Circadian aspects of mammalian parturition: A review

Molecular and Cellular Endocrinology

Volumn 349, Issue 1, 2012, Pages 62-67

  Olcese, James ^a  

^a FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Circadian; Clock; Melatonin; Parturition; Uterus; Zeitgeber

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; CRYPTOCHROME 1; ESTROGEN; MELATONIN; MELATONIN 1 RECEPTOR; MELATONIN 2 RECEPTOR; OXYTOCIN; PER1 PROTEIN; PER2 PROTEIN; PROGESTERONE; PROTEIN BMAL1; TRANSCRIPTION FACTOR CLOCK;

BMAL1 GENE; CHILDBIRTH; CIRCADIAN RHYTHM; CLOCK GENE; CRY1 GENE; FEMALE; GENE; GENE EXPRESSION; HUMAN; LABOR; MAMMAL; MYOMETRIUM; NONHUMAN; PER1 GENE; PER2 GENE; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SPECIES DIFFERENCE; UTERUS CONTRACTION; UTERUS FUNCTION;

ANIMALS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; FEMALE; HORMONES; HUMANS; PARTURITION; PREGNANCY; SPECIES SPECIFICITY; UTERUS;

EID: 83555176423     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.06.041     Document Type: Review

References (86)

1. Abd-Allah A.R., El-Sayed el S.M., Abdel-Wahab M.H., Hamada F.M. Effect of melatonin on estrogen and progesterone receptors in relation to uterine contraction in rats. Pharmacol. Res. 2003, 47:349-354.
2. Abe M., Herzog E.D., Yamazaki S., Straume M., Tei H., Sakaki Y., Menaker M., Block G.D. Circadian rhythms in isolated brain regions. J. Neurosci. 2002, 22:350-356.
3. Akiyama S., Ohta H., Watanabe S., Moriya T., Hariu A., Nakahata N., Chisaka H., Matsuda T., Kimura Y., Tsuchiya S., Tei H., Okamura K., Yaegashi N. The uterus sustains stable biological clock during pregnancy. Tohoku J. Exp. Med. 2010, 221:287-298.
4. Arendt J. Melatonin in humans: it's about time. J. Neuroendocrinol. 2006, 17:537-538.
5. Balsalobre A. Clock genes in mammalian peripheral tissues. Cell Tiss. Res. 2002, 309:193-199.
6. Bethin K.E., Nagai Y., Sladek R., Asada M., Sadovsky Y., Hudson T.J., Muglia L.J. Microarray analysis of uterine gene expression in mouse and human pregnancy. Mol. Endocrinol. 2003, 17:1454-1469.
7. Boer K., Lincoln D.W., Swaab D.F. Effects of electrical stimulation of the neurohypophysis on labour in the rat. J. Endocrinol. 1975, 65:163-176.
8. Burns J.K. Effects of melatonin on some blood constituents and on uterine contractility in the rat. J. Physiol. 1972, 226:106P-107P.
9. Cardinali D.P., Ritta M.N., Fuentes A.M., Gimeno M.F., Gimeno A.L. Prostaglandin E release by rat medial basal hypothalamus in vitro. Inhibition by melatonin at submicromolar concentrations. Eur. J. Pharmacol. 1980, 67:151-153.
10. Challis J.R.G., Workewych J.V., Patrick J.E. Diurnal changes in the concentration of progesterone in the plasma of women at 34-35 weeks of gestation. J. Endocrinol. 1981, 89:337-341.
11. Challis J.R.G., Sprague C., Patrick J.E. Relation between diurnal changes in peripheral plasma progesterone, cortisol, and estriol in normal women at 30-31, 34-35 and 38-39 weeks of gestation. Gynecol. Obstet. Invest. 1983, 16:33-44.
12. Challis J.R.G., Matthews S.G., Gibb W., Lye S.J. Endocrine and paracrine regulation of birth at term and preterm. Endocr. Rev. 2000, 21:514-550.
13. Chard T. Fetal and maternal oxytocin in human parturition. Am. J. Perinatol. 1989, 6:145-152.
14. Cohen M., Roselle D., Chabner B., Schmidt T.J., Lippman M. Evidence for a cytoplasmic melatonin receptor. Nature 1978, 274:894-895.
15. Cooperstock M., England J.E., Wolfe R.A. Circadian incidence of labor onset hour in preterm birth and chorioamnionitis. Obstet. Gynecol. 1987, 70:852-855.
16. Deng W.G., Tang S.T., Tseng H.P., Wu K.K. Melatonin suppresses macrophage cyclo-oxygenase-2 and inducible nitric oxide synthase expression by inhibiting p52 acetylation and binding. Blood 2006, 108:518-524.
17. Dickmeis T. Glucocorticoids and the circadian clock. J. Endocrinol. 2009, 200:3-22.
18. Dolatshad H., Campbell E.A., O'Hara L., Maywood E.S., Hastings M.H., Johnson M.H. Developmental and reproductive performance in circadian mice. Hum. Reprod. 2006, 21:68-79.
19. Dubocovich M.L., Delagrange P., Krause D.N., Sugden D., Cardinali D.P., Olcese J. International Union of Basic and Clinical Pharmacology, LXXV. Nomenclature, classification, and pharmacology of G protein-coupled melatonin receptors. Pharmacol. Rev. 2010, 62:343-380.
20. Ducsay C.A., Yellon S.M. Photoperiod regulation of uterine activity and melatonin rhythms in the pregnant rhesus macaque. Biol. Reprod. 1991, 44:967-974.
21. Ebihara S., Marks T., Hudson D.J., Menaker M. Genetic control of melatonin synthesis in the pineal gland of the mouse. Science 1986, 231:491-493.
22. Esplin M.S., Fausett M.B., Peltier M.R., Hamblin S., Silver R.M., Branch D.W., Adashi E.Y., Whiting D. The use of cDNA microarray to identify differentially expressed labor-associated genes within the human myometrium during labor. Am. J. Obstet. Gynecol. 2005, 193:404-413.
23. Farber D.M., Giussani D.A., Jenkins S.L., Mecenas C.A., Winter J.A., Wentworth R.A., Nathanielsz P.W. Timing of the switch from myometrial contractures to contractions in late-gestation pregnant rhesus monkeys as recorded by myometrial electromyogram during spontaneous term and androstenedione-induced labor. Biol. Reprod. 1997, 56:557-562.
24. Franchi A.M., Gimeno M.F., Cardinali D.P., Vacas M.I. Melatonin, 5-methoxytryptamine and some of their analogs as cyclo-oxygenase inhibitors in rat medial basal hypothalamus. Brain Res. 1987, 405:384-388.
25. Fuchs A.R., Fuchs F., Husslein P., Soloff M.S. Oxytocin receptors in the human uterus during pregnancy and parturition. Am. J. Obstet. Gynecol. 1984, 150:734-741.
26. Gimeno M.F., Landa A., Sterin-Speziale N., Cardinali D.P., Gimeno A.L. Melatonin blocks in vitro generation of prostaglandin by the uterus and hypothalamus. Eur. J. Pharmacol. 1980, 62:309-317.
27. Glattre E., Bjerkedal T. The 24-hour rhythmicity of birth: a population study. Acta Obstet. Gynecol. Scand. 1983, 62:31-36.
28. Goto M., Oshima I., Tomita T., Ebihara S. Melatonin content of the pineal gland in different mouse strains. J. Pineal Res. 1989, 7:195-204.
29. Goto M., Oshima I., Hasegawa M., Ebihara S. The locus controlling pineal serotonin N-acetyltransferase activity (Nat-2) is located on mouse chromosome 11. Brain Res. Mol. Brain Res. 1994, 21:349-354.
30. Gravett M.G., Rubens C.E., Nunes T.M. Global report on preterm birth and stillbirth (2 of 7): discovery science. BMC Pregnancy Childbirth 2010, 10(Suppl. 1):S2.
31. Hastings M., O'Neill J.S., Maywood E.S. Circadian clocks: regulators of endocrine and metabolic rhythms. J. Endocrinol. 2007, 195:187-198.
32. Havelock J.C., Keller P., Muleba N., Mayhew B.A., Casey B.M., Rainey W.E., Word R.A. Human myometrial gene expression before and during parturition. Biol. Reprod. 2005, 72:707-719.
33. He P.J., Hirata M., Yamauchi N., Hashimoto S., Hattori M. The disruption of circadian clockwork in differentiating cells from rat reproductive tissues as identified by in vitro real-time monitoring system. J. Endocrinol. 2007, 193:413-420.
34. He P.J., Hirata M., Yamauchi N., Hattori M. Up-regulation of Per1 expression by estradiol and progesterone in the rat uterus. J. Endocrinol. 2007, 194:511-519.
35. Hertz-Eshel M., Rahamimoff R. Effect of melatonin on uterine contractility. Life Sci. 1965, 4:1367-1372.
36. Hirata M., He P.J., Shibuya N., Uchikawa M., Yamauchi N., Hashimoto S., Hattori M. Progesterone, but not estradiol, synchronizes circadian oscillator in the uterus endometrial stromal cells. Mol. Cell. Biochem. 2009, 324:31-38.
37. Horard B., Rayet B., Triqueneaux G., Laudet V., Delaunay F., Vanacker J.-M. Expression of the orphan nuclear receptor ERRα is under circadian regulation in estrogen-responsive tissues. J Mol. Endocrinol. 2004, 33:87-97.
38. Imbesi M., Dirim D.A., Yildiz S., Sharma R., Gavin D., Tun N., Manev H., Uz T. The melatonin receptor MT1 is required for the differential regulatory actions of melatonin on neuronal clock gene expression in striatal neurons in vitro. J. Pineal Res. 2009, 46:87-94.
39. Junkermann H., Mangold H., Vecsei P., Runnenbaum B. Circadian rhythm of serum progesterone levels in human pregnancy and its relation to the rhythm of cortisol. Acta Endocrinol. 1982, 101:98-104.
40. Kalantaridou S.N., Zoumakis E., Makrigiannakis A., Lavasidis L.G., Vrekoussis T., Chrousos G.P. Corticotropin-releasing hormone, stress and human reproduction: an update. J. Repro. Immun. 2010, 85:33-39.
41. Kasahara T., Abe K., Mekada K., Yoshiki A., Kato T. Genetic variation of melatonin productivity in laboratory mice under domestication. Proc. Natl. Acad. Sci. USA 2010, 107:6412-6417.
42. Kennaway D.J., Boden M.J., Voultsios A. Reproductive performance in female ClockΔ19 mutant mice. Reprod. Fertil. Dev. 2005, 16:801-810.
43. Kiessling S., Eichele G., Oster H. Adrenal glucocorticoids have a key role in circadian resynchronization in a mouse model of jet lag. J. Clin. Invest. 2010, 120:2600-2609.
44. Kivela A. Serum melatonin during human pregnancy. Acta Endocrinol. 1991, 124:233-237.
45. Leake R.D., Weitzman R.E., Glatz T.H., Fisher D.A. Plasma oxytocin cincentratins in men, nonpregnant women and pregnant women before and during spontaneous labor. J. Clin. Endocrinol. Metab. 1981, 53:730-733.
46. Lincoln D.W., Porter D.G. Timing of the photoperiod and the hour of birth in rats. Nature 1976, 260:780-781.
47. Lindow S.W., Jha R.R., Thompson J.W. 24-hour rhythm to the onset of preterm labour. Br. J. Obstet. Gynecol. 2000, 107:1145-1148.
48. Lipschitz D.L., Crowley W.R., Bealer S.L. Central blockade of oxytocin receptors during late gestation disrupts systemic release of oxytocin during suckling in rats. J. Neuroendocrin. 2003, 15:743-748.
49. Martensson L.G., Andersson R.G., Berg G. Melatonin together with noradrenaline augments contractions of human myometrium. Eur. J. Pharmacol. 1996, 316:273-275.
50. Mendelson C.R. Minireview: Fetal-maternal hormonal signaling in pregnancy and labor. Mol. Endocrinol. 2009, 23:947-954.
51. Messager S., Hazlerigg D.G., Mercer J.G., Morgan P.J. Photoperiod differentially regulates the expression of Per1 and ICER in the pars tuberalis and the suprachiasmatic nucleus of the Siberian hamster. Eur. J. Neurosci. 2000, 12:2865-2870.
52. Miller B., Olson S., Turek F., Levine J., Horton T., Takahashi J. Circadian clock mutation disrupts estrous cyclicity and maintenance of pregnancy. Curr. Biol. 2004, 14:1367-1373.
53. Mitchell B.F., Taggart M.J. Are animal models relevant to key aspects of human parturition?. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 297:R525-545.
54. Nakamura T.J., Moriya T., Inoue S., Shimazoe T., Watanabe S., Ebihara S., Shinohara K. Estrogen differentially regulates expression of Per1 and Per2 genes between central and peripheral clocks and between reproductive and nonreproductive tissues in female rats. J. Neurosci. Res. 2005, 82:622-630.
55. Nakamura T.J., Sellix M.T., Menaker M., Block G.D. Estrogen directly modulates circadian rhythms of PER2 expression in the uterus. Amer. J. Physiol. Endocrinol. Metab. 2008, 295:E1025-1031.
56. Nakamura T.J., Sellix M.T., Kudo T., Yoshimura T., Ebihara S., Colwell C.S., Block G.D. Influence of the estrous cycle on clock gene expression in reproductive tissues: Effects of fluctuating ovarian steroid hormone levels. Steroids 2010, 75:203-212.
57. Nathanielsz P.W., Giussani D.A., Mecenas C.A., Wu W., Winter J.A., Garcia-Villar R., Baguma-Nibasheka M., Honnebier M.B.O.M., McDonald T.J. Regulation of the switch from myometrial contractures to contractions in late pregnancy: Studies in the pregnant sheep and monkey. Reprod. Fertil. Dev. 1995, 7:595-602.
58. Nishimori K., Youn L.J., Guo Q., Wang Z., Insel T.R., Matzuk M.M. Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc. Natl. Acad. Sci. USA 1996, 93:11699-11704.
59. Petraglia F., Imperatore A., Challis J.R.G. Neuroendocrine mechanisms in pregnancy and parturition. Endocr. Rev. 2010, 31:783-816.
60. Plaut S.M., Grota L.J., Ader R., Graham C.W. Effects of handling and the light-dark cycle on time of parturition in the rat. Lab. Anim. Care 1970, 20:447-453.
61. Prasai M.J., Pernicova I., Grant P.J., Scott E.M. An endocrinologists guide to the clock. J. Clin. Endocrinal. Metab. 2011, 96:913-922.
62. Reppert S.M., Henshaw D., Schwartz W.J., Weaver D.R. The circadian-gated timing of birth in rats: disruption by maternal SCN lesions or by removal of the fetal brain. Brain Res. 1987, 403:398-402.
63. Reppert S.M., Weaver D.R. Coordination of circadian timing in mammals. Nature 2002, 418:935-941.
64. Ratajczak C.J., Herzog E.D., Muglia L.J. Clock gene expression in gravid uterus and extra-embryonic tissues furing late gestation in the mouse. Reprod. Fertil. Dev. 2010, 22:743-750.
65. Roizen J., Luedke C.E., Herzog E.D., Muglia L.J. Oxytocin in the circadian timing of birth. PLoS ONE 2007, 2:e922.
66. Romero R., Kuivaniemi H., Tromp G. Functional genomics and proteomics in term and preterm parturition. J. Clin. Endocrinol. Metab. 2002, 87:2431-2434.
67. Schlabritz-Loutsevitch N., Hellner N., Middendorf R., Muller D., Olcese J. The human myometrium as a target for melatonin. J. Clin. Endocrinol. Metab. 2003, 88:908-913.
68. Sharkey J.T., Puttaramu R., Word R.A., Olcese J. Melatonin synergizes with oxytocin to enhance contractility of human myometrial smooth muscle cells. J. Clin. Endocrinol. Metab. 2009, 94:421-427.
69. Sharkey J., Cable C., Olcese J. Melatonin sensitizes human myometrial cells to oxytocin in a PKCα/ERK-dependent manner. J. Clin. Endocrinol. Metab. 2010, 95:2902-2908.
70. Siegel H.I., Greenwald G.S. Prepartum onset of maternal behavior in hamsters and the effects of estrogen and progesterone. Horm. Behav. 1975, 6:237-245.
71. Smith R., Nicholson R.C. Corticotropin releasing hormone and the timing of birth. Front. Biosci. 2007, 12:912-918.
72. Sparey C., Robson S.C., Bailey J., Lyall F., Europe-Finner G.N. The differential expression of myometrial connexin-43, cyclooxygenase-1 and -2, and Gsa proteins in the upper and lower segments of the human uterus during pregnancy and labor. J. Clin. Endocrinol. Metab. 1999, 84:1705-1710.
73. Steffens F., Zhou X.-B., Sausbier U., Motejlek K., Knaus H.-G., Ruth P., Olcese J., Korth M., Wieland T. Melatonin receptor signalling in pregnant and nonpregnant rat uterine myocytes as probed by BKCa channel activity. Mol. Endocrinol. 2003, 17:2103-2115.
74. Takayama H., Nakamura Y., Tamura H., Yamaagata Y., Harada A., Nakata M., Sugino N., Kato H. Pineal gland (melatonin) affects the parturition time, but not luteal function and fetal growth, in pregnant rats. Endocrine J. 2003, 50:37-43.
75. Takayanagi Y., Yoshida M., Bielsky I.F., Ross H.E., Kawamata M., Onaka T., Yanagisawa T., Kimura T., Matzuk M.M., Young L.J., Nishimori K. Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc. Natl. Acad. Sci. USA 2005, 102:16096-16101.
76. Thornton S., Davison J.M., Baylis P.H. Plasma oxytocin during the first and second stages of spontaneous human labour. Acta Endocrinol. 1992, 126:425-429.
77. Vatish M., Steer P.J., Blanks A.M., Hon M., Thornton S. Diurnal variation is lost in preterm deliveries before 28 weeks of gestation. Br. J. Obstet. Gynecol. 2010, 117:765-767.
78. von Gall C., Garabette M.L., Kell C.A., Frenzel S., Dehghani F., Schumm-Draeger P.M., Weaver D.R., Korf H.W., Hastings M.H., Stehle J.H. Rhythmic gene expression in pituitary depends on heterologous sensitization by the neurohormone melatonin. Nat. Neurosci. 2002, 5:234-238.
79. Wierrani F., Grin W., Hlawaka B., Kroiss A., Gruenberger W. Elevated serum melatonin levels during human late pregnancy and labour. J. Obstet. Gynecol. 1997, 17:449-451.
80. Wu K.K. Control of cyclooxygenase-2 transcriptional activation by pro-inflammatory mediators. Prostagl. Leukotr. Essent. Fatty Acids 2005, 72:89-93.
81. Yamazaki S., Numano R., Abe M., Hida A., Takahashi R., Ueda M., Block G.D., Sakaki Y., Menaker M., Tei H. Resetting central and peripheral circadian oscillators in transgenic rats. Science 2000, 288:682-685.
82. Young R.C. Myocytes, myometrium and uterine contractions. Ann. N.Y. Acad. Sci. 2007, 1101:72-84.
83. Young W.S., Shepard E., Amico J., Henninghausen L., Wagner K.U., LaMarca M.E., McKinney C., Ginns E.I. Deficiency in mouse oxytocin prevents milk ejection, but not fertility or parturition. J. Neuroendocrin. 1996, 8:847-853.
84. Zakar T., Hertelendy F. Progesterone withdrawal: key to parturition. Am. J. Obstet. Gynecol. 2007, 196:289-296.
85. Zahn V., Hattensperger W. Circadian rhythm of pregnancy contractions. Z. Geburtshilfe Perinatol. 1993, 197:1-10.
86. Zhao H., Poon A.M., Pang S.F. Pharmacological characterization, molecular subtyping, and autoradiographic localization of putative melatonin receptors in the uterine endometrium of estrous rats. Life Sci. 2000, 66:1581-1591.