Regulation of Bone Marrow Angiogenesis by Osteoblasts During Bone Development and Homeostasis

Overview

Journal Front Endocrinol (Lausanne)

Specialty Endocrinology

Date 2013 Jul 13

PMID 23847596

Citations 17

Authors

Ernestina Schipani

Collen Wu

Erinn B Rankin

Amato J Giaccia

Affiliations

Soon will be listed here.

Abstract

Bone marrow is a highly heterogeneous and vascularized tissue. The various cell types populating the bone marrow extensively communicate with each other, and cell-to-cell cross talk is likely to be essential for proper bone development and homeostasis. In particular, the existence of osteogenesis and angiogenesis coupling has been recently proposed. Despite its high degree of vascularization, a gradient of oxygenation is present in the bone marrow, and the endosteal surface of cortical bone appears to be among the most hypoxic areas in the body. Oxygen (O2) is both an essential metabolic substrate and a regulatory signal that is in charge of a specific genetic program. An important component of this program is the family of transcription factors known as hypoxia-inducible factors (HIFs). In this Perspective, we will summarize our current knowledge about the role of the HIF signaling pathway in controlling bone development and homeostasis, and especially in regulating the crosstalk between osteoblasts, progenitor cells, and bone marrow blood vessels.

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References

Le Douarin N, Houssaint E, Jotereau F, Belo M . Origin of hemopoietic stem cells in embryonic bursa of Fabricius and bone marrow studied through interspecific chimeras. Proc Natl Acad Sci U S A. 1975; 72(7):2701-5. PMC: 432838. DOI: 10.1073/pnas.72.7.2701. View

Robinson C, Stringer S . The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J Cell Sci. 2001; 114(Pt 5):853-65. DOI: 10.1242/jcs.114.5.853. View

Kaelin Jr W . The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat Rev Cancer. 2008; 8(11):865-73. DOI: 10.1038/nrc2502. View

Semenza G . Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003; 3(10):721-32. DOI: 10.1038/nrc1187. View

Calvi L, Adams G, Weibrecht K, Weber J, Olson D, Knight M . Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003; 425(6960):841-6. DOI: 10.1038/nature02040. View

Kaelin Jr W . How oxygen makes its presence felt. Genes Dev. 2002; 16(12):1441-5. DOI: 10.1101/gad.1003602. View

Zhu J, Garrett R, Jung Y, Zhang Y, Kim N, Wang J . Osteoblasts support B-lymphocyte commitment and differentiation from hematopoietic stem cells. Blood. 2007; 109(9):3706-12. DOI: 10.1182/blood-2006-08-041384. View

Boyle W, Simonet W, Lacey D . Osteoclast differentiation and activation. Nature. 2003; 423(6937):337-42. DOI: 10.1038/nature01658. View

Winkler I, Barbier V, Wadley R, Zannettino A, Williams S, Levesque J . Positioning of bone marrow hematopoietic and stromal cells relative to blood flow in vivo: serially reconstituting hematopoietic stem cells reside in distinct nonperfused niches. Blood. 2010; 116(3):375-85. DOI: 10.1182/blood-2009-07-233437. View

10.

Chow D, Wenning L, Miller W, Papoutsakis E . Modeling pO(2) distributions in the bone marrow hematopoietic compartment. I. Krogh's model. Biophys J. 2001; 81(2):675-84. PMC: 1301544. DOI: 10.1016/S0006-3495(01)75732-3. View

11.

Gerber H, Malik A, Solar G, Sherman D, Liang X, Meng G . VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature. 2002; 417(6892):954-8. DOI: 10.1038/nature00821. View

12.

Maxwell P, Wiesener M, Chang G, Clifford S, Vaux E, Cockman M . The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature. 1999; 399(6733):271-5. DOI: 10.1038/20459. View

13.

Wang V, Davis D, Haque M, Huang L, Yarchoan R . Differential gene up-regulation by hypoxia-inducible factor-1alpha and hypoxia-inducible factor-2alpha in HEK293T cells. Cancer Res. 2005; 65(8):3299-306. DOI: 10.1158/0008-5472.CAN-04-4130. View

14.

Medici D, Shore E, Lounev V, Kaplan F, Kalluri R, Olsen B . Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med. 2010; 16(12):1400-6. PMC: 3209716. DOI: 10.1038/nm.2252. View

15.

Maes C, Carmeliet G, Schipani E . Hypoxia-driven pathways in bone development, regeneration and disease. Nat Rev Rheumatol. 2012; 8(6):358-66. DOI: 10.1038/nrrheum.2012.36. View

16.

Jogi A, Ora I, Nilsson H, Lindeheim A, Makino Y, Poellinger L . Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype. Proc Natl Acad Sci U S A. 2002; 99(10):7021-6. PMC: 124521. DOI: 10.1073/pnas.102660199. View

17.

Taichman R, Emerson S . Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med. 1994; 179(5):1677-82. PMC: 2191506. DOI: 10.1084/jem.179.5.1677. View

18.

Shively S, Beltaifa S, Gehrs B, Duong H, Smith J, Edwards N . Protracted haemangioblastic proliferation and differentiation in von Hippel-Lindau disease. J Pathol. 2008; 216(4):514-20. PMC: 4762050. DOI: 10.1002/path.2435. View

19.

Taichman R, Reilly M, Emerson S . Human osteoblasts support human hematopoietic progenitor cells in vitro bone marrow cultures. Blood. 1996; 87(2):518-24. View

20.

Maes C, Goossens S, Bartunkova S, Drogat B, Coenegrachts L, Stockmans I . Increased skeletal VEGF enhances beta-catenin activity and results in excessively ossified bones. EMBO J. 2009; 29(2):424-41. PMC: 2824461. DOI: 10.1038/emboj.2009.361. View