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Featured Article

BMC Cancer
April 2015

A microRNA profile associated with Opisthorchis viverrini-induced cholangiocarcinoma in tissue and plasma

Jordan Plieskatt, Gabriel Rinaldi, Yanjun Feng, Jin Peng, Samantha Easley,Xinying Jia, Jeremy Potriquet, Chawalit Pairojkul, Vajarabhongsa Bhudhisawasdi,Banchob Sripa, Paul J Brindley, Jeffrey Bethony and Jason Mulvenna

Background

Intrahepatic cholangiocarcinoma (ICC) is a highly aggressive tumor of the bile duct, and a significant public health problem in East Asia, where it is associated with infection by the parasiteOpisthorchis viverrini. ICC is often detected at an advanced stage and with a poor prognosis, making a biomarker for early detection a priority.

Methods

We have comprehensively profiled miRNA expression levels in ICC tumor tissue using small RNA-Seq and validated these profiles using quantitative PCR on matched plasma samples.

Results

Distinct miRNA profiles were associated with increasing histological differentiation of ICC tumor tissue. We also observed that histologically normal tissue adjacent to ICC tumor displayed miRNA expression profiles more similar to tumor than liver tissue from healthy donors. In plasma samples, an eight-miRNA signature associated with ICC, regardless of the degree of histological differentiation of its matched tissue, forming the basis of a circulating miRNA-based biomarker for ICC.

Conclusions

The association of unique miRNA profiles with different ICC subtypes suggests the involvement of specific miRNAs during ICC tumor progression. In plasma, an eight-miRNA signature associated with ICC could form the foundation of an accessible (plasma-based) miRNA-based biomarker for the early detection of ICC.

Copyright © 2015 BMC Cancer

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2015 Publications

Chaiyadet S, Sotillo J, Smout M, Cantacessi C, Jones MK, Johnson MS, Turnbull L, Whitchurch CB, Potriquet J, Laohaviroj M, Mulvenna J, Brindley PJ, Bethony JM, Laha T, Sripa B, Loukas A.
Carcinogenic Liver Fluke Secretes Extracellular Vesicles That Promote Cholangiocytes to Adopt a Tumorigenic Phenotype.
J Infect Dis. 2015 Nov 15;212(10):1636-45.

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Worasith C, Kamamia C, Yakovleva A, Duenngai K, Wangboon C, Sithithaworn J, Watwiengkam N, Namwat N, Techasen A, Loilome W, Yongvanit P, Loukas A, Sithithaworn P, Bethony JM.
Advances in the Diagnosis of Human Opisthorchiasis: Development of Opisthorchis viverrini Antigen Detection in Urine.
PLoS Negl Trop Dis. 2015 Oct 20;9(10):e0004157.

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Periago MV, Diniz RC, Pinto SA, Yakovleva A, Correa-Oliveira R, Diemert DJ, Bethony JM.
The Right Tool for the Job: Detection of Soil-Transmitted Helminths in Areas Co-endemic for Other Helminths.
PLoS Negl Trop Dis. 2015 Aug 4;9(8):e0003967.

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Saichua P, Yakovleva A, Kamamia C, Jariwala AR, Sithithaworn J, Sripa B, Brindley PJ, Laha T, Mairiang E, Pairojkul C, Khuntikeo N, Mulvenna J, Sithithaworn P, Bethony JM.
Levels of 8-OxodG Predict Hepatobiliary Pathology in Opisthorchis viverrini Endemic Settings in Thailand.
PLoS Negl Trop Dis. 2015 Jul 31;9(7):e0003949.

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Mark S Pearson, Amar R Jariwala, Giovanni Abbenante, Jordan Plieskatt, David Wilson, Maria Elena Bottazzi, Peter J Hotez, Brian Keegan, Jeffrey M Bethony & Alex Loukas.
New tools for NTD vaccines: A case study of quality control assays for product development of the human hookworm vaccine Na-APR-1M74. 
Hum Vaccin Immunother. 2015. May 27. pages 1251-1257.

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Pearson MS, Becker L, Driguez P, Young ND, Gaze S, Mendes T, Li XH, Doolan DL, Midzi N, Mduluza T, McManus DP, Wilson RA, Bethony JM, Nausch N, Mutapi F, Felgner PL, Loukas A. 
Of monkeys and men: immunomic profiling of sera from humans and non-human primates resistant to schistosomiasis reveals novel potential vaccine candidates. 
Front Immunol. 2015 May 5;6:213

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Chaiyadet S, Sotillo J, Smout M, Cantacessi C, Jones MK, Johnson MS, Turnbull L, Whitchurch CB, Potriquet J, Laohaviroj M, Mulvenna J, Brindley PJ, Bethony JM, Laha T, Sripa B, Loukas A. 
Carcinogenic liver fluke secretes extracellular vesicles that promote cholangiocytes to adopt a tumorigenic phenotype.
J Infect Dis. 2015 May 17

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Plieskatt J, Rinaldi G, Feng Y, Peng J, Easley S, Jia X, Potriquet J, Pairojkul C, Bhudhisawasdi V, Sripa B, Brindley PJ, Bethony J, Mulvenna J.
A microRNA profile associated with Opisthorchis viverrini-induced cholangiocarcinoma in tissue and plasma. 
BMC Cancer. 2015 Apr 23;15(1):309.

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2014 Publications

Lobato L, Bethony JM, Pereira FB, Grahek SL, Diemert D, Gazzinelli MF.
Impact of gender on the decision to participate in a clinical trial: a cross-sectional study. 
BMC Public Health. 2014 Nov 6;14:1156. doi: 10.1186/1471-2458-14-1156.

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Gaze S, Bethony JM, Periago MV. 
Immunology of experimental and natural human hookworm infection. 
Parasite Immunol. 2014 Aug;36(8):358-66. Review.

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Papatpremsiri A, Junpue P, Loukas A, Brindley PJ, Bethony JM, Sripa B, Laha T. 
Immunization and challenge shown by hamsters infected with Opisthorchis viverrini following exposure to gamma-irradiated metacercariae of this carcinogenic liver fluke.
J Helminthol. 2014 Oct 15:1-9.

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Levecke B, Montresor A, Albonico M, Ame SM, Behnke JM, Bethony JM, Noumedem CD, Engels D, Guillard B, Kotze AC, Krolewiecki AJ, McCarthy JS, Mekonnen Z, Periago MV, Sopheak H, Tchuem-Tchuenté LA, Duong TT, Huong NT, Zeynudin A, Vercruysse J.
Assessment of anthelmintic efficacy of mebendazole in school children in six countries where soil-transmitted helminths are endemic. 
PLoS Negl Trop Dis. 2014 Oct 9;8(10):e3204. 

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Jin Peng, Yanjun Feng, Gabriel Rinaldi, Paul Levine, Samantha Easley, Elizabeth Martinez, Salman Hashmi, Nader Sadeghi, Paul J. Brindley, Jason P. Mulvenna, Jeffrey M. Bethony, Jordan L. Plieskatt.
The miRNAome of Opisthorchis viverrini induced intrahepatic cholangiocarcinoma.
Genomics Data. 2014. Pages 285-289.

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Jin Peng, Yanjun Feng, Gabriel Rinaldi, Ponlapat Yonglitthipagon, Samantha E. Easley, Therawach Laha, Chawalit Pairojkul, Vajarabhongsa Bhudhisawasdi, Banchob Sripa, Paul J. Brindley, Jason P. Mulvenna, Jeffrey M. Bethony, Jordan L. Plieskatt
Profiling miRNAs in nasopharyngeal carcinoma FFPE tissue by microarray and Next Generation Sequencing.
Genomics Data. 2014. Pages 274-279

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Plieskatt JL, Feng Y, Rinaldi G, Mulvenna JP, Bethony JM, Brindley PJ.
Circumventing qPCR inhibition to amplify miRNAs in plasma.
Biomark Res. 2014 Jul 22;2:13.

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Plieskatt JL, Rinaldi G, Feng Y, Peng J, Yonglitthipagon P, Easley S, Laha T, Pairojkul C, Bhudhisawasdi V, Sripa B, Brindley PJ, Mulvenna JP, Bethony JM.
Distinct miRNA signatures associate with subtypes of cholangiocarcinoma from infection with the tumourigenic liver fluke Opisthorchis viverrini.
J Hepatol. 2014 Jun 3. PubMed PMID: 25017828.

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Plieskatt J, Rinaldi G, Brindley PJ, Jia X, Potriquet J, Bethony J, Mulvenna J. 
Bioclojure: a functional library for the manipulation of biological sequences. 
Bioinformatics. 2014 May 2. PubMed PMID: 24794932.

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Pinot de Moira A, Fitzsimmons CM, Jones FM, Wilson S, Cahen P, Tukahebwa E, Mpairwe H, Mwatha JK, Bethony JM, Skov PS, Kabatereine NB, Dunne DW.
Suppression of Basophil Histamine Release and Other IgE-dependent Responses in Childhood Schistosoma mansoni/hookworm Coinfection.
J Infect Dis. 2014 Apr 29. PubMed PMID: 24782451.

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Gaze S, Driguez P, Pearson MS, Mendes T, Doolan DL, Trieu A, McManus DP, Gobert GN, Periago MV, Correa Oliveira R, Cardoso FC, Oliveira G, Nakajima R, Jasinskas A, Hung C, Liang L, Pablo J, Bethony JM, Felgner PL, Loukas A.
An immunomics approach to schistosome antigen discovery: antibody signatures of naturally resistant and chronically infected individuals from endemic areas.
PLoS Pathog. 2014 Mar 27;10(3):e1004033. PubMed PMID: 24675823.

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Tang YT, Gao X, Rosa BA, Abubucker S, Hallsworth-Pepin K, Martin J, Tyagi R, Heizer E, Zhang X, Bhonagiri-Palsikar V, Minx P, Warren WC, Wang Q, Zhan B, Hotez PJ, Sternberg PW, Dougall A, Gaze ST, Mulvenna J, Sotillo J, Ranganathan S, Rabelo EM, Wilson RK, Felgner PL, Bethony J, Hawdon JM, Gasser RB, Loukas A, Mitreva M.
Genome of the human hookworm Necator americanus.
Nat Genet. 2014 Mar;46(3):261-9. PubMed PMID: 24441737.

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Aka P, Emmanuel B, Vila MC, Jariwala A, Nkrumah F, Periago MV, Neequaye J, Kiruthu C, Levine PH, Biggar RJ, Bhatia K, Bethony JM, Mbulaiteye SM.
Elevated serum levels of interleukin-6 in endemic Burkitt lymphoma in Ghana.
Hematol Oncol. 2014 Jan 6. PubMed PMID: 24493366.

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Plieskatt JL, Rinaldi G, Feng Y, Levine PH, Easley S, Martinez E, Hashmi S, Sadeghi N, Brindley PJ, Bethony JM, Mulvenna JP.
Methods and matrices: approaches to identifying miRNAs for Nasopharyngeal carcinoma.
J Transl Med. 2014 Jan 6;12:3. PubMed PMID: 24393330.

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2013 Publications

Plieskatt JL, Deenonpoe R, Mulvenna JP, Krause L, Sripa B, Bethony JM, Brindley PJ. Infection with the carcinogenic liver fluke Opisthorchis viverrini modifies intestinal and biliary microbiome. FASEB J. 2013 Nov;27(11):4572-84. PubMed PMID: 23925654.

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Curti E, Kwityn C, Zhan B, Gillespie P, Brelsford J, Deumic V, Plieskatt J, Rezende WC, Tsao E, Kalampanayil B, Hotez PJ, Bottazzi ME. Expression at a 20L scale and purification of the extracellular domain of the Schistosoma mansoni TSP-2 recombinant protein: a vaccine candidate for human intestinal schistosomiasis. Hum Vaccin Immunother. 2013 Nov;9(11):2342-50. PubMed PMID: 23899507

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Cheng W, Curti E, Rezende WC, Kwityn C, Zhan B, Gillespie P, Plieskatt J, Joshi SB, Volkin DB, Hotez PJ, Middaugh CR, Bottazzi ME. Biophysical and formulation studies of the Schistosoma mansoni TSP-2 extracellular domain recombinant protein, a lead vaccine candidate antigen for intestinal schistosomiasis. Hum Vaccin Immunother. 2013 Nov;9(11):2351-61. PubMed PMID: 23880663.

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Aka P, Vila MC, Jariwala A, Nkrumah F, Emmanuel B, Yagi M, Palacpac NM, Periago MV, Neequaye J, Kiruthu C, Tougan T, Levine PH, Biggar RJ, Pfeiffer RM, Bhatia K, Horii T, Bethony JM, Mbulaiteye SM. Endemic Burkitt lymphoma is associated with strength and diversity of Plasmodium falciparum malaria stage-specific antigen antibody response. Blood. 2013 Aug 1;122(5):629-35. PubMed PMID: 23645841.

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Goud GN, Deumic V, Gupta R, Brelsford J, Zhan B, Gillespie P, Plieskatt JL, Tsao EI, Hotez PJ, Bottazzi ME. Expression, purification, and molecular analysis of the Necator americanus glutathione S-transferase 1 (Na-GST-1): a production process developed for a lead candidate recombinant hookworm vaccine antigen. Protein Expr Purif. 2012 Jun;83(2):145-51. PubMed PMID: 22503665.

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Plieskatt JL, Rezende WC, Olsen CM, Trefethen JM, Joshi SB, Middaugh CR, Hotez PJ, Bottazzi ME. Advances in vaccines against neglected tropical diseases: enhancing physical stability of a recombinant hookworm vaccine through biophysical and formulation studies. Hum Vaccin Immunother. 2012 Jun;8(6):765-76. PubMed PMID: 22495115.

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Geiger SM, Jardim-Botelho A, Williams W, Alexander N, Diemert DJ, Bethony JM. Serum CCL11 (eotaxin-1) and CCL17 (TARC) are serological indicators of multiple helminth infections and are driven by Schistosoma mansoni infection in humans. Trop Med Int Health. 2013 Jun;18(6):750-60. PubMed PMID: 23496801.

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Saichua P, Sithithaworn P, Jariwala AR, Diemert DJ, Sithithaworn J, Sripa B, Laha T, Mairiang E, Pairojkul C, Periago MV, Khuntikeo N, Mulvenna J, Bethony JM. Microproteinuria during Opisthorchis viverrini infection: a biomarker for advanced renal and hepatobiliary pathologies from chronic opisthorchiasis. PLoS Negl Trop Dis. 2013 May 23;7(5):e2228. PubMed PMID: 23717698.

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Hotez PJ, Diemert D, Bacon KM, Beaumier C, Bethony JM, Bottazzi ME, Brooker S, Couto AR, Freire Mda S, Homma A, Lee BY, Loukas A, Loblack M, Morel CM, Oliveira RC, Russell PK. The Human Hookworm Vaccine. Vaccine. 2013 Apr 18;31 Suppl 2:B227-32. Review. PubMed PMID: 23598487.

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Pinot de Moira A, Jones FM, Wilson S, Tukahebwa E, Fitzsimmons CM, Mwatha JK, Bethony JM, Kabatereine NB, Dunne DW. Effects of treatment on IgE responses against parasite allergen-like proteins and immunity to reinfection in childhood schistosome and hookworm coinfections. Infect Immun. 2013 Jan;81(1):23-32. PubMed PMID: 23071136.

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2012 Publications

Sripa B, Brindley PJ, Mulvenna J, Laha T, Smout MJ, Mairiang E, Bethony JM, Loukas A. The tumorigenic liver fluke Opisthorchis viverrini--multiple pathways to cancer. Trends Parasitol. 2012 Oct;28(10):395-407. Review. PubMed PMID: 22947297

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Yonglitthipagon P, Pairojkul C, Chamgramol Y, Loukas A, Mulvenna J, Bethony J, Bhudhisawasdi V, Sripa B. Prognostic significance of peroxiredoxin 1 and ezrin-radixin-moesin-binding phosphoprotein 50 in cholangiocarcinoma. Hum Pathol. 2012 Oct;43(10):1719-30. PubMed PMID: 22446018.

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Lobato L, Miranda A, Faria IM, Bethony JM, Gazzinelli MF. Development of cognitive abilities of children infected with helminths through health education. Rev Soc Bras Med Trop. 2012 Jul-Aug;45(4):514-9. PubMed PMID: 22930049.

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Pearson MS, Tribolet L, Cantacessi C, Periago MV, Valero MA, Jariwala AR, Hotez P, Diemert D, Loukas A, Bethony J. Molecular mechanisms of hookworm disease: stealth, virulence, and vaccines. J Allergy Clin Immunol. 2012 Jul;130(1):13-21. Review. PubMed PMID: 22742835.

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Diemert DJ, Pinto AG, Freire J, Jariwala A, Santiago H, Hamilton RG, Periago MV, Loukas A, Tribolet L, Mulvenna J, Correa-Oliveira R, Hotez PJ, Bethony JM. Generalized urticaria induced by the Na-ASP-2 hookworm vaccine: implications for the development of vaccines against helminths. J Allergy Clin Immunol. 2012 Jul;130(1):169-76.e6. PubMed PMID: 22633322.

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Sripa B, Thinkhamrop B, Mairiang E, Laha T, Kaewkes S, Sithithaworn P, Periago MV, Bhudhisawasdi V, Yonglitthipagon P, Mulvenna J, Brindley PJ, Loukas A, Bethony JM. Elevated plasma IL-6 associates with increased risk of advanced fibrosis and cholangiocarcinoma in individuals infected by Opisthorchis viverrini. PLoS Negl Trop Dis. 2012;6(5):e1654. PubMed PMID: 22629477.

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Mathias DK, Plieskatt JL, Armistead JS, Bethony JM, Abdul-Majid KB, McMillan A, Angov E, Aryee MJ, Zhan B, Gillespie P, Keegan B, Jariwala AR, Rezende W, Bottazzi ME, Scorpio DG, Hotez PJ, Dinglasan RR. Expression, immunogenicity, histopathology, and potency of a mosquito-based malaria transmission-blocking recombinant vaccine. Infect Immun. 2012 Apr;80(4):1606-14. PubMed PMID: 22311924.

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Pearson MS, Pickering DA, McSorley HJ, Bethony JM, Tribolet L, Dougall AM, Hotez PJ, Loukas A. Enhanced protective efficacy of a chimeric form of the schistosomiasis vaccine antigen Sm-TSP-2. PLoS Negl Trop Dis. 2012;6(3):e1564. Epub 2012 Mar 13. PubMed PMID: 22428079.

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Gaze S, McSorley HJ, Daveson J, Jones D, Bethony JM, Oliveira LM, Speare R, McCarthy JS, Engwerda CR, Croese J, Loukas A. Characterising the mucosal and systemic immune responses to experimental human hookworm infection. PLoS Pathog. 2012 Feb;8(2):e1002520. PubMed PMID: 22346753.

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2011 Publications

Geiger SM, Fujiwara RT, Freitas PA, Massara CL, Dos Santos Carvalho O, Corrêa-Oliveira R, Bethony JM. Excretory-secretory products from hookworm l(3) and adult worms suppress proinflammatory cytokines in infected individuals. J Parasitol Res. 2011;2011:512154. PubMed PMID: 21772981.

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2010 Publications

Jariwala AR, Oliveira LM, Diemert DJ, Keegan B, Plieskatt JL, Periago MV, Bottazzi ME, Hotez PJ, Bethony JM. Potency testing for the experimental Na-GST-1 hookworm vaccine. Expert Rev Vaccines. 2010 Oct;9(10):1219-30. PubMed PMID: 20923271.

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Quinnell RJ, Pullan RL, Breitling LP, Geiger SM, Cundill B, Correa-Oliveira R, Brooker S, Bethony JM. Genetic and household determinants of predisposition to human hookworm infection in a Brazilian community. J Infect Dis. 2010 Sep 15;202(6):954-61. PubMed PMID: 20681887.

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Pearson MS, Pickering DA, Tribolet L, Cooper L, Mulvenna J, Oliveira LM, Bethony JM, Hotez PJ, Loukas A. Neutralizing antibodies to the hookworm hemoglobinase Na-APR-1: implications for a multivalent vaccine against hookworm infection and schistosomiasis. J Infect Dis. 2010 May 15;201(10):1561-9. PubMed PMID: 20367477.

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Pullan RL, Bethony JM, Geiger SM, Correa-Oliveira R, Brooker S, Quinnell RJ. Human helminth co-infection: no evidence of common genetic control of hookworm and Schistosoma mansoni infection intensity in a Brazilian community. Int J Parasitol. 2010 Mar 1;40(3):299-306. PubMed PMID: 19699204.

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2009 Publications

Pearson MS, Bethony JM, Pickering DA, de Oliveira LM, Jariwala A, Santiago H, Miles AP, Zhan B, Jiang D, Ranjit N, Mulvenna J, Tribolet L, Plieskatt J, Smith T, Bottazzi ME, Jones K, Keegan B, Hotez PJ, Loukas A. An enzymatically inactivated hemoglobinase from Necator americanus induces neutralizing antibodies against multiple hookworm species and protects dogs against heterologous hookworm infection. FASEB J. 2009 Sep;23(9):3007-19. PubMed PMID: 19380510.

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2008 Publications

Don TA, Bethony JM, Loukas A. Saposin-like proteins are expressed in the gastrodermis of Schistosoma mansoni and are immunogenic in natural infections. Int J Infect Dis. 2008 Nov;12(6):e39-47. PubMed PMID: 18571965.

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Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J. Helminth infections: the great neglected tropical diseases. J Clin Invest. 2008 Apr;118(4):1311-21. Review. PubMed PMID: 18382743.

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2006 Publications

Brooker S, Alexander N, Geiger S, Moyeed RA, Stander J, Fleming F, Hotez PJ, Correa-Oliveira R, Bethony J. Contrasting patterns in the small-scale heterogeneity of human helminth infections in urban and rural environments in Brazil. Int J Parasitol. 2006 Sep;36(10-11):1143-51. PubMed PMID: 16814294.

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2005 Publications

Bethony J, Loukas A, Smout M, Brooker S, Mendez S, Plieskatt J, Goud G, Bottazzi ME, Zhan B, Wang Y, Williamson A, Lustigman S, Correa-Oliveira R, Xiao S, Hotez PJ. Antibodies against a secreted protein from hookworm larvae reduce the intensity of hookworm infection in humans and vaccinated laboratory animals. FASEB J. 2005 Oct;19(12):1743-5. PubMed PMID: 16037096.

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2004 Publications

Quinnell RJ, Bethony J, Pritchard DI. The immunoepidemiology of human hookworm infection. Parasite Immunol. 2004 Nov-Dec;26(11-12):443-54. Review. PubMed PMID: 15771680.

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Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S. Hookworm infection. N Engl J Med. 2004 Aug 19;351(8):799-807. Review. PubMed PMID:15317893.

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Hsieh GC, Loukas A, Wahl AM, Bhatia M, Wang Y, Williamson AL, Kehn KW, Maruyama H, Hotez PJ, Leitenberg D, Bethony J, Constant SL. A secreted protein from the human hookworm necator americanus binds selectively to NK cells and induces IFN-gamma production. J Immunol. 2004 Aug 15;173(4):2699-704. PubMed PMID: 15294988.

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Portela RW, Bethony J, Costa MI, Gazzinelli A, Vitor RW, Hermeto FM, Correa-Oliveira R, Gazzinelli RT. A multihousehold study reveals a positive correlation between age, severity of ocular toxoplasmosis, and levels of glycoinositolphospholipid-specific immunoglobulin A. J Infect Dis. 2004 Jul 1;190(1):175-83. PubMed PMID: 15195258.

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Loukas A, Bethony JM, Williamson AL, Goud GN, Mendez S, Zhan B, Hawdon JM, Elena Bottazzi M, Brindley PJ, Hotez PJ. Vaccination of dogs with a recombinant cysteine protease from the intestine of canine hookworms diminishes the fecundity and growth of worms. J Infect Dis. 2004 May 15;189(10):1952-61. PubMed PMID: 15122534.

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2003 Publications

Hotez PJ, Ashcom J, Zhan B, Bethony J, Loukas A, Hawdon J, Wang Y, Jin Q, Jones KC, Dobardzic A, Dobardzic R, Bolden J, Essiet I, Brandt W, Russell PK, Zook BC, Howard B, Chacon M. Effect of vaccination with a recombinant fusion protein encoding an astacinlike metalloprotease (MTP-1) secreted by host-stimulated Ancylostoma caninum third-stage infective larvae. J Parasitol. 2003 Aug;89(4):853-5. PubMed PMID: 14533704.

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Hotez PJ, Zhan B, Bethony JM, Loukas A, Williamson A, Goud GN, Hawdon JM, Dobardzic A, Dobardzic R, Ghosh K, Bottazzi ME, Mendez S, Zook B, Wang Y, Liu S, Essiet-Gibson I, Chung-Debose S, Xiao S, Knox D, Meagher M, Inan M, Correa-Oliveira R, Vilk P, Shepherd HR, Brandt W, Russell PK. Progress in the development of a recombinant vaccine for human hookworm disease: the Human Hookworm Vaccine Initiative. Int J Parasitol. 2003 Sep 30;33(11):1245-58. Review. PubMed PMID: 13678639.

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2002 Publications

Bethony J, Williams JT, Blangero J, Kloos H, Gazzinelli A, Soares-Filho B, Coelho L, Alves-Fraga L, Williams-Blangero S, Loverde PT, Correa-Oliveira R. Additive host genetic factors influence fecal egg excretion rates during Schistosoma mansoni infection in a rural area in Brazil. Am J Trop Med Hyg. 2002 Oct;67(4):336-43. PubMed PMID: 12452486.

Silveira AM, Bethony J, Gazzinelli A, Kloos H, Fraga LA, Alvares MC, Prata A, Guerra HL, Loverde PT, Correa-Oliveira R, Gazzinelli G. High levels of IgG4 to Schistosoma mansoni egg antigens in individuals with periportal fibrosis. Am J Trop Med Hyg. 2002 May;66(5):542-9. PubMed PMID: 12201588.

Hotez PJ, Ashcom J, Bin Z, Bethony J, Williamson A, Hawdon JM, Jianjun F, Dobardzic A, Rizo I, Bolden J, Jin Q, Yan W, Dobardzic R, Chung-Debose S, Crowell M, Datu B, Delaney A, Dragonovski D, Jiang Y, Yueyuan L, Ghosh K, Loukas A, Brandt W, Russell PK, Zook BC. Effect of vaccinations with recombinant fusion proteins on Ancylostoma caninum habitat selection in the canine intestine. J Parasitol. 2002 Aug;88(4):684-90. PubMed PMID: 12197114.

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2000 and Prior Publications

Bethony J, Silveira AM, Alves-Oliveira LF, Thakur A, Gazzinelli G, Correa-Oliveira R, LoVerde PT. Familial resemblance in humoral immune response to defined and crude Schistosoma mansoni antigens in an endemic area in Brazil. J Infect Dis. 1999 Nov;180(5):1665-73. Erratum in: J Infect Dis 1999 Dec;180(6):2091. PubMed PMID: 10515830.

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Hotez PJ, Ghosh K, Hawdon J, Narasimhan S, Jones B, Bethony J. Vaccines for hookworm infection. Pediatr Infect Dis J. 1997 Oct;16(10):935-40. Review. PubMed PMID: 9380467.

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