RIG-I-like receptors mediate innate antiviral response in mouse testis

Molecular Endocrinology

Volumn 27, Issue 9, 2013, Pages 1455-1467

  Zhu, Weiwei ^a   Chen, Qiaoyuan ^a   Yan, Keqin ^a   Liu, Zhenghui ^a   Li, Nan ^a   Zhang, Xiaoyan ^a   Yu, Lili ^a   Chen, Yongmei ^a   Han, Daishu ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; ALPHA INTERFERON; BETA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 6; MELANOMA DIFFERENTIATION ASSOCIATED PROTEIN 5; MESSENGER RNA; POLYINOSINIC POLYCYTIDYLIC ACID; RETINOIC ACID INDUCIBLE GENE I LIKE RECEPTOR; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GERM CELL; IMMUNOFLUORESCENCE; INNATE IMMUNITY; LEYDIG CELL; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPERMATOCYTE; UPREGULATION; WESTERN BLOTTING;

ANIMALS; CYTOKINES; DEAD-BOX RNA HELICASES; IMMUNITY, INNATE; INTERFERON REGULATORY FACTOR-3; LEYDIG CELLS; MALE; MICE; MICE, INBRED C57BL; NF-KAPPA B; POLY I-C; SPERMATOZOA; TESTIS;

EID: 84883216872     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2013-1075     Document Type: Article

References (51)

1. Schuppe HC, Meinhardt A, Allam JP, Bergmann M, Weidner W, Haidl G. Chronic orchitis: a neglected cause of male infertility? Andrologia. 2008;40:84-91.
2. Ludwig M. Diagnosis and therapy of acute prostatitis, epididymitis and orchitis. Andrologia. 2008;40:76-80.
3. Xu X. [The possible role of sperm in family HBV infection]. Zhonghua Liu Xing Bing Xue Za Zhi. 1992;13:337-339.
4. Baccetti B, Benedetto A, Burrini AG, et al. HIV-particles in spermatozoa of patients with AIDS and their transfer into the oocyte. J Cell Biol. 1994;127:903-914.
5. Dejucq N, Jégou B. Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev. 2001;65:208-231.
6. Katze MG, He Y, Gale M Jr. Viruses and interferon: a fight for supremacy. Nat Rev Immunol. 2002;2:675-687.
7. Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nat Rev Immunol. 2008;8:559-568.
8. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature. 2007;449:819-826.
9. Dejucq N, Dugast I, Ruffault A, van der Meide PH, Jégou B. Interferon-α and-β expression in the rat testis. Endocrinology. 1995; 136:4925-4931.
10. Dejucq N, Chousterman S, Jégou B. The testicular antiviral defense system: localization, expression, and regulation of 2-5 oligoadenylate synthetase, double-stranded RNA-activated protein kinase, and Mx proteins in the rat seminiferous tubule. J Cell Biol. 1997; 139:865-873.
11. Dejucq N, Lienard MO, Guillaume E, Dorval I, Jégou B. Expression of interferons-α and-β in testicular interstitial tissue and spermatogonia of the rat. Endocrinology. 1998;139:3081-3087.
12. Melaine N, Liénard MO, Guillaume E, Ruffault A, Dejucq-Rainsford N, Jégou B. Production of the antiviral proteins 2-5oligoadenylate synthetase, PKR and Mx in interstitial cells and spermatogonia. J Reprod Immunol. 2003;59:53-60.
13. Le Tortorec A, Denis H, Satie AP, et al. Antiviral responses of human Leydig cells to mumps virus infection or poly I:C stimulation. Hum Reprod. 2008;23:2095-2103.
14. Kumar H, Kawai T, Akira S. Pathogen recognition by the innate immune system. Int Rev Immunol. 2011;30:16-34.
15. Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science. 2010;327:291-295.
16. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol. 2005;17:1-14.
17. Barbalat R, Ewald SE, Mouchess ML, Barton GM. Nucleic acid recognition by the innate immune system. Annu Rev Immunol. 2011;29:185-214.
18. Matsumoto M, Oshiumi H, Seya T. Antiviral responses induced by the TLR3 pathway. Rev Med Virol. 2011;21:67-77.
19. Hedger MP. Toll-like receptors and signalling in spermatogenesis and testicular responses to inflammation-a perspective. J Reprod Immunol. 2011;88:130-141.
20. Bhushan S, Schuppe HC, Tchatalbachev S, et al. Testicular innate immune defense against bacteria. Mol Cell Endocrinol. 2009;306: 37-44.
21. Bhushan S, Tchatalbachev S, Klug J, et al. Uropathogenic Esche-richia coli block MyD88-dependent and activate MyD88-independent signaling pathways in rat testicular cells. J Immunol. 2008; 180:5537-5547.
22. Riccioli A, Starace D, Galli R, et al. Sertoli cells initiate testicular innate immune responses through TLR activation. J Immunol. 2006;177:7122-7130.
23. Wu H, Wang H, Xiong W, Chen S, Tang H, Han D. Expression patterns and functions of toll-like receptors in mouse Sertoli cells. Endocrinology. 2008;149:4402-4412.
24. Starace D, Galli R, Paone A, et al. Toll-like receptor 3 activation induces antiviral immune responses in mouse Sertoli cells. Biol Reprod. 2008;79:766-775.
25. Winnall WR, Muir JA, Hedger MP. Differential responses of epithelial Sertoli cells of the rat testis to Toll-like receptor 2 and 4 ligands: implications for studies of testicular inflammation using bacterial lipopolysaccharides. Innate Immun. 2011;17:123-136.
26. Shang T, Zhang X, Wang T, Sun B, Deng T, Han D. Toll-like receptor-initiated testicular innate immune responses in mouse Leydig cells. Endocrinology. 2011;152:2827-2836.
27. Wang T, Zhang X, Chen Q, et al. Toll-like receptor 3-initiated antiviral responses in mouse male germ cells in vitro. Biol Reprod. 2012;86:106.
28. Loo YM, Gale M Jr. Immune signaling by RIG-I-like receptors. Immunity. 2011;34:680-692.
29. Ireton RC, Gale M Jr. RIG-I like receptors in antiviral immunity and therapeutic applications. Viruses. 2011;3:906-919.
30. Meylan E, Tschopp J. Toll-like receptors and RNA helicases: two parallel ways to trigger antiviral responses. Mol Cell. 2006;22:561-569.
31. Wang H, Wang H, Xiong W, et al. Evaluation on the phagocytosis of apoptotic spermatogenic cells by Sertoli cells in vitro through detecting lipid droplet formation by Oil Red O staining. Reproduction. 2006;132:485-492.
32. Klinefelter GR, Hall PF, Ewing LL. Effect of luteinizing hormone deprivation in situ on steroidogenesis of rat Leydig cells purified by a multistep procedure. Biol Reprod. 1987;36:769-783.
33. Sharpe RM, McKinnell C, Kivlin C, Fisher JS. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction. 2003;125:769-784.
34. Yu Z, Guo R, Ge Y, et al. Gene expression profiles in different stages of mouse spermatogenic cells during spermatogenesis. Biol Reprod. 2003;69:37-47.
35. Chong MM, Metcalf D, Jamieson E, Alexander WS, Kay TW. Suppressor of cytokine signaling-1 in T cells and macrophages is critical for preventing lethal inflammation. Blood. 2005;106:1668-1675.
36. Hume DA, Perry VH, Gordon S. The mononuclear phagocyte system of the mouse defined by immunohistochemical localisation of antigen F4/80: macrophages associated with epithelia. Anat Rec. 1984;210:503-512.
37. Yoneyama M, Fujita T. RNA recognition and signal transduction by RIG-I-like receptors. Immunol Rev. 2009;227:54-65.
38. Staeheli P. Interferon-induced proteins and the antiviral state. Adv Virus Res. 1990;38:147-200.
39. Csata S, KulcsárG. Virus-host studies in human seminal and mouse testicular cells. Acta Chir Hung. 1991;32:83-90.
40. Lang ZW. [Distribution of hepatitis B virus in testicle tissue in patients with hepatitis B infection.] Zhonghua Yi Xue Za Zhi. 1993;73:329-331.
41. Liu FH, Tian GS, Fu XX. [Detection of plus and minus strand hepatitis C virus RNA in peripheral blood mononuclear cells and spermatid.] Zhonghua Yi Xue Za Zhi. 1994;74:284-286.
42. Nuovo GJ, Becker J, Simsir A, Margiotta M, Khalife G, Shevchuk M. HIV-1 nucleic acids localize to the spermatogonia and their progeny. A study by polymerase chain reaction in situ hybridization. Am J Pathol. 1994;144:1142-1148.
43. Bryniarski K, Szczepanik M, Maresz K, Ptak M, Ptak W. Subpopulations of mouse testicular macrophages and their immunoregulatory function. Am J Reprod Immunol. 2004;52:27-35.
44. Li N, Wang T, Han D. Structural, cellular and molecular aspects of immune privilege in the testis. Front Immunol. 2012;3:152.
45. Thompson MR, Kaminski JJ, Kurt-Jones EA, Fitzgerald KA. Pattern recognition receptors and the innate immune response to viral infection. Viruses. 2011;3:920-940.
46. Sun B, Qi N, Shang T, Wu H, Deng T, Han D. Sertoli cell-initiated testicular innate immune response through toll-like receptor-3 activation is negatively regulated by Tyro3, Axl, and mer receptors. Endocrinology. 2010;151:2886-2897.
47. Kawai T, Akira S. Toll-like receptor and RIG-I-like receptor signaling. Ann NY Acad Sci. 2008;1143:1-20.
48. Bruns AM, Horvath CM. Activation of RIG-I-like receptor signal transduction. Crit Rev Biochem Mol Biol. 2012;47:194-206.
49. Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol. 2008;89:1-47.
50. Hedger MP. Macrophages and the immune responsiveness of the testis. J Reprod Immunol. 2002;57:19-34.
51. Bhushan S, Hossain H, Lu Y, et al. A Uropathogenic E. coli induce different immune response in testicular and peritoneal macrophages: implications for testicular immune privilege. PLoS One. 2011;6:e28452.