Home LiteratureArticle Details
PMID: 18456375 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

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 ·Vol. 26 ·No. 26 ·2008-06-19 ·Pages 3322-31

Yuan L, Wen K, Azevedo MS, Gonzalez AM, Zhang W, Saif LJ

Abstract

We examined rotavirus-specific IFN-gamma producing CD4+, CD8+ and CD4+CD8+ T cell responses in gnotobiotic pigs infected with a virulent human rotavirus (VirHRV) or vaccinated with an attenuated (Att) HRV vaccine (AttHRV3x or AttHRV2x) or an AttHRV oral priming and 2/6-virus-like particle (VLP) intranasal boosting (AttHRV-2/6VLP) regimen. In VirHRV infected pigs, HRV-specific IFN-gamma producing T cells reside primarily in ileum. AttHRV-2/6VLP induced similar frequencies of intestinal IFN-gamma producing T cells as the VirHRV, whereas AttHRV3x or 2x vaccines were less effective. Protection rates against rotavirus diarrhea upon VirHRV challenge significantly correlated (r=0.97-1.0, p<0.005) with frequencies of intestinal IFN-gamma producing T cells, suggesting their role in protective immunity.

MeSH Terms
Administration, Intranasal Administration, Oral Animals Diarrhea/immunology,prevention & control Germ-Free Life Humans Immunization, Secondary Interferon-gamma/biosynthesis Intestine, Small/immunology Rotavirus Infections/immunology,prevention & control Rotavirus Vaccines/administration & dosage,immunology Swine T-Lymphocyte Subsets/immunology T-Lymphocytes/immunology Vaccines, Attenuated/administration & dosage,immunology
Chemicals
Rotavirus Vaccines Vaccines, Attenuated Interferon-gamma
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Yuan Lijuan
Food Animal Health Research Program, Ohio Agricultural Research and Development Center, Department of Veterinary Preventive Medicine, The Ohio State University, Wooster, OH 44691, USA. lyuan@vt.edu
Wen Ke
Azevedo Marli S P
Gonzalez Ana M
Zhang Wei
Saif Linda J
References (53)
53 references, click to expand
  1. PROCUREMENT AND MAINTENANCE OF GERM-FREE SEINE FOR MICROBIOLOGICAL INVESTIGATIONS.
    Appl Microbiol. 1964 Jul;12:295-300 PMID: 14199016
  2. Viremia and nasal and rectal shedding of rotavirus in gnotobiotic pigs inoculated with Wa human rotavirus.
    J Virol. 2005 May;79(9):5428-36 PMID: 15827157
  3. 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. 2001 Jun;103(2):188-98 PMID: 11412306
  4. Role of coproantibody in clinical protection of children during reinfection with rotavirus.
    J Clin Microbiol. 1992 Jul;30(7):1678-84 PMID: 1321167
  5. Immunity to rotavirus infection in mice.
    J Infect Dis. 1999 May;179 Suppl 3:S466-9 PMID: 10099121
  6. Number and distribution of T lymphocytes in the small intestinal mucosa of calves inoculated with rotavirus.
    Vet Immunol Immunopathol. 1993 Dec;39(4):355-64 PMID: 7906907
  7. Serum IgA levels induced by rotavirus natural infection, but not following immunization with the RRV-TV vaccine (Rotashield), correlate with protection.
    J Med Virol. 2005 Aug;76(4):608-12 PMID: 15977224
  8. Immunity to rotavirus in T cell deficient mice.
    Virology. 1997 Nov 24;238(2):169-79 PMID: 9400590
  9. 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. 2000 Oct;74(19):8843-53 PMID: 10982326
  10. 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. 2002 Mar 15;20(13-14):1741-53 PMID: 11906761
  11. 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. 2001 Oct;75(19):9229-38 PMID: 11533185
  12. Heterosubtypic immunity to lethal influenza A virus infection is associated with virus-specific CD8(+) cytotoxic T lymphocyte responses induced in mucosa-associated tissues.
    Virology. 1999 Feb 1;254(1):50-60 PMID: 9927573
  13. Preferential localization of effector memory cells in nonlymphoid tissue.
    Science. 2001 Mar 23;291(5512):2413-7 PMID: 11264538
  14. Magnitude of serum and intestinal antibody responses induced by sequential replicating and nonreplicating rotavirus vaccines in gnotobiotic pigs and correlation with protection.
    Clin Diagn Lab Immunol. 2004 Jan;11(1):12-20 PMID: 14715539
  15. Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells.
    J Virol. 1994 Sep;68(9):5945-52 PMID: 8057471
  16. Induction of mucosal immune responses and protection against enteric viruses: rotavirus infection of gnotobiotic pigs as a model.
    Vet Immunol Immunopathol. 2002 Sep 10;87(3-4):147-60 PMID: 12072229
  17. Serum and intestinal isotype antibody responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease.
    J Gen Virol. 1998 Nov;79 ( Pt 11):2661-72 PMID: 9820141
  18. Systematic and intestinal antibody-secreting cell responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease.
    J Virol. 1996 May;70(5):3075-83 PMID: 8627786
  19. Frequencies of virus-specific CD4(+) and CD8(+) T lymphocytes secreting gamma interferon after acute natural rotavirus infection in children and adults.
    J Virol. 2002 May;76(10):4741-9 PMID: 11967291
  20. Defining T-cell-mediated immune responses in rotavirus-infected juvenile rhesus macaques.
    J Virol. 2004 Oct;78(19):10258-64 PMID: 15367591
  21. Porcine bone marrow myeloid cells: phenotype and adhesion molecule expression.
    J Leukoc Biol. 1997 Aug;62(2):176-85 PMID: 9261331
  22. Protection against rotavirus shedding after intranasal immunization of mice with a chimeric VP6 protein does not require intestinal IgA.
    Virology. 2006 Mar 15;346(2):338-47 PMID: 16375942
  23. Lack of correlation between serum rotavirus antibody titers and protection following vaccination with reassortant RRV vaccines. US Rotavirus Vaccine Efficacy Group.
    Vaccine. 1995 Sep;13(13):1226-32 PMID: 8578808
  24. Analysis of the human neonatal thymus: evidence for a transient thymic involution.
    J Immunol. 2000 Jun 15;164(12):6260-7 PMID: 10843679
  25. Rotavirus infection alters peripheral T-cell homeostasis in children with acute diarrhea.
    J Virol. 2007 Apr;81(8):3904-12 PMID: 17267507
  26. Intestinal double-positive CD4+CD8+ T cells are highly activated memory cells with an increased capacity to produce cytokines.
    Eur J Immunol. 2006 Mar;36(3):583-92 PMID: 16506292
  27. Analysis of the frequencies and of the memory T cell phenotypes of human CD8+ T cells specific for influenza A viruses.
    J Infect Dis. 2003 Apr 1;187(7):1075-84 PMID: 12660922
  28. Rotavirus-specific helper T cell responses in newborns, infants, children, and adults.
    J Infect Dis. 1992 Jun;165(6):1107-11 PMID: 1316412
  29. Identification of an immunodominant CD4+ T cell epitope in the VP6 protein of rotavirus following intranasal immunization of BALB/c mice.
    Virology. 2007 Jul 5;363(2):410-8 PMID: 17337285
  30. Peripheral CD4(+)CD8(+) T cells are differentiated effector memory cells with antiviral functions.
    Blood. 2004 Jul 15;104(2):478-86 PMID: 15044252
  31. 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. 2004 Mar;135(3):361-72 PMID: 15008967
  32. Functional and phenotypic analysis of porcine peripheral blood CD4/CD8 double-positive T cells.
    Immunology. 1996 Mar;87(3):500-12 PMID: 8778040
  33. IFN-gamma is the only anti-rotavirus cytokine found after in vitro stimulation of memory CD4+ T cells from mice immunized with a chimeric VP6 protein.
    Viral Immunol. 2007 Dec;20(4):571-84 PMID: 18158731
  34. CD4+ T-cell memory: generation and multi-faceted roles for CD4+ T cells in protective immunity to influenza.
    Immunol Rev. 2006 Jun;211:8-22 PMID: 16824113
  35. IL-13 replaces IL-4 in development of monocyte derived dendritic cells (MoDC) of swine.
    Vet Immunol Immunopathol. 2007 Jan 15;115(1-2):56-67 PMID: 17070934
  36. Extrathymic CD4/CD8 double positive T cells.
    Vet Immunol Immunopathol. 1999 Dec 15;72(1-2):55-66 PMID: 10614493
  37. CD4 T cells are the only lymphocytes needed to protect mice against rotavirus shedding after intranasal immunization with a chimeric VP6 protein and the adjuvant LT(R192G).
    J Virol. 2002 Jan;76(2):560-8 PMID: 11752147
  38. The role of serum antibodies in the protection against rotavirus disease: an overview.
    Clin Infect Dis. 2002 May 15;34(10):1351-61 PMID: 11981731
  39. The functional heterogeneity of type 1 effector T cells in response to infection is related to the potential for IFN-gamma production.
    J Immunol. 2005 Jun 15;174(12):7732-9 PMID: 15944275
  40. Pathogenesis of an attenuated and a virulent strain of group A human rotavirus in neonatal gnotobiotic pigs.
    J Gen Virol. 1996 Jul;77 ( Pt 7):1431-41 PMID: 8757984
  41. Mucosal B cells: phenotypic characteristics, transcriptional regulation, and homing properties.
    Immunol Rev. 2005 Aug;206:32-63 PMID: 16048541
  42. Visualizing the generation of memory CD4 T cells in the whole body.
    Nature. 2001 Mar 1;410(6824):101-5 PMID: 11242050
  43. Association of gamma interferon and interleukin-17 production in intestinal CD4+ T cells with protection against rotavirus shedding in mice intranasally immunized with VP6 and the adjuvant LT(R192G).
    J Virol. 2007 Apr;81(8):3740-8 PMID: 17251301
  44. Evidence that resolution of rotavirus infection in mice is due to both CD4 and CD8 cell-dependent activities.
    J Virol. 1997 Nov;71(11):8735-42 PMID: 9343232
  45. Interaction of rotavirus with human myeloid dendritic cells.
    J Virol. 2005 Dec;79(23):14526-35 PMID: 16282452
  46. Circulating rotavirus-specific antibody-secreting cells (ASCs) predict the presence of rotavirus-specific ASCs in the human small intestinal lamina propria.
    J Infect Dis. 2000 Oct;182(4):1039-43 PMID: 10979897
  47. Development of mucosal and systemic lymphoproliferative responses and protective immunity to human group A rotaviruses in a gnotobiotic pig model.
    Clin Diagn Lab Immunol. 1996 May;3(3):342-50 PMID: 8705681
  48. Rotavirus and severe childhood diarrhea.
    Emerg Infect Dis. 2006 Feb;12(2):304-6 PMID: 16494759
  49. Serum antibody as a marker of protection against natural rotavirus infection and disease.
    J Infect Dis. 2000 Dec;182(6):1602-9 PMID: 11069230
  50. Simultaneous detection of DNA synthesis and cytokine production in staphylococcal enterotoxin B activated CD4+ T lymphocytes by flow cytometry.
    J Immunol Methods. 1997 Oct 13;208(1):49-59 PMID: 9433460
  51. Human rotavirus specific T cells: quantification by ELISPOT and expression of homing receptors on CD4+ T cells.
    Virology. 2003 Sep 30;314(2):671-9 PMID: 14554094
  52. Comparative studies of the pathogenesis, antibody immune responses, and homologous protection to porcine and human rotaviruses in gnotobiotic piglets.
    Adv Exp Med Biol. 1997;412:397-403 PMID: 9192046
  53. Cell-mediated immune response in rotavirus-infected calves: leucocyte migration inhibition assay.
    J Comp Pathol. 1992 Jul;107(1):115-8 PMID: 1430345
Article Info
Journal
Vaccine
Abbr.
Vaccine
ISSN
0264-410X
DOI
10.1016/j.vaccine.2008.03.085
Email
lyuan@vt.edu
Published
2008-06-19
Epub
2008-00-18
Pages
3322-31
Language
English
Region
Netherlands
NLM ID
8406899
PMCID
PMC2574896
Subset
IM
Grants
NIAID NIH HHS · R01 AI033561-11 · United States
NIAID NIH HHS · R01 AI033561 · United States
NCCIH NIH HHS · R21 AT002524-02 · United States
NCCIH NIH HHS · R21 AT 002524 · United States
NCCIH NIH HHS · R21 AT002524 · United States
NIAID NIH HHS · R01 AI 33561 · United States
External Links
PubMed source DOI: 10.1016/j.vaccine.2008.03.085 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2