Developmental and reproductive performance in circadian mutant mice

Human Reproduction

Volumn 21, Issue 1, 2006, Pages 68-79

  Dolatshad, H ^a   Campbell, E A ^a   O'Hara, L ^a   Maywood, E S ^b   Hastings, M H ^b   Johnson, M H ^a  

^a Department of Anatomy ^*  (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Circadian rhythm; Clock mutants; Fecundity; Mice; Uterus

Indexed keywords

TRANSCRIPTION FACTOR CLOCK; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR;

ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; FERTILITY; FERTILIZATION IN VITRO; FETUS; GENOTYPE; HETEROZYGOSITY; HOMOZYGOSITY; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; PREGNANCY RATE; PROGENY; PUERPERIUM; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTIVE HEALTH; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; SUPRAOPTIC NUCLEUS; SURVIVAL; UTERUS; WEANING; WILD TYPE;

EID: 29144442443     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dei313     Document Type: Article

References (76)

1. Akhtar RA, Reddy AB, Maywood ES, Clayton JD, King VM, Smith AG, Gant TW, Hastings MH and Kyriacou CP (2002) Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 12,540-550.
2. Alleva J, Waleski M and Alleva F (1971) A biological clock controlling the estrous cycle of the hamster. Endocrinology 88,1368-1379.
3. Alvarez J, Chen D, Storer E and Sehgal A (2003) Non-cyclic and developmental stage-specific expression of circadian clock proteins during murine spermatogenesis. Biol Reprod 69,81-91.
4. Asnicar M, Koster A, Heiman M, Tinsley F, Smith D, Galbreath E, Fox N, Ma Y, Blum W and Hsiung H (2002) Vasoactive Intestinal Polypeptide/ Pituitary Adenylate Cyclase-Activating Peptide Receptor 2 deficiency in mice results in growth retardation and increased basal metabolic rate. Endocrinology 143,3994-4006.
5. Baisong L and Bishop C (2003) Late onset of spermatogenesis and gain of fertility in POG-deficient mice indicate that POG is not necessary for the proliferation of spermatogonia. Biol Reprod 69,161-168.
6. Barbacka-Surowiak G, Surowiak J and Stoklosowa S (2003) The involvement of suprachiasmatic nuclei in the regulation of estrous cycles in rodents. Reprod Biol 3,99-129.
7. Barkan D, Hurgin V, Dekel N, Amsterdam A and Rubinstein M (2005) Leptin induces ovulation in GnRH-deficient mice. FASEB J 19,133-145.
8. Beaver L and Giebultowicz J (2004) Regulation of copulation duration by period and timeless in Drosophila melanogaster. Curr Biol 14,1492-1497.
9. Beaver L, Gvakharia B, Vollintine T, Hege D, Stanewsky R and Giebultowicz J (2002) Loss of circadian clock function decreases reproductive fitness in males of Drosophila melanogaster. Proc Nat Acad Sci USA 99,2134-2139.
10. Beaver L, Rush B, Gvakharia B and Giebultowicz J (2003) Noncircadian regulation and function of clock genes period and timeless in oogenesis of Drosophila melanogaster. J Biol Rhythms 18,463-472.
11. Bittman E, Doherty L, Huang L and Paroskie A (2003) Period gene expression in mouse endocrine tissues. Am J Physiol 285,R561-R569.
12. Carr A-J, Johnston J, Semikhodskii A, Nolan T, Cagampang F, Stirland J and Loudon A (2003) Photoperiod differentially regulates circadian oscillators in central and peripheral tissues of the Syrian hamster. Curr Biol 13,1543-1548.
13. Chappell P, White R and Mellon P (2003) Circadian gene expression regulates pulsatile gonadotrophin-releasing hormone (GnRH) secretory patterns in the hypothalamic GnRH-secreting GT1-7 cell line. J Neurosci 23,11202-11213.
14. Cutler D, Haraura M, Reed H, Shen S, Sheward W, Morrison C, Marston H, Harmar A and Piggins H (2003) The mouse VPAC2 receptor confers suprachiasmatic nuclei cellular rhythmicity and responsiveness to vasoactive intestinal polypeptide in vitro. Eur J Neurosci 17,197-204.
15. Damiola F, Minh NL, Preitner N, Kornmann B, Fleury-Olela F and Schibler U (2000) Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14,2950-2961.
16. Davidson A, Stokkan K-A, Yamazaki S and Menaker M (2002) Food-anticipatory activity and liver per1-luc activity in diabetic transgenic rats. Physiol Behav 76,21-26.
17. Day ML, Winston N, McConnell JL, Cook DI and Johnson MH (2001) tiK+ toK+: An embryonic clock? Reprod Fertil Dev 13,69-79.
18. Douglas A, Leng G and Russell J (2002) The importance of oxytocin mechanisms in the control of mouse parturition. Reproduction 123,543-552.
19. Easton A, Arbuzova J and Turek FW (2003) The circadian Clock mutation increases exploratory activity and escape-seeking behavior. Genes Brain Behav 2,11-19.
20. Endo A and Wanatabe T (1989) Effects of non-24-hour days on reproductive efficiency and embryonic devleopment in mice. Gamete Res 22,435-441.
21. Gekakis N, Staknis D, Nguen H, Davis F, Wilsbacher L, King D, Takahashi J and Weitz C (1998) Role of the CLOCK protein in the mammalian circadian mechanism. Science 280,1564-1569.
22. Gerhold L, Rosewell K and Wise P (2005) Suppression of vasoactive intestinal polypeptide in the suprachiasmatic nucleus leads to aging-like alterations in cAMP rhythms and activation of gonadotropin-releasing hormone neurons. J Neurosci 25,62-67.
23. Giebultowicz J and Riemann J (1990) Circadian system in the insect testes controls the rhythmic release of sperm. Prog Clin Biol Res 341B,655-660.
24. Gross G, Imamura T and Muglia L (2000) Gene knockout mice in the study of parturition. J Soc Gynecol Invest 7,88-95.
25. Guo H, Brewer J, Champhekar A, Harris R and Bittman E (2005) Differential control of peripheral circadian rhythms by suprachiasmatic-dependent neural signals. Proc Natl Acad Sci USA 102,3111-3116.
26. Hamatani T, Carter M, Sharov A and Ko M (2004) Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 6,117-131.
27. Harmar A, Arimura A, Gozes I, Journot L, Laburthe M, Plsegna J, Rawlings S, Robberecht P, Said S, Sreedharan S et al (1998) International Union of Pharmacology. XVIII. Nomenclature of receptors for vasoactive intestinal polypeptide and pituitary adenylate cyclase-activating polypeptide. Pharm Rev 50,265-270.
28. Harmar A, Marston H, Shen S, Spratt C, West K, Sheward W, Morrison C, Dorin J, Piggins H, Reubi J-C et al (2002) The VPAC2 receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 109,497-506.
29. Harmar A, Sheward W, Morrison C, Waser B, Gugger M and Reubi J (2004) Distribution of the VPAC2 receptor in peripheral tissues of the mouse. Endocrinology 145,1203-1210.
30. Hastings M, Reddy A and Maywood E (2003) A clockwork web: Circadian timing in brain and periphery, in health and disease. Nature Rev Neurosci 4,1-14.
31. Herzog E, Grace M, Harrer C, Williamson J, Shinohara K and Block G (2000) The role of Clock in the developmental expression of neuropeptides in the suprachiasmatic nucleus. J Comp Neurol 424,86-98.
32. Horard B, Rayet B, Triqueneaux G, Laudet V, Delaunay F and Vanacker J-M (2004) Expression of the orphan nuclear receptor ERR is under circadian regulation in estrogen-responsive tissues. J Mol Endocrinol 33,87-97.
33. Johnson M (2001) Time and development. Reprod Biomed 4 (Suppl 1),39-45.
34. Johnson M and Day M (2000) Egg timers: How is developmental time measured in the early vertebrate embryo? BioEssays 22,57-63.
35. Johnson M and Everitt B (2000) Essential Reproduction. 5th edn, Blackwell, Oxford, UK.
36. Johnson MH, Lim A, Fernando D and Day ML (2002) Circadian clockwork genes are expressed in the reproductive tract and conceptus of the early pregnant mouse. Reprod Biomed 4,140-145.
37. Kalsbeek A and Buijis R (2002) Output pathways of the mammalian suprachiasmatic nucleus: Coding circadian time by transmitter selection and specific targetting. Cell Tissue Res 309,109-118.
38. Kennaway D (2002) Programming of the fetal suprachiasmatic nucleus and subsequent adult rhythmicity. Trends Endocrinol Metab 13,398-402.
39. Kennaway D, Varcoe T and Mau V (2003) Rhythmic expression of clock and clock-controlled genes in the rat oviduct. Mol Hum Reprod 9,503-507.
40. Kennaway D, Boden M and Voultsios A (2005) Reproductive performance in female Clock(Delta19) mutant mice. Reprod Fertil Dev 16,801-810.
41. King D and Takahashi J (2000) Molecular genetics of circadian rhythms in mammals. Annu Rev Neurosci 23,713-742.
42. King DP, Vitaterna MH, Chang AM, Dove WF, Pinto LH, Turek FW and Takahashi JS (1997a) The mouse Clock mutation behaves as an antimorph and maps within the W19H deletion, distal of Kit. Genetics 146,1049-1060.
43. King D, Zhao Y, Sangoram A, Wilsbacher L, Tanaka M, Antoch M, Steeves T, Vitaterna M, Kornhauser J, Lowrey P et al (1997b) Positional cloning of the mouse circadian Clock gene. Cell 89,641-653.
44. Krajnak K, Kashon M, Rosewell K and Wise P (1998) Sex differences in the daily rhythm of vasoactive intestinal polypeptide but not arginine vasopressin messenger ribonucleic acid in the suprachiasmatic nuclei. Endocrinology 139,4189-4196.
45. Kriegsfeld L, Silver R, Gore A and Crews D (2002) Vasoactive intestinal polypeptide contacts on gonadotropin-releasing hormone neurones increase following puberty in female rats. J Neuroendocrinol 14,685-690.
46. Kume K, Zylka M, Sriram S, Shearman L, Weaver D, Jin X, Maywood E, Hastings M and Reppert S (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98,193-205.
47. Lincoln G, Andersson H and Loudon A (2003) Clock genes in calendar cells as the basis of annual timekeeping in mammals - a unifying hypothesis. J Endocrinol 179,1-13.
48. Low-Zeddies S and Takahashi J (2001) Chimera analysis of the Clock mutation in mice shows that complex cellular integration determines circadian behaviour. Cell 105,25-42.
49. Mancuso P, Alexander J, McIntire D, Davis E, Burke G and Leveno K (2004) Timing of birth after spontaneous onset of labor. Obstet Gynaecol 103,653-656.
50. Miller B, Olson S, Turek F, Levine J, Horton T and Takahashi J (2004) Circadian Clock mutation disrupts estrous cyclicity and maintenance of pregnancy. Curr Biol 14,1367-1373.
51. Minami Y, Horikawa K, Akiyama M and Shibata S (2002) Restricted feeding induces daily expression of clock genes and Pai-1 mRNA in the heart of Clock mutant mice. FEBS Lett 526,115-118.
52. Morin L, Fitzgerald K and Zucker I (2002) Estradiol shortens the period of hamster circadian rhythms. Science 196,305-307.
53. Morse D, Cermakian N, Brancorsini S, Parvenin M and Sassone-Corsi P (2003) No circadian rhythms in testis: Period 1 gene expression is clock independent and developmentally regulated in the mouse. Mol Endocrinol 17,141-151.
54. Nagoshi E, Saini C, Bauer C, Laroche T, Naef F and Schibler U (2004) Circadian gene expression in individual fibroblasts: Cell-autonomous and selfsustained oscillators pass time to daughter cells. Cell 119,693-705.
55. Nathanielsz P (1998) Comparative studies on the initiation of labor. Eur J Obstet Gynecol Reprod Biol 78,127-132.
56. Naylor M, Oakes S, Gardiner-Garden M, Harris J, Blazek K, Ho T, Li F, Wynick D, Walker A and Ormandy C (2005) Transcriptional changes underlying the secretory activation phase of mammary gland development. Mol Endocrinol 19,1868-1883.
57. Nuesslein-Hildesheim B, O'Brien J, Ebling F, Maywood E and Hastings M (2000) The circadian cycle of mPER clock gene products in the suprachiasmatic nucleus of the siberian hamster encodes both daily and seasonal time. Eur J Neurosci 12,2856-2864.
58. Oishi K, Fukui H and Ishida N (2000) Rhythmic expression of Bmal1 mRNA is altered in Clock mutant mice: Differential regulation in the suprachiasmatic nucleus and peripheral tissues. Biochem Biophys Res Commun 268,164-171.
59. Palm I, VanderBeck E, Swarts H, VanderVliet J, Wiegant V, Buijs R and Kalsbeek A (2001a) Control of the estradiol-induced prolactin surge by the suprachiasmatic nucleus. Endocrinology 142,2296-2302.
60. Palm I, VanderBeck E, Wiegant V, Buijs RM and Kalsbeek A (2001b) The stimulatory effect of vasopressin on the luteinising hormone surge in ovariectomized, estradiol-treated rats is time-dependent. Brain Res 901,109-116.
61. Panda S, Antioch M, Miller B, Su A, Schook A, Straume M, Schultz P, Kay S, Takahashi J and Hogenesch J (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109,307-320.
62. Pittendrigh C (1993) Temporal organization: Reflections of a Darwinian clockwatcher. Annu Rev Physiol 55,16-54.
63. Reese J, Paria B, Brown N, Zhao X, Morrow J and Dey S (2000) Coordinated regulation of fetal and maternal prostaglandins directs successful birth and postnatal adaptation in the mouse. Proc Natl Acad Sci USA 97,9759-9764.
64. Reppert S, Henshaw D, Schwartz W and Weaver D (1987) The circadian-gated timing of birth in rats: Disruption by maternal SCN lesions or by removal of the fetal brain. Brain Res 403,398-402.
65. Stokkan K-A, Yamazaki S, Tei H, Sakaki Y and Menaker M (2001) Entrainment of the circadian clock in the liver by feeding. Science 291,490-493.
66. Storch K, Lipan O, Leykin I, Viswanathan N, Davis F, Wong W and Weitz C (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417,68-83.
67. Tsuchiya Y, Minami I, Kadotani H and Nishida E (2005) Resetting of peripheral circadian clock by prostaglandin E2. EMBO Reports 6,256-261.
68. Turek F, Swann J and Earnest D (1984) Role of the circadian system in reproductive phenomena. Recent Prog Horm Res 40,143-183.
69. Vitaterna M, King D, Chang A-M, Kornhauser J, Lowrey P, McDonald J, Dove W, Pinto L, Turek F and Takahashi J (1994) Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 264,719-725.
70. Wall E, Auchtung T, Dahl G, Ellis S and McFadden T (2005) Exposure to short day photoperiod during the dry period enhances mammary growth in dairy cows. J Dairy Sci 88,1994-2003.
71. Wollnik F and Turek F (1988) Estrous correlated modulations of circadian and ultradian wheel-running activity rhythms in LEW/Ztm rats. Physiol Behav 43,389-396.
72. Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block G, Sakaki Y, Menaker M and Tei H (2000) Resetting central and peripheral circadian oscillators in transgenic rats. Science 288,682-685.
73. Yang Z, Das S, Wang J, Sugimoto Y, Ichikawa A and Dey S (1997) Potential sites of prostaglandin actions in the periimplantation mouse uterus: differential expression and regulation of prostaglandin receptor genes. Biol Reprod 56,368-379.
74. Yoo S Yamazaki S Lowrey P Shimomura K Ko C Buhr E Siepka S Hong H Oh W Yoo O et al (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.
75. Young W, Shepard E, Amico J, Hennighausen L, Wagner K, LaMarca M, McKinney C and Ginns E (1996) Deficiency in mouse oxytocin prevents milk ejection, but not fertility or parturition. J Neuroendocrinol 8,847-853.
76. Zylka M, Shearman L, Weaver D and Reppert S (1998) Three period homologs in mammals: Differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron 20,1103-1110.