Characterization of adipose-derived mesenchymal stem cell combinations for vascularized bone engineering

Tissue Engineering - Part A

Volumn 19, Issue 11-12, 2013, Pages 1373-1385

  Valenzuela, Cristian D ^a   Allori, Alexander C ^a   Reformat, Derek D ^a   Sailon, Alexander M ^a   Allen, Robert J ^a   Davidson, Edward H ^a   Alikhani, Mani ^b   Bromage, Timothy G ^b   Ricci, John L ^b   Warren, Stephen M ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b NEW YORK UNIVERSITY COLLEGE OF DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; CELL CULTURE; CELL PROLIFERATION; ENDOTHELIAL CELLS; GENE EXPRESSION; SELF ASSEMBLY; STEM CELLS;

ADIPOSE DERIVED STEM CELLS; ADIPOSE-DERIVED MESENCHYMAL STEM CELLS; FUNCTIONAL CAPACITY; GENE EXPRESSION PROFILES; OSTEOBLASTIC CELLS; SPECIFIC SEQUENCES; VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULAR NETWORK;

CELL ENGINEERING;

BIOLOGICAL MARKER;

ADIPOSE TISSUE; ADOLESCENT; ADULT; ANGIOGENESIS; ARTICLE; BONE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL LINEAGE; COCULTURE; CYTOLOGY; FEMALE; HUMAN; MESENCHYMAL STROMA CELL; METABOLISM; METHODOLOGY; MICROTUBULE; MIDDLE AGED; OSTEOCYTE; PHYSIOLOGY; TISSUE ENGINEERING; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION;

ADIPOSE TISSUE; ADOLESCENT; ADULT; BIOLOGICAL MARKERS; BONE AND BONES; CELL DIFFERENTIATION; CELL LINEAGE; COCULTURE TECHNIQUES; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MESENCHYMAL STROMAL CELLS; MICROTUBULES; MIDDLE AGED; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOCYTES; OSTEOGENESIS; TISSUE ENGINEERING; YOUNG ADULT;

EID: 84876946846     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0323     Document Type: Article

References (56)

1. Cheng, M.H., Brey, E.M., Allori, A., Satterfield, W.C., Chang, D.W., Patrick, C.W., Jr., and Miller, M.J. Ovine model for engineering bone segments. Tissue Eng 11, 214, 2005.
2. Bouletreau, P.J., Warren, S.M., Spector, J.A., Steinbrech, D.S., Mehrara, B.J., and Longaker, M.T. Factors in the fracture microenvironment induce primary osteoblast angiogenic cytokine production. Plast Reconstr Surg 110, 139, 2002.
3. Eghbali-Fatourechi, G.Z., Lamsam, J., Fraser, D., Nagel, D., Riggs, B.L., and Khosla, S. Circulating osteoblast-lineage cells in humans. N Engl J Med 352, 1959, 2005.
4. Galiano, R.D., Tepper, O.M., Pelo, C.R., Bhatt, K.A., Callaghan, M., Bastidas, N., Bunting, S., Steinmetz, H.G., and Gurtner, G.C. Topical vascular endothelial growth factor accelerates diabetic wound healing through increased angiogenesis and by mobilizing and recruiting bone marrowderived cells. Am J Pathol 164, 1935, 2004.
5. Tepper, O.M., Capla, J.M., Galiano, R.D., Ceradini, D.J., Callaghan, M.J., Kleinman, M.E., and Gurtner, G.C. Adult vasculogenesis occurs through in situ recruitment, proliferation, and tubulization of circulating bone marrow-derived cells. Blood 105, 1068, 2005.
6. Park, S., Tepper, O.M., Galiano, R.D., Capla, J.M., Baharestani, S., Kleinman, M.E., Pelo, C.R., Levine, J.P., and Gurtner, G.C. Selective recruitment of endothelial progenitor cells to ischemic tissues with increased neovascularization. Plast Reconstr Surg 113, 284, 2004.
7. Higashino, K., Viggeswarapu, M., Bargouti, M., Liu, H., Titus, L., and Boden, S.D. Stromal cell-derived factor-1 potentiates bone morphogenic protein-2 induced bone formation. Tissue Eng Part A 17, 523, 2011.
8. Allori, A.C., Sailon, A.M., and Warren, S.M. Biological basis of bone formation, remodeling, and repair-part I: biochemical signaling molecules. Tissue Eng Part B Rev 14, 259, 2008.
9. Allori, A.C., Sailon, A.M., and Warren, S.M. Biological basis of bone formation, remodeling, and repair-part II: extracellular matrix. Tissue Eng Part B Rev 14, 275, 2008.
10. Allori, A.C., Sailon, A.M., Pan, J.H., and Warren, S.M. Biological basis of bone formation, remodeling, and repairpart III: biomechanical forces. Tissue Eng Part B Rev 14, 285, 2008.
11. Gawlitta, D., Fledderus, J.O., van Rijen, M.H., Dokter, I., Alblas, J., Verhaar, M.C., and Dhert, W.J. Hypoxia impedes vasculogenesis of in vitro engineered bone. Tissue Eng Part A 18, 208, 2012.
12. Pietilä, M., Palomäki, S., Lehtonen, S., Ritamo, I., Valmu, L., Nystedt, J., Laitinen, S., Leskelä, H.V., Sormunen, R., Pesälä, J., Nordström, K., Vepsäläinen, A., and Lehenkari, P. Mitochondrial function and energy metabolism in umbilical cord blood-and bone marrow-derived mesenchymal stem cells. Stem Cells Dev 21, 575, 2012.
13. Yang, X.B., Whitaker, M.J., Sebald, W., Clarke, N., Howdle, S.M., Shakesheff, K.M., and Oreffo, R.O. Human osteoprogenitor bone formation using encapsulated bone morphogenetic protein 2 in porous polymer scaffolds. Tissue Eng 10, 1037, 2004.
14. Jeon, O., Song, S.J., Kang, S.W., Putnam, A.J., and Kim, B.S. Enhancement of ectopic bone formation by bone morphogenetic protein-2 released from a heparin-conjugated poly(Llactic-co-glycolic acid) scaffold. Biomaterials 28, 2763, 2007.
15. Beloti, M.M., Sicchieri, L.G., de Oliviera, P.T., and Rosa, A.L. The influence of osteoblast differentiation stage on bone formation in autogenously implanted cell-based poly(lactideco-glycolide) and calcium phosphate constructs. Tissue Eng Part A 18, 999, 2012.
16. Kaigler, D., Wang, Z., Horger, K., Mooney, D.J., and Krebsbach, P.H. VEGF scaffolds enhance angiogenesis and bone regeneration in irradiated osseous defects. J Bone Miner Res 21, 735, 2006.
17. Kanczler, J.M., Ginty, P.J., Barry, J.J., Clarke, N.M., Howdle, S.M., Shakesheff, K.M., and Oreffo, R.O. The effect of mesenchymal populations and vascular endothelial growth factor delivered from biodegradable polymer scaffolds on bone formation. Biomaterials 29, 1892, 2008.
18. Singh, S., Wu, B.M., and Dunn, J.C. Accelerating vascularization in polycaprolactone scaffolds by endothelial progenitor cells. Tissue Eng Part A 17, 1819, 2011.
19. Choong, C.S., Hutmacher, D.W., and Triffitt, J.T. Co-culture of bone marrow fibroblasts and endothelial cells on modified polycaprolactone substrates for enhanced potentials in bone tissue engineering. Tissue Eng 12, 2521, 2006.
20. Jabbarzadeh, E., Starnes, T., Khan, Y.M., Jiang, T., Wirtel, A.J., Deng, M., Lv, Q., Nair, L.S., Doty, S.B., and Laurencin, C.T. Induction of angiogenesis in tissue-engineered scaffolds designed for bone repair: a combined gene therapy-cell transplantation approach. Proc Natl Acad Sci USA 105, 11099, 2008.
21. Hofmann, A., Ritz, U., Verrier, S., Eglin, D., Alini, M., Fuchs, S., Kirkpatrick, C.J., and Rommens, P.M. The effect of human osteoblasts on proliferation and neo-vessel formation of human umbilical vein endothelial cells in a long-term 3D coculture on polyurethane scaffolds. Biomaterials 29, 4217, 2008.
22. Duffy, G.P., Ahsan, T., OBrien, T., Barry, F., and Nerem, R.M. Bone marrow-derived mesenchymal stem cells promote angiogenic processes in a time-and dose-dependent manner in vitro. Tissue Eng Part A 15, 2459, 2009.
23. Koob, S., Torio-Padron, N., Stark, G.B., Hannig, C., Stankovic, Z., and Finkenzeller, G. Bone formation and neovascularization mediated by mesenchymal stem cells and endothelial cells in critical-sized calvarial defects. Tissue Eng Part A 17, 311, 2011.
24. Rouwkema, J., Westerweel, P.E., de Boer, J., Verhaar, M.C., and van Blitterswijk, C.A. The use of endothelial progenitor cells for prevascularized bone tissue engineering. Tissue Eng Part A 15, 2015, 2009.
25. Guillotin, B., Bareille, R., Bourget, C., Bordenave, L., and Amedee, J. Interaction between human umbilical vein endothelial cells and human osteoprogenitors triggers pleiotropic effect that may support osteoblastic function. Bone 42, 1080, 2008.
26. Zuk, P.A., Zhu, M., Mizuno, H., Huang, J., Futrell, J.W., Katz, A.J., Benhaim, P., Lorenz, H.P., and Hedrick, M.H. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7, 211, 2001.
27. Zuk, P.A., Zhu, M., Ashjian, P., De Ugarte, D.A., Huang, J.I., Mizuno, H., Alfonso, Z.C., Fraser, J.K., Benhaim, P., and Hedrick, M.H. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13, 4279, 2002.
28. Planat-Benard, V., Silvestre, J.S., Cousin, B., Andre, M., Nibbelink, M., Tamarat, R., Clergue, M., Manneville, C., Saillan-Barreau, C., Duriez, M., Tedgui, A., Levy, B., Penicaud, L., and Casteilla, L. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 109, 656, 2004.
29. Halvorsen, Y.D., Franklin, D., Bond, A.L., Hitt, D.C., Auchter, C., Boskey, A.L., Paschalis, E.P., Wilkison, W.O., and Gimble, J.M. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng 7, 729, 2001.
30. Erickson, G.R., Gimble, J.M., Franklin, D.M., Rice, H.E., Awad, H., and Guilak, F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun 290, 763, 2002.
31. Toriyama, K., Kawaguchi, N., Kitoh, J., Tajima, R., Inou, K., Kitagawa, Y., and Torii, S. Endogenous adipocyte precursor cells for regenerative soft-tissue engineering. Tissue Eng 8, 157, 2002.
32. Kolbe, M., Xiang, Z., Dohle, E., Tonak, M., Kirkpatrick, C.J., and Fuchs, S. Paracrine effects influenced by cell culture medium and consequences on microvessel-like structures in cocultures of mesenchymal stem cells and outgrowth endothelial cells. Tissue Eng Part A 17, 2199, 2011.
33. Pu, L.L., Coleman, S.R., Cui, X., Ferguson, R.E., Jr., and Vasconez, H.C. Autologous fat grafts harvested and refined by the Coleman technique: a comparative study. Plast Reconstr Surg 122, 932, 2008.
34. Boquest, A.C., Shahdadfar, A., Brinchmann, J.E., and Collas, P. Isolation of stromal stem cells from human adipose tissue. Methods Mol Biol 325, 35, 2006.
35. Diefenderfer, D.L., Osyczka, A.M., Garino, J.P., and Leboy, P.S. Regulation of BMP-induced transcription in cultured human bone marrow stromal cells. J Bone Joint Surg Am 85-A Suppl 3, 19, 2003.
36. Jager, M., Fischer, J., Dohrn, W., Li, X., Ayers, D.C., Czibere, A., Prall, W.C., Lensing-Hohn, S., and Krauspe, R. Dexamethasone modulates BMP-2 effects on mesenchymal stem cells in vitro. J Orthop Res 26, 1440, 2008.
37. Wongkhantee, S., Yongchaitrakul, T., and Pavasant, P. Mechanical stress induces osteopontin via ATP/P2Y1 in periodontal cells. J Dent Res 87, 564, 2008.
38. Morsczeck, C. Gene expression of runx2, Osterix, c-fos, DLX-3, DLX-5, and MSX-2 in dental follicle cells during osteogenic differentiation in vitro. Calcif Tissue Int 78, 98, 2006.
39. Nefussi, J.R., Ollivier, A., Oboeuf, M., and Forest, N. Rapid nodule evaluation computer-aided image analysis procedure for bone nodule quantification. Bone 20, 5, 1997.
40. Baudouin-Cornu, P., and Thomas, D. Evolutionary biology: oxygen at lifes boundaries. Nature 445, 35, 2007.
41. Pacicca, D.M., Patel, N., Lee, C., Salisbury, K., Lehmann, W., Carvalho, R., Gerstenfeld, L.C., and Einhorn, T.A. Expression of angiogenic factors during distraction osteogenesis. Bone 33, 889, 2003.
42. Mayer, H., Bertram, H., Lindenmaier, W., Korff, T., Weber, H., and Weich, H. Vascular endothelial growth factor (VEGF-A) expression in human mesenchymal stem cells: autocrine and paracrine role on osteoblastic and endothelial differentiation. J Cell Biochem 95, 827, 2005.
43. Pountos, I., Georgouli, T., Calori, G.M., and Giannoudis, P.V. Do nonsteroidal anti-inflammatory drugs affect bone healing? a critical analysis. ScientificWorldJournal, 1, 2012 [Epub ahead of print];DOI: 10.1100/2012/606404.
44. Brekken, R.A., and Sage, E.H. SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol 19, 816, 2001.
45. Takahashi, F., Akutagawa, S., Fukumoto, H., Tsukiyama, S., Ohe, Y., Takahashi, K., Fukuchi, Y., Saijo, N., and Nishio, K. Osteopontin induces angiogenesis of murine neuroblastoma cells in mice. Int J Cancer 98, 707, 2002.
46. Marie, P.J. Transcription factors controlling osteoblastogenesis. Arch Biochem Biophys 473, 98, 2008.
47. Karsenty, G., Kronenberg, H.M., and Settembre, C. Genetic control of bone formation. Annu Rev Cell Dev Biol 25, 629, 2009.
48. Deshpande, A.M., Akunowicz, J.D., Reveles, X.T., Patel, B.B., Saria, E.A., Gorlick, R.G., Naylor, S.L., Leach, R.J., and Hansen, M.F. PHC3, a component of the hPRC-H complex, associates with E2F6 during G0 and is lost in osteosarcoma tumors. Oncogene 26, 1714, 2007.
49. Sutherland, R.M., Sordat, B., Bamat, J., Gabbert, H., Bourrat, B., and Mueller-Klieser, W. Oxygenation and differentiation in multicellular spheroids of human colon carcinoma. Cancer Res 46, 5320, 1986.
50. Malaval, L., Modrowski, D., Gupta, A.K., and Aubin, J.E. Cellular expression of bone-related proteins during in vitro osteogenesis in rat bone marrow stromal cell cultures. J Cell Physiol 158, 555, 1994.
51. Chen, J., Singh, K., Mukherjee, B.B., and Sodek, J. Developmental expression of osteopontin (OPN) mRNA in rat tissues: evidence for a role for OPN in bone formation and resorption. Matrix 13, 113, 1993.
52. Aubin, J.E. Advances in the osteoblast lineage. Biochem Cell Biol 76, 899, 1998.
53. Yang, X., and Karsenty, G. ATF4, the osteoblast accumulation of which is determined post-translationally, can induce osteoblast-specific gene expression in non-osteoblastic cells. J Biol Chem 279, 47109, 2004.
54. Eggermann, J., Kliche, S., Jarmy, G., Hoffmann, K., Mayr-Beyrle, U., Debatin, K.M., Waltenberger, J., and Beltinger, C. Endothelial progenitor cell culture and differentiation in vitro: a methodological comparison using human umbilical cord blood. Cardiovasc Res 58, 478, 2003.
55. Hristov, M., Erl, W., and Weber, P.C. Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol 23, 1185, 2003.
56. Nguyen, V.A., Furhapter, C., Obexer, P., Stossel, H., Romani, N., and Sepp, N. Endothelial cells from cord blood CD133 + CD34 + progenitors share phenotypic, functional and gene expression profile similarities with lymphatics. J Cell Mol Med 13, 522, 2009.