Toll-like receptor signaling in hen ovarian granulosa cells is dependent on stage of follicle maturation

Reproduction

Volumn 137, Issue 6, 2009, Pages 987-996

  Woods, Dori C ^a,b   Schorey, Jeffrey S ^a   Johnson, A L ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CASPASE 8; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MESSENGER RNA; PROGESTERONE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 15; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL GROWTH INHIBITOR;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CELL FUNCTION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GRANULOSA CELL; HEN; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY CELL; OVARY CYCLE; OVARY FOLLICLE MATURATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGESTERONE SYNTHESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STEROIDOGENESIS;

ANIMALS; APOPTOSIS; CASPASE 8; CELLS, CULTURED; CHICKENS; FEMALE; FOLLICLE STIMULATING HORMONE; GRANULOSA CELLS; LIPOPOLYSACCHARIDES; LUTEINIZING HORMONE; OVARIAN FOLLICLE; PROGESTERONE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS;

GALLUS; SALMONELLA ENTERITIDIS;

EID: 68949202505     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-08-0320     Document Type: Article

References (43)

1. Asem EK & Conkright MD 1995 Role of progesterone in luteinizing hormone-induced fibronectin production and deposition by chicken granulosa cells in vitro. Comparative Biochemistry and Physiology. Part C, Pharmacology, Toxicology & Endocrinology 112 247-255.
2. Asem EK & Novero RP 1994 Stimulation of fibronectin production and deposition by chicken granulosa cells in vitro by epidermal growth factor and transforming growth factor alpha. Journal of Reproduction and Fertility 101 374-384.
3. Bahr JM & Johnson AL 1984 Regulation of the follicular hierarchy and ovulation. Journal of Experimental Zoology 232 495-500.
4. Braden CR 2006 Salmonella enterica serotype enteritidis and eggs: A national epidemic in the United States. Clinical Infectious Diseases 43 512-517.
5. Calvo FO, Wang SC & Bahr JM 1981 LH-stimulable adenylyl cyclase activity during the ovulatory cycle in granulosa cells of the three largest follicles and the postovulatory follicle of the domestic hen (Gallus domesticus). Biology of Reproduction 25 805-812.
6. Eppig JJ 1979 FSH stimulates hyaluronic acid synthesis by oocyte-cumulus cell complexes from mouse preovulatory follicles. Nature 281 483-484.
7. Fukui A, Inoue N, Matsumoto M, Nomura M, Yamada K, Matsuda Y, Toyoshima K & Seya T 2001 Molecular cloning and functional characterization of chicken toll-like receptors. A single chicken toll covers multiple molecular patterns. Journal of Biological Chemistry 276 47143-47149.
8. Gast RK & Beard CW 1990 Isolation of Salmonella enteritidis from internal organs of experimentally infected hens. Avian Diseases 34 991-993.
9. Girling JE & Hedger MP 2007 Toll-like receptors in the gonads and reproductive tract: Emerging roles in reproductive physiology and pathology. Immunology and Cell Biology 85 481-489.
10. Herath S, Williams EJ, Lilly ST, Gilbert RO, Dobson H, Bryant CE & Sheldon IM 2007 Ovarian follicular cells have innate immune capabilities that modulate their endocrine function. Reproduction 134 683-693.
11. Howard ZR, Moore RW, Zabala-Diaz IB, Landers KL, Byrd JA, Kubena LF, Nisbet DJ, Birkhold SG & Ricke SC 2005 Ovarian laying hen follicular maturation and in vitro Salmonella internalization. Veterinary Microbiology 108 95-100.
12. Iqbal M, Philbin VJ, Withanage GS, Wigley P, Beal RK, Goodchild MJ, Barrow P, McConnell I, Maskell DJ, Young J et al. 2005 Identification and functional characterization of chicken toll-like receptor 5 reveals a fundamental role in the biology of infection with Salmonella enterica serovar typhimurium. Infection and Immunity 73 2344-2350.
13. Jackson JA, Friberg AC & Bahr JM 1991 Preovulatory changes in glycosaminoglycans and collagen content in the stigma region of the follicle of the domestic hen. Biology of Reproduction 45 301-307.
14. Jammongjit M, Gill A & Hammes SR 2005 Epidermal growth factor receptor signaling is required for normal ovarian steroidogenesis and oocyte maturation. PNAS 102 16257-16262.
15. Johnson AL 2000 Granulosa cell apoptosis: Conservation of cell signaling in an avian ovarian model system. Biological Signals and Receptors 9 96-101.
16. Johnson AL & Bridgham JT 2001 Regulation of steroid acute regulatory protein and luteinizing hormone receptor messenger ribonucleic acid in hen granulosa cells. Endocrinology 142 3116-3124.
17. Johnson AL, Bridgham JT & Wagner B 1996 Characterization of a chicken luteinizing hormone receptor (cLH-R) complementary deoxyribonucleic acid, and expression of cLH-R messenger ribonucleic acid in the ovary. Biology of Reproduction 55 304-309.
18. Johnson AL, Bridgham JT, Munks M & Witty JP 1998 Characterization of the chicken interleukin-1beta converting enzyme (caspase-1) cDNA and expression of caspase-1 mRNA in the hen. Gene 219 55-62.
19. Johnson AL, Bridgham JT & Swenson JA 2001 Activation of the Akt/protein kinase B signaling pathway is associated with granulosa cell survival. Biology of Reproduction 64 1566-1574.
20. Johnson AL, Ratajczak C, Haugen MJ, Liu HK & Woods DC 2007 Tumor necrosis factor-related apoptosis inducing ligand expression and activity in hen granulosa cells. Reproduction 133 609-616.
21. Kokia E, Hurwitz A, Ben-Shlomo I, Adashi EY & Yanagishita M 1993 Receptor-mediated stimulatory effect of IL-1 beta on hyaluronic acid and proteoglycan biosynthesis by cultured rat ovarian cells: Role for heterologous cell-cell interactions. Endocrinology 133 609-616.
22. Leveque G, Forgetta V, Morroll S, Smith AL, Bumstead N, Barrow P, Loredo-Osti JC, Morgan K & Malo D 2003 Allelic variation in TLR4 is linked to susceptibility to Salmonella enterica serovar typhimurium infection in chickens. Infection and Immunity 71 1116-1124.
23. Liu Z, Shimada M & Richards JS 2008 The involvement of the toll-like receptor family in ovulation. Journal of Assisted Reproduction and Genetics 25 223-228.
24. -Ct method. Methods 25 402-408.
25. Lynn DJ, Lloyd AT & O'Farrelly C 2003 In silico identification of components of the toll-like receptor (TLR) signaling pathway in clustered chicken expressed sequence tags (ESTs). Veterinary Immunology and Immunopathology 93 177-184.
26. Medzhitov R, Preston-Hurlburt P & Janeway CA Jr 1997 A human homologue of the Drosophila toll protein signals activation of adaptive immunity. Nature 388 394-397.
27. Park JY, Su YQ, Ariga M, Law E, Jin SL & Conti M 2004 EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303 682-684.
28. Philbin V, Iqbal JM, Boyd Y, Goodchild MJ, Beal RK, Bumstead N, Young J & Smith AL 2005 Identification and characterization of a functional, alternatively spliced toll-like receptor 7 (TLR7) and genomic disruption of TLR8 in chickens. Immunology 114 507-521.
29. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robanya I & Richards JS 2006 Induced expression of pattern recognition receptors in cumulus oocyte complexes: Novel evidence for innate immune-like functions during ovulation. Molecular Endocrinology 20 3228-3239.
30. Shimada M, Yanai Y, Okazaki T, Noma N, Kawashima I, Mori T & Richards JS 2008 Hyaluronan fragments generated by sperm-secreted hyaluronidase stimulate cytokine/chemokine production via the TLR2 and TLR4 pathway in cumulus cells of ovulated COCs, which may enhance fertilization. Development 135 2001-2011.
31. Spiller S, Dreher S, Meng G, Hochrein A, Brade H, Bessler W, Wagner H, Carsten J & Kirschning J 2007 Cellular recognition of trimyristoylated peptide or enterobacterial lipopolysaccharide via both TLR2 and TLR4. Journal of Biological Chemistry 282 13190-13198.
32. Su YQ, Wigglesworth K, Pendola FL, O'Brien MJ & Eppig JJ 2002 Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinology 143 2221-2232.
33. Subdei K, Isobe N, Nishibori M & Yoshimura Y 2007 Changes in the expression of toll-like receptor mRNAs during follicular growth and in response to lipopolysaccharide in the ovarian follicles of laying hens. Journal of Reproduction and Development 53 1227-1235.
34. Takeda K & Akira S 2005 Toll-like receptors in innate immunity. International Immunology 17 1-14.
35. Takimoto T, Takahashi K, Sato K & Akiba Y 2005 Molecular cloning and functional characterizations of chicken TL1A. Developmental and Comparative Immunology 29 895-905.
36. Temperly ND, Berlin SB, Paton IR, Griffen DK & Burt DW 2008 Evolution of the chicken toll-like receptor gene family: A story of gene gain and gene loss. BMC Genomics 9 62.
37. Thiagarajan D, Saeed AM & Asem EK 1994 Mechanism of transovarian transmission of Salmonella enteritidis in laying hens. Poultry Science 73 89-98.
38. Tilly JL & Johnson AL 1988 Attenuation of hen granulosa cell steroidogenesis by a phorbol ester and 1-oleoyl-2-acetylglycerol. Biology of Reproduction 38 1-8.
39. Tilly JL, Kowalski KI & Johnson AL 1991 Stage of ovarian follicular development associated with the initiation of steroidogenic competence in avian granulosa cells. Biology of Reproduction 44 305-314.
40. Woods DC, Haugen MJ & Johnson AL 2005 Opposing actions of TGFbeta and MAP kinase signaling in undifferentiated hen granulosa cells. Biochemical and Biophysical Research Communications 336 450-457.
41. Woods DC, Haugen MJ & Johnson AL 2007 Actions of epidermal growth factor receptor/mitogen-activated protein kinase and protein kinase C signaling in granulosa cells from Gallus gallus are dependent upon stage of differentiation. Biology of Reproduction 77 61-70.
42. Zhang Z & Schluesener HJ 2006 Mammalian toll-like receptors: from endogenous ligands to tissue regeneration. Cellular and Molecular Life Sciences 63 2901-2907.
43. Ziegler-Heitbrock HW 1995 Molecular mechanism in tolerance to lipopolysaccharide. Journal of Inflammation 45 13-26.