Genome wide association study of a Circadian Imbalance Index in 312,935 European ancestry UK Biobank participants identifies loci related to diabetes, mood and myocardial infarction.

Magdalena Żebrowska, Matthias Wielscher, Jing Zhang, Ingvild Saksvik-Lehouillier, Lee DiMilia et al.

Other Research square 2025

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Study Design

Type d'étude: genome-wide association study
Taille de l'échantillon: 312935

Intervention: Genome wide association study of a Circadian Imbalance Index in 312,935 European ancestry UK Biobank participants identifies loci related to diabetes, mood and myocardial infarction. None
Comparateur: Placebo
Direction de l'effet: Mixed
Risque de biais: Low

Abstract

The Circadian Imbalance Index (CII) integrates chronotype, sleep duration, neuroticism, caffeine intake, and vitamin D. In a genome wide association study (GWAS) of CII in 312,935 European ancestry UK Biobank participants, we identified 27 loci mapping to 72 genes, including circadian regulators CALCA, DHCR7, KDM5A, HAL, and CRX. Gene-overlap analyses demonstrated shared architecture with CII components, while EPHB1, SERPING1, C12orf74, PLEKHG7, and EEA1 were uniquely associated with CII. A CII polygenic score (CII-PRS) showed phenome-wide associations with type 2 diabetes (T2D), major depressive disorder, and obesity. Genetic correlations linked CII with insomnia, mood symptoms, body mass index (BMI), T2D, coronary artery disease (CAD), and myocardial infarction (MI). Mendelian randomization suggested causal effects of CII on T2D, mood swings, and MI, and reverse effects of CAD, mood, and MI on CII. This work shows that circadian imbalance is a polygenic trait connecting sleep-related biology to metabolic, cardiovascular and mood health outcomes.

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Fig. 1:

Manhattan plot from the genome-wide association study of the Circadian Imbalance Index in 312,935 European ancestry UK Biobank participants, highlighting significant loci.

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Fig. 2:

Regional association plots for lead SNPs identified in the GWAS of the Circadian Imbalance Index, showing loci related to diabetes, mood, and myocardial infarction.

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Fig. 3:

Phenome-wide association results linking the Circadian Imbalance Index genetic loci to related traits including sleep duration, chronotype, and cardiometabolic outcomes.

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Fig. 4:

Pathway or gene-set enrichment analysis for the significant loci from the Circadian Imbalance Index GWAS, revealing biological processes relevant to circadian regulation.

chart

Tables

Table 1

		CII value
		0	1	2	3	4	5	Total
N (%)		29,538 (9.4)	87,028 (27.8)	103,761 (33.2)	65,257 (20.9)	23,254 (7.4)	4,097 (1.3)	312,935
Age *		58.1 ± 7.8	57.2 ± 8.0	56.5 ± 8.0	55.8 ± 8.1	55.2 ± 8.1	54.2 ± 8.1	56.6 ± 8.1
Male, N (%)		15,810 (53.5)	43,253 (49.7)	48,700 (46.9)	29,271 (44.9)	9,781 (42.1)	1,658 (40.5)	148,473 (47.4)
BMI *		26.4 ± 3.9	26.9 ± 4.3	27.4 ± 4.7	27.9 ± 5.1	28.5 ± 5.5	29.2 ± 5.9	27.4 ± 4.7
Average total household income before tax, N (%)	Less than £18,000	4,325 (14.7)	13,504 (15.5)	18,301 (17.7)	13,593 (20.9)	5,979 (25.8)	1,354 (33.3)	5,7056 (18.3)
	£18,000 to £31,000	6,602 (22.4)	19,224 (22.1)	22,747 (22.0)	14,478 (22.3)	5,065 (21.9)	861 (21.2)	68,977 (22.1)
	£31,000 to £52,000	7,213 (24.4)	21,001 (24.2)	24,690 (23.8)	15,105 (23.2)	5,020 (21.7)	774 (19.0)	73,803 (23.6)
	£52,000 to £100,000	6,066 (20.6)	17,882 (20.6)	20,307 (19.6)	11,522 (17.7)	3,446 (14.9)	487 (12.0)	59,710 (19.1)
	Greater than £100,000	1,952 (6.6)	5,221 (6.0)	5,458 (5.3)	2631 (4.0)	750(3.2)	87(2.1)	16,099 (5.2)
	Unknown	3,352 (11.4)	10,070 (11.6)	12,040 (11.6)	7,730 (11.9)	2,879 (12.4)	504 (12.4)	36,575 (11.7)
Education, N (%)	College or University degree	10,544 (35.7)	30,398 (34.9)	34,399 (33.2)	19,617 (30.1)	6,266 (26.9)	980 (23.9)	102,204 (32.7)
	Other	14,788 (50.1)	43,294 (49.7)	52,267 (50.4)	33,678 (51.6)	12,073 (51.9)	2,168 (52.9)	158,268 (50.6)
	Unknown	4,206 (14.2)	13,336 (15.3)	17,095 (16.5)	11,962 (18.3)	4,915 (21.1)	949 (23.2)	52,463 (16.8)
Shift workers, N (% ^(a) )		2,020 (13.0)	6,938 (13.8)	9,628 (15.4)	7,009 (17.8)	2,821 (21.0)	560 (26.3)	28,976 (9.3)
		CII components
		Evening Person	Short Or Long Sleep	High Neuroticism	No Or High Caffeine	Low Vit D	Total
N (%)		105,673 (33.8)	96,903 (31.0)	74,742 (23.9)	161,085 (51.5)	165,419 (52.9)	312,935
Age *		55.7 ± 8.3	57.1 ± 7.9	55.3 ± 8.0	56.2 ± 8.1	56.0 ± 8.1	56.6 ± 8.1
Male, N (%)		49,943 (47.3)	46,105 (47.6)	28,978 (38.8)	72,382 (44.9)	78,472 (47.4)	148,473 (47.4)
BMI *		27.6 ± 4.8	28.0 ±5.1	27.4 ±5.1	27.5 ± 4.9	28.0 ± 5.1	27.4 (4.7)
Average total household income before tax, N (%)	Less than £18,000	19,374 (18.4)	22,205 (23.0)	16,942 (22.7)	31,267 (19.5)	31,783 (19.3)	57,056 (18.3)
	£18,000 to £31,000	23,142 (22.0)	21,574 (22.3)	16,478 (22.1)	35,864 (22.3)	35,659 (21.6)	68,977 (22.1)
	£31,000 to £52,000	25,258 (24.0)	20,912 (21.7)	16,888 (22.7)	37,342 (23.2)	39,246 (23.8)	73,803 (23.6)
	£52,000 to £100,000	20,642 (19.6)	15,169 (15.7)	12,375 (16.6)	29,217 (18.2)	31,878 (19.3)	59,710 (19.1)
		CII value
		0	1	2	3	4	5	Total
	Greater than £100,000	5,507 (5.2)	3,945 (4.1)	2,631 (3.5)	7,147 (4.4)	8,235 (5.0)	16,099 (5.2)
	Unknown	11,505 (10.9)	12,746 (13.2)	9,170 (12.3)	19,818 (12.3)	18,137 (11.0)	36,575 (11.7)
Education, N (%)	College or University degree	35,511 (33.6)	26,268 (27.1)	21,327 (28.5)	47,558 (29.5)	57,347 (34.7)	102,204 (32.7)
	Other	54,562 (51.6)	49,737 (51.3)	38,740 (51.8)	83,752 (52.0)	81,203 (49.1)	158,268 (50.6)
	Unknown	15,600 (14.8)	20,898 (21.6)	14,675 (19.6)	29,775 (18.5)	26,869 (16.2)	52,463 (16.8)
Shift workers, N (%^(a))		11,082 (17.4)	10,515 (19.9)	7,504 (17.3)	15,835 (16.6)	16,369 (16.0)	28,976 (9.3)

Table 2

Genomic Locus	Variant	Chromosome: position	Nearest gene	Effect allele	Effect size (P)	Standard error	P-value
7	rs34265662	4:72617557	GC	TA	0,0793	0,0031	1,49E-147
11	rs117913124	11:14900931	CYP2R1	A	0,2192	0,0085	1,01E-146
14	rs3794060	11:71187679	NADSYN1	T	−0,0434	0,0034	5,05E-37
10	9:140259068_T_TA	9:140259068	EXD3	TA	0,0301	0,0043	1,57E-12
9	rs73198970	8:11040216	XKR6	C	0,0187	0,0028	3,47E-11
12	11:57522200_CCCCT_C	11:57522200	TMX2-CTNND1:RP11-691N7.6:CTNND1	C	0,0196	0,0030	6,42E-11
22	rs567979837	13:60753105	RNY4P28	CT	−0,0185	0,0028	7,51E-11
25	rs1557341	18:35127427	CELF4	C	−0,0193	0,0030	9,28E-11
5	rs7652808	3:85603643	CADM2	G	0,0185	0,0029	2,12E-10
21	rs10859995	12:96375682	HAL	C	0,0178	0,0028	3,08E-10
27	rs2547244	19:48363039	TPRX2P	G	0,0231	0,0037	4,92E-10
17	rs6487365	12:24066460	SOX5	A	0,0183	0,0030	9,12E-10
26	rs2126786	18:53447005	RP11-397A16.1:RP11-397A16.2	C	0,0225	0,0037	1,01E-09
19	12:39098718_GT_G	12:39098718	CPNE8	G	0,0171	0,0028	1,55E-09
16	rs10848644	12:365289	SLC6A13:RP11-283I3.4	T	−0,0167	0,0028	2,81E-09
1	rs61816761	1:152285861	FLG-AS1:FLG	A	−0,0574	0,0097	3,80E-09
8	rs2979241	8:8303353	CTA-398F10.2	C	−0,0162	0,0028	7,34E-09
3	rs11563179	2:51693002	AC007682.1	C	0,0222	0,0039	9,43E-09
2	rs2279681	1:201861016	SHISA4	G	−0,0168	0,0029	1,02E-08
20	rs139923919	12:93222395	EEA1	CAT	−0,0176	0,0031	1,04E-08
13	rs509533	11:66070575	TMEM151A	C	0,0159	0,0028	1,68E-08
23	rs16661	14:75128316	AREL1	C	0,0165	0,0030	2,74E-08
18	rs9668760	12:34611172	RP13-7D7.1	G	−0,0157	0,0028	2,98E-08
24	rs62007299	15:77711719	PEAK1	A	0,0169	0,0031	3,55E-08
4	rs7625384	3:18774357:G:T	AC144521.1	T	0,0170	0,0031	3,89E-08
6	rs4082244	3:134729537:C:G	EPHB1	G	−0,0160	0,0029	4,79E-08
15	rs10750539	11:133548873:A:G	RP11-448P19.1	A	0,0160	0,0029	4,81E-08

Table 3

Ensg	Symbol	Chr	Strand	MsigDB Label	PLI	Min GWAS p	Ind Sig Snps	GL
ENSG00000110680	CALCA	11	−1	WP CLOCKCONTROLLED AUTOPHAGY IN BONE METABOLISM^(a)	0.0014	4.8730e-25	11:14992795_AGGAGCCCACAGACCTT_A; rs61878675	11
ENSG00000172893	DHCR7	11	−1	UEDA PERIFERAL CLOCK^(b)	5.0427e-08	6.1235e-37	rs12793607, rs1540129, rs3794060, rs1790349, rs369124946, 11:71203933_AT_A, rs181766110, rs139168803, rs35708376, rs760165576	14
ENSG00000073614	KDM5A	12	−1	WP CIRCADIAN RHYTHM GENES^(c)	0.99999	6.1331e-07	rs10848644	16
ENSG00000084110	HAL	12	−1	UEDA PERIFERAL CLOCK^(b)	5.9087e-17	3.0841e-10	rs10859995	21
ENSG00000105392	CRX	19	1	WP CIRCADIAN RHYTHM GENES^(c)	0.6237	4.7685e-08	rs2547244	27

Table 4

						GWAS overall			GWAS in women
Ensg	GL	Symbol	Chr	PLI	Ind Sig Snps	Ind Sig SNP p	β	se	Ind Sig SNP p	β	se
ENSG00000154928	6	EPHB1^{(a), (b)}	3	9.98E-01	rs4082244	4.79E-08	−0.0160	0.0029	1.47E-07	−0.0303	0.0058
ENSG00000149131	12	SERPING1^{(a), (b), (d)}	11	9.73E-01	rs1647396	2.46E-07	0.0153	0.0028	-	-	-
ENSG00000214215	20	C12orf74^{(a), (b)}	12	5.22E-04	rs139923919	1.04E-08	−0.0176	0.0031	5.13E-06	0.0178	0.0039
ENSG00000187510	20	PLEKHG7^{(a), (b)}	12	3.68E-11	rs139923919
ENSG00000102189	20	EEA1^{(a), (c)}	12	6.97E-01	rs139923919

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A Vitamine D pour Insomnie

Genome wide association study of a Circadian Imbalance Index in 312,935 European ancestry UK Biobank participants identifies loci related to diabetes, mood and myocardial infarction.

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