Toll-like receptors expression in follicular cells of patients with poor ovarian response

International Journal of Fertility and Sterility

Volumn 8, Issue 2, 2014, Pages 183-192

  Taghavi, Seyed Abdolvahab ^a   Ashrafi, Mahnaz ^a,b   Mehdizadeh, Mehdi ^a,c   Karimian, Leili ^b   Joghataie, Mohammad Taghi ^a,c   Aflatoonian, Reza ^b  

^a IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b ROYAN INSTITUTE FOR REPRODUCTIVE BIOMEDICINE   (Iran)

^c IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Infertility; Innate immunity; MIF; Ovary; TLR

Indexed keywords

BETA ACTIN; CHORIONIC GONADOTROPIN; CYCLOOXYGENASE 2; GONADOTROPIN; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE MIGRATION INHIBITION FACTOR; RECOMBINANT FOLLITROPIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6;

ADULT; ARTICLE; CASE CONTROL STUDY; CLINICAL ARTICLE; CONTROLLED STUDY; DESENSITIZATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; HORMONAL REGULATION; HUMAN; INNATE IMMUNITY; INTRACYTOPLASMIC SPERM INJECTION; OOCYTE RETRIEVAL; OVARY FOLLICLE CELL; OVARY FOLLICLE FLUID; OVULATION INDUCTION; POOR OVARIAN RESPONSE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TREATMENT RESPONSE;

EID: 84904128473     PISSN: 2008076X     EISSN: 20080778     Source Type: Journal    
DOI: None     Document Type: Article

References (56)

1. Keay SD, Liversedge NH, Mathur RS, Jenkins JM. Assisted conception following poor ovarian response to gonadotrophin stimulation. Br J Obstet Gynaecol. 1997; 104(5): 521-527.
2. Veleva Z, Jarvela IY, Nuojua-Huttunen S, Martikainen H, Tapanainen JS. An initial low response predicts poor outcome in in vitro fertilization/intracytoplasmic sperm injection despite improved ovarian response in consecutive cycles. Fertil Steril. 2005; 83(5): 1384-1390.
3. Cai J, Lou HY, Dong MY, Lu XE, Zhu YM, Gao HJ, et al. Poor ovarian response to gonadotropin stimulation is associated with low expression of follicle-stimulating hormone receptor in granulosa cells. Fertil Steril. 2007; 87(6): 1350-1356.
4. Voutilainen R, Franks S, Mason HD, Martikainen H. Expression of insulin-like growth factor (IGF), IGF-binding protein, and IGF receptor messenger ribonucleic acids in normal and polycystic ovaries. J Clin Endocrinol Metab. 1996; 81(3): 1003-1008.
5. Salmassi A, Schmutzler AG, Schaefer S, Koch K, Hedderich J, Jonat W, et al. Is granulocyte colony-stimulating factor level predictive for human IVF outcome?. Hum Reprod. 2005; 20(9): 2434-2440.
6. Hovav Y, Almagor M, Benbenishti D, Margalioth EJ, Kafka I, Yaffe H. Immunity to zona pellucida in women with low response to ovarian stimulation, in unexplained infertility and after multiple IVF attempts. Hum Reprod. 1994; 9(4): 643-645.
7. Janeway CA Jr, Medzhitov R. Innate immune recognition. Annu Rev Immunol. 2002; 20: 197-216.
8. Wira CR, Fahey JV, Sentman CL, Pioli PA, Shen L. Innate and adaptive immunity in female genital tract: cellular responses and interactions. Immunol Rev. 2005; 206: 306-335.
9. Zarember KA, Godowski PJ. Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J Immunol. 2002; 168(2): 554-561.
10. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol. 2005; 17(1): 1-14.
11. Watters TM, Kenny EF, O'Neill LA. Structure, function and regulation of the Toll/IL-1 receptor adaptor proteins. Immunol Cell Biol. 2007; 85(6): 411-419.
12. Frantz S, Kelly RA, Bourcier T. Role of TLR-2 in the activation of nuclear factor kappaB by oxidative stress in cardiac myocytes. J Biol Chem. 2001; 276(7): 5197-5203.
13. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998; 282(5396): 2085-2088.
14. Taylor KR, Trowbridge JM, Rudisill JA, Termeer CC, Simon JC, Gallo RL. Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J Biol Chem. 2004; 279(17): 17079-17084.
15. Wan T, Zhou X, Chen G, An H, Chen T, Zhang W, et al. Novel heat shock protein Hsp70L1 activates dendritic cells and acts as a Th1 polarizing adjuvant. Blood. 2004; 103(5): 1747-1754.
16. Okamura Y, Watari M, Jerud ES, Young DW, Ishizaka ST, Rose J, et al. The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem. 2001; 276(13): 10229-10233.
17. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol. 2001; 167(4): 1882-1885.
18. Fazeli A, Bruce C, Anumba DO. Characterization of Toll-like receptors in the female reproductive tract in humans. Hum Reprod. 2005; 20(5): 1372-1378.
19. Aflatoonian R, Fazeli A. Toll-like receptors in female reproductive tract and their menstrual cycle dependent expression. J Reprod Immunol. 2008; 77(1): 7-13.
20. Aflatoonian R, Tuckerman E, Elliott SL, Bruce C, Aflatoonian A, Li TC, et al. Menstrual cycle-dependent changes of Toll-like receptors in endometrium. Hum Reprod. 2007; 22(2): 586-593.
21. Williams CS, Dubois RN. Prostaglandin endoperoxide synthase: why two isoforms?. Am J Physiol. 1996; 270(3 Pt 1): G393-400.
22. Narko K, Ritvos O, Ristimaki A. Induction of cyclooxygenase-2 and prostaglandin F2alpha receptor expression by interleukin-1beta in cultured human granulosa-luteal cells. Endocrinology. 1997; 138(9): 3638-3644.
23. Tokuyama O, Nakamura Y, Muso A, Honda K, Ishiko O, Ogita S. Expression and distribution of cyclooxygenase-2 in human periovulatory ovary. Int J Mol Med. 2001; 8(6): 603-606.
24. Laurincik J, Oberfranc M, Hyttel P, Grafenau P, Tomanek M, Pivko J. Characterization of the periovulatory period in superovulated heifers. Theriogenology. 1993; 39(2): 537-544.
25. Lotteau V, Teyton L, Peleraux A, Nilsson T, Karlsson L, Schmid SL, et al. Intracellular transport of class II MHC molecules directed by invariant chain. Nature. 1990; 348(6302): 600-605.
26. Aboussahoud W, Aflatoonian R, Bruce C, Elliott S, Ward J, Newton S, et al. Expression and function of Toll-like receptors in human endometrial epithelial cell lines. J Reprod Immunol. 2010; 84(1): 41-51.
27. Matzuk MM, Burns KH, Viveiros MM, Eppig JJ. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science. 2002; 296(5576): 2178-2180.
28. Herath S, Williams EJ, Lilly ST, Gilbert RO, Dobson H, Bryant CE, et al. Ovarian follicular cells have innate immune capabilities that modulate their endocrine function. Reproduction. 2007; 134(5): 683-693.
29. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robanya I, Richards JS. Induced expression of pattern recognition receptors in cumulus oocyte complexes: novel evidence for innate immune-like functions during ovulation. Mol Endocrinol. 2006; 20(12): 3228-3239.
30. Zhou M, McFarland-Mancini MM, Funk HM, Husseinzadeh N, Mounajjed T, Drew AF. Toll-like receptor expression in normal ovary and ovarian tumors. Cancer Immunol Immunother. 2009; 58(9): 1375-1385.
31. Meyer WR, Lavy G, DeCherney AH, Visintin I, Economy K, Luborsky JL. Evidence of gonadal and gonadotropin antibodies in women with a suboptimal ovarian response to exogenous gonadotropin. Obstet Gynecol. 1990; 75(5): 795-799.
32. Rezazadeh Valojerdi M, Eftekhari-Yazdi P, Karimian L, Hassani F, Movaghar B. Vitrification versus slow freezing gives excellent survival, post warming embryo morphology and pregnancy outcomes for human cleaved embryos. J Assist Reprod Genet. 2009; 26(6): 347-354.
33. 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(4): 402-408.
34. Tarlatzis BC, Zepiridis L, Grimbizis G, Bontis J. Clinical management of low ovarian response to stimulation for IVF: a systematic review. Hum Reprod Update. 2003; 9(1): 61-76.
35. Kaisho T, Akira S. Toll-like receptor function and signaling. J Allergy Clin Immunol. 2006; 117(5): 979-987.
36. Price JC, Cronin J, Sheldon IM. Toll-like receptor expression and function in the COV434 granulosa cell line. Am J Reprod Immunol. 2012; 68(3): 205-217.
37. Keay SD, Barlow R, Eley A, Masson GM, Anthony FW, Jenkins JM. The relation between immunoglobulin G antibodies to Chlamydia trachomatis and poor ovarian response to gonadotropin stimulation before in vitro fertilization. Fertil Steril. 1998; 70(2): 214-218.
38. Darville T, O'Neill JM, Andrews CW Jr, Nagarajan UM, Stahl L, Ojcius DM. Toll-like receptor-2, but not Toll-like receptor-4, is essential for development of oviduct pathology in chlamydial genital tract infection. J Immunol. 2003; 171(11): 6187-6197.
39. Salaun B, Romero P, Lebecque S. Toll-like receptors' two-edged sword: when immunity meets apoptosis. Eur J Immunol. 2007; 37(12): 3311-3318.
40. Sirois J, Sayasith K, Brown KA, Stock AE, Bouchard N, Doré M. Cyclooxygenase-2 and its role in ovulation: a 2004 account. Hum Reprod Update. 2004; 10(5): 373-385.
41. Fukata M, Chen A, Klepper A, Krishnareddy S, Vamadevan AS, Thomas LS, et al. Cox-2 is regulated by Toll-like receptor-4 (TLR4) signaling: role in proliferation and apoptosis in the intestine. Gastroenterology. 2006; 131(3): 862-877.
42. Papadimitraki ED, Bertsias GK, Boumpas DT. Toll like receptors and autoimmunity: a critical appraisal. J Autoimmun. 2007; 29(4): 310-318.
43. Pellicer A, Albert C, Mercader A, Bonilla-Musoles F, Remohi J, Simon C. The follicular and endocrine environment in women with endometriosis: local and systemic cytokine production. Fertil Steril. 1998; 70(3): 425-431.
44. Matsushima K, Morishita K, Yoshimura T, Lavu S, Kobayashi Y, Lew W, et al. Molecular cloning of a human monocyte-derived neutrophil chemotactic factor (MDNCF) and the induction of MDNCF mRNA by interleukin 1 and tumor necrosis factor. J Exp Med. 1988; 167(6): 1883-1893.
45. Zeller JM, Henig I, Radwanska E, Dmowski WP. Enhancement of human monocyte and peritoneal macrophage chemiluminescence activities in women with endometriosis. Am J Reprod Immunol Microbiol. 1987; 13(3): 78-82.
46. Agarwal R, Whang DH, Alvero AB, Visintin I, Lai Y, Segal EA, et al. Macrophage migration inhibitory factor expression in ovarian cancer. Am J Obstet Gynecol. 2007; 196(4): 348. e1-e5.
47. Xu X, Wang B, Ye C, Yao C, Lin Y, Huang X, et al. Overexpression of macrophage migration inhibitory factor induces angiogenesis in human breast cancer. Cancer Lett. 2008; 261(2): 147-157.
48. Beswick EJ, Reyes VE. Macrophage migration inhibitory factor and interleukin-8 produced by gastric epithelial cells during Helicobacter pylori exposure induce expression and activation of the epidermal growth factor receptor. Infect Immun. 2008; 76(7): 3233-3240.
49. Yanagawa Y, Onoe K. Enhanced IL-10 production by TLR4-and TLR2-primed dendritic cells upon TLR restimulation. J Immunol. 2007; 178(10): 6173-6180.
50. Punnonen J, Teisala K, Ranta H, Bennett B, Punnonen R. Increased levels of interleukin-6 and interleukin-10 in the peritoneal fluid of patients with endometriosis. Am J Obstet Gynecol. 1996; 174(5): 1522-1526.
51. Williams LM, Ricchetti G, Sarma U, Smallie T, Foxwell BM. Interleukin-10 suppression of myeloid cell activation--a continuing puzzle. Immunology. 2004; 113(3): 281-292.
52. Luborsky JL, Thiruppathi P, Rivnay B, Roussev R, Coulam C, Radwanska E. Evidence for different aetiologies of low estradiol response to FSH: age-related accelerated luteinization of follicles or presence of ovarian autoantibodies. Hum Reprod. 2002; 17(10): 2641-2649.
53. Pires ES, Parikh FR, Mande PV, Uttamchandani SA, Savkar S, Khole VV. Can anti-ovarian antibody testing be useful in an IVF-ET clinic?. J Assist Reprod Genet. 2011; 28(1): 55-64.
54. La Marca A, Brozzetti A, Sighinolfi G, Marzotti S, Volpe A, Falorni A. Primary ovarian insufficiency: autoimmune causes. Curr Opin Obstet Gynecol. 2010; 22(4): 277-282.
55. Haller K, Salumets A, Uibo R. Anti-FSH antibodies associate with poor outcome of ovarian stimulation in IVF. Reprod Biomed Online. 2008; 16(3): 350-355.
56. Simoni M, Gromoll J, Nieschlag E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr Rev. 1997; 18(6): 739-773.