Copyright © 2012 Adema et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.No abstract available

A Baeza Garcia

A-S Stensgaard

AE Lockyer

Christopher J. Bayne

CM Adema

Coen M. Adema

DJ Gray

DP McManus

E Deleury

Eric S. Loker

EY Seto

G Mitta

H Wang

J Keiser

Joanna M. Bridger

M Knight

Matty Knight

MJ Doenhoff

MR Knox

NA Aka

NJ Morley

PC Hanington

S Mas-Coma

S-M Zhang

SD Melman

Si-Ming Zhang

SW Attwood

Timothy P. Yoshino

PLoS Neglected Tropical Diseases

English

PubMed

Adema, CM

Bayne, CJ

Bridger, JM

Knight, M

Loker, ES

Yoshino, TP

Zhang, S-M

Brunel University Research Archive

EditorialWill All Scientists Working on Snails and the DiseasesThey Transmit Please Stand Up?Coen M. Adema1, Christopher J. Bayne2, Joanna M. Bridger3, Matty Knight4*, Eric S. Loker1,Timothy P. Yoshino5, Si-Ming Zhang11CETI, Department of Biology, University of New Mexico, Albuquerque, New Mexico, United States of America, 2Department of Zoology, Oregon State University,Corvallis, Oregon, United States of America, 3 Brunel University, Uxbridge, United Kingdom, 4 Biomedical Research Institute, Rockville, Maryland, United States of America,5Department of Pathobiological Sciences, University of Wisconsin, School of Veterinary Medicine, Madison, Wisconsin, United States of AmericaIf this request had been made duringthe presidential address at the ASTMHmeeting in Philadelphia in 2011, eventhough the room was filled beyondcapacity, only a few people would havestood up. Yet, 300 million disadvantagedpeople suffer from snail-transmitted infec-tions, with consequences ranging from life-threatening cholangiocarcinoma to subtlemorbidity effects that stunt physical andmental development. The disability-ad-justed life year (DALY) scores for thesediseases have long been underestimated.The term ‘‘neglected tropical diseases’’ trulyapplies to all snail-borne infections, in-cluding schistosomiasis, fascioliasis, fascio-lopsiasis, paragonimiasis, opisthorchiasis,clonorchiasis, and angiostrongyliasis [1–7].The prevalence of most of the parasitesinvolved has scarcely diminished in recentdecades. The resilience of the snails thattransmit them, such as Biomphalaria hostingSchistosoma mansoni in Africa, Yemen, orSouth America, or lymnaeid snails sup-porting Fasciola hepatica in Bolivia andelsewhere, provides a remarkable stabilityto the life cycles involved. Snail-borneinfections provide a worthy challenge forany young parasitologist looking for anexciting career.The recent World Health Organization(WHO) announcement of a global effort toeliminate human schistosomiasis by 2025[8] is an inspiring clarion call thatunderscores the need for more emphasison snail-related research. Future control ofsnail-borne parasites needs to be consid-ered outside of the box of current, almostexclusive, reliance on chemotherapy. Al-though it is essential and surely mustcontinue, chemotherapy alone may neverachieve transmission control or elimina-tion [9], and resistance is an ever-presentpossibility [10–12], especially when drugoptions are few, the extent of treatment isbroadened, and the size of drug-sensitiveparasite refugia diminishes [13].So, how can study of relevant snailscontribute to eliminating schistosomiasisand other snail-borne parasites? Adetailed grasp of the role of snails intransmission is essential for developingintegrated control strategies that alsotarget the intramolluscan larval stagesof parasites. For example, what deter-mines the population structure andgeographical distribution of snails thatdefine endemic areas for parasite trans-mission, and how will global warmingaffect these [14]? To what extent is thenumber of infected snails dictated byimmuno-compatibility between parasiteand snail versus ecological factors thatlimit infections? Precise information fromthe field is lacking for how long infectedsnails continue to shed cercariae, andthe number of cercariae produced persnail. Deciphering properties of immu-nity and virulence that have evolved toinfluence snail–parasite compatibilityreveals determinants of host competencethat will facilitate monitoring, predict-ing, and ultimately modifying transmis-sion of schistosomiasis and other snail-borne parasites.Exciting science can be done! Snails(and trematodes parasites) are lophotro-chozoan protostomes, an animal lineage towhich little attention has yet been paid—fundamental discoveries consequently lieahead in a field that is not cluttered bymany competing research groups. Recentnovel basic insights into host–parasiteinteractions include the discovery of so-matic diversification of immune moleculesin invertebrates (Biomphalaria); the involve-ment of antigenic variation by Schistosomato survive in snails; and the epigeneticmodification of snail host chromosomesduring the course of infection [15–17].Much work is needed to clarify themechanisms involved, work that can inCitation: Adema CM, Bayne CJ, Bridger JM, Knight M, Loker ES, et al. (2012) Will All Scientists Working on Snailsand the Diseases They Transmit Please Stand Up? PLoS Negl Trop Dis 6(12): e1835. doi:10.1371/journal.pntd.0001835Published December 27, 2012Copyright:  2012 Adema et al. This is an open-access article distributed under the terms of the CreativeCommons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium,provided the original author and source are credited.Funding: The authors received no funding for this work.Competing Interests: The authors have declared that no competing interests exist.* E-mail: mknight@afbr-bri.comDr. Coen Adema, Associate Professor, studies snail immunity and genomics at the Center of Theoretical andEvolutionary Immunology, Biology, University of New Mexico. Dr. Christopher J. Bayne is a comparativeimmunologist with interests in the evolution of immunity. His research focuses on gaining a deeperunderstanding of innate immune systems and their modulation, and exploits two model organisms: therainbow trout, in which he studies the inflammatory components of the acute phase response and effects ofstress on innate immunity, and molluscan schistosomiasis, in which he investigates the mechanisms thatdetermine susceptibility and resistance in this host–parasite system. Dr. Joanna Bridger is a Reader and a groupleader at Brunel University in London, UK, has spent over 20 years studying the spatial relationship between thestructures in cell nuclei and the regulation of genome behavior and gene expression in a variety of organisms,including the schistosome snail host. Dr. Matty Knight is a principal investigator at the Biomedical ResearchInstitute. For over 20 years, her research has focused on elucidating the molecular and genetic mechanismsunderlying snail–schistosome interactions. Dr. Eric Loker (Sam) has interests in the biological interplay betweenlarval schistosomes and the snails that serve as their intermediate hosts, particularly as they influence theepidemiology of schistosomiasis in Africa. In addition, his research focuses on the use of the snail as a modelsystem to provide new insights into the nature of invertebrate defense responses. Dr. Loker also investigatesthe diversity inherent among both mammalian and avian schistosomes using molecular phylogenetic andother methods. He is also involved in promoting and developing genomic resources for snails involved in thetransmission of schistosomiasis. Dr. Timothy Yoshino currently is a Professor of Parasitology and Director of theNIH-supported Cellular and Molecular Parasitology Training Program in the Department of PathobiologicalSciences, School of Veterinary Medicine, at the University of Wisconsin-Madison. His research is focused on themolecular mechanisms regulating larval schistosome–snail interactions. Dr. Si-Ming Zhang, Research AssociateProfessor, is interested in immunological and genetic mechanisms of snail and parasite interactions, and worksat Center for Evolutionary & Theoretical Immunology, University of New Mexico.PLOS Neglected Tropical Diseases | www.plosntds.org 1 December 2012 | Volume 6 | Issue 12 | e1835today’s difficult funding climate be justi-fied by its applicability to alleviating thelargely undiminished burden of snail-borne diseases. An excellent modernresearch toolkit justifies optimism thatnovel insights into Biomphalaria’s role inschistosomiasis transmission will be forth-coming. Microarray platforms [18,19],next-generation sequencing [20], andRNA interference enable functional tran-scriptomic studies of Biomphalaria snails[21–23]. A draft assembly of the B. glabratagenome sequence is fully available [24],comprising the third component of thegenome triad—human definitive host,parasite, and snail intermediate host—pertinent to schistosomiasis. The prospectsfor rapid development of similar tool kitsfor other important snail such as Bulinus,Lymnaea, and Oncomelania [25] are excellent.Such new molecular capabilities havegreat potential for application to fieldinvestigations and disease control. Theseinclude identifying genetic markers forcompatibility, developing sensitive meansto detect transmission in areas subjected tocontrol, and assessing receptors involvedin chemoattraction of parasite to host.Next-generation sequencing can identifythird party symbionts (bacteria or viruses)influencing snail-trematode interactions.The characterization of regulators ofparasite transmission in natural snailpopulation can contribute to the develop-ment of novel, ecologically friendly snailcontrol methods (e.g., feeding or phero-mone traps), and open up new lines ofstudy such as introduction of snail trans-genes capable of disrupting larval growth/differentiation. With so many snail-trans-mitted infections still at large, and so manyobvious approaches awaiting investigation,we sincerely hope that the decline in snail-related funding, with a concomitant de-cline in the number of trained investiga-tors, can be reversed. The availability ofyoung workers even able to identifymedically relevant snails has dropped toa shockingly low level.To conclude, it is an unchanging realitythat snails are essential for the continuedflourishing of snail-borne parasites, includ-ing those that cause schistosomiasis. Giventhe recent call for global elimination ofschistosomiasis, it is imperative we pursuea broader agenda that incorporates basicand applied snail research. From suchefforts can emerge integrated and moresustainable control strategies. This will alsohelp to arrest the alarming decline inyoung investigators, particularly in endem-ic countries. Given the considerable atten-tion currently focused on other parasiticdiseases such as malaria, could it be thatthe greatest opportunities to make signif-icant new advances in parasitology now liein other fields that have been trulyneglected?AcknowledgmentsThe constructive comments of three anonymousreviewers helped improve the manuscript.References1. Bruun B, Aagaard-Hansen J (2008) The socialcontext of schistosomiasis and its control. Anintroduction and annotated bibliography. Gene-va: World Health Organization, Special Pro-gramme for Research and Training in TropicalDisease.2. McManus DP, Gray DJ, Li Y, Feng Z, WilliamsGM, et al. (2010) Schistosomiasis in the People’sRepublic of China: the era of the Three GorgesDam. Clin Microbiol Rev 23: 442–466.3. Mas-Coma S, Valero MA, Bargues MD (2009)Fasciola, lymnaeids and human fascioliasis, with aglobal overview on disease transmission, epide-miology, evolutionary genetics, molecular epide-miology and control. Adv Parasitol 69: 41–146.4. Keiser J, Utzinger J (2009) Food-borne tremato-diases. Clin Microbiol Rev 22: 466–483.5. Aka NA, Adoubryn K, Rondelaud D, Dreyfuss G(2008) Human paragonimiasis in Africa. Ann AfrMed 7: 153–162.6. Attwood SW (2010) Studies on the parasitology,phylogeography and the evolution of host-para-site interactions for the snail intermediate hosts ofmedically important trematode genera in South-east Asia. Adv Parasitol 73: 405–440.7. Morley NJ (2010) Aquatic molluscs as auxiliaryhosts for terrestrial nematode parasites: implica-tions for pathogen transmission in a changingclimate. Parasitology 137: 1041–1056.8. World Health Organization (2012) Acceleratingwork to overcome the global impact of neglectedtropical diseases - a roadmap for implementation.Geneva: Department of Control of NeglectedTropical Diseases. Available: http://www.who.int/entity/neglected_diseases/NTD_RoadMap_2012_Fullversion.pdf. Accessed November 2012.9. Gray DJ, Mcanus DP, Li Y, Williams GM,Bergquist R, et al. (2010) Schistosomiasis elimi-nation: lessons from the past guide the future.Lancet Infect Dis 10: 733–736.10. Doenhoff MJ, Kusel JR, Coles GC, Cioli D(2002) Resistance of Schistosoma mansoni topraziquantel: is there a problem? Trans R SocTrop Med Hyg 96: 465–469.11. Seto EY, Wong BK, Lu D, Zhong B (2011)Human schistosomiasis resistance to praziquantelin China: should we be worried? Am J Trop MedHyg 85: 74–82.12. Melman SD, Steinauer ML, Cunningham C,Kubatko LS, Mwangi IN, et al. (2009) Reducedsusceptibility to praziquantel among naturallyoccurring Kenyan isolates of Schistosoma man-soni. PLoS Negl Trop Dis 3: e504. doi:10.1371/journal.pntd.0000504.13. Knox MR, Besier RB, Le Jambre LF, KaplanRM, Torres-Acosta JF, et al. (2012) Novelapproaches for the control of helminth parasitesof livestock VI: Summary of discussions andconclusions. Vet Parasitol 186: 143–149.14. Stensgaard A-S, Utzinger J, Vounatsou P, Hu¨rli-mann E, Schur N, et al. (2011) Large-scaledeterminants of intestinal schistosomiasis and inter-mediate host snail distribution across Africa: doesclimate matter? Acta Trop. E-pub ahead of print 28November 2011. doi:10.1016/j.actatropica.2011.11.010.15. Zhang S-M, Adema CM, Kepler TB, Loker ES(2004) Diversification of Ig superfamily genes inan invertebrate. Science 305: 251–254.16. Mitta G, Adema CM, Gourbal B, Loker ES,Theron A. (2012) Compatibility polymorphism insnail/schistosome interactions: from field totheory to molecular mechanisms. Dev CompImmunol 37: 1–8.17. Knight M, Ittiprasert W, Odoemelam EC,Adema CM, Miller A, et al. (2011) Non-randomorganization of the Biomphalaria glabrata ge-nome in interphase Bge cells and the spatialrepositioning of activated genes in cells co-cultured with Schistosoma mansoni. Int J Parasitol41: 61–70.18. Adema CM, Hanington PC, Lun CM, RosenbergGH, Aragon AD, et al. (2010) Differentialtranscriptomic responses of Biomphalaria glabrata(Gastropoda, Mollusca) to bacteria and metazoanparasites, Schistosoma mansoni and Echinostomaparaensei (Digenea, Platyhelminthes). Mol Immu-nol 47: 849–860.19. Lockyer AE, Spinks J, Kane RA, Hoffmann KF,Fitzpatrick JM, et al. (2008) Biomphalaria glabratatranscriptome: cDNA microarray profiling iden-tifies resistant- and susceptible-specific geneexpression in haemocytes from snail strainsexposed to Schistosoma mansoni. BMC Genomics9: 634.20. Deleury E, Dubreuil G, Elangovan N, WajnbergE, Reichhart JM, et al. (2012) Specific versus non-specific immune responses in an invertebratespecies evidenced by a comparative de novosequencing study. PLoS ONE 7: e32512.doi:10.1371/journal.pone.0032512.21. Baeza Garcia A, Pierce RJ, Gourbal B, Werkme-ister E, Colinet D, et al. (2010) Involvement of thecytokine MIF in the snail host immune responseto the parasite Schistosoma mansoni. PLoS Pathog 6:e1001115. doi:10.1371/journal.ppat.1001115.22. Hanington PC, Forys MA, Dragoo JW, Zhang S-M, Adema CM, et al. (2010) A role for asomatically diversified lectin in resistance of aninvertebrate to parasite infection. Proc Natl AcadSci U S A 107: 21087–21092.23. Hanington PC, Forys MA, Loker ES (2012) Asomatically diversified defense factor, FREP3, is adeterminant of snail resistance to schistosomeinfection. PLoS Negl Trop Dis 6: e1591.doi:10.1371/journal.pntd.0001591.24. Biomphalaria glabrata Genome Initiative. The draftassembly of Biomphalaria glabrata is availablethrough combined efforts of the BiomphalariaGenome Initiative, WUGI and NHGRI. Avail-able: http://biology.unm.edu/biomphalaria-genome/index.html. Accessed 26 November2012.25. Wang H, Zhao QP, Nie P, Jiang MS, Song J(2012) Identification of differentially expressedgenes in Oncomelania hupensis chronically infectedwith Schistosoma japonicum. Exp Parasitol 130: 374–83.PLOS Neglected Tropical Diseases | www.plosntds.org 2 December 2012 | Volume 6 | Issue 12 | e1835

A role for a somatically diversified lectin in resistance of an invertebrate to parasite infection.

A somatically diversified defense factor, FREP3, is a determinant of snail resistance to schistosome infection. PLoS Negl Trop Dis 6:

Aquatic molluscs as auxiliary hosts for terrestrial nematode parasites: implications for pathogen transmission in a changing climate.

Biomphalaria glabrata Genome Initiative. The draft assembly of Biomphalaria glabrata is available through combined efforts of the Biomphalaria Genome Initiative,

Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in haemocytes from snail strains exposed to Schistosoma mansoni.

Compatibility polymorphism in snail/schistosome interactions: from field to theory to molecular mechanisms.

Differential transcriptomic responses of Biomphalaria glabrata (Gastropoda, Mollusca) to bacteria and metazoan parasites, Schistosoma mansoni and Echinostoma paraensei (Digenea, Platyhelminthes).

Diversification of Ig superfamily genes in an invertebrate.

Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control.

Food-borne trematodiases.

Human paragonimiasis in Africa.

Human schistosomiasis resistance to praziquantel in China: should we be worried?

Identification of differentially expressed genes in Oncomelania hupensis chronically infected with Schistosoma japonicum.

Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni. PLoS Pathog 6:

Large-scale determinants of intestinal schistosomiasis and intermediate host snail distribution across Africa: does climate matter? Acta Trop.E-pub ahead ofprint 28

Non-random organization of the Biomphalaria glabrata genome in interphase Bge cells and the spatial repositioning of activated genes in cells cocultured with Schistosoma mansoni.

Novel approaches for the control of helminth parasites of livestock VI: Summary of discussions and conclusions.

Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl Trop Dis 3: e504. doi:10.1371/ journal.pntd.0000504.

Resistance of Schistosoma mansoni to praziquantel: is there a problem? Trans R Soc Trop Med Hyg 96:

Schistosomiasis elimination: lessons from the past guide the future.

Schistosomiasis in the People’s Republic of China: the era of the Three Gorges Dam.

Specific versus nonspecific immune responses in an invertebrate species evidenced by a comparative de novo sequencing study.

Studies on the parasitology, phylogeography and the evolution of host-parasite interactions for the snail intermediate hosts of medically important trematode genera in Southeast Asia.

The social context of schistosomiasis and its control. An introduction and annotated bibliography. Geneva: World Health Organization, Special Programme for Research and Training in Tropical Disease.

Tropical Diseases |

Will all scientists working on snails and the diseases they transmit please stand up?

Coen M Adema

Christopher J Bayne

Joanna M Bridger

Eric S Loker

Timothy P Yoshino

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Will All Scientists Working on Snails and the Diseases They Transmit Please Stand Up?

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Will all scientists working on snails and the diseases they transmit please stand up?

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Brunel University Research Archive

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