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*Osteoporosis
Endocrine Reviews 21 (2): 115-137
Copyright © 2000 by The Endocrine Society

Birth and Death of Bone Cells: Basic Regulatory Mechanisms and Implications for the Pathogenesis and Treatment of Osteoporosis1

Stavros C. Manolagas

Division of Endocrinology & Metabolism, Center for Osteoporosis & Metabolic Bone Diseases, University of Arkansas for Medical Sciences, and the Central Arkansas Veterans Healthcare System, Little Rock, Arkansas 72205, USA

The adult skeleton regenerates by temporary cellular structures that comprise teams of juxtaposed osteoclasts and osteoblasts and replace periodically old bone with new. A considerable body of evidence accumulated during the last decade has shown that the rate of genesis of these two highly specialized cell types, as well as the prevalence of their apoptosis, is essential for the maintenance of bone homeostasis; and that common metabolic bone disorders such as osteoporosis result largely from a derangement in the birth or death of these cells. The purpose of this article is 3-fold: 1) to review the role and the molecular mechanism of action of regulatory molecules, such as cytokines and hormones, in osteoclast and osteoblast birth and apoptosis; 2) to review the evidence for the contribution of changes in bone cell birth or death to the pathogenesis of the most common forms of osteoporosis; and 3) to highlight the implications of bone cell birth and death for a better understanding of the mechanism of action and efficacy of present and future pharmacotherapeutic agents for osteoporosis.




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The Wnt Antagonist Secreted Frizzled-Related Protein-1 Is a Negative Regulator of Trabecular Bone Formation in Adult Mice
Mol. Endocrinol., May 1, 2004; 18(5): 1222 - 1237.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
M. Usui, Y. Yoshida, K. Tsuji, K. Oikawa, K. Miyazono, I. Ishikawa, T. Yamamoto, A. Nifuji, and M. Noda
Tob deficiency superenhances osteoblastic activity after ovariectomy to block estrogen deficiency-induced osteoporosis
PNAS, April 27, 2004; 101(17): 6653 - 6658.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
R. S. Weinstein, D. Jia, C. C. Powers, S. A. Stewart, R. L. Jilka, A. M. Parfitt, and S. C. Manolagas
The Skeletal Effects of Glucocorticoid Excess Override Those of Orchidectomy in Mice
Endocrinology, April 1, 2004; 145(4): 1980 - 1987.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
S. Yaccoby, M. J. Wezeman, A. Henderson, M. Cottler-Fox, Q. Yi, B. Barlogie, and J. Epstein
Cancer and the Microenvironment: Myeloma-Osteoclast Interactions as a Model
Cancer Res., March 15, 2004; 64(6): 2016 - 2023.
[Abstract] [Full Text] [PDF]


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Journals of Gerontology Series A: Biological Sciences and Medical SciencesHome page
D. Karasik, M. T. Hannan, L. A. Cupples, D. T. Felson, and D. P. Kiel
Genetic Contribution to Biological Aging: The Framingham Study
J. Gerontol. A Biol. Sci. Med. Sci., March 1, 2004; 59(3): B218 - B226.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
S. Evio, A. Tiitinen, K. Laitinen, O. Ylikorkala, and M. J. Valimaki
Effects of Alendronate and Hormone Replacement Therapy, Alone and in Combination, on Bone Mass and Markers of Bone Turnover in Elderly Women with Osteoporosis
J. Clin. Endocrinol. Metab., February 1, 2004; 89(2): 626 - 631.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
E. Hay, J. Lemonnier, O. Fromigue, H. Guenou, and P. J. Marie
Bone Morphogenetic Protein Receptor IB Signaling Mediates Apoptosis Independently of Differentiation in Osteoblastic Cells
J. Biol. Chem., January 16, 2004; 279(3): 1650 - 1658.
[Abstract] [Full Text] [PDF]


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NEJMHome page
F. E. Vegni, C. Corradini, G. Privitera, T. Sugiyama, H. Tanaka, S. Kawai, P. D. Miller, K. E. Fuller, D. M. Black, J. Bilezikian, et al.
Effects of Parathyroid Hormone and Alendronate Alone or in Combination in Osteoporosis
N. Engl. J. Med., January 8, 2004; 350(2): 189 - 192.
[Full Text] [PDF]


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Am. J. Clin. Nutr.Home page
G. Barera, S. Beccio, M. C. Proverbio, and S. Mora
Longitudinal changes in bone metabolism and bone mineral content in children with celiac disease during consumption of a gluten-free diet
Am. J. Clinical Nutrition, January 1, 2004; 79(1): 148 - 154.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
X. Wu, M. A. McKenna, X. Feng, T. R. Nagy, and J. M. McDonald
Osteoclast Apoptosis: The Role of Fas in Vivo and in Vitro
Endocrinology, December 1, 2003; 144(12): 5545 - 5555.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
J. N. VanHouten and J. J. Wysolmerski
Low Estrogen and High Parathyroid Hormone-Related Peptide Levels Contribute to Accelerated Bone Resorption and Bone Loss in Lactating Mice
Endocrinology, December 1, 2003; 144(12): 5521 - 5529.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
S. Nakayamada, Y. Okada, K. Saito, M. Tamura, and Y. Tanaka
{beta}1 Integrin/Focal Adhesion Kinase-mediated Signaling Induces Intercellular Adhesion Molecule 1 and Receptor Activator of Nuclear Factor {kappa}B Ligand on Osteoblasts and Osteoclast Maturation
J. Biol. Chem., November 14, 2003; 278(46): 45368 - 45374.
[Abstract] [Full Text] [PDF]


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J. Appl. Physiol.Home page
E. Seeman
Invited Review: Pathogenesis of osteoporosis
J Appl Physiol, November 1, 2003; 95(5): 2142 - 2151.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
G. Passeri, G. Pini, L. Troiano, R. Vescovini, P. Sansoni, M. Passeri, P. Gueresi, R. Delsignore, M. Pedrazzoni, and C. Franceschi
Low Vitamin D Status, High Bone Turnover, and Bone Fractures in Centenarians
J. Clin. Endocrinol. Metab., November 1, 2003; 88(11): 5109 - 5115.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
G. Van den Berghe, D. Van Roosbroeck, P. Vanhove, P. J. Wouters, L. De Pourcq, and R. Bouillon
Bone Turnover in Prolonged Critical Illness: Effect of Vitamin D
J. Clin. Endocrinol. Metab., October 1, 2003; 88(10): 4623 - 4632.
[Abstract] [Full Text] [PDF]


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J Child NeurolHome page
S. S. Budden and M. E. Gunness
Possible Mechanisms of Osteopenia in Rett Syndrome: Bone Histomorphometric Studies
J Child Neurol, October 1, 2003; 18(10): 698 - 702.
[Abstract] [PDF]


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EndocrinologyHome page
F. Elefteriou, S. Takeda, X. Liu, D. Armstrong, and G. Karsenty
Monosodium Glutamate-Sensitive Hypothalamic Neurons Contribute to the Control of Bone Mass
Endocrinology, September 1, 2003; 144(9): 3842 - 3847.
[Abstract] [Full Text] [PDF]


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Genes Dev.Home page
S. Kim, T. Koga, M. Isobe, B. E. Kern, T. Yokochi, Y. E. Chin, G. Karsenty, T. Taniguchi, and H. Takayanagi
Stat1 functions as a cytoplasmic attenuator of Runx2 in the transcriptional program of osteoblast differentiation
Genes & Dev., August 15, 2003; 17(16): 1979 - 1991.
[Abstract] [Full Text] [PDF]


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J. Appl. Physiol.Home page
N. A. McHugh, H. M. Vercesi, R. W. Egan, and J. A. Hey
Receptor activator of NF-{kappa}B ligand arrests bone growth and promotes cortical bone resorption in growing rats
J Appl Physiol, August 1, 2003; 95(2): 672 - 676.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
H. Enomoto, S. Shiojiri, K. Hoshi, T. Furuichi, R. Fukuyama, C. A. Yoshida, N. Kanatani, R. Nakamura, A. Mizuno, A. Zanma, et al.
Induction of Osteoclast Differentiation by Runx2 through Receptor Activator of Nuclear Factor-{kappa}B Ligand (RANKL) and Osteoprotegerin Regulation and Partial Rescue of Osteoclastogenesis in Runx2-/- Mice by RANKL Transgene
J. Biol. Chem., June 20, 2003; 278(26): 23971 - 23977.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
A. M. Delany, I. Kalajzic, A. D. Bradshaw, E. H. Sage, and E. Canalis
Osteonectin-Null Mutation Compromises Osteoblast Formation, Maturation, and Survival
Endocrinology, June 1, 2003; 144(6): 2588 - 2596.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
S. S. Ahuja, S. Zhao, T. Bellido, L. I. Plotkin, F. Jimenez, and L. F. Bonewald
CD40 Ligand Blocks Apoptosis Induced by Tumor Necrosis Factor {alpha}, Glucocorticoids, and Etoposide in Osteoblasts and the Osteocyte-Like Cell Line Murine Long Bone Osteocyte-Y4
Endocrinology, May 1, 2003; 144(5): 1761 - 1769.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
Y. Hu, E. Chan, S. X. Wang, and B. Li
Activation of p38 Mitogen-Activated Protein Kinase Is Required for Osteoblast Differentiation
Endocrinology, May 1, 2003; 144(5): 2068 - 2074.
[Abstract] [Full Text] [PDF]


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Arch Intern MedHome page
B. H. Ascott-Evans, N. Guanabens, S. Kivinen, B. G. A. Stuckey, C. H. Magaril, K. Vandormael, B. Stych, and M. E. Melton
Alendronate Prevents Loss of Bone Density Associated With Discontinuation of Hormone Replacement Therapy: A Randomized Controlled Trial
Arch Intern Med, April 14, 2003; 163(7): 789 - 794.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
S. Cuzzocrea, E. Mazzon, L. Dugo, T. Genovese, R. Di Paola, Z. Ruggeri, E. Vegeto, A. P. Caputi, F. A. J. Van de Loo, D. Puzzolo, et al.
Inducible Nitric Oxide Synthase Mediates Bone Loss in Ovariectomized Mice
Endocrinology, March 1, 2003; 144(3): 1098 - 1107.
[Abstract] [Full Text] [PDF]


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Exp. Biol. Med.Home page
S. Yakar and C. J. Rosen
From Mouse to Man: Redefining the Role of Insulin-Like Growth Factor-I in the Acquisition of Bone Mass
Experimental Biology and Medicine, March 1, 2003; 228(3): 245 - 252.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
Y. Engelbrecht, H. de Wet, K. Horsch, C. R. Langeveldt, F. S. Hough, and P. A. Hulley
Glucocorticoids Induce Rapid Up-Regulation of Mitogen-Activated Protein Kinase Phosphatase-1 and Dephosphorylation of Extracellular Signal-Regulated Kinase and Impair Proliferation in Human and Mouse Osteoblast Cell Lines
Endocrinology, February 1, 2003; 144(2): 412 - 422.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
S. L. Ferrari, L. Ahn-Luong, P. Garnero, S. E. Humphries, and S. L. Greenspan
Two Promoter Polymorphisms Regulating Interleukin-6 Gene Expression Are Associated with Circulating Levels of C-Reactive Protein and Markers of Bone Resorption in Postmenopausal Women
J. Clin. Endocrinol. Metab., January 1, 2003; 88(1): 255 - 259.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
Y. Takeuchi, S. Watanabe, G. Ishii, S. Takeda, K. Nakayama, S. Fukumoto, Y. Kaneta, D. Inoue, T. Matsumoto, K. Harigaya, et al.
Interleukin-11 as a Stimulatory Factor for Bone Formation Prevents Bone Loss with Advancing Age in Mice
J. Biol. Chem., December 6, 2002; 277(50): 49011 - 49018.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
A. Grey, Q. Chen, K. Callon, X. Xu, I. R. Reid, and J. Cornish
The Phospholipids Sphingosine-1-Phosphate and Lysophosphatidic Acid Prevent Apoptosis in Osteoblastic Cells via a Signaling Pathway Involving Gi Proteins and Phosphatidylinositol-3 Kinase
Endocrinology, December 1, 2002; 143(12): 4755 - 4763.
[Abstract] [Full Text] [PDF]


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J. Cell Sci.Home page
J.-P. David, K. Sabapathy, O. Hoffmann, M. H. Idarraga, and E. F. Wagner
JNK1 modulates osteoclastogenesis through both c-Jun phosphorylation-dependent and -independent mechanisms
J. Cell Sci., November 15, 2002; 115(22): 4317 - 4325.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. A. Karsdal, L. Larsen, M. T. Engsig, H. Lou, M. Ferreras, A. Lochter, J.-M. Delaisse, and N. T. Foged
Matrix Metalloproteinase-dependent Activation of Latent Transforming Growth Factor-beta Controls the Conversion of Osteoblasts into Osteocytes by Blocking Osteoblast Apoptosis
J. Biol. Chem., November 8, 2002; 277(46): 44061 - 44067.
[Abstract] [Full Text] [PDF]


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ScienceHome page
S. Kousteni, J.-R. Chen, T. Bellido, L. Han, A. A. Ali, C. A. O'Brien, L. Plotkin, Q. Fu, A. T. Mancino, Y. Wen, et al.
Reversal of Bone Loss in Mice by Nongenotropic Signaling of Sex Steroids
Science, October 25, 2002; 298(5594): 843 - 846.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
B. Demiralp, H.-L. Chen, A. J. Koh, E. T. Keller, and L. K. McCauley
Anabolic Actions of Parathyroid Hormone during Bone Growth Are Dependent on c-fos
Endocrinology, October 1, 2002; 143(10): 4038 - 4047.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
B. Arko, J. Prezelj, R. Komel, A. Kocijancic, P. Hudler, and J. Marc
Sequence Variations in the Osteoprotegerin Gene Promoter in Patients with Postmenopausal Osteoporosis
J. Clin. Endocrinol. Metab., September 1, 2002; 87(9): 4080 - 4084.
[Abstract] [Full Text] [PDF]




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