Molecular Cloning,Characterisation,Tissue Distribution,and mRNA Expression Changes under Different Light Regimes of Brain and Muscle Arnt-Like Protein-1 (BMAL1) in Columba Livia
Restricted accessResearch articleFirst published online August, 2017
Molecular Cloning,Characterisation,Tissue Distribution,and mRNA Expression Changes under Different Light Regimes of Brain and Muscle Arnt-Like Protein-1 (BMAL1) in Columba Livia
Brain and muscle Arnt-like protein-1 (BMAL1) plays an important role in circadian rhythm, which is involved in daily behaviours and physiological activities. However, little is known about the molecular function of BMAL1 in the Pigeon (Columba livia). In our study, the full-length cDNA of Bmal1 was cloned and sequenced from the Pigeon for the first time, and submitted to the GenBank to obtain the accession number (KF906247). The full-length cDNA of Bmal1 consists of 2,488 nucleotides, and encodes 634 amino acids. Phylogenetic analysis showed that it bore the greatest similarity to Bmal1 from the Chicken (Gallus gallus) and Barn Owl (Tyto alba). The amino acid sequence of the Pigeon BMAL1 contained a HLH domain and two PAS domains, which are involved in forming hetero-homodimers with the CLOCK as the positive element of the circadian rhythm. The results of real-time quantitative PCR of Bmal1 under different light regimes showed that the amplitude and expression pattern of Bmal1 were strongly affected by day length. Bmal1 was most highly expressed in the pancreas. Relative to Bmal1 expression level under 12 h of light exposure, it was increased significantly in the pituitary gland, ovary and uterus under 15 h of light exposure (P < 0.05). However, other tissues, including the hypothalamus, heart, liver, spleen, kidney, intestines, crureus, and pectorals exhibited no significant difference (P < 0.05) under the two light regimes. This is the first study to investigate Bmal1 mRNA levels in various tissues under different light cycles, and thereby provide data for further study of the molecular and regulatory mechanisms of Bmal1 and circadian clock genes of the Pigeon.
BodenM.J., VarcoeT.J., VoultsiosA. and KennawayD.J. (2010) Reproductive biology of female Bmal1 null mice. Reproduction, 139, 1077–1090.
2.
BungerM.K., WilsbacherL.D., MoranS.M., ClendeninC., RadcliffeL.A., HogeneschJ.B. and BradfieldC.A. (2000) Mop3 is an essential component of the master circadian pacemaker in mammals. Cell, 103, 1009–1017.
3.
BurI.M., ZouaouiS., FontanaudP., CoutryN., MolinoF., MartinA.O. and BonnefontX. (2010) The comparison between circadian oscillators in mouse liver and pituitary gland reveals different integration of feeding and light schedules. PloS one, 5, e15316.
4.
ChiesaJ.J., CambrasT., Carpentieriá.R. and Díez-NogueraA. (2010) Arrhythmic rats after SCN lesions and constant light differ in short time scale regulation of locomotor activity. J. Biol. Rhythm., 25, 37–46.
5.
ChuA., ZhuL., BlumI.D., MaiO., LeliavskiA., FahrenkrugJ. and StorchK.F. (2013) Global but not gonadotrope-specific disruption of Bmal1 abolishes the luteinizing hormone surge without affecting ovulation. Endocrinology, 154, 2924–2935.
6.
DibnerC., SchiblerU. and AlbrechtU. (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol., 72, 517–549.
7.
FidlerA.E. and GwinnerE. (2003) Comparative analysis of avian BMAL1 and CLOCK protein sequences: a search for features associated with owl nocturnal behaviour. Comp. Biochem. Phys. B, 136, 861–874.
8.
GekakisN., StaknisD., NguyenH.B., DavisF.C., WilsbacherL.D., KingD.P. and WeitzC.J. (1998) Role of the CLOCK protein in the mammalian circadian mechanism. Science, 280, 1564–1569.
9.
GvakhariaB.O., KilgoreJ.A., BebasP. and GiebultowiczJ.M. (2000) Temporal and spatial expression of the period gene in the reproductive system of the codling moth. J. Biol. Rhythm., 15, 4–12.
10.
HoffmannK. (1981) Biological rhythms. In: AschoffJ. (ed.), Handbook of behavioral neurobiology, pp. 449–473. Plenum Press, New York and London.
11.
HogeneschJ.B. and HerzogE.D. (2011) Intracellular and intercellular processes determine robustness of the circadian clock. FEBS Lett., 585, 1427–1434.
12.
HuangZ.J., EderyI. and RosbashM. (1993) PAS is a dimerization domain common to Drosophila period and several transcription factors. Nature, 364, 259–262.
13.
IkedaM. and NomuraM. (1997) cDNA cloning and tissue-specific expression of a novel basic helix–loop–helix/PAS protein (BMAL1) and identification of alternatively spliced variants with alternative translation initiation site usage. Biochem. Biophys. Res. Commun., 233, 258–264.
14.
IwaiS., FukuiY., FujiwaraY. and TakedaM. (2006) Structure and expressions of two circadian clock genes, period and timeless in the commercial silkmoth, Bombyx mori. J. Insect. Physiol., 52, 625–637.
15.
JohnstonJ.D., EblingF.J. and HazleriggD.G. (2005) Photoperiod regulates multiple gene expression in the suprachiasmatic nuclei and pars tuberalis of the Siberian hamster (Phodopus sungorus). Eur. J. Neurosci., 21, 2967–2974.
16.
KennawayD.J. (2005) The role of circadian rhythmicity in reproduction. Hum. Reprod. Update, 11, 91–101.
17.
KennawayD.J., BodenM.J. and VarcoeT.J. (2012) Circadian rhythms and fertility. Mol. Cell. Endocrinol., 349, 56–61.
18.
KondratovR.V., ChernovM.V., KondratovaA.A., GorbachevaV.Y., GudkovA.V. and AntochM.P. (2003) BMAL1-dependent circadian oscillation of nuclear CLOCK: posttranslational events induced by dimerization of transcriptional activators of the mammalian clock system. Genes Dev., 17, 1921–1932.
19.
KumeK., ZylkaM.J., SriramS., ShearmanL.P., WeaverD.R., JinX. and ReppertS.M. (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell, 98, 193–205.
20.
LiM.D., RuanH.B., HughesM.E., LeeJ.S., SinghJ.P., JonesS.P. and YangX. (2013) O-GlcNAc signaling entrains the circadian clock by inhibiting BMAL1/CLOCK ubiquitination. Cell Metab., 17, 303–310.
21.
LiuY., JohnsonB.P., ShenA.L., WallisserJ.A., KrentzK.J., MoranS.M. and SchulerL.A. (2014) Loss of BMAL1 in ovarian steroidogenic cells results in implantation failure in female mice. Proc. Natl Acad. Sci. USA, 111, 14295–14300.
22.
LivakK.J. and SchmittgeT.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the2-ΔΔCT method. Methods, 25, 402–408.
23.
MarchevaB., RamseyK.M., BuhrE.D., KobayashiY., SuH., KoC.H. and LopezJ.P. (2010) Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature, 466, 627–631.
24.
MarkovaE.P., UedaH., SakamotoK., OishiK., ShimadaT. and TakedaM. (2003) Cloning of Cyc (Bmal1) homolog in Bombyx mori: structural analysis and tissue specific distributions. Comp. Biochem. Phys. B, 134, 535–542.
25.
MooreR.Y. (1996) Hypothalamic integration of circadian rhythms. In: BuijsR.M., KalsbeekA., RomijnH.J., MirmiranM. and PennartzC.M.A. (eds), Entrainment pathways and the functional organization of the circadian timing system, pp. 101–117. Elsevier Science B.V., Netherlands.
26.
NakaoN., YasuoS., NishimuraA., YamamuraT., WatanabeT., AnrakuT. and YoshimuraT. (2007) Circadian clock gene regulation of steroidogenic acute regulatory protein gene expression in preovulatory ovarian follicles. Endocrinology, 148, 3031–3038.
27.
NishideS.Y., HonmaS., NakajimaY., IkedaM., BabaK., OhmiyaY. and HonmaK.I. (2006) New reporter system for Per1 and Bmal1 expressions revealed self-sustained circadian rhythms in peripheral tissues. Genes Cells, 11, 1173–1182.
28.
NovákováM., PolidarováL., SládekM. and SumováA. (2011) Restricted feeding regime affects clock gene expression profiles in the suprachiasmatic nucleus of rats exposed to constant light. Neurosci., 197, 65–71.
29.
Nuesslein-HildesheimB., O'BrienJ.A., EblingF.J., MaywoodE.S. and HastingsM.H. (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.
30.
OkanoT., YamamotoK., OkanoK., HirotaT., KasaharaT., SasakiM. and FukadaY. (2001) Chicken pineal clock genes: implication of BMAL2 as a bidirectional regulator in circadian clock oscillation. Genes Cells, 6, 825–836.
31.
PittendrighC.L. (1981) Circadian systems: entrainment. In: AschoffJ. (ed.), Biological rhythms handbook of behavioral, pp. 95–124. Plenum Press, New York and London.
32.
PittendrighCS. (1993) Temporal organization: reflections of a Darwinian clock-watcher. Annu. Rev. Physiol., 55, 16–54.
33.
ReyesH., Reisz-PorszaszS. and HankinsonO. (1992) Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor. Science, 256, 1193.
34.
SanadaK. and OkanoT.Y. (2002) Mitogen-activated protein kinase phosphorylates and negatively regulates basic helix-loop-helix-PAS transcription factor BMAL1. J. Bio. Chemist, 277, 267–271.
35.
SchiblerU. (2005) The daily rhythms of genes, cells and organs. Biological clocks and circadian timing in cells. EMBO Rep., 6, S9–S13.
36.
ShimbaS., IshiiN., OhtaY., OhnoT., WatabeY., HayashiM. and TezukaM. (2005) Brain and muscle Arnt-like protein-1 (BMAL1), a component of the molecular clock, regulates adipogenesis. Proc. Natl Acad. Sci. USA, 102, 12071–12076.
37.
SumováA., JáčM., SládekM., ŠaumanI. and IllnerováH. (2003) Clock gene daily profiles and their phase relationship in the rat suprachiasmatic nucleus are affected by photoperiod. J. Biol. Rhythm., 18, 134–144.
38.
TakahashiJ.S, HongH.K, KoC.H. and McDearmonE.L. (2008) The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet, 9, 764–775.
39.
WelshD., LogothetisD., MeisterM. and ReppertS. (1995) Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron, 14, 697–706.
40.
WidemanC.H. and MurphyH.M. (2009) Constant light induces alterations in melatonin levels, food intake, feed efficiency, visceral adiposity, and circadian rhythms in rats. Nutr. Neurosci., 12, 233–240.
