Circadian clocks during embryonic and fetal development

Birth Defects Research Part C - Embryo Today: Reviews

Volumn 81, Issue 3, 2007, Pages 204-214

  Seron Ferre, Maria ^a,b,d   Valenzuela, Gullermo J ^c   Torres Farfan, Claudia ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSIDAD DE TARAPACÁ   (Chile)

^c ARROWHEAD REGIONAL MEDICAL CENTER   (United States)

^d NONE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

MELATONIN;

BMAL 1 GENE; CELL FUNCTION; CIRCADIAN RHYTHM; CLOCK GENE; CRY1 GENE; CRY2 GENE; EMBRYO DEVELOPMENT; FETUS DEVELOPMENT; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HYPOTHALAMUS; MAMMAL; NONHUMAN; PER1 GENE; PER2 GENE; PERINATAL PERIOD; PREGNANCY; PRIORITY JOURNAL; REVIEW; SUPRACHIASMATIC NUCLEUS;

ANIMALS; BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; EMBRYO, MAMMALIAN; FEMALE; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MELATONIN; MODELS, BIOLOGICAL; OSCILLOMETRY; PREGNANCY; SUPRACHIASMATIC NUCLEUS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

MAMMALIA; PRIMATES; RATTUS;

EID: 36049004974     PISSN: 1542975X     EISSN: None     Source Type: Journal    
DOI: 10.1002/bdrc.20101     Document Type: Review

References (107)

1. Adam CL, Kyle CE, Young P. 1994. Influence of prenatal photoperiod on postnatal reproductive development in male red deer (Cervus elaphus). J Reprod Fertil 100:607-611.
2. Alonso-Vale MI, Andreotti S, Peres SB, et al. 2005. Melatonin enhances leptin expression by rat adipocytes in the presence of insulin. Am J Physiol Endocrinol Metab 288:E805-E812.
3. Balsalobre A, Brown SA, Marcacci L, et al. 2000. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289:2344-2347.
4. Balsalobre A. 2002. Clock genes in mammalian peripheral tissues. Cell Tissue Res 309:193-199.
5. Barker DJ, Bagby SP, Hanson MA. 2006. Mechanisms of disease: in utero programming in the pathogenesis of hypertension. Nat Clin Pract Nephrol 2:700-707.
6. Bellavia SL, Carpentieri AR, Vaque AM, et al. 2006. Pup circadian rhythm entrainment - effect of maternal ganglionectomy or pinealectomy. Physiol Behav 89:342-349.
7. Boden MJ, Kennaway DJ. 2006. Circadian rhythms and reproduction. Reproduction 132:379-392.
8. Breen S, Rees S, Walker D. 1996. The development of diurnal rhythmicity in fetal suprachiasmatic neurons as demonstrated by fos immunohistochemistry. Neuroscience 74:917-926.
9. Cannon B, Nedergaard J. 2004. Brown adipose tissue: function and physiological significance. Physiol Rev 84:277-359.
10. Caldelas I, Tejadilla D, Gonzalez B, et al. 2007. Diurnal pattern of clock gene expression in the hypothalamus of the newborn rabbit. Neuroscience 144:395-401.
11. Chen ST, Choo KB, Hou MF, et al. 2005. Deregulated expression of the PER1, PER2 and PER3 genes in breast cancers. Carcinogenesis 26:1241-1246.
12. Constandil L, Parraguez VH, Torrealba F, et al. 1995. Day-night changes in c-fos expression in the fetal sheep suprachiasmatic nucleus at late gestation. Reprod Fertil Dev 7:411-413.
13. Croteau A, Marcoux S, Brisson C. 2006. Work activity in pregnancy, preventive measures, and the risk of delivering a small-for-gestational-age infant. Am J Public Health 96:846-855.
14. Davis FC, Gorski RA. 1985. Development of hamster circadian rhythms. I. Within-litter synchrony of mother and pups activity rhythms at weaning. Biol Reprod 33:353-362.
15. Davis FC, Mannion J. 1988. Entrainment of hamster pup circadian rhythms by prenatal melatonin injections to the mother. Am J Physiol 255:439-448.
16. Davis FC, Reppert SM. 2001. Development of mammalian circadian rhythms. In: Takahashi JS, Turek FW, Moore RY, editors. Handbook of Behavioral Neurobiology. Vol 12. Circadian Clocks. New York: Kluwer Academic/Plenum Publishers. pp. 247-290.
17. Damiola F, Le Minh N, Preitner N, et al. 2000. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14:2950-2961.
18. Deguchi T. 1975. Ontogenesis of a biological clock for serotonin: acetyl coenzyme A N-acetyltransferase in pineal gland of rat. Proc Natl Acad Sci USA 72:2814-2818.
19. Drew JE, Williams LM, Hannah LT, et al. 1998. Melatonin receptors in the human fetal kidney: 2-[125I]iodomelatonin binding sites correlated with expression of Mel1a and Mel1b receptor genes. J Endocrinol 156:261-267.
20. Ebling FJ, Wood RI, Suttie JM, et al. 1989. Prenatal photoperiod influences neonatal prolactin secretion in the sheep. Endocrinology 125:384-391.
21. Edery I. 2000. Circadian rhythms in a nutshell. Physiol Genomics 3:59-74.
22. Fahrenkrug J, Georg B, Hannibal J, et al. 2006. Diurnal rhythmicity of the clock genes Per1 and Per2 in the rat ovary. Endocrinology 147:3769-3776.
23. Fowden AL, Giussani DA, Forhead AJ. 2006. Intrauterine programming of physiological systems: causes and consequences. Physiology 21:29-37.
24. Gonzalez-Mariscal G. 2007. Mother rabbits and their offspring: timing is everything. Dev Psychobiol 49:71-76.
25. Gorman MR, Goldman BD, Zucker I. 2001. Mammalian photoperiodism. In: Takahashi JS, Turek FW, Moore RY, editors.Handbook of Behavioral Neurobiology. Vol 12. Circadian Clocks. New York: Kluwer Academic/Plenum Publishers. pp. 481-528.
26. Grechez-Cassiau A, Panda S, Lacoche S, et al. 2004. The transcriptional repressor STRA13 regulates a subset of peripheral circadian outputs. J Biol Chem 279:1141-1150.
27. Grumbach MM, Kaplan SL. 1998. The pituitary. In: Polin RA, Fox WW, editors. Fetal and Neonatal Physiology. 2nd ed. Philadelphia: WB Saunders. pp. 2395-2442.
28. Guo H, Brewer JM, Champhekar A, et al. 2005. Differential control of peripheral circadian rhythms by suprachiasmatic-dependent neural signals. Proc Natl Acad Sci USA 102:3111-3116.
29. Guo H, Brewer JM, Lehman MN, Bittman EL. 2006. Suprachiasmatic regulation of circadian rhythms of gene expression in hamster peripheral organs: effects of transplanting the pacemaker. J Neurosci 26:6406-6412.
30. Hammer F, Stewart PM. 2006. Cortisol metabolism in hypertension. Best Pract Res Clin Endocrinol Metab 20:337-353.
31. Honma S, Kawamoto T, Takagi Y, et al. 2002. Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature 419:841-844.
32. Horard B, Rayet B, Triqueneaux G, et al. 2004. Expression of the orphan nuclear receptor ERRalpha is under circadian regulation in estrogen-responsive tissues. J Mol Endocrinol 33:87-97.
33. Ishida A, Mutoh T, Ueyama T, et al. 2005. Light activates the adrenal gland: timing of gene expression and glucocorticoids release. Cell Metab 2:297-307.
34. Jan JE, Wasdell MB, Freeman RD, Bax M. 2007. Evidence supporting the use of melatonin in short gestation infants. J Pineal Res 42:22-27.
35. Johnson MH, Lim A, Fernando D, Day ML. 2002. Circadian clockwork genes are expressed in the reproductive tract and conceptus of the early pregnant mouse. Reprod Biomed Online 4:140-145.
36. Johnston JD, Ebling FJ, Hazlerigg DG. 2005. Photoperiod regulates multiple gene expression in the suprachiasmatic nuclei and pars tuberalis of the Siberian hamster (Phodopus sungorus). Eur J Neurosci 21:2967-2974.
37. Johnston JD, Schuster C, Barrett P, Hazlerigg DG. 2007. Regulation of the ovine MT1 melatonin receptor promoter: interaction between multiple pituitary transcription factors at different phases of development. Mol Cell Endocrinol 268:59-66.
38. Jones CR, Campbell SS, Zone SE, et al. 1999. Familial advanced sleep-phase syndrome: a short-period circadian rhythm variant in humans. Nat Med 5:1062-1065.
39. Jud C, Albrecht U. 2006. Circadian rhythms in murine pups develop in absence of a functional maternal circadian clock. J Biol Rhythms 21:149-154.
40. Karlsson B, Knutsson A, Lindahl B. 2001. Is there an association between shift work and having a metabolic syndrome? Results from a population based study of 27,485 people. Occup Environ Med 58:747-752.
41. Karman BN, Tischkau SA. 2006. Circadian clock gene expression in the ovary: effects of luteinizing hormone. Biol Reprod 75:624-632.
42. Kennaway DJ, Stamp GE, Goble FC. 1992. Development of melatonin production in infants and the impact of prematurity. J Clin Endocrinol Metab 75:367-379.
43. Kennaway DJ, Varcoe TJ, Mau VJ. 2003. Rhythmic expression of clock and clock-controlled genes in the rat oviduct. Mol Hum Reprod 9:503-507.
44. Ko MS, Kitchen JR, Wang X, et al. 2000. Large-scale cDNA analysis reveals phased gene expression patterns during preimplantation mouse development. Development 127:1737-1749.
45. Krieger DT, Hauser H, Krey LC. 1977. Suprachiasmatic nuclear lesions do not abolish food-shifted circadian adrenal and temperature rhythmicity. Science 197:398-399.
46. Le Minh N, Damiola F, Tronche F, et al. 2001 Glucocorticoid hormones inhibit food-induced phase-shifting of peripheral circadian oscillators. EMBO J 17:7128-136.
47. Lee C, Etchegaray JP, Cagampang FR, et al. 2001. Posttranslational mechanisms regulate the mammalian circadian clock. Cell 107:855-867.
48. Lemos DR, Downs JL, Urbanski HF. 2006. Twenty-four hour rhythmic gene expression in the rhesus macaque adrenal gland. Mol Endocrinol 20:1164-1176.
49. Levi F, Schibler U. 2007. Circadian rhythms: mechanisms and therapeutic implications. Annu Rev Pharmacol Toxicol 47:593-628.
50. Li X, Davis FC. 2005. Developmental expression of clock genes in the Syrian hamster. Brain Res Dev Brain Res 158:31-40.
51. Liu C, Li S, Liu T, et al. 2007. Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature 447:477-481.
52. Lincoln G, Messager S, Andersson H, Hazlerigg D. 2002. 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 99:13890-13895.
53. Lincoln GA, Andersson H, Hazlerigg D. 2003. Clock genes and the long-term regulation of prolactin secretion: evidence for a photoperiod/circannual timer in the pars tuberalis. J Neuroendocrinol 15:390-397.
54. Lowrey PL, Shimomura K, Antoch MP, et al. 2000. Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science 288:483-492.
55. Maeda Y, Muro M, Shono M, et al. 2006. Diurnal rhythms in fetal heart rate baseline and sustained fetal tachycardia in twin pregnancy. Early Hum Dev 82:637-644.
56. Merrow M, Mazzotta G, Chen Z, Roenneberg T. 2006. The right place at the right time: regulation of daily timing by phosphorylation. Genes Dev 20:2629-2633.
57. Meyer-Bernstein EL, Jetton AE, Matsumoto SI, et al. 1999. Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology 140:207-218.
58. Miller BH, McDearmon EL, Panda S, et al. 2007. Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc Natl Acad Sci USA 104:3342-3347.
59. Moore-Ede MC, Sulzman FM, Fuller CA. 1982. Characteristics of a circadiana-lock. In: The clocks that time us. Cambridge, MA: Harvard University Press. pp. 30-133.
60. Nathanielsz PW. 2006. Animal models that elucidate basic principles of the developmental origins of adult diseases. ILAR J 47:73-82.
61. Nowak R, Young IR, McMillen IC. 1990. Emergence of the diurnal rhythm in plasma melatonin concentrations in newborn lambs delivered to intact or pinealectomized ewes. J Endocrinol 125:97-102.
62. Ohta H, Honma S, Abe H, Honma K. 2002. Effects of nursing mothers on rPer1 and rPer2 circadian expressions in the neonatal rat suprachiasmatic nuclei vary with developmental stage. Eur J Neurosci 15:1953-1960.
63. Oishi K, Sakamoto K, Okada T, et al. 1998a. Antiphase circadian expression between BMAL1 and period homologue mRNA in the suprachiasmatic nucleus and peripheral tissues of rats. Biochem Biophys Res Commun 253:199-203.
64. Oishi K, Sakamoto K, Okada T, et al. 1998b Humoral signals mediate the circadian expression of rat period homologue (rPer2) mRNA in peripheral tissues. Neurosci Lett 256:117-119.
65. Oishi K, Amagai N, Shirai H, et al. 2005. Genome-wide expression analysis reveals 100 adrenal gland-dependent circadian genes in the mouse liver. DNA Res 12:191-202.
66. Okamura H, Yamaguchi S, Yagita K, 2002. Molecular machinery of the circadian clock in mammals. Cell Tissue Res 309:47-56.
67. Oster H, Damerow S, Kiessling S, et al. 2006. The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock. Cell Metab 4:163-173.
68. Panda S, Antoch MP, Miller BH, et al. 2002. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307-320.
69. Parraguez VH, Valenzuela GJ, Vergara M, et al. 1996. Effect of constant light on fetal and maternal prolactin rhythms in sheep. Endocrinology 137:2355-2361.
70. Pittendrigh C. 1981. Circadian systems: general perspective. In: Aschoff J, editor.Handbook of behavioral neurobiology. Vol. 4: Biological rhythms. New York: Plenum Press. pp. 57-80.
71. Polk DH, Fisher DA. 1998. The fetal adrenal and fetal thyroid systems In: Polin RA, Fox WW, editors. Fetal and neonatal physiology. 2nd ed. Philadelphia: WB Saunders. pp. 2460-2467.
72. Preitner N, Damiola F, Lopez-Molina L, et al. 2002. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110:251-260.
73. Recabarren MP, Valdes JL, Farias P, et al. 2005. Differential effects of infralimbic cortical lesions on temperature and locomotor activity responses to feeding in rats. Neuroscience 134:1413-1422.
74. Reppert SM, Schwartz WJ. 1983. Maternal coordination of the fetal biological clock in utero. Science 220:969-971.
75. Reppert SM, Schwartz WJ. 1984. Functional activity of the suprachiasmatic nuclei in the fetal primate. Neurosci Lett 46:145-149.
76. Reppert SM, Uhl GR. 1987 Vasopressin messenger ribonucleic acid in supraoptic and suprachiasmatic nuclei: appearance and circadian regulation during development. Endocrinology 120:2483-2487.
77. Reppert SM, Weaver DR. 2002. Coordination of circadian timing in mammals. Nature 418:935-941.
78. Richter HG, Torres-Farfan C, Rojas-García P, et al. 2004. The circadian timing system: making sense of day/night gene expression. Biol Res 37:11-28.
79. Rivkees SA. 2003. Developing circadian rhythmicity in infants. Pediatr Endocrinol Rev 1:38-45.
80. Sakamoto K, Nagase T, Fukui H, et al. 1998. Multitissue circadian expression of rat period homolog (rPer2) mRNA is governed by the mammalian circadian clock, the suprachiasmatic nucleus in the brain. J Biol Chem 273:27039-27042.
81. Saxena MT, Aton SJ, Hildebolt C, et al. 2007. Bioluminescence imaging of period 1 gene expression in utero. Mol Imaging 6:68-72.
82. Seron-Ferre M, Ducsay CA, Valenzuela GJ. 1993. Circadian rhythms during pregnancy. Endocr Rev 14:594-609.
83. Seron-Ferre M, Torres-Farfan C, Forcelledo ML, Valenzuela GJ. 2001. The development of circadian rhythms in the fetus and neonate. Semin Perinatol 25:363-370.
84. Shibata S, Moore RY. 1987. Development of neuronal activity in the rat suprachiasmatic nucleus. Brain Res 431:311-315.
85. Shimba S, Ishii N, Ohta Y, et al. 2005. Brain and muscle Arnt-like protein-1 (BMAL1), a component of the molecular clock, regulates adipogenesis. Proc Natl Acad Sci USA 102:12071-12076.
86. Shimomura H, Moriya T, Sudo M, et al. 2001. Differential daily expression of Per1 and Per2 mRNA in the suprachiasmatic nucleus of fetal and early postnatal mice. Eur J Neurosci 13:687-693.
87. Sladek M, Sumova A, Kovacikova Z, et al. 2004. Insight into molecular core clock mechanism of embryonic and early postnatal rat suprachiasmatic nucleus. Proc Natl Acad Sci USA 101:6231-6236.
88. Sladek M, Jindrakova Z, Bendova Z, Sumova A. 2007. Postnatal ontogenesis of the circadian clock within the rat liver. Am J Physiol Regul Integr Comp Physiol 292:R1224-R1229.
89. Stokkan KA, Yamazaki S, Tei H, et al. 2001. Entrainment of the circadian clock in the liver by feeding. Science 291:490-493.
90. Stratmann M, Schibler U. 2006 Properties, entrainment, and physiological functions of mammalian peripheral oscillators. J Biol Rhythms 21:494-506.
91. Thomas L, Purvis CC, Drew JE, et al. 2002. Melatonin receptors in human fetal brain: 2-[(125)I]iodomelatonin binding and MT1 gene expression. J Pineal Res 33:218-224.
92. Toh KL, Jones CR, He Y, et al. 2001. An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 291:1040-1043.
93. Torres-Farfan C, Richter HG, Germain AM, et al. 2004. Maternal melatonin selectively inhibits cortisol production in the primate fetal adrenal gland. J Physiol 554:841-856.
94. Torres-Farfan C, Rocco V, Monso C, et al. 2006a. Maternal melatonin effects on clock gene expression in a nonhuman primate fetus. Endocrinology 147:4618-4626.
95. Torres-Farfan C, Seron-Ferre M, Dinet V, Korf HW. 2006b. Immunocytochemical demonstration of day/night changes of clock gene protein levels in the murine adrenal gland: differences between melatonin-proficient (C3H) and melatonin-deficient (C57BL) mice. J Pineal Res 40:64-70.
96. Turek FW, Joshu C, Kohsaka A, et al. 2005. Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308:1043-1045.
97. Ueda HR, Hayashi S, Chen W, et al. 2005. System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat Genet 37:187-192.
98. Vanselow K, Vanselow JT, Westermark PO, et al. 2006. Differential effects of PER2 phosphorylation: molecular basis for the human familial advanced sleep phase syndrome (FASPS). Genes Dev 20:2660-2672.
99. Watanabe T, Kojima M, Tomida S, et al. 2006. Peripheral clock gene expression in CS mice with bimodal locomotor rhythms. Neurosci Res 54:295-301.
100. Weaver DR, Reppert SM. 1989. Periodic feeding of SCN-lesioned pregnant rats entrains the fetal biological clock. Brain Res Dev Brain Res 46:291-296.
101. Weaver DR, Reppert SM. 1996. The Mel1a melatonin receptor gene is expressed in human suprachiasmatic nuclei. Neuroreport 8:109-112.
102. Weinert D. 2005. Ontogenetic development of the mammalian circadian system. Chronobiol Int 22:179-205.
103. Xu Y, Toh KL, Jones CR, et al. 2007. Modeling of a human circadian mutation yields insights into clock regulation by PER2. Cell. 128:59-70.
104. Yellon SM, Longo LD. 1988. Effect of maternal pinealectomy and reverse photoperiod on the circadian melatonin rhythm in the sheep, fetus during the last trimester of pregnancy. Biol Reprod 39:1093-1099.
105. Yoo SH, Yamazaki S, Lowrey PL, et ai. 2004. PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA 101:5339-5346.
106. Zhu JL, Hjollund NH, Olsen J. 2004. Shift work, duration of pregnancy, and birth weight: the National Birth Cohort in Denmark. Am J Obstet Gynecol 191:285-291.
107. Zylka MJ, Shearman LP, Weaver DR, Reppert SM. 1998. Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron 20:1103-1110.