Journal of Veterinary Science

The Korean Society of Veterinary Science (대한수의학회)
권호 표지
DOI QR코드

DOI QR Code

Expression of Toll-like receptors 3, 7, 9 and cytokines in feline infectious peritonitis virus-infected CRFK cells and feline peripheral monocytes

  • Received : 2021.08.10
  • Accepted : 2021.11.29
  • Published : 2022.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Background: The role of Toll-like receptors (TLRs) in a feline infectious peritonitis virus (FIPV) infection is not completely understood. Objectives: This study examined the expression of TLR3, TLR7, TLR9, tumor necrosis factor-alpha (TNF-α), interferon (IFN)-β, and interleukin (IL)-10 upon an FIPV infection in Crandell-Reese feline kidney (CRFK) cells and feline monocytes. Methods: CRFK cells and monocytes from feline coronavirus (FCoV)-seronegative cats and FCoV-seropositive cats were infected with type II FIPV-79-1146. At four, 12, and 24 hours post-infection (hpi), the expression of TLR3, TLR7, TLR9, TNF-α, IFN-β, and IL-10, and the viral load were measured using reverse transcription quantitative polymerase chain reaction. Viral protein production was confirmed using immunofluorescence. Results: FIPV-infected CRFK showed the upregulation of TLR9, TNF-α, and IFN-β expression between 4 and 24 hpi. Uninfected monocytes from FCoV-seropositive cats showed lower TLR3 and TLR9 expression but higher TLR7 expression compared to uninfected monocytes from FCoV-seronegative cats. FIPV-infected monocytes from FCoV-seropositive cats downregulated TLR7 and TNF-α expression between 4 and 24 hpi, and 4 and 12 hpi, respectively. IFN-β was upregulated early in FIPV-infected monocytes from FCoV-seropositive cats, with a significant difference observed at 12 hpi compared to FCoV-seronegative cats. The viral load in the CRFK and FIPV-infected monocytes in both cohorts of cats was similar over time.ConclusionTLR7 may be the key TLR involved in evading the innate response against inhibiting TNF-α production. Distinct TLR expression profiles between FCoV-seronegative and FCoV-seropositive cats were observed. The associated TLR that plays a role in the induction of IFN-β needs to be explored further.

Keywords

Acknowledgement

The authors would like to acknowledge Dr. Tan Sheau Wei for the technical assistance in conducting the real-time PCR assay.

References

  1. Addie DD, Schaap IA, Nicolson L, Jarrett O. Persistence and transmission of natural type I feline coronavirus infection. J Gen Virol. 2003;84(Pt 10):2735-2744. https://doi.org/10.1099/vir.0.19129-0
  2. Herrewegh AA, Smeenk I, Horzinek MC, Rottier PJ, de Groot RJ. Feline coronavirus type II strains 79-1683 and 79-1146 originate from a double recombination between feline coronavirus type I and canine coronavirus. J Virol. 1998;72(5):4508-4514. https://doi.org/10.1128/jvi.72.5.4508-4514.1998
  3. Vennema H, Poland A, Foley J, Pedersen NC. Feline infectious peritonitis viruses arise by mutation from endemic feline enteric coronaviruses. Virology. 1998;243(1):150-157. https://doi.org/10.1006/viro.1998.9045
  4. Pedersen NC. A review of feline infectious peritonitis virus infection: 1963-2008. J Feline Med Surg. 2009;11(4):225-258. https://doi.org/10.1016/j.jfms.2008.09.008
  5. Addie DD, Toth S, Murray GD, Jarrett O. Risk of feline infectious peritonitis in cats naturally infected with feline coronavirus. Am J Vet Res. 1995;56(4):429-434.
  6. de Groot-Mijnes JD, van Dun JM, van der Most RG, de Groot RJ. Natural history of a recurrent feline coronavirus infection and the role of cellular immunity in survival and disease. J Virol. 2005;79(2):1036-1044. https://doi.org/10.1128/JVI.79.2.1036-1044.2005
  7. Kipar A, Kohler K, Leukert W, Reinacher M. A comparison of lymphatic tissues from cats with spontaneous feline infectious peritonitis (FIP), cats with FIP virus infection but no FIP, and cats with no infection. J Comp Pathol. 2001;125(2-3):182-191. https://doi.org/10.1053/jcpa.2001.0501
  8. Kipar A, Meli ML, Failing K, Euler T, Gomes-Keller MA, Schwartz D, et al. Natural feline coronavirus infection: differences in cytokine patterns in association with the outcome of infection. Vet Immunol Immunopathol. 2006;112(3-4):141-155. https://doi.org/10.1016/j.vetimm.2006.02.004
  9. Mustaffa-Kamal F, Liu H, Pedersen NC, Sparger EE. Characterization of antiviral T cell responses during primary and secondary challenge of laboratory cats with feline infectious peritonitis virus (FIPV). BMC Vet Res. 2019;15(1):165. https://doi.org/10.1186/s12917-019-1909-6
  10. Petersen NC, Boyle JF. Immunologic phenomena in the effusive form of feline infectious peritonitis. Am J Vet Res. 1980;41(6):868-876.
  11. Weiss RC, Scott FW. Antibody-mediated enhancement of disease in feline infectious peritonitis: comparisons with dengue hemorrhagic fever. Comp Immunol Microbiol Infect Dis. 1981;4(2):175-189. https://doi.org/10.1016/0147-9571(81)90003-5
  12. Hohdatsu T, Yamada M, Tominaga R, Makino K, Kida K, Koyama H. Antibody-dependent enhancement of feline infectious peritonitis virus infection in feline alveolar macrophages and human monocyte cell line U937 by serum of cats experimentally or naturally infected with feline coronavirus. J Vet Med Sci. 1998;60(1):49-55. https://doi.org/10.1292/jvms.60.49
  13. Takano T, Azuma N, Hashida Y, Satoh R, Hohdatsu T. B-cell activation in cats with feline infectious peritonitis (FIP) by FIP-virus-induced B-cell differentiation/survival factors. Arch Virol. 2009;154(1):27-35. https://doi.org/10.1007/s00705-008-0265-9
  14. Ignacio G, Nordone S, Howard KE, Dean GA. Toll-like receptor expression in feline lymphoid tissues. Vet Immunol Immunopathol. 2005;106(3-4):229-237. https://doi.org/10.1016/j.vetimm.2005.02.022
  15. Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 2011;34(5):637-650. https://doi.org/10.1016/j.immuni.2011.05.006
  16. Cervantes-Barragan L, Zust R, Weber F, Spiegel M, Lang KS, Akira S, et al. Control of coronavirus infection through plasmacytoid dendritic-cell-derived type I interferon. Blood. 2007;109(3):1131-1137. https://doi.org/10.1182/blood-2006-05-023770
  17. Channappanavar R, Fehr AR, Zheng J, Wohlford-Lenane C, Abrahante JE, Mack M, et al. IFN-I response timing relative to virus replication determines MERS coronavirus infection outcomes. J Clin Invest. 2019;129(9):3625-3639. https://doi.org/10.1172/jci126363
  18. Temeeyasen G, Sinha A, Gimenez-Lirola LG, Zhang JQ, Pineyro PE. Differential gene modulation of pattern-recognition receptor TLR and RIG-I-like and downstream mediators on intestinal mucosa of pigs infected with PEDV non S-INDEL and PEDV S-INDEL strains. Virology. 2018;517:188-198. https://doi.org/10.1016/j.virol.2017.11.024
  19. Addie D. The diagnosis and prevention of FIP and recent research into feline Coronavirus shedding. In: Presented at the ESVIM Proceedings: 8th Annual Congress of the European Society of Veterinary Internal Medicine, Vienna, Austria, September 24-26, 1998. Stockton on Tees: European Society of Veterinary Internal Medicine; 1998.
  20. Freer G, Matteucci D, Mazzetti P, Bozzacco L, Bendinelli M. Generation of feline dendritic cells derived from peripheral blood monocytes for in vivo use. Clin Diagn Lab Immunol. 2005;12(10):1202-1208. https://doi.org/10.1128/CDLI.12.10.1202-1208.2005
  21. Gut M, Leutenegger CM, Huder JB, Pedersen NC, Lutz H. One-tube fluorogenic reverse transcription-polymerase chain reaction for the quantitation of feline coronaviruses. J Virol Methods. 1999;77(1):37-46. https://doi.org/10.1016/S0166-0934(98)00129-3
  22. Kipar A, Leutenegger CM, Hetzel U, Akens MK, Mislin CN, Reinacher M, et al. Cytokine mRNA levels in isolated feline monocytes. Vet Immunol Immunopathol. 2001;78(3-4):305-315. https://doi.org/10.1016/S0165-2427(01)00240-9
  23. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) Method. Methods. 2001;25(4):402-408. https://doi.org/10.1006/meth.2001.1262
  24. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3:RESEARCH0034.
  25. Ng SW, Selvarajah GT, Cheah YK, Mustaffa Kamal F, Omar AR. Cellular metabolic profiling of CrFK cells infected with feline infectious peritonitis virus using phenotype microarrays. Pathogens. 2020;9(5):9.
  26. Takano T, Azuma N, Satoh M, Toda A, Hashida Y, Satoh R, et al. Neutrophil survival factors (TNF-alpha, GM-CSF, and G-CSF) produced by macrophages in cats infected with feline infectious peritonitis virus contribute to the pathogenesis of granulomatous lesions. Arch Virol. 2009;154(5):775-781. https://doi.org/10.1007/s00705-009-0371-3
  27. Li SW, Wang CY, Jou YJ, Huang SH, Hsiao LH, Wan L, et al. SARS coronavirus papain-like protease inhibits the TLR7 signaling pathway through removing Lys63-linked polyubiquitination of TRAF3 and TRAF6. Int J Mol Sci. 2016;17(5):678. https://doi.org/10.3390/ijms17050678
  28. Malbon AJ, Meli ML, Barker EN, Davidson AD, Tasker S, Kipar A. Inflammatory mediators in the mesenteric lymph nodes, site of a possible intermediate phase in the immune response to feline coronavirus and the pathogenesis of feline infectious peritonitis? J Comp Pathol. 2019;166:69-86. https://doi.org/10.1016/j.jcpa.2018.11.001
  29. Regan AD, Cohen RD, Whittaker GR. Activation of p38 MAPK by feline infectious peritonitis virus regulates pro-inflammatory cytokine production in primary blood-derived feline mononuclear cells. Virology. 2009;384(1):135-143. https://doi.org/10.1016/j.virol.2008.11.006
  30. 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(2-4):121-131. https://doi.org/10.1016/j.vetmic.2006.08.033
  31. Takano T, Hohdatsu T, Toda A, Tanabe M, Koyama H. TNF-alpha, produced by feline infectious peritonitis virus (FIPV)-infected macrophages, upregulates expression of type II FIPV receptor feline aminopeptidase N in feline macrophages. Virology. 2007;364(1):64-72. https://doi.org/10.1016/j.virol.2007.02.006
  32. Malbon AJ, Russo G, Burgener C, Barker EN, Meli ML, Tasker S, et al. The effect of natural feline coronavirus infection on the host immune response: a whole-transcriptome analysis of the mesenteric lymph nodes in cats with and without feline infectious peritonitis. Pathogens. 2020;9(7):524. https://doi.org/10.3390/pathogens9070524
  33. Doki T, Yabe M, Takano T, Hohdatsu T. Differential induction of type I interferon by type I and type II feline coronaviruses in vitro. Res Vet Sci. 2018;120:57-62. https://doi.org/10.1016/j.rvsc.2018.09.002
  34. Arango Duque G, Descoteaux A. Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol. 2014;5:491. https://doi.org/10.3389/fimmu.2014.00491
  35. Watanabe R, Eckstrand C, Liu H, Pedersen NC. Characterization of peritoneal cells from cats with experimentally-induced feline infectious peritonitis (FIP) using RNA-seq. Vet Res (Faisalabad). 2018;49(1):81. https://doi.org/10.1186/s13567-018-0578-y
  36. Malbon AJ, Michalopoulou E, Meli ML, Barker EN, Tasker S, Baptiste K, et al. Colony stimulating factors in early feline infectious peritonitis virus infection of monocytes and in end stage feline infectious peritonitis; a combined in vivo and in vitro approach. Pathogens. 2020;9(11):893. https://doi.org/10.3390/pathogens9110893
  37. Netea MG, Joosten LA, Latz E, Mills KH, Natoli G, Stunnenberg HG, et al. Trained immunity: a program of innate immune memory in health and disease. Science. 2016;352(6284):aaf1098. https://doi.org/10.1126/science.aaf1098
  38. Stoddart CA, Scott FW. Intrinsic resistance of feline peritoneal macrophages to coronavirus infection correlates with in vivo virulence. J Virol. 1989;63(1):436-440. https://doi.org/10.1128/jvi.63.1.436-440.1989
  39. Van Hamme E, Dewerchin HL, Cornelissen E, Nauwynck HJ. Attachment and internalization of feline infectious peritonitis virus in feline blood monocytes and Crandell feline kidney cells. J Gen Virol. 2007;88(Pt 9):2527-2532. https://doi.org/10.1099/vir.0.82991-0
  40. Dewerchin HL, Cornelissen E, Nauwynck HJ. Replication of feline coronaviruses in peripheral blood monocytes. Arch Virol. 2005;150(12):2483-2500. https://doi.org/10.1007/s00705-005-0598-6