Changes in the expression of Toll-like receptors in the chicken testis during sexual maturation and Salmonella infection

Animal Reproduction Science

Volumn 128, Issue 1-4, 2011, Pages 93-99

  Anastasiadou, M ^a   Theodoridis, A ^b   Avdi, M ^a   Michailidis, G ^a  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

Author keywords

Chicken; Salmonella; Sexual maturation; Testis; Toll like receptors

Indexed keywords

MESSENGER RNA; TOLL LIKE RECEPTOR;

AGING; ANIMAL; ANIMAL SALMONELLOSIS; ARTICLE; CHICKEN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; MALE; METABOLISM; PHYSIOLOGY; SEXUAL MATURATION; TESTIS;

AGING; ANIMALS; CHICKENS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MALE; RNA, MESSENGER; SALMONELLA INFECTIONS, ANIMAL; SEXUAL MATURATION; TESTIS; TOLL-LIKE RECEPTORS;

AVES; SALMONELLA; SALMONELLA ENTERITIDIS; VERTEBRATA;

EID: 80655146985     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2011.09.003     Document Type: Article

References (41)

1. Abasht B., Kaiser M.G., Lamont S.J. Toll-like receptor gene expression in cecum and spleen of advanced intercross line chicks infected with Salmonella enterica serovar Enteritidis. Vet. Immunol. Immunopathol. 2008, 123:314-323.
2. Akira S., Takeda K., Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2001, 2:675-680.
3. Andersen J.M., Al-Khairy D., Ingalls R.R. Innate immunity at the mucosal surface: role of Toll-like receptor 3 and Toll-like receptor 9 in cervical epithelial cell responses to microbial pathogens. Biol. Reprod. 2006, 74:824-831.
4. Bhushan S., Schuppe H.C., Tchatalbachev S., Fijaka M., Weidnerd W., Chakraborty T., Meinhardta A. Testicular innate immune defense against bacteria. Mol. Cell Endocrinol. 2009, 306:37-44.
5. Boltz D.A., Zimmerman C.R., Nakai M., Bunick D., Scherba G., Bahr J.M. Epididymal stone formation and decreased sperm production in roosters vaccinated with a killed strain of avian infectious bronchitis virus. Avian Dis. 2006, 50:594-598.
6. Boyd A., Philbin V.J., Smith A.L. Conserved and distinct aspects of the avian Toll-like receptor (TLR) system: implications for transmission and control of bird borne zoonoses. Biochem. Soc. Trans. 2007, 35:1504-1507.
7. Brownlie R., Allan B. Avian toll-like receptors. Cell Tissue Res. 2010, 343:121-130.
8. Caruso C., Buffa S., Candore G., Colonna-Romano G., Dunn-Walters D., Kipling D., Pawelec G. Mechanisms of immunosenescence. Immun. Ageing 2009, 22:6-10.
9. Com E., Bourgeon F., Evrard B., Ganz T., Colleu D., Jegou B., Pineau C. Expression of antimicrobial defensins in the male reproductive tract of rats, mice, and humans. Biol. Reprod. 2003, 68:95-104.
10. Crespo R., Shivaprasad H.L. Decrease of fertility in a broiler breeder flock due to testicular atrophy. Avian Dis. 2010, 54:142-145.
11. 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.
12. Ekawa T., Terai S., Amano F., Hanatani Y., Ohta H. Diverse pathogenicity of Salmonella enteritidis clones isolated from poultry farms in chicks and BALB/cMice. J. Poult. Sci. 2009, 46:370-376.
13. Fazeli A., Bruce C., Anumba D.O. Characterization of Toll-like receptors in the female reproductive tract in humans. Hum. Reprod. 2005, 20:1372-1378.
14. Hall S.H., Hamil K.G., French F.S. Host defense proteins of the male reproductive tract. J. Androl. 2002, 23:585-597.
15. Herath S., Williams E.J., Lilly S.T., Gilbert R.O., Dodson H., Bryant C.E., Sheldon I.M. Ovarian follicular cells have innate immune capabilities that modulate their endocrine functions. Reproduction 2007, 134:683-693.
16. Higgs R., Cormican P., Cahalane S., Allan B., Lloyd A.T., Meade K., James T., Lynn D.J., Babiuk L.A., O'Farrelly C. Induction of a novel chicken like receptor following Salmonella enterica serovar Typhimurium infection. Infect. Immun. 2006, 74:1692-1698.
17. Iqbal M., Philbin V.J., Withanage G.S., Wigley P., Beal R.K., Goodchild M.J., Barrow P., McConnell I., Maskell D.J., Young J., Bumstead N., Boyd Y., Smith A.L. Identification and functional characterization of chicken toll-like receptor 5 reveals a fundamental role in the biology of infection with Salmonella enterica serovar Typhimurium. Infect. Immun. 2005, 73:2344-2350.
18. Jackson H.J., Boltz D.A., Nakai M., Scherba G., Bunick D., Bahr J.M. Prepubertal exposure to the live attenuated avian infectious bronchitis virus induces epididymal stones in the rooster after puberty. Jpn. Poult. Sci. 2006, 43:280-285.
19. Keestra A.M., de Zoete M.R., Bouwman L.I., van Putten J.P. Chicken TLR21 is an innate CpG DNA receptor distinct from mammalian TLR9. J. Immunol. 2010, 185:460-467.
20. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC[T]) method. Methods 2001, 25:402-408.
21. Michailidis G., Theodoridis A., Avdi M. Transcriptional profiling of Toll-like receptors in chicken embryos and in the ovary during sexual maturation and in response to Salmonella enteritidis infection. Anim. Reprod. Sci. 2010, 122:294-302.
22. Michailidis G., Theodoridis A., Avdi M. Effects of sexual maturation and Salmonella infection on the expression of Toll-like receptors in the chicken vagina. Anim. Reprod. Sci. 2011, 123:234-241.
23. Monleon R., Martin M.P., Barnes H.J. Bacterial orchitis and epididymo-orchitis in broiler breeders. Avian Pathol. 2008, 37:613-617.
24. Nishimura M., Naito S. Tissue-specific mRNA expression profiles of human toll-like receptors and related genes. Biol. Pharm. Bull. 2005, 28:886-892.
25. Ozoe A., Isobe N., Yoshimura Y. Expression of Toll-like receptors (TLRs) and TLR4 response to lipopolysaccharide in hen oviduct. Vet. Immunol. Immunopathol. 2009, 127:259-268.
26. Palladino M.A., Mallonga T.A., Mishra M.S. Messenger RNA (mRNA) expression for the antimicrobial peptides b-defensin-1 and b-defensin-2 in the male rat reproductive tract: b-defensin-1 mRNA in initial segment and caput epididymidis is regulated by androgens and not bacterial lipopolysaccharides. Biol. Reprod. 2003, 68:509-515.
27. Palladino M.A., Johnson T.A., Gupta R., Chapman J.L., Ojha P. Members of the Toll-like receptor family of innate immunity pattern-recognition receptors are abundant in the male rat reproductive tract. Biol. Reprod. 2007, 76:958-964.
28. Riccioli A., Starace D., Galli R., Fuso A., Scarpa A., 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.
29. Rodrigues A., Queiroz D.B.C., Honda L., Silva E.J.R., Hall S.H., Avellar M.C.W. Activation of Toll-like receptor 4 (TLR4) by in vivo and in vitro exposure of rat epididymis to lipopolysaccharide from Escherichia coli. Biol. Reprod. 2008, 79:1135-1147.
30. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Prot. 2008, 3:1101-1108.
31. Schwarz H., Schneider K., Ohnemus A., Lavric M., Kothlow S., Bauer S., Kaspers B., Staeheli P. Chicken toll-like receptor 3 recognizes its cognate ligand when ectopically expressed in human cells. J. Interferon Cytokine Res. 2007, 27:97-101.
32. Shimada M., Hernandez-Gonzalez I., Gonzalez-Robanya I., Richards J.S. Induced expression of pattern recognition receptors (PRRs) in cumulus oocyte complexes (COCs): novel evidence for innate immune-like cells functions during ovulation. Mol. Endocrinol. 2006, 20:3228-3239.
33. Shimizu M., Watanabe Y., Isobe N., Yoshimura Y. Expression of avian β-Defensin 3, an antimicrobial peptide, by sperm in the male reproductive organs and oviduct in chickens: an immunohistochemical study. Poult. Sci. 2008, 87:2653-2659.
34. Shaughnessy R.G., Meade K.G., Cahalane S., Allan B., Reiman C., Callanan J.J., O'Farrelly C. Innate immune gene expression differentiates the early avian intestinal response between Salmonella and Campylobacter. Vet. Immunol. Immunopathol. 2009, 132:191-198.
35. Soboll G., Schaefer T.M., Wira C.R. Effect of Toll-like receptor (TLR) agonists on TLR and microbicide expression in uterine and vaginal tissues of the mouse. Am. J. Reprod. Immunol. 2006, 55:434-446.
36. 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.
37. Subedi K., Isobe N., Nishibori M., Yoshimura Y. Changes in the expression of Toll-like receptor mRNAs during follicular growth and in response to lipopolyshaccharide in the ovarian follicles of laying hens. J. Reprod. Dev. 2007, 53:1227-1235.
38. Wick M.J. Living in the danger zone: innate immunity to Salmonella. Curr. Opin. Microbiol. 2004, 7:51-57.
39. Woods D.C., Schorey J.S., Johnson A.L. Toll-like receptor signalling in hen ovarian granulosa cells is dependent on stage of follicle maturation. Reproduction 2009, 137:987-996.
40. 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.
41. Yoshimura Y., Tamura Y., Liang J.X., Okamoto T. Immunolocalization of lymphocyte subsets in the testis and epididymis of roosters. Jpn. Poult. Sci. 2004, 41:315-321.