A history of hookworm vaccine development

Human Vaccines

Volumn 7, Issue 11, 2011, Pages 1234-1244

  Schneider, Brent ^a   Jariwala, Amar R ^a   Periago, Maria Victoria ^b   Gazzinelli, Maria Flávia ^c   Bose, Swaroop N ^a   Hotez, Peter J ^d   Diemert, David J ^a   Bethony, Jeffrey M ^a  

^a GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

^b Instituto René   (Brazil)

^c FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Canine hookworm vaccine; Hookworm diseases; Necator americanus; Neglected tropical disease; Recombinant protein vaccine

Indexed keywords

ANCYLOSTOMA CEYLANICUM ANTIGEN; ANCYLOSTOMA CEYLANICUM ASPARTIC PROTEASE 1; ANCYLOSTOMA CEYLANICUM GLUTATHIONE S TRANSFERASE 1; ATTENUATED ANCYLOSTOMA CANINUM VACCINE; HOOKWORM VACCINE; NECATOR AMERICANUS ASPARTIC PROTEASE 1; NECATOR AMERICANUS GLUTATHIONE S TRANSFERASE 1; RECOMBINANT NECATOR AMERICANUS ANCYLOSTOMA SECRETED PROTEIN 2; UNCLASSIFIED DRUG; VACCINE;

DISEASE MODEL; DRUG RESEARCH; DRUG SAFETY; DRUG SCREENING; DRUG WITHDRAWAL; EXPERIMENTAL ANIMAL; EXPERIMENTAL INFECTION; HISTORY; HOOKWORM; HOOKWORM INFECTION; HUMAN; IMMEDIATE TYPE HYPERSENSITIVITY; IMMUNE RESPONSE; INFECTION CONTROL; INJECTION SITE URTICARIA; NECATOR AMERICANUS; NECATORIASIS; NEMATODE LIFE CYCLE STAGE; NONHUMAN; REVIEW; SINGLE DRUG DOSE;

EID: 81855174780     PISSN: 15548600     EISSN: 15548619     Source Type: Journal    
DOI: 10.4161/hv.7.11.18443     Document Type: Review

References (88)

1. Brooker S, Bethony J, Hotez PJ. Human hookworm infection in the 21st century. Adv Parasitol 2004; 58:197-288; PMID:15603764; DOI:10.1016/S0065- 308X(04)58004-1.
2. Thompson RC, Reynoldson JA, Garrow SC, McCarthy JS, Behnke JM. Towards the eradication of hookworm in an isolated Australian community. Lancet 2001; 357:770-1; PMID:11253974; DOI:10.1016/S0140-6736(00)04162-3.
3. Bethony JM, Cole RN, Guo X, Kamhawi S, Lightowlers MW, Loukas A, et al. Vaccines to combat the neglected tropical diseases. Immunol Rev 2011; 239:237-70; PMID:21198676; DOI:10.1111/j.1600-065X.2010.00976.x.
4. Hotez PJ, Bethony JM, Diemert DJ, Pearson M, Loukas A. Developing vaccines to combat hookworm infection and intestinal schistosomiasis. Nat Rev Microbiol 2010; 8:814-26; PMID:20948553; DOI:10.1038/nrmicro2438.
5. Hotez PJ, Bethony JM, Oliveira SC, Brindley PJ, Loukas A. Multivalent anthelminthic vaccine to prevent hookworm and schistosomiasis. Expert Rev Vaccines 2008; 7:745-52; PMID:18665774; DOI:10.1586/14760584.7.6.745.
6. Keiser J, Utzinger J. Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA 2008; 299:1937-48; PMID:18430913; DOI:10.1001/jama.299.16.1937.
7. Gonçalves ML, Araujo A, Ferreira LF. Human intestinal parasites in the past: new findings and a review. Mem Inst Oswaldo Cruz 2003; 98:103-18; PMID:12687769; DOI:10.1590/S0074-02762003000900016.
8. Dock G, Bass C. Hookworm Disease. St. Louis: Mosby Co. 1910.
9. Stiles CW. A new species of hookworm (Uncinaria americana) parasite in man. American Medicine 1902; 3:777-8.
10. Stiles CW. Frequency ofhookworm disease or ground itch anemia among public school children in Southern Florida. Public Health Rep 1910; 25:351-4; PMID:19314191; DOI:10.2307/4564592.
11. Farley J. To Cast Out Disease: A History of the International Health Division of Rockefeller Foundation [1913-1951], Oxford University Press 2004.
12. Stiles CW, Leonard G. Hookworm Diseases: number of treatments and number of doses of thymol adminisered in 61 hospital and 22 home-cured cases of hookworm infection. Public Health Rep 1913; 28:119-24; DOI:10.2307/4569192.
13. Stiles CW, Miller H. Observatioins on the viability of the eggs of hookworms (Necator americanus) and of eelworms (Ascaris lumbricoides) in feces allowed to decompose in water. Public Health Rep 1911; 26:1565-600; PMID:19314272; DOI:10.2307/4566877.
14. Stoll NR. This wormy world. J Parasitol 1947; 33:1-18; PMID:20284977.
15. de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol 2003; 19:547-51; PMID:14642761; DOI:10.1016/j.pt.2003.10.002.
16. Nawalinski T, Schad G. Historical Introduction. In: Gilles H, Ball P, Eds. Human parasitic dieases: Hookwrom Infection 1991; 4:1-4.
17. Bundy D. Is hookworm just another geohelminth? In: Schad GA, Warren K, Eds. Hookworm Diseases-current status and new directions. London: Taylor and Francis 1990; 146-64.
18. Stiles CW. Is It "Fair to Say That Hookworm Disease Has Almost Disappeared from the United States?". Science 1933; 77:237-9; PMID:17773059; DOI:10.1126/science.77.1992.237.
19. Ministry of Health PRC, National Institute of Parasitic Diseases. Report on the national survey of the current situation of major human parasitic diseases in China. Beijing: Ministry of Health 2005.
20. Ehrenberg JP, Ault SK. Neglected diseases of neglected populations: thinking to reshape the determinants of health in Latin America and the Caribbean. BMC Public Health 2005; 5:119; PMID:16283932; DOI:10.1186/1471-2458- 5-119.
21. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis and hookworm. Lancet 2006; 367:1521-32; PMID:16679166; DOI:10.1016/ S0140-6736(06)68653-4.
22. Crompton DW. The public health importance of hookworm disease. Parasitology 2000; 121:39-50; PMID:11386690; DOI:10.1017/ S0031182000006454.
23. Loukas A, Constant SL, Bethony JM. Immunobiology of hookworm infection. FEMS Immunol Med Microbiol 2005; 43:115-24; PMID:15681140; DOI:10.1016/j.femsim. 2004.11.006.
24. Plotkin SA. Immunologic correlates of protection induced by vaccination. Pediatr Infect Dis J 2001; 20:63-75; PMID:11176570; DOI:10.1097/00006454- 200101000-00013.
25. Plotkin SA. Correlates of protection induced by vaccination. Clin Vaccine Immunol 2010; 17:1055-65; PMID:20463105; DOI:10.1128/CVI.00131-10.
26. Geiger SM, Caldas IR, Mc Glone BE, Campi-Azevedo AC, De Oliveira LM, Brooker S, et al. Stage-specific immune responses in human Necator americanus infection. Parasite Immunol 2007; 29:347-58; PMID:17576364; DOI:10.1111/j.1365- 3024.2007.00950.x.
27. Geiger SM, Fujiwara RT, Santiago H, Correa-Oliveira R, Bethony JM. Early stage-specific immune responses in primary experimental human hookworm infection. Microbes Infect 2008; 10:1524-35; PMID:18848637; DOI:10.1016/j. micinf.2008.09.003.
28. Maizels RM, Holland MJ, Falcone FH, Zang XX, Yazdanbakhsh M. Vaccination against helminth parasites-the ultimate challenge for vaccinologists? Immunol Rev 1999; 171:125-47; PMID:10582168; DOI:10.1111/j.1600-065X.1999.tb01345.x.
29. Maizels RM, Pearce EJ, Artis D, Yazdanbakhsh M, Wynn TA. Regulation of pathogenesis and immunity in helminth infections. J Exp Med 2009; 206:2059-66; PMID:19770272; DOI:10.1084/jem.20091903.
30. Maizels RM, Yazdanbakhsh M. T-cell regulation in helminth parasite infections: implications for inflammatory diseases. Chem Immunol Allergy 2008; 94:112-23; PMID:18802342; DOI:10.1159/000154944.
31. Maizels RM, Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 2003; 3:733-44; PMID:12949497; DOI:10.1038/nri1183.
32. Yazdanbakhsh M, van den Biggelaar A, Maizels RM. Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol 2001; 22:372-7; PMID:11429321; DOI:10.1016/S1471- 4906(01)01958-5.
33. Hagan P. IgE and protective immunity to helminth infections. Parasite Immunol 1993; 15:1-4; PMID:8433850; DOI:10.1111/j.1365-3024.1993.tb00565.x.
34. Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 1991; 349:243-5; PMID:1898985; DOI:10.1038/349243a0.
35. Bethony J, Loukas A, Smout M, Brooker S, Mendez S, Plieskatt J, et al. Antibodies against a secreted protein from hookworm larvae reduce the intensity of hookworm infection in humans and vaccinated laboratory animals. FASEB J 2005; 19:1743-5; PMID:16037096.
36. Erb KJ. Helminths, allergic disorders and IgE-mediated immune responses: where do we stand? Eur J Immunol 2007; 37:1170-3; PMID:17447233; DOI:10.1002/eji.200737314.
37. Leonardi-Bee J, Pritchard D, Britton J. Asthma and current intestinal parasite infection: systematic review and meta-analysis. Am J Respir Crit Care Med 2006; 174:514-23; PMID:16778161; DOI:10.1164/ rccm.200603-331OC.
38. Qin L, Gilbert PB, Corey L, McElrath MJ, Self SG. A framework for assessing immunological correlates of protection in vaccine trials. J Infect Dis 2007; 196:1304-12; PMID:17922394; DOI:10.1086/522428.
39. Loukas A, Bethony J, Brooker S, Hotez P. Hookworm vaccines: past, present and future. Lancet Infect Dis 2006; 6:733-41; PMID:17067922; DOI:10.1016/ S1473-3099(06)70630-2.
40. Fujiwara RT, Geiger SM, Bethony J, Mendez S. Comparative immunology of human and animal models of hookworm infection. Parasite Immunol 2006; 28:285-93; PMID:16842265; DOI:10.1111/j.1365- 3024.2006.00821.x.
41. Miller TA. Vaccination against the canine hookworm diseases. Adv Parasitol 1971; 9:153-83; PMID:4932829; DOI:10.1016/S0065-308X(08)60161-X.
42. Miller TA. Industrial development and field use of the canine hookworm vaccine. Adv Parasitol 1978; 16:333-42; PMID:364958; DOI:10.1016/S0065-308X(08) 60577-1.
43. Xiao S, Zhan B, Xue J, Goud GN, Loukas A, Liu Y, et al. The evaluation of recombinant hookworm antigens as vaccines in hamsters (Mesocricetus auratus) challenged with human hookworm, Necator americanus. Exp Parasitol 2008; 118:32-40; PMID:17645877; DOI:10.1016/j.exppara.2007.05.010.
44. Miller TA. Effect of X-irradiation upon the infective larvae of Ancylostoma caninum and the immunogenic effect in dogs of a single infection with 40 Kr-Irradiated larvae. J Parasitol 1964; 50:735-42; PMID:14244804; DOI:10.2307/3276194.
45. Miller TA. Effect of age of the dog on immunogenic efficiency of double vaccination with x-irradiated Ancylostoma caninum larvae. Am J Vet Res 1965; 26:1383-90; PMID:5882555.
46. Miller TA. Effect of route of administration of vaccine and challenge on the immunogenic efficiency of double vaccination with irradiated Ancylostoma Caninum Larvae. J Parasitol 1965; 51:200-6; PMID:14275207; DOI:10.2307/3276081.
47. Wilson RA, Coulson PS, Mountford AP. Immune responses to the radiation-attenuated schistosome vaccine: what can we learn from knock-out mice? Immunol Lett 1999; 65:117-23; PMID:10065637; DOI:10.1016/S0165-2478(98)00134-5.
48. Jennings FW, Mulligan W, Urquhart GM. Variables in X-ray "inactivation" of Nippostrongylus Brasiliensis larvae. Exp Parasitol 1963; 13:367-73; DOI:10.1016/0014-4894(63)90087-0.
49. Miller TA. Transfer of immunity to Ancylostoma caninum infection in pups by serum and lymphoid cells. Immunology 1967; 12:231-41; PMID:6020124.
50. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE. Helminth parasites-masters of regulation. Immunol Rev 2004; 201:89-116; PMID:15361235; DOI:10.1111/j.0105-2896.2004.00191.x.
51. Bethony JM, Loukas A, Hotez PJ, Knox DP. Vaccines against blood-feeding nematodes of humans and livestock. Parasitology 2006; 133:63-79; PMID:17274849; DOI:10.1017/S0031182006001818.
52. Diemert DJ, Bethony JM, Hotez PJ. Hookworm vaccines. Clin Infect Dis 2008; 46:282-8; PMID:18171264; DOI:10.1086/524070.
53. Carroll SM, Grove DI, Heenan PJ. Kinetics of cells in the intestinal mucosa of mice following oral infection with Ancylostoma ceylanicum. Int Arch Allergy Appl Immunol 1986; 79:26-32; PMID:3941009; DOI:10.1159/000233937.
54. Carroll SM, Howse DJ, Grove DI. The anticoagulant effects of the hookworm, Ancylostoma ceylanicum: observations on human and dog blood in vitro and infected dogs in vivo. Thromb Haemost 1984; 51:222-7; PMID:6740554.
55. Carroll SM, Karthigasu KT, Grove DI. Serodiagnosis of human strongyloidiasis by an enzyme-linked immunosorbent assay. Trans R Soc Trop Med Hyg 1981; 75:706-9; PMID:7036430; DOI:10.1016/0035-9203(81)90156-5.
56. Carroll SM, Mayrhofer G, Dawkins HJ, Grove DI. Kinetics of intestinal lamina propria mast cells, globule leucocytes, intraepithelial lymphocytes, goblet cells and eosinophils in murine strongyloidiasis. Int Arch Allergy Appl Immunol 1984; 74:311-7; PMID:6735488; DOI:10.1159/000233566.
57. Carroll SM, Pryor J, Kennett DW, Grove DI. Investigation of the haemolytic effects of Ancylostoma ceylanicum: observations on infected dogs in vivo and human and dog blood in vitro. Southeast Asian J Trop Med Public Health 1984; 15:129-34; PMID:6740375.
58. Carroll SM, Robertson TA, Papadimitriou JM, Grove DI. Transmission electron microscopical studies of the site of attachment of Ancylostoma ceylanicum to the small bowel mucosa of the dog. J Helminthol 1984; 58:313-20; PMID:6520374; DOI:10.1017/ S0022149X00025189.
59. Hotez PJ, Le Trang N, Cerami A. Hookworm antigens: the potential for vaccination. Parasitol Today 1987; 3:247-9; PMID:15462967; DOI:10.1016/0169- 4758(87)90148-7.
60. Hotez PJ, Trang NL, McKerrow JH, Cerami A. Isolation and characterization of a proteolytic enzyme from the adult hookworm Ancylostoma caninum. J Biol Chem 1985; 260:7343-8; PMID:3888998.
61. Asojo OA, Homma K, Sedlacek M, Ngamelue M, Goud GN, Zhan B, et al. X-ray structures of Na-GST-1 and Na-GST-2 two glutathione S-transferase from the human hookworm Necator americanus. BMC Struct Biol 2007; 7:42; PMID:17594497; DOI:10.1186/1472-6807-7-42.
62. Hawdon JM, Jones BF, Hoffman DR, Hotez PJ. Cloning and characterization of Ancylostoma-secreted protein. A novel protein associated with the transition to parasitism by infective hookworm larvae. J Biol Chem 1996; 271:6672-8; PMID:8636085.
63. Hawdon JM, Narasimhan S, Hotez PJ. Ancylostoma secreted protein 2: cloning and characterization of a second member of a family of nematode secreted proteins from Ancylostoma caninum. Mol Biochem Parasitol 1999; 99:149-65; PMID:10340481; DOI:10.1016/ S0166-6851(99)00011-0.
64. Parkinson J, Mitreva M, Whitton C, Thomson M, Daub J, Martin J, et al. A transcriptomic analysis of the phylum Nematoda. Nat Genet 2004; 36:1259-67; PMID:15543149; DOI:10.1038/ng1472.
65. Bethony JM, Simon G, Diemert DJ, Parenti D, Desrosiers A, Schuck S, et al. Randomized, placebocontrolled, double-blind trial of the Na-ASP-2 hookworm vaccine in unexposed adults. Vaccine 2008; 26:2408-17; PMID:18396361; DOI:10.1016/j.vaccine.2008.02.049.
66. Diemert DJ, Pinto AG, Freire J, Jariwala A, Hamilton R, Periago MV, et al. Generalized Urticaria Induced by the Na-ASP-2 hookworm vaccine-implications for the development of vaccines against helminths. J Allergy Clin Immunol 2011; submitted.
67. Bohlke K, Davis RL, Marcy SM, Braun MM, DeStefano F, Black SB, et al. Risk of anaphylaxis after vaccination of children and adolescents. Pediatrics 2003; 112:815-20; PMID:14523172; DOI:10.1542/ peds.112.4.815.
68. Madaan A, Maddox DE. Vaccine allergy: diagnosis and management. Immunol Allergy Clin North Am 2003; 23:555-88; PMID:14753381; DOI:10.1016/S0889-8561(03) 00099-7.
69. Edelman R, Wasserman SS, Kublin JG, Bodison SA, Nardin EH, Oliveira GA, et al. Immediatetype hypersensitivity and other clinical reactions in volunteers immunized with a synthetic multiantigen peptide vaccine (PfCS-MAP1NYU) against Plasmodium falciparum sporozoites. Vaccine 2002; 21:269-80; PMID:12450702; DOI:10.1016/S0264-410X(02)00468-1.
70. Chapman MD, Pomes A, Breiteneder H, Ferreira F. Nomenclature and structural biology of allergens. J Allergy Clin Immunol 2007; 119:414-20; PMID:17166572; DOI:10.1016/j.jaci.2006.11.001.
71. Traidl-Hoffmann C, Jakob T, Behrendt H. Determinants of allergenicity. J Allergy Clin Immunol 2009; 123:558-66; PMID:19152966; DOI:10.1016/j.jaci.2008. 12.003.
72. Fitzsimmons CM, Dunne DW. Survival of the fittest: allergology or parasitology? Trends Parasitol 2009; 25:447-51; PMID:19744885; DOI:10.1016/j. pt.2009.07.004.
73. Goud GN, Bottazzi ME, Zhan B, Mendez S, Deumic V, Plieskatt J, et al. Expression of the Necator americanus hookworm larval antigen Na-ASP-2 in Pichia pastoris and purification of the recombinant protein for use in human clinical trials. Vaccine 2005; 23:4754-64; PMID:16054275; DOI:10.1016/j.vaccine. 2005.04.040.
74. Williamson AL, Lecchi P, Turk BE, Choe Y, Hotez PJ, McKerrow JH, et al. A multi-enzyme cascade of hemoglobin proteolysis in the intestine of bloodfeeding hookworms. J Biol Chem 2004; 279:35950-7; PMID:15199048; DOI:10.1074/jbc. M405842200.
75. Ranjit N, Zhan B, Hamilton B, Stenzel D, Lowther J, Pearson M, et al. Proteolytic degradation of hemoglobin in the intestine of the human hookworm Necator americanus. J Infect Dis 2009; 199:904-12; PMID:19434933; DOI:10.1086/597048.
76. Loukas A, Bethony JM, Mendez S, Fujiwara RT, Goud GN, Ranjit N, et al. Vaccination with recombinant aspartic hemoglobinase reduces parasite load and blood loss after hookworm infection in dogs. PLoS Med 2005; 2:295; PMID:16231975; DOI:10.1371/journal. pmed.0020295.
77. Pearson MS, Bethony JM, Pickering DA, de Oliveira LM, Jariwala A, Santiago H, et al. An enzymatically inactivated hemoglobinase from Necator americanus induces neutralizing antibodies against multiple hookworm species and protects dogs against heterologous hookworm infection. FASEB J 2009; 23:3007-19; PMID:19380510; DOI:10.1096/fj.09-131433.
78. Perally S, Lacourse EJ, Campbell AM, Brophy PM. Heme transport and detoxification in nematodes: subproteomics evidence of differential role of glutathione transferases. J Proteome Res 2008; 7:4557-65; PMID:18720983; DOI:10.1021/pr800395x.
79. Zhan B, Liu S, Perally S, Xue J, Fujiwara R, Brophy P, et al. Biochemical characterization and vaccine potential of a heme-binding glutathione transferase from the adult hookworm Ancylostoma caninum. Infect Immun 2005; 73:6903-11; PMID:16177370; DOI:10.1128/ IAI.73.10.6903-11.2005.
80. Zhan B, Perally S, Brophy PM, Xue J, Goud G, Liu S, et al. Molecular cloning, biochemical characterization and partial protective immunity of the heme-binding glutathione S-transferases from the human hookworm Necator americanus. Infect Immun 2010; 78:1552-63; PMID:20145100; DOI:10.1128/IAI.00848- 09.
81. Pearson MS, Pickering DA, Tribolet L, Cooper L, Mulvenna J, Oliveira LM, et al. Neutralizing antibodies to the hookworm hemoglobinase Na-APR-1: implications for a multivalent vaccine against hookworm infection and schistosomiasis. J Infect Dis 2010; 201:1561-9; PMID:20367477; DOI:10.1086/651953.
82. Coler RN, Bertholet S, Moutaftsi M, Guderian JA, Windish HP, Baldwin SL, et al. Development and characterization of synthetic glucopyranosyl lipid adjuvant system as a vaccine adjuvant. PLoS ONE 2011; 6:16333; PMID:21298114; DOI:10.1371/journal. pone.0016333.
83. Coler RN, Baldwin SL, Shaverdian N, Bertholet S, Reed SJ, Raman VS, et al. A synthetic adjuvant to enhance and expand immune responses to influenza vaccines. PLoS ONE 2010; 5:13677; PMID:21060869; DOI:10.1371/journal.pone. 0013677.
84. Coler RN, Carter D, Friede M, Reed SG. Adjuvants for malaria vaccines. Parasite Immunol 2009; 31:520-8; PMID:19691556; DOI:10.1111/j.1365-3024.2009. 01142.x.
85. Reed SG, Bertholet S, Coler RN, Friede M. New horizons in adjuvants for vaccine development. Trends Immunol 2009; 30:23-32; PMID:19059004; DOI:10.1016/j.it.2008.09.006.
86. Bethony J, Chen J, Lin S, Xiao S, Zhan B, Li S, et al. Emerging patterns of hookworm infection: influence of aging on the intensity of Necator infection in Hainan Province, People's Republic of China. Clin Infect Dis 2002; 35:1336-44; PMID:12439796; DOI:10.1086/344268.
87. Gandhi NS, Jizhang C, Khoshnood K, Fuying X, Shanwen L, Yaoruo L, et al. Epidemiology of Necator americanus hookworm infections in Xiulongkan Village, Hainan Province, China: high prevalence and intensity among middle-aged and elderly residents. J Parasitol 2001; 87:739-43; PMID:11534635.
88. Quinnell RJ, Pullan RL, Breitling LP, Geiger SM, Cundill B, Correa-Oliveira R, et al. Genetic and household determinants of predisposition to human hookworm infection in a Brazilian community. J Infect Dis 2010; 202:954-61; PMID:20681887; DOI:10.1086/655813.