Differential activation of inflammatory pathways in testicular macrophages provides a rationale for their subdued inflammatory capacity

Journal of Immunology

Volumn 194, Issue 11, 2015, Pages 5455-5464

  Bhushan, Sudhanshu ^a   Tchatalbachev, Svetlin ^a   Lu, Yongning ^a   Fröhlich, Suada ^a   Fijak, Monika ^a   Vijayan, Vijith ^a   Chakraborty, Trinad ^a   Meinhardt, Andreas ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD163 ANTIGEN; CD68 ANTIGEN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; POLYINOSINIC POLYCYTIDYLIC ACID; STAT3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA; I KAPPA B; MITOGEN ACTIVATED PROTEIN KINASE; NF-KAPPAB INHIBITOR ALPHA; STAT3 PROTEIN, RAT; TOLL LIKE RECEPTOR;

ADULT; ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE; MACROPHAGE ACTIVATION; MALE; NONHUMAN; PERITONEUM MACROPHAGE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TESTICULAR MACROPHAGE; UBIQUITINATION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; SECRETION (PROCESS); TESTIS; WISTAR RAT;

ANIMALS; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; I-KAPPA B PROTEINS; IMMUNE TOLERANCE; IMMUNITY, INNATE; INFLAMMATION; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MACROPHAGES; MALE; MAP KINASE SIGNALING SYSTEM; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; POLY I-C; RATS; RATS, WISTAR; STAT3 TRANSCRIPTION FACTOR; TESTIS; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTOR AP-1; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITINATION;

EID: 84929649899     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401132     Document Type: Article

References (42)

1. Fijak, M., and A. Meinhardt. 2006. The testis in immune privilege. Immunol. Rev. 213: 66-81.
2. Mellor, A. L., and D. H. Munn. 2008. Creating immune privilege: active local suppression that benefits friends, but protects foes. Nat. Rev. Immunol. 8: 74-80.
3. Head, J. R., W. B. Neaves, and R. E. Billingham. 1983. Immune privilege in the testis. I. Basic parameters of allograft survival. Transplantation 36: 423-431.
4. Tung, K. S., C. Teuscher, and A. L. Meng. 1981. Autoimmunity to spermatozoa and the testis. Immunol. Rev. 55: 217-255.
5. Meinhardt, A., and M. P. Hedger. 2011. Immunological, paracrine and endocrine aspects of testicular immune privilege. Mol. Cell. Endocrinol. 335: 60-68.
6. Li, N., T. Wang, and D. Han. 2012. Structural, cellular and molecular aspects of immune privilege in the testis. Front. Immunol. 3: 152.
7. Dal Secco, V., A. Riccioli, F. Padula, E. Ziparo, and A. Filippini. 2008. Mouse Sertoli cells display phenotypical and functional traits of antigen-presenting cells in response to interferon gamma. Biol. Reprod. 78: 234-242.
8. Campese, A. F., P. Grazioli, P. de Cesaris, A. Riccioli, D. Bellavia, M. Pelullo, F. Padula, C. Noce, S. Verkhovskaia, A. Filippini, et al. 2014. Mouse Sertoli cells sustain de novo generation of regulatory T cells by triggering the notch pathway through soluble JAGGED1. Biol. Reprod. 90: 53.
9. Winnall, W. R., and M. P. Hedger. 2013. Phenotypic and functional heterogeneity of the testicular macrophage population: a new regulatory model. J. Reprod. Immunol. 97: 147-158.
10. Hutson, J. C. 2006. Physiologic interactions between macrophages and Leydig cells. Exp. Biol. Med. (Maywood) 231: 1-7.
11. Gaytan, F., C. Bellido, E. Aguilar, and N. van Rooijen. 1994. Requirement for testicular macrophages in Leydig cell proliferation and differentiation during prepubertal development in rats. J. Reprod. Fertil. 102: 393-399.
12. Hedger, M. P. 2002. Macrophages and the immune responsiveness of the testis. J. Reprod. Immunol. 57: 19-34.
13. Hedger, M. P. 1997. Testicular leukocytes: what are they doing? Rev. Reprod. 2: 38-47.
14. Winnall, W. R., J. A. Muir, and M. P. Hedger. 2011. Rat resident testicular macrophages have an alternatively activated phenotype and constitutively produce interleukin-10 in vitro. J. Leukoc. Biol. 90: 133-143.
15. Bhushan, S., H. Hossain, Y. Lu, A. Geisler, S. Tchatalbachev, Z. Mikulski, G. Schuler, J. Klug, A. Pilatz, F. Wagenlehner, et al. 2011. Uropathogenic E. coli induce different immune response in testicular and peritoneal macrophages: implications for testicular immune privilege. PLoS ONE 6: e28452.
16. Ghosh, S., and M. S. Hayden. 2008. New regulators of NF-kB in inflammation. Nat. Rev. Immunol. 8: 837-848.
17. Kawai, T., and S. Akira. 2006. TLR signaling. Cell Death Differ. 13: 816-825.
18. Palladino, M. A., T. A. Johnson, R. Gupta, J. L. Chapman, and P. Ojha. 2007. Members of the Toll-like receptor family of innate immunity pattern-recognition receptors are abundant in the male rat reproductive tract. Biol. Reprod. 76: 958-964.
19. Nishimura, M., and S. Naito. 2005. Tissue-specific mRNA expression profiles of human toll-like receptors and related genes. Biol. Pharm. Bull. 28: 886-892.
20. Bhushan, S., S. Tchatalbachev, J. Klug, M. Fijak, C. Pineau, T. Chakraborty, and A. Meinhardt. 2008. Uropathogenic Escherichia coli block MyD88-dependent and activate MyD88-independent signaling pathways in rat testicular cells. J. Immunol. 180: 5537-5547.
21. Kern, S., S. A. Robertson, V. J. Mau, and S. Maddocks. 1995. Cytokine secretion by macrophages in the rat testis. Biol. Reprod. 53: 1407-1416.
22. Wen, A. Y., K. M. Sakamoto, and L. S. Miller. 2010. The role of the transcription factor CREB in immune function. J. Immunol. 185: 6413-6419.
23. Ananieva, O., J. Darragh, C. Johansen, J. M. Carr, J. McIlrath, J. M. Park, A. Wingate, C. E. Monk, R. Toth, S. G. Santos, et al. 2008. The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat. Immunol. 9: 1028-1036.
24. World Health Organization. 2010. WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th Ed. WHO Press, Geneva, Switzerland.
25. Schuppe, H. C., A. Meinhardt, J. P. Allam, M. Bergmann, W. Weidner, and G. Haidl. 2008. Chronic orchitis: a neglected cause of male infertility? Andrologia 40: 84-91.
26. Carty, M., R. Goodbody, M. Schröder, J. Stack, P. N. Moynagh, and A. G. Bowie. 2006. The human adaptor SARM negatively regulates adaptor protein TRIFdependent Toll-like receptor signaling. Nat. Immunol. 7: 1074-1081.
27. Divanovic, S., A. Trompette, S. F. Atabani, R. Madan, D. T. Golenbock, A. Visintin, R. W. Finberg, A. Tarakhovsky, S. N. Vogel, Y. Belkaid, et al. 2005. Inhibition of TLR-4/MD-2 signaling by RP105/MD-1. J. Endotoxin Res. 11: 363-368.
28. Smythies, L. E., R. Shen, D. Bimczok, L. Novak, R. H. Clements, D. E. Eckhoff, P. Bouchard, M. D. George, W. K. Hu, S. Dandekar, and P. D. Smith. 2010. Inflammation anergy in human intestinal macrophages is due to Smad-induced IkBa expression and NF-kB inactivation. J. Biol. Chem. 285: 19593-19604.
29. Nezames, C. D., and X.W. Deng. 2012. The COP9 signalosome: its regulation of cullin-based E3 ubiquitin ligases and role in photomorphogenesis. Plant Physiol. 160: 38-46.
30. Schweitzer, K., P. M. Bozko, W. Dubiel, and M. Naumann. 2007. CSN controls NF-kB by deubiquitinylation of IkBa. EMBO J. 26: 1532-1541.
31. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4: 499-511.
32. Beutler, B. 2004. Inferences, questions and possibilities in Toll-like receptor signalling. Nature 430: 257-263.
33. Schmitt, E. G., D. Haribhai, J. B. Williams, P. Aggarwal, S. Jia, L. M. Charbonnier, K. Yan, R. Lorier, A. Turner, J. Ziegelbauer, et al. 2012. IL- 10 produced by induced regulatory T cells (iTregs) controls colitis and pathogenic ex-iTregs during immunotherapy. J. Immunol. 189: 5638-5648.
34. Kennedy, R. J., M. Hoper, K. Deodhar, P. J. Erwin, S. J. Kirk, and K. R. Gardiner. 2000. Interleukin 10-deficient colitis: new similarities to human inflammatory bowel disease. Br. J. Surg. 87: 1346-1351.
35. Biswas, S. K., and A. Mantovani. 2010. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 11: 889-896.
36. Cao, S., X. Zhang, J. P. Edwards, and D. M. Mosser. 2006. NF-kB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. J. Biol. Chem. 281: 26041-26050.
37. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3: 23-35.
38. Chawla, A. 2010. Control of macrophage activation and function by PPARs. Circ. Res. 106: 1559-1569.
39. Galli, S. J., N. Borregaard, and T. A. Wynn. 2011. Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat. Immunol. 12: 1035-1044.
40. Kern, S., and S. Maddocks. 1995. Indomethacin blocks the immunosuppressive activity of rat testicular macrophages cultured in vitro. J. Reprod. Immunol. 28: 189-201.
41. Lee, T. S., and L. Y. Chau. 2002. Heme oxygenase-1 mediates the antiinflammatory effect of interleukin-10 in mice. Nat. Med. 8: 240-246.
42. Wheeler, K., S. Tardif, C. Rival, B. Luu, E. Bui, R. Del Rio, C. Teuscher, T. Sparwasser, D. Hardy, and K. S. Tung. 2011. Regulatory T cells control tolerogenic versus autoimmune response to sperm in vasectomy. Proc. Natl. Acad. Sci. USA 108: 7511-7516.