Peptidoglycan inhibits progesterone and androstenedione production in bovine ovarian theca cells

Toxicology in Vitro

Volumn 28, Issue 5, 2014, Pages 961-967

  Magata, F ^a   Horiuchi, M ^a   Miyamoto, A ^a   Shimizu, T ^a  

^a OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

Author keywords

Androstenedione; Dairy cow; Follicles; Peptidoglycan; Progesterone; Theca cells

Indexed keywords

ANDROSTENEDIONE; BACTERIAL TOXIN; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CELL RECEPTOR; LIPOPOLYSACCHARIDE; LUTEINIZING HORMONE RECEPTOR; MESSENGER RNA; PEPTIDOGLYCAN; PEPTIDOGLYCAN RECEPTOR; PROGESTERONE; STEROID 17ALPHA MONOOXYGENASE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG; PHOSPHOPROTEIN;

ANDROSTENEDIONE PRODUCTION; ANIMAL CELL; ARTICLE; CATTLE; CELL ISOLATION; CELL MATURATION; CONTROLLED STUDY; FEMALE; FEMALE INFERTILITY; GENE EXPRESSION; HORMONE SYNTHESIS; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROGESTERONE SYNTHESIS; PROTEIN EXPRESSION; THECA CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; BOVINAE; CELL CULTURE; DRUG EFFECTS; GENETICS; METABOLISM; STAPHYLOCOCCUS AUREUS; TOXICITY;

ANDROSTENEDIONE; ANIMALS; BACTERIAL TOXINS; CATTLE; CELLS, CULTURED; FEMALE; LIPOPOLYSACCHARIDES; NOD1 SIGNALING ADAPTOR PROTEIN; NOD2 SIGNALING ADAPTOR PROTEIN; PEPTIDOGLYCAN; PHOSPHOPROTEINS; PROGESTERONE; RECEPTORS, LH; RNA, MESSENGER; STAPHYLOCOCCUS AUREUS; STEROID 17-ALPHA-HYDROXYLASE; THECA CELLS; TOLL-LIKE RECEPTOR 2;

EID: 84900313313     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2014.04.005     Document Type: Article

References (35)

1. Acosta T.J., Miyamoto A., Ozawa T., Wijayagunawardane M.P., Sato K. Local release of steroid hormones, prostaglandin E2, and endothelin-1 from bovine mature follicles in vitro: effects of luteinizing hormone, endothelin-1, and cytokines. Biol. Reprod. 1998, 59:437-443. 10.1095/biolreprod59.2.437.
2. Akira S., Takeda K. Toll-like receptor signalling. Nat. Rev. Immunol. 2004, 4:499-511. 10.1038/nri1391.
3. Allegrucci C., Hunter M.G., Webb R., Luck M.R. Interaction of bovine granulosa and theca cells in a novel serum-free co-culture system. Reproduction 2003, 126:527-538. 10.1007/s11010-008-9764-y.
4. Beutler B. Inferences, questions and possibilities in toll-like receptor signalling. Nature 2004, 430:257-263. 10.1038/nature02761.
5. Bonnett B.N., Martin S.W., Gannon V.P., Miller R.B., Etherington W.G. Endometrial biopsy in Holstein-Friesian dairy cows. III. Bacteriological analysis and correlations with histological findings. Can. J. Vet. Res. 1991, 55:168-173. (PMCID: PMC1263438).
6. Bromfield J.J., Sheldon I.M. Lipopolysaccharide initiates inflammation in bovine granulosa cells via the TLR4 pathway and perturbs oocyte meiotic progression in vitro. Endocrinology 2011, 152:5029-5040. 10.1210/en.2011-1124.
7. Chamaillard M., Hashimoto M., Horie Y., Masumoto J., Qiu S., Saab L., Ogura Y., Kawasaki A., Fukase K., Kusumoto S., Valvano M.A., Foster S.J., Mak T.W., Nunez G., Inohara N. An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat. Immunol. 2003, 4:702-707. 10.1038/ni945.
8. Dohmen M.J.W., Lohuis J.A.C.M., Huszenicza G., Nagy P., Gacs M. The relationship between bacteriological and clinical findings in cows with subacute chronic endometritis. Theriogenology 1995, 43:1379-1388. 10.1016/0093-691X(95)00123-P.
9. Dow T.L., Rogers-Nieman G., Holaskova I., Elsasser T.H., Dailey R.A. Tumor necrosis factor-alpha and acute-phase proteins in early pregnant ewes after challenge with peptidoglycan-polysaccharide. Domest. Anim. Endocrinol. 2010, 39:147-154. 10.1016/j.
10. Dziarski R. Recognition of bacterial peptidoglycan by the innate immune system. Cell. Mol. Life Sci. 2003, 60:1793-1804. 10.1007/s00018-003-3019-6.
11. Ginther O.J. Selection of the dominant follicle in cattle and horses. Anim. Reprod. Sci. 2000, 60-61:61-79. 10.1016/S0378-4320(00)00083-X.
12. Herath S., Williams E.J., Lilly S.T., Gilbert R., Dobson H., Bryant C.E., Sheldon I.M. Ovarian follicular cells have innate immune capabilities that modulate their endocrine function. Reproduction 2007, 134:683-693. 10.1530/REP-07-0229.
13. Hussain A.M., Daniel R.C., O'boyle D. Postpartum uterine flora following normal and abnormal puerperium in cows. Theriogenology 1990, 34:291-302. 10.1016/0093-691X(90)90522-U.
14. Huszenicza G., Fodor M., Gacs M., Kulcsar M., Dohmen M.J.W., Vamos M., Porkolab L., Kegl T., Bartyik J., Lohuis J.A.C.M., Janosi S., Szita G. Uterine bacteriology, resumption of cyclic ovarian activity and fertility in postpartum cows kept in large-scale dairy herds. Reprod. Domest. Anim. 1999, 34:237-245. 10.1111/j.1439-0531.1999.tb01246.x.
15. Inohara N., Ogura Y., Fontalba A., Gutierrez O., Pons F., Crespo J., Fukase K., Inamura S., Kusumoto S., Hashimoto M., Foster S.J., Moran A.P., Fernandez-Luna J.L., Nunez G. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J. Biol. Chem. 2003, 278:5509-5512. 10.1074/jbc.C200673200.
16. Kaneko K., Kawakami S. Influence of experimental intrauterine infusion of Arcanobacterium pyogenes solution on ovarian activity in cycling cows. J. Vet. Med. Sci. 2008, 70:77-83. 10.1292/jvms.70.77.
17. Kawai T., Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011, 34:637-650. 10.1016/j.immuni.2011.05.006.
18. Klinge C.M. Estrogen receptor interaction with co-activators and co-repressors. Steroids 2000, 65:227-251. 10.1016/S0039-128X(99)00107-5.
19. Leblanc S.J. Postpartum uterine disease and dairy herd reproductive performance: a review. Vet. J. 2008, 176:102-114. 10.1016/j.tvjl.2007.12.019.
20. Magoffin D.A. Ovarian theca cell. Int. J. Biochem. Cell Biol. 2005, 37:1344-1349. 10.1016/j.biocel.2005.01.016.
21. Mateus L., da Costa L.L., Bernardo F., Silva J.R. Influence of puerperal uterine infection on uterine involution and postpartum ovarian activity in dairy cows. Reprod. Domest. Anim. 2002, 37:31-35. 10.1046/j.1439-0531.2002.00317.x.
22. Mateus L., Lopes da Costa L., Diniz P., Ziecik A.J. Relationship between endotoxin and prostaglandin (PGE2 and PGFM) concentrations and ovarian function in dairy cows with puerperal endometritis. Anim. Reprod. Sci. 2003, 76:143-154. 10.1016/S0378-4320(02)00248-8).
23. Miyamoto A., Okuda K., Schweigert F.J., Schams D. Effects of basic fibroblast growth factor, transforming growth factor-beta and nerve growth factor on the secretory function of the bovine corpus luteum in vitro. J. Endocrinol. 1992, 135:103-114. 10.1677/joe.0.1350103.
24. Murasawa M., Takahashi T., Nishimoto H., Yamamoto S., Hamano S., Tetsuka M. Relationship between ovarian weight and follicular population in heifers. J. Reprod. Dev. 2005, 51:689-693. 10.1262/jrd.17014.
25. Opsomer G., Grohn Y.T., Hertl J., Coryn M., Deluyker H., de Kruif A. Risk factors for post partum ovarian dysfunction in high producing dairy cows in Belgium: a field study. Theriogenology 2000, 53:841-857. 10.1016/S0093-691X(00)00234-X.
26. Price J.C., Cronin J., Sheldon I.M. Toll-like receptor expression and function in the COV434 granulosa cell line. Am. J. Reprod. Immunol. 2012, 68:205-217. 10.1111/j.1600-0897.2011.01103.x.
27. Richards J.S. Perspective: the ovarian follicle-a perspective in 2001. Endocrinology 2001, 142:2184-2193. 10.1210/en.142.6.2184.
28. Sheldon I.M., Cronin J., Goetze L., Donofrio G., Schuberth H.J. Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biol. Reprod. 2009, 81:1025-1032. 10.1095/biolreprod.109.077370.
29. Shimizu T., Miyauchi K., Shirasuna K., Bollwein H., Magata F., Murayama C., Miyamoto A. Effects of lipopolysaccharide (LPS) and peptidoglycan (PGN) on estradiol production in bovine granulosa cells from small and large follicles. Toxicol. In Vitro 2012, 26:1134-1142. 10.1016/j.tiv.2012.06.014.
30. Stewart A.B., Inskeep E.K., Townsend E.C., Dailey R.A. Effects of gram-positive bacterial pathogens in ewes: peptidoglycan as a potential mediator of interruption of early pregnancy. Reproduction 2003, 125:295-299. 10.1530/rep.0.1250295.
31. Suzuki C., Yoshioka K., Iwamura S., Hirose H. Endotoxin induces delayed ovulation following endocrine aberration during the proestrous phase in Holstein heifers. Domest. Anim. Endocrinol. 2001, 20:267-278. 10.1016/S0739-7240(01)00098-4.
32. Takada H., Yokoyama S., Yang S.H. Enhancement of endotoxin activity by muramyldipeptide. J. Endotoxin Res. 2002, 8:337-342. 10.1179/096805102125000669.
33. Uehara, A., Yang, S., Fujimoto, Y., Fukase, K., Kusumoto, S., Shibata, K., Sugawara, S., Takada, H., 2005. Muramyldipeptide and diaminopimelic acid-containing desmuramylpeptides in combination with chemically synthesized toll-like receptor agonists synergistically induced production of interleukin-8 in a NOD2- and NOD1-dependent manner, respectively, in human monocytic cells in culture. Cell Microbiol. 7, 53-61. http://dx.doi.org/0.1111/j.1462-5822.2004.00433.x.
34. Williams E.J., Fischer D.P., Pfeiffer D.U., England G.C.W., Noakes D.E., Dobson H., Sheldon I.M. Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology 2005, 63:102-117. 10.1016/j.theriogenology.2004.03.017.
35. Williams E.J., Fischer D.P., Noakes D.E., England G.C., Rycroft A., Dobson H., Sheldon I.M. The relationship between uterine pathogen growth density and ovarian function in the postpartum dairy cow. Theriogenology 2007, 68:549-559. 10.1016/j.theriogenology.2007.04.056.