Sonic Hedgehog-activated engineered blood vessels enhance bone tissue formation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 12, 2012, Pages 4413-4418

  Rivron, Nicolas C ^a   Raiss, Christian C ^a   Liu, Jun ^a   Nandakumar, Anandkumar ^a   Sticht, Carsten ^b   Gretz, Norbert ^b   Truckenmul̈ler, Roman ^a   Rouwkema, Jeroen ^a   Van Blitterswijk, Clemens A ^a  

^a UNIVERSITY OF TWENTE   (Netherlands)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Angiogenesis; Endochondral ossification; Regenerative medicine; Tissue engineering

Indexed keywords

AGGRECAN; COLLAGEN TYPE 1; COLLAGEN TYPE 2; SONIC HEDGEHOG PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTIFICIAL ORGAN; BLOOD VESSEL; BONE REMODELING; BONE TISSUE; CONTROLLED STUDY; ENDOTHELIUM; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OSSIFICATION; PERFUSION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TISSUE ENGINEERING; TISSUE REGENERATION;

ANIMALS; BLOOD VESSEL PROSTHESIS; BONE AND BONES; BONE MARROW CELLS; CELL DIFFERENTIATION; EXTRACELLULAR MATRIX; HEDGEHOG PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; NEOVASCULARIZATION, PATHOLOGIC; OSTEOGENESIS; REGENERATIVE MEDICINE; TIME FACTORS; TISSUE ENGINEERING;

ERINACEIDAE;

EID: 84863380653     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1117627109     Document Type: Article

References (36)

1. Shapiro F (2008) Bone development and its relation to fracture repair. The role of mesenchymal osteoblasts and surface osteoblasts. Eur Cell Mater 15:53-76.
2. Glowacki J (1998) Angiogenesis in fracture repair. Clin Orthop Relat Res 355S:S82-89.
3. Siddappa R, et al. (2008) cAMP/PKA pathway activation in human mesenchymal stem cells in vitro results in robust bone formation in vivo. Proc Natl Acad Sci USA 105:7281-7286. (Pubitemid 351754469)
4. Scotti C, et al. (2010) Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc Natl Acad Sci USA 107:7251-7256.
5. Rivron NC, Liu JJ, Rouwkema J, de Boer J, van Blitterswijk CA (2008) Engineering vascularised tissues in vitro. Eur Cell Mater 15:27-40. (Pubitemid 351955730)
6. Levenberg S, et al. (2005) Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23:879-884. (Pubitemid 43093132)
7. Au P, Tam J, Fukumura D, Jain RK (2008) Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 111:4551-4558.
8. Koike N, et al. (2004) Tissue engineering: Creation of long-lasting blood vessels. Nature 428:138-139. (Pubitemid 38374298)
9. Koffler J, et al. (2011) Improved vascular organization enhances functional integration of engineered skeletal muscle grafts. Proc Natl Acad Sci USA 108(36):14789-14794.
10. Murakami S, Noda M (2000) Expression of Indian hedgehog during fracture healing in adult rat femora. Calcif Tissue Int 66:272-276. (Pubitemid 30151800)
11. Pola R, et al. (2001) The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors. Nat Med 7:706-711. (Pubitemid 32588027)
12. Pola R, et al. (2003) Postnatal recapitulation of embryonic hedgehog pathway in response to skeletal muscle ischemia. Circulation 108:479-485. (Pubitemid 36935543)
13. Le H, et al. (2008) Hedgehog signaling is essential for normal wound healing. Wound Repair Regen 16:768-773.
14. Kusano KF, et al. (2005) Sonic hedgehog myocardial gene therapy: tissue repair through transient reconstitution of embryonic signaling. Nat Med 11:1197-1204. (Pubitemid 43093667)
15. Emans PJ, et al. (2007) A novel in vivo model to study endochondral bone formation; HIF-1alpha activation and BMP expression. Bone 40:409-418. (Pubitemid 46054546)
16. Vokes SA, et al. (2004) Hedgehog signaling is essential for endothelial tube formation during vasculogenesis. Development 131:4371-4380. (Pubitemid 39276203)
17. Straface G, et al. (2008) Sonic Hedgehog regulates angiogenesis and myogenesis during post-natal skeletal muscle regeneration. J Cell Mol Med 13:2424-2435.
18. Asai J, et al. (2006) Topical sonic hedgehog gene therapy accelerates wound healing in diabetes by enhancing endothelial progenitor cell-mediated microvascular remodeling. Circulation 113:2413-2424. (Pubitemid 43948049)
19. Rouwkema J, de Boer J, Van Blitterswijk CA (2006) Endothelial cells assemble into a 3-dimensional prevascular network in a bone tissue engineering construct. Tissue Eng 12:2685-2693. (Pubitemid 46141291)
20. Rouwkema J, Westerweel PE, de Boer J, Verhaar MC, van Blitterswijk CA (2009) The use of endothelial progenitor cells for prevascularized bone tissue engineering. Tissue Eng Part A 15:2015-2027.
21. Taipale J, et al. (2000) Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406:1005-1009.
22. Iruela-Arispe ML, Davis GE (2009) Cellular and molecular mechanisms of vascular lumen formation. Dev Cell 16:222-231.
23. Dessaud E, et al. (2007) Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 450:717-720. (Pubitemid 350207693)
24. Sinha S, Chen JK (2006) Purmorphamine activates the Hedgehog pathway by targeting Smoothened. Nat Chem Biol 2:29-30.
25. Muller G, Behrens J, Nussbaumer U, Bohlen P, Birchmeier W (1987) Inhibitory action of transforming growth factor beta on endothelial cells. Proc Natl Acad Sci USA 84:5600-5604.
26. Korff T, Kimmina S, Martiny-Baron G, Augustin HG (2001) Blood vessel maturation in a 3-dimensional spheroidal coculture model: direct contact with smooth muscle cells regulates endothelial cell quiescence and abrogates VEGF responsiveness. FASEB J 15:447-457. (Pubitemid 32141436)
27. Yuan H, et al. (1998) Osteoinduction by calcium phosphate biomaterials. J Mater Sci Mater Med 9:723-726. (Pubitemid 29043277)
28. Armulik A, Abramsson A, Betsholtz C (2005) Endothelial/pericyte interactions. Circ Res 97:512-523. (Pubitemid 41361741)
29. Chan CK, et al. (2009) Endochondral ossification is required for haematopoietic stem-cell niche formation. Nature 457:490-494.
30. Meijer GJ, de Bruijn JD, Koole R, van Blitterswijk CA (2007) Cell-based bone tissue engineering. PLoS Med 4:e9.
31. Rouwkema J, Rivron NC, van Blitterswijk CA (2008) Vascularization in tissue engineering. Trends Biotechnol 26:434-441.
32. Chinchilla P, Xiao L, Kazanietz MG, Natalia AN, Riobo GM (2010) Hedgehog proteins activate pro-angiogenic responses in endothelial cells through non-canonical signaling pathways. Cell Cycle 9:570-579.
33. Zelzer E, et al. (2004) VEGFA is necessary for chondrocyte survival during bone development. Development 131:2161-2171. (Pubitemid 38702047)
34. Wan C, et al. (2010) Role of HIF-1alpha in skeletal development. Ann NY Acad Sci 1192:322-326.
35. Villars F, et al. (2002) Effect of HUVEC on human osteoprogenitor cell differentiation needs heterotypic gap junction communication. Am J Physiol Cell Physiol 282: C775-785. (Pubitemid 34663140)
36. Yuan H, van Blitterswijk CA, de Groot K, de Bruijn JD (2006) Cross-species comparison of ectopic bone formation in biphasic calcium phosphate (BCP) and hydroxyapatite (HA) scaffolds. Tissue Eng 12:1607-1615. (Pubitemid 44174794)