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Insights Into the Functional Biology of Schistosomes Anthony John Walker

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Insights Into the Functional Biology of Schistosomes Anthony John Walker Walker Parasites & Vectors 2011, 4:203 http://www.parasitesandvectors.com/content/4/1/203 PRIMER Open Access Insights into the functional biology of schistosomes Anthony John Walker Abstract The need to discover new treatments for human schistosomiasis has been an important driver for molecular research on schistosomes, a major breakthrough being the publication of the Schistosoma mansoni and Schistosoma japonicum genomes in 2009. This ‘Primer’ considers recent advances in the understanding of schistosome biology by providing a snapshot of selected areas of contemporary functional schistosome research, including that on the genome, the tegument, cell signalling and developmental biology, offering biologists a valuable insight into the life of these fascinating parasites at the basic and molecular level. What are schistosomes? parasite relationships. Not only has co-evolution Schistosomes (phylum: Platyhelminthes) are blood- resulted in intricate interplay between the parasite and dwelling parasites that mature as separate-sex adults in its snail or vertebrate host but also between the adult the veins of mammals and birds. Throughout their com- male and female worms. Much recent research on the plex life-cycle, these trematodes undergo striking mor- basic biology of schistosomes has been driven strategi- phological and physiological changes with individual cally by the need better to control human schistosomia- life-stages displaying distinct adaptations both to parasi- sis, with the identification of new drug targets [8,9] and tic life, and also to free-living life that permits move- vaccine development [9,10] being key determinants. ment between definitive-vertebrate and intermediate- This is not without good reason; schistosomiasis is esti- snail hosts. Such adaptations include cilia or tails for mated to affect over 200 million people in 76 developing swimming, secretory glands for host penetration, a tegu- countries [7,11], with over 700 million people at risk, ment and glycocalyx for parasite protection/host and the currently-available drug, praziquantel, has been immuno-modulation, a gynaecophoric canal for sus- used in mono-therapy for several decades, so wide- tained pairing between sexes, muscular suckers for spread emergence of drug resistance is possible. Pathol- attachment/feeding, and highly organised reproductive ogy associated with human schistosomiasis is not due systems for efficient fertilization and egg production directly to the adult worms but rather the large numbers (Figure 1, [1-7]; for a downloadable version of the poster of eggs that become trapped in tissues during egg see Additional File 1). Research on schistosomes con- migration, or after embolism in organs such as the liver, tinues to largely centre on three species of schistosome spleen or lungs. The fibrotic granulomas that form that infect humans (Schistosoma mansoni, Schistosoma around the eggs develop as a consequence of a strong haematobium, and Schistosoma japonicum)andarethe CD4+ Th2 response that is regulated by various cell focus of this ‘Primer’, with most studies having been types, cytokines and chemokines with certain reactions performed on S. mansoni. limited by CD4+ regulatory T-cells [12]. Given the importance of the eggs to disease progression and trans- Why study the biology of schistosomes? mission, schistosome development, pairing, sexual Like many other parasites with complex life-cycles, maturation and egg production remain active areas of schistosomes are fascinating organisms to study, particu- fundamental research. In this ‘Primer’, selected areas of larly in the context of developmental biology and host- contemporary functional research on schistosomes are introduced by exploring three advances made in the last Correspondence: [email protected] decade; three topics of schistosome biology that are ripe School of Life Sciences, Kingston University, Kingston upon Thames, Surrey, KT1 2EE, UK for investigation are then considered. © 2011 Walker; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Walker Parasites & Vectors 2011, 4:203 Page 2 of 6 http://www.parasitesandvectors.com/content/4/1/203 Primers on Parasites The Biology of Schistosome Life Stages & Vectors Anthony J. Walker Cercariae Schistosomula t 'SFFMJWJOH OPOGFFEJOH DFSDBSJBF UPUBMMFOHUI_çN FTDBQFUISPVHIUIFCJSUIQPSFTPGEBVHIUFS t 8IFO DFSDBSJBF QFOFUSBUF UIF EFmOJUJWF IPTU UIFZ USBOTGPSN TUSVDUVSBMMZ BOE QIZTJPMPHJDBMMZ JOUP TLJO TDIJTUPTPNVMB "OUFSJPS TQPSPDZTUTBOEFNFSHFGSPNUIFJOGFDUFETOBJMBQQSPYJNBUFMZoXFFLTQPTUTOBJMJOGFDUJPO GPS PSHBO DIBOHFTJODMVEFMPTTPGUBJM SFMFBTFPGQSFBDFUBCVMBSHMBOEDPOUFOUT MPTTPGUIFDFSDBSJBMHMZDPDBMZY EFWFMPQNFOUPGB Schistosoma mansoni .PTUTQFDJFTTXJNUBJMmSTUVTJOHJOUFSNJUUFOUCVSTUTPGBDUJWJUZUPMPDBUFB EPVCMFCJMBZFSPVUFSNFNCSBOF BOEQSFTFOUBUJPOPGOFXHMZDPQSPUFJOT4VDDFTTGVMUSBOTGPSNBUJPOJTDPOTJEFSFEFTTFOUJBM "DFUBCVMVN TVJUBCMFEFmOJUJWFIPTUUIJTDPOUJOVFTGPSTFWFSBMIPVSTVOUJMDFSDBSJBMHMZDPHFOSFTFSWFTBSFEFQMFUFE GPSQBSBTJUFTVSWJWBM )PTU mOEJOH JT JOnVFODFE CZ XBUFS UVSCVMFODF TIBEPXT BOE DFSUBJO TLJO DIFNJDBMT JODMVEJOH Pre- t 4DIJTUPTPNVMB SFNBJO JO UIF TLJO GPS BU MFBTU I UIFZ UIFO FNCBSL PO B DPNQMJDBUFE KPVSOFZ mSTU QFOFUSBUJOH UIF BDFUBCVMBS DFSBNJEFT BSHJOJOFBOEMJOPMFJDBDJE HMBOET Y IPTUEFSNJTBOEWFOVMFXBMMBOEFOUFSJOHUIFDJSDVMBUJPO/FYUUIFZNJHSBUFUISPVHIUIFQVMNPOBSZDBQJMMBSJFT MVOH 1PTU t 5IF CPEZ BOE UBJM PG B DFSDBSJB JT FOWFMPQFE XJUI B TJOHMF DPOUJOVPVT TZODZUJBM UFHVNFOU UIBU JT TDIJTUPTPNVMB UPFOUFSUIFTZTUFNJDDJSDVMBUJPO-BSWBFUIFOQBTTUPUIFIFQBUJDQPSUBMTZTUFNBOECFHJOUPCMPPEGFFE BDFUBCVMBS HMBOET Y )FBEUBJM DPWFSFECZBDBSCPIZESBUFSJDIHMZDPDBMZY$JMJBUFETFOTPSZQBQJMMBFFYJTUBOEBSFUIPVHIUUPGBDJMJUBUF QBJSVQBOENJHSBUFUPUIFQPSUBMWFTTFMT'PSS. haematobium UIFXPSNTmOBMMZQBTTUPUIFWFTJDBMWFOVMFTBSPVOEUIF KVODUJPO IPTUEFUFDUJPO CMBEEFSXIFSFBTS. mansoni SFTJEFJOUIFNFTFOUFSJDWFOVMFT t 5IFBDFUBCVMVN WFOUSBMTVDLFS JTXFMMEFWFMPQFEBOPFTPQIBHVTBOEUXPTNBMMHVUDBFDFBBSFBMTP t 8IFOJOUIJTmOBMMPDBUJPO TDIJTUPTPNVMBHSPXSBQJEMZUIFUFHVNFOUBMTPNBUVSFT TFFBEVMU QSFTFOU7BSJPVTHMBOETFYJTUUIBUBSFJNQPSUBOUGPSIPTUQFOFUSBUJPOBOEDFSDBSJBMGVODUJPOQSF XPSNT .BMFTHSPXMBSHFSUIBOGFNBMFTBOEEJTQMBZIJHIFSNJUPUJDBDUJWJUZ%FWFMPQNFOUPG BDFUBCVMBSHMBOETUIBUDPOUBJONVMUJQMFFO[ZNFTJODMVEJOHQSPUFBTFTUIBUBJETLJOQFOFUSBUJPOQPTU UIFTFYPSHBOTPDDVSTBGUFSBQQSPYJNBUFMZXFFLT GPSS. mansoni BOEDPQVMBUJPOCFHJOT .VTDVMBS BDFUBCVMBSHMBOETUIBUTFDSFUFNVDVTUPIFMQUIFDFSDBSJBFBEIFSFUPTVSGBDFT BOEQSPUFBTFTBOEB BGUFSXFFLT1BJSFETDIJTUPTPNFTUIFONBUVSFUPBEVMUT CJGVSDBUFE UBJM IFBEHMBOEXJUIJOUIFBOUFSJPSPSHBO t 1SPUPDPMT GPS USBOTGPSNBUJPO PG DFSDBSJBF UP TDIJTUPTPNVMB BOE DVMUVSF PG t "T JO UIF NJSBDJEJVN B OFVSBM NBTT FYJTUT BOE nBNF DFMMT GVODUJPO JO UIFTFMBSWBFBSFXFMMFTUBCMJTIFECVUQSPEVDUJPOPGWJBCMFFHHTUISPVHITVDI PTNPSFHVMBUJPO(FSNDFMMTBSFQSFTFOUXIJDIVMUJNBUFMZEFWFMPQJOUP in vitroNFUIPETSFNBJOTBDIBMMFOHF UIFBEVMUXPSNSFQSPEVDUJWFTZTUFN SCHISTOSOMULA t 5IFCJGVSDBUFEUBJM XIJDIJTBNVTDVMBSUFNQPSBSZMPDPNPUPSPSHBOJT Growth and development of schistosomula. Rapid growth begins when (skin, lung, liver-stage) TIFEVQPOQFOFUSBUJPOPGUIFEFmOJUJWFIPTU CERCARIAE schistosomula reach the blood vessels of the liver. For 4NBOTPOJ, the first Confocal microscopy image of an 4NBOTPOJcercaria stained CERCARIAE schistosomules arrive around day 7; the gut caeca join posteriorly around day with the fluorescent probe CFDA. 15; sex organs then begin to develop after approximately 21 days. SPOROCYSTS (mother, daughter) Miracidia and sporocysts Adult worms t .JSBDJEJBFNFSHFGSPNFYDSFUFEFHHTVQPODPOUBDUXJUIGSFTIXBUFS5IFTFMBSWBF _çN MIRACIDIA PAIRED ADULT t .BUVSFBEVMUNBMFBOEGFNBMFXPSNT oNNMPOH BSFJOUJNBUFMZBTTPDJBUFEUIFGFNBMF MPOH BSFOPOGFFEJOHBOETXJNSBQJEMZ NNTGPS_I VTJOHDJMJBBUUBDIFEUPFQJEFSNBMQMBUFT WORMS SFTJEFTJOUIFHZOBFDPQIPSJDDBOBMPGUIFNPSFNVTDVMBSNBMF.PMFDVMBSTJHOBMMJOHBQQFBST UPMPDBUFBDPNQBUJCMFTOBJMJOUFSNFEJBUFIPTU4XJNNJOHCFIBWJPVSJTQPTJUJWFMZQIPUPLJOFUJD EGGS UPUBLFQMBDFCFUXFFOUIFXPSNTFOTVSJOHXPSNNBUVSBUJPO&HHQSPEVDUJPOCFHJOTo BOEQPTTJCMZDIFNPLJOFUJDUPXBSETTOBJMDPNQPOFOUT XFFLTQPTUJOGFDUJPOBOEDPOUJOVFTGPSVQUPZFBST)PXUIFNBUVSFXPSNTFWBEFUIF IPTUEFGFODFSFTQPOTFFOBCMJOHTVSWJWBMJTOPUGVMMZVOEFSTUPPE t 8PSNTQPTTFTTUXPUFSNJOBMTVDLFSTGPSBUUBDINFOU BDPNQMFYTZODZUJBMUFHVNFOUUIBUQMBZTBSPMFJOIPTUJNNVOFFWBTJPO t 5IFTFOTPSZUFSFCSBUPSJVN BQJDBMQBQJMMB GBDJMJUBUFTBUUBDINFOUUPUIFTOBJMTVSGBDFQFOFUSBUJPOJTQPTTJCMZBDIJFWFECZ NPEVMBUJPOBOEFYDSFUJPO BCMJOEEJHFTUJWFUSBDU BOEXFMMEFWFMPQFEOFVSBM FYDSFUPSZ BOESFQSPEVDUJWFTZTUFNT.BUVSF SFMFBTFPGQSPUFBTFTGSPNHMBOET MBUFSBMBOEBQJDBM BOENFDIBOJDBMNPWFNFOU GFNBMFXPSNTDBOQSPEVDFIVOESFET FHS. mansoni, S. haematobium UPUIPVTBOET FHS. japonicum PGFHHTQFSEBZ BQSPQPSUJPOPGXIJDIFTDBQFGSPNUIFIPTUviaUIFHVU FHS. mansoni, S. japonicum PSCMBEEFSXBMM S. haematobium t *OTJEFUIFTOBJMIPTUUIFNJSBDJEJVNTIFETJUTDJMJBUFEQMBUFTBOECFDPNFTBQPTUNJSBDJEJVN"OFXTZODZUJBMUFHVNFOU UPFOUFSUIFFYDSFUB&HHTOPUWPJEFECFDPNFUSBQQFEJOPSHBOT FHMJWFS DBVTJOHJNNVOFSFBDUJPOTUIBUSFTVMUJOIVNBO JTGPSNFEBOEUIFMBSWBEJGGFSFOUJBUFTJOUPBNPUIFSTQPSPDZTUUIBUQSPEVDFTHFSNDFMMEFSJWFEEBVHIUFSTQPSPDZTUTUIBU TDIJTUPTPNJBTJT EFWFMPQBOEQSPEVDFMBSHFOVNCFSTPGDFSDBSJBFGPSJOGFDUJPOPGUIFEFmOJUJWFIPTU5IFNFDIBOJTNTCZXIJDIUIFQBSBTJUF FWBEFTUIFTOBJMIPTUEFGFODFSFTQPOTFBSFOPUDVSSFOUMZXFMMVOEFSTUPPECVUBSFMJLFMZUPCFNVMUJGBDUPSJBM/VUSJFOUT 7FOUSBMTVDLFS HOST BLOOD (A) Confocal microscopy GSPNUIFTOBJMQMBTNBBSFBCTPSCFEBDSPTTUIFUFHVNFOUBOEFYDSFUPSZQSPEVDUTBSFSFMFBTFEUISPVHIUIFFYDSFUPSZQPSFT
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