Skip to main content
SpringerLink
Log in

Ovulation: A Molecular View

  • Chapter
  • First Online:
Reproductive Endocrinology and Infertility

Abstract

Ovulation is a complex process that after initiation by LH involves cascades of several pathways that interact within cell types and between cell compartments. Major functions of these pathways are to promote permeability and increased blood flow, to accelerate ECM remodelling leading to degradation of the follicular apex and restructuring of the cystic follicle into a solid corpus luteum, to induce expansion within the cumulus granulosa cells, to modify steroidogenesis within granulosa and theca cells toward secretion of progesterone, and to maintain a positive intra-follicular pressure so the follicular wall eventually ruptures and that the cumulus-enclosed oocyte is expelled.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Lofman CO, Janson PO, Kallfelt BJ, Ahren K, LeMaire WJ (1982) The study of ovulation in the isolated perfused rabbit ovary. II. Photographic and cinematographic observation. Biol Reprod 26(3):467-473

    Article  PubMed  CAS  Google Scholar 

  2. Lofman CO, Brannstrom M, Holmes PV, Janson PO (1989) Ovulation in the isolated perfused rat ovary as documented by intravital microscopy. Steroids 54(5):481-490

    Article  PubMed  CAS  Google Scholar 

  3. Dahm-Kahler P, Lofman C, Fujii R, Axelsson M, Janson PO, Brannstrom M (2006) An intravital microscopy method permitting continuous long-term observations of ovulation in vivo in the rabbit. Hum Reprod 21(3):624-631

    Article  PubMed  Google Scholar 

  4. Shimada M, Nishibori M, Isobe N, Kawano N, Terada T (2003) Luteinizing hormone receptor formation in cumulus cells surrounding porcine oocytes and its role during meiotic maturation of porcine oocytes. Biol Reprod 68(4):1142-1149

    Article  PubMed  CAS  Google Scholar 

  5. Hillensjo T, Magnusson C, Svensson U, Thelander H (1981) Effect of luteinizing hormone and follicle-stimulating hormone on progesterone synthesis by cultured rat cumulus cells. Endocrinology 108(5):1920-1924

    Article  PubMed  CAS  Google Scholar 

  6. Tsafriri A, Lieberman ME, Koch Y et al (1976) Capacity of immunologically purified FSH to stimulate cyclic AMP accumulation and steroidogenesis in Graafian follicles and to induce ovum maturation and ovulation in the rat. Endocrinology 98(3):655-661

    Article  PubMed  CAS  Google Scholar 

  7. Sogn JH, Curry TE Jr, Brannstrom M et al (1987) Inhibition of follicle-stimulating hormone-induced ovulation by indomethacin in the perfused rat ovary. Biol Reprod 36(3):536-542

    Article  PubMed  CAS  Google Scholar 

  8. Peng XR, Hsueh AJ, LaPolt PS, Bjersing L, Ny T (1991) Localization of luteinizing hormone receptor messenger ribonucleic acid expression in ovarian cell types during follicle development and ovulation. Endocrinology 129(6):3200-3207

    Article  PubMed  CAS  Google Scholar 

  9. Rao CV, Lei ZM (2002) Consequences of targeted inactivation of LH receptors. Mol Cell Endocrinol 187(1-2):57-67

    Article  PubMed  CAS  Google Scholar 

  10. Couse JF, Yates MM, Deroo BJ, Korach KS (2005) Estrogen receptor-beta is critical to granulosa cell differentiation and the ovulatory response to gonadotropins. Endocrinology 146(8):3247-3262

    Article  PubMed  CAS  Google Scholar 

  11. Russell DL, Doyle KM, Gonzales-Robayna I, Pipaon C, Richards JS (2003) Egr-1 induction in rat granulosa cells by follicle-stimulating hormone and luteinizing hormone: combinatorial regulation by transcription factors cyclic adenosine 3′, 5′-monophosphate regulatory element binding protein, serum response factor, sp1, and early growth response factor-1. Mol Endocrinol 17(4):520-533

    Article  PubMed  CAS  Google Scholar 

  12. Maizels ET, Mukherjee A, Sithanandam G et al (2001) Developmental regulation of mitogen-activated protein kinase-activated kinases-2 and -3 (MAPKAPK-2/-3) in vivo during corpus luteum formation in the rat. Mol Endocrinol 15(5):716-733

    Article  PubMed  CAS  Google Scholar 

  13. Das S, Maizels ET, DeManno D, St Clair E, Adam SA, Hunzicker-Dunn M (1996) A stimulatory role of cyclic adenosine 3′, 5′-monophosphate in follicle-stimulating hormone-activated mitogen-activated protein kinase signaling pathway in rat ovarian granulosa cells. Endocrinology 137(3):967-974

    Article  PubMed  CAS  Google Scholar 

  14. Davis JS, West LA, Farese RV (1984) Effects of luteinizing hormone on phosphoinositide metabolism in rat granulosa cells. J Biol Chem 259(24):15028-15034

    PubMed  CAS  Google Scholar 

  15. Gudermann T, Birnbaumer M, Birnbaumer L (1992) Evidence for dual coupling of the murine luteinizing hormone receptor to adenylyl cyclase and phosphoinositide breakdown and Ca2+ mobilization. Studies with the cloned murine luteinizing hormone receptor expressed in L cells. J Biol Chem 267(7):4479-4488

    PubMed  CAS  Google Scholar 

  16. Tanaka N, Espey LL, Kawano T, Okamura H (1991) Comparison of inhibitory actions of indomethacin and epostane on ovulation in rats. Am J Physiol 260(2 Pt 1):E170-E174

    PubMed  CAS  Google Scholar 

  17. Andersen AG, Als-Nielsen B, Hornnes PJ, Franch Andersen L (1995) Time interval from human chorionic gonadotrophin (HCG) injection to follicular rupture. Hum Reprod 10(12):3202-3205

    PubMed  CAS  Google Scholar 

  18. Stouffer RL, Zelinski-Wooten MB (2004) Overriding follicle selection in controlled ovarian stimulation protocols: quality vs. quantity. Reprod Biol Endocrinol 2:32

    Article  PubMed  Google Scholar 

  19. Sharma SC, Richards JS (2000) Regulation of AP1 (Jun/Fos) factor expression and activation in ovarian granulosa cells. Relation of JunD and Fra2 to terminal differentiation. J Biol Chem 275(43):33718-33728

    Article  PubMed  CAS  Google Scholar 

  20. Tullet JM, Pocock V, Steel JH, White R, Milligan S, Parker MG (2005) Multiple signaling defects in the absence of RIP140 impair both cumulus expansion and follicle rupture. Endocrinology 146(9):4127-4137

    Article  PubMed  CAS  Google Scholar 

  21. White R, Leonardsson G, Rosewell I, Ann Jacobs M, Milligan S, Parker M (2000) The nuclear receptor co-repressor nrip1 (RIP140) is essential for female fertility. Nat Med 6(12):1368-1374

    Article  PubMed  CAS  Google Scholar 

  22. Pall M, Hellberg P, Brannstrom M et al (1997) The transcription factor C/EBP-beta and its role in ovarian function; evidence for direct involvement in the ovulatory process. EMBO J 16(17):5273-5279

    Article  PubMed  CAS  Google Scholar 

  23. Jo M, Curry TE Jr (2006) Luteinizing hormone-induced RUNX1 regulates the expression of genes in granulosa cells of rat periovulatory follicles. Mol Endocrinol 20(9):2156-2172

    Article  PubMed  CAS  Google Scholar 

  24. Sriraman V, Sharma SC, Richards JS (2003) Transactivation of the progesterone receptor gene in granulosa cells: evidence that Sp1/Sp3 binding sites in the proximal promoter play a key role in luteinizing hormone inducibility. Mol Endocrinol 17(3):436-449

    Article  PubMed  CAS  Google Scholar 

  25. Doyle KM, Russell DL, Sriraman V, Richards JS (2004) Coordinate transcription of the ADAMTS-1 gene by luteinizing hormone and progesterone receptor. Mol Endocrinol 18(10):2463-2478

    Article  PubMed  CAS  Google Scholar 

  26. Natraj U, Richards JS (1993) Hormonal regulation, localization, and functional activity of the progesterone receptor in granulosa cells of rat preovulatory follicles. Endocrinology 133(2):761-769

    Article  PubMed  CAS  Google Scholar 

  27. Conneely OM, Mulac-Jericevic B, Lydon JP, De Mayo FJ (2001) Reproductive functions of the progesterone receptor isoforms: lessons from knock-out mice. Mol Cell Endocrinol 179(1-2):97-103

    Article  PubMed  CAS  Google Scholar 

  28. Duffy DM, Wells TR, Haluska GJ, Stouffer RL (1997) The ratio of progesterone receptor isoforms changes in the monkey corpus luteum during the luteal phase of the menstrual cycle. Biol Reprod 57(4):693-699

    Article  PubMed  CAS  Google Scholar 

  29. Stouffer RL (2003) Progesterone as a mediator of gonadotrophin action in the corpus luteum: beyond steroidogenesis. Hum Reprod Update 9(2):99-117

    Article  PubMed  CAS  Google Scholar 

  30. Mori T, Suzuki A, Nishimura T, Kambegawa A (1977) Inhibition of ovulation in immature rats by anti-progesterone antiserum. J Endocrinol 73(1):185-186

    Article  PubMed  CAS  Google Scholar 

  31. Brannstrom M, Janson PO (1989) Progesterone is a mediator in the ovulatory process of the in vitro perfused rat ovary. Biol Reprod 40:1170-1178

    Article  PubMed  CAS  Google Scholar 

  32. Brannstrom M (1993) Inhibitory effect of mifepristone (RU 486) on ovulation in the isolated perfused rat ovary. Contraception 48(4):393-402

    Article  PubMed  CAS  Google Scholar 

  33. Lydon JP, DeMayo FJ, Funk CR et al (1995) Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9(18):2266-2278

    Article  PubMed  CAS  Google Scholar 

  34. Mulac-Jericevic B, Conneely OM (2004) Reproductive tissue selective actions of progesterone receptors. Reproduction 128(2):139-146

    Article  PubMed  CAS  Google Scholar 

  35. Robker RL, Russell DL, Espey LL, Lydon JP, O'Malley BW, Richards JS (2000) Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases. Proc Natl Acad Sci USA 97(9):4689-4694

    Article  PubMed  CAS  Google Scholar 

  36. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, Richards JS (2006) Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol 20(6):1352-1365

    Article  PubMed  CAS  Google Scholar 

  37. Hibbert ML, Stouffer RL, Wolf DP, Zelinski-Wooten MB (1996) Midcycle administration of a progesterone synthesis inhibitor prevents ovulation in primates. Proc Natl Acad Sci USA 93(5):1897-1901

    Article  PubMed  CAS  Google Scholar 

  38. Tjugum J, Dennefors B, Norstrom A (1984) Influence of progesterone, androstenedione and oestradiol-17 beta on the incorporation of [3H]proline in the human follicular wall. Acta Endocrinol (Copenh) 105(4):552-557

    CAS  Google Scholar 

  39. Armstrong DT (1981) Prostaglandins and follicular functions. J Reprod Fertil 62(1):283-291

    Article  PubMed  CAS  Google Scholar 

  40. Morris JK, Richards JS (1995) Luteinizing hormone induces prostaglandin endoperoxide synthase-2 and luteinization in vitro by A-kinase and C-kinase pathways. Endocrinology 136(4):1549-1558

    Article  PubMed  CAS  Google Scholar 

  41. Bauminger A, Lindner HR (1975) Periovulatory changes in ovarian prostaglandin formation and their hormonal control in the rat. Prostaglandins 9(5):737-751

    Article  PubMed  CAS  Google Scholar 

  42. LeMaire WJ, Leidner R, Marsh JM (1975) Pre and post ovulatory changes in the concentration of prostaglandins in rat graafian follicles. Prostaglandins 9(2):221-229

    Article  PubMed  CAS  Google Scholar 

  43. Mikuni M, Pall M, Peterson CM et al (1998) The selective prostaglandin endoperoxide synthase-2 inhibitor, NS-398, reduces prostaglandin production and ovulation in vivo and in vitro in the rat. Biol Reprod 59(5):1077-1083

    Article  PubMed  CAS  Google Scholar 

  44. Davis BJ, Lennard DE, Lee CA et al (1999) Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1beta. Endocrinology 140(6):2685-2695

    Article  PubMed  CAS  Google Scholar 

  45. Langenbach R, Morham SG, Tiano HF et al (1995) Prostaglandin synthase 1 gene disruption in mice reduces arachidonic acid-induced inflammation and indomethacin-induced gastric ulceration. Cell 83(3):483-492

    Article  PubMed  CAS  Google Scholar 

  46. Segi E, Haraguchi K, Sugimoto Y et al (2003) Expression of messenger RNA for prostaglandin E receptor subtypes EP4/EP2 and cyclooxygenase isozymes in mouse periovulatory follicles and oviducts during superovulation. Biol Reprod 68(3):804-811

    Article  PubMed  CAS  Google Scholar 

  47. Takahashi T, Morrow JD, Wang H, Dey SK (2006) Cyclooxygenase-2-derived prostaglandin E(2) directs oocyte maturation by differentially influencing multiple signaling pathways. J Biol Chem 281(48):37117-37129

    Article  PubMed  CAS  Google Scholar 

  48. Duffy DM, Stouffer RL (2001) The ovulatory gonadotrophin surge stimulates cyclooxygenase expression and prostaglandin production by the monkey follicle. Mol Hum Reprod 7(8):731-739

    Article  PubMed  CAS  Google Scholar 

  49. Duffy DM, Seachord CL, Dozier BL (2005) An ovulatory gonadotropin stimulus increases cytosolic phospholipase A2 expression and activity in granulosa cells of primate periovulatory follicles. J Clin Endocrinol Metab 90(10):5858-5865

    Article  PubMed  CAS  Google Scholar 

  50. Killick S, Elstein M (1987) Pharmacologic production of luteinized unruptured follicles by prostaglandin synthetase inhibitors. Fertil Steril 47(5):773-777

    PubMed  CAS  Google Scholar 

  51. Pall M, Friden BE, Brannstrom M (2001) Induction of delayed follicular rupture in the human by the selective COX-2 inhibitor rofecoxib: a randomized double-blind study. Hum Reprod 16(7):1323-1328

    Article  PubMed  CAS  Google Scholar 

  52. Chandras C, Ragoobir J, Barrett GE et al (2004) Roles for prostaglandins in the steroidogenic response of human granulosa cells to high-density lipoproteins. Mol Cell Endocrinol 222(1-2):1-8

    Article  PubMed  CAS  Google Scholar 

  53. Harris TE, Squires PE, Michael AE, Bernal AL, Abayasekara DR (2001) Human granulosa-lutein cells express functional EP1 and EP2 prostaglandin receptors. Biochem Biophys Res Commun 285(5):1089-1094

    Article  PubMed  CAS  Google Scholar 

  54. Higuchi Y, Yoshimura T, Tanaka N, Ogino H, Sumiyama M, Kawakami S (1995) Different time-course production of peptidic and nonpeptidic leukotrienes and prostaglandins E2 and F2 alpha in the ovary during ovulation in gonadotropin-primed immature rats. Prostaglandins 49(3):131-140

    Article  PubMed  CAS  Google Scholar 

  55. Mikuni M, Yoshida M, Hellberg P et al (1998) The lipoxygenase inhibitor, nordihydroguaiaretic acid, inhibits ovulation and reduces leukotriene and prostaglandin levels in the rat ovary. Biol Reprod 58(5):1211-1216

    Article  PubMed  CAS  Google Scholar 

  56. Matousek M, Mitsube K, Mikuni M, Brannstrom M (2001) Inhibition of ovulation in the rat by a leukotriene B(4) receptor antagonist. Mol Hum Reprod 7(1):35-42

    Article  PubMed  CAS  Google Scholar 

  57. Janson PO (1975) Effects of the luteinizing hormone on blood flow in the follicular rabbit ovary, as measured by radioactive microspheres. Acta Endocrinol (Copenh) 79(1):122-133

    CAS  Google Scholar 

  58. Brannstrom M, Zackrisson U, Hagstrom HG et al (1998) Preovulatory changes of blood flow in different regions of the human follicle. Fertil Steril 69(3):435-442

    Article  PubMed  CAS  Google Scholar 

  59. Abisogun AO, Daphna-Iken D, Reich R, Kranzfelder D, Tsafriri A (1988) Modulatory role of eicosanoids in vascular changes during the preovulatory period in the rat. Biol Reprod 38(4):756-762

    Article  PubMed  CAS  Google Scholar 

  60. Gerdes U, Gafvels M, Bergh A, Cajander S (1992) Localized increases in ovarian vascular permeability and leucocyte accumulation after induced ovulation in rabbits. J Reprod Fertil 95(2):539-550

    Article  PubMed  CAS  Google Scholar 

  61. Murakami T, Ikebuchi Y, Ohtsuka A, Kikuta A, Taguchi T, Ohtani O (1988) The blood vascular wreath of rat ovarian follicle, with special reference to its changes in ovulation and luteinization: a scanning electron microscopic study of corrosion casts. Arch Histol Cytol 51(4):299-313

    Article  PubMed  CAS  Google Scholar 

  62. Mitsube K, Mikuni M, Matousek M, Brannstrom M (1999) Effects of a nitric oxide donor and nitric oxide synthase inhibitors on luteinizing hormone-induced ovulation in the ex-vivo perfused rat ovary. Hum Reprod 14(10):2537-2543

    Article  PubMed  CAS  Google Scholar 

  63. Mitsube K, Zackrisson U, Brannstrom M (2002) Nitric oxide regulates ovarian blood flow in the rat during the periovulatory period. Hum Reprod 17(10):2509-2516

    Article  PubMed  CAS  Google Scholar 

  64. Mitsube K, Mikuni M, Matousek M, Zackrisson U, Brannstrom M (2003) Role of the angiotensin II system in regulation of ovulation and blood flow in the rat ovary. Reproduction 125(3):425-435

    Article  PubMed  CAS  Google Scholar 

  65. Xu F, Hazzard TM, Evans A, Charnock-Jones S, Smith S, Stouffer RL (2005) Intraovarian actions of anti-angiogenic agents disrupt periovulatory events during the menstrual cycle in monkeys. Contraception 71(4):239-248

    Article  PubMed  CAS  Google Scholar 

  66. Ko C, Gieske MC, Al-Alem L et al (2006) Endothelin-2 in ovarian follicle rupture. Endocrinology 147(4):1770-1779

    Article  PubMed  CAS  Google Scholar 

  67. 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(5658):682-684

    Article  PubMed  CAS  Google Scholar 

  68. Ashkenazi H, Cao X, Motola S, Popliker M, Conti M, Tsafriri A (2005) Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 146(1):77-84

    Article  PubMed  CAS  Google Scholar 

  69. Freimann S, Ben-Ami I, Dantes A, Ron-El R, Amsterdam A (2004) EGF-like factor epiregulin and amphiregulin expression is regulated by gonadotropins/cAMP in human ovarian follicular cells. Biochem Biophys Res Commun 324(2):829-834

    Article  PubMed  CAS  Google Scholar 

  70. Lind AK, Weijdegard B, Dahm-Kahler P, Molne J, Sundfeldt K, Brannstrom M (2006) Collagens in the human ovary and their changes in the perifollicular stroma during ovulation. Acta Obstet Gynecol Scand 85(12):1476-1484

    Article  PubMed  Google Scholar 

  71. Matousek M, Carati C, Gannon B, Brannstrom M (2001) Novel method for intrafollicular pressure measurements in the rat ovary: increased intrafollicular pressure after hCG stimulation. Reproduction 121(2):307-314

    Article  PubMed  CAS  Google Scholar 

  72. Ny T, Wahlberg P, Brandstrom IJ (2002) Matrix remodeling in the ovary: regulation and functional role of the plasminogen activator and matrix metalloproteinase systems. Mol Cell Endocrinol 187(1-2):29-38

    Article  PubMed  CAS  Google Scholar 

  73. Smith MF, Ricke WA, Bakke LJ, Dow MP, Smith GW (2002) Ovarian tissue remodeling: role of matrix metalloproteinases and their inhibitors. Mol Cell Endocrinol 191(1):45-56

    Article  PubMed  CAS  Google Scholar 

  74. Curry TE Jr, Osteen KG (2003) The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 24(4):428-465

    Article  PubMed  CAS  Google Scholar 

  75. Goldman S, Shalev E (2003) The role of the matrix metalloproteinases in human endometrial and ovarian cycles. Eur J Obstet Gynecol Reprod Biol 111(2):109-121

    Article  PubMed  CAS  Google Scholar 

  76. Curry TE Jr, Smith MF (2006) Impact of extracellular matrix remodeling on ovulation and the folliculo-luteal transition. Semin Reprod Med 24(4):228-241

    Article  PubMed  CAS  Google Scholar 

  77. Liu YX (2004) Plasminogen activator/plasminogen activator inhibitors in ovarian physiology. Front Biosci 9:3356-3373

    Article  PubMed  CAS  Google Scholar 

  78. Sternlicht MD, Werb Z (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17:463-516

    Article  PubMed  CAS  Google Scholar 

  79. Somerville RP, Oblander SA, Apte SS (2003) Matrix metalloproteinases: old dogs with new tricks. Genome Biol 4(6):216

    Article  PubMed  Google Scholar 

  80. Birkedal-Hansen H, Moore WG, Bodden MK et al (1993) Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 4(2):197-250

    PubMed  CAS  Google Scholar 

  81. Visse R, Nagase H (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92(8):827-839

    Article  PubMed  CAS  Google Scholar 

  82. Brew K, Dinakarpandian D, Nagase H (2000) Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 1477(1-2):267-283

    PubMed  CAS  Google Scholar 

  83. Gomez DE, Alonso DF, Yoshiji H, Thorgeirsson UP (1997) Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol 74(2):111-122

    PubMed  CAS  Google Scholar 

  84. Lambert E, Dasse E, Haye B, Petitfrere E (2004) TIMPs as multifacial proteins. Crit Rev Oncol Hematol 49(3):187-198

    Article  PubMed  Google Scholar 

  85. Woessner JF, Nagase H (2000) Matrix metalloproteinases and TIMPs. Oxford University Press, New York

    Google Scholar 

  86. Reich R, Tsafriri A, Mechanic GL (1985) The involvement of collagenolysis in ovulation in the rat. Endocrinology 116(2):522-527

    Article  PubMed  CAS  Google Scholar 

  87. Brannstrom M, Woessner JF Jr, Koos RD, Sear CH, LeMaire WJ (1988) Inhibitors of mammalian tissue collagenase and metalloproteinases suppress ovulation in the perfused rat ovary. Endocrinology 122(5):1715-1721

    Article  PubMed  CAS  Google Scholar 

  88. Curry TE, Komar CM, Burns PD, Nothnick WB (2000) Periovulatory changes in ovarian metalloproteinases and tissue inhibitors of metalloproteinases (TIMPS) following indomethacin treatment. In: Adashi EY, Serono Symposia USA (eds) Ovulation: evolving scientific and clinical concepts. Springer, New York, pp 265-276

    Google Scholar 

  89. Hagglund AC, Ny A, Leonardsson G, Ny T (1999) Regulation and localization of matrix metalloproteinases and tissue inhibitors of metalloproteinases in the mouse ovary during gonadotropin-induced ovulation. Endocrinology 140(9):4351-4358

    Article  PubMed  CAS  Google Scholar 

  90. Vu TH, Shipley JM, Bergers G et al (1998) MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93(3):411-422

    Article  PubMed  CAS  Google Scholar 

  91. Hurwitz A, Dushnik M, Solomon H et al (1993) Cytokine-mediated regulation of rat ovarian function: interleukin-1 stimulates the accumulation of a 92-kilodalton gelatinase. Endocrinology 132(6):2709-2714

    Article  PubMed  CAS  Google Scholar 

  92. Hurwitz A, Finci-Yeheskel Z, Dushnik M et al (1995) Interleukin-1-mediated regulation of plasminogen activation in pregnant mare serum gonadotropin-primed rat granulosa cells is independent of prostaglandin production. J Soc Gynecol Investig 2(5):691-699

    Article  PubMed  CAS  Google Scholar 

  93. Curry TE Jr, Song L, Wheeler SE (2001) Cellular localization of gelatinases and tissue inhibitors of metalloproteinases during follicular growth, ovulation, and early luteal formation in the rat. Biol Reprod 65(3):855-865

    Article  PubMed  CAS  Google Scholar 

  94. Inderdeo DS, Edwards DR, Han VK, Khokha R (1996) Temporal and spatial expression of tissue inhibitors of metalloproteinases during the natural ovulatory cycle of the mouse. Biol Reprod 55(3):498-508

    Article  PubMed  CAS  Google Scholar 

  95. Mann JS, Kindy MS, Edwards DR, Curry TE Jr (1991) Hormonal regulation of matrix metalloproteinase inhibitors in rat granulosa cells and ovaries. Endocrinology 128(4):1825-1832

    Article  PubMed  CAS  Google Scholar 

  96. Chun SY, Popliker M, Reich R, Tsafriri A (1992) Localization of preovulatory expression of plasminogen activator inhibitor type-1 and tissue inhibitor of metalloproteinase type-1 mRNAs in the rat ovary. Biol Reprod 47(2):245-253

    Article  PubMed  CAS  Google Scholar 

  97. Curry TE Jr, Komar CM, Burns PD, Nothnick WB (2000) Periovulatory changes in ovarian metalloproteinases and tissue inhibitors of metalloproteinases (TIMPS) following indomethacin treatment. In: Adashi EY (ed) Ovulation: evolving scientific and clinical concepts. Springer-Verlag, New York

    Google Scholar 

  98. Nothnick WB, Soloway P, Curry TE Jr (1997) Assessment of the role of tissue inhibitor of metalloproteinase-1 (TIMP-1) during the periovulatory period in female mice lacking a functional TIMP-1 gene. Biol Reprod 56(5):1181-1188

    Article  PubMed  CAS  Google Scholar 

  99. Boujrad N, Ogwuegbu SO, Garnier M, Lee CH, Martin BM, Papadopoulos V (1995) Identification of a stimulator of steroid hormone synthesis isolated from testis. Science 268(5217):1609-1612

    Article  PubMed  CAS  Google Scholar 

  100. Nothnick WB (2003) Tissue inhibitor of metalloproteinase-1 (TIMP-1) deficient mice display reduced serum progesterone levels during corpus luteum development. Endocrinology 144(1):5-8

    Article  PubMed  CAS  Google Scholar 

  101. Strongin AY, Collier I, Bannikov G, Marmer BL, Grant GA, Goldberg GI (1995) Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem 270(10):5331-5338

    Article  PubMed  CAS  Google Scholar 

  102. Jo M, Thomas LE, Wheeler SE, Curry TE Jr (2004) Membrane type 1-matrix metalloproteinase (MMP)-associated MMP-2 activation increases in the rat ovary in response to an ovulatory dose of human chorionic gonadotropin. Biol Reprod 70(4):1024-1032

    Article  PubMed  CAS  Google Scholar 

  103. Chaffin CL, Stouffer RL (1999) Expression of matrix metalloproteinases and their tissue inhibitor messenger ribonucleic acids in macaque periovulatory granulosa cells: time course and steroid regulation. Biol Reprod 61(1):14-21

    Article  PubMed  CAS  Google Scholar 

  104. Young KA, Hennebold JD, Stouffer RL (2002) Dynamic expression of mRNAs and proteins for matrix metalloproteinases and their tissue inhibitors in the primate corpus luteum during the menstrual cycle. Mol Hum Reprod 8(9):833-840

    Article  PubMed  CAS  Google Scholar 

  105. Duffy DM, Stouffer RL (2003) Luteinizing hormone acts directly at granulosa cells to stimulate periovulatory processes: modulation of luteinizing hormone effects by prostaglandins. Endocrine 22(3):249-256

    Article  PubMed  CAS  Google Scholar 

  106. Puistola U, Salo T, Martikainen H, Ronnberg L (1986) Type IV collagenolytic activity in human preovulatory follicular fluid. Fertil Steril 45(4):578-580

    PubMed  CAS  Google Scholar 

  107. Postawski K, Rechberger T, Jakimiuk AJ, Skorupski P, Bogusiewicz M, Jakowicki JA (1999) Interstitial collagenase (MMP-1) activity in human ovarian tissue. Gynecol Endocrinol 13(4):273-278

    Article  PubMed  CAS  Google Scholar 

  108. Lind AK, Dahm-Kahler P, Weijdegard B, Sundfeldt And K, Brannstrom M (2006) Gelatinases and their tissue inhibitors during human ovulation: increased expression of tissue inhibitor of matrix metalloproteinase-1. Mol Hum Reprod 12(12):725-736

    Article  PubMed  CAS  Google Scholar 

  109. Curry TE Jr, Mann JS, Estes RS, Jones PB (1990) Alpha 2-macroglobulin and tissue inhibitor of metalloproteinases: collagenase inhibitors in human preovulatory ovaries. Endocrinology 127(1):63-68

    Article  PubMed  CAS  Google Scholar 

  110. D’Ascenzo S, Giusti I, Millimaggi D et al (2004) Intrafollicular expression of matrix metalloproteinases and their inhibitors in normally ovulating women compared with patients undergoing in vitro fertilization treatment. Eur J Endocrinol 151(1):87-91

    Article  PubMed  Google Scholar 

  111. Ben-Shlomo I, Goldman S, Shalev E (2003) Regulation of matrix metalloproteinase-9 (MMP-9), tissue inhibitor of MMP, and progesterone secretion in luteinized granulosa cells from normally ovulating women with polycystic ovary disease. Fertil Steril 79(Suppl 1):694-701

    Article  PubMed  Google Scholar 

  112. Myohanen H, Vaheri A (2004) Regulation and interactions in the activation of cell-associated plasminogen. Cell Mol Life Sci 61(22):2840-2858

    Article  PubMed  CAS  Google Scholar 

  113. Peng XR, Hsueh AJ, Ny T (1993) Transient and cell-specific expression of tissue-type plasminogen activator and plasminogen-activator-inhibitor type 1 results in controlled and directed proteolysis during gonadotropin-induced ovulation. Eur J Biochem 214(1):147-156

    Article  PubMed  CAS  Google Scholar 

  114. Hagglund AC, Ny A, Liu K, Ny T (1996) Coordinated and cell-specific induction of both physiological plasminogen activators creates functionally redundant mechanisms for plasmin formation during ovulation. Endocrinology 137(12):5671-5677

    Article  PubMed  CAS  Google Scholar 

  115. Politis I, Srikandakumar A, Turner JD, Tsang BK, Ainsworth L, Downey BR (1990) Changes in and partial identification of the plasminogen activator and plasminogen activator inhibitor systems during ovarian follicular maturation in the pig. Biol Reprod 43(4):636-642

    Article  PubMed  CAS  Google Scholar 

  116. Liu YX, Liu K, Feng Q et al (2004) Tissue-type plasminogen activator and its inhibitor plasminogen activator inhibitor type 1 are coordinately expressed during ovulation in the rhesus monkey. Endocrinology 145(4):1767-1775

    Article  PubMed  CAS  Google Scholar 

  117. Jones PB, Muse KN, Wilson EA, Curry TE Jr (1988) Expression of plasminogen activator (PA) and a PA inhibitor in human granulosa cells from preovulatory follicles. J Clin Endocrinol Metab 67(4):857-860

    Article  PubMed  CAS  Google Scholar 

  118. Jones PB, Vernon MW, Muse KN, Curry TE Jr (1989) Plasminogen activator and plasminogen activator inhibitor in human preovulatory follicular fluid. J Clin Endocrinol Metab 68(6):1039-1045

    Article  PubMed  CAS  Google Scholar 

  119. Leonardsson G, Peng XR, Liu K et al (1995) Ovulation efficiency is reduced in mice that lack plasminogen activator gene function: functional redundancy among physiological plasminogen activators. Proc Natl Acad Sci USA 92(26):12446-12450

    Article  PubMed  CAS  Google Scholar 

  120. Ny A, Leonardsson G, Hagglund AC et al (1999) Ovulation in plasminogen-deficient mice. Endocrinology 140(11):5030-5035

    Article  PubMed  CAS  Google Scholar 

  121. Espey LL, Yoshioka S, Russell DL, Robker RL, Fujii S, Richards JS (2000) Ovarian expression of a disintegrin and metalloproteinase with thrombospondin motifs during ovulation in the gonadotropin-primed immature rat. Biol Reprod 62(4):1090-1095

    Article  PubMed  CAS  Google Scholar 

  122. Boerboom D, Russell DL, Richards JS, Sirois J (2003) Regulation of transcripts encoding ADAMTS-1 (a disintegrin and metalloproteinase with thrombospondin-like motifs-1) and progesterone receptor by human chorionic gonadotropin in equine preovulatory follicles. J Mol Endocrinol 31(3):473-485

    Article  PubMed  CAS  Google Scholar 

  123. Richards JS, Hernandez-Gonzalez I, Gonzalez-Robayna I et al (2005) Regulated expression of ADAMTS family members in follicles and cumulus oocyte complexes: evidence for specific and redundant patterns during ovulation. Biol Reprod 72(5):1241-1255

    Article  PubMed  CAS  Google Scholar 

  124. Russell DL, Ochsner SA, Hsieh M, Mulders S, Richards JS (2003) Hormone-regulated expression and localization of versican in the rodent ovary. Endocrinology 144(3):1020-1031

    Article  PubMed  CAS  Google Scholar 

  125. Russell DL, Doyle KM, Ochsner SA, Sandy JD, Richards JS (2003) Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. J Biol Chem 278(43):42330-42339

    Article  PubMed  CAS  Google Scholar 

  126. Park PW, Reizes O, Bernfield M (2000) Cell surface heparan sulfate proteoglycans: selective regulators of ligand-receptor encounters. J Biol Chem 275(39):29923-29926

    Article  PubMed  CAS  Google Scholar 

  127. Mittaz L, Russell DL, Wilson T et al (2004) Adamts-1 is essential for the development and function of the urogenital system. Biol Reprod 70(4):1096-1105

    Article  PubMed  CAS  Google Scholar 

  128. Brown HM, Dunning KR, Robker RL, Pritchard M, Russell DL (2006) Requirement for ADAMTS-1 in extracellular matrix remodeling during ovarian folliculogenesis and lymphangiogenesis. Dev Biol 300(2):699-709

    Article  PubMed  CAS  Google Scholar 

  129. Ohnishi J, Ohnishi E, Shibuya H, Takahashi T (2005) Functions for proteinases in the ovulatory process. Biochim Biophys Acta 1751(1):95-109

    PubMed  CAS  Google Scholar 

  130. Young KA, Tumlinson B, Stouffer RL (2004) ADAMTS-1/METH-1 and TIMP-3 expression in the primate corpus luteum: divergent patterns and stage-dependent regulation during the natural menstrual cycle. Mol Hum Reprod 10(8):559-565

    Article  PubMed  CAS  Google Scholar 

  131. Gao S, De Geyter C, Kossowska K, Zhang H (2007) FSH stimulates the expression of the ADAMTS-16 protease in mature human ovarian follicles. Mol Hum Reprod 13(7):465-471

    Article  PubMed  CAS  Google Scholar 

  132. Hellberg P, Thomsen P, Janson PO, Brannstrom M (1991) Leukocyte supplementation increases the luteinizing hormone-induced ovulation rate in the in vitro-perfused rat ovary. Biol Reprod 44(5):791-797

    Article  PubMed  CAS  Google Scholar 

  133. Brannstrom M, Mayrhofer G, Robertson SA (1993) Localization of leukocyte subsets in the rat ovary during the periovulatory period. Biol Reprod 48(2):277-286

    Article  PubMed  CAS  Google Scholar 

  134. Cohen PE, Zhu L, Pollard JW (1997) Absence of colony stimulating factor-1 in osteopetrotic (csfmop/csfmop) mice disrupts estrous cycles and ovulation. Biol Reprod 56(1):110-118

    Article  PubMed  CAS  Google Scholar 

  135. Van der Hoek KH, Maddocks S, Woodhouse CM, van Rooijen N, Robertson SA, Norman RJ (2000) Intrabursal injection of clodronate liposomes causes macrophage depletion and inhibits ovulation in the mouse ovary. Biol Reprod 62(4):1059-1066

    Article  PubMed  Google Scholar 

  136. Wu R, Van der Hoek KH, Ryan NK, Norman RJ, Robker RL (2004) Macrophage contributions to ovarian function. Hum Reprod Update 10(2):119-133

    Article  PubMed  Google Scholar 

  137. Brannstrom M, Bonello N, Norman RJ, Robertson SA (1995) Reduction of ovulation rate in the rat by administration of a neutrophil-depleting monoclonal antibody. J Reprod Immunol 29(3):265-270

    Article  PubMed  CAS  Google Scholar 

  138. Smith MP, Flannery GR, Randle BJ, Jenkins JM, Holmes CH (2005) Leukocyte origin and profile in follicular aspirates at oocyte retrieval. Hum Reprod 20(12):3526-3531

    Article  PubMed  CAS  Google Scholar 

  139. Brannstrom M, Pascoe V, Norman RJ, McClure N (1994) Localization of leukocyte subsets in the follicle wall and in the corpus luteum throughout the human menstrual cycle. Fertil Steril 61(3):488-495

    PubMed  CAS  Google Scholar 

  140. Best CL, Pudney J, Welch WR, Burger N, Hill JA (1996) Localization and characterization of white blood cell populations within the human ovary throughout the menstrual cycle and menopause. Hum Reprod 11(4):790-797

    PubMed  CAS  Google Scholar 

  141. Takaya R, Fukaya T, Sasano H, Suzuki T, Tamura M, Yajima A (1997) Macrophages in normal cycling human ovaries; immunohistochemical localization and characterization. Hum Reprod 12(7):1508-1512

    Article  PubMed  CAS  Google Scholar 

  142. Brannstrom M, Wang L, Norman RJ (1993) Ovulatory effect of interleukin-1 beta on the perfused rat ovary. Endocrinology 132(1):399-404

    Article  PubMed  CAS  Google Scholar 

  143. Peterson CM, Hales HA, Hatasaka HH, Mitchell MD, Rittenhouse L, Jones KP (1993) Interleukin-1 beta (IL-1 beta) modulates prostaglandin production and the natural IL-1 receptor antagonist inhibits ovulation in the optimally stimulated rat ovarian perfusion model. Endocrinology 133(5):2301-2306

    Article  PubMed  CAS  Google Scholar 

  144. Ellman C, Corbett JA, Misko TP, McDaniel M, Beckerman KP (1993) Nitric oxide mediates interleukin-1-induced cellular cytotoxicity in the rat ovary. A potential role for nitric oxide in the ovulatory process. J Clin Invest 92(6):3053-3056

    Article  PubMed  CAS  Google Scholar 

  145. Wang LJ, Norman RJ (1992) Concentrations of immunoreactive interleukin-1 and interleukin-2 in human preovulatory follicular fluid. Hum Reprod 7(2):147-150

    PubMed  CAS  Google Scholar 

  146. Brannstrom M, Bonello N, Wang LJ, Norman RJ (1995) Effects of tumour necrosis factor alpha (TNF alpha) on ovulation in the rat ovary. Reprod Fertil Dev 7(1):67-73

    Article  PubMed  CAS  Google Scholar 

  147. Gottsch ML, Van Kirk EA, Murdoch WJ (2000) Tumour necrosis factor alpha up-regulates matrix metalloproteinase-2 activity in periovulatory ovine follicles: metamorphic and endocrine implications. Reprod Fertil Dev 12(1-2):75-80

    Article  PubMed  CAS  Google Scholar 

  148. Wang LJ, Brannstrom M, Robertson SA, Norman RJ (1992) Tumor necrosis factor alpha in the human ovary: presence in follicular fluid and effects on cell proliferation and prostaglandin production. Fertil Steril 58(5):934-940

    PubMed  CAS  Google Scholar 

  149. Nishimura K, Tanaka N, Ohshige A, Fukumatsu Y, Matsuura K, Okamura H (1995) Effects of macrophage colony-stimulating factor on folliculogenesis in gonadotrophin-primed immature rats. J Reprod Fertil 104(2):325-330

    Article  PubMed  CAS  Google Scholar 

  150. Brannstrom M, Norman RJ, Seamark RF, Robertson SA (1994) Rat ovary produces cytokines during ovulation. Biol Reprod 50(1):88-94

    Article  PubMed  CAS  Google Scholar 

  151. Jasper MJ, Robertson SA, Van der Hoek KH, Bonello N, Brannstrom M, Norman RJ (2000) Characterization of ovarian function in granulocyte-macrophage colony-stimulating factor-deficient mice. Biol Reprod 62(3):704-713

    Article  PubMed  CAS  Google Scholar 

  152. Jasper MJ, Brannstrom M, Olofsson JI et al (1996) Granulocyte-macrophage colony-stimulating factor: presence in human follicular fluid, protein secretion and mRNA expression by ovarian cells. Mol Hum Reprod 2(8):555-562

    Article  PubMed  CAS  Google Scholar 

  153. Luster AD (1998) Chemokines-chemotactic cytokines that mediate inflammation. N Engl J Med 338(7):436-445

    Article  PubMed  CAS  Google Scholar 

  154. Wong KH, Negishi H, Adashi EY (2002) Expression, hormonal regulation, and cyclic variation of chemokines in the rat ovary: key determinants of the intraovarian residence of representatives of the white blood cell series. Endocrinology 143(3):784-791

    Article  PubMed  CAS  Google Scholar 

  155. Zhou C, Wu J, Borillo J et al (2005) Transient expression of CC chemokine TECK in the ovary during ovulation: its potential role in ovulation. Am J Reprod Immunol 53(5):238-248

    Article  PubMed  CAS  Google Scholar 

  156. Arici A, Oral E, Bukulmez O, Buradagunta S, Engin O, Olive DL (1996) Interleukin-8 expression and modulation in human preovulatory follicles and ovarian cells. Endocrinology 137(9):3762-3769

    Article  PubMed  CAS  Google Scholar 

  157. Runesson E, Bostrom EK, Janson PO, Brannstrom M (1996) The human preovulatory follicle is a source of the chemotactic cytokine interleukin-8. Mol Hum Reprod 2(4):245-250

    Article  PubMed  CAS  Google Scholar 

  158. Runesson E, Ivarsson K, Janson PO, Brannstrom M (2000) Gonadotropin- and cytokine-regulated expression of the chemokine interleukin 8 in the human preovulatory follicle of the menstrual cycle. J Clin Endocrinol Metab 85(11):4387-4395

    Article  PubMed  CAS  Google Scholar 

  159. Buscher U, Chen FC, Kentenich H, Schmiady H (1999) Cytokines in the follicular fluid of stimulated and non-stimulated human ovaries; is ovulation a suppressed inflammatory reaction? Hum Reprod 14(1):162-166

    Article  PubMed  CAS  Google Scholar 

  160. Shinetugs B, Runesson E, Bonello NP, Brannstrom M, Norman RJ (1999) Colony stimulating factor-1 concentrations in blood and follicular fluid during the human menstrual cycle and ovarian stimulation: possible role in the ovulatory process. Hum Reprod 14(5):1302-1306

    Article  PubMed  CAS  Google Scholar 

  161. Machelon V, Nome F, Emilie D (2000) Regulated on activation normal T expressed and secreted chemokine is induced by tumor necrosis factor-alpha in granulosa cells from human preovulatory follicle. J Clin Endocrinol Metab 85(1):417-424

    Article  PubMed  CAS  Google Scholar 

  162. Callard R, Gearing A (1994) The Cytokine. Academic Press Limited, London, Great Britain

    Google Scholar 

  163. Baggiolini M, Dewald B, Moser B (1994) Interleukin-8 and related chemotactic cytokines-CXC and CC chemokines. Adv Immunol 55:97-179

    Article  PubMed  CAS  Google Scholar 

  164. Cushing SD, Fogelman AM (1992) Monocytes may amplify their recruitment into inflammatory lesions by inducing monocyte chemotactic protein. Arterioscler Thromb 12(1):78-82

    PubMed  CAS  Google Scholar 

  165. Arefieva TI, Kukhtina NB, Antonova OA, Krasnikova TL (2005) MCP-1-stimulated chemotaxis of monocytic and endothelial cells is dependent on activation of different signaling cascades. Cytokine 31(6):439-446

    Article  PubMed  CAS  Google Scholar 

  166. Zhou C, Borillo J, Wu J, Torres L, Lou YH (2004) Ovarian expression of chemokines and their receptors. J Reprod Immunol 63(1):1-9

    Article  PubMed  CAS  Google Scholar 

  167. Arici A, Oral E, Bukulmez O, Buradagunta S, Bahtiyar O, Jones EE (1997) Monocyte chemotactic protein-1 expression in human preovulatory follicles and ovarian cells. J Reprod Immunol 32(3):201-219

    Article  PubMed  CAS  Google Scholar 

  168. Kawano Y, Kawasaki F, Nakamura S, Matsui N, Narahara H, Miyakawa I (2001) The production and clinical evaluation of macrophage colony-stimulating factor and macrophage chemoattractant protein-1 in human follicular fluids. Am J Reprod Immunol 45(1):1-5

    Article  PubMed  CAS  Google Scholar 

  169. Dahm-Kahler P, Runesson E, Lind AK, Brannstrom M (2006) Monocyte chemotactic protein-1 in the follicle of the menstrual and IVF cycle. Mol Hum Reprod 12(1):1-6

    Article  PubMed  CAS  Google Scholar 

  170. Kawano Y, Fukuda J, Itoh H, Takai N, Nasu K, Miyakawa I (2004) The effect of inflammatory cytokines on secretion of macrophage colony-stimulating factor and monocyte chemoattractant protein-1 in human granulosa cells. Am J Reprod Immunol 52(2):124-128

    Article  PubMed  Google Scholar 

  171. Dahm-Kähler P, Ghahremani M, Lind AK, Sundfeldt K, Brännström M (2009) Monocyte chemotactic protein-1 (MCP-1), its receptor and macrophages in the perifollicular stroma during the human ovulatory process. Fertil Steril 91(1):231-9

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Obstetrics and Gynecology, Sahlgrenska Academy at University of Gothenburg, Göteborg, Sweden

    Mats Brännström, Anna Karin Lind & Pernilla Dahm-Kähler

Authors
  1. Mats Brännström
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anna Karin Lind
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pernilla Dahm-Kähler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mats Brännström .

Editor information

Editors and Affiliations

  1. School of Medicine, University of Utah, Arapeen Dr. 675, Salt Lake City, 84108, USA

    Douglas T. Carrell

  2. School of Medicine, University of Utah, North Medical Drive 50, Salt Lake City, 84132, USA

    C. Matthew Peterson

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Brännström, M., Lind, A.K., Dahm-Kähler, P. (2010). Ovulation: A Molecular View. In: Carrell, D., Peterson, C. (eds) Reproductive Endocrinology and Infertility. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1436-1_9

Download citation

  • DOI: https://doi.org/10.1007/978-1-4419-1436-1_9

  • Published:

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4419-1435-4

  • Online ISBN: 978-1-4419-1436-1

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation