Role of Angiocrine Signals in Bone Development, Homeostasis and Disease

Overview

Journal Open Biol

Specialties Biology
Cell Biology
Molecular Biology

Date 2019 Oct 3

PMID 31575330

Citations 30

Authors

Unnikrishnan Sivan

Jessica De Angelis

Anjali P Kusumbe

Affiliations

Soon will be listed here.

Abstract

Skeletal vasculature plays a central role in the maintenance of microenvironments for osteogenesis and haematopoiesis. In addition to supplying oxygen and nutrients, vasculature provides a number of inductive factors termed as angiocrine signals. Blood vessels drive recruitment of osteoblast precursors and bone formation during development. Angiogenesis is indispensable for bone repair and regeneration. Dysregulation of the angiocrine crosstalk is a hallmark of ageing and pathobiological conditions in the skeletal system. The skeletal vascular bed is complex, heterogeneous and characterized by distinct capillary subtypes (type H and type L), which exhibit differential expression of angiocrine factors. Furthermore, distinct blood vessel subtypes with differential angiocrine profiles differentially regulate osteogenesis and haematopoiesis, and drive disease states in the skeletal system. This review provides an overview of the role of angiocrine signals in bone during homeostasis and disease.

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References

Dai J, Rabie A . VEGF: an essential mediator of both angiogenesis and endochondral ossification. J Dent Res. 2007; 86(10):937-50. DOI: 10.1177/154405910708601006. View

Kang S, Kumanogoh A . Semaphorins in bone development, homeostasis, and disease. Semin Cell Dev Biol. 2012; 24(3):163-71. DOI: 10.1016/j.semcdb.2012.09.008. View

Serini G, Valdembri D, Zanivan S, Morterra G, Burkhardt C, Caccavari F . Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature. 2003; 424(6947):391-7. DOI: 10.1038/nature01784. View

Ding B, Nolan D, Guo P, Babazadeh A, Cao Z, Rosenwaks Z . Endothelial-derived angiocrine signals induce and sustain regenerative lung alveolarization. Cell. 2011; 147(3):539-53. PMC: 3228268. DOI: 10.1016/j.cell.2011.10.003. View

Romeo S, Alawi K, Rodrigues J, Singh A, Kusumbe A, Ramasamy S . Endothelial proteolytic activity and interaction with non-resorbing osteoclasts mediate bone elongation. Nat Cell Biol. 2019; 21(4):430-441. DOI: 10.1038/s41556-019-0304-7. View

Matsumoto K, Yoshitomi H, Rossant J, Zaret K . Liver organogenesis promoted by endothelial cells prior to vascular function. Science. 2001; 294(5542):559-63. DOI: 10.1126/science.1063889. View

Wang L, Zhou F, Zhang P, Wang H, Qu Z, Jia P . Human type H vessels are a sensitive biomarker of bone mass. Cell Death Dis. 2017; 8(5):e2760. PMC: 5520742. DOI: 10.1038/cddis.2017.36. View

Chen J, Miyanishi M, Wang S, Yamazaki S, Sinha R, Kao K . Hoxb5 marks long-term haematopoietic stem cells and reveals a homogenous perivascular niche. Nature. 2016; 530(7589):223-7. PMC: 4854608. DOI: 10.1038/nature16943. View

Suva L, Gaddy D, Perrien D, Thomas R, Findlay D . Regulation of bone mass by mechanical loading: microarchitecture and genetics. Curr Osteoporos Rep. 2005; 3(2):46-51. DOI: 10.1007/s11914-005-0003-0. View

10.

Yuan K, Shamskhou E, Orcholski M, Nathan A, Reddy S, Honda H . Loss of Endothelium-Derived Wnt5a Is Associated With Reduced Pericyte Recruitment and Small Vessel Loss in Pulmonary Arterial Hypertension. Circulation. 2018; 139(14):1710-1724. PMC: 6443444. DOI: 10.1161/CIRCULATIONAHA.118.037642. View

11.

Kriegsmann J, Keyszer G, Geiler T, Lagoo A, Gay R, Gay S . Expression of E-selectin messenger RNA and protein in rheumatoid arthritis. Arthritis Rheum. 1995; 38(6):750-4. DOI: 10.1002/art.1780380606. View

12.

Street J, Bao M, deGuzman L, Bunting S, Peale Jr F, Ferrara N . Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci U S A. 2002; 99(15):9656-61. PMC: 124965. DOI: 10.1073/pnas.152324099. View

13.

Kusumbe A . Vascular niches for disseminated tumour cells in bone. J Bone Oncol. 2016; 5(3):112-116. PMC: 5063228. DOI: 10.1016/j.jbo.2016.04.003. View

14.

Veeriah V, Zanniti A, Paone R, Chatterjee S, Rucci N, Teti A . Interleukin-1β, lipocalin 2 and nitric oxide synthase 2 are mechano-responsive mediators of mouse and human endothelial cell-osteoblast crosstalk. Sci Rep. 2016; 6:29880. PMC: 4949438. DOI: 10.1038/srep29880. View

15.

Kusumbe A, Ramasamy S, Starsichova A, Adams R . Sample preparation for high-resolution 3D confocal imaging of mouse skeletal tissue. Nat Protoc. 2015; 10(12):1904-14. DOI: 10.1038/nprot.2015.125. View

16.

Cui Z, Crane J, Xie H, Jin X, Zhen G, Li C . Halofuginone attenuates osteoarthritis by inhibition of TGF-β activity and H-type vessel formation in subchondral bone. Ann Rheum Dis. 2015; 75(9):1714-21. PMC: 5013081. DOI: 10.1136/annrheumdis-2015-207923. View

17.

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

18.

Ria R, Todoerti K, Berardi S, Coluccia A, De Luisi A, Mattioli M . Gene expression profiling of bone marrow endothelial cells in patients with multiple myeloma. Clin Cancer Res. 2009; 15(17):5369-78. DOI: 10.1158/1078-0432.CCR-09-0040. View

19.

Acar M, Kocherlakota K, Murphy M, Peyer J, Oguro H, Inra C . Deep imaging of bone marrow shows non-dividing stem cells are mainly perisinusoidal. Nature. 2015; 526(7571):126-30. PMC: 4850557. DOI: 10.1038/nature15250. View

20.

Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett N . Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell. 2002; 109(5):625-37. PMC: 2826110. DOI: 10.1016/s0092-8674(02)00754-7. View