Bioluminescent and micro-computed tomography imaging of bone repair induced by fibrin-binding growth factors

Acta Biomaterialia

Volumn 10, Issue 10, 2014, Pages 4377-4389

  Vila, Olaia F ^a,b   Martino, Mikaël M ^c   Nebuloni, Laura ^d   Kuhn, Gisela ^d   Pérez Amodio, Soledad ^b,e   Müller, Ralph ^d   Hubbell, Jeffrey A ^c   Rubio, Nuria ^a,b   Blanco, Jerónimo ^a,b  

^a INSTITUTE OF ADVANCED CHEMISTRY OF CATALONIA IQAC CSIC   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c EPFL   (Switzerland)

^d ETH ZURICH   (Switzerland)

^e INSTITUTE FOR BIOENGINEERING OF CATALONIA IBEC   (Spain)

Author keywords

Angiogenesis; Bioluminescence imaging; Bone regeneration; Fibrin; Mesenchymal stem cell

Indexed keywords

BIOLUMINESCENCE; BONE; CELL ADHESION; CELL CULTURE; CELL GROWTH; COMPUTERIZED TOMOGRAPHY; DEFECTS; ENDOTHELIAL CELLS; GENE EXPRESSION; GROWTH KINETICS; PLATELETS; REPAIR; STEM CELLS;

ADIPOSE TISSUE; ANGIOGENESIS; BIOLUMINESCENCE IMAGING; BONE MORPHOGENETIC PROTEIN-2; BONE REGENERATION; FIBRIN; HUMAN MESENCHYMAL STEM CELLS; MESENCHYMAL STEM CELL; OSTEOCALCIN; PLATELET-DERIVED GROWTH FACTORS;

TISSUE REGENERATION;

BONE MORPHOGENETIC PROTEIN 2; CD31 ANTIGEN; FIBRIN; LENTIVIRUS VECTOR; OSTEOCALCIN; PLATELET DERIVED GROWTH FACTOR BB; BMP2 PROTEIN, HUMAN; LUCIFERASE; PLATELET DERIVED GROWTH FACTOR B; PLATELET-DERIVED GROWTH FACTOR BB;

ADIPOSE DERIVED STEM CELL; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; BONE REGENERATION; BONE REMODELING; CELL COUNT; CELL DIFFERENTIATION; CELL GROWTH; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOMEGALOVIRUS; DRUG ACTIVITY; ENDOTHELIUM CELL; GENE EXPRESSION; HISTOLOGY; HUMAN; HUMAN CELL; IMAGE ANALYSIS; LOW DRUG DOSE; LUCIFERASE ASSAY; MESENCHYMAL STEM CELL; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; PROMOTER REGION; SKULL DEFECT; VASCULARIZATION; VIRAL GENE DELIVERY SYSTEM; ADIPOSE TISSUE; ANIMAL; BIOSYNTHESIS; CHEMISTRY; EXTRACELLULAR MATRIX; GENETICS; INJURIES; LUMINESCENCE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; SCID MOUSE; SKULL;

ADIPOSE TISSUE; ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE REGENERATION; CELL DIFFERENTIATION; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; FIBRIN; HUMANS; LUCIFERASES; LUMINESCENT MEASUREMENTS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, SCID; OSTEOBLASTS; PROTO-ONCOGENE PROTEINS C-SIS; SKULL; X-RAY MICROTOMOGRAPHY;

EID: 84908229553     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.05.028     Document Type: Article

References (45)

1. M. Kanitkar, H.D. Tailor, and W.S. Khan The use of growth factors and mesenchymal stem cells in orthopaedics Open Orthop J 5 Suppl. 2 2011 271 275
2. S. Govender, C. Csimma, H.K. Genant, A. Valentin-Opran, Y. Amit, and R. Arbel Recombinant human bone morphogenetic protein-2 for treatment of open tibial fractures: a prospective, controlled, randomized study of four hundred and fifty patients J Bone Joint Surg Am 84-A 2002 2123 2134
3. P. Levéen, M. Pekny, S. Gebre-Medhin, B. Swolin, E. Larsson, and C. Betsholtz Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities Genes Dev 8 1994 1875 1887
4. T.P. Richardson, M.C. Peters, A.B. Ennett, and D.J. Mooney Polymeric system for dual growth factor delivery Nat Biotechnol 19 2001 1029 1034
5. M.C. Phipps, Y. Xu, and S.L. Bellis Delivery of platelet-derived growth factor as a chemotactic factor for mesenchymal stem cells by bone-mimetic electrospun scaffolds PLoS One 7 2012 e40831
6. K. Chadwick, L. Wang, L. Li, P. Menendez, B. Murdoch, and A. Rouleau Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells Blood 102 2003 906 915
7. M. Lind, E.F. Eriksen, and C. Bünger Bone morphogenetic protein-2 but not bone morphogenetic protein-4 and -6 stimulates chemotactic migration of human osteoblasts, human marrow osteoblasts, and U2-OS cells Bone 18 1996 53 57
8. A.H. Reddi, and N.S. Cunningham Initiation and promotion of bone differentiation by bone morphogenetic proteins J Bone Miner Res 8 Suppl. 2 1993 S499 S502
9. N.K. Kanakaris, N. Lasanianos, G.M. Calori, R. Verdonk, T.J. Blokhuis, and P. Cherubino Application of bone morphogenetic proteins to femoral non-unions: a 4-year multicentre experience Injury 40 Suppl. 3 2009 S54 S61
10. G.M. Calori, L. Tagliabue, L. Gala, M. d'Imporzano, G. Peretti, and W. Albisetti Application of rhBMP-7 and platelet-rich plasma in the treatment of long bone non-unions: a prospective randomised clinical study on 120 patients Injury 39 2008 1391 1402
11. M. Ronga, F. Baldo, G. Zappalà, and P. Cherubino Recombinant human bone morphogenetic protein-7 for treatment of long bone non-union: an observational, retrospective, non-randomized study of 105 patients Injury 37 Suppl. 3 2006 S51 S56
12. L. Grgurevic, B. Macek, M. Mercep, M. Jelic, T. Smoljanovic, and I. Erjavec Bone morphogenetic protein (BMP)1-3 enhances bone repair Biochem Biophys Res Commun 408 2011 25 31
13. J.O. Hollinger, J.M. Schmitt, D.C. Buck, R. Shannon, S.P. Joh, and H.D. Zegzula Recombinant human bone morphogenetic protein-2 and collagen for bone regeneration J Biomed Mater Res 43 1998 356 364
14. E.J. Carragee, E.L. Hurwitz, and B.K. Weiner A critical review of recombinant human bone morphogenetic protein-2 trials in spinal surgery: emerging safety concerns and lessons learned Spine J 11 2011 471 491
15. I.J. Frieden Addendum: commentary on becaplermin gel (Regranex) for hemangiomas Pediatr Dermatol 25 2008 590
16. M.M. Martino, and J.A. Hubbell The 12th-14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain FASEB J 24 2010 4711 4721
17. M.M. Martino, P.S. Briquez, E. Güç, F. Tortelli, W.W. Kilarski, and S. Metzger Growth factors engineered for super-affinity to the extracellular matrix enhance tissue healing Science 343 2014 885 888
18. J. Polak, and L. Hench Gene therapy progress and prospects: in tissue engineering Gene Ther 12 2005 1725 1733
19. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, and J.D. Mosca Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147
20. P. Bianco, M. Riminucci, S. Gronthos, and P.G. Robey Bone marrow stromal stem cells: nature, biology, and potential applications Stem Cells 19 2001 180 192
21. G. Chamberlain, J. Fox, B. Ashton, and J. Middleton Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing Stem Cells 25 2007 2739 2749
22. A. Pansky, B. Roitzheim, and E. Tobiasch Differentiation potential of adult human mesenchymal stem cells Clin Lab 53 2007 81 84
23. P.A. Zuk, M. Zhu, P. Ashjian, D.A. De Ugarte, J.I. Huang, and H. Mizuno Human adipose tissue is a source of multipotent stem cells Mol Biol Cell 13 2002 4279 4295
24. D.A. De Ugarte, K. Morizono, A. Elbarbary, Z. Alfonso, P.A. Zuk, and M. Zhu Comparison of multi-lineage cells from human adipose tissue and bone marrow Cells Tissues Organs (Print) 174 2003 101 109
25. S. Kern, H. Eichler, J. Stoeve, H. Klüter, and K. Bieback Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue Stem Cells 24 2006 1294 1301
26. M. Vilalta, I.R. Dégano, J. Bagó, D. Gould, M. Santos, and M. García-Arranz Biodistribution, long-term survival, and safety of human adipose tissue-derived mesenchymal stem cells transplanted in nude mice by high sensitivity non-invasive bioluminescence imaging Stem Cells Dev 17 2008 993 1003
27. M. Iyer, L. Wu, M. Carey, Y. Wang, A. Smallwood, and S.S. Gambhir Two-step transcriptional amplification as a method for imaging reporter gene expression using weak promoters Proc Natl Acad Sci USA 98 2001 14595 14600
28. C.H. Contag, S.D. Spilman, P.R. Contag, M. Oshiro, B. Eames, and P. Dennery Visualizing gene expression in living mammals using a bioluminescent reporter Photochem Photobiol 66 1997 523 531
29. M. Vilalta, C. Jorgensen, I.R. Dégano, Y. Chernajovsky, D. Gould, and D. Noël Dual luciferase labelling for non-invasive bioluminescence imaging of mesenchymal stromal cell chondrogenic differentiation in demineralized bone matrix scaffolds Biomaterials 30 2009 4986 4995
30. K. Briot, and C. Roux Biochemical markers of bone remodeling Gynecol Obstet Fertil 33 2005 1009 1013
31. F. Yeung, W.K. Law, C.-H. Yeh, J.J. Westendorf, Y. Zhang, and R. Wang Regulation of human osteocalcin promoter in hormone-independent human prostate cancer cells J Biol Chem 277 2002 2468 2476
32. P.J. Newman, and S.M. Albelda Cellular and molecular aspects of PECAM-1 Nouv Rev Fr Hematol 34 Suppl. 1992 S9 S13
33. P. Ray, A. De, J.-J. Min, R.Y. Tsien, and S.S. Gambhir Imaging tri-fusion multimodality reporter gene expression in living subjects Cancer Res 64 2004 1323 1330
34. J.R. Bagó, E. Aguilar, M. Alieva, C. Soler-Botija, O.F. Vila, and S. Claros In vivo bioluminescence imaging of cell differentiation in biomaterials a platform for scaffold development Tissue Eng Part A 2012
35. J.C. Schense, and J.A. Hubbell Cross-linking exogenous bifunctional peptides into fibrin gels with factor XIIIa Bioconjug Chem 10 1999 75 81
36. M.M. Martino, F. Tortelli, M. Mochizuki, S. Traub, D. Ben-David, and G.A. Kuhn Engineering the growth factor microenvironment with fibronectin domains to promote wound and bone tissue healing Sci Transl Med 3 2011 100ra89
37. I.R. Dégano, M. Vilalta, J.R. Bagó, A.M. Matthies, J.A. Hubbell, and H. Dimitriou Bioluminescence imaging of calvarial bone repair using bone marrow and adipose tissue-derived mesenchymal stem cells Biomaterials 29 2008 427 437
38. M.P. Lutolf, F.E. Weber, H.G. Schmoekel, J.C. Schense, T. Kohler, and R. Müller Repair of bone defects using synthetic mimetics of collagenous extracellular matrices Nat Biotechnol 21 2003 513 518
39. N. Beckmann, A. Schuler, T. Mueggler, E.P. Meyer, K.-H. Wiederhold, and M. Staufenbiel Age-dependent cerebrovascular abnormalities and blood flow disturbances in APP23 mice modeling Alzheimer's disease J Neurosci 23 2003 8453 8459
40. T. Krucker, A. Lang, and E.P. Meyer New polyurethane-based material for vascular corrosion casting with improved physical and imaging characteristics Microsc Res Tech 69 2006 138 147
41. D.L. Hutton, E.M. Moore, J.M. Gimble, and W.L. Grayson Platelet-derived growth factor and spatiotemporal cues induce development of vascularized bone tissue by adipose-derived stem cells Tissue Eng Part A 19 2013 2076 2086
42. P.U. Magnusson, C. Looman, A. Ahgren, Y. Wu, L. Claesson-Welsh, and R.L. Heuchel Platelet-derived growth factor receptor-beta constitutive activity promotes angiogenesis in vivo and in vitro Arterioscler Thromb Vasc Biol 27 2007 2142 2149
43. D. Cantinieaux, R. Quertainmont, S. Blacher, L. Rossi, T. Wanet, and A. Noël Conditioned medium from bone marrow-derived mesenchymal stem cells improves recovery after spinal cord injury in rats: an original strategy to avoid cell transplantation PLoS One 8 2013 e69515
44. M. Song, J. Heo, J.-Y. Chun, H.S. Bae, J.W. Kang, and H. Kang The paracrine effects of mesenchymal stem cells stimulate the regeneration capacity of endogenous stem cells in the repair of a bladder outlet obstruction-induced overactive bladder Stem Cells Dev 2013
45. S.H. Lee, S.Y. Jin, J.S. Song, K.K. Seo, and K.H. Cho Paracrine effects of adipose-derived stem cells on keratinocytes and dermal fibroblasts Ann Dermatol 24 2012 136 143