Defining the age-dependent and tissue-specific circadian transcriptome in male mice

Christopher A. Wolff; Miguel A. Gutierrez-Monreal; Lingsong Meng; Xiping Zhang; Lauren G. Douma; Hannah M. Costello; Collin M. Douglas; Elnaz Ebrahimi; Ann Pham; Aline C. Oliveira; Chunhua Fu; Amy Nguyen; Bryan R. Alava; Stuart J. Hesketh; Andrew R. Morris; Mehari M. Endale; G. Ryan Crislip; Kit yan Cheng; Elizabeth A. Schroder; Brian P. Delisle; Andrew J. Bryant; Michelle L. Gumz; Zhiguang Huo; Andrew C. Liu; Karyn A. Esser

doi:10.1016/j.celrep.2022.111982

Defining the age-dependent and tissue-specific circadian transcriptome in male mice

Christopher A. Wolff, Miguel A. Gutierrez-Monreal, Lingsong Meng, Xiping Zhang, Lauren G. Douma, Hannah M. Costello, Collin M. Douglas, Elnaz Ebrahimi, Ann Pham, Aline C. Oliveira, Chunhua Fu, Amy Nguyen, Bryan R. Alava, Stuart J. Hesketh, Andrew R. Morris, Mehari M. Endale, G. Ryan Crislip, Kit yan Cheng, Elizabeth A. Schroder, Brian P. DelisleAndrew J. Bryant, Michelle L. Gumz, Zhiguang Huo, Andrew C. Liu, Karyn A. Esser

Research output: Contribution to journal › Article › peer-review

61 Scopus citations

Abstract

Cellular circadian clocks direct a daily transcriptional program that supports homeostasis and resilience. Emerging evidence has demonstrated age-associated changes in circadian functions. To define age-dependent changes at the systems level, we profile the circadian transcriptome in the hypothalamus, lung, heart, kidney, skeletal muscle, and adrenal gland in three age groups. We find age-dependent and tissue-specific clock output changes. Aging reduces the number of rhythmically expressed genes (REGs), indicative of weakened circadian control. REGs are enriched for the hallmarks of aging, adding another dimension to our understanding of aging. Analyzing differential gene expression within a tissue at four different times of day identifies distinct clusters of differentially expressed genes (DEGs). Increased variability of gene expression across the day is a common feature of aged tissues. This analysis extends the landscape for understanding aging and highlights the impact of aging on circadian clock function and temporal changes in gene expression.

Original language	English
Article number	111982
Journal	Cell Reports
Volume	42
Issue number	1
DOIs	https://doi.org/10.1016/j.celrep.2022.111982
State	Published - Jan 31 2023

Bibliographical note

Funding Information:
We thank the members of the Esser, Liu, Bryant, Gumz, and Huo laboratories for their work with the circadian collection, sample preparations, and lively discussions while developing this dataset and manuscript. We also thank Drs. Yanping Zhang and David Moraga from the University of Florida Interdisciplinary Center for Biotechnology Research (ICBR) for library preparation and sequencing (RRID: SCR_019152 ) and the UF high-performance computing cluster. This work was supported by grants ( R01HL141343 to B.P.D.; R01HL142776 and R01HL142887 to A.J.B.; R56DK128271 and R01DK109570 to M.L.G.; R01NS054794 and R01NS117457 to A.C.L.; R01HL153042 to B.P.D. and K.A.E.; and R01AR079220 to K.A.E.) and support from the UF NIH Claude D. Pepper Older Americans Independence Center ( P30AG028740 ) to A.C.L. and K.A.E. and the Office of Research Affairs , UF College of Medicine.

Funding Information:
We thank the members of the Esser, Liu, Bryant, Gumz, and Huo laboratories for their work with the circadian collection, sample preparations, and lively discussions while developing this dataset and manuscript. We also thank Drs. Yanping Zhang and David Moraga from the University of Florida Interdisciplinary Center for Biotechnology Research (ICBR) for library preparation and sequencing (RRID:SCR_019152) and the UF high-performance computing cluster. This work was supported by grants (R01HL141343 to B.P.D.; R01HL142776 and R01HL142887 to A.J.B.; R56DK128271 and R01DK109570 to M.L.G.; R01NS054794 and R01NS117457 to A.C.L.; R01HL153042 to B.P.D. and K.A.E.; and R01AR079220 to K.A.E.) and support from the UF NIH Claude D. Pepper Older Americans Independence Center (P30AG028740) to A.C.L. and K.A.E. and the Office of Research Affairs, UF College of Medicine. Conceptualization, C.A.W. M.A.G. A.C.L. M.L.G. A.J.B. and K.A.E.; methodology, C.A.W. L.M. Z.H.; investigation, C.A.W. X.Z. M.A.G. C.M.D. A.R.M. M.M.E. E.E. E.A.S. and B.P.D.; writing – original draft, C.A.W. M.A.G. A.C.L. and K.A.E.; writing – review & editing, all authors reviewed and approved the final version of this manuscript; funding acquisition, B.P.D. A.J.B. M.L.G. Z.H. A.C.L. and K.A.E.; resources, A.C.L. M.L.G. A.J.B. Z.H. and K.A.E.; supervision, A.C.L. M.L.G. Z.H. A.J.B. and K.A.E. The authors declare no competing interests. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in their field of research or within their geographical location. One or more authors of this paper self-identifies as a member of the LGBTQIA+ community. One or more of the authors of this paper received support from a program designed to increase minority representation in their field of research.

Publisher Copyright:
© 2022 The Author(s)

Keywords

adrenal gland
aging
circadian clock
CP: Developmental biology
CP: Molecular biology
heart
hypothalamus
kidney
lung
RNA-seq
skeletal muscle

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

Access to Document

10.1016/j.celrep.2022.111982

Cite this

Wolff, C. A., Gutierrez-Monreal, M. A., Meng, L., Zhang, X., Douma, L. G., Costello, H. M., Douglas, C. M., Ebrahimi, E., Pham, A., Oliveira, A. C., Fu, C., Nguyen, A., Alava, B. R., Hesketh, S. J., Morris, A. R., Endale, M. M., Crislip, G. R., Cheng, K. Y., Schroder, E. A., ... Esser, K. A. (2023). Defining the age-dependent and tissue-specific circadian transcriptome in male mice. Cell Reports, 42(1), Article 111982. https://doi.org/10.1016/j.celrep.2022.111982

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title = "Defining the age-dependent and tissue-specific circadian transcriptome in male mice",

abstract = "Cellular circadian clocks direct a daily transcriptional program that supports homeostasis and resilience. Emerging evidence has demonstrated age-associated changes in circadian functions. To define age-dependent changes at the systems level, we profile the circadian transcriptome in the hypothalamus, lung, heart, kidney, skeletal muscle, and adrenal gland in three age groups. We find age-dependent and tissue-specific clock output changes. Aging reduces the number of rhythmically expressed genes (REGs), indicative of weakened circadian control. REGs are enriched for the hallmarks of aging, adding another dimension to our understanding of aging. Analyzing differential gene expression within a tissue at four different times of day identifies distinct clusters of differentially expressed genes (DEGs). Increased variability of gene expression across the day is a common feature of aged tissues. This analysis extends the landscape for understanding aging and highlights the impact of aging on circadian clock function and temporal changes in gene expression.",

keywords = "adrenal gland, aging, circadian clock, CP: Developmental biology, CP: Molecular biology, heart, hypothalamus, kidney, lung, RNA-seq, skeletal muscle",

author = "Wolff, {Christopher A.} and Gutierrez-Monreal, {Miguel A.} and Lingsong Meng and Xiping Zhang and Douma, {Lauren G.} and Costello, {Hannah M.} and Douglas, {Collin M.} and Elnaz Ebrahimi and Ann Pham and Oliveira, {Aline C.} and Chunhua Fu and Amy Nguyen and Alava, {Bryan R.} and Hesketh, {Stuart J.} and Morris, {Andrew R.} and Endale, {Mehari M.} and Crislip, {G. Ryan} and Cheng, {Kit yan} and Schroder, {Elizabeth A.} and Delisle, {Brian P.} and Bryant, {Andrew J.} and Gumz, {Michelle L.} and Zhiguang Huo and Liu, {Andrew C.} and Esser, {Karyn A.}",

note = "Funding Information: We thank the members of the Esser, Liu, Bryant, Gumz, and Huo laboratories for their work with the circadian collection, sample preparations, and lively discussions while developing this dataset and manuscript. We also thank Drs. Yanping Zhang and David Moraga from the University of Florida Interdisciplinary Center for Biotechnology Research (ICBR) for library preparation and sequencing (RRID: SCR_019152 ) and the UF high-performance computing cluster. This work was supported by grants ( R01HL141343 to B.P.D.; R01HL142776 and R01HL142887 to A.J.B.; R56DK128271 and R01DK109570 to M.L.G.; R01NS054794 and R01NS117457 to A.C.L.; R01HL153042 to B.P.D. and K.A.E.; and R01AR079220 to K.A.E.) and support from the UF NIH Claude D. Pepper Older Americans Independence Center ( P30AG028740 ) to A.C.L. and K.A.E. and the Office of Research Affairs , UF College of Medicine. Funding Information: We thank the members of the Esser, Liu, Bryant, Gumz, and Huo laboratories for their work with the circadian collection, sample preparations, and lively discussions while developing this dataset and manuscript. We also thank Drs. Yanping Zhang and David Moraga from the University of Florida Interdisciplinary Center for Biotechnology Research (ICBR) for library preparation and sequencing (RRID:SCR_019152) and the UF high-performance computing cluster. This work was supported by grants (R01HL141343 to B.P.D.; R01HL142776 and R01HL142887 to A.J.B.; R56DK128271 and R01DK109570 to M.L.G.; R01NS054794 and R01NS117457 to A.C.L.; R01HL153042 to B.P.D. and K.A.E.; and R01AR079220 to K.A.E.) and support from the UF NIH Claude D. Pepper Older Americans Independence Center (P30AG028740) to A.C.L. and K.A.E. and the Office of Research Affairs, UF College of Medicine. Conceptualization, C.A.W. M.A.G. A.C.L. M.L.G. A.J.B. and K.A.E.; methodology, C.A.W. L.M. Z.H.; investigation, C.A.W. X.Z. M.A.G. C.M.D. A.R.M. M.M.E. E.E. E.A.S. and B.P.D.; writing – original draft, C.A.W. M.A.G. A.C.L. and K.A.E.; writing – review & editing, all authors reviewed and approved the final version of this manuscript; funding acquisition, B.P.D. A.J.B. M.L.G. Z.H. A.C.L. and K.A.E.; resources, A.C.L. M.L.G. A.J.B. Z.H. and K.A.E.; supervision, A.C.L. M.L.G. Z.H. A.J.B. and K.A.E. The authors declare no competing interests. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in their field of research or within their geographical location. One or more authors of this paper self-identifies as a member of the LGBTQIA+ community. One or more of the authors of this paper received support from a program designed to increase minority representation in their field of research. Publisher Copyright: {\textcopyright} 2022 The Author(s)",

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doi = "10.1016/j.celrep.2022.111982",

language = "English",

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Wolff, CA, Gutierrez-Monreal, MA, Meng, L, Zhang, X, Douma, LG, Costello, HM, Douglas, CM, Ebrahimi, E, Pham, A, Oliveira, AC, Fu, C, Nguyen, A, Alava, BR, Hesketh, SJ, Morris, AR, Endale, MM, Crislip, GR, Cheng, KY, Schroder, EA , Delisle, BP, Bryant, AJ, Gumz, ML, Huo, Z, Liu, AC & Esser, KA 2023, 'Defining the age-dependent and tissue-specific circadian transcriptome in male mice', Cell Reports, vol. 42, no. 1, 111982. https://doi.org/10.1016/j.celrep.2022.111982

TY - JOUR

T1 - Defining the age-dependent and tissue-specific circadian transcriptome in male mice

AU - Wolff, Christopher A.

AU - Gutierrez-Monreal, Miguel A.

AU - Meng, Lingsong

AU - Zhang, Xiping

AU - Douma, Lauren G.

AU - Costello, Hannah M.

AU - Douglas, Collin M.

AU - Ebrahimi, Elnaz

AU - Pham, Ann

AU - Oliveira, Aline C.

AU - Fu, Chunhua

AU - Nguyen, Amy

AU - Alava, Bryan R.

AU - Hesketh, Stuart J.

AU - Morris, Andrew R.

AU - Endale, Mehari M.

AU - Crislip, G. Ryan

AU - Cheng, Kit yan

AU - Schroder, Elizabeth A.

AU - Delisle, Brian P.

AU - Bryant, Andrew J.

AU - Gumz, Michelle L.

AU - Huo, Zhiguang

AU - Liu, Andrew C.

AU - Esser, Karyn A.

N1 - Funding Information: We thank the members of the Esser, Liu, Bryant, Gumz, and Huo laboratories for their work with the circadian collection, sample preparations, and lively discussions while developing this dataset and manuscript. We also thank Drs. Yanping Zhang and David Moraga from the University of Florida Interdisciplinary Center for Biotechnology Research (ICBR) for library preparation and sequencing (RRID: SCR_019152 ) and the UF high-performance computing cluster. This work was supported by grants ( R01HL141343 to B.P.D.; R01HL142776 and R01HL142887 to A.J.B.; R56DK128271 and R01DK109570 to M.L.G.; R01NS054794 and R01NS117457 to A.C.L.; R01HL153042 to B.P.D. and K.A.E.; and R01AR079220 to K.A.E.) and support from the UF NIH Claude D. Pepper Older Americans Independence Center ( P30AG028740 ) to A.C.L. and K.A.E. and the Office of Research Affairs , UF College of Medicine. Funding Information: We thank the members of the Esser, Liu, Bryant, Gumz, and Huo laboratories for their work with the circadian collection, sample preparations, and lively discussions while developing this dataset and manuscript. We also thank Drs. Yanping Zhang and David Moraga from the University of Florida Interdisciplinary Center for Biotechnology Research (ICBR) for library preparation and sequencing (RRID:SCR_019152) and the UF high-performance computing cluster. This work was supported by grants (R01HL141343 to B.P.D.; R01HL142776 and R01HL142887 to A.J.B.; R56DK128271 and R01DK109570 to M.L.G.; R01NS054794 and R01NS117457 to A.C.L.; R01HL153042 to B.P.D. and K.A.E.; and R01AR079220 to K.A.E.) and support from the UF NIH Claude D. Pepper Older Americans Independence Center (P30AG028740) to A.C.L. and K.A.E. and the Office of Research Affairs, UF College of Medicine. Conceptualization, C.A.W. M.A.G. A.C.L. M.L.G. A.J.B. and K.A.E.; methodology, C.A.W. L.M. Z.H.; investigation, C.A.W. X.Z. M.A.G. C.M.D. A.R.M. M.M.E. E.E. E.A.S. and B.P.D.; writing – original draft, C.A.W. M.A.G. A.C.L. and K.A.E.; writing – review & editing, all authors reviewed and approved the final version of this manuscript; funding acquisition, B.P.D. A.J.B. M.L.G. Z.H. A.C.L. and K.A.E.; resources, A.C.L. M.L.G. A.J.B. Z.H. and K.A.E.; supervision, A.C.L. M.L.G. Z.H. A.J.B. and K.A.E. The authors declare no competing interests. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in their field of research or within their geographical location. One or more authors of this paper self-identifies as a member of the LGBTQIA+ community. One or more of the authors of this paper received support from a program designed to increase minority representation in their field of research. Publisher Copyright: © 2022 The Author(s)

PY - 2023/1/31

Y1 - 2023/1/31

N2 - Cellular circadian clocks direct a daily transcriptional program that supports homeostasis and resilience. Emerging evidence has demonstrated age-associated changes in circadian functions. To define age-dependent changes at the systems level, we profile the circadian transcriptome in the hypothalamus, lung, heart, kidney, skeletal muscle, and adrenal gland in three age groups. We find age-dependent and tissue-specific clock output changes. Aging reduces the number of rhythmically expressed genes (REGs), indicative of weakened circadian control. REGs are enriched for the hallmarks of aging, adding another dimension to our understanding of aging. Analyzing differential gene expression within a tissue at four different times of day identifies distinct clusters of differentially expressed genes (DEGs). Increased variability of gene expression across the day is a common feature of aged tissues. This analysis extends the landscape for understanding aging and highlights the impact of aging on circadian clock function and temporal changes in gene expression.

AB - Cellular circadian clocks direct a daily transcriptional program that supports homeostasis and resilience. Emerging evidence has demonstrated age-associated changes in circadian functions. To define age-dependent changes at the systems level, we profile the circadian transcriptome in the hypothalamus, lung, heart, kidney, skeletal muscle, and adrenal gland in three age groups. We find age-dependent and tissue-specific clock output changes. Aging reduces the number of rhythmically expressed genes (REGs), indicative of weakened circadian control. REGs are enriched for the hallmarks of aging, adding another dimension to our understanding of aging. Analyzing differential gene expression within a tissue at four different times of day identifies distinct clusters of differentially expressed genes (DEGs). Increased variability of gene expression across the day is a common feature of aged tissues. This analysis extends the landscape for understanding aging and highlights the impact of aging on circadian clock function and temporal changes in gene expression.

KW - adrenal gland

KW - aging

KW - circadian clock

KW - CP: Developmental biology

KW - CP: Molecular biology

KW - heart

KW - hypothalamus

KW - kidney

KW - lung

KW - RNA-seq

KW - skeletal muscle

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UR - http://www.scopus.com/inward/citedby.url?scp=85146087656&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2022.111982

DO - 10.1016/j.celrep.2022.111982

M3 - Article

C2 - 36640301

AN - SCOPUS:85146087656

SN - 2211-1247

VL - 42

JO - Cell Reports

JF - Cell Reports

IS - 1

M1 - 111982

ER -

Defining the age-dependent and tissue-specific circadian transcriptome in male mice

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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