Reproductive Biology and Endocrinology | |
Ovarian responses to undernutrition in pregnant ewes, USA | |
Stephen P Ford1  Kimberly A Vonnahme1  Edward A Van Kirk1  William J Murdoch1  | |
[1] Address: Department of Animal Science, University of Wyoming, Laramie 82071 | |
关键词: corpus luteum; follicle; fetal oogenesis; pregnancy; nutrition; sheep; | |
Others : 1157024 DOI : 10.1186/1477-7827-1-6 |
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received in 2003-01-23, accepted in 2003-02-05, 发布年份 2003 | |
【 摘 要 】
In most mammals oogonia proliferate by mitosis and begin meiotic development during fetal life. Previous studies indicated that there is a delay in the progression to the first stage of meiotic arrest in germ cells of female fetuses of undernourished ewes. We report that underfeeding (50% NRC requirement beginning on Day 28 of pregnancy) provokes an increase in oxidative base lesions within DNA of mid-gestational (Day 78) fetal oogonia; this condition was associated with up-regulation of the tumor suppressor/cell-cycle arrest modulator p53, antiapoptotic factor Bcl-2, and base-excision repair polymerase β. Fetal ovarian weights and germ cell concentrations were not altered by nutrient deprivation. Ovaries of ewes on control diets (100% NRC) contained more tertiary follicles than their restricted counterparts; however, peripheral venous estradiol-17β was not different between groups. There was no effect of treatment on p53 accumulation in maternal oocytes. Luteal structure-function was not perturbed by undernutrition. No fetal losses were attributed to the dietary restriction. It is proposed that DNA of interphase fetal oogonia is vulnerable to oxidative insults perpetrated by a nutritional stress to the dam, and that multiple/integrated adaptive molecular response mechanisms of cell-cycle inhibition (providing the time required for base repairs) and survival hence sustain the genomic integrity and population stability of the germline.
【 授权许可】
2003 Murdoch et al; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL.
【 预 览 】
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【 参考文献 】
- [1]Rhind SM, Rae MT, Brooks AN: Effects of nutrition and environmental factors on the fetal programming of the reproductive axis. Reproduction 2001, 122:205-214.
- [2]Borwick SC, Rhind SM, McMillen SR, Racey PA: Effect of undernutrition of ewes from the time of mating on fetal ovarian development in mid gestation. Reprod Fertil Dev 1997, 9:711-715.
- [3]Rae MT, Palassio S, Kyle CE, Brooks AN, Lea RG, Miller DW, Rhind SM: Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses. Reproduction 2001, 122:915-922.
- [4]Amundson SA, Myers TG, Fornace AJ: Roles for p53 in growth arrest and apoptosis: putting on the breaks after genotoxic stress. Oncogene 1998, 17:3287-3299.
- [5]Evan G, Littlewood T: A matter of life and death. Science 1998, 281:1317-1322.
- [6]Eastman A, Rigas JR: Modulation of apoptosis signaling pathways and cell cycle regulation. Semin Oncol 1999, 26:7-16.
- [7]Sionov RV, Haupt Y: The cellular response to p53: the decision between life and death. Oncogene 1999, 18:6145-6157.
- [8]Wathes DC: Embryonic mortality and the uterine environment. J Endocrinol 1992, 134:321-325.
- [9]Niswender GD, Juengel JL, Silva PJ, Rollyson MK, McIntush EW: Mechanisms controlling the function and life span of the corpus luteum. Physiol Rev 2000, 80:1-29.
- [10]Rexroad CE, Casida LE: Ovarian follicular development in cows, sows and ewes in different stages of pregnancy as affected by number of corpora lutea in the same ovary. J Anim Sci 1975, 41:1090-1097.
- [11]Taylor C, Rajamahendran R: Follicular dynamics and corpus luteum growth and function in pregnant versus nonpregnant cows. J Dairy Sci 1991, 74:115-123.
- [12]Bartlewski PM, Beard AP, Rawlings NC: Ultrasonographic study of ovarian function during early pregnancy and after parturition in the ewe. Theriogenology 2000, 53:673-689.
- [13]Compton MM: A biochemical hallmark of apoptosis: internucleosomal degradation of the genome. Cancer Metast Rev 1992, 11:105-119.
- [14]de Zwart LL: Biomarkers of free radical damage: applications in experimental animals and in humans. Free Rad Biol Med 1999, 26:202-226.
- [15]Adams JM, Cory S: The Bcl-2 protein family: arbiters of cell survival. Science 1998, 281:1322-1326.
- [16]Wilson SH: Mammalian base excision repair and DNA polymerase β. Mutat Res 1998, 407:203-215.
- [17]Murdoch WJ, Townsend RS, McDonnel AC: Ovulation-induced DNA damage in ovarian surface epithelial cells of ewes: prospective regulatory mechanisms of repair/survival and apoptosis. Biol Reprod 2001, 65:1417-1424.
- [18]Murdoch WJ: Programmed cell death in preovulatory ovine follicles. Biol Reprod 1995, 53:8-12.
- [19]Allen RT, Hunter WJ, Agrawal DK: Morphological and biochemical characterization and analysis of apoptosis. J Pharmacol Toxicol Meth 1997, 37:215-228.
- [20]Eggleston DL, Wilken C, Van Kirk EA, Slaughter RG, Ji TH, Murdoch WJ: Progesterone induces expression of endometrial messenger RNA encoding for cyclooxygenase. Prostaglandins 1990, 39:675-683.
- [21]Field RA, Maiorano G, Hinds FC, Murdoch WJ, Riley ML: Bone ossification and carcass characteristics of wethers given silastic implants containing estradiol. J Anim Sci 1990, 68:3663-3668.
- [22]McPherson LA, Van Kirk EA, Murdoch WJ: Localization of stress protein-70 in ovine corpora lutea during prostaglandin-induced luteolysis. Prostaglandins 1993, 46:433-440.
- [23]Sawyer HR: Structural and functional properties of the corpus luteum of pregnancy. J Reprod Fertil Suppl 1995, 49:97-110.
- [24]Grollman AP, Moriya M: Mutagenesis by 8-oxoguanine: an enemy within. Trends Genet 1993, 9:246-249.
- [25]Schwartz D, Goldfinger N, Kam Z, Rotter V: p53 controls low DNA damage-dependent premeiotic checkpoint and facilitates DNA repair during spermatogenesis. Cell Growth Diff 1999, 10:665-675.
- [26]Hunt PA, Hassold TJ: Sex matters in meiosis. Science 2002, 296:2181-2183.
- [27]Baarends WM, van der Laan R, Grootegoed JA: DNA repair mechanisms and gametogenesis. Reproduction 2001, 121:31-39.
- [28]Tsujimoto Y, Shimizu S: Bcl-2 family: life-or-death switch. FEBS Lett 2000, 466:6-10.
- [29]Dianov G, Bischoff C, Piotrowski J, Bohr VA: Repair pathways for processing of 8-oxoguanine in DNA by mammalian cell extracts. J Biol Chem 1998, 273:33811-33816.
- [30]Albertini DF, Carabatsos MJ: Comparative aspects of meiotic cell cycle control in mammals. J Mol Med 1998, 76:795-799.
- [31]McNatty KP, Smith P, Hudson NL, Heath DA, Tisdall DJ, O WS, Braw-Tal R: Development of the sheep ovary during fetal and early neonatal life and the effect of fecundity genes. J Reprod Fertil Suppl 1995, 49:123-135.
- [32]Picton H, Briggs D, Gosden R: The molecular basis of oocyte growth and development. Mol Cell Endocrinol 1998, 145:27-37.
- [33]Sawyer HR, Smith P, Heath DA, Juengel JL, Wakefield SJ, McNatty KP: Formation of ovarian follicles during fetal development in sheep. Biol Reprod 2002, 66:1134-1150.
- [34]Collins AR: Oxidative DNA damage, antioxidants, and cancer. Bioessays 1999, 21:238-246.
- [35]Bauer MK, Harding JE, Bassett NS, Brier BH, Oliver MH, Gallaher BH, Evans PC, Woodall SM, Gluckman PD: Fetal growth and placental function. Mol Cell Endocrinol 1998, 140:115-129.
- [36]Li C, Jackson RM: Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 2002, 282:C227-C241.
- [37]Ashworth CJ, Antipatis C: Micronutrient programming of development throughout gestation. Reproduction 2001, 122:527-535.
- [38]Matova N, Cooley L: Comparative aspects of animal oogenesis. Dev Biol 2001, 231:291-320.
- [39]Tilly JL: Commuting the death sentence: how oocytes strive to survive. Nat Rev Mol Cell Biol 2001, 2:838-848.
- [40]Smith P, O WS, Hudson NL, Shaw L, Heath DA, Condell L, Phillips DJ, McNatty KP: Effects of the Booroola gene (FecB) on body weight, ovarian development and hormone concentrations during fetal life. J Reprod Fertil 1993, 98:41-54.
- [41]Lumey LH, Stein AD: In utero exposure to famine and subsequent fertility: the Dutch famine birth cohort study. Am J Public Health 1997, 87:1962-1966.
- [42]Osgerby JC, Wathes DC, Howard D, Gadd TS: The effect of maternal undernutrition on ovine fetal growth. J Endocrinol 2002, 173:131-141.
- [43]Robles R, Morita Y, Mann KK, Perez GI, Yang S, Matikainen T, Sherr DH, Tilly JL: The aryl hydrocarbon receptor, a basic helix-loop-helix transcription factor of the PAS gene family, is required for normal ovarian germ cell dynamics in the mouse. Endocrinology 2000, 141:450-453.
- [44]Matikainen TM, Moriyama T, Morita Y, Perez GI, Korsmeyer SJ, Sherr DH, Tilly JL: Ligand activation of the aromatic hydrocarbon receptor transcription factor drives Bax-dependent apoptosis in developing fetal ovarian germ cells. Endocrinology 2002, 143:615-620.
- [45]Symonds ME, Budge H, Stephenson T, McMillen IC: Fetal endocrinology and development – manipulation and adaptation to long-term nutritional and environmental challenges. Reproduction 2001, 121:853-862.
- [46]Hard DL, Anderson LL: Maternal starvation and progesterone secretion, litter size, and growth in the pig. Am J Physiol 1979, 237:E273-E278.