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Proc Natl Acad Sci U S A. 2014 Nov 11;111(45):16047-52. doi: 10.1073/pnas.1412372111. Epub 2014 Oct 20.

Remodeling in bone without osteocytes: billfish challenge bone structure-function paradigms.

Author information

1
Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 76100, Israel;
2
Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14476 Potsdam, Germany;
3
Department of Integrative Biology, University of South Florida, Tampa, FL 33613;
4
Department of Structural Biology, Weizmann Institute of Science, Rehovot 76100, Israel; and.
5
Department of Biology, University of York, York YO10 5DD, United Kingdom.
6
Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot 76100, Israel; ron.shahar1@mail.huji.ac.il.

Abstract

A remarkable property of tetrapod bone is its ability to detect and remodel areas where damage has accumulated through prolonged use. This process, believed vital to the long-term health of bone, is considered to be initiated and orchestrated by osteocytes, cells within the bone matrix. It is therefore surprising that most extant fishes (neoteleosts) lack osteocytes, suggesting their bones are not constantly repaired, although many species exhibit long lives and high activity levels, factors that should induce considerable fatigue damage with time. Here, we show evidence for active and intense remodeling occurring in the anosteocytic, elongated rostral bones of billfishes (e.g., swordfish, marlins). Despite lacking osteocytes, this tissue exhibits a striking resemblance to the mature bone of large mammals, bearing structural features (overlapping secondary osteons) indicating intensive tissue repair, particularly in areas where high loads are expected. Billfish osteons are an order of magnitude smaller in diameter than mammalian osteons, however, implying that the nature of damage in this bone may be different. Whereas billfish bone material is as stiff as mammalian bone (unlike the bone of other fishes), it is able to withstand much greater strains (relative deformations) before failing. Our data show that fish bone can exhibit far more complex structure and physiology than previously known, and is apparently capable of localized repair even without the osteocytes believed essential for this process. These findings challenge the unique and primary role of osteocytes in bone remodeling, a basic tenet of bone biology, raising the possibility of an alternative mechanism driving this process.

KEYWORDS:

anosteocytic bone; bone toughness; damage-driven remodeling; fish skeleton; osteon

PMID:
25331870
PMCID:
PMC4234560
DOI:
10.1073/pnas.1412372111
[Indexed for MEDLINE]
Free PMC Article

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