Osteocyte Transcriptome Mapping Identifies a Molecular Landscape Controlling Skeletal Homeostasis and Susceptibility to Skeletal Disease

Abstract Osteocytes are master regulators of the skeleton. We mapped the transcriptome of osteocytes from different skeletal sites, across age and sexes in mice to reveal genes and molecular programs that control this complex cellular-network. We define an osteocyte transcriptome signature of 1239 g...

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Main Authors Youlten, Scott E, Kemp, John P, Logan, John G, Ghirardello, Elena J, Sergio, Claudio M, Dack, Michael R G, Guilfoyle, Siobhan E, Leitch, Victoria D, Butterfield, Natalie C, Komla-Ebri, Davide, Chai, Ryan C, Corr, Alexander P, Smith, James T, Mohanty, Sindhu, Morris, John A, Mcdonald, Michelle M, Quinn, Julian M W, Mcglade, Amelia R, Bartonicek, Nenad, Jansson, Matt, Hatzikotoulas, Konstantinos, Irving, Melita D, Beleza-Meireles, Ana, Rivadeneira, Fernando, Duncan, Emma, Richards, J Brent, Adams, David J, Lelliott, Christopher J, Brink, Robert, Tri Giang Phan, Eisman, John A, Evans, David M, Zeggini, Eleftheria, Baldock, Paul A, Duncan Bassett, J H, Williams, Graham R, Croucher, Peter I
Format Paper
LanguageEnglish
Published Cold Spring Harbor Cold Spring Harbor Laboratory Press 04.11.2020
Cold Spring Harbor Laboratory
Edition1.2
Subjects
Cancer immunotherapy
Dormancy
Gene expression
Homeostasis
Immunotherapy
Osteoarthritis
Osteocytes
Osteoporosis
Skeleton
Structure-function relationships
Systems Biology
Online AccessGet full text
ISSN2692-8205
2692-8205
DOI10.1101/2020.04.20.051409

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Abstract Abstract Osteocytes are master regulators of the skeleton. We mapped the transcriptome of osteocytes from different skeletal sites, across age and sexes in mice to reveal genes and molecular programs that control this complex cellular-network. We define an osteocyte transcriptome signature of 1239 genes that distinguishes osteocytes from other cells. 77% have no previously known role in the skeleton and are enriched for genes regulating neuronal network formation, suggesting this program is important in osteocyte communication. We evaluated 19 skeletal parameters in 733 knockout mouse lines and reveal 26 osteocyte transcriptome signature genes that control bone structure and function. We showed osteocyte transcriptome signature genes are enriched for human orthologs that cause monogenic skeletal disorders (P=2.4×10-22) and are associated with the polygenic diseases osteoporosis (P=1.8×10-13) and osteoarthritis (P=1.6×10-7). Thus, we reveal the molecular landscape that regulates osteocyte network formation and function and establish the importance of osteocytes in human skeletal disease. Competing Interest Statement T.G.P is a consultant for Imugene Pty Ltd, an Australian biotech working in cancer immunotherapy. P.I.C has funding from AMGEN for studies of cancer dormancy. Neither competing interests are the subject of this manuscript. Footnotes * ↵27 Co-senior author
AbstractList Abstract Osteocytes are master regulators of the skeleton. We mapped the transcriptome of osteocytes from different skeletal sites, across age and sexes in mice to reveal genes and molecular programs that control this complex cellular-network. We define an osteocyte transcriptome signature of 1239 genes that distinguishes osteocytes from other cells. 77% have no previously known role in the skeleton and are enriched for genes regulating neuronal network formation, suggesting this program is important in osteocyte communication. We evaluated 19 skeletal parameters in 733 knockout mouse lines and reveal 26 osteocyte transcriptome signature genes that control bone structure and function. We showed osteocyte transcriptome signature genes are enriched for human orthologs that cause monogenic skeletal disorders (P=2.4×10-22) and are associated with the polygenic diseases osteoporosis (P=1.8×10-13) and osteoarthritis (P=1.6×10-7). Thus, we reveal the molecular landscape that regulates osteocyte network formation and function and establish the importance of osteocytes in human skeletal disease. Competing Interest Statement T.G.P is a consultant for Imugene Pty Ltd, an Australian biotech working in cancer immunotherapy. P.I.C has funding from AMGEN for studies of cancer dormancy. Neither competing interests are the subject of this manuscript. Footnotes * ↵27 Co-senior author
Osteocytes are master regulators of the skeleton. We mapped the transcriptome of osteocytes from different skeletal sites, across age and sexes in mice to reveal genes and molecular programs that control this complex cellular-network. We define an osteocyte transcriptome signature of 1239 genes that distinguishes osteocytes from other cells. 77% have no previously known role in the skeleton and are enriched for genes regulating neuronal network formation, suggesting this program is important in osteocyte communication. We evaluated 19 skeletal parameters in 733 knockout mouse lines and reveal 26 osteocyte transcriptome signature genes that control bone structure and function. We showed osteocyte transcriptome signature genes are enriched for human orthologs that cause monogenic skeletal disorders (P=2.4×10-22) and are associated with the polygenic diseases osteoporosis (P=1.8×10-13) and osteoarthritis (P=1.6×10-7). Thus, we reveal the molecular landscape that regulates osteocyte network formation and function and establish the importance of osteocytes in human skeletal disease.
Author Brink, Robert
Bartonicek, Nenad
Morris, John A
Duncan Bassett, J H
Irving, Melita D
Croucher, Peter I
Hatzikotoulas, Konstantinos
Smith, James T
Duncan, Emma
Butterfield, Natalie C
Lelliott, Christopher J
Zeggini, Eleftheria
Chai, Ryan C
Guilfoyle, Siobhan E
Adams, David J
Youlten, Scott E
Corr, Alexander P
Ghirardello, Elena J
Dack, Michael R G
Richards, J Brent
Rivadeneira, Fernando
Williams, Graham R
Quinn, Julian M W
Baldock, Paul A
Komla-Ebri, Davide
Jansson, Matt
Mcglade, Amelia R
Kemp, John P
Mcdonald, Michelle M
Sergio, Claudio M
Logan, John G
Tri Giang Phan
Beleza-Meireles, Ana
Mohanty, Sindhu
Eisman, John A
Leitch, Victoria D
Evans, David M
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Cites_doi 10.1016/j.chemolab.2011.08.009
10.1136/annrheumdis-2014-205327
10.1002/ajmg.a.61366
10.1038/s41586-018-0590-4
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Competing Interest Statement: T.G.P is a consultant for Imugene Pty Ltd, an Australian biotech working in cancer immunotherapy. P.I.C has funding from AMGEN for studies of cancer dormancy. Neither competing interests are the subject of this manuscript.
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Snippet Abstract Osteocytes are master regulators of the skeleton. We mapped the transcriptome of osteocytes from different skeletal sites, across age and sexes in...
Osteocytes are master regulators of the skeleton. We mapped the transcriptome of osteocytes from different skeletal sites, across age and sexes in mice to...
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SubjectTerms Cancer immunotherapy
Dormancy
Gene expression
Homeostasis
Immunotherapy
Osteoarthritis
Osteocytes
Osteoporosis
Skeleton
Structure-function relationships
Systems Biology
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Title Osteocyte Transcriptome Mapping Identifies a Molecular Landscape Controlling Skeletal Homeostasis and Susceptibility to Skeletal Disease
URI https://www.proquest.com/docview/2393247120
https://www.biorxiv.org/content/10.1101/2020.04.20.051409
https://www.biorxiv.org/content/biorxiv/early/2020/11/04/2020.04.20.051409.full.pdf
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