Parathyroid hormone may maintain bone formation in hibernating black bears (Ursus americanus) to prevent disuse osteoporosis

Seth W. Donahue, Sarah A. Galley, Michael R. Vaughan, Patricia Patterson-Buckendahl, Laurence M. Demers, Josef L. Vance, Meghan E. McGee

Research output: Contribution to journalArticle

55 Citations (Scopus)

Abstract

Mechanical unloading of bone causes an imbalance in bone formation and resorption leading to bone loss and increased fracture risk. Black bears (Ursus americanus) are inactive for up to six months during hibernation, yet bone mineral content and strength do not decrease with disuse or aging. To test whether hibernating bears have biological mechanisms to prevent disuse osteoporosis, we measured the serum concentrations of hormones and growth factors involved in bone metabolism and correlated them with the serum concentration of a bone formation marker (osteocalcin). Serum was obtained from black bears over a 7-month duration that included periods of activity and inactivity. Both resorption and formation markers increased during hibernation, suggesting high bone turnover occurred during inactivity. However, bone formation appeared to be balanced with bone resorption. The serum concentration of parathyroid hormone (PTH) was higher in the hibernation (P=0.35) and post-hibernation (P=0.006) seasons relative to pre-hibernation levels. Serum leptin was lower (P<0.004) post-hibernation relative to pre-hibernation and hibernation periods. Insulin-like growth factor I (IGF-I) decreased (P<0.0001) during hibernation relative to pre-hibernation and reached its highest value during remobilization. There was no difference (P=0.64) in 25-OH vitamin D between the three seasons. Serum osteocalcin (bone formation marker) was significantly correlated with PTH, but not with leptin, IGF-I or 25-OH vitamin D. Osteocalcin and PTH were positively correlated when samples from all seasons were pooled and when only hibernation samples were considered, raising the possibility that the anabolic actions of PTH help maintain bone formation to prevent disuse osteoporosis. Prostaglandin E2 (PGE2) release from MC3T3 osteoblastic cells was significantly affected by treatment with bear serum from different seasons (i.e. hibernation versus active periods). The seasonal changes in PGE2 release showed trends similar to the seasonal changes in serum IGF-I. Since both PGE2 and IGF-I are associated with collagenous bone formation, it is possible that seasonal changes in a circulating factor influence IGF-I levels in vivo in bears and PGE 2 release in osteoblastic cells in vitro. The significant decrease in serum leptin following arousal from hibernation may promote bone formation during remobilization, assuming there is a similar decrease in intracerebroventricular leptin. These findings support the idea that seasonal changes in the concentration of circulating molecules help regulate bone formation activity and may be important for preventing disuse osteoporosis in bears.

Original languageEnglish (US)
Pages (from-to)1630-1638
Number of pages9
JournalJournal of Experimental Biology
Volume209
Issue number9
DOIs
StatePublished - May 1 2006

Fingerprint

Ursidae
Hibernation
Ursus americanus
parathyroid hormone
hibernation
osteoporosis
bone formation
Parathyroid Hormone
Osteogenesis
Osteoporosis
hormone
bone
serum
insulin-like growth factor I
Insulin-Like Growth Factor I
Serum
Leptin
leptin
osteocalcin
Osteocalcin

Keywords

  • Black bear
  • Bone remodeling
  • Disuse osteoporosis
  • Hibernation
  • IGF-I
  • Leptin
  • PTH
  • Ursus americanus

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Aquatic Science
  • Animal Science and Zoology
  • Molecular Biology
  • Insect Science

Cite this

Parathyroid hormone may maintain bone formation in hibernating black bears (Ursus americanus) to prevent disuse osteoporosis. / Donahue, Seth W.; Galley, Sarah A.; Vaughan, Michael R.; Patterson-Buckendahl, Patricia; Demers, Laurence M.; Vance, Josef L.; McGee, Meghan E.

In: Journal of Experimental Biology, Vol. 209, No. 9, 01.05.2006, p. 1630-1638.

Research output: Contribution to journalArticle

Donahue, Seth W. ; Galley, Sarah A. ; Vaughan, Michael R. ; Patterson-Buckendahl, Patricia ; Demers, Laurence M. ; Vance, Josef L. ; McGee, Meghan E. / Parathyroid hormone may maintain bone formation in hibernating black bears (Ursus americanus) to prevent disuse osteoporosis. In: Journal of Experimental Biology. 2006 ; Vol. 209, No. 9. pp. 1630-1638.
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