{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T18:29:37Z","timestamp":1791224977102,"version":"4.1.0"},"reference-count":70,"publisher":"American Society for Microbiology","issue":"4","license":[{"start":{"date-parts":[[2010,4,1]],"date-time":"2010-04-01T00:00:00Z","timestamp":1270080000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["Infect Immun"],"published-print":{"date-parts":[[2010,4]]},"abstract":"<jats:title>ABSTRACT<\/jats:title><jats:p>Hookworm glutathione<jats:italic>S<\/jats:italic>-transferases (GSTs) are critical for parasite blood feeding and survival and represent potential targets for vaccination. Three cDNAs, each encoding a full-length GST protein from the human hookworm<jats:italic>Necator americanus<\/jats:italic>(and designated<jats:italic>Na<\/jats:italic>-GST-1,<jats:italic>Na<\/jats:italic>-GST-2, and<jats:italic>Na<\/jats:italic>-GST-3, respectively) were isolated from cDNA based on their sequence similarity to<jats:italic>Ac<\/jats:italic>-GST-1, a GST from the dog hookworm<jats:italic>Ancylostoma caninum<\/jats:italic>. The open reading frames of the three<jats:italic>N. americanus<\/jats:italic>GSTs each contain 206 amino acids with 51% to 69% sequence identity between each other and<jats:italic>Ac<\/jats:italic>-GST-1. Sequence alignment with GSTs from other organisms shows that the three<jats:italic>Na<\/jats:italic>-GSTs belong to a nematode-specific nu-class GST family. All three<jats:italic>Na<\/jats:italic>-GSTs, when expressed in<jats:italic>Pi<\/jats:italic><jats:italic>chia pastoris<\/jats:italic>, exhibited low lipid peroxidase and glutathione-conjugating enzymatic activities but high heme-binding capacities, and they may be involved in the detoxification and\/or transport of heme. In two separate vaccine trials, recombinant<jats:italic>Na<\/jats:italic>-GST-1 formulated with Alhydrogel elicited 32 and 39% reductions in adult hookworm burdens (<jats:italic>P<\/jats:italic>&lt; 0.05) following<jats:italic>N. americanus<\/jats:italic>larval challenge relative to the results for a group immunized with Alhydrogel alone. In contrast, no protection was observed in vaccine trials with<jats:italic>Na<\/jats:italic>-GST-2 or<jats:italic>Na<\/jats:italic>-GST-3. On the basis of these and other preclinical data,<jats:italic>Na<\/jats:italic>-GST-1 is under possible consideration for further vaccine development.<\/jats:p>","DOI":"10.1128\/iai.00848-09","type":"journal-article","created":{"date-parts":[[2010,2,10]],"date-time":"2010-02-10T05:06:30Z","timestamp":1265778390000},"page":"1552-1563","update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":100,"title":["Molecular Cloning, Biochemical Characterization, and Partial Protective Immunity of the Heme-Binding Glutathione<i>S<\/i>-Transferases from the Human Hookworm<i>Necator americanus<\/i>"],"prefix":"10.1128","volume":"78","author":[{"given":"Bin","family":"Zhan","sequence":"first","affiliation":[{"name":"Department of Microbiology, Immunology and Tropical Medicine, The George Washington University, and Sabin Vaccine Institute, Washington, DC 20037"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samirah","family":"Perally","sequence":"additional","affiliation":[{"name":"Institute of Biological, Environmental and Rural Sciences (IBERS), Aberystwyth University, Aberystwyth, Wales SY23 3DA, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter M.","family":"Brophy","sequence":"additional","affiliation":[{"name":"Institute of Biological, Environmental and Rural Sciences (IBERS), Aberystwyth University, Aberystwyth, Wales SY23 3DA, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jian","family":"Xue","sequence":"additional","affiliation":[{"name":"National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai 200025, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gaddam","family":"Goud","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology and Tropical Medicine, The George Washington University, and Sabin Vaccine Institute, Washington, DC 20037"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sen","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology and Tropical Medicine, The George Washington University, and Sabin Vaccine Institute, Washington, DC 20037"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vehid","family":"Deumic","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology and Tropical Medicine, The George Washington University, and Sabin Vaccine Institute, Washington, DC 20037"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luciana M.","family":"de Oliveira","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology and Tropical Medicine, The George Washington University, and Sabin Vaccine Institute, Washington, DC 20037"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeffrey","family":"Bethony","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology and Tropical Medicine, The George Washington University, and Sabin Vaccine Institute, Washington, DC 20037"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Elena","family":"Bottazzi","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology and Tropical Medicine, The George Washington University, and Sabin Vaccine Institute, Washington, DC 20037"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Desheng","family":"Jiang","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology and Tropical Medicine, The George Washington University, and Sabin Vaccine Institute, Washington, DC 20037"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Portia","family":"Gillespie","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology and Tropical Medicine, The George Washington University, and Sabin Vaccine Institute, Washington, DC 20037"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shu-hua","family":"Xiao","sequence":"additional","affiliation":[{"name":"National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai 200025, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richi","family":"Gupta","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology and Tropical Medicine, The George Washington University, and Sabin Vaccine Institute, Washington, DC 20037"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alex","family":"Loukas","sequence":"additional","affiliation":[{"name":"Queensland Institute of Medical Research, Brisbane, Queensland 4006, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Najju","family":"Ranjit","sequence":"additional","affiliation":[{"name":"Queensland Institute of Medical Research, Brisbane, Queensland 4006, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara","family":"Lustigman","sequence":"additional","affiliation":[{"name":"Department of Virology and Parasitology, The Lindsley F. Kimball Research Institute of the New York Blood Center, New York, New York 10021"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yelena","family":"Oksov","sequence":"additional","affiliation":[{"name":"Department of Virology and Parasitology, The Lindsley F. Kimball Research Institute of the New York Blood Center, New York, New York 10021"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Hotez","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology and Tropical Medicine, The George Washington University, and Sabin Vaccine Institute, Washington, DC 20037"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_2_2_2","first-page":"343","volume":"81","year":"2003","unstructured":"Albonico, M., Q. Bickle, M. Ramsan, A. Montresor, L. Savioli, and M. Taylor. 2003. Efficacy of mebendazole and levamisole alone or in combination against intestinal nematode infections after repeated targeted mebendazole treatment in Zanzibar. Bull. World Health Organ.81:343-352.","journal-title":"Bull. World Health Organ."},{"key":"e_1_3_2_3_2","doi-asserted-by":"publisher","DOI":"10.1016\/0035-9203(95)90101-9"},{"key":"e_1_3_2_4_2","doi-asserted-by":"publisher","DOI":"10.1186\/1472-6807-7-42"},{"key":"e_1_3_2_5_2","doi-asserted-by":"crossref","first-page":"3448","DOI":"10.4049\/jimmunol.138.10.3448","volume":"138","year":"1987","unstructured":"Balloul, J. M., J. M. Grzych, R. J. Pierce, and A. Capron. 1987. A purified 28,000 dalton protein from Schistosoma mansoni adult worms protects rats and mice against experimental schistosomiasis. J. Immunol.138:3448-3453.","journal-title":"J. Immunol."},{"key":"e_1_3_2_6_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0166-6851(02)00253-0"},{"key":"e_1_3_2_7_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0169-4758(99)01544-6"},{"key":"e_1_3_2_8_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0264-410X(98)00202-3"},{"key":"e_1_3_2_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/0006-2952(91)90699-6"},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0000291"},{"key":"e_1_3_2_11_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.trstmh.2006.05.012"},{"key":"e_1_3_2_12_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0031182000061369"},{"key":"e_1_3_2_13_2","doi-asserted-by":"publisher","DOI":"10.1016\/0001-706X(95)00084-R"},{"key":"e_1_3_2_14_2","doi-asserted-by":"publisher","DOI":"10.1016\/0020-7519(92)90061-O"},{"key":"e_1_3_2_15_2","first-page":"233","volume":"5","year":"1989","unstructured":"Cabot, E. L., and A. T. Beckenbach. 1989. Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Comput. Appl. Biosci.5:233-234.","journal-title":"Comput. Appl. Biosci."},{"key":"e_1_3_2_16_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.pt.2005.01.003"},{"key":"e_1_3_2_17_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.282.5396.2012"},{"key":"e_1_3_2_18_2","doi-asserted-by":"publisher","DOI":"10.1017\/S003118209900517X"},{"key":"e_1_3_2_19_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0169-4758(97)01144-7"},{"key":"e_1_3_2_20_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0968-0004(00)88975-6"},{"key":"e_1_3_2_21_2","doi-asserted-by":"publisher","DOI":"10.4269\/ajtmh.1997.57.25"},{"key":"e_1_3_2_22_2","first-page":"547","volume":"12","year":"2003","unstructured":"DeSilva, N., S. Brooker, P. Hotez, A. Montresor, D. Engels, and L. Savioli. 2003. Soil transmitted helminth infections: updating the global picture. Trends Parasitol.12:547-551.","journal-title":"Trends Parasitol."},{"key":"e_1_3_2_23_2","doi-asserted-by":"publisher","DOI":"10.1086\/524070"},{"key":"e_1_3_2_24_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.00573-09"},{"key":"e_1_3_2_25_2","doi-asserted-by":"publisher","DOI":"10.1086\/498528"},{"key":"e_1_3_2_26_2","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1522-2683(20000401)21:6<1037::AID-ELPS1037>3.0.CO;2-V"},{"key":"e_1_3_2_27_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2005.04.040"},{"key":"e_1_3_2_28_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0076-6879(81)77053-8"},{"key":"e_1_3_2_29_2","first-page":"821","volume":"383","year":"2002","unstructured":"Harwaldt, P., S. Rahlfs, and K. Becker. 2002. Glutathione S-transferase of the malarial parasite Plasmodium falciparum: characterization of a potential drug target. Biol. Chem.383:821-830.","journal-title":"Biol. Chem."},{"key":"e_1_3_2_30_2","doi-asserted-by":"publisher","DOI":"10.1016\/0166-6851(94)00203-Y"},{"key":"e_1_3_2_31_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMra032492"},{"key":"e_1_3_2_32_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2006.05.008"},{"key":"e_1_3_2_33_2","doi-asserted-by":"publisher","DOI":"10.1654\/1525-2647(2002)069[0072:NHOPCH]2.0.CO;2"},{"key":"e_1_3_2_34_2","doi-asserted-by":"publisher","DOI":"10.1016\/S1074-5521(02)00296-X"},{"key":"e_1_3_2_35_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0022-2836(02)01174-9"},{"key":"e_1_3_2_36_2","first-page":"1937","volume":"299","year":"2008","unstructured":"Keiser, J., and J. Utzinger. 2008. Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA299:1937-1948.","journal-title":"JAMA"},{"key":"e_1_3_2_37_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.8424176"},{"key":"e_1_3_2_38_2","doi-asserted-by":"publisher","DOI":"10.1517\/phgs.5.3.305.29827"},{"key":"e_1_3_2_39_2","doi-asserted-by":"publisher","DOI":"10.1016\/S1473-3099(06)70630-2"},{"key":"e_1_3_2_40_2","doi-asserted-by":"publisher","DOI":"10.1080\/10425170290019900"},{"key":"e_1_3_2_41_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(18)41931-X"},{"key":"e_1_3_2_42_2","doi-asserted-by":"publisher","DOI":"10.1128\/CMR.00046-07"},{"key":"e_1_3_2_43_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.73.6.3402-3407.2005"},{"key":"e_1_3_2_44_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2004.12.022"},{"key":"e_1_3_2_45_2","doi-asserted-by":"publisher","DOI":"10.1084\/jem.148.2.569"},{"key":"e_1_3_2_46_2","doi-asserted-by":"publisher","DOI":"10.1002\/pmic.200600068"},{"key":"e_1_3_2_47_2","doi-asserted-by":"publisher","DOI":"10.1093\/emboj\/18.22.6282"},{"key":"e_1_3_2_48_2","first-page":"1","volume":"37","year":"2006","unstructured":"Nguyen, P. H., K. C. Nguyen, B. Le Mai, T. V. Nguyen, K. H. Ha, C. Bern, R. Flores, and R. Martorell. 2006. Risk factors for anemia in Vietnam. Southeast Asian J. Trop. Med. Public Health37:1-11.","journal-title":"Southeast Asian J. Trop. Med. Public Health"},{"key":"e_1_3_2_49_2","first-page":"357","volume":"12","year":"1996","unstructured":"Page, R. D. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci.12:357-358.","journal-title":"Comput. Appl. Biosci."},{"key":"e_1_3_2_50_2","doi-asserted-by":"publisher","DOI":"10.1021\/pr800395x"},{"key":"e_1_3_2_51_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.96.23.13056"},{"key":"e_1_3_2_52_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0500877102"},{"key":"e_1_3_2_53_2","first-page":"1029","volume":"15","year":"1966","unstructured":"Roche, M., and M. Layrisse. 1966. Nature and causes of \u201chookworm anemia.\u201d Am. J. Trop. Med. Hyg.15:1029-1102.","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"e_1_3_2_54_2","doi-asserted-by":"publisher","DOI":"10.1016\/S1367-5931(99)80028-3"},{"key":"e_1_3_2_55_2","doi-asserted-by":"publisher","DOI":"10.1002\/prot.20649"},{"key":"e_1_3_2_56_2","first-page":"223","volume":"55","year":"1997","unstructured":"Stoltzfus, R. J., M. L. Dreyfuss, H. M. Chwaya, and M. Albonico. 1997. Hookworm control as a strategy to prevent iron deficiency. Nutr. Rev.55:223-232.","journal-title":"Nutr. Rev."},{"key":"e_1_3_2_57_2","doi-asserted-by":"publisher","DOI":"10.1093\/emboj\/cdf516"},{"key":"e_1_3_2_58_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.actatropica.2007.08.005"},{"key":"e_1_3_2_59_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.76.9.4350"},{"key":"e_1_3_2_60_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.72.5.2780-2790.2004"},{"key":"e_1_3_2_61_2","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.203.8.1253"},{"key":"e_1_3_2_62_2","unstructured":"Deworming for health and development. 2005"},{"key":"e_1_3_2_63_2","doi-asserted-by":"publisher","DOI":"10.1096\/fj.02-0181fje"},{"key":"e_1_3_2_64_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M405842200"},{"key":"e_1_3_2_65_2","first-page":"516","volume":"79","year":"2008","unstructured":"Wu, B., L. Conway, J. Novelli, J. Foster, and B. Slatko. 2008. Wolbachia heme biosynthesis as a potential anti-filariasis target set. Am. J. Trop. Med. Hyg.79:516.","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"e_1_3_2_66_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.exppara.2007.05.010"},{"key":"e_1_3_2_67_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.exppara.2003.12.016"},{"key":"e_1_3_2_68_2","doi-asserted-by":"publisher","DOI":"10.4269\/ajtmh.2002.66.238"},{"key":"e_1_3_2_69_2","first-page":"26","volume":"18","year":"2000","unstructured":"Zhan, B., J. Hawdon, Q. Shan, H. Ren, H. Qiang, S. H. Xiao, T. H. Li, Z. Feng, and P. Hotez. 2000. Construction and analysis of cDNA library of the third stage larvae of Necator americanus. Zhongguo ji sheng chong xue yu ji sheng chong bing za zhi18:26-28.","journal-title":"Zhongguo ji sheng chong xue yu ji sheng chong bing za zhi"},{"key":"e_1_3_2_70_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.73.10.6903-6911.2005"},{"key":"e_1_3_2_71_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijpara.2004.04.015"}],"container-title":["Infection and Immunity"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/IAI.00848-09","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/IAI.00848-09","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,30]],"date-time":"2023-05-30T04:47:21Z","timestamp":1685422041000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/IAI.00848-09"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2010,4]]},"references-count":70,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2010,4]]}},"alternative-id":["10.1128\/IAI.00848-09"],"URL":"https:\/\/doi.org\/10.1128\/iai.00848-09","relation":{},"ISSN":["0019-9567","1098-5522"],"issn-type":[{"value":"0019-9567","type":"print"},{"value":"1098-5522","type":"electronic"}],"subject":[],"published":{"date-parts":[[2010,4]]},"assertion":[{"value":"2009-07-28","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2010-01-06","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2010-04-01","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}