Disruption of paternal circadian rhythm affects metabolic health in male offspring via nongerm cell factors

. 2021 May ; 7 (22) : . [epub] 20210526

Jazyk angličtina Země Spojené státy americké Médium electronic-print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34039610

Circadian rhythm synchronizes each body function with the environment and regulates physiology. Disruption of normal circadian rhythm alters organismal physiology and increases disease risk. Recent epidemiological data and studies in model organisms have shown that maternal circadian disruption is important for offspring health and adult phenotypes. Less is known about the role of paternal circadian rhythm for offspring health. Here, we disrupted circadian rhythm in male mice by night-restricted feeding and showed that paternal circadian disruption at conception is important for offspring feeding behavior, metabolic health, and oscillatory transcription. Mechanistically, our data suggest that the effect of paternal circadian disruption is not transferred to the offspring via the germ cells but initiated by corticosterone-based parental communication at conception and programmed during in utero development through a state of fetal growth restriction. These findings indicate paternal circadian health at conception as a newly identified determinant of offspring phenotypes.

Komentář v

PubMed

Zobrazit více v PubMed

Pittendrigh C. S., Temporal organization: Reflections of a Darwinian clock-watcher. Annu. Rev. Physiol. 55, 17–54 (1993). PubMed

Dibner C., Schibler U., Albrecht U., The mammalian circadian timing system: Organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72, 517–549 (2010). PubMed

Golombek D. A., Rosenstein R. E., Physiology of circadian entrainment. Physiol. Rev. 90, 1063–1102 (2010). PubMed

Yoo S.-H., Yamazaki S., Lowrey P. L., Shimomura K., Ko C. H., Buhr E. D., Siepka S. M., Hong H.-K., Oh W. J., Yoo O. J., Menaker M., Takahashi J. S., PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl. Acad. Sci. U.S.A. 101, 5339–5346 (2004). PubMed PMC

Takahashi J. S., Transcriptional architecture of the mammalian circadian clock. Nat. Rev. Genet. 18, 164–179 (2017). PubMed PMC

Vetter C., Circadian disruption: What do we actually mean? Eur. J. Neurosci. 51, 531–550 (2020). PubMed PMC

Bedrosian T. A., Fonken L. K., Nelson R. J., Endocrine effects of circadian disruption. Annu. Rev. Physiol. 78, 109–131 (2016). PubMed

Huang W., Ramsey K. M., Marcheva B., Bass J., Circadian rhythms, sleep, and metabolism. J. Clin. Invest. 121, 2133–2141 (2011). PubMed PMC

Logan R. W., McClung C. A., Rhythms of life: Circadian disruption and brain disorders across the lifespan. Nat. Rev. Neurosci. 20, 49–65 (2019). PubMed PMC

Shafi A. A., Knudsen K. E., Cancer and the Circadian Clock. Cancer Res. 79, 3806–3814 (2019). PubMed PMC

Walker W. H. II, Walton J. C., DeVries A. C., Nelson R. J., Circadian rhythm disruption and mental health. Transl. Psychiatry 10, 28 (2020). PubMed PMC

Bates K., Herzog E. D., Maternal-fetal circadian communication during pregnancy. Front Endocrinol. 11, 198 (2020). PubMed PMC

Canaple L., Gréchez-Cassiau A., Delaunay F., Dkhissi-Benyahya O., Samarut J., Maternal eating behavior is a major synchronizer of fetal and postnatal peripheral clocks in mice. Cell. Mol. Life Sci. 75, 3991–4005 (2018). PubMed PMC

Olejníková L., Polidarova L., Behuliak M., Sladek M., Sumova A., Circadian alignment in a foster mother improves the offspring’s pathological phenotype. J. Physiol. 596, 5757–5775 (2018). PubMed PMC

Smarr B. L., Grant A. D., Perez L., Zucker I., Kriegsfeld L. J., Maternal and early-life circadian disruption have long-lasting negative consequences on offspring development and adult behavior in mice. Sci. Rep. 7, 3326 (2017). PubMed PMC

Varcoe T. J., Gatford K. L., Kennaway D. J., Maternal circadian rhythms and the programming of adult health and disease. Am. J. Physiol. Regul. Integr. Comp. Physiol. 314, R231–R241 (2018). PubMed

Leliavski A., Dumbell R., Ott V., Oster H., Adrenal clocks and the role of adrenal hormones in the regulation of circadian physiology. J. Biol. Rhythms 30, 20–34 (2015). PubMed

Leliavski A., Shostak A., Husse J., Oster H., Impaired glucocorticoid production and response to stress in Arntl-deficient male mice. Endocrinology 155, 133–142 (2014). PubMed

Oster H., Challet E., Ott V., Arvat E., de Kloet E. R., Dijk D.-J., Lightman S., Vgontzas A., van Cauter E., The functional and clinical significance of the 24-hour rhythm of circulating glucocorticoids. Endocr. Rev. 38, 3–45 (2017). PubMed PMC

Ikeda Y., Sasaki H., Ohtsu T., Shiraishi T., Tahara Y., Shibata S., Feeding and adrenal entrainment stimuli are both necessary for normal circadian oscillation of peripheral clocks in mice housed under different photoperiods. Chronobiol. Int. 32, 195–210 (2015). PubMed

Soták M., Bryndová J., Ergang P., Vagnerová K., Kvapilová P., Vodička M., Pácha J., Sumová A., Peripheral circadian clocks are diversely affected by adrenalectomy. Chronobiol. Int. 33, 520–529 (2016). PubMed

Whirledge S., DeFranco D. B., Glucocorticoid signaling in health and disease: Insights from tissue-specific GR knockout mice. Endocrinology 159, 46–64 (2018). PubMed PMC

Fowden A. L., Forhead A. J., Glucocorticoids as regulatory signals during intrauterine development. Exp. Physiol. 100, 1477–1487 (2015). PubMed

E. Turkay, A. Ozmen, G. Unek, I. Mendilcioglu, in Glucocorticoids - New Recognition of Our Familiar Friend (2012), chap. Chapter 13.

Moisiadis V. G., Matthews S. G., Glucocorticoids and fetal programming part 2: Mechanisms. Nat. Rev. Endocrinol. 10, 403–411 (2014). PubMed

Moisiadis V. G., Matthews S. G., Glucocorticoids and fetal programming part 1: Outcomes. Nat. Rev. Endocrinol. 10, 391–402 (2014). PubMed

Quinn M. A., McCalla A., He B., Xu X., Cidlowski J. A., Silencing of maternal hepatic glucocorticoid receptor is essential for normal fetal development in mice. Commun. Biol. 2, 104 (2019). PubMed PMC

Whirledge S. D., Oakley R. H., Myers P. H., Lydon J. P., DeMayo F., Cidlowski J. A., Uterine glucocorticoid receptors are critical for fertility in mice through control of embryo implantation and decidualization. Proc. Natl. Acad. Sci. U.S.A. 112, 15166–15171 (2015). PubMed PMC

Zhu P., Wang W., Zuo R., Sun K., Mechanisms for establishment of the placental glucocorticoid barrier, a guard for life. Cell. Mol. Life Sci. 76, 13–26 (2019). PubMed PMC

Fowden A. L., Forhead A. J., Endocrine mechanisms of intrauterine programming. Reproduction 127, 515–526 (2004). PubMed

Seckl J. R., Cleasby M., Nyirenda M. J., Glucocorticoids, 11beta-hydroxysteroid dehydrogenase, and fetal programming. Kidney Int. 57, 1412–1417 (2000). PubMed

Mukherji A., Kobiita A., Chambon P., Shifting the feeding of mice to the rest phase creates metabolic alterations, which, on their own, shift the peripheral circadian clocks by 12 hours. Proc. Natl. Acad. Sci. U.S.A. 112, E6683–E6690 (2015). PubMed PMC

Mukherji A., Kobiita A., Damara M., Misra N., Meziane H., Champy M. F., Chambon P., Shifting eating to the circadian rest phase misaligns the peripheral clocks with the master SCN clock and leads to a metabolic syndrome. Proc. Natl. Acad. Sci. U.S.A. 112, E6691–E6698 (2015). PubMed PMC

Meyer-Kovac J., Kolbe I., Ehrhardt L., Leliavski A., Husse J., Salinas G., Lingner T., Tsang A. H., Barclay J. L., Oster H., Hepatic gene therapy rescues high-fat diet responses in circadian Clock mutant mice. Mol. Metab. 6, 512–523 (2017). PubMed PMC

INFRAFRONTIER Consortium , INFRAFRONTIER––providing mutant mouse resources as research tools for the international scientific community. Nucleic Acids Res. 43, D1171–D1175 (2015). PubMed PMC

Raess M., de Castro A. A., Gailus-Durner V., Fessele S., de Angelis M. H.; INFRAFRONTIER Consortium , INFRAFRONTIER: A European resource for studying the functional basis of human disease. Mamm. Genome 27, 445–450 (2016). PubMed PMC

Huypens P., Sass S., Wu M., Dyckhoff D., Tschöp M., Theis F., Marschall S., de Angelis M. H., Beckers J., Epigenetic germline inheritance of diet-induced obesity and insulin resistance. Nat. Genet. 48, 497–499 (2016). PubMed

Tarazona S., Garcia-Alcalde F., Dopazo J., Ferrer A., Conesa A., Differential expression in RNA-seq: A matter of depth. Genome Res. 21, 2213–2223 (2011). PubMed PMC

Metsalu T., Vilo J., ClustVis: A web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Res. 43, W566–W570 (2015). PubMed PMC

Huang D. W., Sherman B. T., Lempicki R. A., Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1–13 (2009). PubMed PMC

Huang D. W., Sherman B. T., Lempicki R. A., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44–57 (2009). PubMed

Hughes M. E., Hogenesch J. B., Kornacker K., JTK_CYCLE: An efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J. Biol. Rhythms 25, 372–380 (2010). PubMed PMC

Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.-Y., White D. J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A., Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012). PubMed PMC

Stojanovska V., Dijkstra D. J., Vogtmann R., Gellhaus A., Scherjon S. A., Plösch T., A double-hit pre-eclampsia model results in sex-specific growth restriction patterns. Dis. Model. Mech. 12, dmm035980 (2019). PubMed PMC

Vogtmann R., Kühnel E., Dicke N., Verkaik-Schakel R. N., Plösch T., Schorle H., Stojanovska V., Herse F., Köninger A., Kimmig R., Winterhager E., Gellhaus A., Human sFLT1 Leads to severe changes in placental differentiation and vascularization in a Transgenic hsFLT1/rtTA FGR Mouse Model. Front. Endocrinol. 10, 165 (2019). PubMed PMC

Quagliarini F., Mir A. A., Balazs K., Wierer M., Dyar K. A., Jouffe C., Makris K., Hawe J., Heinig M., Filipp F. V., Barish G. D., Uhlenhaut N. H., Cistromic reprogramming of the diurnal glucocorticoid hormone response by high-fat diet. Mol. Cell 76, 531–545.e5 (2019). PubMed PMC

Karp N. A., Mason J., Beaudet A. L., Benjamini Y., Bower L., Braun R. E., Brown S. D. M., Chesler E. J., Dickinson M. E., Flenniken A. M., Fuchs H., de Angelis M. H., Gao X., Guo S., Greenaway S., Heller R., Herault Y., Justice M. J., Kurbatova N., Lelliott C. J., Lloyd K. C. K., Mallon A.-M., Mank J. E., Masuya H., Kerlie C. M., Meehan T. F., Mott R. F., Murray S. A., Parkinson H., Ramirez-Solis R., Santos L., Seavitt J. R., Smedley D., Sorg T., Speak A. O., Steel K. P., Svenson K. L.; International Mouse Phenotyping Consortium, Wakana S., West D., Wells S., Westerberg H., Yaacoby S., White J. K., Prevalence of sexual dimorphism in mammalian phenotypic traits. Nat. Commun. 8, 15475 (2017). PubMed PMC

Aiken C. E., Ozanne S. E., Sex differences in developmental programming models. Reproduction 145, R1–R13 (2013). PubMed

Pembrey M. E., Bygren L. O., Kaati G., Edvinsson S., Northstone K., Sjöström M., Golding J.; ALSPAC Study Team , Sex-specific, male-line transgenerational responses in humans. Eur. J. Hum. Genet. 14, 159–166 (2006). PubMed

Wever R. A., Sex differences in human circadian rhythms: Intrinsic periods and sleep fractions. Experientia 40, 1226–1234 (1984). PubMed

Lacagnina S., The Developmental Origins of Health and Disease (DOHaD). Am. J. Lifestyle Med. 14, 47–50 (2020). PubMed PMC

Dearden L., Ozanne S. E., Early life origins of metabolic disease: Developmental programming of hypothalamic pathways controlling energy homeostasis. Front. Neuroendocrinol. 39, 3–16 (2015). PubMed

Fukami T., Sun X., Li T., Desai M., Ross M. G., Mechanism of programmed obesity in intrauterine fetal growth restricted offspring: Paradoxically enhanced appetite stimulation in fed and fasting states. Reprod. Sci. 19, 423–430 (2012). PubMed PMC

Hart B., Morgan E., Alejandro E. U., Nutrient sensor signaling pathways and cellular stress in fetal growth restriction. J. Mol. Endocrinol. 62, R155–R165 (2019). PubMed PMC

Yung H. w., Hemberger M., Watson E. D., Senner C. E., Jones C. P., Kaufman R. J., Charnock-Jones D. S., Burton G. J., Endoplasmic reticulum stress disrupts placental morphogenesis: Implications for human intrauterine growth restriction. J. Pathol. 228, 554–564 (2012). PubMed PMC

Horseman N. D., Ehret C. F., Glucocorticosteroid injection is a circadian zeitgeber in the laboratory rat. Am. J. Physiol. 243, R373–R378 (1982). PubMed

Le Minh N., Damiola F., Tronche F., Schütz G., Schibler U., Glucocorticoid hormones inhibit food-induced phase-shifting of peripheral circadian oscillators. EMBO J. 20, 7128–7136 (2001). PubMed PMC

Schjenken J. E., Robertson S. A., Seminal fluid signalling in the female reproductive tract: Implications for reproductive success and offspring health. Adv. Exp. Med. Biol. 868, 127–158 (2015). PubMed

Bromfield J. J., Schjenken J. E., Chin P. Y., Care A. S., Jasper M. J., Robertson S. A., Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc. Natl. Acad. Sci. U.S.A. 111, 2200–2205 (2014). PubMed PMC

Chan J. C., Morgan C. P., Leu N. A., Shetty A., Cisse Y. M., Nugent B. M., Morrison K. E., Jašarević E., Huang W., Kanyuch N., Rodgers A. B., Bhanu N. V., Berger D. S., Garcia B. A., Ament S., Kane M., Epperson C. N., Bale T. L., Reproductive tract extracellular vesicles are sufficient to transmit intergenerational stress and program neurodevelopment. Nat. Commun. 11, 1499 (2020). PubMed PMC

Lane M., Robker R. L., Robertson S. A., Parenting from before conception. Science 345, 756–760 (2014). PubMed

Watkins A. J., Dias I., Tsuro H., Allen D., Emes R. D., Moreton J., Wilson R., Ingram R. J. M., Sinclair K. D., Paternal diet programs offspring health through sperm- and seminal plasma-specific pathways in mice. Proc. Natl. Acad. Sci. U.S.A. 115, 10064–10069 (2018). PubMed PMC

Qian J., Scheer F. A. J. L., Circadian system and glucose metabolism: Implications for physiology and disease. Trends Endocrinol. Metab. 27, 282–293 (2016). PubMed PMC

Skvortsova K., Iovino N., Bogdanović O., Functions and mechanisms of epigenetic inheritance in animals. Nat. Rev. Mol. Cell Biol. 19, 774–790 (2018). PubMed

Caminos J. E., Bravo S. B., González C. R., Garcés M. F., Cepeda L. A., González A. C., Cordido F., López M., Diéguez C., Food-intake-regulating-neuropeptides are expressed and regulated through pregnancy and following food restriction in rat placenta. Reprod. Biol. Endocrinol. 6, 14 (2008). PubMed PMC

Li C., McDonald T. J., Wu G., Nijland M. J., Nathanielsz P. W., Intrauterine growth restriction alters term fetal baboon hypothalamic appetitive peptide balance. J. Endocrinol. 217, 275–282 (2013). PubMed PMC

Matthews S. G., McGowan P. O., Developmental programming of the HPA axis and related behaviours: Epigenetic mechanisms. J. Endocrinol. 242, T69–T79 (2019). PubMed

Schmidt M., Rauh M., Schmid M. C., Huebner H., Ruebner M., Wachtveitl R., Cordasic N., Rascher W., Menendez-Castro C., Hartner A., Fahlbusch F. B., Influence of low protein diet-induced fetal growth restriction on the neuroplacental corticosterone axis in the rat. Front. Endocrinol. 10, 124 (2019). PubMed PMC

Son G. H., Chung S., Choe H. K., Kim H.-D., Baik S.-M., Lee H., Lee H.-W., Choi S., Sun W., Kim H., Cho S., Lee K. H., Kim K., Adrenal peripheral clock controls the autonomous circadian rhythm of glucocorticoid by causing rhythmic steroid production. Proc. Natl. Acad. Sci. U.S.A. 105, 20970–20975 (2008). PubMed PMC

Claydon A. J., Ramm S. A., Pennington A., Hurst J. L., Stockley P., Beynon R., Heterogenous turnover of sperm and seminal vesicle proteins in the mouse revealed by dynamic metabolic labeling. Mol. Cell. Proteomics 11, M111.014993 (2012). PubMed PMC

Binder N. K., Sheedy J. R., Hannan N. J., Gardner D. K., Male obesity is associated with changed spermatozoa Cox4i1 mRNA level and altered seminal vesicle fluid composition in a mouse model. Mol. Hum. Reprod. 21, 424–434 (2015). PubMed

Eisenberg M. L., Kim S., Chen Z., Sundaram R., Schisterman E. F., Buck Louis G. M., The relationship between male BMI and waist circumference on semen quality: Data from the LIFE study. Hum. Reprod. 29, 193–200 (2014). PubMed PMC

Hampl R., Kubátová J., Sobotka V., Heráček J., Steroids in semen, their role in spermatogenesis, and the possible impact of endocrine disruptors. Horm. Mol. Biol. Clin. Investig. 13, 1–5 (2013). PubMed

Olesti E., Garcia A., Rahban R., Rossier M. F., Boccard J., Nef S., González-Ruiz V., Rudaz S., Steroid profile analysis by LC-HRMS in human seminal fluid. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 1136, 121929 (2020). PubMed

Kieffer T. E. C., Chin P. Y., Green E. S., Moldenhauer L. M., Prins J. R., Robertson S. A., Prednisolone in early pregnancy inhibits regulatory T cell generation and alters fetal and placental development in mice. Mol. Hum. Reprod. 26, 340–352 (2020). PubMed

Whirledge S., Cidlowski J. A., Glucocorticoids and reproduction: Traffic control on the road to reproduction. Trends Endocrinol. Metab. 28, 399–415 (2017). PubMed PMC

Cuffe J. S., O’Sullivan L., Simmons D. G., Anderson S. T., Moritz K. M., Maternal corticosterone exposure in the mouse has sex-specific effects on placental growth and mRNA expression. Endocrinology 153, 5500–5511 (2012). PubMed

Vaughan O. R., Sferruzzi-Perri A. N., Fowden A. L., Maternal corticosterone regulates nutrient allocation to fetal growth in mice. J. Physiol. 590, 5529–5540 (2012). PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...