Aging impairs the osteocytic regulation of collagen integrity and bone quality

Schurman, Charles A.; Kaya, Serra; Dole, Neha; Luna, Nadja Maldonado; Castillo, Natalia; Potter, Ryan; Rose, Jacob P.; Bons, Joanna; King, Christina D.; Burton, Jordan B.; Schilling, Birgit; Melov, Simon; Tang, Simon; Schaible, Eric; Alliston, Tamara

doi:10.1038/s41413-023-00303-7

Title: Aging impairs the osteocytic regulation of collagen integrity and bone quality

Journal Article · 25 February 2024 · Bone Research

DOI: https://doi.org/10.1038/s41413-023-00303-7 · OSTI ID:2470702

^[1];

^[2]; Dole, Neha ^[2]; Luna, Nadja Maldonado ^[3]; Castillo, Natalia ^[2]; Potter, Ryan ^[4]; Rose, Jacob P. ^[5];

^[5]; King, Christina D. ^[5];

^[5];

^[5]; Tang, Simon ^[4]; Schaible, Eric ^[6];

^[3]

Univ. of California, San Francisco, CA (United States); University of California, Berkeley, CA (United States); Buck Institute for Research on Aging, Novato, CA (United States)
Univ. of California, San Francisco, CA (United States)
Univ. of California, San Francisco, CA (United States); University of California, Berkeley, CA (United States)
Washington Univ., St. Louis, MO (United States)
Buck Institute for Research on Aging, Novato, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)

Poor bone quality is a major factor in skeletal fragility in elderly individuals. The molecular mechanisms that establish and maintain bone quality, independent of bone mass, are unknown but are thought to be primarily determined by osteocytes. We hypothesize that the age-related decline in bone quality results from the suppression of osteocyte perilacunar/canalicular remodeling (PLR), which maintains bone material properties. We examined bones from young and aged mice with osteocyte-intrinsic repression of TGFβ signaling (TβRII^ocy–/–) that suppresses PLR. The control aged bone displayed decreased TGFβ signaling and PLR, but aging did not worsen the existing PLR suppression in male TβRII^ocy–/– bone. This relationship impacted the behavior of collagen material at the nanoscale and tissue scale in macromechanical tests. The effects of age on bone mass, density, and mineral material behavior were independent of osteocytic TGFβ. We determined that the decline in bone quality with age arises from the loss of osteocyte function and the loss of TGFβ-dependent maintenance of collagen integrity.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2470702

Journal Information:: Bone Research, Journal Name: Bone Research Journal Issue: 1 Vol. 12; ISSN 2095-6231

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

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