Systemic immune response after rotavirus inoculation of neonatal mice depends on source and level of purification of the virus: Implications for the use of heterologous vaccine candidates

Journal of General Virology

Volumn 88, Issue 2, 2007, Pages 604-612

  Reimerink, Johan H J ^a   Boshuizen, Jos A ^b   Einerhand, Alexandra W C ^b   Duizer, Erwin ^a   van Amerongen, Geert ^a   Schmidt, Nico ^a   Koopmans, Marion P G ^a  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b Subdivision Molecular Endocrinology   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CESIUM CHLORIDE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; LIVE VACCINE; ROTAVIRUS VACCINE; SIMIAN ROTAVIRUS VACCINE; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; DIARRHEA; FEMALE; HISTOPATHOLOGY; IMMUNE RESPONSE; INTESTINE INFECTION; MOUSE; NEWBORN; NEWBORN INFECTION; NONHUMAN; PRIORITY JOURNAL; ROTAVIRUS; SMALL INTESTINE MUCOSA; TH2 CELL; VIRUS INFECTION; VIRUS PARTICLE; VIRUS PURIFICATION; VIRUS REPLICATION; VIRUS SHEDDING; VIRUS STRAIN;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; CENTRIFUGATION, ISOPYCNIC; CESIUM; CHLORIDES; FEMALE; INTESTINE, SMALL; MICE; MICE, INBRED BALB C; PREGNANCY; ROTAVIRUS; ROTAVIRUS INFECTIONS; ROTAVIRUS VACCINES; TH1 CELLS; TH2 CELLS; VIRAL PROTEINS;

MURINE ROTAVIRUS EDIM; MUS; ROTAVIRUS; SIMIAN ROTAVIRUS;

EID: 33846783005     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.82126-0     Document Type: Article

References (44)

1. Ball, J. M., Tian, P., Zang, C. Q., Morris, A. P. & Estes, M. K. (1996). Age-dependent diarrhea induced by a rotaviral nonstructural glycoprotein. Science 272, 101-104.
2. Bell, L. M., Clark, H. F., O'Brien, E. A., Kornstein, M. J., Plotkin, S. A. & Offit, P. A. (1987). Gastroenteritis caused by human rotaviruses (serotype three) in a suckling mouse model. Proc Soc Exp Biol Med 184, 127-132.
3. Blutt, S. E., Kirkwood, C. D., Parreno, V., Warfield, K. L., Ciarlet, M., Estes, M. K., Bok, K., Bishop, R. F. & Conner, M. E. (2003). Rotavirus antigenaemia and viraemia: a common event? Lancet 362, 1445-1449.
4. Boshuizen, J. A., Reimerink, J. H., Korteland-van Male, A. M., van Ham, V. J., Koopmans, M. P., Buller, H. A., Dekker, J. & Einerhand, A. W. (2003). Changes in small intestinal homeostasis, morphology, and gene expression during rotavirus infection of infant mice. J Virol 77, 13005-13016.
5. Boshuizen, J. A., Rossen, J. W. A., Sitaram, C. K, Kimenai, F. F. P., Simons-Oosterhuis, Y., Laffeber, C., Büller, H. A. & Einerhand, A. W. C. (2004). Rotavirus enterotoxin NSP4 binds to the extra-cellular matrix proteins laminin-beta3 and fibronectin. J Virol 78, 10045-10053.
6. Burns, J. W., Krishnaney, A. A., Vo, P. T., Rouse, R. V., Anderson, L. J. & Greenberg, H. B. (1995). Analyses of homologous rotavirus infection in the mouse model. Virology 207, 143-153.
7. Ciarlet, M., Conner, M. E., Finegold, M. J. & Estes, M. K. (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.
8. Cox, K. H., DeLeon, D. V., Angerer, L. M. & Angerer, R. C. (1984). Detection of mRNAs in sea urchin embryos by in situ hybridization using asymmetric RNA probes. Dev Biol 101, 485-502.
9. Crawford, S. E., Patel, D. G., Chang, E., Berkova, Z., Hyser, J. M., Ciarlet, M., Finegold, M. J., Conner, M. E. & Estes, M. K. (2006). Rotavirus viremia and extraintestinal viral infection in the neonatal rat model. J Virol 80, 4820-4832.
10. de Wit, M. A., Koopmans, M. P., van der Blij, J. F. & van Duynhoven, Y. T. (2000). Hospital admissions for rotavirus infection in the Netherlands. Clin Infect Dis 31, 698-704.
11. Fenaux, M., Cuadras, M. A., Feng, N., Jaimes, M. & Greenberg, H. B. (2006). Extraintestinal spread and replication of a homologous EC rotavirus strain and a heterologous rhesus rotavirus in BALB/c mice. J Virol 80, 5219-5232.
12. Feng, N., Burns, J. W., Bracy, L. & Greenberg, H. B. (1994). Comparison of mucosal and systemic humoral immune responses and subsequent protection in mice orally inoculated with a homologous or a heterologous rotavirus. J Virol 68, 7766-7773.
13. Fireman, P. (2003). Understanding asthma pathophysiology. Allergy Asthma Proc 24, 79-83.
14. Fromantin, C., Piroth, L., Petitpas, I., Pothier, P. & Kohli, E. (1998). Oral delivery of homologous and heterologous strains of rotavirus to BALB/c mice induces the same profile of cytokine production by spleen cells. Virology 244, 252-260.
15. Gouvea, V. S., Alencar, A. A., Barth, O. M., de Castro, L., Fialho, A. M., Araújo, H. P., Majerowicz, S. & Pereira, H. G. (1986). Diarrhoea in mice infected with a human rotavirus. J Gen Virol 67, 577-581.
16. Ishida, S. I., Feng, N., Gilbert, J. M., Tang, B. & Greenberg, H. B. (1997). Immune responses to individual rotavirus proteins following heterologous and homologous rotavirus infection in mice. J Infect Dis 175, 1317-1323.
17. Katyal, R., Rana, S. V., Vaiphei, K., Ohja, S., Singh, K. & Singh, V. (1999). Effect of rotavirus infection on small gut pathophysiology in a mouse model. J Gastroenterol Hepatol 14, 779-784.
18. Kitamoto, N., Ramig, R. F., Matson, D. O. & Estes, M. K (1991). Comparative growth of different rotavirus strains in differentiated cells (MA104, HepG2, and CaCo-2). Virology 184, 729-737.
19. Lundgren, O. & Svensson, L. (2001). Pathogenesis of rotavirus diarrhea. Microbes Infect 3, 1145-1156.
20. Majerowicz, S., Kubelka, C. F., Stephens, P. & Barth, O. M. (1994). Ultrastructural study on experimental infection of rotavirus in a murine heterologous model. Mem Inst Oswaldo Cruz 89, 395-402.
21. Matricardi, P. M., Rosmini, F., Riondino, S., Fortini, M., Ferrigno, L., Rapicetta, M. & Bonini, S. (2000). Exposure to foodborne and orofecal microbes versus airborne viruses in relation to atopy and allergic asthma: epidemiological study. BMJ 320, 412-417.
22. Matricardi, P. M., Rosmini, F., Panetta, V., Ferrigno, L. & Bonini, S. (2002). Hay fever and asthma in relation to markers of infection in the United States. J Allergy Clin Immunol 110, 381-387.
23. McNeal, M. M., Broome, R. L. & Ward, R. L. (1994). Active immunity against rotavirus infection in mice is correlated with viral replication and titers of serum rotavirus IgA following vaccination. Virology 204, 642-650.
24. Merchant, A. A., Groene, W. S., Cheng, E. H. & Shaw, R. D. (1991). Murine intestinal antibody response to heterologous rotavirus infection. J Clin Microbiol 29, 1693-1701.
25. Moon, A. & Kleinman, R. E. (1995). Allergic gastroenteropathy in children. Ann Allergy Asthma Immunol 74, 5-12.
26. Murphy, T. V., Gargiullo, P. M., Massoudi, M. S., Nelson, D. B., Jumaan, A. O., Okoro, C. A., Zanardi, L. R., Setia, S., Fair, E. & other authors (2001). Intussusception among infants given an oral rotavirus; vaccine. N Engl J Med 344, 564-572.
27. Osborne, M. P., Haddon, S. J., Spencer, A. J., Collins, J., Starkey, W. G., Wallis, T. S., Clarke, G. J., Worton, K. J., Candy, D. C. & Stephen, J. (1988). An electron microscopic investigation of time-related changes in the intestine of neonatal mice infected with murine rotavirus. J Pediatr Gastroenterol Nutr 7, 236-248.
28. Parashar, U. D., Hummelman, E. G., Bresee, J. S., Miller, M. A. & Glass, R. I. (2003). Global illness and deaths caused by rotavirus disease in children. Emerg Infect Dis 9, 565-572.
29. Renes, I. B., Verburg, M., Bulsing, N. P., Ferdinandusse, S., Buller, H. A., Dekker, J. & Einerhand, A. W. (2002). Protection of the Peyer's patch-associated crypt and villus epithelium against methotrexate-induced damage is based on its distinct regulation of proliferation. J Pathol 198, 60-68.
30. Rose, J., Franco, M. & Greenberg, H. (1998). The immunology of rotavirus infection in the mouse. Adv Virus Res 51, 203-235.
31. Rothenberg, M. E., Mishra, A., Collins, M. H. & Putnam, P. E. (2001). Pathogenesis and clinical features of eosinophilic esophagitis. J Allergy Clin Immunol 108, 891-894.
32. Shaw, R. D. & Hempson, S. J. (1996). Replication as a determinant of the intestinal response to rotavirus. J Infect Dis 174, 1328-1331.
33. Shaw, R. D., Hempson, S. J. & Mackow, E. R. (1995). Rotavirus diarrhea is caused by nonreplicating viral particles. J Virol 69, 5946-5950.
34. Sherman, M. P. & Cox, K. L. (1982). Neonatal eosinophilic colitis. J Pediatr 100, 587-589.
35. Strachan, D. P. (1989). Hay fever, hygiene, and household size. BMJ 299, 1259-1260.
36. Targan, S. R. & Murphy, L. K. (1995). Clarifying the causes of Crohn's. Nat Med 1, 1241-1243.
37. Torpier, G., Colombel, J. F., Mathieu-Chandelier, C., Capron, M., Dessaint, J. P., Cortot, A., Paris, J. C. & Capron, A. (1988). Eosinophilic gastroenteritis: ultrastructural evidence for a selective release of eosinophil major basic protein. Clin Exp Immunol 74, 404-408.
38. Uhnoo, I., Riepenhoff-Taity, M., Dharakul, T., Chagas, P., Fisher, J. E., Greenberg, H. B. & Ogra, P. L. (1990). Extramucosal spread and development of hepatitis in immunodeficient and normal mice infected with rhesus rotavirus. J Virol 64, 361-368.
39. Verburg, M., Renes, I. B., Meijer, H. P., Taminiau, J. A., Buller, H. A., Einerhand, A. W. & Dekker, J. (2000). Selective sparing of goblet cells and paneth cells in the intestine of methotrexate-treated rats. Am J Physiol Gastrointest Liver Physiol 279, G1037-G1047.
40. Walsh, R. E. & Gaginella, T. S. (1991). The eosinophil in inflammatory bowel disease. Scand J Gastroenterol 26, 1217-1224.
41. Ward, R. L. (2003). Possible mechanisms of protection elicited by candidate rotavirus vaccines as determined with the adult mouse model. Viral Immunol 16, 17-24.
42. Ward, R. L., McNeal, M. M. & Sheridan, J. F. (1990). Development of an adult mouse model for studies on protection against rotavirus. J Virol 64, 5070-5075.
43. Westerwoudt, R. J., Naipal, A. M. & Harrisson, C. M. (1984). Improved fusion technique. II. Stability and purity of hybrid clones. J Immunol Methods 68, 89-101.
44. Zhang, M., Zeng, C. Q., Morris, A. P. & Estes, M. K. (2000). A functional NSP4 enterotoxin peptide secreted from rotavirus-infected cells. J Virol 74, 11663-11670.