Circadian clock genes in reproductive tissues and the developing conceptus

Reproduction, Fertility and Development

Volumn 21, Issue 1, 2009, Pages 1-9

  Dolatshad, Hamid ^a   Davis, Fred C ^a   Johnson, Martin H ^b  

^a NORTHEASTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LUCIFERASE; MESSENGER RNA; PROTEIN BMAL1;

ANIMAL TISSUE; BIOLOGICAL RHYTHM; BMAL GENE; CIRCADIAN RHYTHM; CLOCK GENE; CONFERENCE PAPER; DEVELOPMENTAL GENE; DEVELOPMENTAL GENETICS; FEEDBACK SYSTEM; FEMALE; FETUS; FETUS DEVELOPMENT; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MALE; NONHUMAN; OVARY; OVIDUCT; PER GENE; PROMOTER REGION; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; SUPRACHIASMATIC NUCLEUS; TESTIS; TRANSGENIC MOUSE; UTERUS;

ANIMALS; BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENITALIA; HUMANS; MALE;

EID: 57449102666     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD08223     Document Type: Conference Paper

References (72)

1. Akhtar, R. A., Reddy, A. B., Maywood, E. S., Clayton, J. D., King, V. M., Smith, A. G., Gant, T. W., Hastings, M. H., and Kyriacou, C. P. (2002). Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr. Biol. 12, 540-550. doi:10.1016/S0960-9822(02)00759-5
2. Alvarez, J. D., Chen, D., Storer, E., and Sehgal, A. (2003). Noncyclic and developmental stage-specific expression of circadian clock proteins during murine spermatogenesis. Biol. Reprod. 69, 81-91. doi:10.1095/BIOLREPROD.102.011833
3. Alvarez, J. D., Hansen, A., Ord, T., Bebas, P., Chappell, P. E., Giebultowicz, J. M., Williams, C., Moss, S., and Sehgal, A. (2008). The circadian clock protein BMAL1 is necessary for fertility and proper testosterone production in mice. J. Biol. Rhythms 23, 26-36. doi:10.1177/ 0748730407311254
4. 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.
5. Beaver, L. M., Rush, B. L., Gvakharia, B. O., and Giebultowicz, J. M. (2003). Noncircadian regulation and function of clock genes period and timeless in oogenesis of Drosophila melanogaster. J. Biol. Rhythms 18, 463-472. doi:10.1177/0748730403259108
6. Bittman, E. L., Doherty, L. S., Huang, L., and Paroskie, A. (2003). Period gene expression in mouse endocrine tissues. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R561-R569.
7. Boden, M. J., and Kennaway, D. J. (2006). Circadian rhythms and reproduction. Reproduction 132, 379-392. doi:10.1530/REP.1.00614
8. Curran, K. L., LaRue, S., Bronson, B., Solis, J., Trow, A., Sarver, N., and Zhu, H. (2008). Circadian genes are expressed during early development in Xenopus laevis. PLoS One 3, e2749. doi:10.1371/JOURNAL. PONE.0002749
9. Davis, F. C., and Mannion, J. (1988). Entrainment of hamster pup circadian rhythms by prenatal melatonin injections to the mother. Am. J. Physiol. 255, R439-R448.
10. Day, M. L., Winston, N., McConnell, J. L., Cook, D., and Johnson, M. H. (2001). tiK+toK+: an embryonic clock? Reprod. Fertil. Dev. 13, 69-79. doi:10.1071/RD00048
11. Della Ragione, F., Comitato, R., Angelini, F., D'Esposito, M., and Cardone, A. (2005). Molecular cloning and characterization of the clock gene period2 in the testis of lizard Podarcis sicula and its expression during seasonal reproductive cycle. Gene 363, 105-112. doi:10.1016/J.GENE.2005.08.018
12. Dolatshad, H. (2006). Expression and role of circadian canonical genes in reproductive tissues. PhD thesis, University of Cambridge.
13. Dolatshad, H., Campbell, E. A., O'Hara, L., Maywood, E. S., Hastings, M. H., and Johnson, M. H. (2006). Developmental and reproductive performance in circadian mutant mice. Hum. Reprod. 21, 68-79. doi:10.1093/HUMREP/DEI313
14. Endo, A., and Watanabe, T. (1989). Effects of non-24-hour days on reproductive efficacy and embryonic development in mice. Gamete Res. 22, 435-441. doi:10.1002/MRD.1120220409
15. Fahrenkrug, J., Georg, B., Hannibal, J., Hindersson, P., and Gras, S. (2006). Diurnal rhythmicity of the clock genes Per1 and Per2 in the rat ovary. Endocrinology 147, 3769-3776. doi:10.1210/EN.2006-0305
16. Godinho, S. I. H., Maywood, E. S., Shaw, L., Tucci, V., Barnard, A. R., et al. (2007). The after-hours mutant reveals a role for Fbxl3 in determining mammalian circadian period. Science 316, 897-900. doi:10.1126/SCIENCE.1141138
17. Gozeri, E., Celik, H., Ozercan, I., Gurates, B., Polat, S. A., and Hanay, F. (2008). The effect of circadian rhythm changes on fetal and placental development (experimental study). Neuroendocrinol. Lett. 29, 87-90.
18. Hacker-Klom, U. B. (1994). Diurnal changes in murine spermatogenesis. Z. Naturforsch. [C] 49, 522-525.
19. Hamatani, T., Carter, M. G., Sharov, A. A., and Ko, M. S. H. (2004). Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6, 117-131. doi:10.1016/S1534-5807(03) 00373-3
20. Hardin, P. E. (1994). Analysis of period mRNA cycling in Drosophila head and body tissues indicates that body oscillators behave differently from head oscillators. Mol. Cell. Biol. 14, 7211-7218.
21. Harmar, A. J., Marston, H. M., Shen, S., Spratt, C., West, K. M., et al. (2002). The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 109, 497-508. doi:10.1016/S0092-8674(02)00736-5
22. Hastings, M. H., Reddy, A. B., McMahon, D. G., Maywood, E. S., and Michael, W. Y. (2005). Analysis of circadian mechanisms in the suprachiasmatic nucleus by transgenesis and biolistic transfection. In 'Methods in Enzymology'. (Ed. M. Young.) pp. 579-592. (Academic Press.)
23. Hastings, M., O'Neill, J. S., and Maywood, E. S. (2007). Circadian clocks: regulators of endocrine and metabolic rhythms. J. Endocrinol. 195, 187-198. doi:10.1677/JOE-07-0378
24. He, P.-J., Hirata, M., Yamauchi, N., Hashimoto, S., and Hattori, M.-a. (2007a). The disruption of circadian clockwork in differentiating cells from rat reproductive tissues as identified by in vitro real-time monitoring system. J. Endocrinol. 193, 413-420. doi:10.1677/JOE-07-0044
25. He, P.-J., Hirata, M., Yamauchi, N., and Hattori, M.-a. (2007b). Up-regulation of Per1 expression by estradiol and progesterone in the rat uterus. J. Endocrinol. 194, 511-519. doi:10.1677/JOE-07-0172
26. Horard, B., Rayet, B., Triqueneaux, G., Laudet, V., Delaunay, F., and Vanacker, J. M. (2004). Expression of the orphan nuclear receptor ERRalpha is under circadian regulation in estrogen-responsive tissues. J. Mol. Endocrinol. 33, 87-97. doi:10.1677/JME.0.0330087
27. Hoshino, K., Wakatsuki, Y., Iigo, M., and Shibata, S. (2006). Circadian clock mutation in dams disrupts nursing behavior and growth of pups. Endocrinology 147, 1916-1923. doi:10.1210/EN.2005-1343
28. Johnson, M. H. (2002). Time and development. Reprod. Biomed. Online 4(Suppl. 1), 39-45.
29. Johnson, M. H. (2007). 'Essential Reproduction.' (Wiley-Blackwell: Oxford.)
30. Johnson, M. H., and Day, M. L. (2000). Egg timers: how is developmental time measured in the early vertebrate embryo? Bioessays 22, 57-63. doi:10.1002/(SICI)1521-1878(200001)22:1〈57::AID-BIES10〉 3.0.CO;2-L
31. Johnson, M. H., Lim, A., Fernando, D., and Day, M. L. (2002). Circadian clockwork genes are expressed in the reproductive tract and conceptus of the early pregnant mouse. Reprod. Biomed. Online 4, 140-145.
32. Kabrita, C. S., and Davis, F. C. (2008). Development of the mouse suprachiasmatic nucleus: determination of time of cell origin and spatial arrangements within the nucleus. Brain Res. 1195, 20-27. doi:10.1016/J.BRAINRES.2007.12.020
33. Karman, B. N., and Tischkau, S. A. (2006). Circadian clock gene expression in the ovary: effects of luteinizing hormone. Biol. Reprod. 75, 624-632. doi:10.1095/BIOLREPROD.106.050732
34. Kennaway, D. J. (2005). The role of circadian rhythmicity in reproduction. Hum. Reprod. Update 11, 91-101. doi:10.1093/HUMUPD/ DMH054
35. Kennaway, D. J., Varcoe, T. J., and Mau, V. J. (2003). Rhythmic expression of clock and clock-controlled genes in the rat oviduct. Mol. Hum. Reprod. 9, 503-507. doi:10.1093/MOLEHR/GAG067
36. Kennaway, D. J., Boden, M. J., and Voultsios, A. (2004). Reproductive performance in female Clock(Delta19) mutant mice. Reprod. Fertil. Dev. 16, 801-810. doi:10.1071/RD04023
37. King, D. P., and Takahashi, J. S. (2000). Molecular genetics of circadian rhythms in mammals. Annu. Rev. Neurosci. 23, 713-742.
38. Ko, M. S., Kitchen, J. R., Wang, X., Threat, T. A., Wang, X., et al. (2000). Large-scale cDNA analysis reveals phased gene expression patterns during preimplantation mouse development. Development 127, 1737-1749.
39. Kouba, A. J., Burkhardt, B. R., Alvarez, I. M., Goodenow, M. M., and Buhi, W. C. (2000). Oviductal plasminogen activator inhibitor-1 (PAI-1): mRNA, protein, and hormonal regulation during the estrous cycle and early pregnancy in the pig. Mol. Reprod. Dev. 56, 378-386. doi:10.1002/1098- 2795(200007)56:3〈378::AID-MRD8〈3.0.CO;2-B
40. Lambert, C. M., and Weaver, D. R. (2006). Peripheral gene expression rhythms in a diurnal rodent. J. Biol. Rhythms 21, 77-79. doi:10.1177/ 0748730405281843
41. Li, X., and Davis, F. C. (2005). Developmental expression of clock genes in the Syrian hamster. Brain Res. Dev. Brain Res. 158, 31-40. doi:10.1016/J.DEVBRAINRES.2005.05.005
42. Liu, S., Cai, Y., Sothern, R. B., Guan, Y., and Chan, P. (2007). Chronobiological analysis of circadian patterns in transcription of seven key clock genes in six peripheral tissues in mice. Chronobiol. Int. 24, 793-820. doi:10.1080/07420520701672556
43. Lowrey, P. L., Shimomura, K., Antoch, M. P., Yamazaki, S., Zemenides, P.D., Ralph, M. R., Menaker, M., and Takahashi, J. S. (2000). Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science 288, 483-491. doi:10.1126/SCIENCE. 288.5465.483
44. Miller, B. H., Olson, S. L., Turek, F. W., Levine, J. E., Horton, T. H., and Takahashi, J. S. (2004). Circadian clock mutation disrupts estrous cyclicity and maintenance of pregnancy. Curr. Biol. 14, 1367-1373. doi:10.1016/J.CUB.2004.07.055
45. Morin, L. P., Fitzgerald, K. M., and Zucker, I. (1977). Estradiol shortens the period of hamster circadian rhythms. Science 196, 305-307. doi:10.1126/SCIENCE.557840
46. Morse, D., Cermakian, N., Brancorsini, S., Parvinen, M., and Sassone-Corsi, P. (2003). No circadian rhythms in testis: Period1 expression is clock independent and developmentally regulated in the mouse. Mol. Endocrinol. 17, 141-151. doi:10.1210/ME.2002-0184
47. Nakamura, T. J., Moriya, T., Inoue, S., Shimazoe, T., Watanabe, S., Ebihara, S., and Shinohara, K. (2005). 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. 82, 622-630. doi:10.1002/JNR.20677
48. Nakamura, T. J., Sellix, M. T., Menaker, M., and Block, G. D. (2008). Estrogen directly modulates circadian rhythms of PER2 expression in the uterus. Am. J. Physiol. Endocrinol. Metab., in press.
49. Ohta, H., Xu, S., Moriya, T., Iigo, M., Watanabe, T., et al. (2008). Maternal feeding controls fetal biological clock. PLoS One 3, e2601. doi:10.1371/JOURNAL.PONE.0002601
50. Oishi, K., Sakamoto, K., Okada, T., Nagase, T., and Ishida, N. (1998). 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. doi:10.1006/ BBRC.1998.9779
51. 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. doi:10.1006/BBRC.1999.2054
52. Okamura, H., Yamaguchi, S., Yagita, K., King, D. P., and Takahashi, J. S. (2002). Molecular machinery of the circadian clock in mammals. Cell Tissue Res. 309, 47-56.
53. Panda, S., Antoch, M. P., Miller, B. H., Su, A. I., Schook, A. B., Straume, M., Schultz, P. G., Kay, S. A., Takahashi, J. S., and Hogenesch, J. B. (2002). Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109, 307-320. doi:10.1016/S0092-8674(02)00722-5
54. Pilorz, V., and Steinlechner, S. (2008). Low reproductive success in Per1 and Per2 mutant mouse females due to accelerated ageing? Reproduction 135, 559-568. doi:10.1530/REP-07-0434
55. 14C-labeled deoxyglucose. J. Neurosci. 4, 1677-1682.
56. Reppert, S. M., and Uhl, G. R. (1987). Vasopressin messenger ribonucleic acid in supraoptic and suprachiasmatic nuclei: appearance and circadian regulation during development. Endocrinology 120, 2483-2487.
57. Reppert, S. M., Henshaw, D., Schwartz, W. J., and Weaver, D. R. (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. doi:10.1016/0006-8993(87)90084-9
58. Rush, B. L., Murad, A., Emery, P., and Giebultowicz, J. M. (2006). Ectopic CRYPTOCHROME renders TIM light sensitive in the Drosophila ovary. J. Biol. Rhythms 21, 272-278. doi:10.1177/0748730406290416
59. Saxena, M. T., Aton, S. J., Hildebolt, C., Prior, J. L., Abraham, U., Piwnica-Worms, D., and Herzog, E. D. (2007). Bioluminescence imaging of period1 gene expression in utero. Mol. Imaging 6, 68-72.
60. Seron-Ferre, M., Valenzuela, G. J., and Torres-Farfan, C. (2007). Circadian clocks during embryonic and fetal development. Birth Defects Res. C Embryo Today 81, 204-214. doi:10.1002/BDRC.20101
61. Shimomura, H., Moriya, T., Sudo, M., Wakamatsu, H., Akiyama, M., Miyake, Y., and Shibata, S. (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. doi:10.1046/J.0953-816X.2000.01438.X
62. Sládek, M., Sumová, A., Kováciková, Z., Bendová, Z., Laurinová, K., and Illnerová, H. (2004). Insight into molecular core clock mechanism of embryonic and early postnatal rat suprachiasmatic nucleus. Proc. Natl Acad. Sci. USA 101, 6231-6236. doi:10.1073/PNAS.0401149101
63. Tei, H., Okamura, H., Shigeyoshi, Y., Fukuhara, C., Ozawa, R., Hirose, M., and Sakaki, Y. (1997). Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature 389, 512-516. doi:10.1038/39086
64. Tong, Y., Guo, H., Brewer, J. M., Lee, H., Lehman, M. N., and Bittman, E. L. (2004). Expression of haPer1 and haBmal1 in Syrian hamsters: heterogeneity of transcripts and oscillations in the periphery. J. Biol. Rhythms 19, 113-125. doi:10.1177/0748730403262871
65. Torres-Farfan, C., Rocco, V., Monso, C., Valenzuela, F. J., Campino, C., Germain, A., Torrealba, F., Valenzuela, G. J., and Seron-Ferre, M. (2006). Maternal melatonin effects on clock gene expression in a nonhuman primate fetus. Endocrinology 147, 4618-4626. doi:10.1210/EN.2006-0628
66. Turek, F. W., Swann, J., and Earnest, D. J. (1984). Role of the circadian system in reproductive phenomena. Recent Prog. Horm. Res. 40, 143-183.
67. Viswanathan, N., and Davis, F. C. (1997). Single prenatal injections of melatonin or the D1-dopamine receptor agonist SKF 38393 to pregnant hamsters sets the offsprings' circadian rhythms to phases 180 degrees apart. J. Comp. Physiol. [A] 180, 339-346. doi:10.1007/S003590050053
68. Yamada, K., Kawata, H., Mizutani, T., Arima, T., Yazawa, T., et al. (2004). Gene expression of basic helix-loop-helix transcription factor, SHARP-2, is regulated by gonadotropins in the rat ovary and MA-10 cells. Biol. Reprod. 70, 76-82. doi:10.1095/BIOLREPROD.103.020107
69. Yamamoto, T., Nakahata, Y., Soma, H., Akashi, M., Mamine, T., and Takumi, T. (2004). Transcriptional oscillation of canonical clock genes in mouse peripheral tissues. BMC Mol. Biol. 5, 18. doi:10.1186/1471-2199-5- 18
70. Yoo, S. H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., 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. doi:10.1073/PNAS.0308709101
71. Ziv, L., and Gothilf, Y. (2006). Circadian time-keeping during early stages of development. Proc. Natl Acad. Sci. USA 103, 4146-4151. doi:10.1073/PNAS.0600571103
72. Zylka, M. J., Shearman, L. P., Weaver, D. R., and Reppert, S. M. (1998). Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron 20, 1103-1110. doi:10.1016/S0896-6273(00)80492-4