DNA methylation networks underlying mammalian traits-Reference-Cited by-同舟云学术

DNA methylation networks underlying mammalian traits

Published:2023-08-11 Issue:6658 Volume:381 Page:
ISSN:0036-8075
Container-title:Science
language:en
Short-container-title:Science

Author:

Haghani Amin¹²^ORCID,Li Caesar Z.³⁴^ORCID,Robeck Todd R.⁵^ORCID,Zhang Joshua¹^ORCID,Lu Ake T.¹²^ORCID,Ablaeva Julia⁶^ORCID,Acosta-Rodríguez Victoria A.⁷^ORCID,Adams Danielle M.⁸^ORCID,Alagaili Abdulaziz N.⁹^ORCID,Almunia Javier¹⁰^ORCID,Aloysius Ajoy¹¹^ORCID,Amor Nabil M.S.¹²^ORCID,Ardehali Reza¹³^ORCID,Arneson Adriana¹⁴¹⁵^ORCID,Baker C. Scott¹⁶^ORCID,Banks Gareth¹⁷^ORCID,Belov Katherine¹⁸^ORCID,Bennett Nigel C.¹⁹^ORCID,Black Peter²⁰^ORCID,Blumstein Daniel T.²¹²²^ORCID,Bors Eleanor K.¹⁶^ORCID,Breeze Charles E.²³^ORCID,Brooke Robert T.²⁴^ORCID,Brown Janine L.²⁵,Carter Gerald²⁶^ORCID,Caulton Alex²⁷²⁸^ORCID,Cavin Julie M.²⁹^ORCID,Chakrabarti Lisa³⁰^ORCID,Chatzistamou Ioulia³¹^ORCID,Chavez Andreas S.²⁶³²^ORCID,Chen Hao³³^ORCID,Cheng Kaiyang³⁴,Chiavellini Priscila³⁵^ORCID,Choi Oi-Wa³⁶³⁷,Clarke Shannon²⁷^ORCID,Cook Joseph A.³⁸^ORCID,Cooper Lisa N.³⁹,Cossette Marie-Laurence⁴⁰^ORCID,Day Joanna⁴¹^ORCID,DeYoung Joseph³⁶³⁷,Dirocco Stacy⁴²^ORCID,Dold Christopher⁵^ORCID,Dunnum Jonathan L.³⁸^ORCID,Ehmke Erin E.⁴³^ORCID,Emmons Candice K.⁴⁴^ORCID,Emmrich Stephan⁶^ORCID,Erbay Ebru⁴⁵⁴⁶⁴⁷^ORCID,Erlacher-Reid Claire⁴²^ORCID,Faulkes Chris G.⁴⁸⁴⁹,Fei Zhe³⁵⁰^ORCID,Ferguson Steven H.⁵¹⁵²^ORCID,Finno Carrie J.⁵³^ORCID,Flower Jennifer E.⁵⁴,Gaillard Jean-Michel⁵⁵,Garde Eva⁵⁶^ORCID,Gerber Livia⁵⁷⁵⁸^ORCID,Gladyshev Vadim N.⁵⁹^ORCID,Goya Rodolfo G.³⁵^ORCID,Grant Matthew J⁶⁰^ORCID,Green Carla B.⁷^ORCID,Hanson M. Bradley⁴⁴^ORCID,Hart Daniel W.¹⁹^ORCID,Haulena Martin⁶¹^ORCID,Herrick Kelsey⁶²,Hogan Andrew N.⁶³,Hogg Carolyn J.¹⁸^ORCID,Hore Timothy A.⁶⁴^ORCID,Huang Taosheng⁶⁵^ORCID,Izpisua Belmonte Juan Carlos²,Jasinska Anna J.³⁶⁶⁶⁶⁷^ORCID,Jones Gareth⁶⁸^ORCID,Jourdain Eve⁶⁹,Kashpur Olga⁷⁰,Katcher Harold⁷¹,Katsumata Etsuko⁷²,Kaza Vimala⁷³^ORCID,Kiaris Hippokratis⁷⁴^ORCID,Kobor Michael S.⁷⁵^ORCID,Kordowitzki Pawel⁷⁶^ORCID,Koski William R.⁷⁷^ORCID,Krützen Michael⁷⁸^ORCID,Kwon Soo Bin¹⁴¹⁵^ORCID,Larison Brenda²¹⁷⁹^ORCID,Lee Sang-Goo⁵⁹^ORCID,Lehmann Marianne³⁵,Lemaître Jean-François⁵⁵^ORCID,Levine Andrew J.⁸⁰,Li Xinmin⁸¹,Li Cun⁸²⁸³^ORCID,Lim Andrea R.¹^ORCID,Lin David T. S.⁸⁴^ORCID,Lindemann Dana M.⁴²^ORCID,Liphardt Schuyler W.⁸⁵^ORCID,Little Thomas J.⁸⁶^ORCID,Macoretta Nicholas⁶,Maddox Dewey⁸⁷,Matkin Craig O.⁸⁸,Mattison Julie A.⁸⁹^ORCID,McClure Matthew⁹⁰^ORCID,Mergl June⁹¹,Meudt Jennifer J.⁹²,Montano Gisele A.⁵^ORCID,Mozhui Khyobeni⁹³^ORCID,Munshi-South Jason⁹⁴^ORCID,Murphy William J.⁹⁵⁹⁶^ORCID,Naderi Asieh⁷⁴^ORCID,Nagy Martina⁹⁷^ORCID,Narayan Pritika⁶⁰^ORCID,Nathanielsz Peter W.⁸²⁸³^ORCID,Nguyen Ngoc B.¹³^ORCID,Niehrs Christof⁹⁸⁹⁹^ORCID,Nyamsuren Batsaikhan¹⁰⁰,O’Brien Justine K.⁴¹^ORCID,Ginn Perrie O’Tierney⁷⁰^ORCID,Odom Duncan T¹⁰¹¹⁰²^ORCID,Ophir Alexander G.¹⁰³^ORCID,Osborn Steve¹⁰⁴,Ostrander Elaine A.⁶³^ORCID,Parsons Kim M.⁴⁴^ORCID,Paul Kimberly C.⁸⁰^ORCID,Pedersen Amy B.⁸⁶^ORCID,Pellegrini Matteo¹⁰⁵^ORCID,Peters Katharina J.⁷⁸¹⁰⁶^ORCID,Petersen Jessica L.¹⁰⁷^ORCID,Pietersen Darren W.¹⁰⁸^ORCID,Pinho Gabriela M.²¹^ORCID,Plassais Jocelyn⁶³^ORCID,Poganik Jesse R.⁵⁹^ORCID,Prado Natalia A.¹⁰⁹¹¹⁰^ORCID,Reddy Pradeep²¹¹¹^ORCID,Rey Benjamin⁵⁵^ORCID,Ritz Beate R.⁸⁰¹¹²¹¹³^ORCID,Robbins Jooke¹¹⁴^ORCID,Rodriguez Magdalena¹¹⁵^ORCID,Russell Jennifer¹⁰⁴^ORCID,Rydkina Elena⁶,Sailer Lindsay L.¹⁰³^ORCID,Salmon Adam B.¹¹⁶^ORCID,Sanghavi Akshay⁷¹^ORCID,Schachtschneider Kyle M.¹¹⁷¹¹⁸¹¹⁹^ORCID,Schmitt Dennis¹²⁰^ORCID,Schmitt Todd⁶²^ORCID,Schomacher Lars⁹⁸^ORCID,Schook Lawrence B.¹¹⁷¹²¹,Sears Karen E.²¹^ORCID,Seifert Ashley W.¹¹^ORCID,Shafer Aaron B.A.¹²²^ORCID,Shindyapina Anastasia V.⁵⁹^ORCID,Simmons Melanie⁴³^ORCID,Singh Kavita¹²³^ORCID,Sinha Ishani²¹,Slone Jesse⁶⁵^ORCID,Snell Russel G.⁶⁰^ORCID,Soltanmohammadi Elham⁷⁴^ORCID,Spangler Matthew L.¹⁰⁷^ORCID,Spriggs Maria²⁰,Staggs Lydia⁴²^ORCID,Stedman Nancy²⁰^ORCID,Steinman Karen J.¹²⁴^ORCID,Stewart Donald T¹²⁵,Sugrue Victoria J.⁶⁴^ORCID,Szladovits Balazs¹²⁶^ORCID,Takahashi Joseph S.⁷¹²⁷^ORCID,Takasugi Masaki⁶,Teeling Emma C.¹²⁸^ORCID,Thompson Michael J.¹⁰⁵^ORCID,Van Bonn Bill¹²⁹,Vernes Sonja C.¹³⁰¹³¹^ORCID,Villar Diego¹³²^ORCID,Vinters Harry V.¹³³,Vu Ha¹⁴¹⁵^ORCID,Wallingford Mary C.⁷⁰^ORCID,Wang Nan³⁶³⁷^ORCID,Wilkinson Gerald S.⁸^ORCID,Williams Robert W.¹³⁴^ORCID,Yan Qi²³^ORCID,Yao Mingjia³,Young Brent G.⁵²^ORCID,Zhang Bohan⁵⁹^ORCID,Zhang Zhihui⁶^ORCID,Zhao Yang⁶^ORCID,Zhao Peng¹³¹³⁵^ORCID,Zhou Wanding¹³⁶¹³⁷^ORCID,Zoller Joseph A.³^ORCID,Ernst Jason¹⁴¹⁵^ORCID,Seluanov Andrei¹³⁸^ORCID,Gorbunova Vera¹³⁸^ORCID,Yang X. William³⁶³⁷^ORCID,Raj Ken¹³⁹^ORCID,Horvath Steve¹²¹³⁹^ORCID

Affiliation:

1. Department of Human Genetics, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA.

2. Altos Labs, San Diego, CA, USA.

3. Department of Biostatistics, Fielding School of Public Health, University of California Los Angeles, Los Angeles, CA, USA.

4. Janssen Research & Development, Spring House, PA, USA.

5. Zoological Operations, SeaWorld Parks and Entertainment, Orlando, FL, USA.

6. Department of Biology, University of Rochester, Rochester, NY, USA.

7. Department of Neuroscience, Peter O’Donnell Jr. Brain Institute, University of Texas Southwestern Medical Center, Dallas, TX, USA.

8. Department of Biology, University of Maryland, College Park, MD, USA.

9. Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia.

10. Loro Parque Fundacion, Avenida Loro Parque, Puerto de la Cruz, Tenerife, Spain.

11. Department of Biology, University of Kentucky, Lexington, KY, USA.

12. Laboratory of Biodiversity, Parasitology, and Ecology, University of Tunis El Manar, Tunis, Tunisia.

13. Division of Cardiology, Department of Internal Medicine, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.

14. Bioinformatics Interdepartmental Program, University of California, Los Angeles, CA, USA.

15. Department of Biological Chemistry, University of California, Los Angeles, Los Angeles, CA, USA.

16. Marine Mammal Institute, Oregon State University, Newport, OR, USA.

17. Mammalian Genetics Unit, MRC Harwell Institute, Harwell Science and Innovation Campus, Oxfordshire, UK.

18. School of Life and Environmental Sciences, The University of Sydney, Sydney, New South Wales, Australia.

19. Department of Zoology and Entomology, University of Pretoria, Hatfield, South Africa.

20. Busch Gardens Tampa, Tampa, FL, USA.

21. Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA, USA.

22. The Rocky Mountain Biological Laboratory, Crested Butte, CO, USA.

23. Altius Institute for Biomedical Sciences, Seattle, WA, USA.

24. Epigenetic Clock Development Foundation, Los Angeles, CA, USA.

25. Center for Species Survival, Smithsonian National Zoo and Conservation Biology, Front Royal, VA, USA.

26. Department of Evolution, Ecology and Organismal Biology, The Ohio State University, Columbus, OH, USA.

27. AgResearch, Invermay Agricultural Centre, Mosgiel, Otago, New Zealand.

28. Department of Biochemistry, University of Otago, Dunedin, Otago, New Zealand.

29. Gulf World Marine Park - Dolphin Company, Panama City Beach, FL, USA.

30. School of Veterinary Medicine and Science, University of Nottingham, Nottingham, UK.

31. Department of Pathology, Microbiology & Immunology, School of Medicine, University of South Carolina, Columbia, SC, USA.

32. Translational Data Analytics Institute, The Ohio State University, Columbus, OH, USA.

33. Department of Pharmacology, Addiction Science and Toxicology, The University of Tennessee Health Science Center, Memphis, TN, USA.

34. Medical Informatics, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.

35. Biochemistry Research Institute of La Plata, Histology and Pathology, School of Medicine, University of La Plata, La Plata, Argentina.

36. Center for Neurobehavioral Genetics, Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, Los Angeles, CA, USA.

37. Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA.

38. University of New Mexico, Department of Biology and Museum of Southwestern Biology, Albuquerque, NM, USA.

39. Department of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, OH, USA.

40. Department of Environmental & Life Sciences, Trent University, Peterborough, Ontario, Canada.

41. Taronga Institute of Science and Learning, Taronga Conservation Society Australia, Mosman, New South Wales, Australia.

42. SeaWorld Orlando, Orlando, FL, USA.

43. Duke Lemur Center, Durham, NC, USA.

44. Conservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, WA, USA.

45. Altos Labs, Bay Area Institute of Science, Redwood City, CA, USA.

46. Department of Cardiology, Smidt Heart Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA.

47. David Geffen School of Medicine, University of California, Los Angeles, CA, USA.

48. School of Biological and Chemical Sciences, Queen Mary University of London, London, UK.

49. School of Biological and Behavioural Sciences, Queen Mary University of London, London, UK.

50. Department of Statistics, University of California, Riverside, CA, USA.

51. Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba, Canada.

52. Fisheries and Oceans Canada, Winnipeg, Manitoba, Canada.

53. Department of Population Health and Reproduction, University of California, Davis School of Veterinary Medicine, Davis, CA, USA.

54. Mystic Aquarium, Mystic, CT, USA.

55. University of Lyon, CNRS, Laboratoire de Biométrie et Biologie Evolutive, Villeurbanne, France.

56. Greenland Institute of Natural Resources, Nuuk, Greenland.

57. School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, Australia.

58. Australian National Wildlife Collection, CSIRO, Canberra, Australia.

59. Division of Genetics, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA.

60. Applied Translational Genetics Group, School of Biological Sciences, Centre for Brain Research, The University of Auckland, Auckland, New Zealand.

61. Vancouver Aquarium, Vancouver, British Columbia, Canada.

62. SeaWorld San Diego, San Diego, CA, USA.

63. Cancer Genetics and Comparative Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA.

64. Department of Anatomy, University of Otago, Dunedin, New Zealand.

65. Division of Human Genetics, Department of Pediatrics, University at Buffalo, Buffalo, NY, USA.

66. Division of Infectious Diseases, Department of Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA, USA.

67. Department of Molecular Genetics, Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznan, Poland.

68. School of Biological Sciences, University of Bristol, Bristol, UK.

69. Norwegian Orca Survey, Andenes, Norway.

70. Mother Infant Research Institute, Tufts Medical Center, Boston, MA, USA.

71. Yuvan Research, Mountain View, CA, USA.

72. Kamogawa Sea World, Kamogawa, Chiba, Japan.

73. Peromyscus Genetic Stock Center, University of South Carolina, Columbia, SC, USA.

74. Department of Drug Discovery and Biomedical Sciences, College of Pharmacy, University of South Carolina, Columbia, SC, USA.

75. Edwin S. H. Leong Healthy Aging Program, Centre for Molecular Medicine and Therapeutics, University of British Columbia, Vancouver, British Columbia, Canada.

76. Institute of Veterinary Medicine, Nicolaus Copernicus University, Torun, Poland.

77. LGL Limited, King City, Ontario, Canada.

78. Evolutionary Genetics Group, Department of Anthropology, University of Zurich, Zurich, Switzerland.

79. Center for Tropical Research, Institute of the Environment and Sustainability, University of California, Los Angeles, Los Angeles, CA, USA.

80. Department of Neurology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA.

81. Technology Center for Genomics and Bioinformatics, Department of Pathology and Laboratory Medicine, University of California, Los Angeles, Los Angeles, CA, USA.

82. Texas Pregnancy and Life-course Health Center, Southwest National Primate Research Center, San Antonio, TX, USA.

83. Department of Animal Science, College of Agriculture and Natural Resources, Laramie, WY, USA.

84. Centre for Molecular Medicine and Therapeutics, BC Children’s Hospital Research Institute, University of British Columbia, Vancouver, British Columbia, Canada.

85. Biology Department, University of New Mexico, Albuquerque, NM, USA.

86. Institute of Ecology and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh, UK.

87. White Oak Conservation Center, Yulee, FL, USA.

88. North Gulf Oceanic Society, Homer, AK, USA.

89. Translational Gerontology Branch, National Institute on Aging Intramural Research Program, National Institutes of Health, Baltimore, MD, USA.

90. ABS Global, DeForest, WI, USA.

91. Marineland of Canada, Niagara Falls, Ontario, Canada.

92. Biomedical and Genomic Research Group, Department of Animal and Dairy Sciences, University of Wisconsin Madison, Madison, WI, USA.

93. Department of Preventive Medicine, University of Tennessee Health Science Center, College of Medicine, Memphis, TN, USA.

94. Louis Calder Center - Biological Field Station, Department of Biological Sciences, Fordham University, Armonk, NY, USA.

95. Veterinary Integrative Biosciences, Texas A&M University, College Station, TX, USA.

96. Interdisciplinary Program in Genetics and Genomics, Texas A&M University, College Station, TX, USA.

97. Museum fur Naturkunde, Leibniz-Institute for Evolution and Biodiversity Science, Berlin, Germany.

98. Institute of Molecular Biology (IMB), Mainz, Germany.

99. Division of Molecular Embryology, DKFZ-ZMBH Alliance, Heidelberg, Germany.

100. Mammalogical Society of Mongolia, Ulaanbaatar, Mongolia.

101. Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, UK.

102. Deutsches Krebsforschungszentrum, Division of Regulatory Genomics and Cancer Evolution, Heidelberg, Germany.

103. Department of Psychology, Cornell University, Ithaca, NY, USA.

104. SeaWorld San Antonio, San Antonio, TX, USA.

105. Department Molecular Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, CA, USA.

106. School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, New South Wales, Australia.

107. Department of Animal Science, University of Nebraska, Lincoln, NE, USA.

108. Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Hatfield, South Africa.

109. Department of Biology, College of Arts and Science, Adelphi University, Garden City, NY, USA.

110. Center for Species Survival, Smithsonian Conservation Biology Institute, Front Royal, VA, USA.

111. Salk Institute for Biological Studies, La Jolla, CA, USA.

112. Department of Epidemiology, UCLA Fielding School of Public Health, Los Angeles, CA, USA.

113. Department of Environmental Health Sciences, UCLA Fielding School of Public Health, Los Angeles, CA, USA.

114. Center for Coastal Studies, Provincetown, MA, USA.

115. Miami Seaquarium, Miami, FL, USA.

116. The Sam and Ann Barshop Institute for Longevity and Aging Studies and Department of Molecular Medicine, UT Health San Antonio, and the Geriatric Research Education and Clinical Center, South Texas Veterans Healthcare System, San Antonio, TX, USA.

117. Department of Radiology, University of Illinois at Chicago, Chicago, IL, USA.

118. Department of Biochemistry and Molecular Genetics, University of Illinois at Chicago, Chicago, IL, USA.

119. National Center for Supercomputing Applications, University of Illinois at Urbana-Champaign, Urbana, IL, USA.

120. College of Agriculture, Missouri State University, Springfield, MO, USA.

121. Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, USA.

122. Department of Forensic Science, Environmental & Life Sciences, Trent University, Peterborough, Ontario, Canada.

123. Shobhaben Pratapbhai Patel School of Pharmacy & Technology Management, SVKM’S NMIMS University, Mumbai, India.

124. Species Preservation Laboratory, SeaWorld San Diego, San Diego, CA, USA.

125. Biology Department, Acadia University, Wolfville, Nova Scotia, Canada.

126. Department of Pathobiology and Population Sciences, Royal Veterinary College, Hatfield, UK.

127. Howard Hughes Medical Institute, Department of Neuroscience, University of Texas Southwestern Medical Center, Dallas, TX, USA.

128. School of Biology and Environmental Science, University College Dublin, Belfield, Dublin, Ireland.

129. Animal Care and Science Division, John G. Shedd Aquarium, Chicago, IL, USA.

130. School of Biology, The University of St. Andrews, Fife, UK

131. Neurogenetics of Vocal Communication Group, Max Planck Institute for Psycholinguistics, Nijmegen, Netherlands.

132. Blizard Institute, Faculty of Medicine and Dentistry, Queen Mary University of London, London, UK.

133. Department of Pathology and Laboratory Medicine, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA.

134. Department of Genetics, Genomics and Informatics, University of Tennessee Health Science Center, College of Medicine, Memphis, TN, USA.

135. Eli and Edythe Broad Center of Regenerative Medicine and Stem Cell Research, University of California, Los Angeles, Los Angeles, CA, USA.

136. Center for Computational and Genomic Medicine, Children’s Hospital of Philadelphia, Philadelphia, PA, USA.

137. Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA, USA.

138. Departments of Biology and Medicine, University of Rochester, Rochester, NY, USA.

139. Altos Labs, Cambridge, UK.

Abstract

Using DNA methylation profiles ( n = 15,456) from 348 mammalian species, we constructed phyloepigenetic trees that bear marked similarities to traditional phylogenetic ones. Using unsupervised clustering across all samples, we identified 55 distinct cytosine modules, of which 30 are related to traits such as maximum life span, adult weight, age, sex, and human mortality risk. Maximum life span is associated with methylation levels in HOXL subclass homeobox genes and developmental processes and is potentially regulated by pluripotency transcription factors. The methylation state of some modules responds to perturbations such as caloric restriction, ablation of growth hormone receptors, consumption of high-fat diets, and expression of Yamanaka factors. This study reveals an intertwined evolution of the genome and epigenome that mediates the biological characteristics and traits of different mammalian species.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

Link

https://www.science.org/doi/pdf/10.1126/science.abq5693

Reference95 articles.

1. Comparative Epigenomic Annotation of Regulatory DNA

2. Enhancer Evolution across 20 Mammalian Species

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4. Comparative analysis of genome-scale, base-resolution DNA methylation profiles across 580 animal species

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