P204-initiated innate antiviral response in mouse leydig cells

Biology of Reproduction

Volumn 91, Issue 1, 2014, Pages

  Zhu, Weiwei ^a   Liu, Peng ^a   Yu, Lili ^a   Chen, Qiaoyuan ^a   Liu, Zhenghui ^a   Yan, Keqin ^a   Lee, Will M ^b   Cheng, C Yan ^c   Han, Daishu ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c POPULATION COUNCIL   (United States)

Author keywords

antiviral response; herpes simplex virus; Leydig cell; p204

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; ANTIVIRUS AGENT; GAMMA GLUTAMYLTRANSFERASE; HSV 60; HSV60; IMMUNOMODULATING AGENT; INTERFERON; MX GLUTAMYL TRANSPEPTIDASE 1; NUCLEIC ACID BINDING PROTEIN; P204 PROTEIN; SMALL INTERFERING RNA; TESTOSTERONE; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN; IFI16 PROTEIN, MOUSE; MEMBRANE PROTEIN; MPYS PROTEIN, MOUSE; NUCLEAR PROTEIN; PHOSPHOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIVIRAL ACTIVITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG TARGETING; GENE EXPRESSION; IMMUNE RESPONSE GENE; IMMUNOMODULATION; INNATE IMMUNITY; INTERFERON STIMULATING GENE 15; LEYDIG CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SIGNALING ADAPTOR STIMULATOR OF INTERFERON GENE; STEROIDOGENESIS; TESTIS FUNCTION; TESTOSTERONE SYNTHESIS; TREATMENT RESPONSE; ANIMAL; GENETICS; MALE; METABOLISM;

2',5'-OLIGOADENYLATE SYNTHETASE; ANIMALS; GAMMA-GLUTAMYLTRANSFERASE; IMMUNITY, INNATE; LEYDIG CELLS; MALE; MEMBRANE PROTEINS; MICE; NUCLEAR PROTEINS; PHOSPHOPROTEINS; RNA, SMALL INTERFERING;

EID: 84906225335     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.119396     Document Type: Article

References (51)

1. Hedger MP. Immune privilege of the testis: meaning, mechanisms, and manifestations. In: Stein-Streilein J (ed.), Infection, Immune Homeostasis and Immune Privilege. Basel: Springer; 2012:31. Birkhäuser Advances in Infectious Diseases series.
2. 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.
3. Dejucq N, Jegou B. Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev 2001; 65: 208-231.
4. Kumar H, Kawai T, Akira S. Pathogen recognition by the innate immune system. Int Rev Immunol 2011; 30:16-34.
5. 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.
6. Barbalat R, Ewald SE, Mouchess ML, Barton GM. Nucleic acid recognition by the innate immune system. Annu Rev Immunol 2011; 29:185-214.
7. Hedger MP. Toll-like receptors and signalling in spermatogenesis and testicular responses to inflammation: a perspective. J Reprod Immunol 2011; 88:130-141.
8. Riccioli A, Starace D, Galli R, Fuso A, Scarpa S, Palombi F, De Cesaris P, Ziparo E, Filippini A. Sertoli cells initiate testicular innate immune responses through TLR activation. J Immunol 2006; 177:7122-7130.
9. 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.
10. Starace D, Galli R, Paone A, De Cesaris P, Filippini A, Ziparo E, Riccioli A. Toll-like receptor 3 activation induces antiviral immune responses in mouse Sertoli cells. Biol Reprod 2008; 79:766-775.
11. 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.
12. Shang T, Zhang X, Wang T, Sun B, Deng T, Han D. Toll-like receptorinitiated testicular innate immune responses in mouse Leydig cells. Endocrinology 2011; 152:2827-2836.
13. Wang T, Zhang X, Chen Q, Deng T, Zhang Y, Li N, Shang T, Chen Y, Han D. Toll-like receptor 3-initiated antiviral responses in mouse male germ cells in vitro. Biol Reprod 2012; 86:e106.
14. Chen Q, Zhu W, Liu Z, Yan K, Zhao S, Han D. Toll-like receptor 11-initiated innate immune response in male mouse germ cells. Biol Reprod 2014; 90:e38.
15. Zhu W, Chen Q, Yan K, Liu Z, Li N, Zhang X, Yu L, Chen Y, Han D. RIG-I-like receptors mediate innate antiviral response in mouse testis. Mol Endocrinol 2013; 27:1455-1467.
16. Takaoka A, Wang Z, Choi MK, Yanai H, Negishi H, Ban T, Lu Y, Miyagishi M, Kodama T, Honda K, Ohba Y, Taniguchi T. DAI (DLM-1/ ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007; 448:501-505.
17. Chiu YH, Macmillan JB, Chen ZJ. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 2009; 138:576-591.
18. Sun L, Wu J, Du F, Chen X, Chen ZJ. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013; 339:786-791.
19. Veeranki S, Choubey D. Interferon-inducible p200-family protein IFI16, an innate immune sensor for cytosolic and nuclear double-stranded DNA: regulation of subcellular localization. Mol Immunol 2012; 49:567-571.
20. Wang Z, Choi MK, Ban T, Yanai H, Negishi H, Lu Y, Tamura T, Takaoka A, Nishikura K, Taniguchi T. Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules. Proc Natl Acad Sci U S A 2008; 105:5477-5482.
21. Samuel CE. Antiviral actions of interferons. Clin Microbiol Rev 2001; 14: 778-809.
22. Schoggins JW, Rice CM. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 2011; 1:519-525.
23. Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nat Rev Immunol 2008; 8:559-568.
24. 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.
25. Winnall WR, Muir JA, Hedger MP. Rat resident testicular macrophages have an alternatively activated phenotype and constitutively produce interleukin-10 in vitro. J Leukoc Biol 2011; 90:133-143.
26. Gribencha SV, Bragina EE, Abdumalikov RA, Bocharova EN, Kurilo LF. Detection of type 2 herpes simplex virus in cells of spermatogenic epithelium in infected testes of guinea pigs. Bull Exp Biol Med 2007; 144: 73-76.
27. Wang H, Xiong W, Chen Y, Ma Q, Ma J, Ge Y, Han D. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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; 25:402-408.
33. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, Sharma S, Sirois CM, Jin T, Latz E, Xiao TS, Fitzgerald KA, Paludan SR, et al. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 2010; 11: 997-1004.
34. Haidl G, Allam JP, Schuppe HC. Chronic epididymitis: impact on semen parameters and therapeutic options. Andrologia 2008; 40:92-96.
35. Ludwig M. Diagnosis and therapy of acute prostatitis, epididymitis and orchitis. Andrologia 2008; 40:76-80.
36. Jalal H, Bahadur G, Knowles W, Jin L, Brink N. Mumps epididymoorchitis with prolonged detection of virus in semen and the development of anti-sperm antibodies. J Med Virol 2004; 73:147-150.
37. Kapranos N, Petrakou E, Anastasiadou C, Kotronias D. Detection of herpes simplex virus, cytomegalovirus, and Epstein-Barr virus in the semen of men attending an infertility clinic. Fertil Steril 2003; 79(suppl 3): 1566-1570.
38. Lai YM, Lee JF, Huang HY, Soong YK, Yang FP, Pao CC. The effect of human papillomavirus infection on sperm cell motility. Fertil Steril 1997; 67:1152-1155.
39. Erles K, Rohde V, Thaele M, Roth S, Edler L, Schlehofer JR. DNA of adeno-associated virus (AAV) in testicular tissue and in abnormal semen samples. Hum Reprod 2001; 16:2333-2337.
40. Keating SE, Baran M, Bowie AG. Cytosolic DNA sensors regulating type I interferon induction. Trends Immunol 2011; 32:574-581.
41. Barber GN. STING-dependent cytosolic DNA sensing pathways. Trends Immunol 2014; 35:88-93.
42. Li T, Diner BA, Chen J, Cristea IM. Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16. Proc Natl Acad Sci U S A 2012; 109:10558-10563.
43. Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 2008; 89:1-47.
44. Katze MG, He Y, Gale M Jr. Viruses and interferon: a fight for supremacy. Nat Rev Immunol 2002; 2:675-687.
45. Kawai T, Akira S. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int Immunol 2009; 21:317-337.
46. Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 2009; 22:240-273.
47. Bornstein SR, Rutkowski H, Vrezas I. Cytokines and steroidogenesis. Mol Cell Endocrinol 2004; 215:135-141.
48. Hong CY, Park JH, Ahn RS, Im SY, Choi HS, Soh J, Mellon SH, Lee K. Molecular mechanism of suppression of testicular steroidogenesis by proinflammatory cytokine tumor necrosis factor alpha. Mol Cell Biol 2004; 24:2593-2604.
49. Theas MS, Rival C, Jarazo-Dietrich S, Jacobo P, Guazzone VA, Lustig L. Tumour necrosis factor-alpha released by testicular macrophages induces apoptosis of germ cells in autoimmune orchitis. Hum Reprod 2008; 23: 1865-1872.
50. Ochsendorf FR. Sexually transmitted infections: impact on male fertility. Andrologia 2008; 40:72-75.
51. Davis NF, McGuire BB, Mahon JA, Smyth AE, O'Malley KJ, Fitzpatrick JM. The increasing incidence of mumps orchitis: a comprehensive review. BJU Int 2010; 105:1060-1065.