Altered toll-like receptor 9 signaling in Mycobacterium avium subsp. paratuberculosis-infected bovine monocytes reveals potential therapeutic targets

Infection and Immunity

Volumn 81, Issue 1, 2013, Pages 226-237

  Arsenault, Ryan J ^a,b,c   Li, Yue ^b,d   Maattanen, Pekka ^a   Scruten, Erin ^a   Doig, Kimberley ^a   Potter, Andrew ^a   Griebel, Philip ^a   Kusalik, Anthony ^b   Napper, Scott ^a,b  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c SOUTHERN PLAINS AGRICULTURAL RESEARCH CENTER   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; CPG OLIGODEOXYNUCLEOTIDE; FOCAL ADHESION KINASE 2; INTERLEUKIN 10; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ARTICLE; ATYPICAL MYCOBACTERIOSIS; BACTERIAL CLEARANCE; CONTROLLED STUDY; COW; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME INHIBITION; MONOCYTE; MYCOBACTERIUM AVIUM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

EID: 84871886189     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00785-12     Document Type: Article

References (58)

1. Tiwari A, VanLeeuwen JA, McKenna SL, Keefe GP, Barkema HW. 2006. Johne's disease in Canada. Part I: clinical symptoms, pathophysiology, diagnosis, and prevalence in dairy herds. Can. Vet. J. 47:874-882.
2. McKenna SL, Keefe GP, Tiwari A, VanLeeuwen J, Barkema HW. 2006.Johne's disease in Canada. Part II: disease impacts, risk factors, and control programs for dairy producers. Canadian Veterinary Journal, 47(11)10 9-1099, 2006.
3. Chi J, VanLeeuwen JA, Weersink A, Keefe GP. 2002. Direct production losses and treatment costs from bovine viral diarrhoea virus, bovine leukosis virus, Mycobacterium avium subspecies paratuberculosis, and Neospora caninum. Prev. Vet. Med. 55:137-153.
4. Khare S, Nunes JS, Figueiredo JF, Lawhon SD, Rossetti CA, Gull T, Rice-Ficht AC, Adams LG. 2009. Early phase morphological lesions and transcriptional responses of bovine ileum infected with Mycobacterium avium subsp. paratuberculosis. Vet. Pathol. 46:717-728.
5. Momotani E, Whipple DL, Thiermann AB, Cheville NF. 1988. Role ofM cells and macrophages in the entrance of Mycobacterium paratuberculosis into domes of ileal Peyer's patches in calves. Vet. Pathol. 25:131-137.
6. Weiss DJ, Souza CD. 2008. Review paper: modulation of mononuclear phagocyte function by Mycobacterium avium subsp. paratuberculosis. Vet. Pathol. 45:829-841.
7. Woo SR, Heintz JA, Albrecht R, Barletta RG, Czuprynski CJ. 2007. Life and death in bovine monocytes: the fate of Mycobacterium avium subsp. paratuberculosis. Microb. Pathog. 43:106-113.
8. Ting LM, Kim AC, Cattamanchi A, Ernst JD. 1999. Mycobacterium tuberculosis inhibits IFN-gamma transcriptional responses without inhibiting activation of STAT1. J. Immunol. 163:3898-3906.
9. Jayachandran R, Sundaramurthy V, Combaluzier B, Mueller P, Korf H, Huygen K, Miyazaki T, Albrecht I, Massner J, Pieters J. 2007. Survival of mycobacteria in macrophages is mediated by coronin 1-dependent activation of calcineurin. Cell 130:37-50.
10. Li Q, Ding X, Thomas JJ, Harding CV, Pecora ND, Ziady AG, Shank S, Boom WH, Lancioni CL, Rojas RE. 2012. Rv2468c, a novel Mycobacterium tuberculosis protein that costimulates human CD4+T cells through VLA-5. J. Leukoc. Biol. 91:311-320.
11. Sharma AK, Naithani R, Kumar V, Sandhu SS. 2011. Iron regulation in tuberculosis research: promise and challenges. Curr. Med. Chem. 18: 1723-1731.
12. Sweet L, Singh PP, Azad AK, Rajaram MV, Schlesinger LS, Schorey JS. 2010. Mannose receptor-dependent delay in phagosome maturation by Mycobacterium avium glycopeptidolipids. Infect. Immun. 78:518-526.
13. Wong D, Bach H, Sun J, Hmama Z, Av-Gay Y. 2011. Mycobacterium tuberculosis protein tyrosine phosphatase (PtpA) excludes host vacuolar-H+-ATPase to inhibit phagosome acidification. Proc. Natl. Acad. Sci. U. S. A. 108:19371-19376.
14. Weiss DJ, Souza CD, Evanson OA, Sanders M, Rutherford M. 2008. Bovine monocyte TLR2 receptors differentially regulate the intracellular fate of Mycobacterium avium subsp. paratuberculosis and Mycobacterium avium subsp. avium. J. Leukoc. Biol. 83:48-55.
15. Finlay BB, McFadden G. 2006. Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124:767-782.
16. Waters WR, Miller JM, Palmer MV, Stabel JR, Jones DE, Koistinen KA, Steadham EM, Hamilton MJ, Davis WC, Bannantine JP. 2003. Early induction of humoral and cellular immune responses during experimental Mycobacterium avium subsp. paratuberculosis infection of calves. Infect. Immun. 71:5130-5138.
17. Arsenault RJ, Yue L, Bell K, Doig K, Potter A, Griebel P, Kusalik A, Napper S. 11 June 2012. Mycobacterium avium subsp. paratuberculosis inhibits interferon gamma-induced signaling in bovine monocytes: insights into the cellular mechanisms of Johne's disease. Infect. Immun. doi:10.1128/IAI.00406-12.
18. Krutzik SR, Modlin RL. 2004. The role of Toll-like receptors in combating mycobacteria. Semin. Immunol. 16:35-41.
19. Barton GM, Kagan JC. 2009. A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 9:535-542.
20. Mucha R, Bhide MR, Chakurkar EB, Novak M, Mikula I, Sr. 2009. Toll-like receptors TLR1, TLR2 and TLR4 gene mutations and natural resistance to Mycobacterium avium subsp. paratuberculosis infection in cattle. Vet. Immunol. Immunopathol. 128:381-388.
21. Ruiz-Larrañaga O, Manzano C, Iriondo M, Garrido JM, Molina E, Vazquez P, Juste RA, Estonba A. 2011. Genetic variation of Toll-like receptor genes and infection by Mycobacterium avium ssp. paratuberculosis in Holstein-Friesian cattle. J. Dairy Sci. 94:3635-3641.
22. Taylor DL, Zhong L, Begg DJ, de Silva K, Whittington RJ. 2008. Toll-like receptor genes are differentially expressed at the sites of infection during the progression of Johne's disease in outbred sheep. Vet. Immunol. Immunopathol. 124:132-151.
23. Kleinnijenhuis J, Oosting M, Joosten LA, Netea MG, Van Crevel R. 2011. Innate immune recognition of Mycobacterium tuberculosis. Clin. Dev. Immunol. doi:10.1155/2011/405310.
24. Fisher CA, Bhattarai EK, Osterstock JB, Dowd SE, Seabury PM, Whilock RH, Schukken YH, Schnabel RD, Taylor JF, Womack JE, Sebury CM. 2011. Evolution of the TLR gene family and member associations with Mycobacterium avium subspecies paratuberculosis infection. PLoS One 6:e27744. doi:10.1371/journal.pone.0027744.
25. Subharat S, Shu D, de Lisle GW, Buddle BM, Wedlock DN. 2012. Altered patterns of Toll-like receptor gene expression in cull cows infected with Mycobacterium avium subsp. paratuberculosis. Vet. Immunol. Immunopathol. 145:471-478.
26. Bafica A, Scanga CA, Feng CG, Leifer C, Cheever A, Sher A. 2005. TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J. Exp. Med. 202:1715-1724.
27. Noss EH, Pai RK, Sellati TJ, Radolf JD, Belisle J, Golenbock DT, Boom WH, Harding CV. 2001. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J. Immunol. 167:910-918.
28. Sanjuan MA, Milasta S, Green DR. 2009. Toll-like receptor signaling in the lysosomal pathways. Immunol. Rev. 227:203-220.
29. Krieg AM, Yi AK, Matson S, Waldschmidt TJ, Bishop GA, Teasdale R, Koretzky GA, Klinman DM. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374:546-549.
30. Zimmermann S, Egeter O, Hausmann S, Lipford GB, Rocken M, Wagner H, Heeg K. 1998. CpG oligodeoxynucleotides trigger protective and curative Th1 responses in lethal murine leishmaniasis. J. Immunol. 160:3627-3630.
31. Elkins KL, Rhinehart-Jones TR, Stibitz S, Conover JS, Klinman DM. 1999. Bacterial DNA containing CpG motifs stimulates lymphocytedependent protection of mice against lethal infection with intracellular bacteria. J. Immunol. 162:2291-2298.
32. Wang JP, Hayashi T, Datta SK, Kornbluth RS, Raz E, Guiney DG. 2005. CpG oligonucleotides partially inhibit growth of Mycobacterium tuberculosis, but not Salmonella or Listeria, in human monocyte-derived macrophages. FEMS Immunol. Med. Microbiol. 45:303-310.
33. Juffermans NP, Leemans JC, Florquin S, Verbon A, Kolk AH, Speelman P, van Deventer SJ, van der Poll T. 2002. CpG oligodeoxynucleotides enhance host defense during murine tuberculosis. Infect. Immun. 70:147-152.
34. Hayden MS, Ghosh S. 2008. Shared principles in NF-kappaB signaling. Cell 132:344-362.
35. Hoarau C, Gerard B, Lescanne E, Henry D, Francois S, Lacapere JJ, El Benna J, Dang PM, Grandchamp B, Lebranchu Y, Gougerot-Pocidalo MA, Elbim C. 2007. TLR9 activation induces normal neutrophil responses in a child with IRAK-4 deficiency: involvement of the direct PI3K pathway. J. Immunol. 179:4754-4765.
36. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, Sanjo H, Takeuchi O, Sugiyama M, Okabe M, Takeda K, Akira S. 2003. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301:640-643.
37. Hazeki K, Masuda N, Funami K, Sukenobu N, Matsumoto M, Akira S, Takeda K, Seya T, Hazeki O. 2003. Toll-like receptor-mediated tyrosine phosphorylation of paxillin via MyD88-dependent and -independent pathways. Eur. J. Immunol. 33:740-747.
38. Scanga Bafica CA, Bafica A, Feng CG, Cheever AW, Hieny S, Sher A. 2004. MyD88-deficient mice display a profound loss in resistance to Mycobacterium tuberculosis associated with partially impaired Th1 cytokine and nitric oxide synthase 2 expression. Infect. Immun. 72:2400-2404.
39. Sun D, Ding A. 2006. MyD88-mediated stabilization of interferongamma-induced cytokine and chemokine mRNA. Nat. Immunol. 7:375-381.
40. Hines ME, II, Stabel JR, Sweeney RW, Griffin F, Talaat AM, Bakker D, Benedictus G, Davis WC, de Lisle GW, Gardner IA, Juste RA, Kapur V, Koets A, Pruitt G, Whitlock RH. 2007. Experimental models for Johne'sdisease: a review and proposed international guidelines. Vet. Microbiol. 122:197-222.
41. Arsenault RJ, Jalal S, Babiuk LA, Potter A, Griebel PJ, Napper S. 2009. Kinome analysis of Toll-like receptor signaling in bovine monocytes. J.Recept. Signal Transduct. Res. 29:299-311.
42. Charavaryamath C, Fries P, Gomis S, Bell C, Doig K, le Guan L, Napper S, Griebel PJ. 2011. Mucosal changes in a long-term bovine intestinal segment model following removal of ingesta and microflora. Gut Microbes 2:134-144.
43. Booth JS, Arsenault R, Napper S, Griebel PJ, Potter AA, Babiuk LA, Mutwiri GK. 2010. TLR9 signaling failure renders Peyer's patch regulatoryv cells unresponsive to stimulation with CpG oligodeoxynucleotides. J. Innate Immun. 2:483-494.
44. Jalal S, Arsenault R, Potter AA, Babiuk LA, Griebel PJ, Napper S. 2009. Genome to kinome: species-specific peptide arrays for kinome analysis. Sci. Signal. 2:pl1. doi:10.1126/scisignal.254pl1.
45. Li Y, Arsenault RJ, Trost B, Slind J, Griebel PJ, Napper S, Kusalik A. 2012. A systematic approach for approach analysis of peptide array kinome data. Sci. Signal. 5:pl2. doi:10.1126/scisignal.2002429.
46. Lynn DJ, Winsor GL, Chan C, Richard N, Laird MR, Barsky A, Gardy JL, Roche F, Chan MTH, Shah N, Lo R, Naseer M, Que J, Yau M, Acab M, Tulpan D, Whiteside MD, Chikatamarla A, Mah B, Munzner T, Hokamp K, Hancock RE, Brinkman FS. 2008. InnateDB: facilitating systems-level analyses of the mammalian innate immune response. Mol. Syst. Biol. 4:218.
47. Waibler Z, Anzaghe M, Konur A, Akira S, Muller W, Kalinke U. 2008. Excessive CpG 1668 stimulation triggers IL-10 production by cDC that inhibits IFN-alpha responses by pDC. Eur. J. Immunol. 38:3127-3137.
48. Duramad O, Fearon KL, Chan JH, Kanzler H, Marshall JD, Coffman RL, Barrat FJ. 2003. IL-10 regulates plasmacytoid dendritic cell response to CpG-containing immunostimulatory sequences. Blood 102:4487-4492.
49. Khalifeh MS, Stabel JR. 2004. Upregulation of transforming growth factor-beta and interleukin-10 in cows with clinical Johne's disease. Vet. Immunol. Immunopathol. 99:39-46.
50. Griebel PJ, Brownlie R, Manuja A, Nichani A, Mookherjee N, Popowych Y, Mutwiri G, Hecker R, Babiuk LA. 2005. Bovine Toll-like receptor 9: a comparative analysis of molecular structure, function and expression. Vet. Immunol. Immunopathol. 108:11-16.
51. Nalubamba K, Smeed J, Gossner A, Watkins C, Dalziel R, Hopkins J. 2008. Differential expression of pattern recognition receptors in the three pathological forms of sheep paratuberculosis. Microbes Infect. 10:598-604.
52. Okigaki M, Davis C, Falasca M, Harroch S, Felsenfeld DP, Sheetz MP, Schlessinger J. 2003. Pyk2 regulates multiple signaling events crucial for acrophage morphology and migration. Proc. Natl. Acad. Sci. U. S. A. 100:10740-10745.
53. Xi CX, Xiong F, Zhou Z, Mei L, Xiong WC. 2010. PYK2 interacts with MyD88 and regulates MyD88-mediated NF-kappaB activation in macrophages. J. Leukoc. Biol. 87:415-423.
54. Weiss DJ, Evanson OA, Moritz A, Deng MQ, Abrahamsen MS. 2002. Differential responses of bovine macrophages to Mycobacterium avium subsp. paratuberculosis and Mycobacterium avium subsp. avium. Infect.Immun. 70:5556-5561.
55. Weiss DJ, Evanson OA, de Souza C, Abrahamsen MS. 2005. A critical role of interleukin-10 in the response of bovine macrophages to infection by Mycobacterium avium subsp. paratuberculosis. Am. J. Vet. Res. 66: 721-726.
56. Anand AR, Cucchiarini M, Terwilliger EF, Ganju RK. 2008. The tyrosine kinase Pyk2 mediates lipopolysaccharide-induced IL-8 expression in human endothelial cells. J. Immunol. 180:5636-5644.
57. Consonni A, Cipolla L, Guidetti G, Canobbio I, Ciraolo E, Hirsch E, Falasca M, Okigaki M, Balduini C, Torti M. 2012. Role and regulation of phosphatidylinositol 3-kinase beta in platelet integrin alpha2beta1 signaling. Blood 119:847-856.
58. Burdick AD, Ivnitski-Steele ID, Lauer FT, Burchiel SW. 2006. PYK2 mediates anti-apoptoticAKTsignaling in response to benzo[a]pyrene diol epoxide in mammary epithelial cells. Carcinogenesis 27:2331-2340.