptors in schistosome development. Parasitol Today, 2000, 16(6): 233―240
doi: 10.1016/S0169-4758(00)01641-0
|
|
Ravindran B. Are inflammation and immunological hyperactivity neededfor filarial parasite development? TrendsParasitol, 2001, 17(2): 70―73
doi: 10.1016/S1471-4922(00)01835-3
|
|
Escobedo G, Roberts C W, Carrero J C, Morales-Montor J. Parasite regulation by host hormones:an old mechanism of host exploitation? Trends Parasitol, 2005, 21(12): 588―593
doi: 10.1016/j.pt.2005.09.013
|
|
Schistosoma japonicumGenome Sequencing and Functional Analysis Consortium. The Schistosoma japonicum genome reveals features ofhost-parasite interplay. Nature, 2009, 460(7253): 345―351
|
|
Hu W, Yan Q, Shen D K, Liu F, Zhu Z D, Song H D, Xu X R, Wang Z J, Rong Y P, Zeng L C, Wu J, Zhang X, Wang J J, Xu X N, Wang S Y, Fu G, Zhang X L, Wang Z Q, Brindley P J, McManus D P, Xue C L, Feng Z, Chen Z, Han Z G. Evolutionary and biomedical implications of a Schistosoma japonicumcomplementary DNA resource. Nat Genet, 2003, 35(2): 139―147
doi: 10.1038/ng1236
|
|
Liu F, Lu J, Hu W, Wang S Y, Cui S J, Chi M, Yan Q, Wang X R, Song H D, Xu X N, Wang J J, Zhang X L, Zhang X, Wang Z Q, Xue C L, Brindley P J, McManus D P, Yang P Y, Feng Z, Chen Z, Han Z G. New perspectives on host-parasite interplay by comparative transcriptomicand proteomic analyses of Schistosoma japonicum. PLoS Pathog, 2006, 2(4): e29
doi: 10.1371/journal.ppat.0020029
|
|
Liu F, Hu W, Cui S J, Chi M, Fang C Y, Wang Z Q, Yang P Y, Han Z G. Insight into the host-parasite interplayby proteomic study of host proteins copurified with the human parasite,Schistosoma japonicum. Proteomics, 2007, 7(3): 450―462
doi: 10.1002/pmic.200600465
|
|
Liu F, Cui S J, Hu W, Feng Z, Wang Z Q, Han Z G. Excretory/secretory proteome of the adult developmental stage ofhuman blood fluke, Schistosoma japonicum. Mol Cell Proteomics, 2009, 8(6): 1236―1251
doi: 10.1074/mcp.M800538-MCP200
|
|
Huang J, Hao P, Chen H, Hu W, Yan Q, Liu F, Han Z G. Genome-wideidentification of Schistosoma japonicum microRNAs using a deep-sequencingapproach. PLoS One, 2009, 4(12): e8206
doi: 10.1371/journal.pone.0008206
|
|
|
|
|
|
Han Z G, Brindley P J, Wang S Y, Chen Z. Schistosoma genomics: new perspectives on schistosomebiology and host-parasite interaction. Annu Rev Genomics Hum Genet, 2009,10: 211―240
doi: 10.1146/annurev-genom-082908-150036
|
|
Brindley P J, Mitreva M, Ghedin E, Lustigman S. Helminth genomics: The implications for human health. PLoS Negl Trop Dis, 2009, 3(10): e538
doi: 10.1371/journal.pntd.0000538
|
|
Hu W, Brindley P J, McManus D P, Feng Z, Han Z G. Schistosometranscriptomes: new insights into the parasite and schistosomiasis. Trends Mol Med, 2004, 10(5): 217―225
doi: 10.1016/j.molmed.2004.03.002
|
|
Simpson A J, Sher A, McCutchan T F. The genome of Schistosomamansoni: isolation of DNA, its size, bases and repetitive sequences. Mol Biochem Parasitol, 1982, 6(2): 125―137
doi: 10.1016/0166-6851(82)90070-6
|
|
Johnston D A, Blaxter M L, Degrave W M, Foster J, Ivens A C, Melville S E. Genomics and the biologyof parasites. Bioessays, 1999, 21(2): 131―147
doi: 10.1002/(SICI)1521-1878(199902)21:2<131::AID-BIES7>3.0.CO;2-I
|
|
Franco G R, Valadão A F, Azevedo V, Rabelo E M. The Schistosoma gene discovery program: state of theart. Int J Parasitol, 2000, 30(4): 453―463
doi: 10.1016/S0020-7519(00)00020-5
|
|
Shrivastava J, Qian B Z, Mcvean G, Webster J P. An insight into the genetic variation of Schistosoma japonicum inmainland China using DNA microsatellite markers. Mol Ecol, 2005, 14(3): 839―849
doi: 10.1111/j.1365-294X.2005.02443.x
|
|
Hokke C H, Fitzpatrick J M, Hoffmann K F. Integrating transcriptome,proteome and glycome analyses of Schistosoma biology. Trends Parasitol, 2007, 23(4): 165―174
doi: 10.1016/j.pt.2007.02.007
|
|
van Hellemond J J, van Balkom B W, Tielens A G. Schistosome biology and proteomics:progress and challenges. Exp Parasitol, 2007, 117(3): 267―274
doi: 10.1016/j.exppara.2007.05.004
|
|
Wilson R A, Ashton P D, Braschi S, Dillon G P, Berriman M, Ivens A. 'Oming in on schistosomes:prospects and limitations for post-genomics. Trends Parasitol, 2007, 23(1): 14―20
doi: 10.1016/j.pt.2006.10.002
|
|
Cheng G F, Lin J J, Feng X G, Fu Z Q, Jin Y M, Yuan C X, Zhou Y C, Cai Y M. Proteomic analysis of differentiallyexpressed proteins between the male and female worm of Schistosomajaponicum after pairing. Proteomics, 2005, 5(2): 511―521
doi: 10.1002/pmic.200400953
|
|
McLaren D J, Hockley D J. Blood flukes have a double outer membrane. Nature, 1977, 269(5624): 147―149
doi: 10.1038/269147a0
|
|
Jenkins S J, Hewitson J P, Jenkins G R, Mountford A P. Modulation of the host's immune response by schistosomelarvae. Parasite Immunol, 2005, 27(10―11): 385―393
|
|
Lightowlers M W, Rickard M D. Excretory-secretory products of helminth parasites: effects on hostimmune responses. Parasitology, 1988, 96(Suppl): S123―166
|
|
Nicholson J K, Lindon J C. Systems biology – metabonomics. Nature, 2008, 455 (7216): 1054―1056
doi: 10.1038/4551054a
|
|
Wang Y, Holmes E, Nicholson J K, Cloarec O, Chollet J, Tanner M, Singer B H, Utzinger J. Metabonomicinvestigations in mice infected with Schistosoma mansoni: an approachfor biomarker identification. Proc NatlAcad Sci USA, 2004, 101(34): 12676―12681
doi: 10.1073/pnas.0404878101
|
|
Wang Y, Utzinger J, Xiao S H, Xue J, Nicholson J K, Tanner M, Singer B H, Holmes E. Systemlevel metabolic effects of a Schistosoma japonicum infection in theSyrian hamster. Mol Biochem Parasitol, 2006, 146(1): 1―9
doi: 10.1016/j.molbiopara.2005.10.010
|
|
Wu J F, Holmes E, Xue J, Xiao S H, Singer B H, Tang H R, Utzinger J, Wang Y L. Metabolicalterations in the hamster co-infected with Schistosoma japonicumand Necator americanus. Int J Parasitol, 2010, 40(6): 695―703
doi: 10.1016/j.ijpara.2009.11.003
|
|
Skelly P J, Kim J W, Cunningham J, Shoemaker C B. Cloning, characterization, and functional expressionof cDNAs encoding glucose transporter proteins from the human parasiteSchistosoma mansoni. J Biol Chem, 1994, 269(6): 4247―4253
|
|
Skelly P J, Shoemaker C B. Rapid appearance and asymmetric distribution of glucose transporterSGTP4 at the apical surface of intramammalian-stage Schistosoma mansoni. Proc Natl Acad Sci U S A, 1996, 93(8): 3642―3646
doi: 10.1073/pnas.93.8.3642
|
|
Cohen L M, Neimark H, Eveland L K. Schistosoma mansoni: responseof cercariae to a thermal gradient. J Parasitol, 1980, 66(2): 362―364
doi: 10.2307/3280843
|
|
Maizels R M, Bundy D A, Selkirk M E, Smith D F, Anderson R M. Immunological modulationand evasion by helminth parasites in human populations. Nature, 1993, 365(6449): 797―805
doi: 10.1038/365797a0
|
|
McKerrow J H. Cytokine induction and exploitation in schistosome infections. Parasitology, 1997, 115(Suppl): 107―112
doi: 10.1017/S0031182097001765
|
|
Dvorák J, Mashiyama S T, Braschi S, Sajid M, Knudsen G M, Hansell E, Lim K C, Hsieh I, Bahgat M, Mackenzie B, Medzihradszky K F, Babbitt P C, Caffrey C R, McKerrow J H. Differential use of proteasefamilies for invasion by schistosome cercariae. Biochimie, 2008, 90(2): 345―358
doi: 10.1016/j.biochi.2007.08.013
|
|
Koehler J W, Morales M E, Shelby B D, Brindley P J. Aspartic protease activities of schistosomes cleave mammalianhemoglobins in a host-specific manner. Mem Inst Oswaldo Cruz, 2007, 102(1): 83―85
doi: 10.1590/S0074-02762007000100014
|
|
Zhou X N, Wang L Y, Chen M G, Wu X H, Jiang Q W, Chen X Y, Zheng J, Utzinger J. The public health significance and controlof schistosomiasis in China- then and now. Acta Trop, 2005, 96(2―3): 97―105
doi: 10.1016/j.actatropica.2005.07.005
|
|
Utzinger J, Zhou X N, Chen M G, Bergquist R. Conqueringschistosomiasis in China: the long march. Acta Trop, 2005, 96(2―3): 69―96
|
|
Li Y S, Raso G, Zhao Z Y, He Y K, Ellis M K, McManus D P. Large water management projects and schistosomiasis control,Dongting Lake region, China. Emerg InfectDis, 2007, 13(7): 973―979
|
|
Bergquist R, Utzinger J, McManus D P. Trick or treat: the roleof vaccines in integrated schistosomiasis control. PLoS Negl Trop Dis, 2008, 2(6): e244
doi: 10.1371/journal.pntd.0000244
|
|
Ismail M, Botros S, Metwally A, William S, Farghally A, Tao L F, Day T A, Bennett J L. Resistance to praziquantel: direct evidence from Schistosoma mansoniisolated from Egyptian villagers. Am JTrop Med Hyg, 1999, 60(6): 932―935
|
|
Stelma F F, Talla I, Sow S, Kongs A, Niang M, Polman K, Deelder A M, Gryseels B. Efficacy and side effectsof praziquantel in an epidemic focus of Schistosoma mansoni. Am J Trop Med Hyg, 1995, 53(2): 167―170
|
|
Doenhoff M J, Cioli D, Utzinger J. Praziquantel: mechanisms of action, resistanceand new derivatives for schistosomiasis. Curr Opin Infect Dis, 2008, 21(6): 659―667
doi: 10.1097/QCO.0b013e328318978f
|
|
Gourlay L J, Angelucci F, Baiocco P, Boumis G, Brunori M, Bellelli A, Miele A E. The three-dimensional structure of two redox states ofcyclophilin A from Schistosoma mansoni. Evidence for redox regulationof peptidyl-prolyl cis-trans isomerase activity. J Biol Chem, 2007, 282(34): 24851―24857
doi: 10.1074/jbc.M702714200
|
|
Sayed A A, Simeonov A, Thomas C J, Inglese J, Austin C P, Williams D L. Identification of oxadiazolesas new drug leads for the control of schistosomiasis. Nat Med, 2008, 14(4): 407―412
doi: 10.1038/nm1737
|
|
Kuntz A N, Davioud-Charvet E, Sayed A A, Califf L L, Dessolin J, Arnér E S, Williams D L. Thioredoxin glutathione reductase from Schistosoma mansoni:an essential parasite enzyme and a key drug target. PLoS Med, 2007, 4(6): e206
doi: 10.1371/journal.pmed.0040206
|
|
Wu W, Niles E G, Hirai H, LoVerde P T. Evolution of a novel subfamily of nuclear receptors with membersthat each contain two DNA binding domains. BMC Evol Biol, 2007, 7: 27
doi: 10.1186/1471-2148-7-27
|
|
Freitas T C, Jung E, Pearce E J. TGF-beta signaling controls embryo developmentin the parasitic flatworm Schistosoma mansoni. PLoS Pathog, 2007, 3(4): e52
doi: 10.1371/journal.ppat.0030052
|
|
Osman A, Niles E G, Verjovski-Almeida S, LoVerde P T. Schistosoma mansoni TGF-beta receptor II: role in hostligand-induced regulation of a schistosome target gene. PLoS Pathog, 2006, 2(6): e54
doi: 10.1371/journal.ppat.0020054
|
|
Morales M E, Rinaldi G, Gobert G N, Kines K J, Tort J F, Brindley P J. RNA interference of Schistosomamansoni cathepsin D, the apical enzyme of the hemoglobin proteolysiscascade. Mol Biochem Parasitol, 2008, 157(2): 160―168
doi: 10.1016/j.molbiopara.2007.10.009
|
|
Correnti J M, Brindley P J, Pearce E J. Long-term suppression ofcathepsin B levels by RNA interference retards schistosome growth. Mol Biochem Parasitol, 2005, 143(2): 209―215
doi: 10.1016/j.molbiopara.2005.06.007
|
|
McManus D P, Loukas A. Thecurrent status of vaccines for schistosomiasis. Clin Microbiol Rev, 2008, 21(1): 225―242
doi: 10.1128/CMR.00046-07
|
|
Loukas A, Tran M, Pearson M S. Schistosome membrane proteins as vaccines. Int J Parasitol, 2007, 37(3―4): 257―263
doi: 10.1016/j.ijpara.2006.12.001
|
|
Tran M H, Pearson M S, Bethony J M, Smyth D J, Jones M K, Duke M, Don T A, McManus D P, Correa-Oliveira R, Loukas A. Tetraspaninson the surface of Schistosoma mansoni are protective antigens againstschistosomiasis. Nat Med, 2006, 12(7): 835―840
doi: 10.1038/nm1430
|
|
Hotez P J, Molyneux D H, Fenwick A, Kumaresan J, Sachs S E, Sachs J D, Savioli L. Controlof neglected tropical diseases. N EnglJ Med, 2007, 357(10): 1018―1027
doi: 10.1056/NEJMra064142
|
|
Wang L D, Chen H G, Guo J G, Zeng X J, Hong X L, Xiong J J, Wu X H, Wang X H, Wang L Y, Xia G, Hao Y, Chin D P, Zhou X N. A strategy to control transmission ofSchistosoma japonicum in China. N EnglJ Med, 2009, 360(2): 121―128
doi: 10.1056/NEJMoa0800135
|
|
Bergquist R, Johansen M V, Utzinger J. Diagnostic dilemmas in helminthology:what tools to use and when? Trends Parasitol, 2009, 25(4): 151―156
doi: 10.1016/j.pt.2009.01.004
|
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