The role of vasculature in bone development, regeneration and proper systemic functioning

Dai J, Rabie BM (2007) VEGF: an essential mediator of both angiogenesis and endochondral ossification. J Dent Res 86(10):937–950

Hankenson KD, Dishowitz M, Gray C, Schenker M (2011) Angiogenesis in bone regeneration. Injury 42(6):556–561

Huang B, Wang W, Li Q, Wang Z, Yan B, Zhang Z, Wang L, Huang M, Jia C, Lu J, Liu S, Chen H, Li M, Cai D, Jiang Y, Jin D, Bai X (2016) Osteoblasts secrete Cxcl9 to regulate angiogenesis in bone. Nat Commun 7:13885

Tomlinson RE, Silva MJ (2013) Skeletal blood flow in bone repair and maintenance. Bone Res 1(4):311–322

Niedźwiedzki T, Filipowska J (2015) Bone remodeling in the context of cellular and systemic regulation: the role of osteocytes and the nervous system. J Mol Endocrinol 55(2):R23–R36

Brandi ML, Collin-Osdoby P (2006) Vascular biology and the skeleton. J Bone Miner Res 21(2):183–192

Percival CJ (2013) The influence of angiogenesis on craniofacial development and evolution, Ph.D. Thesis, Penn State

Percival CJ, Richtsmeier JT (2014) Angiogenesis and intramembranous osteogenesis. Dev Dyn 242(8):909–922

Chan WP, Liu YJ, Huang GS, Lin MF, Huang S, Chang YC, Jiang CC (2011) Relationship of idiopathic osteonecrosis of the femoral head to perfusion changes in the proximal femur by dynamic contrast-enhanced MRI. AJR Am J Roentgenol 196(3):637–643

Hayashi S, Kim JH, Hwang SE, Shibata S, Fujimiya M, Murakami G, Cho BH (2014) Interface between intramembranous and endochondral ossification in human foetuses. Folia Morphol (Warsz) 73(2):199–205

Berendsen AD, Olsen BR (2015) Bone development. Bone 80:14–18

Liu Y, Olsen BR (2014) Distinct VEGF functions during bone development and homeostasis. Arch Immunol Ther Exp (Warsz) 62(5):363–368

Hu K, Olsen BR (2016) Osteoblast-derived VEGF regulates osteoblast differentiation and bone formation during bone repair. J Clin Investig 126(2):509–526

Maes C, Carmeliet P, Moermans K, Stockmans I, Smets N, Collen D, Carmeliet G (2002) Impaired angiogenesis and endochondral bone formation in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Mech Dev 111(1–2):61–73

Azimi-Nezhad M (2014) Vascular endothelial growth factor from embryonic status to cardiovascular pathology. Rep Biochem Mol Biol 2(2):59–69

Maes C, Stockmans I, Moermans K, Van Looveren R, Smets N, Carmeliet P, Carmeliet G (2004) Soluble VEGF isoforms are essential for establishing epiphyseal vascularization and regulating chondrocyte development and survival. J Clin Investig 113(2):188–199

Maes C, Goossens S, Bartunkova S, Drogat B, Coenegrachts L, Stockmans I, Haigh JJ (2010) Increased skeletal VEGF enhances beta-catenin activity and results in excessively ossified bones. EMBO J 29(2):424–441

Ben Shoham A, Rot C, Stern T, Krief S, Akiva A, Dadosh T, Zelzer E (2016) Deposition of collagen type I onto skeletal endothelium reveals a new role for blood vessels in regulating bone morphology. Development 143(21):3933–3943

Skawina A, Litwin JA, Gorczyca J, Miodoński A (1994) Blood vessels in epiphyseal cartilage of human fetal femoral bone: a scanning electron microscopic study of corrosion casts. Anat Embryol (Berl) 189(5):457–462

Thompson TJ, Owens PD, Wilson DJ (1989) Intramembranous osteogenesis and angiogenesis in the chick embryo. J Anat 166:55–65

Maes C, Kobayashi T, Selig MK, Torrekens S, Sanford I, Mackem S, Kronenberg HM (2010) Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell 19(2):329–344

Patan S (2004) Vasculogenesis and angiogenesis. Cancer Treat Res 117:3–32

Patan S (2000) Vasculogenesis and angiogenesis as mechanisms of vascular network formation, growth and remodeling. J Neuro Oncol 50(1–2):1–15

Kanczler JM, Oreffo RO (2008) Osteogenesis and angiogenesis: the potential for engineering bone. Eur Cell Mater 15:100–114

Portal-Núñez S, Lozano D, Esbrit P (2012) Role of angiogenesis on bone formation. Histol Histopathol 27(5):559–566

Breier G, Albrecht U, Sterrer S, Risau W (1992) Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 114(2):521–532

Wiszniak S, Mackenzie FE, Anderson P, Kabbara S, Ruhrberg C, Schwarz Q (2015) Neural crest cell-derived VEGF promotes embryonic jaw extension. Proc Natl Acad Sci USA 112(19):6086–6091

Trueta J, Harrison H (1953) The normal vascular anatomy of the femoral head in adult man. J Bone Jt Surg Br 35–B(3):442–461

Trueta J, Morgan JD (1960) The vascular contribution to osteogenesis. I. Studies by the injection method. J Bone Jt Surg Br 42–B:97–109

Brookes M (1963) Cortical vascularization and growth in foetal tubular bones. J Anat 97:597–609

Skawina A (1982) Nutrient foramina in femoral, tibial and fibular bones in human fetuses. Folia Morphol (Warsz) 41(4):469–481

Skawina A (1986) Cortical vascularization of the femoral, tibial and fibular bones during prenatal development. Folia Morphol (Warsz) 45(4):290–295

Skawina A, Litwin JA, Gorczyca J, Miodoński AJ (1997) The architecture of internal blood vessels in human fetal vertebral bodies. J Anat 191:259–267

Georgia R, Albu I, Sicoe M, Georoceanu M (1982) Comparative aspects of the density and diameter of Haversian canals in the diaphyseal compact bone of man and dog. Morphol Embryol (Bucur) 28(1):11–14

Brookes M, Elkin AC, Harrison RG, Heald C (1961) A new concept of capillary circulation in bone cortex: some clinical applications. Lancet 277(7186):1078–1081

Shin KJ, Kim JN, Lee SH, Paik DJ, Song WC, Koh KS, Gil YC (2016) Arterial supply and anastomotic pattern of the infraspinous fossa focusing on the surgical significance. J Plast Reconstr Aesthet Surg 69(4):512–518

Trias A, Fery A (1979) Cortical circulation of long bones. J Bone Jt Surg Am 61(7):1052–1059

Aharinejad S, Marks SC Jr, Böck P, MacKay CA, Larson EK, Tahamtani A, Mason-Savas A, Firbas W (1995) Microvascular pattern in the metaphysis during bone growth. Anat Rec 242(1):111–122

Kobayashi S, Mwaka ES, Baba H, Takeno K, Miyazaki T, Matsuo H, Meir A (2010) Microvascular system of the lumbar dorsal root ganglia in rats. Part I: a 3D analysis with scanning electron microscopy of vascular corrosion casts. J Neurosurg Spine 12(2):197–202

Yang M, Yang L (2012) A simple method to detect human intraosseous vascular structures: using the calcaneus as an example. Surg Radiol Anat 34(9):839–846

Shenk R (1998) Biology of fracture repair. In: Brown BD, Jupiter JB, Levine AM et al (eds) Skeletal trauma: fractures, dislocations, ligamentous bone injuries, 2nd edn. W. B. Saunders, Philadelphia

Pazzaglia UE, Congiu T, Raspanti M, Ranchetti F, Quacci D (2009) Anatomy of the intracortical canal system: scanning electron microscopy study in rabbit femur. Clin Orthop Relat Res 467(9):2446–2456

Brookes M, Revell WJ (eds) (1998) Blood supply of flat bones. In: Blood supply of bone. Springer, London

Flanagan D (2003) Important arterial supply of the mandible, control of an arterial hemorrhage, and report of a hemorrhagic incident. J Oral Implantol 29(4):165–173

Pannarale L, Morini S, D’Ubaldo E, Gaudio E, Marinozzi G (1997) SEM corrosion-casts study of the microcirculation of the flat bones in the rat. Anat Rec 247(4):462–471

Ding L, Morrison S (2013) Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 495(7440):231–235

Acar M, Kocherlakota KS, Murphy MM, Peyer JG, Oguro H, Inra CN, Jaiyeola C, Zhao Z, Luby-Phelps K, Morrison SJ (2015) Deep imaging of bone marrow shows non-dividing stem cells are mainly perisinusoidal. Nature 526(7571):126–130

Kunisaki Y, Bruns I, Scheiermann C, Ahmed J, Pinho S, Zhang D, Mizoguchi T, Wei Q, Lucas D, Ito K, Mar JC, Bergman A, Frenette P (2013) Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502(7473):637–643

Kusumbe AP, Ramasamy SK, Itkin T, Mäe MA, Langen UH, Betsholtz C, Lapidot T, Adams RH (2016) Age-dependent modulation of vascular niches for haematopoietic stem cells. Nature 532(7599):380–384

Itkin T, Gur-Cohen S, Spencer JA, Schajnovitz A, Ramasamy SK, Kusumbe AP, Ledergor G, Jung Y, Milo I, Poulos MG, Kalinkovich A, Ludin A, Kollet O, Shakhar G, Butler JM, Rafii S, Adams RH, Scadden DT, Lin CP, Lapidot T (2016) Distinct bone marrow blood vessels differentially regulate haematopoiesis. Nature 532(7599):323–328

Kusumbe AP, Ramasamy SK, Adams RH (2014) Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature 507(7492):323–328

Ramasamy SK, Kusumbe AP, Wang L, Adams RH (2014) Endothelial Notch activity promotes angiogenesis and osteogenesis in bone. Nature 507(7492):376–380

Maes C, Clemens TL (2014) Angiogenic–osteogenic coupling: the endothelial perspective. BoneKEy Rep 3:578

Eman RM, Meijer HA, Oner FC, Dhert WJ, Alblas J (2016) Establishment of an early vascular network promotes the formation of ectopic bone. Tissue Eng Part A 22(3–4):253–262

Claesson-Welsh L (2016) VEGF receptor signal transduction—a brief update. Vasc Pharmacol 86:14–17. doi: 10.1016/j.vph.2016.05.011

Schipani E, Maes C, Carmeliet G, Semenza GL (2009) Perspective regulation of osteogenesis-angiogenesis coupling by HIFs and VEGF. J Bone Miner Res 2424(8):1347–1353

Cui M, Kanemoto S, Cui X, Kaneko M, Asada R, Matsuhisa K, Imaizumi K (2015) OASIS modulates hypoxia pathway activity to regulate bone angiogenesis. Sci Rep 5:16455

Kaushik AP, Das A, Cui Q (2012) Osteonecrosis of the femoral head: an update in year 2012. World J Orthop 3(5):49–57

Pouya F, Kerachian M (2015) Avascular necrosis of the femoral head: are any genes involved? Arch Bone Jt Surg 3(3):149–155

Feng Y, Yang SH, Xiao BJ, Xu WH, Ye SN, Xia T, Liao YF (2010) Decreased in the number and function of circulation endothelial progenitor cells in patients with avascular necrosis of the femoral head. Bone 46(1):32–40

Asahara T, Murohara T, Sullivan A, Silver M, Van R, Asahara T, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275(5302):964–967

Lee DY, Cho TJ, Kim JA, Lee HR, Yoo WJ, Chung CY, Choi IH (2008) Mobilization of endothelial progenitor cells in fracture healing and distraction osteogenesis. Bone 42(5):932–941

Matsumoto T, Mifune Y, Kawamoto A, Kuroda R, Shoji T, Iwasaki H, Asahara T (2008) Fracture induced mobilization and incorporation of bone marrow-derived endothelial progenitor cells for bone healing. J Cell Physiol 215(1):234–242

Zhao Q, Shen X, Zhang W, Zhu G, Qi J, Deng L (2012) Mice with increased angiogenesis and osteogenesis due to conditional activation of HIF pathway in osteoblasts are protected from ovariectomy induced bone loss. Bone 50(3):763–770

Liu X, Tu Y, Zhang L, Qi J, Ma T, Deng L (2014) Prolyl hydroxylase inhibitors protect from the bone loss in ovariectomy rats by increasing bone vascularity. Cell Biochem Biophys 69(1):141–149

Peng J, Hui K, Hao C, Peng Z, Gao QX, Jin Q, Fu DL (2016) Low bone turnover and reduced angiogenesis in streptozotocin-induced osteoporotic mice. Connect Tissue Res 57(4):277–289

Stabley JN, Prisby RD, Behnke BJ, Delp MD (2015) Type 2 diabetes alters bone and marrow blood flow and vascular control mechanisms in the ZDF rat. J Endocrinol 225(1):47–58

Oikawa A, Siragusa M, Quaini F, Katare RG, Caporali A, Buul JD, Van Madeddu P (2013) Diabetes mellitus induces bone marrow microangiopathy. Arterioscler Thromb Vasc Biol 30(3):498–508

Peng J, Qu H, Peng J, Luo TY, Lv FJ, Chen L, Cheng QF (2016) Abnormal spontaneous brain activity in type 2 diabetes with and without microangiopathy revealed by regional homogeneity. Eur J Radiol 85(3):607–615

Portal-Núñez S, Ardura JA, Lozano D, Bolívar OH, López-Herradón A, Gutiérrez-Rojas I, Proctor A, van der Eerden B, Schreuders-Koedam M, van Leeuwen J, Alcaraz MJ, Mulero F, de la Fuente M, Esbrit P (2016) Adverse effects of diabetes mellitus on the skeleton of aging mice. J Gerontol A Biol Sci Med Sci 71(3):290–299

Bandeira E, Neves AP, Costa C, Bandeira F (2012) Association between vascular calcification and osteoporosis in men with type 2 diabetes. J Clin Densitom 15(1):55–60

Yamagishi S, Nakamura N (2015) Advanced glycation end products: a molecular target for vascular complications in diabetes. Mol Med 21(suppl 1):S32–S34

Prasad M, Reriani M, Khosla S, Gössl M, Lennon R, Gulati R, Lerman A (2014) Coronary microvascular endothelial dysfunction is an independent predictor of development of osteoporosis in postmenopausal women. Vasc Health Risk Manag 10:533–538

Liu Y, Almeida M, Weinstein RS, O’Brien CA, Manolagas SC, Jilka RL (2016) Skeletal inflammation and attenuation of Wnt signaling, Wnt ligand expression and bone formation in atherosclerotic ApoE null mice. Am J Physiol Endocrinol Metab 310(9):E762–E773

Li Y, Zhang CG, Wang XH, Liu DH (2016) Progression of atherosclerosis in ApoE-knockout mice fed on a high-fat diet. Eur Rev Med Pharmacol Sci 20(18):3863–3867

Pederson WC, Person DW (2007) Long bone reconstruction with vascularized bone grafts. Orthop Clin North Am 38(1):23–35

Zhao D, Liu B, Wang B, Yang L, Xie H, Huang S, Wei X (2015) Autologous bone marrow mesenchymal stem cells associated with tantalum rod implantation and vascularized iliac grafting for the treatment of end-stage osteonecrosis of the femoral head. BioMed Res Int. doi: 10.1155/2015/240506

Oryan A, Alidadi S, Moshiri A, Maffulli N (2014) Bone regenerative medicine: classic options, novel strategies, and future directions. J Orthop Surg Res 9(1):18

Sathy BN, Mony U, Menon D, Baskaran VK, Mikos AG, Nair S (2015) Bone tissue engineering with multilayered scaffolds-Part I: an approach for vascularizing engineered constructs in vivo. Tissue Eng Part A 21(19–20):2480–2494

Wei J, Herrler T, Dai C, Liu K, Han D, Li Q (2016) Guided self-generation of vascularized neo-bone for autologous reconstruction of large mandibular defects. J Craniofac Surg 27(4):958–962

Mercado-Pagán ÁE, Stahl AM, Shanjani Y, Yang Y (2015) Vascularization in bone tissue engineering constructs. Ann Biomed Eng 43(3):718–729

Weigand A, Beier JP, Hess A, Gerber T, Arkudas A, Horch RE, Boos AM (2015) Acceleration of vascularized bone tissue-engineered constructs in a large animal model combining intrinsic and extrinsic vascularization. Tissue Eng Part A 21(9–10):1680–1694

Zhang C, Ma J, Li M, Li XH, Dang XQ, Wang KZ (2015) Repair effect of coexpression of the hVEGF and hBMP genes via an adeno-associated virus vector in a rabbit model of early steroid-induced avascular necrosis of the femoral head. Transl Res 166(3):269–280

Cao K, Huang W, An H, Jiang D, Shu Y, Han Z (2009) Deproteinized bone with VEGF gene transfer to facilitate the repair of early avascular necrosis of femoral head of rabbit. Chin J Traumatol 12(5):269–274