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01-01-2009 | Original Article

B-cell activation in cats with feline infectious peritonitis (FIP) by FIP-virus-induced B-cell differentiation/survival factors

Authors: Tomomi Takano, Natsuko Azuma, Yoshikiyo Hashida, Ryoichi Satoh, Tsutomu Hohdatsu

Published in: Archives of Virology | Issue 1/2009

Abstract

It has been suggested that antibody overproduction plays a role in the pathogenesis of feline infectious peritonitis (FIP). However, only a few studies on the B-cell activation mechanism after FIP virus (FIPV) infection have been reported. The present study shows that: (1) the ratio of peripheral blood sIg⁺ CD21⁻ B-cells was higher in cats with FIP than in SPF cats, (2) the albumin-to-globulin ratio has negative correlation with the ratio of peripheral blood sIg⁺ CD21⁻ B-cell, (3) cells strongly expressing mRNA of the plasma cell master gene, B-lymphocyte-induced maturation protein 1 (Blimp-1), were increased in peripheral blood in cats with FIP, (4) mRNA expression of B-cell differentiation/survival factors, IL-6, CD40 ligand, and B-cell-activating factor belonging to the tumor necrosis factor family (BAFF), was enhanced in macrophages in cats with FIP, and (5) mRNAs of these B-cell differentiation/survival factors were overexpressed in antibody-dependent enhancement (ADE)-induced macrophages. These data suggest that virus-infected macrophages overproduce B-cell differentiation/survival factors, and these factors act on B-cells and promote B-cell differentiation into plasma cells in FIPV-infected cats.

Addie DD, Jarrett O (1998) Feline coronavirus infection. In: Greene CE (ed) Infectious diseases of the dog and cat. WB Saunders, Pennsylvania, pp 58–69

Addie DD, Toth S, Murray GD, Jarrett O (1995) Risk of feline infectious peritonitis in cats naturally infected with feline coronavirus. Am J Vet Res 56:429–434PubMed

Armitage RJ, Fanslow WC, Strockbine L, Sato TA, Clifford KN, Macduff BM, Anderson DM, Gimpel SD, Davis-Smith T, Maliszewski CR, Clark EA, Smith CA, Grabstein KH, Cosman D, Spriggs MK (1992) Molecular and biological characterization of a murine ligand for CD40. Nature 357:80–82PubMedCrossRef

Avery PR, Hoover EA (2004) Gamma interferon/interleukin 10 balance in tissue lymphocytes correlates with down modulation of mucosal feline immunodeficiency virus infection. J Virol 78:4011–4019PubMedCrossRef

Corapi WV, Olsen CW, Scott FW (1992) Monoclonal antibody analysis of neutralization and antibody-dependent enhancement of feline infectious peritonitis virus. J Virol 66:6695–6705PubMed

Craxton A, Magaletti D, Ryan EJ, Clark EA (2003) Macrophage- and dendric cell-dependent regulation of human B cell proliferation requires the TNF family ligand BAFF. Blood 101:4464–4471PubMedCrossRef

Dolcetti R, Boiocchi M (1996) Cellular and molecular bases of B-cell clonal expansions. Clin Exp Rheumatol 14:3–13

Goitsuka R, Ohashi T, Ono K, Yasukawa K, Koishibara Y, Fukui H, Ohsugi Y, Hasegawa A (1990) IL-6 activity in feline infectious peritonitis. J Immunol 144:2599–2603PubMed

Goules A, Tzioufas AG, Manousakis MN, Kirou KA, Crow MK, Routsias JG (2006) Elevated levels of soluble CD40 ligand (sCD40L) in serum of patients with systemic autoimmune diseases. J Autoimmun 26:165–171PubMedCrossRef

10.

Halstead SB (2003) Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 60:421–467PubMedCrossRef

11.

Herrewegh AA, Vennema H, Horzinek MC, Rottier PJ, de Groot RJ (1995) The molecular genetics of feline coronaviruses: comparative sequence analysis of the ORF7a/7b transcription unit of different biotypes. Virology 212:622–631PubMedCrossRef

12.

Hohdatsu T, Nakamura M, Ishizuka Y, Yamada H, Koyama H (1991) A study on the mechanism of antibody-dependent enhancement of feline infectious peritonitis virus infection in feline macrophages by monoclonal antibodies. Arch Virol 120:207–217PubMedCrossRef

13.

Hohdatsu T, Okada S, Koyama H (1991) Characterization of monoclonal antibodies against feline infectious peritonitis virus type II and antigenic relationship between feline, porcine and canine coronaviruses. Arch Virol 117:85–95PubMedCrossRef

14.

Hohdatsu T, Yamada H, Ishizuka Y, Koyama H (1993) Enhancement and neutralization of feline infectious peritonitis virus infection in feline macrophages by neutralizing monoclonal antibodies recognizing different epitopes. Microbiol Immunol 37:499–504PubMed

15.

Hohdatsu T, Tokunaga J, Koyama H (1994) The role of IgG subclass of mouse monoclonal antibodies in antibody-dependent enhancement of feline infectious peritonitis virus infection of feline macrophages. Arch Virol 139:273–285PubMedCrossRef

16.

Hokazono Y, Adachi T, Wabl M, Tada N, Amagasa T, Tsubata T (2003) Inhibitory co-receptors activated by antigens but not by anti-immunoglobulin heavy chain antibodies install requirement of co-stimulation through CD40 for survival and proliferation of B cells. J Immunol 171:1835–1843PubMed

17.

Holder MJ, Wang H, Milner AE, Casamayor M, Armitage R, Spriggs MK, Fanslow WC, MacLennan IC, Gregory CD, Gordon J (1993) Suppression of apoptosis in normal and neoplastic human B lymphocytes by CD40 ligand is independent of Bcl-2 induction. Eur J Immunol 23:2368–2371PubMedCrossRef

18.

Kawano MM, Mihara K, Huang N, Tsujimoto T, Kuramoto A (1995) Differentiation of early plasma cells on bone marrow stromal cells requires Interleukin-6 for escaping from apoptosis. Blood 85:487–494PubMed

19.

Klein B, Tarte K, Jourdan M, Mathouk K, Moreaux J, Jourdan E, Legouffe E, De Vos J, Rossi JF (2003) Survival and proliferation factors of normal and malignant plasma cells. Int J Hematol 78:106–113PubMedCrossRef

20.

Mach F, Schonbeck U, Sukhova GK, Bourcier T, Bonnefoy JY, Pober JS, Libby P (1997) Functional CD40 ligand is expressed on human vascular endothelial cells, smooth muscle cells, and macrophages: implications for CD40-CD40 ligand signaling in atherosclerosis. Proc Natl Acad Sci U S A 94:1931–1936PubMedCrossRef

21.

Mackay F, Woodcock SA, Lawton P, Ambrose C, Baetscher M, Schneider P, Tschopp J, Browning JL (1999) Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med 190:1697–1710PubMedCrossRef

22.

Matsushita T, Sato S (2005) The role of BAFF in autoimmune disease. Jpn J Clin Immunol 28:333–342CrossRef

23.

Olsen CW, Corapi WV, Ngichabe CK, Baines JD, Scott FW (1992) Monoclonal antibodies to the spike protein of feline infectious peritonitis virus mediate antibody-dependent enhancement of infection of feline macrophages. J Virol 66:956–965PubMed

24.

Olsen CW (1993) A review of feline infectious peritonitis virus: molecular biology, immunopathogenesis, clinical aspects, and vaccination. Vet Microbiol 36:1–37PubMedCrossRef

25.

Pedersen NC, Boyle JF (1980) Immunologic phenomena in the effusive form of feline infectious peritonitis. Am J Vet Res 41:868–876

26.

Poland AM, Vennema H, Foley JE, Pedersen NC (1996) Two related strains of feline infectious peritonitis virus isolated from immunocompromised cats infected with a feline enteric coronavirus. J Clin Microbiol 34:3180–3184PubMed

27.

Rottier PJ, Nakamura K, Schellen P, Volders H, Haijema BJ (2005) Acquisition of macrophage tropism during the pathogenesis of feline infectious peritonitis is determined by mutations in the feline coronavirus spike protein. J Virol 79:14122–14130PubMedCrossRef

28.

Shapiro-Shelef M, Calame K (2005) Regulation of plasma-cell development. Nat Rev Immunol 5:230–242PubMedCrossRef

29.

Stoddart CA, Scott FW (1989) Intrinsic resistance of feline peritoneal macrophages to coronavirus infection correlates with in vivo virulence. J Virol 63:436–440PubMed

30.

Takano T, Hohdatsu T, Hashida Y, Kaneko Y, Tanabe M, Koyama H (2007) A “possible” involvement of TNF-alpha in apoptosis induction in peripheral blood lymphocytes of cats with feline infectious peritonitis. Vet Microbiol 119:121–131PubMedCrossRef

31.

Takano T, Hohdatsu T, Toda A, Tanabe M, Koyama H (2007) TNF-alpha, produced by feline infectious peritonitis virus (FIPV)-induced macrophages, upregulates expression of type II FIPV receptor feline aminopeptidase N in feline macrophages. Virology 364:64–72PubMedCrossRef

32.

Takano T, Katada Y, Moritoh S, Ogasawara M, Satoh K, Satoh R, Tanabe M, Hohdatsu T (2008) Analysis of the mechanism of antibody-dependent enhancement of feline infectious peritonitis virus infection: aminopeptidase N is not important and a process of acidification of the endosome is necessary. J Gen Virol 89:1025–1029PubMedCrossRef

33.

Takeda A, Sweet RW, Ennis FA (1990) Two receptors are required for antibody- dependent enhancement of human immunodeficiency virus type 1 infection: CD4 and Fc gamma R. J Virol 64:5605–5610PubMed

34.

Tedder TF, Clement LT, Cooper MD (1984) Expression of C3d receptors during human B cell differentiation: immunofluorescence analysis with the HB-5 monoclonal antibody. J Immunol 133:678–683PubMed

35.

Tirado SM, Yoon KJ (2003) Antibody-dependent enhancement of virus infection and disease. Viral Immunol 16:69–86PubMedCrossRef

36.

Tumang JR, Hsia CY, Tian W, Bromberg JF, Liou HC (2002) IL-6 rescues the hyporesponsiveness of c-Rel deficient B cells independent of Bcl-xL, Mcl-1, and Bcl-2. Cell Immunol 217:47–57PubMedCrossRef

37.

Vennema H, Poland A, Foley J, Pedersen NC (1998) Feline infectious peritonitis viruses arise by mutation from endemic feline enteric coronaviruses. Virology 243:150–157PubMedCrossRef

Title: B-cell activation in cats with feline infectious peritonitis (FIP) by FIP-virus-induced B-cell differentiation/survival factors
Authors: Tomomi Takano
Natsuko Azuma
Yoshikiyo Hashida
Ryoichi Satoh
Tsutomu Hohdatsu
Publication date: 01-01-2009
Publisher: Springer Vienna
Published in: Archives of Virology / Issue 1/2009
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-008-0265-9

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