Mystery of rhythmic signal emergence within the suprachiasmatic nuclei
Jazyk angličtina Země Francie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
Grantová podpora
16-03932S
Czech Science Foundation - International
RV0: 67985823
Czech Science Foundation - International
CZ.2.16/3.1.00/21544
OPPK BrainView - International
PubMed
30188597
DOI
10.1111/ejn.14141
Knihovny.cz E-zdroje
- Klíčová slova
- circadian clock, clock gene, fetal development, mPer2luc mouse, rat,
- MeSH
- cirkadiánní hodiny * MeSH
- cirkadiánní rytmus * MeSH
- fotoperioda MeSH
- lidé MeSH
- nucleus suprachiasmaticus MeSH
- plod MeSH
- těhotenství MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- těhotenství MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
The circadian system provides organisms with a temporal organization that optimizes their adaptation to environmental fluctuations on a 24-hr basis. In mammals, the circadian clock in the suprachiasmatic nuclei (SCN) develops during the perinatal period. The rhythmicity first appears at the level of individual SCN neurons during the fetal stage, and this step is often misinterpreted as the time of complete SCN clock development. However, the process is only finalized when the SCN begin to play a role of the central clock in the body, that is, when they are able to generate robust rhythmicity at the cell population level, entrain the rhythmic signal with external light-dark cycles and convey this signal to the rest of the body. The development is gradual and correlates with morphological maturation of the SCN structural complexity, which is based on intercellular network formation. The aim of this review is to summarize events related to the first emergence of circadian oscillations in the fetal SCN clock. Although a large amount of data on ontogenesis of the circadian system have been accumulated, how exactly the immature SCN converts into a functional central clock has still remained rather elusive. In this review, the hypothesis of how the SCN attains its rhythmicity at the tissue level is discussed in context with the recent advances in the field. For an extensive summary of the complete ontogenetic development of the circadian system, the readers are referred to other previously published reviews.
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Ansari, N., Agathagelidis, M., Lee, C., Korf, H. W., & von Gall, C. (2009). Differential maturation of circadian rhythms in clock gene proteins in the suprachiasmatic nucleus and the pars tuberalis during mouse ontogeny. European Journal of Neuroscience, 29, 477-489. https://doi.org/10.1111/j.1460-9568.2008.06605.x
Bedont, J. L., & Blackshaw, S. (2015). Constructing the suprachiasmatic nucleus: A watchmaker's perspective on the central clockworks. Frontiers in Systems Neuroscience, 9, 74.
Bedont, J. L., LeGates, T. A., Slat, E. A., Byerly, M. S., Wang, H., Hu, J., … Blackshaw, S. (2014). Lhx1 controls terminal differentiation and circadian function of the suprachiasmatic nucleus. Cell Reports, 7, 609-622. https://doi.org/10.1016/j.celrep.2014.03.060
Carmona-Alcocer, V., Abel, J. H., Sun, T. C., Petzold, L. R., Doyle, F. J., Simms, C. L., & Herzog, E. D. (2018). Ontogeny of circadian rhythms and synchrony in the suprachiasmatic nucleus. Journal of Neuroscience, 38, 1326-1334. https://doi.org/10.1523/JNEUROSCI.2006-17.2017
Challet, E., Poirel, V. J., Malan, A., & Pévet, P. (2003). Light exposure during daytime modulates expression of Per1 and Per2 clock genes in the suprachiasmatic nuclei of mice. Journal of Neuroscience Research, 72, 629-637. https://doi.org/10.1002/jnr.10616
Christ, E., Korf, H. W., & von Gall, C. (2012). When does it start ticking? Ontogenetic development of the mammalian circadian system. Progress in Brain Research, 199, 105-118. https://doi.org/10.1016/B978-0-444-59427-3.00006-X
Daan, S., Spoelstra, K., Albrecht, U., Schmutz, I., Daan, M., Daan, B., … Lipp, H. P. (2011). Lab mice in the field: Unorthodox daily activity and effects of a dysfunctional circadian clock allele. Journal of Biological Rhythms, 26, 118-129. https://doi.org/10.1177/0748730410397645
Damiola, F., Le Minli, N., Preitner, N., Kornmann, B., Fleury-Olela, F., & Schibler, U. (2000). Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes & Development, 14, 2950-2961. https://doi.org/10.1101/gad.183500
Davis, F. C., & Gorski, R. A. (1988). Development of hamster circadian rhythms: Role of the maternal suprachiasmatic nucleus. Journal of Comparative Physiology A, 162, 601-610. https://doi.org/10.1007/BF01342635
Deguchi, T. (1975). Ontogenesis of a biological clock for serotonin:Acetyl coenzyme A N-acetyltransferase in pineal gland of rat. Proceedings of the National Academy of Sciences of the United States of America, 72, 2814-2818. https://doi.org/10.1073/pnas.72.7.2814
Dibner, C., Schibler, U., & Albrecht, U. (2010). The mammalian circadian timing system: Organization and coordination of central and peripheral clocks. Annual Review of Physiology, 72, 517-549. https://doi.org/10.1146/annurev-physiol-021909-135821
Dolatshad, H., Cary, A. J., & Davis, F. C. (2010). Differential expression of the circadian clock in maternal and embryonic tissues of mice. PLoS One, 5, e9855. https://doi.org/10.1371/journal.pone.0009855
El-Hennamy, R., Matějů, K., Bendová, Z., Sosniyenko, S., & Sumová, A. (2008). Maternal control of the fetal and neonatal rat suprachiasmatic nucleus. Journal of Biological Rhythms, 23, 435-444. https://doi.org/10.1177/0748730408322635
Groos, G., & Hendriks, J. (1982). Circadian rhythms in electrical discharge of rat suprachiasmatic neurones recorded in vitro. Neuroscience Letters, 34, 283-288. https://doi.org/10.1016/0304-3940(82)90189-6
Hara, R., Wan, K., Wakamatsu, H., Aida, R., Moriya, T., Akiyama, M., & Shibata, S. (2001). Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus. Genes to Cells, 6, 269-278. https://doi.org/10.1046/j.1365-2443.2001.00419.x
Hatori, M., Gill, S., Mure, L. S., Goulding, M., O'leary, D. D. M., & Panda, S. (2014). Lhx1 maintains synchrony among circadian oscillator neurons of the SCN. Elife, 3, 1-16. https://doi.org/10.1073/pnas.0308709101
Herzog, E. D., Aton, S. J., Numano, R., Sakaki, Y., & Tei, H. (2004). Temporal precision in the mammalian circadian system: A reliable clock from less reliable neurons. Journal of Biological Rhythms, 19, 35-46. https://doi.org/10.1177/0748730403260776
Herzog, E. D., Takahashi, J. S., & Block, G. D. (1998). Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nature Neuroscience, 1, 708-713. https://doi.org/10.1038/3708
Houdek, P., & Sumová, A. (2014). In vivo initiation of clock gene expression rhythmicity in fetal rat suprachiasmatic nuclei. PLoS One, 9, e107360. https://doi.org/10.1371/journal.pone.0107360
Jáč, M., Kiss, A., Sumová, A., Illnerová, H., & Ježová, D. (2000). Daily profiles of arginine vasopressin mRNA in the suprachiasmatic, supraoptic and paraventricular nuclei of the rat hypothalamus under various photoperiods. Brain Research, 887, 472-476.
Kabrita, C. S., & Davis, F. C. (2008). Development of the mouse suprachiasmatic nucleus: Determination of time of cell origin and spatial arrangements within the nucleus. Brain Research, 1195, 20-27. https://doi.org/10.1016/j.brainres.2007.12.020
Kornhauser, J. M., Nelson, D. E., Mayo, K. E., & Takahashi, J. S. (1992). Regulation of jun-B messenger RNA and AP-1 activity by light and a circadian clock. Science, 255, 1581-1584. https://doi.org/10.1126/science.1549784
Kováčiková, Z., Sládek, M., Bendová, Z., Illnerová, H., & Sumová, A. (2006). Expression of clock and clock-driven genes in the rat suprachiasmatic nucleus during late fetal and early postnatal development. Journal of Biological Rhythms, 21, 140-148.
Kuhlman, S. J., Silver, R., Le Sauter, J., Bult-Ito, A., & McMahon, D. G. (2003). Phase resetting light pulses induce Per1 and persistent spike activity in a subpopulation of biological clock neurons. Journal of Neuroscience, 23, 1441-1450. https://doi.org/10.1523/JNEUROSCI.23-04-01441.2003
Laemle, L. K. (1988). Vasoactive intestinal polypeptide (VIP)-like immunoreactivity in the suprachiasmatic nucleus of the perinatal rat. Brain Research, 469, 308-312. https://doi.org/10.1016/0165-3806(88)90193-9
Landgraf, D., Achten, C., Dallmann, F., & Oster, H. (2015). Embryonic development and maternal regulation of murine circadian clock function. Chronobiology International, 32, 416-427. https://doi.org/10.3109/07420528.2014.986576
Landgraf, D., Koch, C. E., & Oster, H. (2014). Embryonic development of circadian clocks in the mammalian suprachiasmatic nuclei. Frontiers in Neuroanatomy, 8, 1-7.
Li, X., & Davis, F. C. (2005). Developmental expression of clock genes in the Syrian hamster. Developmental Brain Research, 158, 31-40. https://doi.org/10.1016/j.devbrainres.2005.05.005
Liu, A. C., Welsh, D. K., Ko, C. H., Tran, H. G., Zhang, E. E., Priest, A. A., … Kay, S. A. (2007). Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell, 129(3), 605-616.
Maywood, E. S., Reddy, A. B., Wong, G. K. Y., O'Neill, J. S., O'Brien, J. A., McMahon, D. G., … Hastings, M. H. (2006). Synchronization and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling. Current Biology, 16, 599-605. https://doi.org/10.1016/j.cub.2006.02.023
Mohr, E., & Richter, D. (1990). Sequence analysis of the promoter region of the rat vasopressin gene. FEBS Letters, 260, 305-308. https://doi.org/10.1016/0014-5793(90)80130-B
Moore, R. Y., & Eichler, V. B. (1972). Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Research, 42, 201-206. https://doi.org/10.1016/0006-8993(72)90054-6
Nishide, S. Y., Honma, S., & Honma, K. I. (2008). The circadian pacemaker in the cultured suprachiasmatic nucleus from pup mice is highly sensitive to external perturbation. European Journal of Neuroscience, 27, 2686-2690. https://doi.org/10.1111/j.1460-9568.2008.06231.x
Nováková, M., Sládek, M., & Sumová, A. (2010). 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. Journal of Biological Rhythms, 25, 350-360. https://doi.org/10.1177/0748730410377967
Ohta, H., Honma, S., Abe, H., & Honma, K. I. (2002). Effects of nursing mothers on rPer1 and rPer2 circadian expressions in the neonatal rat suprachiasmatic nuclei vary with developmental stage. European Journal of Neuroscience, 15, 1953-1960. https://doi.org/10.1046/j.1460-9568.2002.02016.x
Ohta, H., Honma, S., Abe, H., & Honma, K. I. (2003). Periodic absence of nursing mothers phase-shifts circadian rhythms of clock genes in the suprachiasmatic nucleus of rat pups. European Journal of Neuroscience, 17, 1628-1634. https://doi.org/10.1046/j.1460-9568.2003.02584.x
Ohta, H., Yamazaki, S., & McMahon, D. G. (2005). Constant light desynchronizes mammalian clock neurons. Nature Neuroscience, 8, 267-269. https://doi.org/10.1038/nn1395
Okamoto, K., & Aoki, K. (1963). Development of a strain of spontaneously hypertensive rats. Japanese Circulation Journal, 27, 282-293. https://doi.org/10.1253/jcj.27.282
Olejníková, L., Polidarová, L., Paušlyová, L., Sládek, M., & Sumová, A. (2015). Diverse development and higher sensitivity of the circadian clocks to changes in maternal-feeding regime in a rat model of cardio-metabolic disease. Chronobiology International, 32, 531-547. https://doi.org/10.3109/07420528.2015.1014095
O'Neill, J. S., & Reddy, A. B. (2012). The essential role of cAMP/Ca 2+ signalling in mammalian circadian timekeeping. Biochemical Society Transactions, 40, 44-50. https://doi.org/10.1042/BST20110691
Panda, S., Antoch, M. P., Miller, B. H., Su, A. I., Schook, A. B., Straume, M., … Hogenesch, J. B. (2002). Coordinated transcription of key pathways in the mouse by the circadian clock. Cell, 109, 307-320. https://doi.org/10.1016/S0092-8674(02)00722-5
Paulose, J. K., Rucker, E. B., & Cassone, V. M. (2012). Toward the beginning of time: Circadian rhythms in metabolism precede rhythms in clock gene expression in mouse embryonic stem cells. PLoS One, 7, e49555. https://doi.org/10.1371/journal.pone.0049555
Polidarová, L., Sládek, M., Nováková, M., Parkanová, D., & Sumová, A. (2013). Increased sensitivity of the circadian system to temporal changes in the feeding regime of spontaneously hypertensive rats - a potential role for Bmal2 in the liver. PLoS One, 8, 1-18.
Prolo, L. M., Takahashi, J. S., & Herzog, E. D. (2005). Circadian rhythm generation and entrainment in astrocytes. Journal of Neuroscience, 25, 404-408. https://doi.org/10.1523/JNEUROSCI.4133-04.2005
Ralph, M. R., Foster, R. G., Davis, F. C., & Menaker, M. (1990). Transplanted suprachiasmatic nucleus determines circadian period. Science, 247, 975-978. https://doi.org/10.1126/science.2305266
Ralph, M. R., & Menaker, M. (1988). A mutation of the circadian system in golden hamsters. Science, 241, 1225-1227. https://doi.org/10.1126/science.3413487
Reppert, S. M., Coleman, R. J., Heath, H. W., & Swedlow, J. R. (1984). Pineal N-acetyltransferase activity in 10-day-old rats: A paradigm for studying the developing circadian system. Endocrinology, 115, 918-925. https://doi.org/10.1210/endo-115-3-918
Reppert, S. M., & Schwartz, W. J. (1986). Maternal suprachiasmatic nuclei are necessary for maternal coordination of the developing circadian system. Journal of Neuroscience, 6, 2724-2729. https://doi.org/10.1523/JNEUROSCI.06-09-02724.1986
Reppert, S. M., & Uhl, G. R. (1982). Vasopressin mesenger ribonucleic acid in supraoptic and suprachiasmatic nuclei: Appearance and circadian regulation during development. Endocrinology, 120, 2483-2487.
Schibler, U., Ripperger, J., & Brown, S. A. (2003). Peripheral circadian oscillators in mammals: Time and food. Journal of Biological Rhythms, 18, 250-260. https://doi.org/10.1177/0748730403018003007
Schubert, K. A., Vaanholt, L. M., Stavasius, F., Demas, G. E., Daan, S., & Visser, G. H. (2008). Female mice respond differently to costly foraging versus food restriction. Journal of Experimental Biology, 211, 2214-2223. https://doi.org/10.1242/jeb.017525
Schwartz, W. J., & Gainer, H. (1977). Suprachiasmatic nucleus: Use of 14C-labeled deoxyglucose uptake as a functional marker. Science, 197, 1089-1091. https://doi.org/10.1126/science.887940
Seron-Ferre, M., Valenzuela, G. J., & Torres-Farfan, C. (2007). Circadian clocks during embryonic and fetal development. Birth Defects Research, Part C: Embryo Today, Reviews, 81, 204-214. https://doi.org/10.1002/(ISSN)1542-9768
Shibata, S., & Moore, R. Y. (1987). Development of neuronal activity in the rat suprachiasmatic nucleus. Brain Research, 431, 311-315. https://doi.org/10.1016/0165-3806(87)90220-3
Shimada, M., & Nakamura, T. (1973). Time of neuron origin in mouse hypothalamic nuclei. Experimental Neurology, 41, 163-173. https://doi.org/10.1016/0014-4886(73)90187-8
Shimogori, T., Lee, D. A., Miranda-Angulo, A., Yang, Y., Wang, H., Jiang, L., … Blackshaw, S. (2010). A genomic atlas of mouse hypothalamic development. Nature Neuroscience, 13, 767. https://doi.org/10.1038/nn.2545
Shimomura, H., Moriya, T., Sudo, M., Wakamatsu, H., Akiyama, M., Miyake, Y., & Shibata, S. (2001). Differential daily expression of Per1 and Per2 mRNA in the suprachiasmatic nucleus of fetal and early postnatal mice. European Journal of Neuroscience, 13, 687-693. https://doi.org/10.1046/j.0953-816x.2000.01438.x
Sládek, M., Polidarová, L., Nováková, M., Parkanová, D., & Sumová, A. (2012). Early chronotype and tissue-specific alterations of circadian clock function in spontaneously hypertensive rats. PLoS One, 7, e46951. https://doi.org/10.1371/journal.pone.0046951
Sládek, M., Sumová, A., Kováčiková, Z., Bendová, Z., Laurinová, K., & Illnerová, H. (2004). Insight into molecular core clock mechanism of embryonic and early postnatal rat suprachiasmatic nucleus. Proceedings of the National Academy of Sciences of the United States of America, 101, 6231-6236. https://doi.org/10.1073/pnas.0401149101
Stephan, F. K., & Zucker, I. (1972). Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proceedings of the National Academy of Sciences of the United States of America, 69, 1583-1586. https://doi.org/10.1073/pnas.69.6.1583
Sumová, A., Bendová, Z., Sládek, M., El-Hennamy, R., Laurinová, K., Jindráková, Z., & Illnerová, H. (2006). Setting the biological time in central and peripheral clocks during ontogenesis. FEBS Letters, 580, 2836-2842. https://doi.org/10.1016/j.febslet.2006.03.023
Sumová, A., Bendová, Z., Sládek, M., El-Hennamy, R., Matejů, K., Polidarová, L., … Illnerová, H. (2008). Circadian molecular clocks tick along ontogenesis. Physiological Research, 57(Suppl 3), S139-S148.
Sumová, A., Sládek, M., Jác, M., & Illnerová, H. (2002). The circadian rhythm of Per1 gene product in the rat suprachiasmatic nucleus and its modulation by seasonal changes in daylength. Brain Research, 947, 260-270. https://doi.org/10.1016/S0006-8993(02)02933-5
Sumová, A., Sládek, M., Polidarová, L., Nováková, M., & Houdek, P. (2012). Circadian system from conception till adulthood. Progress in Brain Research, 199, 83-103.
Sumová, A., Trávníčková, Z., Mikkelsen, J. D., & Illnerová, H. (1998). Spontaneous rhythm in c-Fos immunoreactivity in the dorsomedial part of the rat suprachiasmatic nucleus. Brain Research, 801, 254-258. https://doi.org/10.1016/S0006-8993(98)00619-2
Swislocki, A., & Tsuzuki, A. (1993). Insulin resistance and hypertension: Glucose intolerance, hyperinsulinemia, and elevated free fatty acids in the lean spontaneously hypertensive rat. American Journal of the Medical Sciences, 306, 282-286. https://doi.org/10.1097/00000441-199311000-00002
Takahashi, J. S. (2017). Transcriptional architecture of the mammalian circadian clock. Nature Reviews Genetics, 18, 164-179. https://doi.org/10.1038/nrg.2016.150
Takahashi, K., Hayafuji, C., & Murakami, N. (1982). Foster mother rat entrains circadian adrenocortical rhythm in blinded pups. American Journal of Physiology, 243, E443-E449.
VanDunk, C., Hunter, L. A., & Gray, P. A. (2011). Development, maturation, and necessity of transcription factors in the mouse suprachiasmatic nucleus. Journal of Neuroscience, 31, 6457-6467. https://doi.org/10.1523/JNEUROSCI.5385-10.2011
Viswanathan, N., & 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. Journal of Comparative Physiology A, 180, 339-346. https://doi.org/10.1007/s003590050053
Viswanathan, N., Weaver, D. R., Reppert, S. M., & Davis, F. C. (1994). Entrainment of the fetal hamster circadian pacemaker injections of the dopamine agonist SKF 38393 by prenatal. Journal of Neuroscience, 14, 5393-5398. https://doi.org/10.1523/JNEUROSCI.14-09-05393.1994
Weaver, D. R., & Reppert, S. M. (1989). Periodic feeding of SCN-lesioned pregnant rats entrains the fetal biological clock. Developmental Brain Research, 46, 291-295. https://doi.org/10.1016/0165-3806(89)90292-7
Webb, A. B., Angelo, N., Huettner, J. E., & Herzog, E. D. (2009). Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons. Proceedings of the National Academy of Sciences of the United States of America, 106, 16493-16498. https://doi.org/10.1073/pnas.0902768106
Weinert, D. (2005). Ontogenetic development of the mammalian circadian system. Chronobiology International, 22, 179-205. https://doi.org/10.1081/CBI-200053473
Welsh, D. K., Logothetis, D. E., Meister, M., & Reppert, S. M. (1995). Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron, 14, 697-706. https://doi.org/10.1016/0896-6273(95)90214-7
Wreschnig, D., Dolatshad, H., & Davis, F. C. (2014). Embryonic development of circadian oscillations in the mouse hypothalamus. Journal of Biological Rhythms, 29, 299-310. https://doi.org/10.1177/0748730414545086
Yagita, K., Horie, K., Koinuma, S., Nakamura, W., Yamanaka, I., Urasaki, A., … Uchiyama, Y. (2010). Development of the circadian oscillator during differentiation of mouse embryonic stem cells in vitro. Proceedings of the National Academy of Sciences of the United States of America, 107, 3846-3851. https://doi.org/10.1073/pnas.0913256107
Yambe, Y., Arima, H., Kakiya, S., Murase, T., & Oiso, Y. (2002). Diurnal changes in arginine vasopressin gene transcription in the rat suprachiasmatic nucleus. Brain Research. Molecular Brain Research, 104, 132-136. https://doi.org/10.1016/S0169-328X(02)00327-3
Yoo, S. H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., Buhr, E. D., … Takahashi, J. S. (2004). PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proceedings of the National Academy of Sciences of the United States of America, 101, 5339-5346.