Circadian rhythms in the fetus

Molecular and Cellular Endocrinology

Volumn 349, Issue 1, 2012, Pages 68-75

  Serón Ferré, María ^a   Mendez, Natalia ^b   Abarzua Catalan, Lorena ^b   Vilches, Nelson ^a   Valenzuela, Francisco J ^a   Reynolds, Henry E ^a   Llanos, Aníbal J ^a   Rojas, Auristela ^a   Valenzuela, Guillermo J ^c   Torres Farfan, Claudia ^b  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^c ARROWHEAD REGIONAL MEDICAL CENTER   (United States)

Author keywords

Clock genes; Fetal adrenal function; Fetal programming; Maternal melatonin; Peripheral oscillator

Indexed keywords

CRYPTOCHROME 1; CRYPTOCHROME 2; MELATONIN; MESSENGER RNA; PER1 PROTEIN; PER2 PROTEIN; PROTEIN BMAL1; TRANSCRIPTION FACTOR CLOCK;

ADRENAL FUNCTION; BMAL1 GENE; CIRCADIAN RHYTHM; CLOCK GENE; CRY1 GENE; CRY2 GENE; FETUS; FETUS DEVELOPMENT; GENE; GESTATION PERIOD; HUMAN; HYPOTHALAMUS; MATERNAL BLOOD; NONHUMAN; ONTOGENY; PER1 GENE; PER2 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS;

ADRENAL GLANDS; ANIMALS; CIRCADIAN RHYTHM; FEMALE; FETUS; HUMANS; MATERNAL-FETAL EXCHANGE; MELATONIN; PREGNANCY; SUPRACHIASMATIC NUCLEUS;

EID: 84860423634     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.07.039     Document Type: Review

References (63)

1. Adam C.L., Kyle C.E., Young P. Influence of prenatal photoperiod on postnatal reproductive development in male red deer (Cervus elaphus). J. Reprod. Fertil. 1994, 100:607-611.
2. Ansari N., Agathagelidis M., Lee C., Korf H.W., von Gall C. Differential maturation of circadian rhythms in clock gene proteins in the suprachiasmatic nucleus and the pars tuberalis during mouse ontogeny. Eur. J. Neurosci. 2009, 29:477-489.
3. Bauer J., Janecke A., Gerss J., Masjosthusmann K., Werner C., Hoffmann G. Circadian variation on oxygen consumption in preterm infants. J. Perinat. Med. 2009, 37:413-417.
4. Bass J., Takahashi J.S. Circadian integration of metabolism and energetics. Science 2010, 330:1349-1354.
5. Bellavia S.L., Carpentieri A.R., Vaque A.M., Macchione A.F., Vermouth N.T. Pup circadian rhythm entrainment-effect of maternal ganglionectomy or pinealectomy. Physiol. Behav. 2006, 89:342-349.
6. Brunton P.J. Resetting the dynamic range of hypothalamic-pituitary-adrenal axis stress responses through pregnancy. J. Neuroendocrinol. 2010, 11:1198-1213.
7. Constandil L., Parraguez V.H., Torrealba F., Valenzuela G., Serón-Ferré M. Day-night changes in c-fos expression in the fetal sheep suprachiasmatic nucleus at late gestation. Reprod. Fertil. Dev. 1995, 7:411-413.
8. Deguchi T. Ontogenesis of a biological clock for serotonin:acetyl coenzyme A N-acetyltransferase in pineal gland of rat. Proc. Natl. Acad. Sci. USA 1975, 72:2814-2818.
9. Dolatshad H., Cary A.J., Davis F.C. Differential expression of the circadian clock in maternal and embryonic tissues of mice. PLoS One 2010, 5:e9855.
10. Damiola F., Le Minh N., Preitner N., Kornmann B., Fleury-Olela F., Schibler U. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 2000, 14:2950-2961.
11. Davis F.C., Gorski R.A. Development of hamster circadian rhythms. I. Within-litter synchrony of mother and pups activity rhythms at weaning. Biol. Reprod. 1985, 33:353-362.
12. Davis F.C., Reppert S.M. Development of mammalian circadian rhythms. Handbook of Behavioral Neurobiology 2001, vol. Vol 12:247-290. Kluwer Academic/Plenum Publishers, Circadian Clocks. New York.
13. Ebling F.J., Wood R.I., Suttie J.M., Adel T.E., Foster D.L. Prenatal photoperiod influences neonatal prolactin secretion in the sheep. Endocrinology 1989, 125:384-391.
14. El-Hennamy R., Mateju K., Bendová Z., Sosniyenko S., Sumová A. Maternal control of the fetal and neonatal rat suprachiasmatic nucleus. J. Biol. Rhythms. 2008, 23:435-444.
15. Entringer S., Buss C., Wadhwa P.D. Prenatal stress and developmental programming of human health and disease risk: concepts and integration of empirical findings. Curr. Opin. Endocrinol. Diabetes Obes. 2010, 17:507-516.
16. Gorman M.R., Goldman B.D., Zucker I. Mammalian photoperiodism. Handbook of Behavioral Neurobiology 2001, vol. 12:481-528. Kluwer Academic/Plenum Publishers, Circadian Clocks. New York.
17. Johnson, M.H., Lim, A., Fernando, D., Day, M.L., 2002. Circadian clockwork genes are expressed in the reproductive tract and conceptus of the early pregnant mouse. Reprod. Biomed. Online. 4140:145.
18. Johnston J.D., Ebling F.J., Hazlerigg D.G. Photoperiod regulates multiple gene expression in the suprachiasmatic nuclei and pars tuberalis of the Siberian hamster (Phodopus sungorus). Eur. J. Neurosci. 2005, 21:2967-2974.
19. Jud C., Albrecht U. Circadian rhythms in murine pups develop in absence of a functional maternal circadian clock. J. Biol. Rhythms. 2006, 21:149-154.
20. Kennaway D.J., Stamp G.E., Goble F.C. Development of melatonin production in infants and the impact of prematurity. J. Clin. Endocrinol. Metab. 1992, 75:367-369.
21. Kennaway D.J., Goble F.C., Stamp G.E. Factors influencing the development of melatonin rhythmicity in humans. J. Clin. Endocrinol. Metab. 1996, 81:1525-1532.
22. Kittrell E.M., Satinoff E. Diurnal rhythms of body temperature, drinking and activity over reproductive cycles. Physiol. Behav. 1988, 42:477-484.
23. Ko M.S., Kitchen J.R., Wang X., Threat T.A., Wang X., Hasegawa A., Sun T., Grahovac M.J., Kargul G.J., Lim M.K., Cui Y., Sano Y., Tanaka T., Liang Y., Mason S., Paonessa P.D., Sauls A.D., DePalma G.E., Sharara R., Rowe L.B., Eppig J., Morrell C., Doi H. Large-scale cDNA analysis reveals phased gene expression patterns during preimplantation mouse development. Development 2000, 127:1737-1749.
24. Li X., Davis F.C. Developmental expression of clock genes in the Syrian hamster. Brain Res. Dev. Brain Res. 2005, 158:31-40.
25. Liggins G.C. The role of cortisol in preparing the fetus for birth. Reprod. Fertil. Dev. 1994, 6:141-150.
26. Lincoln G., Messager S., Andersson H., Hazlerigg D. Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: evidence for an internal coincidence timer. Proc. Natl. Acad. Sci. USA 2002, 99:13890-13895.
27. McCurdy C.E., Bishop J.M., Williams S.M., Grayson B.E., Smith M.S., Friedman J.E., Grove K.L. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J. Clin. Invest. 2009, 119:323-335.
28. Matsumoto, T., Hess D.L., Kaushal, K.M., Valenzuela, G.J., Yellon, S.M., Ducsay, C.A., 1991. Circadian myometrial and endocrine rhythms in the pregnant rhesus macaque: effects of of constant light and timed melatonin infusion. Am. J. Obstet. Gynecol. 165(6 Pt 1):1777-1784.
29. McMillen I.C., Nowak R. Maternal pinealectomy abolishes the diurnal rhythm in plasma melatonin concentrations in the fetal sheep, pregnant ewe during late gestation. J. Endocrinol. 1989, 120:459-464.
30. Mirmiran M., Kok J.H., de Kleine M.J.K., Koppe J.G., Overdijk J., Witting W. Circadian rhythms in preterm infants: a preliminary study. Early Hum. Dev. 1990, 23:139-146.
31. Nováková M., Sládek M., Sumová A. Exposure of pregnant rats to restricted feeding schedule synchronizes the SCN clocks of their fetuses under constant light but not under a light-dark regime. J. Biol. Rhythms. 2010, 25:350-360.
32. Ohta H., Xu S., Moriya T., Ligo M., Watanabe T., Nakahata N., Chisaka H., Hanita T., Matsuda T., Ohura T., Kimura Y., Yaegashi N., Tsuchiya S., Tei H., Okamura K. Maternal feeding controls fetal biological clock. PLoS One 2008, 3:e2601.
33. Oishi K., Sakamoto K., Okada T., Nagase T., Ishida N. Antiphase circadian expression between BMAL1 and period homologue mRNA in the suprachiasmatic nucleus and peripheral tissues of rats. Biochem. Biophys. Res. Commun. 1998, 253:199-203.
34. O'Neill J.S., Reddy A.B. Circadian clocks in human red blood cells. Nature 2011, 469:498-503.
35. Reppert S.M., Schwartz W.J. Maternal coordination of the fetal biological clock in utero. Science 1983, 220:969-971.
36. Reppert S.M., Schwartz W.J. Functional activity of the suprachiasmatic nuclei in the fetal primate. Neurosci. Lett. 1984, 46:145-149.
37. Saxena M.T., Aton S.J., Hildebolt C., Prior J.L., Abraham U., Piwnica-Worms D., Herzog E.D. Bioluminescence imaging of period1 gene expression in utero. Mol. Imaging 2007, 6:68-72.
38. Schrader J.A., Walaszczyk E.J., Smale L. Changing patterns of daily rhythmicity across reproductive states in diurnal female Nile grass rats (Arvicanthis niloticus). Physiol. Behav. 2009, 98:547-556.
39. Schrader J.A., Nunez A.A., Smale L. Changes in and dorsal to the rat suprachiasmatic nucleus during early pregnancy. Neuroscience 2010, 171:513-523.
40. Serón-Ferré M., Ducsay C.A., Valenzuela G.J. Circadian rhythms during pregnancy. Endocr. Rev. 1993, 14:594-609.
41. Serón-Ferré M., Riffo R., Valenzuela G.J., Germain A.M. Twenty-four-hour pattern of cortisol in the human fetus at term. Am. J. Obstet. Gynecol. 2001, 184:1278-1283.
42. Serón-Ferré M., Torres-Farfan C., Forcelledo M.L., Valenzuela G.J. The development of circadian rhythms in the fetus and neonate. Semin. Perinatol. 2001, 25:363-370.
43. Serón-Ferré M., Valenzuela G.J., Torres-Farfan C. Circadian clocks during embryonic and fetal development. Birth Defects Res. C Embryo Today 2007, 81:204-214.
44. Shimomura H., Moriya T., Sudo M., Wakamatsu H., Akiyama M., Miyake Y., Shibata S. Differential daily expression of Per1 and Per2 mRNA in the suprachiasmatic nucleus of fetal and early postnatal mice. Eur. J. Neurosci. 2001, 13:687-693.
45. Sladek M., Jindrakova Z., Bendova Z., Sumova A. Postnatal ontogenesis of the circadian clock within the rat liver. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R1224-R1229.
46. Sladek M., Sumova A., Kovacikova Z., Bendova Z., Laurinova K., Illnerova H. Insight into molecular core clock mechanism of embryonic and early postnatal rat suprachiasmatic nucleus. Proc. Natl. Acad. Sci. USA 2004, 101:6231-6236.
47. Sumová, A., Bendová, Z., Sládek, M., El-Hennamy, R., Matejů, K., Polidarová, L., Sosniyenko, S., Illnerová, H., 2008. Circadian molecular clocks tick along ontogenesis. Physiol. Res. 57 Suppl 3:S139-S148.
48. Suter M., Bocock P., Showalter L., Hu M., Shope C., McKnight R., Grove K., Lane R., Aagaard-Tillery K. Epigenomics: maternal high-fat diet exposure in utero disrupts peripheral circadian gene expression in nonhuman primates. FASEB J. 2011, 25:714-726.
49. Sutton G.M., Centanni A.V., Butler A.A. Protein malnutrition during pregnancy in C57BL/6J mice results in offspring with altered circadian physiology before obesity. Endocrinology 2010, 151:1570-1580.
50. Tamura H., Nakamura Y., Terron M.P., Flores L.J., Manchester L.C., Tan D.X., Sugino N., Reiter R.J. Melatonin and pregnancy in the human. Reprod. Toxicol. 2008, 25:291-303.
51. Thomas L., Purvis C.C., Drew J.E., Abramovich D.R., Williams L.M. Melatonin receptors in human fetal brain: 2-[(125)I]iodomelatonin binding and MT1 gene expression. J. Pineal Res. 2002, 33:218-224.
52. Torres-Farfan C., Mendez N., Abarzua-Catalan L., Vilches N., Valenzuela G.J., Serón-Ferré M. A circadian clock cntrained by melatonin is ticking in the rat fetal adrenal. Endocrinology 2011, 152:1891-1900.
53. Torres-Farfan C., Rocco V., Monso C., Valenzuela F.J., Campino C., Germain A., Torrealba F., Valenzuela G.J., Serón-Ferré M. Maternal melatonin effects on clock gene expression in a nonhuman primate fetus. Endocrinology 2006, 147:4618-4626.
54. Torres-Farfan C., Richter H.G., Germain A.M., Valenzuela G.J., Campino C., Rojas-García P., Forcelledo M.L., Torrealba F., Serón-Ferré M. Maternal melatonin selectively inhibits cortisol production in the primate fetal adrenal gland. J. Physiol. 2004, 554:841-856.
55. Valenzuela F.J., Torres-Farfan C., Richter H.G., Mendez N., Campino C., Torrealba F., Valenzuela G.J., Serón-Ferré M. Clock gene expression in adult primate suprachiasmatic nuclei and adrenal: is the adrenal a peripheral clock responsive to melatonin?. Endocrinology 2008, 149:1454-1561.
56. Varcoe T.J., Wight N., Voultsios A., Salkeld M.D., Kennaway D.J. Chronic phase shifts of the photoperiod throughout pregnancy programs glucose Intolerance and insulin resistance in the rat. PLoS One 2011, 6:e18504.
57. Vujovic N., Davidson A.J., Menaker M. Sympathetic input modulates, but does not determine, phase of peripheral circadian oscillators. Am. J. Physiol. Regul Integr. Comp. Physiol. 2008, 295:R355-R360.
58. Watanabe T., Kojima M., Tomida S., Nakamura T.J., Yamamura T., Nakao N., Yasuo S., Yoshimura T., Ebihara S. Peripheral clock gene expression in CS mice with bimodal locomotor rhythms. Neurosci. Res. 2006, 54:295-301.
59. Weerth C., Buitelaar J.K. Physiological stress reactivity in human pregnancy-a review. Neurosci. Biobehav. Rev. 2005, 29:295-312.
60. Weinert D. Ontogenetic development of the mammalian circadian system. Chronobiol. Int. 2005, 22:179-205.
61. Yamazaki S., Yoshikawa T., Biscoe E.W., Numano R., Gallaspy L.M., Soulsby S., Papadimas E., Pezuk P., Doyle S.E., Tei H., Sakaki Y., Block G.D., Menaker M. Ontogeny of circadian organization in the rat. J. Biol. Rhythms. 2009, 24:55-63.
62. Zhu J.L., Hjollund N.H., Andersen A.M., Olsen J. Shift work, job stress, and late fetal loss: The National Birth Cohort in Denmark. J. Occup. Environ. Med. 2004, 46:1144-1149.
63. Zylka M.J., Shearman L.P., Weaver D.R., Reppert S.M. Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron 1998, 20:1103-1110.