Reproduction in Domestic Animals

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56 M Mihm and ACO Evanswaves of ovarian follicular development in a single estrouscycle. Biol Reprod 68, 822–828.Prendiville DJ, Enright WJ, Crowe MA, Finnerty M, HynesN, Roche JF, 1995: Immunization of heifers againstgonadotropin releasing hormone: antibody titres, ovarianfunction, body growth and carcass characteristics. J AnimSci 73, 2382–2389.Rivera GM, Fortune JE, 2003: Selection of the dominantfollicle and insulin-like growth factor (IGF)-binding proteins:evidence that pregnancy-associated plasma protein Acontributes to proteolysis of IGF-binding protein 5 inbovine follicular fluid. Endocrinology 144, 437–446.Rivera GM, Chandrasekher YA, Giudice LC, Evans ACO,Fortune JE, 2001: A potential role for insulin-like growthfactor binding protein-4 proteolysis in the establishment ofovarian follicular dominance in cattle. Biol Reprod 65, 102–111.Roberts AJ, Echternkamp SE, 2003: Insulin-like growth factorbinding proteins in granulosa and thecal cells from bovineovarian follicles at different stages of development. J AnimSci 81, 2826–2839.Roche JF, Mihm M, Diskin M, Ireland JJ, 1998: A reviewof regulation of follicle growth in cattle. J Anim Sci76(Suppl. 3), 16–29.Rozell TG, Monteiro AM, Baker PJ, Mihm M, 2005: Evidencefor differential expression of FSH receptor exons 10 and 11during follicular wave development in the cow. Biol Reprod,Special Issue, 179 (Abstract M445).Ryan KE, Casey SM, Canty MJ, Crowe MA, Martin F, EvansACO, 2007: Akt and Erk signal transduction pathways areearly markers of differentiation in dominant and subordinateovarian follicles in cattle. Reproduction 133, 617–626.San Roman GA, Magoffin DA, 1993: Insulin-like growthfactor-binding proteins in healthy and atretic follicles duringnatural menstrual cycles. J Clin Endocrinol Metab 76, 625–632.Savio JD, Keenan L, Boland MP, Roche JF, 1988: Pattern ofgrowth of dominant follicles during the oestrous cycle ofheifers. J Reprod Fertil 83, 663–671.Schipper I, Hop WCJ, Fauser BCJM, 1998: The folliclestimulatinghormone (FSH) threshold ⁄ window conceptexamined by different interventions with exogenous FSHduring the follicular phase of the normal menstrual cycle:duration, rather than magnitude, of FSH increase affectsfollicle development. J Clin Endocrinol Metab 83, 1292–1298.Schneyer AL, Fujiwara T, Fox J, Welt CK, Adams J,Messerlian GM, Taylor AE, 2000: Dynamic changes in theintrafollicular inhibin ⁄ activin ⁄ follistatin axis during humanfollicular development: relationship to circulating hormoneconcentrations. J Clin Endocrinol Metab 85, 3319–3330.Schuller AGP, Lindenberghkortleve DJ, Pache TD, ZwarthoffEC, Fauser BCJM, Drop SLS, 1993: Insulin-like growthfactorbinding protein-2, 28-kDa and 24-kDa insulin-likegrowth-factor binding-protein levels are decreased in fluid ofdominant follicles, obtained from normal and polycysticovaries. Regul Pept 48, 157–163.Sisco B, Hagemann LJ, Shelling AN, Pfeffer PL, 2003:Isolation of genes differentially expressed in dominant andsubordinate bovine follicles. Endocrinology 144, 3904–3913.Spicer LJ, Aad PY, 2007: Insulin-like growth factor (IGF) 2stimulates steroidogenesis and mitosis of bovine granulosacells through the IGF1 receptor: role of follicle-stimulatinghormone and IGF2 receptor. Biol Reprod 77, 18–27.Stagg K, Spicer LJ, Diskin MG, Sreenan JM, Roche JF, 1998:Effect of calf isolation on follicular wave dynamics, gonadotropinand metabolic hormone changes, and interval tofirst ovulation in beef cows fed either of two energy levelspostpartum. Biol Reprod 59, 777–783.Stewart RE, Spicer LJ, Hamilton TD, Keefer BE, Dawson LJ,Morgan GL, Echternkamp SE, 1996: Levels of insulin-likegrowth factor (IGF) binding proteins, luteinizing hormoneand IGF-I receptors, and steroids in dominant folliclesduring the first follicular wave in cattle exhibiting regularestrous cycles. Endocrinology 137, 2842–2850.Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ,1994: Selection, dominance and atresia of follicles during theoestrous cycle of heifers. J Reprod Fertil 101, 547–555.Sunderland SJ, Knight PG, Boland MP, Roche JF, Ireland JJ,1996: Alterations in intrafollicular levels of different molecularmass forms of inhibin during development of follicularandluteal-phase dominant follicles in heifers. Biol Reprod54, 453–462.Van Santbrink EJP, Hop WC, Van Dessel TJHM, De JongFH, Fauser BCJM, 1995: Decremental follicle-stimulatinghormoneand dominant follicle development during thenormal menstrual-cycle. Fertil Steril 64, 37–43.Watson ED, Al-zi’abi MO, 2002: Characterization of morphologyand angiogenesis in follicles of mares during springtransition and the breeding season. Reproduction 124, 227–234.Watson ED, Thomassen R, Steele M, Heald M, Leask R,Groome NP, Riley SC, 2002: Concentrations of inhibin,progesterone and oestradiol in fluid from dominant andsubordinate follicles from mares during spring transitionand the breeding season. Anim Reprod Sci 74, 55–67.Wiltbank MC, Fricke PM, Sangsritavong S, Sartori R,Ginther OJ, 2000: Mechanisms that prevent and producedouble ovulations in dairy cattle. J Dairy Sci 83, 2998–3007.Zeleznik AJ, 2001: Follicle selection in primates: ‘many arecalled but few are chosen’. Biol Reprod 65, 655–659.Zielak AE, Forde N, Park SD, Doohan F, Coussens PM,Smith GW, Ireland JJ, Lonergan P, Evans AC, 2007:Identification of novel genes associated with dominant follicledevelopment in cattle. Reprod Fertil Dev 19, 967–975.Author’s address (for correspondence): M Mihm, Division of CellSciences, Faculty of Veterinary Medicine, University of Glasgow,Bearsden Road, Glasgow, G61 1QH, UK. E-mail: m.mihm@vet.gla.ac.ukConflict of interest: The authors declare no conflict of interests.Ó 2008 The Authors. Journal compilation Ó 2008 Blackwell Verlag
Reprod Dom Anim 43 (Suppl. 2), 57–65 (2008); doi: 10.1111/j.1439-0531.2008.01143.xISSN 0936-6768Regulation of Luteal Function and Corpus Luteum Regression in Cows: HormonalControl, Immune Mechanisms and Intercellular CommunicationDJ Skarzynski 1 , G Ferreira-Dias 2 and K Okuda 31 Department of Reproductive Immunology, Institute of Animal Reproduction and Food Research of PAS, Olsztyn, Poland; 2 C.I.I.S.A., Facultyof Veterinary Medicine, TU Lisbon, Portugal; 3 Laboratory of Reproductive Endocrinology, Graduate School of Natural Science andTechnology, Okayama University, Okayama, JapanContentsThe main function of the corpus luteum (CL) is production ofprogesterone (P4). Adequate luteal function to secrete P4 iscrucial for determining the physiological duration of theoestrous cycle and for achieving a successful pregnancy. Thebovine CL grows very fast and regresses within a few days atluteolysis. Mechanisms controlling development and secretoryfunction of the bovine CL may involve many factors that areproduced both within and outside the CL. Some of theseregulators seem to be prostaglandins (PGs), oxytocin, growthand adrenergic factors. Moreover, there is evidence that P4acts within the CL as an autocrine or paracrine regulator. Eachof these factors may act on the CL independently or maymodify the actions of others. Although uterine PGF 2a isknown to be a principal luteolytic factor, its direct action onthe CL is mediated by local factors: cytokines, endothelin-1,nitric oxide. The changes in ovarian blood flow have also beensuggested to have some role in regulation of CL development,maintenance and regression.IntroductionThe corpus luteum (CL) is a transient ovarian organthat is established by cells of a follicle after ovulation.The mammalian CL is composed of a heterogeneousmixture of cell types. There are at least two types ofsteroidogenic cells, large and small luteal cells, whichoriginate from the granulosa and thecal cells of thefollicle ruptured at ovulation, respectively. The CLconsists of not only steroidogenic luteal cells but alsonon-steroidogenic cells, i.e. vascular endothelial cells,fibroblasts, pericytes and immune cells such as lymphocytes,leucocytes and macrophages (Lei et al. 1991).Macrophages and endothelial cells infiltrate into thenewly formed CL concomitant with vascular angiogenesis(Reynolds and Redmer 1999). Most of the cellsproliferating during growth of the CL are endothelialcells under hypoxic conditions, although leucocytes havebeen shown to proliferate in CL as well (Reynolds andRedmer 1999; Towson et al. 2002). There is evidencethat steroids, protein hormones, growth factors, eicosanoidsand cytokines produced by the component cells ofthe CL play roles in establishing CL (Reynolds andRedmer 1999; Berisha and Schams 2005).Progesterone (P4), the primary product of the CL, isrequired for establishment and maintenance of pregnancy.P4 concentration in blood increases during thedeveloping luteal stage. The CL continues to secrete ahigh level of P4 until late luteal stage, and then its abilityrapidly decreases in the regressing luteal stage. Indomestic animals, luteinizing hormone (LH) releasedin a pulsatile fashion from the anterior pituitary is oneof the most potent regulators of synthesis and secretionof P4 in the CL (Niswender et al. 2007). Luteinizinghormone stimulates P4 production in small luteal cellsvia the LH receptor. In addition to pituitary hormones,intraluteal substances produced by the component cellsof the CL play important roles in regulating P4production during the luteal stages in bovine CL.Moreover, the changes in P4 concentration throughoutthe luteal phase are closely associated with blood flow aswell as steroidogenic capacity of luteal cells. Duringluteal regression, the decrease in P4 is concerned withreduced blood flow and loss of LH receptors in the CL(Niswender et al. 1976).When animals do not become pregnant, regression ofthe CL, termed luteolysis, is essential for normalcyclicity as it allows development of a new ovulatoryfollicle. In the cow, luteolysis is initiated by prostaglandin(PG)F 2a released from the uterus at the late lutealstage. Luteolysis consists of two phases, functionalluteolysis and structural luteolysis in mammals (McCrackenet al. 1999). A rapid functional regression of CLis characterized by a decrease of P4 production,followed by a phase of structural regression (McCrackenet al. 1999). During structural luteolysis, CL cellsundergo apoptosis, a process that has been describedby morphological and biochemical parameters in ruminants(Juengel et al. 1993; Rueda et al. 1995, 1997). It isgenerally accepted that the immune response playscentral roles in apoptosis of several tissues and celltypes (Nagata 1997). Recently, intraluteal mediatorsincluding cytokines and nitric oxide (NO) are thought toplay some roles as pro-apoptotic and anti-apoptoticfactors in the bovine CL, respectively (Petroff et al.2001; Skarzynski et al. 2005).This review focuses on mediators for regulatingbovine CL function throughout the oestrous cycle.Furthermore, some of our and others’ data on mediators(EDN1, cytokines, NO) of uterine PGF 2a action onbovine CL as well cell-to-cell contact and interactionsduring luteolysis have also been reviewed. Moreover,intra-luteal mechanisms controlling sensitivity of the CLto extragonadal PGF 2a are discussed.Development and Maintenance of the CorpusLuteumThe mechanism controlling development, maintenanceand secretory function of the CL may involve factorsthat are produced both within the CL and outside theovary (Fig. 1). Some of these regulators, that act asÓ 2008 The Authors. Journal compilation Ó 2008 Blackwell Verlag
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