Activation of Toll-Like Receptor 4 (TLR4) by in vivo and in vitro exposure of rat epididymis to lipopolysaccharide from Escherichia coli

Biology of Reproduction

Volumn 79, Issue 6, 2008, Pages 1135-1147

  Rodrigues, Alexandre ^a   Queiróz, Daniel B C ^a   Honda, Luciana ^a   Silva, Erick José R ^a   Hall, Susan H ^b   Avellar, Maria Christina W ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Epididymis; Gene regulation; Lipopolysaccharide; Rodent; Transcription factor

Indexed keywords

ESCHERICHIA COLI LIPOPOLYSACCHARIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PYRROLIDINE DITHIOCARBAMATE; TOLL LIKE RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPIDIDYMIS; EPITHELIUM CELL; GENE EXPRESSION REGULATION; IMMUNOREACTIVITY; INFLAMMATION; LEYDIG CELL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; ANTIGENS, CD14; BLOTTING, WESTERN; CORTICOSTERONE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPIDIDYMIS; EPITHELIAL CELLS; ESCHERICHIA COLI; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MALE; NF-KAPPA B; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TESTOSTERONE; TOLL-LIKE RECEPTOR 4;

ESCHERICHIA COLI; RATTUS; RODENTIA;

EID: 56749090905     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.069930     Document Type: Article

References (90)

1. Orgebin-Crist MC. Sperm maturation in rabbit epididymis. Nature 1967; 216:816-818.
2. Robaire B, Hermo L. Efferent ducts, epididymis and vas deferens: structure, functions and their regulation. In: Knobil E, Neill J (eds.), The Physiology of Reproduction, vol. 1. New York: Raven Press Ltd; 1988:999-1080.
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. Mikuz G, Damjanov I. Inflammation of the testis, epididymis, peritesticular membranes, and scrotum. Pathol Annu 1982; 17:101-128.
5. Purvis K, Christiansen E. Infection in the male reproductive tract. Impact, diagnosis and treatment in relation to male infertility. Int J Androl 1993; 16:1-13.
6. Somekh E, Gorenstein A, Serour F. Acute epididymitis in boys: evidence of a post-infectious etiology. J Urol 2004; 171:391-394.
7. Tracy CR, Steers WD, Costabile R. Diagnosis and management of epididymitis. Urol Clin North Am 2008; 35:101-108.
8. Li P, Chan HC, He B, So SC, Chung YW, Shang Q, Zhang YD, Zhang YL. An antimicrobial peptide gene found in the male reproductive system of rats. Science 2001; 291:1783-1785.
9. Yamaguchi Y, Nagase T, Makita R, Fukuhara S, Tomita T, Tominaga T, Kurihara H, Ouchi Y. Identification of multiple novel epididymis-specific beta-defensin isoforms in humans and mice. J Immunol 2002; 169:2516-2523.
10. Avellar MC, Honda L, Hamil KG, Yenugu S, Grossman G, Petrusz P, French FS, Hall SH. Differential expression and antibacterial activity of epididymis protein 2 isoforms in the male reproductive tract of human and rhesus monkey (Macaca mulatta). Biol Reprod 2004; 71:1453-1460.
11. O'Rand MG, Widgren EE, Sivashanmugam P, Richardson RT, Hall SH, French FS, VandeVoort CA, Ramachandra SG, Ramesh V, Jagannadha Rao A. Reversible immunocontraception in male monkeys immunized with eppin. Science 2004; 306:1189-1190.
12. Patil AA, Cai Y, Sang Y, Blecha F, Zhang G. Cross-species analysis of the mammalian beta-defensin gene family: presence of syntenic gene clusters and preferential expression in the male reproductive tract. Physiol Genomics 2005; 23:5-17.
13. Hall SH, Hamil KG, French FS. Host defense proteins of the male reproductive tract. J Androl 2002; 23:585-597.
14. Hall SH, Yenugu S, Radhakrishnan Y, Avellar MC, Petrusz P, French FS. Characterization and functions of beta defensins in the epididymis. Asian J Androl 2007; 9:453-462.
15. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004; 4:499-511.
16. Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK, Smith KD, Hood LE, Aderem A. The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci U S A 2005; 102:9577-9582.
17. Zhang D, Zhang G, Hayden MS, Greenblatt MB, Bussey C, Flavell RA, Ghosh S. A toll-like receptor that prevents infection by uropathogenic bacteria. Science 2004; 303:1522-1526.
18. Ortega-Cava CF, Ishihara S, Rumi MA, Kawashima K, Ishimura N, Kazumori H, Udagawa J, Kadowaki Y, Kinoshita Y. Strategic compartmentalization of Toll-like receptor 4 in the mouse gut. J Immunol 2003; 170:3977-3985.
19. Guillot L, Medjane S, Le-Barillec K, Balloy V, Danel C, Chignard M, Si-Tahar M. Response of human pulmonary epithelial cells to lipopolysaccharide involves Toll-like receptor 4 (TLR4)-dependent signaling pathways: evidence for an intracellular compartmentalization of TLR4. J Biol Chem 2004; 279:2712-2718.
20. Wolfs TG, Buurman WA, van Schadewijk A, de Vries B, Daemen MA, Hiemstra PS, van 't Veer C. In vivo expression of Toll-like receptor 2 and 4 by renal epithelial cells: IFN-gamma and TNF-alpha mediated upregulation during inflammation. J Immunol 2002; 168:1286-1293.
21. Aflatoonian R, Fazeli A. Toll-like receptors in female reproductive tract and their menstrual cycle dependent expression. J Reprod Immunol 2008; 77:7-13.
22. Fazeli A, Bruce C, Anumba DO. Characterization of Toll-like receptors in the female reproductive tract in humans. Hum Reprod 2005; 20:1372-1378.
23. Samuelsson P, Hang L, Wullt B, Irjala H, Svanborg C. Toll-like receptor 4 expression and cytokine responses in the human urinary tract mucosa. Infect Immun 2004; 72:3179-3186.
24. Watari M, Watari H, Nachamkin I, Strauss JF. Lipopolysaccharide induces expression of genes encoding pro-inflammatory cytokines and the elastin-degrading enzyme, cathepsin S, in human cervical smooth-muscle cells. J Soc Gynecol Investig 2000; 7:190-198.
25. Morris GE, Whyte MK, Martin GF, Jose PJ, Dower SK, Sabroe I. Agonists of toll-like receptors 2 and 4 activate airway smooth muscle via mononuclear leukocytes. Am J Respir Crit Care Med 2005; 171:814-822.
26. Yang X, Coriolan D, Murthy V, Schultz K, Golenbock DT, Beasley D. Proinflammatory phenotype of vascular smooth muscle cells: role of efficient Toll-like receptor 4 signaling. Am J Physiol Heart Circ Physiol 2005; 289:H1069-H1076.
27. Girling JE, Hedger MP. Toll-like receptors in the gonads and reproductive tract: emerging roles in reproductive physiology and pathology. Immunol Cell Biol 2007; 85:481-489.
28. Palladino MA, Johnson TA, Gupta R, Chapman JL, 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.
29. Quintar AA, Roth FD, De Paul AL, Aoki A, Maldonado CA. Toll-like receptor 4 in rat prostate: modulation by testosterone and acute bacterial infection in epithelial and stromal cells. Biol Reprod 2006; 75:664-672.
30. Bhushan S, Tchatalbachev S, Klug J, Fijak M, Pineau C, Chakraborty T, Meinhardt A. Uropathogenic Escherichia coli block MyD88-dependent and activate MyD88-independent signaling pathways in rat testicular cells. J Immunol 2008; 180:5537-5547.
31. Gatti G, Rivero V, Motrich RD, Maccioni M. Prostate epithelial cells can act as early sensors of infection by up-regulating TLR4 expression and proinflammatory mediators upon LPS stimulation. J Leukoc Biol 2006; 79:989-998.
32. Malm J, Nordahl EA, Bjartell A, Sorensen OE, Frohm B, Dentener MA, Egesten A. Lipopolysaccharide-binding protein is produced in the epididymis and associated with spermatozoa and prostasomes. J Reprod Immunol 2005; 66:33-43.
33. Chan PT, Schlegel PN. Inflammatory conditions of the male excurrent ductal system. Part I. J Androl 2002; 23:453-460.
34. Jantos C, Baumgartner W, Durchfeld B, Schiefer HG. Experimental epididymitis due to Chlamydia trachomatis in rats. Infect Immun 1992; 60:2324-2328.
35. Luzzi GA, O'Brien TS. Acute epididymitis. BJU Int 2001; 87:747-755.
36. Miller KE. Diagnosis and treatment of Chlamydia trachomatis infection. Am Fam Physician 2006; 73:1411-1416.
37. Glezer I, Munhoz CD, Kawamoto EM, Marcourakis T, Avellar MC, Scavone C. MK-801 and 7-Ni attenuate the activation of brain NF-kappa B induced by LPS. Neuropharmacology 2003; 45:1120-1129.
38. Reddy MM, Mahipal SV, Subhashini J, Reddy MC, Roy KR, Reddy GV, Reddy PR, Reddanna P. Bacterial lipopolysaccharide-induced oxidative stress in the impairment of steroidogenesis and spermatogenesis in rats. Reprod Toxicol 2006; 22:493-500.
39. Polfliet MMJ, Fabriek BO, Daniëls WP, Dijkstra CD, van den Berg TK. The rat macrophage scavenger receptor CD163: expression, regulation and role in inflammatory mediator production. Immunobiology 2006; 211:419-425.
40. Cabrini DA, Campos MM, Tratsk KS, Merino VF, Silva JA Jr, Souza GE, Avellar MC, Pesquero JB, Calixto JB. Molecular and pharmacological evidence for modulation of kinin B(1) receptor expression by endogenous glucocorticoids hormones in rats. Br J Pharmacol 2001; 132:567-577.
41. Naumann M, Wessler S, Bartsch C, Wieland B, Meyer TF. Neisseria gonorrhoeae epithelial cell interaction leads to the activation of the transcription factors nuclear factor kappaB and activator protein 1 and the induction of inflammatory cytokines. J Exp Med 1997; 186:247-258.
42. Picarelli ZP, Hyppolito N, Valle JR. Synergistic effect of 5-hydroxytryptamine on the response of rats's seminal vesicles to adrenaline and noradrenaline. Arch Int Pharmacodyn Ther 1962; 138:354-363.
43. Avellar MC, Gregory CW, Power SG, French FS. Androgen-dependent protein interactions within an intron 1 regulatory region of the 20-kDa protein gene. J Biol Chem 1997; 272:17623-17631.
44. Queiróz DBC, Silva AM, Gutierrez-Ospina G, Porto CS, Grossman G, Petrusz P, Avellar MCW. Cells positive for microtubule-associated protein 1B (MAP 1B) are present along rat and human efferent ductules and epididymis. Cell Tissue Res 2006; 325:125-133.
45. Laflamme N, Rivest S. Effects of systemic immunogenic insults and circulating proinflammatory cytokines on the transcription of the inhibitory factor kappaB alpha within specific cellular populations of the rat brain. J Neurochem 1999; 73:309-321.
46. Quan N, He L, Lai W, Shen T, Herkenham M. Induction of IkappaBalpha mRNA expression in the brain by glucocorticoids: a negative feedback mechanism for immune-to-brain signaling. J Neurosci 2000; 20:6473-6477.
47. Adamopoulos DA, Lawrence DM, Vassilopoulos P, Contoyiannis PA, Swyer GI. Pituitary-testicular interrelationships in mumps orchitis and other viral infections. Br Med J 1978; 1:1177-1180.
48. Buch JP, Havlovec SK. Variation in sperm penetration assay related to viral illness. Fertil Steril 1991; 55:844-846.
49. Cutolo M, Balleari E, Giusti M, Monachesi M, Accardo S. Sex hormone status of male patients with rheumatoid arthritis: evidence of low serum concentrations of testosterone at baseline and after human chorionic gonadotropin stimulation. Arthritis Rheum 1988; 31:1314-1317.
50. O'Bryan MK, Schlatt S, Phillips DJ, de Kretser DM, Hedger MP. Bacterial lipopolysaccharide-induced inflammation compromises testicular function at multiple levels in vivo. Endocrinology 2000; 141:238-246.
51. Stenzel-Poore M, Vale WW, Rivier C. Relationship between antigen-induced immune stimulation and activation of the hypothalamic-pituitary-adrenal axis in the rat. Endocrinology 1993; 132:1313-1318.
52. Wolff SM. Biological effects of bacterial endotoxins in man. J Infect Dis 1973; 128:259-264.
53. Ghosh S, May MJ, Kopp EB. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 1998; 16:225-260.
54. Ganchi PA, Sun SC, Greene WC, Ballard DW. A novel NF-kappa B complex containing p65 homodimers: implications for transcriptional control at the level of subunit dimerization. Mol Cell Biol 1993; 13:7826-7835.
55. Ledebur HC, Parks TP. Transcriptional regulation of the intercellular adhesion molecule-1 gene by inflammatory cytokines in human endothelial cells. Essential roles of a variant NF-kappa B site and p65 homodimers. J Biol Chem 1995; 270:933-943.
56. Sandersen C, Bureau F, Turlej R, Fievez L, Dogne S, Kirschvink N, Lekeux P. p65 Homodimer activity in distal airway cells determines lung dysfunction in equine heaves. Vet Immunol Immunopathol 2001; 80:315-326.
57. Schulte R, Grassl GA, Preger S, Fessele S, Jacobi CA, Schaller M, Nelson PJ, Autenrieth IB. Yersinia enterocolitica invasin protein triggers IL-8 production in epithelial cells via activation of Rel p65-p65 homodimers. FASEB J 2000; 14:1471-1484.
58. Matsukura S, Stellato C, Plitt JR, Bickel C, Miura K, Georas SN, Casolaro V, Schleimer RP. Activation of eotaxin gene transcription by NF-kappa B and STAT6 in human airway epithelial cells. J Immunol 1999; 163:6876-6883.
59. Marchant A, Duchow J, Delville JP, Goldman M. Lipopolysaccharide induces up-regulation of CD14 molecule on monocytes in human whole blood. Eur J Immunol 1992; 22:1663-1665.
60. Matsuura K, Ishida T, Setoguchi M, Higuchi Y, Akizuki S, Yamamoto S. Upregulation of mouse CD14 expression in Kupffer cells by lipopolysaccharide. J Exp Med 1994; 179:1671-1676.
61. Han SJ, Ko HM, Choi JH, Seo KH, Lee HS, Choi EK, Choi IW, Lee HK, Im SY. Molecular mechanisms for lipopolysaccharide-induced biphasic activation of nuclear factor-kappa B (NF-kappa B). J Biol Chem 2002; 277:44715-44721.
62. Gukovsky I, Gukovskaya AS, Blinman TA, Zaninovic V, Pandol SJ. Early NF-kappaB activation is associated with hormone-induced pancreatitis. Am J Physiol 1998; 275:G1402-G1414.
63. Yurochko AD, Kowalik TF, Huong SM, Huang ES. Human cytomegalovirus upregulates NF-kappa B activity by transactivating the NF-kappa B p105/p50 and p65 promoters. J Virol 1995; 69:5391-5400.
64. Haddad JJ, Lauterbach R, Saadé NE, Safieh-Garabedian B, Land SC. Alpha-melanocyte-related tripeptide, Lys-d-Pro-Val, ameliorates endotoxin-induced nuclear factor kappaB translocation and activation: evidence for involvement of an interleukin-1beta193-195 receptor antagonism in the alveolar epithelium. Biochem J 2001; 355:29-38.
65. McIntyre TM, Modur V, Prescott SM, Zimmerman GA. Molecular mechanisms of early inflammation. Thromb Haemost 1997; 78:302-305.
66. Steinhorn DM, Cerra FB. Comparative effects of lipopolysaccharide on newborn versus adult rat hepatocyte and nonparenchymal cell cocultures. Crit Care Med 1997; 25:121-127.
67. Okuma Y, O'Connor AE, Muir JA, Stanton PG, de Kretser DM, Hedger MP. Regulation of activin A and inhibin B secretion by inflammatory mediators in adult rat Sertoli cell cultures. J Endocrinol 2005; 187:125-134.
68. Paterson HM, Murphy TJ, Purcell EJ, Shelley O, Kriynovich SJ, Lien E, Mannick JA, Lederer JA. Injury primes the innate immune system for enhanced Toll-like receptor reactivity. J Immunol 2003; 171:1473-1483.
69. Schaefer TM, Desouza K, Fahey JV, Beagley KW, Wira CR. Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells. Immunology 2004; 112:428-436.
70. Hornef MW, Normark BH, Vandewalle A, Normark S. Intracellular recognition of lipopolysaccharide by toll-like receptor 4 in intestinal epithelial cells. J Exp Med 2003; 198:1225-1235.
71. MacRedmond R, Greene C, Taggart CC, McElvaney N, O'Neill S. Respiratory epithelial cells require Toll-like receptor 4 for induction of human beta-defensin 2 by lipopolysaccharide. Respir Res 2005; 6:116.
72. Uehara A, Sugawara S, Takada H. Priming of human oral epithelial cells by interferon-gamma to secrete cytokines in response to lipopolysaccharides, lipoteichoic acids and peptidoglycans. J Med Microbiol 2002; 51:626-634.
73. Latz E, Visintin A, Lien E, Fitzgerald KA, Monks BG, Kurt-Jones EA, Golenbock DT, Espevik T. Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction. J Biol Chem 2002; 277:47834-47843.
74. Hooper P, Smythe E, Richards RC, Howard CV, Lynch RV, Lewis-Jones DI. Total number of immunocompetent cells in the normal rat epididymis and after vasectomy. J Reprod Fertil 1995; 104:193-198.
75. Nashan D, Jantos C, Ahlers D, Bergmann M, Schiefer HG, Sorg C, Nieschlag E. Immuno-competent cells in the murine epididymis following infection with Escherichia coli. Int J Androl 1993; 16:47-52.
76. Wang YF, Holstein AF. Intraepithelial lymphocytes and macrophages in the human epididymis. Cell Tissue Res 1983; 233:517-521.
77. Hedger MP. Macrophages and the immune responsiveness of the testis. J Reprod Immunol 2002; 57:19-34.
78. Serre V, Robaire B. Distribution of immune cells in the epididymis of the aging Brown Norway rat is segment-specific and related to the luminal content. Biol Reprod 1999; 61:705-714.
79. Yeung CH, Nashan D, Sorg C, Oberpenning F, Schulze H, Nieschlag E, Cooper TG. Basal cells of the human epididymis - antigenic and ultrastructural similarities to tissue-fixed macrophages. Biol Reprod 1994; 50:917-926.
80. Sawamoto O, Yamate J, Kuwamura M, Kotani T, Kurisu K. Macrophage populations in L-cysteine-induced rat sperm granulomas. J Comp Pathol 2003; 129:308-312.
81. Shehu-Xhilaga M, Kent S, Batten J, Ellis S, van der Meulen J, O'Bryan M, Cameron PU, Lewin SR, Hedger MP. The testis and epididymis are productively infected by SIV and SHIV in juvenile macaques during the post-acute stage of infection. Retrovirology 2007; 4:7.
82. Rival C, Lustig L, Iosub R, Guazzone VA, Schneider E, Meinhardt A, Fijak M. Identification of a dendritic cell population in normal testis and in chronically inflamed testis of rats with autoimmune orchitis. Cell Tissue Res 2006; 324:311-318.
83. Hedger MP, Meinhardt A. Cytokines and the immune-testicular axis. J Reprod Immunol 2003; 58:1-26.
84. Dijkstra CD, Döpp EA, Joling P, Kraal G. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 1985; 54:589-599.
85. Bañuls MP, Alvarez A, Ferrero I, Zapata A, Ardavin C. Cell-surface marker analysis of rat thymic dendritic cells. Immunology 1993; 79:298-304.
86. Meinhardt A, Bacher M, Metz C, Bucala R, Wreford N, Lan H, Atkins R, Hedger M. Local regulation of macrophage subsets in the adult rat testis: examination of the roles of the seminiferous tubules, testosterone, and macrophage-migration inhibitory factor. Biol Reprod 1998; 59:371-378.
87. Wang J, Wreford NG, Lan HY, Atkins R, Hedger MP. Leukocyte populations of the adult rat testis following removal of the Leydig cells by treatment with ethane dimethane sulfonate and subcutaneous testosterone implants. Biol Reprod 1994; 51:551-561.
88. O'Bryan MK, Gerdprasert O, Nikolic-Paterson DJ, Meinhardt A, Muir JA, Foulds LM, Phillips DJ, de Kretser DM, Hedger MP. Cytokine profiles in the testes of rats treated with lipopolysaccharide reveal localized suppression of inflammatory responses. Am J Physiol Regul Integr Comp Physiol 2005; 288:R1744-R1755.
89. Gerdprasert O, O'Bryan MK, Muir JA, Caldwell AM, Schlatt S, de Kretser DM, Hedger MP. The response of testicular leukocytes to lipopolysaccharide- induced inflammation: further evidence for heterogeneity of the testicular macrophage population. Cell Tissue Res 2002; 308:277-285.
90. Fan J, Kapus A, Marsden PA, Li YH, Oreopoulos G, Marshall JC, Frantz S, Kelly RA, Medzhitov R, Rotstein OD. Regulation of Toll-like receptor 4 expression in the lung following hemorrhagic shock and lipopolysaccharide. J Immunol 2002; 168:5252-5259.