Suppression of NK cells and regulatory T lymphocytes in cats naturally infected with feline infectious peritonitis virus

Veterinary Microbiology

Volumn 164, Issue 1-2, 2013, Pages 46-59

  Vermeulen, Ben L ^a   Devriendt, Bert ^a   Olyslaegers, Dominique A ^a   Dedeurwaerder, Annelike ^a   Desmarets, Lowiese M ^a   Favoreel, Herman W ^a   Dewerchin, Hannah L ^a   Nauwynck, Hans J ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Adaptive immunity; Cat; Feline infectious peritonitis; Innate immunity; Natural killer cells; Regulatory T cells

Indexed keywords

CD11B ANTIGEN; CD16 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD5 ANTIGEN; CD8 ANTIGEN; L SELECTIN; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAT; CD25+ T LYMPHOCYTE; CELL FUNCTION; CELL ISOLATION; CELL MIGRATION; CELL VIABILITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CORONAVIRUS; CYTOTOXICITY; INNATE IMMUNITY; KIDNEY; MESENTERY; MESENTERY LYMPH NODE; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; REGULATORY T LYMPHOCYTE; T CELL DEPLETION; UPREGULATION;

ANIMALS; CATS; CORONAVIRUS, FELINE; FELINE INFECTIOUS PERITONITIS; IMMUNE TOLERANCE; IMMUNITY, CELLULAR; KILLER CELLS, NATURAL; SPLEEN; T-LYMPHOCYTES, REGULATORY;

ANIMALIA; FELIDAE; FELINE INFECTIOUS PERITONITIS VIRUS;

EID: 84875852032     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2013.01.042     Document Type: Article

References (57)

1. Addie D., Belak S., Boucraut-Baralon C., Egberink H., Frymus T., Gruffydd-Jones T., Hartmann K., Hosie M.J., Lloret A., Lutz H., Marsilio F., Pennisi M.G., Radford A.D., Thiry E., Truyen U., Horzinek M.C. Feline infectious peritonitis ABCD guidelines on prevention and management. J. Feline Med. Surg. 2009, 11:594-604.
2. Andersson J., Boasso A., Nilsson J., Zhang R., Shire N.J., Lindback S., Shearer G.M., Chougnet C.A. Cutting edge: the prevalence of regulatory T cells lymphoid tissue is correlated with viral load HIV-infected patients. J. Immunol. 2005, 174:3143-3147.
3. Belkaid Y., Rouse B.T. Natural regulatory T cells in infectious disease. Nat. Immunol. 2005, 6:353-360.
4. Belkaid Y., Tarbell K.V. Arming Treg cells at the inflammatory site. Immunity 2009, 30:322-323.
5. Berg A.L., Ekman K., Belak S., Berg M. Cellular composition and interferon-gamma expression of the local inflammatory response in feline infectious peritonitis (FIP). Vet. Microbiol. 2005, 111:15-23.
6. Blue J., Weiss L. Species variation in the structure and function of the marginal zone-an electron-microscope study of cat spleen. Am. J. Anat. 1981, 161:169-187.
7. Brandstadter J.D., Yang Y.P. Natural killer cell responses to viral infection. J. Innate Immun. 2011, 3:274-279.
8. Bull M., Lee D., Stucky J., Chiu Y.L., Rubin A., Horton H., McElrath M.J. Defining blood processing parameters for optimal detection of cryopreserved antigen-specific responses for HIV vaccine trials. J. Immunol. Methods 2007, 322:57-69.
9. Campbell D.J., Koch M.A. Phenotypical and functional specialization of FOXP3(+) regulatory T cells. Nat. Rev. Immunol. 2011, 11:119-130.
10. Chang H.W., de Groot R.J., Egberink H.F., Rottier P.J.M. Feline infectious peritonitis: insights into feline coronavirus pathobiogenesis and epidemiology based on genetic analysis of the viral 3c gene. J. Gen. Virol. 2010, 91:415-420.
11. Cornelissen E., Dewerchin H.L., Van Hamme E., Nauwynck H.J. Absence of surface expression of feline infectious peritonitis virus (FIPV) antigens on infected cells isolated from cats with FIP. Vet. Microbiol. 2007, 121:131-137.
12. Crozat K., Eidenschenk C., Jaeger B.N., Krebs P., Guia S., Beutler B., Vivier E., Ugolini S. Impact of beta 2 integrin deficiency on mouse natural killer cell development and function. Blood 2011, 117:2874-2882.
13. Denney L., Aitken C., Li C.K.F., Wilson-Davies E., Kok W.L., Clelland C., Rooney K., Young D., Dong T., McMichael A.J., Carman W.F., Ho L.P. Reduction of natural killer but not effector CD8 T lymphocytes in three consecutive cases of severe/lethal H1N1/09 influenza a virus infection. Plos ONE 2010, 5.
14. Dewerchin H.L., Cornelissen E., Nauwynck H.J. Feline infectious peritonitis virus-infected monocytes internalize viral membrane-bound proteins upon antibody addition. J. Gen. Virol. 2006, 87:1685-1690.
15. Dewerchin H.L., Cornelissen E., Van Hamme E., Smits K., Verhasselt B., Nauwynck H.J. Surface-expressed viral proteins in feline infectious peritonitis virus-infected monocytes are internalized through a clathrin- and caveolae-independent pathway. J. Gen. Virol. 2008, 89:2731-2740.
16. Fu B.Q., Wang F.Y., Sun R., Ling B., Tian Z.G., Wei H.M. CD11b and CD27 reflect distinct population and functional specialization in human natural killer cells. Immunology 2011, 133:350-359.
17. Gomez-Ochoa P., Sabate D., Homedes J., Ferrer L. Use of the nitroblue tetrazolium reduction test for the evaluation of Domperidone effects on the neutrophilic function of healthy dogs. Vet. Immunol. Immunopathol. 2012, 146:97-99.
18. Grubor-Bauk B., Arthur J.L., Mayrhofer G. Importance of NKT cells in resistance to herpes simplex virus, fate of virus-infected neurons, and level of latency in mice. J. Virol. 2008, 82:11073-11083.
19. Haagmans B.L., Egberink H.F., Horzinek M.C. Apoptosis and T-cell depletion during feline infectious peritonitis. J. Virol. 1996, 70:8977-8983.
20. Han Y., Guo Q., Zhang M., Chen Z., Cao X. CD69+CD4+CD25- T cells, a new subset of regulatory T cells, suppress T cell proliferation through membrane-bound TGF-β1. J. Immunol. 2009, 182:111-120.
21. Hartmann K. Feline infectious peritonitis. Vet. Clin. North Am. 2005, 35:39-79.
22. Hartmann K., Ritz S. Treatment of cats with feline infectious peritonitis. Vet. Immunol. Immunopathol. 2008, 123:172-175.
23. He Z.P., Zhao C.H., Dong Q.M., Zhuang H., Song S.J., Peng G., Dwyer D.E. Effects of severe acute respiratory syndrome (SARS) coronavirus infection on peripheral blood lymphocytes and their subsets. Int. J. Infect. Dis. 2005, 9:323-330.
24. Holzworth J. Some important disorders of cats. Cornell Vet. 1963, 53:157-160.
25. Howard K.E., Reckling S.K., Egan E.A., Dean G.A. Acute mucosal pathogenesis of feline immunodeficiency virus is independent of viral dose in vaginally infected cats. Retrovirology 2010, 7:2-16.
26. Jonjic S., Babic M., Polic B., Krmpotic A. Immune evasion of natural killer cells by viruses. Curr. Opin. Immunol. 2008, 20:30-38.
27. Juelke K., Killig M., Luetke-Eversloh M., Parente E., Gruen J., Morandi B., Ferlazzo G., Thiel A., Schmitt-Knosalla I., Romagnani C. CD62L expression identifies a unique subset of polyfunctional CD56(dim) NK cells. Blood 2010, 116:1299-1307.
28. Keynan Y., Card C.M., McLaren P.J., Dawood M.R., Kasper K., Fowke K.R. The role of regulatory T cells in chronic and acute viral infections. Clin. Infect. Dis. 2008, 46:1046-1052.
29. Kos F.J., Engleman E.G. Immune regulation: a critical link between NK cells and CTLs. Immunol. Today 1996, 17:174-176.
30. Kuylenstierna C., Bjorkstrom N.K., Andersson S.K., Sahlstrom P., Bosnjak L., Paquin-Proulx D., Malmberg K.J., Ljunggren H.G., Moll M., Sandberg J.K. NKG2D performs two functions in invariant NKT cells: direct TCR-independent activation of NK-like cytolysis and co-stimulation of activation by CD1d. Eur. J. Immunol. 2011, 41:1913-1923.
31. Lankford S., Petty C., La Voy A., Reckling S., Tompkins W., Dean G.A. Cloning of feline FOXP3 and detection of expression in CD4+CD25+ regulatory T cells. Vet. Immunol. Immunopathol. 2008, 122:159-166.
32. Leavy O. Regulatory T cells Cd8(+) T-reg cells join the fold. Nat. Rev. Immunol. 2010, 10:680.
33. Li S., Gowans E.J., Chougnet C., Plebanski M., Dittmer U. Natural regulatory T cells and persistent viral infection. J. Virol. 2008, 82:21-30.
34. Long B.R., Erickson A.E., Chapman J.M., Barbour J.D., Vu B.A.N., Ho E.L., Lanier L.L., Sauer M.M., Carvalho K.I., Nixon D.F., Kallas E.G. Increased number and function of natural killer cells in human immunodeficiency virus 1-positive subjects co-infected with herpes simplex virus 2. Immunology 2010, 129:186-196.
35. Luhn K., Simmons C.P., Moran E., Dung N.T.P., Chau T.N.B., Quyen N.T.H., Thao L.T.T., Van Ngoc T., Dung N.M., Wills B., Farrar J., McMichael A.J., Dong T., Rowland-Jones S. Increased frequencies of CD4(+) CD25(high) regulatory T cells in acute dengue infection. J. Exp. Med. 2007, 204:979-985.
36. Mao H.W., Tu W.W., Qin G., Law H.L.K.W., Sia S.F., Chan P.L., Liu Y.P., Lam K.T., Zheng J., Peiris M., Lau Y.L. Influenza virus directly infects human natural killer cells and induces cell apoptosis. J. Virol. 2009, 83:9215-9222.
37. Mauri C., Bosma A. Immune regulatory function of B cells. Annu. Rev. Immunol. 2012, 30:221-241.
38. Mebius R.E., Kraal G. Structure and function of the spleen. Nat. Rev. Immunol. 2005, 5:606-616.
39. Meier U.C., Owen R.E., Taylor E., Worth A., Naoumov N., Willberg C., Tang K., Newton P., Pellegrino P., Williams I., Klenerman P., Borrow P. Shared alterations in NK cell frequency, phenotype, and function in chronic human immunodeficiency virus and hepatitis C virus infections. J. Virol. 2005, 79:12365-12374.
40. Mizoguchi A., Bhan A.K. A case for regulatory B cells. J. Immunol. 2006, 176:705-710.
41. Morgan M.E., van Bilsen J.H.M., Bakker A.M., Heemskerk B., Schilham M.W., Hartgers F.C., Elferink B.G., van der Zanden L., de Vries R.R.P., Huizinga T.W.J., Ottenhoff T.H.M., Toes R.E.M. Expression of FOXP3 mRNA is not confined to CD4(+)CD25(+) T regulatory cells in humans. Hum. Immunol. 2005, 66:13-20.
42. Morishima C., Paschal D.M., Wang C.C., Yoshihara C.S., Wood B.L., Yeo A.E.T., Emerson S.S., Shuhart M.C., Gretch D.R. Decreased NK cell frequency in chronic hepatitis C does not affect ex vivo cytolytic killing. Hepatology 2006, 43:573-580.
43. Nauwynck H.J., Pensaert M.B. Effect of specific antibodies on the cell-associated spread of pseudorabies virus in monolayers of different cell types. Arch. Virol. 1995, 140:1137-1146.
44. Nishimura Y., Shimojima M., Sato E., Izumiya Y., Tohya Y., Mikami T., Miyazawa T. Downmodulation of CD3 epsilon expression CD8 alpha(+)beta(-) T cells of feline immunodeficiency virus-infected cats. J. Gen. Virol. 2004, 85:2585-2589.
45. Noh J., Choi W.S., Noh G., Lee J.H. Presence of Foxp3-expressing CD19(+)CD5(+) B cells in human peripheral blood mononuclear cells: human CD19(+)CD5(+)Foxp3(+) regulatory B cell (Breg). Immune Netw. 2010, 10:247-249.
46. Paltrinieri S., Ponti W., Comazzi S., Giordano A., Poli G. Shifts in circulating lymphocyte subsets in cats with feline infectious peritonitis (FIP): pathogenic role and diagnostic relevance. Vet. Immunol. Immunopathol. 2003, 96:141-148.
47. Pedersen N.C., Black J.W. Attempted immunization of cats against feline infectious peritonitis, using avirulent live virus or sublethal amounts of virulent virus. Am. J. Vet. Res. 1983, 44:229-234.
48. Pedersen N.C., Boyle J.F. Immunologic phenomena in the effusive form of feline infectious peritonitis. Am. J. Vet. Res. 1980, 41:868-876.
49. Robbins S.H., Bessou G., Cornillon A., Zucchini N., Rupp B., Ruzsics Z., Sacher T., Tomasello E., Vivier E., Koszinowski U.H., Dalod M. Natural killer cells promote early CD8 T cell responses against cytomegalovirus. PLoS Path 2007, 3:1152-1164.
50. Romagnani C., Juelke K., Falco M., Morandi B., D'Agostino A., Costa R., Ratto G., Forte G., Carrega P., Lui G., Conte R., Strowig T., Moretta A., Munz C., Thiel A., Moretta L., Ferlazzo G. CD56(bright) CD16(-) killer Ig-like receptor(-) NK cells display longer telomeres and acquire features of CD56(dim) NK cells upon activation. J. Immunol. 2007, 178:4947-4955.
51. Shimojima M., Nishimura Y., Miyazawa T., Kato K., Tohya Y., Akashi H. CD56 expression in feline lymphoid cells. J. Vet. Med. Sci. 2003, 65:769-773.
52. Takano T., Hohdatsu T., Hashida Y., Kaneko Y., Tanabe M., Koyama H. A " possible" involvement of TNF-alpha in apoptosis induction in peripheral blood lymphocytes of cats with feline infectious peritonitis. Vet. Microbiol. 2007, 119:121-131.
53. Tessmer M.S., Fatima A., Paget C., Trottein F., Brossay L. NKT cell immune responses to viral infection. Expert Opin. Ther. Targets 2009, 13:153-162.
54. Vermeulen B.L., Devriendt B., Olyslaegers D.A., Dedeurwaerder A., Desmarets L.M., Grauwet K.L., Favoreel H.W., Dewerchin H.L., Nauwynck H.J. Natural killer cells: frequency, phenotype and function in healthy cats. Vet. Immunol. Immunopathol. 2012, 150:69-78.
55. Wood S.M., Ljunggren H.G., Bryceson Y.T. Insights into NK cell biology from human genetics and disease associations. Cell. Mol. Life Sci. 2011, 68:3479-3493.
56. Zhang N., Schroppel B., Lal G., Jakubzick C., Mao X., Chen D., Yin N., Jessberger R., Ochando J.C., Ding Y.Z., Bromberg J.S. Regulatory T cells sequentially migrate from inflamed tissues to draining lymph nodes to suppress the alloimmune response. Immunity 2009, 30:458-469.
57. Zingoni A., Sornasse T., Cocks B.G., Tanaka Y., Santoni A., Lanier L.L. NK cell regulation of T cell-mediated responses. Mol. Immunol. 2005, 42:451-454.