Clock Gene in Animal Update: 2009.8.17 Site Map
List of clock genes Outline of clock genes Animal model List of animals

Outline of Clock Genes

Core Loop
PERIOD CLOCK ARNTL (BMAL) CRY (mammal) timeless (fly)
Interlocking Loop
DEC1,2 ID1-4 E4BP4 (vri) Pdp1 (fly) REV-ERB  ROR  SIRT1
cry (fly) GSK3B CSNK1E, D CSNK2A BTRC (slmb) FBXL3 JET  PP
Appendix Phosphorylation of Clock Proeins, Domains of Clock Gene Product

Conceptual diagram of molecular oscillation of circadian clock (Modified from Hamilton2008).

PERIOD →Homolog list→Mutant list

Synonyms PERIOD,PER; per, Clk, clk-6, CG2647 (fly)
Class Transcription regulatory protein (Repressor of CLOCK/ARNTL)
Outline Period is one of the "core loop" gene.
In Drosophila, PER/TIM complex was transported into the nucleus, then inhibit CLK/CYC activity. Loss of function mutant of Drosophila, per01, shows arrhythmic behavior. perL and perS show 28-30 h and 19 h period of activity, respectively.
In Mammal, PER was transported into the nucleus with CRY. Single KO mouse for Per1, 2 or 3 shows altered period. Per1 and Per2 W-KO mouse shows arrhythmic behavior (See mutant list of Period). Per3 is not necessary for circadian rhythms in mice (Shearman2000).
In human FASPS, a polymorphism in PER2 phosphorylation site (S662G) was reported (Toh2001).
In human DSPS, a polymorphism in PER3 was reported (Ebisawa2001).
Drosophila period is the first found mutant of circadian behavior (Konopka1971), and the first clock gene (Bargiello1984, Zehring1984, Reddy1984).
Human (OMIM) PER1, PER2, PER3 Mouse (MGI) Per1, Per2, Per3 Fly (Flybase) per
Domains PASPAC
Mouse PER2
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CLOCK, NPAS2 →Homolog list→Mutant list

Synonyms CLOCK, CLK, Circadian locomoter output cycles kaput (mouse); NPAS2, MOP4, neuronal PAS domain protein 2; Jrk, CG7391 (fly)
Class Transcription factor, positive. HAT
Outline Clock is one of "core loop" gene.
CLOCK forms heterodimer with ARNTL(BMAL). CLOCK/ARNTL binds to E-Box and activates transcription of "clock genes" and "clock controlled genes (CGG)".
Circadian period was prolonged and diminished in the "Clock mouse" (semidominant mutation) (Vitaterna1994). E-Box dependent transcription was diminished or eliminated in the "Clock mouse".
Rhythmic behavior of a null KO-mouse was normal (Debruyne2006), and a doubleKO of "Clock and Npas2 shows arrhythmic behavior (Debruyne2007).
HAT(histone acetyltransferase) activity in CLK was reported (Doi2006).
"Clock is the first found clock gene in mammal (Vitaterna1994, King1997, Antoch1997).
Human (OMIM) CLOCK, NPAS2 Mouse (MGI) Clock, Npas2 Fly (Flybase) clk
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ARNTL  →Homolog list→Mutant list

Synonyms ARNTL, BMAL1, MOP3, ARNT3; ARNTL2, BMAL2, MOP9, CLIF; cycle, CG8727 (fly)
Class Transcription factor, positive
Outline ARNTL(BMAL) is one of the "core loop" gene.
ARNTL forms heterodimer with CLOCK. CLOCK/ARNTL binds to E-Box and activates transcription of "clock genes" and "clock controlled genes (CGG)". KO mouse of ARNTL (BMAL1) shows arrhythmic phenotype (Bunger2000).
Rhythmic expression of ARNTL was mediated by RORE sequences in the promoter (Preitner2002).
Human (OMIM) ARNTL, ARNTL2 Mouse (MGI) Arntl, Arntl2 Fly (Flybase) cyc

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BHLHE40, 41 (DEC1, 2) →Homolog list→Mutant list

Synonyms DEC1(differentiation of human embryo chondrocytes 1), BHLHB2, BHLHE40, STRA13, Stra14, SHARP-2, CR8; DEC2, BHLHB3, SHARP1, SHARP-1, BHLHE41; cwo, clockwork orange, CG17100 (fly)
Class Transcription factor, negative
Outline BHLHE40, 41 (DEC1, 2) are one of "interlocking loop" gene (Honma2002).
cwo is one of "interlocking loop" gene (Lim2007, Matsumoto2007, Kadener2007).
BHLHE40, 41 and cwo are rhythmically expressed in E-Box dependent manner. BHLHE40, 41 and CWO bind to E-Box and suppress transcription by CLOCK/ARNTL.
Though the feature of BHLHE40, 41 and cwo (clockwork orange) are closely related, it is difficult to conclude that they are homolog or not.
W-KO mouse of BHLHE40, 41 showed almost normal behavioral rhythm, but altered response to light Rossner2008).
Regulation of sleep length by SNP of DEC2 was reported. Human and transgenic fly carrying P385R allele showed short sleep length (He2009)
Human (OMIM) BHLHE40, BHLHE41 Mouse (MGI) Bhlhe40, Bhlhe41 Fly (Flybase) cwo
Mouse BHLHE40 (DEC1)

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ID1-4 →Homolog list→Mutant list

Synonyms ID1 (inhibitor of DNA binding 1, dominant negative helix-loop-helix protein), bHLHb24; ID2, bHLHb26, GIG8; ID3, HEIR-1, bHLHb25; ID4, IDB4, bHLHb27;
Class Transcription factor, negative
Outline Id2 KO mice exhibit abnormally rapid entrainment, and 1/4 of them were arrhythmic. Id4 KO mice exhibit normal entrainment (Duffield2009).
In mammal, IDs have been  isolated as HLH containing protein which have dominant negative effect to bHLH proteins because IDs lack basic region for DNA binding (Sun1991).  IDs are involved in proliferation and differentiation of neuron and immune cells (see Mutant list).
In Drosophila, good candidate for ID is emc, which is involved in body cell fate specification and differentiation  (van Doren1991). Clock function in insect is unknown.
Human (OMIM) ID1, ID2, ID3, ID4 Mouse (MGI) Id1, Id2, Id3, Id4 Fly (Flybase) emc
Domains HLH
Mouse ID2

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NFIL3 (E4BP4), vrille →Homolog list, →Mutant list

Synonyms NFIL3, E4BP4, IL3BP1, NF-IL3A; vrille, vri, argo, jf23, CG14029 (fly)
Class Transcription factor, negative
Outline NFIL3 and vri are transcription factor with bHLH domain.
NFIL3 and VRI bind to "VP-Box" then regulate transcription negatively.
vri was isolated as vital gene involved in development (George1997). Circadian function of vri was reported by Blau1999. They found vri as a rhythmic expressed gene by Differential Display method. Expression rhythm of vri was Clk and cyc dependent. vri was expressed in "clock neurons". Heterozygote of DN mutant showed shortened period. Overexpression of vri prolonged period.
NFIL3 (E4BP4) was isolated as an adenovirus E4 (early region 4) promoter binding protein (E4 binding lambda-P4. #4 is a serial number of clone and there is no E4BP1-3) (Cowell1992). Role of NFIL3 in regulation of clock gene expression was reported in cultured cells (Mitsui2001Doi2001,  Ohno2007,  Ohno2007).
Human (OMIM) NFIL3 Mouse (MGI) Nfil3 Fly (Flybase) vri
Domains BRLZ(bZIP)
Mouse NFIL3 (E4BP4)

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DBP, HLF, TEF, Pdp1 →Homolog list→Mutant list

Synonyms DBP; HLF; TEF; Pdp1, PAR-domain protein 1, CG17888(fly)
Class Transcription factor, positive
Outline Pdp1, DBP, TEF and HLF belong to PAR bZIP (proline and acidic amino acid-rich basic leucine zipper) transcription factor family.
They bind to D-box of target gene promoter and activate transcription.
Pdp1 was isolated as transcriptional regulator of somatic muscle genes (Lin1997). Function in Clock was suggested (Blau&Cyran2001CSHLmeeting, McDonald2001, Ueda2001). The model of second feed loop with vri and Pdp1 was suggested by Cyran2003.
DBP was isolated as a "D-site of albumin promoter (albumin D-box) binding protein" (Mueller1990). Dbp shows strong expression rhythm (Wuarin1990), then the function in circadian clock was speculated. Role of DBP in the circadian oscillatory mechanism of mouse Per1 expression was reported Yamaguchi2000).
TEF (thyrotroph embryonic factor)was isolated as a regulator for thyroid-stimulating hormone (Drolet1991), and relationship to circadian rhythm was reported (Fonjallaz1996).
HLF (Hepatic leukemia factor) was found as a gene fused to E2A in leukemia cells (Inaba1992Hunger1992).
Normal circadian rhythm in Dbp, Tef and Hlf triple KO mouse was reported, suggesting these gene are not clock gene(Gachon2004).
Human (OMIM) DBP, HLF, TEF Mouse (MGI) Dbp, Hlf, Tef Fly (Flybase) Pdp1
Domains BRLZ(bZIP)
Fly PDP1

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NR1D1, NR1D2 (REV-ERB-Alpha, BETA) →Homolog list→Mutant list

Synonyms NR1D1 (nuclear receptor subfamily 1, group D, member 1), REV-ERBA (REV-ERB ALPHA), EAR1; NR1D2 (nuclear receptor subfamily 1, group D, member 2), REV-ERBB (REV-ERB BETA), EAR-1r
Class Transcription factor, negative
Outline NR1D1, 2 (REV-ERBA, B) belong to orphan nuclear receptor, and bind to RORE, then suppress transcription.
REV-ERB alpha was decided to the major regulator of cyclic ARNTL(BMAL1) transcription (Preitner2002). They found ROREs in mouse ARNTL promoter, then focused on RORE binding proteins (RORs and REV-ERBs). They generated a KO mouse of Nr1d1, which shows rhythmic expression. In the KO mouse, Per2 and Cry2 expression was normal. The KO mouse showed shorter period under constant conditions (DD and LL), and enhanced response to light exposure in dawn.
The ligand for REV-ERB ALPHA was idntified to heme (haem) (Yin2007).
REV-ERB alpha was isolated as a nuclear receptor encoded in the reverse strand of c-erbA (Lazer1989).
Human (OMIM) NR1D1, NR1D2 Mouse (MGI) Nr1d1, Nr1d2 Fly (Flybase) Eip75B
Domains ZnF_C4, HOLI
Mouse NR1D1 (REV-ERB-alpha)

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RORA-C (RAR-related orphan receptor, NR1F1-3) →Homolog list→Mutant list

Synonyms RORA (RAR-related orphan receptor Alpha), NR1F1; RORB, NR1F2; RORC, RORG (ROR Gamma), NR1F3, TOR
Class Transcription factor, positive
Outline RORA belongs to orphan nuclear receptor, and bind to RORE, then activates transcription.
In three paralog for mouse Ror, clock function was reported in Rora (ROR Alpha) (Sato2004).
RORA controls Purkinje cell survival and differentiation. KO mouse died shortly after birth (Dussault1998), (Steinmayr1998).
Human (OMIM) RORA, RORB, RORC Mouse (MGI) Rora, Rorb, Rorc Fly (Flybase) Hr46
Domains ZnF_C4, HOLI
Mouse RORA

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SIRT1 →Homolog list→Mutant list

Synonyms SIRT1 (sirtuin (silent mating type information regulation 2 homolog) 1), SIR2L1
Class mono-ADP-ribosyltransferase, Histone Deacetylase (HDAC)
Outline SIRT1 was found as homolog for yeast Sir2. SIRT1/Sir2 encode a NAD+-dependent histone deacetylase.
The gene is involved in response to stresses and longevity.
Role of SIRT1 in transcriptional regulation of clock genes was reported in cultured cells including MEF from KO mouse (Asher2008Nakahata2008). Involvement in behavioral rhythm in animal was not reported.
Human (OMIM) SIRT1 Mouse (MGI) Sirt1 Fly (Flybase) Sir2
Domains -
Mouse SIRT1. (drawn by NCBI CDART)

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CRY →Homolog list→Mutant list

Synonyms CRY1 (cryptochrome 1); CRY2; cry, CG3772 (fly)
Class Repressor of CLOCK/ARNTL (mammal), Circadian photopigment (Fly)
Outline CRY (cryptochrome = [Greek] hidden color) belong to DNA photolyase/cryptochrome protein family.
CRY was found in plant. Reviewed in "Cryptochrome Signaling in Plants" (Li2007).
Drosophila cry (D-cry) act as blue light photoreceptor of circadian clock (Emery1998, Stanewsky1998).
Mammalian CRYs (m-CRY) act as repressor for CLOCK/ARNTL. (Vitaterna1999van der Horst1999). Simgle KO mouse of Cry1 or Cry2 exhibit altered period, and W-KO shows arrhythmic behavior.
Human (OMIM) CRY1, CRY2 Mouse (MGI) Cry1, Cry2 Fly (Flybase) cry
Domains DNA-photolyase, FAD-binding
Fly CRY. (drawn by NCBI CDART)

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Timeless →Homolog list→Mutant list

Synonyms Timeless, tim, Ritsu, CG3234(fly)
Class Regulator of PERIOD
Outline timeless is an essential gene for circadian rhythm in fruit fly(Myers1995). TIM interacts with PER, and regulates nuclear entry of PER/TIM complex (Saez1996). TIM protein was degraded by D-CRY in light-dependent manner (Ceriani1999).
Mammalian "TIMELESS" is the counterpart of insect "timeout". Clock function of mammalian TIMELESS is still unclear.
Human (OMIM) - Mouse (MGI) - Fly (Flybase) tim
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GSK3, shaggy →Homolog list→Mutant list

Synonyms GSK3A (glycogen synthase kinase 3 alpha); GSK3B; shaggy, sgg, zw3, CG2621 (fly)
Class S/T Kinase
Outline A role for shaggy in circadian clock was identified in Drosophila (Martinek2001). Clock function of sgg was found by overexpression screening. Overexpression of sgg shortened period (-3 h), and mutant for sgg prolonged period (+2h). SGG phosphorylates TIM protein.
Clock function of mammalian homolog, GSK3-beta, was reported in cultured cells (Iitaka2005).
See "Phosphorylation of Clock Proeins↓".
Human (OMIM) GSK3A, GSK3B Mouse (MGI) Gsk3a, Gsk3b Fly (Flybase) sgg
Domains S/T-kinase
Mouse GSK3B

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CSNK1E, CSNK1D, dco (dbt) →Homolog list→Mutant list

Synonyms CSNK1E (casein kinase 1, epsilon); dco (1(3)discs overgrown), dbt (double time), CG2048 (fly)
Class Kinase
Outline DCO phosphorylates PER and CLK in fruit fly.
In mammal, CSNK1E phosphorylates PER, CRY and ARNTL. And CSNK1D phosphorylates PER.
Clock function of dco was identified as "double-time" mutants of Drosophila (Kloss1998, Price1998). CK1E, CK1D and DBT phosphorylate PER, and  promotes ubiquitination and degradation of PER.
The "tau" mutant of hamster had been isolated as the first clock mutant in mammal (Ralph1988). Then, the corresponding gene was decided to point mutation of CSNK1E (Lowrey2000).
Targeted mutant mouse carrying tau allele showed same phenotype to hamster model (Meng2008).
In human FASPS, T44A mutation of CSNK1D was identified (Xu2005).
Liver specific KO of Csnk1d showed prolonged Per2::luc rhythm (Etchegaray2009).
See "Phosphorylation of Clock Proeins↓".
Human (OMIM) CSNK1D, CSNK1E Mouse (MGI) Csnk1d, Csnk1e Fly (Flybase) dco
Domains STYKc (Protein kinase; unclassified specificity)*S/T-kinase
Mouse CSNK1E

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CSNK2A1, CkIIalpha (CK2) →Homolog list→Mutant list

Synonyms CSNK2A1 (casein kinase 2, alpha 1); CkIIalpha, CK-2, CG17520 (fly)
Class Kinase
Outline CK-2 phosrhprylates and stabilizes PER. In Drosophila, Clock function of this gene was identified as the "Timekeeper" allele which showed long period (+2.8h) in heterozygote (Lin2002, Akten2003, Nawathean2004).
In mammal, CK2 role in the circadian clock was reported using RNAi in cultured cells (Maier2009).
Clock function of CK2 was also reported in fungi (Yang2002, Yang2003) and plant (Sugano1999).
See "Phosphorylation of Clock Proeins↓".
Human (OMIM) CSNK2A1 Mouse (MGI) Csnk2a1 Fly (Flybase) CkIIalpha
Domains S/T-kinase
Mouse CSNK2A1

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BTRC, slmb →Homolog list→Mutant list

Synonyms BTRC (betaTrCP, beta-transducin repeat containing), FBW1A (F-box Proteins with WD-40 Domains 1a); BTRC2, FBXW11 (F-box and WD repeat domain containing 11), FBW1B; slmb (slimb, supernumerary limbs), shv, CG3412 (fly)
Class Ubiquitin-protein ligase
Outline slmb is an essential component of the Drosophila circadian clock (Grima2002, Ko2002). Loss-of-function mutant for slmb is lethal, then Adult fly was produced using heat inducible transgene. Most of adult flies showed arrhythmic behavior, and period of rhythmic fly was prolonged.
There are two paralog on slmb in mouse. Signle mutant of BTRC showed normal behavioral rhythm under DD. DD
slmb had been identified as a regulator of Hh and Wg pathways (Jiang1998).
Human (OMIM) BTRC, FBXW11 Mouse (MGI) Btrc, Fbxw11 Fly (Flybase) slmb
Domains FBOXWD40
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FBXL3 (Overtime, After-hours) →Homolog list→Mutant list

Synonyms FBXL3 (F-box and leucine-rich repeat protein 3); Ovtm (Overtime), Afh (After-hours) (mouse)
Class Ubiquitin-protein ligase
Outline F- box proteins are component of Skp1-cullin-F-box (SCF) complex and recognize ubiquitination targets.
FBXL3 was identified as the responsible gene for Overtime and After-hours mutants of mouse (Godinho2007Siepka2007). Both mutants show longer period than the wild type by +3h.
Human (OMIM) FBXL3, FBXL21 Mouse (MGI) Fbxl3, Fbxl21 Fly (Flybase) Not found
Domains FBOX, LRR (leucine-rich repeats)
Mouse FBXL3

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FBXL15, jet →Homolog lis→Mutant list

Synonyms FBXL15 (F-box and leucine-rich repeat protein 15), JET; jet (jetlag), Veela CG8873 (fly)
Class Ubiquitin-protein ligase
Outline FBXL15 was identified as the responsible gene for  jet (jetlag) mutant of Drosophil. Like the cryb mutant, the jet mutant shows rhythmic behavior under LL. Phase response and TIM degradation by light pulses was reduced (Koh2006). The mutant was also named as Veela (Peschel2006).
Human (OMIM) FBXL15 Mouse (MGI) Fbxl15 Fly (Flybase) jet
Domains FBOX, LRR (leucine-rich repeats)
Human JET

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Protein Phosphatase

Synonyms -
Class Protein phosphatase
Outline Gene for phosphatase was not listed. Because these enzymes consist of multiple subunits, and most of study used not genetics but inhibitor.
In eukaryote, 25 genes for protein phosphatase have been reported (Honkanen&Golden2002).
Involvement in molecular clock was reported in PP1, PP2A, PP5.
Protein phosphatase was well conserved from plant to animal.
See "Phosphorylation of Clock Proeins↓".
Domains Protein phosphatase
Reference Sathyanarayanan2004(fly PP2A<tws and wdb>), Fan2007
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Phosphorylation of Clock Proeins

Phosphorylation of Clock Proteins
Arrows indicate not activation but target.

Domains of Clock Gene Product

Description Protein ↑ SMART
PAS PAS domain PAS (PERIOD ARNT SIM)domains were found in proteins involved in sensing for environmental signals.About 100 amino acid motif. PERIOD
PAC PAC domain
PAC (PAS-associated,C-terminal)domains were found in C-terminal of PAS domains. PERIOD
HLH domain
bHLH (basic Helix-Loop-Helix) is a DNA binding domain. About 60 amino acids. The N-terminal basic region (15 aa) is involved in DNA binding. C-terminal HLH involved in dimerization. HLH only proteins (ID1-4) work as dominant negativefactors. CLOCK
Orange Orange domain Orange domain is conserved in Hairy/E(SPL) family. DEC, CWO SM00511
bZIP (BRLZ) bZIP domain
bZIP (basic-leucine ZIPper; BRLZ, Basic Region Leucin Zipper) is a DNA binding domain. NFIL3
zf-C4 (ZnF_C4) Zn-C4 domain
zf-C4 (c4 zinc finger in nuclear hormone receptors) is a DNA binding domain.  NF1D1
HOLI HOLI domain HOLI is the ligand binding domain of hormone receptors. NF1D1
S_TKc S/T kinase
Serine/Threonine protein kinases, catalytic domain. GSK3
FBOX F-box
F-box is a receptor for ubiquitination targets. About 40 amino acid motif. BTRC, SLMB
WD40 WD40 repeat
WD-40 repeats is involved in protein-protein interaction. One unit consists of ~40 amino acid. BTRC, SLMB SM00320
LRR LRR Leucine-rich repeats. Protein-binding.  One unit consists of 22~28mino acid. FBXL3
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Clock neurons
Clock neurons are the master pacemaker (center of circadian rhythm) in Drorophila, brain.
Clock neurons consist of  6~7 group of neurons: s-LNv, l-LNv, LND, DN1, DN2, DN3 and LPN.
Clock neuron can be recognized as neurons with highly expression of clock genes.
D-box (D site)
D-box is a DNA sequence motif found in albumin promoter.
D-box is recognized by DBP (D-box Binding Protein), TEF and HLF.
Consensus of D-box is 5'-RTTAYGTAAY-3' (R = A or G, Y=T or C)(Falvey1996).
Almost same to E4BP4 site and V/P-box (VRI/PDP1-box).
DD (Dark: Dark)
DD means constant dark condition.
CT (Circadian Time) is used to indicate time under DD or LL.
DSPS (Delayed sleep phase syndrome)
DSPS is one of circadian rhythm sleep disorder. Sleep and activity phase were delayed. DSPS people are difficult to wake up in morning, and to go to shcool and to work.

E-box is one of DNA sequence motif recognized by bHLH transcription factors (Muree1989).
Consensus of E-box is 5'-CANNTG-3' in general.
Consensus for CLOCK-ARNTL is 5'-CACGTG-3'. 
E-Box is frequently found in the promoters of "Clock Genes" (ex., Per) and "Clock Controlled Genes" (ex., Dbp). (Hao1997Gekakis1998Darlington1998)
Role of noncanonical E'-box (5'-CACGTT-3') in rhythmic expression of Per2 and Cry1 was reported (Yoo2005).
E4BP4 site and V/P-box (VRI/PDP1-box)
E4BP4 site is a DNA sequence motif recognized by E4BP4.
Consensus of E4BP4 site is 5'-RTKAYGTAAY-3' (R = A or G, K = G or T, Y = C or T) (Cowell1992).
V/P box a DNA sequence motif recognized by VRI and PDP1.
Consensus of V/P box  is 5'-ATTTTGTAAC-3' (Lin1997, Cyran2003, reviewed in Hardin2005).
Almost same to D-Box.
Familial Advanced Sleep Phase Syndrome is one of circadian rhythm sleep disorder.
Activity phase was shifted to early morning: 03:00 - 18:00.
Polymorphism in PER2(↑) (Toh2000) and CSNK1D(↑) (Xu2005) were reported to be causal genes.

Knockout mouse by gene targeting (homologous recombination based target gene replacement).
LD (Light: Dark)
LD means Light: Dark condition. Usually 12h: 12h cycle of photoperiod.
ZT (Zeitgeber time) is used to indicate time under LD. Usually, ZT0 = Light ON and ZT12 = Light OFF.
LL (Light: Light)
LL means constant light condition.
Wild type Drosophila shows arrhythmic behavior under LL. 
CT (Circadian Time) is used to indicate time under DD or LL.
MEF (mouse embryonic fibroblasts)
Primary culture of mouse embryo. MEF was used if KO animal was embryonic or postnatal lethal.
Orphan nuclear receptor
Orphan nuclear receptor is generic name for nuclear receptors, which lack identified ligands.
RORE (ROR responsible Element)
RORE is one of DNA sequence motif recognized by RORs and REV-ERBs
Consensus of RORE is 5'-WAWNTRGGTCA-3' (W = A or T, N = ANY, R = A or G).
RORE was found in ARNTL promoter.
Synonyms are different names for identical genes, and separated by commas.
The different genes are separated by semicolon.

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