Environmental control of biological rhythms: Effects on development, fertility and metabolism

Journal of Neuroendocrinology

Volumn 26, Issue 9, 2014, Pages 603-612

  Amaral, F G ^a   Castrucci, A M ^a   Cipolla Neto, J ^a   Poletini, M O ^b   Mendez, N ^c   Richter, H G ^c   Sellix, M T ^d  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^d UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Circadian; Clock gene; Melatonin; Mouse; Rat; Reproduction

Indexed keywords

GLUCOSE; INSULIN; MELANOPSIN; STEROID; MELATONIN;

BIOLOGICAL RHYTHM; CIRCADIAN RHYTHM; COGNITIVE DEFECT; DEVELOPMENT; ENERGY METABOLISM; ENVIRONMENTAL FACTOR; FERTILITY; GENETIC TRANSCRIPTION; GLUCOSE HOMEOSTASIS; HORMONAL REGULATION; INFERTILITY; INSULIN RELEASE; LIGHT DARK CYCLE; MACROMOLECULE; METABOLIC REGULATION; MOLECULAR CLOCK; OVARY POLYCYSTIC DISEASE; PATHOPHYSIOLOGY; PINEAL BODY; POLLUTION; PREGNANCY; PRIORITY JOURNAL; PROGENY; RETINA GANGLION CELL; REVIEW; SHIFT WORKER; ANIMAL; BRAIN; CHILD; CHILD DEVELOPMENT; FETUS DEVELOPMENT; HUMAN; PHOTOPERIODICITY; PHYSIOLOGY; REPRODUCTION; SLEEP DISORDER;

ANIMALS; BIOLOGICAL CLOCKS; BRAIN; CHILD; CHILD DEVELOPMENT; CHRONOBIOLOGY DISORDERS; CIRCADIAN RHYTHM; ENERGY METABOLISM; FERTILITY; FETAL DEVELOPMENT; HUMANS; MELATONIN; PHOTOPERIOD; REPRODUCTION;

EID: 84906496626     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12144     Document Type: Review

References (133)

1. Pittendrigh CS. Temporal organization: reflections of a Darwinian clock-watcher. Annu Rev Physiol 1993; 55:16.
2. Bass J, Takahashi JS. Circadian integration of metabolism and energetics. Science 2010; 330: 1349-1354.
3. Huang W, Ramsey KM, Marcheva B, Bass J. Circadian rhythms, sleep, and metabolism. J Clin Invest 2011; 121: 2133-2141.
4. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR, Eckel RH, Takahashi JS, Bass J. Obesity and metabolic syndrome in circadian Clock mutant mice. Science 2005; 308: 1043-1045.
5. Hall JC, Rosbash M. Mutations and molecules influencing biological rhythms. Annu Rev Neurosci 1988; 11: 373-393.
6. Konopka RJ, Benzer S. Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci USA 1971; 68: 2112.
7. Ralph MR, Menaker M. A mutation of the circadian system in golden hamsters. Science 1988; 241: 1225.
8. Kobayashi Y, Ishikawa T, Hirayama J, Daiyasu H, Kanai S, Toh H, Fukuda I, Tsujimura T, Terada N, Kamei Y, Yuba S, Iwai S, Todo T. Molecular analysis of zebrafish photolyase/cryptochrome family: two types of cryptochromes present in zebrafish. Genes Cells 2000; 5: 725-738.
9. Dibner C, Schibler U, Albrecht U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 2010; 72: 517-549.
10. Albrecht U. Timing to perfection: the biology of central and peripheral circadian clocks. Neuron 2012; 74: 246-260.
11. Mohawk JA, Green CB, Takahashi JS. Central and peripheral circadian clocks in mammals. Annu Rev Neurosci 2012; 35: 445-462.
12. Yagita K, Yamaguchi S, Tamanini F, van Der Horst GT, Hoeijmakers JH, Yasui A, Loros JJ, Dunlap JC, Okamura H. Dimerization and nuclear entry of mPER proteins in mammalian cells. Genes Dev 2000; 14: 1353-1363.
13. Young MW, Kay SA. Time zones: a comparative genetics of circadian clocks. Nat Rev Genet 2001; 2: 702.
14. Okamura H, Yamaguchi S, Yagita K. Molecular machinery of the circadian clock in mammals. Cell Tissue Res 2002; 309: 47-56.
15. Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, Schibler U. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 2002; 110: 251.
16. Albrecht U, Eichele G. The mammalian circadian clock. Curr Opin Genet Dev 2003; 13: 271-277.
17. Hastings MH. Neuroendocrine rhythms. Pharmacol Ther 1991; 50: 35.
18. Zordan M, Costa R, Fukuhara C, Tosini G. The molecular biology of the mammalian circadian clock. Chronobiology International 2000; 4: 433-51.
19. Bruce VG, Weight F, Pittendrigh CS. Resetting the sporulation rhythm in Pilobolus with short light flashes of high intensity. Science 1960; 131: 728-730.
20. Shen WL, Kwon Y, Adegbola AA, Luo J, Chess A, Montell C. Function of rhodopsin in temperature discrimination in Drosophila. Science 2011; 331: 1333-1336.
21. Menaker M, Moreira LF, Tosini G. Evolution of circadian organization in vertebrates. Braz J Med Biol Res 1997; 30: 305-313.
22. Menaker M, Roberts R, Elliott J, Underwood H. Extraretinal light perception in the sparrow. 3. The eyes do not participate in photoperiodic photoreception. Proc Natl Acad Sci USA 1970; 67: 320-325.
23. Foster RG, Provencio I, Hudson D, Fiske S, De Grip W, Menaker M. Circadian photoreception in the retinally degenerate mouse (rd/rd). J Comp Physiol A 1991; 169: 39-50.
24. Provencio I, Rollag MD, Castrucci AM. Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature 2002; 415: 493.
25. Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science 2002; 295: 1070-1073.
26. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD. Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci USA 1998; 95: 340-345.
27. Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD. A novel human opsin in the inner retina. J Neurosci 2000; 20: 600-605.
28. Panda S, Sato TK, Castrucci AM, Rollag MD, DeGrip WJ, Hogenesch JB, Provencio I, Kay SA. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 2002; 298: 2213.
29. Panda S, Provencio I, Tu DC, Pires SS, Rollag MD, Castrucci AM, Pletcher MT, Sato TK, Wiltshire T, Andahazy M, Kay SA, Van Gelder RN, Hogenesch JB. Melanopsin is required for non-image-forming photic responses in blind mice. Science 2003; 301: 525-527.
30. Menaker M, Murphy ZC, Sellix MT. Central control of peripheral circadian oscillators. Curr Opin Neurobiol 2013; 23: 741-746.
31. Plautz JD, Kaneko M, Hall JC, Kay SA. Independent photoreceptive circadian clocks throughout Drosophila. Science 1997; 278: 1632-1635.
32. Aschoff J, Wever R. Human circadian rhythms: a multioscillatory system. Fed Proc 1976; 35: 236-32.
33. Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M, Tei H. Resetting central and peripheral circadian oscillators in transgenic rats. Science 2000; 288: 682.
34. Yoo SH, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED, Siepka SM, Hong HK, Oh WJ, Yoo OJ, Menaker M, Takahashi JS. PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA 2004; 101: 5339.
35. Balsalobre A. Clock genes in mammalian peripheral tissues. Cell Tissue Res 2002; 309: 193-199.
36. Welsh DK, Yoo SH, Liu AC, Takahashi JS, Kay SA. Bioluminescence imaging of individual fibroblasts reveals persistent, independently phased circadian rhythms of clock gene expression. Curr Biol 2004; 14: 2289-2295.
37. Bluhm AP, Obeid NN, Castrucci AM, Visconti MA. The expression of melanopsin and clock genes in Xenopus laevis melanophores and their modulation by melatonin. Braz J Med Biol Res 2012; 45: 730-736.
38. Farhat FP, Martins CB, De Lima LH, Isoldi MC, Castrucci AM. Melanopsin and clock genes: regulation by light and endothelin in the zebrafish ZEM-2S cell line. Chronobiol Int 2009; 26: 1090-1119.
39. de Lima LH, dos Santos KP, de Lauro Castrucci AM. Clock genes, melanopsins, melatonin, and dopamine key enzymes and their modulation by light and glutamate in chicken embryonic retinal cells. Chronobiol Int. 2011; 28: 89-100.
40. Whitmore D, Foulkes NS, Strahle U, Sassone-Corsi P. Zebrafish Clock rhythmic expression reveals independent peripheral circadian oscillators. Nat Neurosci 1998; 1: 701-707.
41. Guo H, Brewer JM, Lehman MN, Bittman EL. Suprachiasmatic regulation of circadian rhythms of gene expression in hamster peripheral organs: effects of transplanting the pacemaker. J Neurosci 2006; 26: 6406-6412.
42. LeSauter J, Lehman MN, Silver R. Restoration of circadian rhythmicity by transplants of SCN 'micropunches'. J Biol Rhythms 1996; 11: 163.
43. Sujino M, Masumoto KH, Yamaguchi S, van der Horst GT, Okamura H, Inouye ST. Suprachiasmatic nucleus grafts restore circadian behavioral rhythms of genetically arrhythmic mice. Curr Biol 2003; 13: 664-668.
44. McDearmon EL, Patel KN, Ko CH, Walisser JA, Schook AC, Chong JL, Wilsbacher LD, Song EJ, Hong HK, Bradfield CA, Takahashi JS. Dissecting the functions of the mammalian clock protein BMAL1 by tissue-specific rescue in mice. Science 2006; 314: 1304-1308.
45. Pando MP, Morse D, Cermakian N, Sassone-Corsi P. Phenotypic rescue of a peripheral clock genetic defect via SCN hierarchical dominance. Cell 2002; 110: 107.
46. Davidson AJ, Yamazaki S, Menaker M. SCN: ringmaster of the circadian circus or conductor of the circadian orchestra? Novartis Found Symp. 2003; 253: 110-121; discussion 21-5, 281-4.
47. Bartell PA, Miranda-Anaya M, Menaker M. Period and phase control in a multioscillatory circadian system (Iguana iguana). J Biol Rhythms 2004; 19: 47-57.
48. Davidson AJ, London B, Block GD, Menaker M. Cardiovascular tissues contain independent circadian clocks. Clin Exp Hypertens 2005; 27: 307-311.
49. Kornmann B, Schaad O, Reinke H, Saini C, Schibler U. Regulation of circadian gene expression in liver by systemic signals and hepatocyte oscillators. Cold Spring Harb Symp Quant Biol 2007; 72: 319-330.
50. Kornmann B, Schaad O, Bujard H, Takahashi JS, Schibler U. System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol 2007; 5: e34.
51. Balsalobre A, Damiola F, Schibler U. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 1998; 93: 929.
52. Carr AJ, Whitmore D. Imaging of single light-responsive clock cells reveals fluctuating free-running periods. Nat Cell Biol 2005; 7: 319-321.
53. Reiter RJ. The pineal gland: an intermediary between the environment and the endocrine system. Psychoneuroendocrinology 1983; 8: 31-40.
54. Campos LA, Cipolla-Neto J, Amaral FG, Michelini LC, Bader M, Baltatu OC. The angiotensin-melatonin axis. Int J Hypertens 2013; 2013: 521783.
55. Wolden-Hanson T, Mitton DR, McCants RL, Yellon SM, Wilkinson CW, Matsumoto AM, Rasmussen DD. Daily melatonin administration to middle-aged male rats suppresses body weight, intraabdominal adiposity, and plasma leptin and insulin independent of food intake and total body fat. Endocrinology 2000; 141: 487-497.
56. Zanuto R, Siqueira-Filho MA, Caperuto LC, Bacurau RF, Hirata E, Peliciari-Garcia RA, do Amaral FG, Marcal AC, Ribeiro LM, Camporez JP, Carpinelli AR, Bordin S, Cipolla-Neto J, Carvalho CR. Melatonin improves insulin sensitivity independently of weight loss in old obese rats. J Pineal Res. 2013; 55: 156-65.
57. Mendes C, Lopes AM, do Amaral FG, Peliciari-Garcia RA, Turati Ade O, Hirabara SM, Scialfa Falcao JH, Cipolla-Neto J. Adaptations of the aging animal to exercise: role of daily supplementation with melatonin. J Pineal Res. 2013; 55: 229-39.
58. Tan DX, Manchester LC, Fuentes-Broto L, Paredes SD, Reiter RJ. Significance and application of melatonin in the regulation of brown adipose tissue metabolism: relation to human obesity. Obes Rev 2011; 12: 167-188.
59. Anhe GF, Caperuto LC, Pereira-Da-Silva M, Souza LC, Hirata AE, Velloso LA, Cipolla-Neto J, Carvalho CR. In vivo activation of insulin receptor tyrosine kinase by melatonin in the rat hypothalamus. J Neurochem 2004; 90: 559-566.
60. Lima FB, Machado UF, Bartol I, Seraphim PM, Sumida DH, Moraes SM, Hell NS, Okamoto MM, Saad MJ, Carvalho CR, Cipolla-Neto J. Pinealectomy causes glucose intolerance and decreases adipose cell responsiveness to insulin in rats. Am J Physiol 1998; 275: E934-E941.
61. Zanquetta MM, Seraphim PM, Sumida DH, Cipolla-Neto J, Machado UF. Calorie restriction reduces pinealectomy-induced insulin resistance by improving GLUT4 gene expression and its translocation to the plasma membrane. J Pineal Res 2003; 35: 141-148.
62. Nogueira TC, Lellis-Santos C, Jesus DS, Taneda M, Rodrigues SC, Amaral FG, Lopes AM, Cipolla-Neto J, Bordin S, Anhe GF. Absence of melatonin induces night-time hepatic insulin resistance and increased gluconeogenesis due to stimulation of nocturnal unfolded protein response. Endocrinology 2011; 152: 1253-1263.
63. Kivimaki M, Batty GD, Hublin C. Shift work as a risk factor for future type 2 diabetes: evidence, mechanisms, implications, and future research directions. PLoS Med 2011; 8: e1001138.
64. Erren TC, Reiter RJ, Piekarski C. Light, timing of biological rhythms, and chronodisruption in man. Naturwissenschaften 2003; 90: 485-494.
65. Richter HG, Torres-Farfan C, Rojas-Garcia PP, Campino C, Torrealba F, Seron-Ferre M. The circadian timing system: making sense of day/night gene expression. Biol Res 2004; 37: 11-28.
66. Erren TC, Reiter RJ. Light hygiene: time to make preventive use of insights-old and new-into the nexus of the drug light, melatonin, clocks, chronodisruption and public health. Med Hypotheses 2009; 73: 537-541.
67. Pan A, Schernhammer ES, Sun Q, Hu FB. Rotating night shift work and risk of type 2 diabetes: two prospective cohort studies in women. PLoS Med 2011; 8: e1001141.
68. Gamble KL, Motsinger-Reif AA, Hida A, Borsetti HM, Servick SV, Ciarleglio CM, Robbins S, Hicks J, Carver K, Hamilton N, Wells N, Summar ML, McMahon DG, Johnson CH. Shift work in nurses: contribution of phenotypes and genotypes to adaptation. PLoS ONE 2011; 6: e18395.
69. Garaulet M, Madrid JA. Chronobiological aspects of nutrition, metabolic syndrome and obesity. Adv Drug Deliv Rev 2010; 62: 967-978.
70. Wyse CA, Selman C, Page MM, Coogan AN, Hazlerigg DG. Circadian desynchrony and metabolic dysfunction; did light pollution make us fat? Med Hypotheses 2011; 77: 1139-1144.
71. Knutsson A. Health disorders of shift workers. Occup Med (Lond) 2003; 53: 103-108.
72. Croteau A, Marcoux S, Brisson C. Work activity in pregnancy, preventive measures, and the risk of delivering a small-for-gestational-age infant. Am J Public Health 2006; 96: 846-855.
73. Abeysena C, Jayawardana P, De ASR. Maternal sleep deprivation is a risk factor for small for gestational age: a cohort study. Aust N Z J Obstet Gynaecol 2009; 49: 382-387.
74. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 2008; 359: 61-73.
75. Seron-Ferre M, Forcelledo ML, Torres-Farfan C, Valenzuela FJ, Rojas A, Vergara M, Rojas-Garcia PP, Recabarren MP, Valenzuela GJ. Impact of chronodisruption during primate pregnancy on the maternal and newborn temperature rhythms. PLoS ONE 2013; 8: e57710.
76. Seron-Ferre M, Mendez N, Abarzua-Catalan L, Vilches N, Valenzuela FJ, Reynolds HE, Llanos AJ, Rojas A, Valenzuela GJ, Torres-Farfan C. Circadian rhythms in the fetus. Mol Cell Endocrinol 2011; 349: 68-75.
77. Ciarleglio CM, Axley JC, Strauss BR, Gamble KL, McMahon DG. Perinatal photoperiod imprints the circadian clock. Nat Neurosci 2010; 14: 25-27.
78. Varcoe TJ, Wight N, Voultsios A, Salkeld MD, Kennaway DJ. Chronic phase shifts of the photoperiod throughout pregnancy programs glucose intolerance and insulin resistance in the rat. PLoS ONE 2011; 6: e18504.
79. Summa KC, Vitaterna MH, Turek FW. Environmental perturbation of the circadian clock disrupts pregnancy in the mouse. PLoS ONE 2012; 7: e37668.
80. Torres-Farfan C, Mendez N, Abarzua-Catalan L, Vilches N, Valenzuela GJ, Seron-Ferre M. A circadian clock entrained by melatonin is ticking in the rat fetal adrenal. Endocrinology 2011; 152: 1891-1900.
81. Mendez N, Abarzua-Catalan L, Vilches N, Galdames HA, Spichiger C, Richter HG, Valenzuela GJ, Seron-Ferre M, Torres-Farfan C. Timed maternal melatonin treatment reverses circadian disruption of the fetal adrenal clock imposed by exposure to constant light. PLoS ONE 2012; 7: e42713.
82. Vilches NSC, Mendez N, Abarzua-Catalan L, Galdames HA, Hazlerigg DG, Richter HG, Torres-Farfan C. Gestational chronodisruption impairs hippocampal expression of NMDA receptor subunits Grin1b/Grin3a and spatial memory in the adult offspring. PLoS ONE. 2014; in press.
83. Galdames HAT-FC, Spichiger C, Mendez N, Abarzua-Catalan L, Alonso-Vazquez P, Richter HG. Impact of gestational chronodisruption on fetal cardiac genomics. J Mol Cell Cardiol 2013; 66: 1-11.
84. Kennaway DJ, Boden MJ, Varcoe TJ. Circadian rhythms and fertility. Mol Cell Endocrinol 2012; 349: 56-61.
85. Mahoney MM. Shift work, jet lag, and female reproduction. Int J Endocrinol 2010; 2010: 813764.
86. Kennaway DJ. The role of circadian rhythmicity in reproduction. Hum Reprod Update 2005; 11: 91.
87. Arble DM, Ramsey KM, Bass J, Turek FW. Circadian disruption and metabolic disease: findings from animal models. Best Pract Res Clin Endocrinol Metab 2010; 24: 785-800.
88. de la Iglesia HO, Schwartz WJ. Minireview: timely ovulation: circadian regulation of the female hypothalamo-pituitary-gonadal axis. Endocrinology 2006; 147: 1148-1153.
89. Chappell PE. Clocks and the black box: circadian influences on gonadotropin-releasing hormone secretion. J Neuroendocrinol 2005; 17: 119-130.
90. Tonsfeldt KJ, Chappell PE. Clocks on top: the role of the circadian clock in the hypothalamic and pituitary regulation of endocrine physiology. Mol Cell Endocrinol 2012; 349: 3-12.
91. Sellix MT. Clocks underneath: the role of peripheral clocks in the timing of female reproductive physiology. Front Endocrinol (Lausanne) 2013; 4: 91.
92. Yoshikawa T, Sellix M, Pezuk P, Menaker M. Timing of the ovarian circadian clock is regulated by gonadotrophins. Endocrinology 2009; 150: 4338-4347.
93. Sellix MT, Yoshikawa T, Menaker M. A circadian egg timer gates ovulation. Curr Biol 2010; 20: R266-R267.
94. Gras S, Georg B, Jorgensen HL, Fahrenkrug J. Expression of the clock genes Per1 and Bmal1 during follicle development in the rat ovary. Effects of gonadotropin stimulation and hypophysectomy. Cell Tissue Res 2012; 350: 539-548.
95. He PJ, Hirata M, Yamauchi N, Hashimoto S, Hattori MA. Gonadotropic regulation of circadian clockwork in rat granulosa cells. Mol Cell Biochem 2007; 302: 111-118.
96. Ratajczak CK, Boehle KL, Muglia LJ. Impaired steroidogenesis and implantation failure in Bmal1-/- mice. Endocrinology 2009; 150: 1879-1885.
97. Ratajczak CK, Herzog ED, Muglia LJ. Clock gene expression in gravid uterus and extra-embryonic tissues during late gestation in the mouse. Reprod Fertil Dev 2010; 22: 743-750.
98. Ratajczak CK, Asada M, Allen GC, McMahon DG, Muglia LM, Smith D, Bhattacharyya S, Muglia LJ. Generation of myometrium-specific Bmal1 knockout mice for parturition analysis. Reprod Fertil Dev 2012; 24: 759-767.
99. 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.
100. Kennaway DJ, Varcoe TJ, Mau VJ. Rhythmic expression of clock and clock-controlled genes in the rat oviduct. Mol Hum Reprod 2003; 9: 503-507.
101. Uchikawa M, Kawamura M, Yamauchi N, Hattori MA. Down-regulation of circadian clock gene period 2 in uterine endometrial stromal cells of pregnant rats during decidualization. Chronobiol Int 2011; 28: 1-9.
102. Crain DA, Janssen SJ, Edwards TM, Heindel J, Ho SM, Hunt P, Iguchi T, Juul A, McLachlan JA, Schwartz J, Skakkebaek N, Soto AM, Swan S, Walker C, Woodruff TK, Woodruff TJ, Giudice LC, Guillette LJ Jr. Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil Steril 2008; 90: 911-940.
103. Zama AM, Uzumcu M. Epigenetic effects of endocrine-disrupting chemicals on female reproduction: an ovarian perspective. Front Neuroendocrinol 2010; 31: 420-439.
104. Franks S. Genetic and environmental origins of obesity relevant to reproduction. Reprod Biomed Online 2006; 12: 526-531.
105. Fernandez M, Bourguignon N, Lux-Lantos V, Libertun C. Neonatal exposure to bisphenol a and reproductive and endocrine alterations resembling the polycystic ovarian syndrome in adult rats. Environ Health Perspect 2010; 118: 1217-1222.
106. Padmanabhan V, Veiga-Lopez A. Developmental origin of reproductive and metabolic dysfunctions: androgenic versus estrogenic reprogramming. Semin Reprod Med 2011; 29: 173-186.
107. Savabieasfahani M, Kannan K, Astapova O, Evans NP, Padmanabhan V. Developmental programming: differential effects of prenatal exposure to bisphenol-A or methoxychlor on reproductive function. Endocrinology 2006; 147: 5956-5966.
108. Rubin BS. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol 2011; 127: 27-34.
109. Hamilton-Fairley D, Kiddy D, Watson H, Paterson C, Franks S. Association of moderate obesity with a poor pregnancy outcome in women with polycystic ovary syndrome treated with low dose gonadotrophin. Br J Obstet Gynaecol 1992; 99: 128-131.
110. Franks S, McCarthy MI, Hardy K. Development of polycystic ovary syndrome: involvement of genetic and environmental factors. Int J Androl 2006; 29: 278-285; discussion 86-90.
111. Xita N, Tsatsoulis A. Review: fetal programming of polycystic ovary syndrome by androgen excess: evidence from experimental, clinical, and genetic association studies. J Clin Endocrinol Metab 2006; 91: 1660-1666.
112. Dunaif A. Insulin resistance and the polycystic ovary syndrome: mechanism and implications for pathogenesis. Endocr Rev 1997; 18: 774-800.
113. Ehrmann DA. Polycystic ovary syndrome. N Engl J Med 2005; 352: 1223-1236.
114. Dumesic DA, Abbott DH, Padmanabhan V. Polycystic ovary syndrome and its developmental origins. Rev Endocr Metab Disord 2007; 8: 127-141.
115. Padmanabhan V, Manikkam M, Recabarren S, Foster D. Prenatal testosterone excess programs reproductive and metabolic dysfunction in the female. Mol Cell Endocrinol 2006; 246: 165-174.
116. Franks S, Berga SL. Does PCOS have developmental origins? Fertil Steril 2012; 97: 2-6.
117. Walters KA, Allan CM, Handelsman DJ. Rodent models for human polycystic ovary syndrome. Biol Reprod 2012; 86: 149, 1-12.
118. Gilling-Smith C, Story H, Rogers V, Franks S. Evidence for a primary abnormality of thecal cell steroidogenesis in the polycystic ovary syndrome. Clin Endocrinol 1997; 47: 93-99.
119. Franks S. Polycystic ovary syndrome. Arch Dis Child 1997; 77: 89-90.
120. Franks S, Gharani N, Waterworth D, Batty S, White D, Williamson R, McCarthy M. Genetics of polycystic ovary syndrome. Mol Cell Endocrinol 1998; 145: 123-128.
121. Litinski M, Scheer FA, Shea SA. Influence of the circadian system on disease severity. Sleep Med Clin 2009; 4: 143-163.
122. Ruger M, Scheer FA. Effects of circadian disruption on the cardiometabolic system. Rev Endocr Metab Disord 2009; 10: 245-260.
123. Scheer FA, Hilton MF, Mantzoros CS, Shea SA. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc Natl Acad Sci USA 2009; 106: 4453-4458.
124. Buxton OM, Cain SW, O'Connor SP, Porter JH, Duffy JF, Wang W, Czeisler CA, Shea SA. Adverse metabolic consequences in humans of prolonged sleep restriction combined with circadian disruption. Sci Transl Med. 2012; 4: 129ra43.
125. Sellix MT, Murphy ZC, Menaker M. Excess androgen during puberty disrupts circadian organization in female rats. Endocrinology 2013; 154: 1636-1647.
126. Pezuk P, Mohawk JA, Yoshikawa T, Sellix MT, Menaker M. Circadian organization is governed by extra-SCN pacemakers. J Biol Rhythms 2010; 25: 432-441.
127. Coomans CP, van den Berg SA, Lucassen EA, Houben T, Pronk AC, van der Spek RD, Kalsbeek A, Biermasz NR, Willems van Dijk K, Romijn JA, Meijer JH. The suprachiasmatic nucleus controls circadian energy metabolism and hepatic insulin sensitivity. Diabetes 2013; 62:1102-1108.
128. Karatsoreos INWA, Silver R. Androgens Restructure Circadian Behavior and the Brain Clock. Atlanta, GA: Society for Neuroscience, 2006.
129. Karatsoreos IN, Wang A, Sasanian J, Silver R. A role for androgens in regulating circadian behavior and the suprachiasmatic nucleus. Endocrinology 2007; 148: 5487-5495.
130. Iwahana E, Karatsoreos I, Shibata S, Silver R. Gonadectomy reveals sex differences in circadian rhythms and suprachiasmatic nucleus androgen receptors in mice. Horm Behav 2008; 53: 422-430.
131. Karatsoreos IN, Butler MP, Lesauter J, Silver R. Androgens modulate structure and function of the suprachiasmatic nucleus brain clock. Endocrinology 2011; 152: 1970-1978.
132. Daan S, Damassa D, Pittendrigh CS, Smith ER. An effect of castration and testosterone replacement on a circadian pacemaker in mice (Mus musculus). Proc Natl Acad Sci USA 1975; 72: 3744.
133. Cao Q, Gery S, Dashti A, Yin D, Zhou Y, Gu J, Koeffler HP. A role for the clock gene per1 in prostate cancer. Cancer Res 2009; 69: 7619-7625.