Circadian Clock Genes of Goldfish,Carassius auratus : cDNA Cloning and Rhythmic Expression of Period and Cryptochrome Transcripts in Retina,Liver,and Gut
Free accessResearch articleFirst published online April, 2009
Circadian Clock Genes of Goldfish,Carassius auratus : cDNA Cloning and Rhythmic Expression of Period and Cryptochrome Transcripts in Retina,Liver,and Gut
Clock genes are known to be the molecular core of biological clocks of vertebrates. They are expressed not only in those tissues considered central pacemakers, but also in peripheral tissues. In the present study, partial cDNAs for 6 of the principal clock genes (Period 1-3 and Cryptochrome 1-3) were cloned from a teleost fish, the goldfish (Carassius auratus ). These genes showed high homology (approximately 90%) with the respective cDNAs of zebrafish (Danio rerio), the only other teleost from which clock genes have been cloned. The daily expression pattern of each gene in retina, gut, and liver of goldfish was investigated using quantitative RT-PCR and cosinor analysis. All clock genes analyzed in the retina showed circadian rhythmicity; however, only Per 2-3 and Cry 2-3 were rhythmic in goldfish liver and gut. The amplitude and phase of the expression in liver and gut were different from those found in goldfish retina. Such differences suggest that other cues, such as feeding time, may contribute to the entrainment of oscillators in goldfish liver and gut. Our results support the use of goldfish as a teleost model to investigate the location and functioning of the circadian oscillators.
Andersson H., Johnston JP, Messager S., Hazlerigg D., and Lincoln G. (2005) Photoperiod regulates clock gene rhythms in the ovine liver. Gen Comp Endocrinol142:357-363.
2.
Aranda A., Madrid JA, and Sánchez-Vázquez FJ (2001) Influence of light on feeding anticipatory activity in goldfish. J Biol Rhythms16:50-57.
3.
Balsalobre A. (2002) Clock genes in mammalian peripheral tissues. Cell Tissue Res309:193-199.
4.
Boujard T. and Leatherland JF (1992) Circadian rhythms and feeding time in fishes. Environ Biol Fish35: 109-131.
5.
Brown SA, Zumbrunn G., Fleury-Olela F., Preitner N., and Schibler U. (2002) Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Curr Biol12:1574-1583.
6.
Cahill GM (2002) Clock mechanisms in zebrafish. Cell Tissue Res309:27-34.
7.
Castillo MR, Hochstetler KJ, Tavernier Jr RJ, Greene DM, and Bult-Ito A. (2004) Entrainment of the master circadian clock by scheduled feeding. Am J Physiol Regul Integr Comp Physiol287:R551-R555.
8.
Chaurasia SS, Pozdeyev N., Haque R., Visser A., Ivanova TN, and Iuvone PM (2006) Circadian clockwork machinery in neural retina: evidence for the presence of functional clock components in photoreceptor-enriched chick retinal cell cultures. Mol Vis12:215-223.
9.
Chong NW, Chaurasia SS, Haque R., Klein DC, and Iuvone PM (2003) Temporal-spatial characterization of chicken clock genes: circadian expression in retina, pineal gland and peripheral tissues . J Neurochem85:851-860.
10.
Damiola F., Le Minh N., 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 . Gene Dev14:2950-2961.
11.
DeBruyne JP, Weaver DR, and Reppert SM (2007) Peripheral circadian oscillators require CLOCK . Curr Biol17:R538-R539.
12.
Delaunay F., Thisse C., Marchand O., Laudet V., and Thisse B. (2000) An inherited functional circadian clock in zebrafish embryos. Science289:297-300.
13.
Delaunay F., Thisse C., Thisse B., and Laudet V. (2003) Differential regulation of Period 2 and Period 3 expression during development of the zebrafish circadian clock. Gene Expr Patterns3:319-324.
14.
Delgado MJ, Alonso-Gómez AL, Gancedo B., De Pedro N., Valenciano AI, and Alonso-Bedate M. (1993) Serotonin N-acetyltransferase (NAT) activity and melatonin levels in the frog retina are not correlated during the seasonal cycle. Gen Comp Endocrinol92:143-150.
15.
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. Gene363:105-112.
16.
Falcon J. (1999) Cellular circadian clocks in the pineal. Prog Neurobiol58:121-162.
17.
Feillet CA, Ripperger JA, Magnone MC, Dulloo A., Albrecht U., and Challet E. (2006) Lack of food anticipation in Per2 mutant mice. Curr Biol16:2016-2022.
18.
Fu Z., Inaba M., Noguchi T., and Kato H. (2002) Molecular cloning and circadian regulation of Cryptochrome genes in Japanese quail (Coturnix coturnix japonica). J Biol Rhythms17:14-27.
19.
Haque R., Chaurasia SS, Wessel JH III, and Iuvone PM (2002) Dual regulation of cryptochrome 1 mRNA expression in chicken retina by light and circadian oscillators. Neuroreport13:2247-2251.
20.
Hoogerwerf WA, Hellmich HL, Cornelissen G., Halberg F., Shahinian VB, Bostwick J., Savidge TC, and Cassone V. (2007) Clock gene expression in the murine gastrointestinal tract: Endogenous rhythmicity and effects of a feeding regimen. Gastroenterology133:1250-1260.
21.
Iijima M., Yamaguchi S., van der Horst GTJ, Bonnefont X., Okamura H., and Shibata S. (2005) Altered food-anticipatory activity rhythm in Cryptochrome-deficient mice. Neurosci Res52:166-173.
22.
Iuvone PM, Tosini G., Pozdeyev N., Haque R., Klein DC, and Chaurasia SS (2005) Circadian clocks, clock networks, arylalkylamine N-acetyltransferase, and melatonin in the retina. Prog Retin Eye Res24:433-456.
23.
Kaneko M., Hernandez-Borsetti N., and Cahill GM (2006) Diversity of zebrafish peripheral oscillators revealed by luciferase reporting. Proc Natl Acad Sci U S A103:14614-14619.
24.
Kamphuis W., Cailotto C., Dijk F., Bergen A., and Buijs RM (2005) Circadian expression of clock genes and clock-controlled genes in the rat retina. Biochem Biophys Res Commun330:18-26.
25.
Klein DC, Moore RY, and Reppert SM (1991) Suprachiasmatic Nucleus: The Mind's Clock. New York: Oxford University Press.
26.
Kobayashi K., Kanno S., Smit B., van der Host GT, Takao M., and Yasui A. (1998) Characterization of photolyase/bluelight receptor homologs in mouse and human cells. Nucleic Acids Res26:5086-5092.
27.
Kobayashi Y., Ishikawa T., Hirayama J., Daiyasu H., Kanai S., Toh H., Fukuda I., Tsujimura T., Terada N., Kamei Y., et al. (2000) Molecular analysis of zebrafish photolyase/cryptochrome family: Two types of cryptochromes present in zebrafish. Genes Cells5:725-738.
28.
Mendoza J. (2007) Circadian clocks: Setting time by food. J Neuroendocrinol19:127-137.
29.
Mendoza J., Graff C., Dardente H., Pevet P., and Challet E. (2005) Feeding cues alter clock gene oscillation and photic responses in the suprachiasmatic nuclei of mice exposed to a light/dark cycle . J Neurosci25:1514-1522.
30.
Muhlbauer E., Wolgast S., Finckh U., Peschke D., and Peschke E. (2004) Indication of circadian oscillations in the rat pancreas. FEBS Lett564:91-96.
31.
Okamura H., Yamaguchi S., and Yagita K. (2002) Molecular machinery of the circadian clock in mammals . Cell Tissue Res309:47-56.
32.
Panda S., Hogenesch JB, and Kay SA (2002) Circadian rhythms from flies to human. Nature417:329-335.
33.
Pardini L., Kaeffer B., Trubuil A., Bourreille A., and Galmiche JP (2005) Human intestinal circadian clock: expression of clock genes in colonocytes lining the crypt. Chronobiol Int22:951-961.
34.
Peirson SN, Butler JN, Duffield GE, Takher S., Sharma P., and Foster RG (2006) Comparison of clock gene expression in SCN, retina, heart, and liver of mice. Biochem Biophys Res Commun351:800-807.
35.
Pitts S., Perone E., and Silver R. (2003) Food-entrained circadian rhythms are sustained in arrhythmic Clk/Clk mutant mice. Am J Physiol Regul Integr Comp Physiol285:R57-R67.
36.
Polakof S., Ceinos RM, Fernández-Durán B., Míguez JM, and Soengas JL (2007) Daily changes in parameters of energy metabolism in liver, white muscle, and gills of rainbow trout: dependence on feeding . Comp Biochem Physiol146:265-273.
37.
Postlethwait JH, Yan YL, Gates M., Horne S., Amores A., Brownlie A., Donovan A., Egan E., Force A., Gong Z., et al. (1998) Vertebrate genome evolution and the zebrafish genome map. Nat Genet18:345-349.
38.
Reyes BA, Pendergast JS, and Yamazaki S. (2008) Mammalian circadian peripheral oscillators are temperature compensated. J Biol Rhythms23:95-98.
39.
Stanewsky R (2002) Clock mechanisms in Drosophila. Cell Tissue Res309:11-26.
40.
Stephan FK, Swann JM, and Sisk CL (1979) Entrainment of circadian rhythms by feeding schedules in rats with suprachiasmatic lesions. Behav Neural Biol25:545-554.
41.
Stokkan KA, Yamazaki S., Tei H., Sakaki Y., and Menaker M. (2001) Entrainment of the circadian clock in the liver by feeding. Science291:490-493.
42.
Underwood H., Steele CT, and Zivokovic B. (2001) Circadian organization and the role of the pineal in birds. Microsc Res Techn53:48-62.
43.
Vallone D., Frigato E., Vernesi C., Foa A., Foulkes NS, and Bertolucci C. (2007) Hypothermia modulates circadian clock gene expression in lizard peripheral tissues. Am J Physiol Regul Integr Comp Physiol292:R160-R166.
44.
Vera LM, De Pedro N., Gómez-Milán E., Delgado MJ, Sánchez-Muros MJ, Madrid JA, and Sánchez-Vázquez FJ (2007) Feeding entrainment of locomotor activity rhythms, digestive enzymes and neuroendocrine factors in goldfish. Physiol Behav90:518-524.
45.
Whitmore D., Foulkes NS, Strahle U., and Sassone-Corsi P. (1998) Zebrafish Clock rhythmic expression reveals independent peripheral circadian oscillators. Nat Neurosci1:701-707.
46.
Yoo SH, Yamazaki S., Lowrey PL, Shimomura K., Ko CH, Burh ED, Siepka SM, Hong HK, Oh WJ, Yoo OJ, et al. (2004) PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A101:5339-5346.
47.
Yoshimura T., Suzuki Y., Makino E., Suzuki T., Kuroiwa A., Matsuda Y., Namikawa T., and Ebihara S. (2000) Molecular analysis of avian circadian clock genes . Brain Res Mol Brain Res78:207-215.
48.
Zhuang M., Wang Y., Steenhard BM, and Besharse JC (2000) Differential regulation of two period genes in the Xenopus eye. Brain Res Mol Brain Res82:52-64.
49.
Zvonic S., Ptitsyn AA, Conrad SA, Scott LK, Floyd ZE, Kilroy G., Wu X., Goh BC, Mynatt RL, and Gimble JM (2006) Characterization of peripheral circadian clocks in adipose tissues. Diabetes55:962-970.
