Role of IGF1 and IGF1/VEGF on human mesenchymal stromal cells in bone healing: Two sources and two fates

Tissue Engineering - Part A

Volumn 20, Issue 17-18, 2014, Pages 2473-2482

  Ferretti, Concetta ^a   Vozzi, Giovanni ^b   Falconi, Mirella ^c   Orciani, Monia ^a   Gesi, Marco ^b   Di Primio, Roberto ^a   Mattioli Belmonte, Monica ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSITY OF PISA   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ENGINEERING; FLOWCHARTING; TISSUE ENGINEERING; TRANSCRIPTION;

BONE TISSUE ENGINEERING; GENE EXPRESSION PROFILES; MESENCHYMAL STROMAL CELLS; OSTEOBLASTIC DIFFERENTIATION; PERIOSTEUM-DERIVED PROGENITOR CELLS; PI3K/AKT SIGNALING; VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULARIZATION;

CELL CULTURE;

BETA CATENIN; BONE MORPHOGENETIC PROTEIN 2; COLLAGENASE 3; GROWTH FACTOR; INSULIN GROWTH FACTOR 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 3; OCTAMER TRANSCRIPTION FACTOR 4; OSTEOCALCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; VASCULOTROPIN; IGF1 PROTEIN, HUMAN; SOMATOMEDIN C; VASCULOTROPIN A;

ADULT; ANGIOGENESIS; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; FRACTURE HEALING; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MESENCHYMAL STROMA CELL; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PERIOSTEUM; PERIOSTEUM DERIVED PROGENITOR CELL; PHENOTYPE; STIMULATION; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; MIDDLE AGED; PHYSIOLOGY;

ADULT; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MALE; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; OSTEOBLASTS; OSTEOGENESIS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84907063495     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0453     Document Type: Article

References (52)

1. Colnot, C. Cell sources for bone tissue engineering: insights from basic science. Tissue Eng Part B Rev 17, 449, 2011.
2. Gamie, Z., Tran, G.T., Vyzas, G., Korres, N., Heliotis, M., Mantalaris, A., and Tsiridis, E. Stem cells combined with bone graft substitutes in skeletal tissue engineering. Expert Opin Biol Ther 12, 713, 2012.
3. Zhang, X., Awad, H.A., O'Keefe, R.J., Guldberg, R.E., and Schwarz, E.M. A perspective: engineering periosteum for structural bone graft healing. Clin Orthop Relat Res 466, 1777, 2008.
4. Meijer, G.J., de Bruijn, J.D., Koole, R., and van Blitterswijk, C.A. Cell-based bone tissue engineering. PLoS Med 4, e9, 2007.
5. Lo, D.D., Hyun, J.S., Chung, M.T., Montoro, D.T., Zimmermann, A., Grova, M.M., Lee, M., Wan, D.C., and Longaker, M.T. Repair of a critical-sized calvarial defect model using adipose-derived stromal cells harvested from lipoaspirate. J Vis Exp 68, pii:4221, 2012.
6. Zheng, B., Li, G., Chen, W.C., Deasy, B.M., Pollett, J.B., Sun, B., Drowley, L., Gharaibeh, B., Usas, A., Péault, B., and Huard, J. Human myogenic endothelial cells exhibit chondrogenic and osteogenic potentials at the clonal level. J Orthop Res 31, 1089, 2013.
7. Orciani, M., Di Primio, R., Ferretti, C., Orsini G., Salvolini E., Lazzarini R., Mattioli Belmonte, M. In vitro evaluation of Mesenchymal stem cell isolation possibility from different intra-oral tissues. J Biol Regul Homeost Agents 26, 57S, 2012.
8. Orciani, M., Trubiani, O., Vignini, A., Mattioli-Belmonte, M., Di Primio, R., and Salvolini, E. Nitric oxide production during the osteogenic differentiation of human periodontal ligament mesenchymal stem cells. Acta Histochem 111, 15, 2009.
9. Gigante A., Cappella M., Manzotti S., Cecconi S., Greco F., Di Primio R., and Mattioli-Belmonte, M. Osteoinduction properties of different growth factors on cells from nonunion patients: In vitro study for clinical application. J Biol Regul Homeost Agents 24, 51, 2010.
10. Augello, A., Kurth, T.B., and De Bari, C. Mesenchymal stem cells: a perspective from in vitro cultures to in vivo migration and niches. Eur Cell Mater 20, 121, 2010.
11. Salvolini, E., Orciani, M., Vignini, A., Mattioli-Belmonte, M., Mazzanti, L., and Di Primio, R. Skin-derived mesenchymal stem cells (S-MSCs) induce endothelial cell activation by paracrine mechanisms. Exp Dermatol 19, 848, 2010.
12. Ferretti, C., Borsari, V., Falconi, M., Gigante, A., Lazzarini, R., Fini, M., Di Primio, R., and Mattioli-Belmonte, M. Human periosteum-derived stem cells for tissue engineering applications: the role of VEGF. Stem Cell Rev 8, 882, 2012.
13. Rieger, K., Marinets, O., Fietz, T., Körper, S., Sommer, D., Mücke, C., Reufi, B., Blau, W.I., Thiel, E., and Knauf, W.U. Mesenchymal stem cells remain of host origin even a long time after allogeneic peripheral blood stem cell or bone marrow transplantation. Exp Hematol 33, 605, 2005.
14. Dominici, M., Marino, R., Rasini, V., Spano, C., Paolucci, P., Conte, P., Hofmann, T.J., and Horwitz, E.M. Donor cellderived osteopoiesis originates from a self-renewing stem cell with a limited regenerative contribution after transplantation. Blood 111, 4386, 2008.
15. Colnot, C. Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration. J Bone Miner Res 24, 274, 2009.
16. Chang, H., and Knothe Tate, M.L. Concise review: the periosteum: tapping into a reservoir of clinically useful progenitor cells. Stem Cells Transl Med 1, 480, 2012.
17. Zhang, X., Xie, C., Lin, A.S., Ito, H., Awad, H., Lieberman, J.R., Rubery, P.T., Schwarz, E.M., O'Keefe, R.J., and Guldberg, R.E. Periosteal progenitor cell fate in segmental cortical bone graft transplantations: implications for functional tissue engineering. J Bone Miner Res 20, 2124, 2005.
18. Takeda, K., Gosiewska, A., and Peterkofsky, B. Similar, but not identical, modulation of expression of extracellular matrix components during in vitro and in vivo aging of human skin fibroblasts. J Cell Physiol 153, 450, 1992.
19. Vishnubalaji, R., Manikandan, M., Al-Nbaheen, M., Kadalmani, B., Aldahmash, A., and Alajez, N.M. In vitro differentiation of human skin-derived multipotent stromal cells into putative endothelial-like cells. BMC Dev Biol 12, 7, 2012.
20. Giannoudis, P.V., Einhorn, T.A., and Marsh, D. Fracture healing: the diamond concept. Injury 38, S3, 2007.
21. Huang, Z., Ren, P.G., Ma, T., Smith, R.L., and Goodman, S.B. Modulating osteogenesis of mesenchymal stem cells by modifying growth factor availability. Cytokine 51, 305, 2010.
22. 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.
23. Kanczler, J.M., and Oreffo, R.O. Osteogenesis and angiogenesis: the potential for engineering bone. Eur Cell Mater 15, 100, 2008.
24. Nguyen, L.H., Annabi, N., Nikkhah, M., Bae, H., Binan, L., Park, S., Kang, Y., Yang, Y., and Khademhosseini, A. Vascularized bone tissue engineering: approaches for potential improvement. Tissue Eng Part B 18, 363, 2012.
25. Kyriakidou K., Lucarini, G., Zizzi, A., Salvolini, E., Mattioli-Belmonte, M., Mollica, F., Gloria, A., and Ambrosio, L. Dynamic co-seeding of osteoblast and endothelial cells on 3D polycaprolactone scaffold for enhanced bone tissueengineering prospective. J Bioact Comp Polym 23, 227, 2008.
26. Cao, L., Liu, X., Liu, S., Jiang, Y., Zhang, X., Zhang, C., and Zeng, B. Experimental repair of segmental bone defects in rabbits by angiopoietin-1 gene transfected MSCs seeded on porous β-TCP scaffolds. J Biomed Mater Res B Appl Biomater 100, 1229, 2012.
27. Reyes, M., Lund, T., Lenvik, T., Aguiar, D., Koodie, L., and Verfaillie, C.M. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 98, 2615, 2001.
28. Reyes, M., Dudek, A., Jahagirdar, B., Koodie, L., Marker, P.H., and Verfaillie, C.M. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 109, 337, 2002.
29. Oswald, J., Boxberger, S., Jørgensen, B., Feldmann, S., Ehninger, G., Bornhäuser, M., and Werner, C. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22, 377, 2004.
30. Pal, R., Hanwate, M., Jan, M., and Totey, S. Phenotypic and functional comparison of optimum culture conditions for upscaling of bone marrow-derived mesenchymal stem cells. J Tissue Eng Regen Med 3, 163, 2009.
31. Orciani, M., Gorbi, S., Benedetti, M., Di Benedetto, G., Mattioli-Belmonte, M., Regoli, F., and Di Primio, R. Oxidative stress defense in human-skin-derived mesenchymal stem cells versus human keratinocytes: Different mechanisms of protection and cell selection. Free Radic Biol Med 49, 830, 2010.
32. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D.J., and Horwitz, E. Minimal criteria for deifying multipotent mesenchymal stem cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315, 2006.
33. Peterson, L., Minas, T., Brittberg, M., Nilsson, A., Sjögren-Jansson, E., and Lindahl, A. Two-to 9-year outcome after autologous chondrocyte transplantation of the knee. Clin Orthop Relat Res 374, 212, 2000.
34. Uematsu, K., Kawase, T., Nagata, M., Suzuki, K., Okuda, K., Yoshie, H., Burns, D.M., and Takagi, R. Tissue culture of human alveolar periosteal sheets using a stem-cell culture medium (MesenPRO-RS™): In vitro expansion of CD146-positive cells and concomitant upregulation of osteogenic potential in vivo. Stem Cell Res 10, 1, 2013.
35. Mirabella, T., Gentili, C., Daga, A., and Cancedda, R. Amniotic fluid stem cells in a bone microenvironment: driving host angiogenic response. Stem Cell Res 11, 540, 2013.
36. Levi, B., Hyun, J.S., Montoro, D.T., Lo, D.D., Chan, C.K., Hu, S., Sun, N., Lee, M., Grova, M., Connolly, A.J., Wu, J.C., Gurtner, G.C., Weissman, I.L., Wan, D.C., and Longaker, M.T. In vivo directed differentiation of pluripotent stem cells for skeletal regeneration. Proc Natl Acad Sci U S A 109, 20379, 2012.
37. Bai, Y., Yin, G., Huang, Z., Liao, X., Chen, X., Yao, Y., and Pu, X. (2013) Localized delivery of growth factors for angiogenesis and bone formation in tissue engineering. Int Immunopharmacol 16, 214, 2013.
38. Helmrich, U., Di Maggio, N., Güven, S., Groppa, E., Melly, L., Largo, R.D., Heberer, M., Martin, I., Scherberich, A., and Banfi, A. Osteogenic graft vascularization and bone resorption by VEGF-expressing human mesenchymal progenitors. Biomaterials 34, 5025, 2013.
39. Piecewicz, S.M., Pandey, A., Roy, B., Xiang, S.H., Zetter, B.R., and Sengupta, S. Insulin-like growth factors promote vasculogenesis in embryonic stem cells. PLoS One. 7, e32191, 2012.
40. Hsiao, S.T., Asgari, A., Lokmic, Z., Sinclair, R., Dusting, G.J., Lim, S.Y., and Dilley, R.J. Comparative analysis of paracrine factor expression in human adult mesenchymal stem cells derived from bone marrow, adipose, and dermal tissue. Stem Cells Dev 21, 2189, 2012.
41. He, J., Rosen, C.J., Adams, D.J., and Kream, B.E. Postnatal growth and bone mass in mice with IGF-I haploinsufficiency. Bone 38, 826, 2006.
42. Marcellini, S., Henriquez, J.P., and Bertin, A. Control of osteogenesis by the canonical Wnt and BMP pathways in vivo: cooperation and antagonism between the canonical Wnt and BMP pathways as cells differentiate from osteochondroprogenitors to osteoblasts and osteocytes. Bioessays 34, 953, 2012.
43. Chen, Y., Whetstone, H.C., Youn, A., Nadesan, P., Chow, E.C.Y., Lin, A.C., and Alman, A.B. Beta-catenin signaling pathway is crucial for bone morphogenetic protein 2 to induce new bone formation. J Biol Chem 282, 526, 2007.
44. Fowlkes, J.L., Bunn, C.R., and Thrailkill, K.M. Contributions of the insulin/insulin-like growth factor-1 axis to diabetic osteopathy. J Diabetes Metab 1, S1, 2011.
45. Yu, Y., Mu, J., Fan, Z., Lei, G., Yan, M., Wang, S., Tang, C., Wang, Z., Yu, J., and Zhang, G. Insulin-like growth factor 1 enhances the proliferation and osteogenic differentiation of human periodontal ligament stem cells via ERK and JNK MAPK pathways. Histochem Cell Biol 137, 513, 2012.
46. Qiao, M., Shapiro, P., Kumar, R., and Passaniti, A. Insulinlike growth factor-1 regulates endogenous RUNX2 activity in endothelial cells through a phosphatidylinositol 3-kinase/ERK-dependent and Akt-independent signaling pathway. J Biol Chem 279, 42709, 2014.
47. Zhang, C., Tang, W., and Li, Y. Matrix metalloproteinase 13 (MMP13) is a direct target of osteoblast-specific tran-scription factor osterix (Osx) in osteoblasts. PLoS One 7, e50525, 2013.
48. Moreno-Miralles, I., Ren, R., Moser, M., Hartnett, M.E., and Patterson, C. Bone morphogenetic protein endothelial cell precursor-derived regulator regulates retinal angiogenesis in vivo in a mouse model of oxygen-induced retinopathy. Arterioscler Thromb Vasc Biol 31, 2216, 2011.
49. Ogasawara, T., Ohba, S., Yano, F., Kawaguchi, H., Chung, U.I., Saito, T., Yonehara, Y., Nakatsuka, T., Mori, Y., Takato, T., and Hoshi, K. Nanog promotes osteogenic differentiation of the mouse mesenchymal cell line C3H10T1/2 by modulating bone morphogenetic protein (BMP) signaling. J Cell Physiol 228, 163, 2013.
50. Rodda, D.J., Chew, J.L., Lim, L.H., Loh, Y.H., Wang, B., Ng, H.H., and Robson, P. Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 280, 24731, 2005.
51. Go, M.J., Takenaka, C., and Ohgushi, H. Forced expression of Sox2 or Nanog in human bone marrow derived mesenchymal stem cells maintains their expansion and differentiation capabilities. Exp Cell Res 314, 1147, 2008.
52. Liu, L., Wei, X., Huang, R., Ling, J., Wu, L., and Xiao, Y. Effect of bone morphogenetic protein-4 on the expression of Sox2, Oct-4, and c-Myc in human periodontal ligament cells during long-term culture. Stem Cells Dev 22, 1670, 2013.