An oral versus intranasal prime/boost regimen using attenuated human rotavirus or VP2 and VP6 virus-like particles with immunostimulating complexes influences protection and antibody-secreting cell responses to rotavirus in a neonatal gnotobiotic pig model

Clinical and Vaccine Immunology

Volumn 17, Issue 3, 2010, Pages 420-428

  Azevedo, Marli S P ^a,b   Gonzalez, Ana Maria ^a,c   Yuan, Lijuan ^a,d   Jeong, Kwang Il ^a,e   Iosef, Cristiana ^a,f   Van Nguyen, Trang ^a,g   Lovgren Bengtsson, Karin ^a,h   Morein, Bror ^a,h   Saif, Linda J ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

^e TUFTS UNIVERSITY   (United States)

^f UNIVERSITY OF WESTERN ONTARIO   (Canada)

^g NATIONAL INSTITUTE OF HYGIENE AND EPIDEMIOLOGY   (Viet Nam)

^h SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; LIVE VACCINE; PROTEIN VP2; PROTEIN VP6; ROTAVIRUS VACCINE;

ANIMAL DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DIARRHEA; DOSE RESPONSE; DRUG DELIVERY SYSTEM; ENZYME LINKED IMMUNOSPOT ASSAY; GNOTOBIOTICS; IMMUNOSTIMULATION; NONHUMAN; PRIORITY JOURNAL; ROTAVIRUS; TISSUE DISTRIBUTION; VIRUS LIKE AGENT; VIRUS REPLICATION;

ADMINISTRATION, INTRANASAL; ADMINISTRATION, ORAL; ANIMALS; ANIMALS, NEWBORN; ANTIBODY-PRODUCING CELLS; ANTIGENS, VIRAL; CAPSID PROTEINS; GERM-FREE LIFE; HUMANS; IMMUNIZATION, SECONDARY; ROTAVIRUS; ROTAVIRUS VACCINES; SWINE; VACCINATION; VACCINES, ATTENUATED; VIRION;

EID: 77649252796     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00395-09     Document Type: Article

References (45)

1. Agnello, D., C. A. Herve, A. Lavaux, M. Darniot, P. Guillon, A. Charpilienne, and P. Pothier. 2006. Intrarectal immunization with rotavirus 2/6 virus-like particles induces an antirotavirus immune response localized in the intestinal mucosa and protects against rotavirus infection in mice. J. Virol. 80:3823-3832.
2. Azevedo, M. S., L. Yuan, K. I. Jeong, A. Gonzalez, T. V. Nguyen, S. Pouly, M. Gochnauer, W. Zhang, A. Azevedo, and L. J. Saif. 2005. Viremia and nasal and rectal shedding of rotavirus in gnotobiotic pigs inoculated with Wa human rotavirus. J. Virol. 79:5428-5436.
3. Bennett, E., A. B. Mullen, and V. A. Ferro. 2009. Translational modifications to improve vaccine efficacy in an oral influenza vaccine. Methods 49:322-327.
4. Bertolotti-Ciarlet, A., M. Ciarlet, S. E. Crawford, M. E. Conner, and M. K. Estes. 2003. Immunogenicity and protective efficacy of rotavirus 2/6-viruslike particles produced by a dual baculovirus expression vector and administered intramuscularly, intranasally, or orally to mice. Vaccine 21:3885-3900.
5. Blutt, S. E., K. L. Warfield, C. M. O'Neal, M. K. Estes, and M. E. Conner. 2006. Host, viral, and vaccine factors that determine protective efficacy induced by rotavirus and virus-like particles (VLPs). Vaccine 24:1170-1179.
6. Brandtzaeg, P., I. N. Farstad, and G. Haraldsen. 1999. Regional specialization in the mucosal immune system: primed cells do not always home along the same track. Immunol. Today 20:267-277.
7. Brandtzaeg, P., T. S. Halstensen, K. Kett, P. Krajci, D. Kvale, T. O. Rognum, H. Scott, and L. M. Sollid. 1989. Immunobiology and immunopathology of human gut mucosa: humoral immunity and intraepithelial lymphocytes. Gastroenterology 97:1562-1584.
8. Brown, K. A., J. A. Kriss, C. A. Moser, W. J. Wenner, and P. A. Offit. 2000. Circulating rotavirus-specific antibody-secreting cells (ASCs) predict the presence of rotavirus-specific ASCs in the human small intestinal lamina propria. J. Infect. Dis. 182:1039-1043.
9. Burns, J. W., A. A. Krishnaney, P. T. Vo, R. V. Rouse, L. J. Anderson, and H. B. Greenberg. 1995. Analyses of homologous rotavirus infection in the mouse model. Virology 207:143-153.
10. Ciarlet, M., M. E. Conner, M. J. Finegold, and M. K. Estes. 2002. Group A rotavirus infection and age-dependent diarrheal disease in rats: a new animal model to study the pathophysiology of rotavirus infection. J. Virol. 76:41-57.
11. Conner, M. E., C. D. Zarley, B. Hu, S. Parsons, D. Drabinski, S. Greiner, R. Smith, B. Jiang, B. Corsaro, V. Barniak, H. P. Madore, S. Crawford, and M. K. Estes. 1996. Virus-like particles as a rotavirus subunit vaccine. J. Infect. Dis. 174(Suppl. 1):S88-S92.
12. Coulson, B. S., K. Grimwood, I. L. Hudson, G. L. Barnes, and R. F. Bishop. 1992. Role of coproantibody in clinical protection of children during reinfection with rotavirus. J. Clin. Microbiol. 30:1678-1684.
13. Crawford, S. E., M. Labbe, J. Cohen, M. H. Burroughs, Y. J. Zhou, and M. K. Estes. 1994. Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells. J. Virol. 68:5945-5952.
14. Feng, N., P. T. Vo, D. Chung, T. V. Vo, Y. Hoshino, and H. B. Greenberg. 1997. Heterotypic protection following oral immunization with live heterologous rotaviruses in a mouse model. J. Infect. Dis. 175:330-341.
15. Fernandez, F. M., M. E. Conner, A. V. Parwani, D. Todhunter, K. L. Smith, S. E. Crawford, M. K. Estes, and L. J. Saif. 1996. Isotype-specific antibody responses to rotavirus and virus proteins in cows inoculated with subunit vaccines composed of recombinant SA11 rotavirus core-like particles (CLP) or virus-like particles (VLP). Vaccine 14:1303-1312.
16. Gonzalez, A. M., T. V. Nguyen, M. S. Azevedo, K. Jeong, F. Agarib, C. Iosef, K. Chang, K. Lovgren-Bengtsson, B. Morein, and L. J. Saif. 2004. Antibody responses to human rotavirus (HRV) in gnotobiotic pigs following a new prime/boost vaccine strategy using oral attenuated HRV priming and intranasal VP2/6 rotavirus-like particle (VLP) boosting with ISCOM. Clin. Exp. Immunol. 135:361-372.
17. Greenberg, H. B., and M. K. Estes. 2009. Rotaviruses: from pathogenesis to vaccination. Gastroenterology 136:1939-1951.
18. Iosef, C., T. Van Nguyen, K. Jeong, K. Bengtsson, B. Morein, Y. Kim, K. O. Chang, M. S. Azevedo, L. Yuan, P. Nielsen, and L. J. Saif. 2002. Systemic and intestinal antibody secreting cell responses and protection in gnotobiotic pigs immunized orally with attenuated Wa human rotavirus and Wa 2/6-rotavirus-like-particles associated with immunostimulating complexes. Vaccine 20: 1741-1753.
19. Johansson, E., C. Istrate, A. Charpilienne, J. Cohen, J. Hinkula, D. Poncet, L. Svensson, and K. Johansen. 2008. Amount of maternal rotavirus-specific antibodies influence the outcome of rotavirus vaccination of newborn mice with virus-like particles. Vaccine 26:778-785.
20. Joura, E. A., S. Leodolter, M. Hernandez-Avila, C. M. Wheeler, G. Perez, L. A. Koutsky, S. M. Garland, D. M. Harper, G. W. K. Tang, D. G. Ferris, M. Steben, R. W. Jones, J. Bryan, F. J. Taddeo, O. M. Bautista, M. T. Esser, H. L. Sings, M. Nelson, J. W. Boslego, C. Sattler, E. Barr, and J. Paavonen. 2007. Efficacy of a quadrivalent prophylactic human papillomavirus (types 6, 11, 16, and 18) L1 virus-like-particle vaccine against high-grade vulval and vaginal lesions: a combined analysis of three randomised clinical trials. Lancet 369:1693-1702.
21. Labbe, M., A. Charpilienne, S. E. Crawford, M. K. Estes, and J. Cohen. 1991. Expression of rotavirus VP2 produces empty corelike particles. J. Virol. 65:2946-2952.
22. McGhee, J. R., M. E. Lamm, and W. Strober. 1999. Mucosal immune responses: an overview, p. 485-506. In P. L. Ogra (ed.), Mucosal immunology, 2nd ed. Academic Press, San Diego, CA.
23. Meyer, R. C., E. H. Bohl, and E. M. Kohler. 1964. Procurement and maintenance of germ-free swine for microbiological investigations. Appl. Microbiol. 12:295-300.
24. Moser, C. A., and P. A. Offit. 2001. Distribution of rotavirus-specific memory B cells in gut-associated lymphoid tissue after primary immunization. J. Gen. Virol. 82:2271-2274.
25. Nguyen, T. V., L. Yuan, M. S. Azevedo, K. I. Jeong, A. M. Gonzalez, C. Iosef, K. Lovgren-Bengtsson, B. Morein, P. Lewis, and L. J. Saif. 2006. High titers of circulating maternal antibodies suppress effector and memory B-cell responses induced by an attenuated rotavirus priming and rotavirus-like particle-immunostimulating complex boosting vaccine regimen. Clin. Vaccine Immunol. 13:475-485.
26. Nigro, G., and M. Midulla. 1983. Acute laryngitis associated with rotavirus gastroenteritis. J. Infect. 7:81-82.
27. O'Neal, C. M., J. D. Clements, M. K. Estes, and M. E. Conner. 1998. Rotavirus 2/6 viruslike particles administered intranasally with cholera toxin, Escherichia coli heat-labile toxin (LT), and LT-R192G induce protection from rotavirus challenge. J. Virol. 72:3390-3393.
28. O'Neal, C. M., S. E. Crawford, M. K. Estes, and M. E. Conner. 1997. Rotavirus virus-like particles administered mucosally induce protective immunity. J. Virol. 71:8707-8717.
29. Parashar, U. D., C. J. Gibson, J. S. Bresse, and R. I. Glass. 2006. Rotavirus and severe childhood diarrhea. Emerg. Infect. Dis. 12:304-306.
30. Parez, N., C. Fourgeux, A. Mohamed, C. Dubuquoy, M. Pillot, A. Dehee, A. Charpilienne, D. Poncet, I. Schwartz-Cornil, and A. Garbarg-Chenon. 2006. Rectal immunization with rotavirus virus-like particles induces systemic and mucosal humoral immune responses and protects mice against rotavirus infection. J. Virol. 80:1752-1761.
31. Prince, D. S., C. Astry, S. Vonderfecht, G. Jakab, F. M. Shen, and R. H. Yolken. 1986. Aerosol transmission of experimental rotavirus infection. Pediatr. Infect. Dis. 5:218-222.
32. Saif, L., L. Yuan, L. Ward, and T. To. 1997. Comparative studies of the pathogenesis, antibody immune responses, and homologous protection to porcine and human rotaviruses in gnotobiotic piglets. Adv. Exp. Med. Biol. 412:397-403.
33. Saif, L. J., and F. M. Fernandez. 1996. Group A rotavirus veterinary vaccines. J. Infect. Dis. 174(Suppl. 1):S98-S106.
34. Simerska, P., P. M. Moyle, C. Olive, and I. Toth. 2009. Oral vaccine delivery-new strategies and technologies. Curr. Drug Deliv. 6:347-358.
35. VanCott, J. L., T. A. Brim, R. A. Simkins, and L. J. Saif. 1993. Isotypespecific antibody-secreting cells to transmissible gastroenteritis virus and porcine respiratory coronavirus in gut- and bronchus-associated lymphoid tissues of suckling pigs. J. Immunol. 150:3990-4000.
36. Ward, L. A., B. I. Rosen, L. Yuan, and L. J. Saif. 1996. Pathogenesis of an attenuated and a virulent strain of group A human rotavirus in neonatal gnotobiotic pigs. J. Gen. Virol. 77:1431-1441.
37. World Health Organization. 2009. Meeting of the Immunization Strategic Advisory Group of Experts, April 2009-conclusions and recommendations. Wkly. Epidemiol. Rec. 84:220-236.
38. Youngman, K. R., M. A. Franco, N. A. Kuklin, L. S. Rott, E. C. Butcher, and H. B. Greenberg. 2002. Correlation of tissue distribution, developmental phenotype, and intestinal homing receptor expression of antigen-specific B cells during the murine anti-rotavirus immune response. J. Immunol. 168: 2173-2181.
39. Yuan, L., A. Geyer, D. C. Hodgins, Z. Fan, Y. Qian, K. O. Chang, S. E. Crawford, V. Parreno, L. A. Ward, M. K. Estes, M. E. Conner, and L. J. Saif. 2000. Intranasal administration of 2/6-rotavirus-like particles with mutant Escherichia coli heat-labile toxin (LT-R192G) induces antibody-secreting cell responses but not protective immunity in gnotobiotic pigs. J. Virol. 74:8843-8853.
40. Yuan, L., A. Geyer, and L. J. Saif. 2001. Short-term immunoglobulin A B-cell memory resides in intestinal lymphoid tissues but not in bone marrow of gnotobiotic pigs inoculated with Wa human rotavirus. Immunology 103:188-198.
41. Yuan, L., C. Iosef, M. S. Azevedo, Y. Kim, Y. Qian, A. Geyer, T. V. Nguyen, K. O. Chang, and L. J. Saif. 2001. Protective immunity and antibody-secreting cell responses elicited by combined oral attenuated Wa human rotavirus and intranasal Wa 2/6-VLPs with mutant Escherichia coli heat-labile toxin in gnotobiotic pigs. J. Virol. 75:9229-9238.
42. Yuan, L., S. Y. Kang, L. A. Ward, T. L. To, and L. J. Saif. 1998. Antibodysecreting cell responses and protective immunity assessed in gnotobiotic pigs inoculated orally or intramuscularly with inactivated human rotavirus. J. Virol. 72:330-338.
43. Yuan, L., and L. J. Saif. 2002. Induction of mucosal immune responses and protection against enteric viruses: rotavirus infection of gnotobiotic pigs as a model. Vet. Immunol. Immunopathol. 87:147-160.
44. Yuan, L., L. A. Ward, B. I. Rosen, T. L. To, and L. J. Saif. 1996. Systematic and intestinal antibody-secreting cell responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease. J. Virol. 70:3075-3083.
45. Yuan, L., K. Wen, M. S. Azevedo, A. M. Gonzalez, W. Zhang, and L. J. Saif. 2008. Virus-specific intestinal IFN-gamma producing T cell responses induced by human rotavirus infection and vaccines are correlated with protection against rotavirus diarrhea in gnotobiotic pigs. Vaccine 26:3322-3331.