Effects of biologic scaffolds on human stem cells and implications for CNS tissue engineering

Tissue Engineering - Part A

Volumn 20, Issue 1-2, 2014, Pages 313-323

  Crapo, Peter M ^a,b   Tottey, Stephen ^a   Slivka, Peter F ^a   Badylak, Stephen F ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b C R BARD INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTOLOGY; HYDROGELS; MAMMALS; NEURONS; STEM CELLS; TISSUE;

CENTRAL NERVOUS SYSTEM TISSUES; DECELLULARIZATION; EXTRACELLULAR MATRICES; INNATE IMMUNE RESPONSE; NEURITE EXTENSION; SCAFFOLD MATERIALS; STEM CELL VIABILITIES; THREE-DIMENSIONAL CULTURE;

SCAFFOLDS (BIOLOGY);

BETA III TUBULIN; BETA TUBULIN; TISSUE SCAFFOLD; UNCLASSIFIED DRUG;

ARTICLE; BLADDER; BRAIN; CELL PROLIFERATION; CHEMOTAXIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYDROGEL; IN VITRO STUDY; MITOGENESIS; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD; TISSUE ENGINEERING;

ANIMALS; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CHEMOTAXIS; EXTRACELLULAR MATRIX; HUMANS; NEURAL STEM CELLS; NEURITES; SOLUBILITY; SUS SCROFA; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84891516179     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0186     Document Type: Article

References (62)

1. Johansson, C.B., Svensson, M., Wallstedt, L., Janson, A.M., and Frisen, J. Neural stem cells in the adult human brain. Exp Cell Res 253, 733, 1999.
2. Nunes, M.C., Roy, N.S., Keyoung, H.M., Goodman, R.R., McKhann, G., 2nd, Jiang, L., Kang, J., Nedergaard, M., and Goldman, S.A. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 9, 439, 2003.
3. Dromard, C., Guillon, H., Rigau, V., Ripoll, C., Sabourin, J.C., Perrin, F.E., Scamps, F., Bozza, S., Sabatier, P., Lonjon, N., Duffau, H., Vachiery-Lahaye, F., Prieto, M., Tran Van Ba, C., Deleyrolle, L., Boularan, A., Langley, K., Gaviria, M., Privat, A., Hugnot, J.P., and Bauchet, L. Adult human spinal cord harbors neural precursor cells that generate neurons and glial cells in vitro. J Neurosci Res 86, 1916, 2008.
4. Bible, E.,Dell'Acqua, F., Solanky, B., Balducci, A., Crapo, P.M., Badylak, S.F., Ahrens, E.T., and Modo, M. Non-invasive imaging of transplanted human neural stem cells and ECM scaffold remodeling in the stroke-damaged rat brain by (19)Fand diffusion-MRI. Biomaterials 33, 2858, 2012.
5. Smith, E.J., Stroemer, R.P., Gorenkova, N., Nakajima, M., Crum, W.R., Tang, E., Stevanato, L., Sinden, J.D., and Modo, M. Implantation site and lesion topology determine efficacy of a human neural stem cell line in a rat model of chronic stroke. Stem Cells 30, 785, 2012.
6. Stroemer, P., Patel, S., Hope, A., Oliveira, C., Pollock, K., and Sinden, J. The neural stem cell line CTX0E03 promotes behavioral recovery and endogenous neurogenesis after experimental stroke in a dose-dependent fashion. Neurorehabil Neural Repair 23, 895, 2009.
7. Miljan, E.A., Hines, S.J., Pande, P., Corteling, R.L., Hicks, C., Zbarsky, V., Umachandran, M., Sowinski, P., Richardson, S., Tang, E., Wieruszew, M., Patel, S., Stroemer, P., and Sinden, J.D. Implantation of c-mycER TAM immortalized human mesencephalic-derived clonal cell lines ameliorates behavior dysfunction in a rat model of Parkinson's disease. Stem Cells Dev 18, 307, 2009.
8. Windrem, M.S., Nunes, M.C., Rashbaum, W.K., Schwartz, T.H., Goodman, R.A., McKhann, G., 2nd, Roy, N.S., and Goldman, S.A. Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat Med 10, 93, 2004.
9. Amariglio, N., Hirshberg, A., Scheithauer, B.W., Cohen, Y., Loewenthal, R., Trakhtenbrot, L., Paz, N., Koren-Michowitz, M., Waldman, D., Leider-Trejo, L., Toren, A., Constantini, S., and Rechavi, G. Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med 6, e1000029, 2009.
10. Ben-David, U., Mayshar, Y., and Benvenisty, N. Large-scale analysis reveals acquisition of lineage-specific chromosomal aberrations in human adult stemcells.Cell StemCell 9, 97, 2011.
11. Kazanis, I., and ffrench-Constant, C. Extracellular matrix and the neural stem cell niche. Dev Neurobiol 71, 1006, 2011.
12. Massirer, K.B., Carromeu, C., Griesi-Oliveira, K., and Muotri, A.R. Maintenance and differentiation of neural stem cells. Wiley Interdiscip Rev Syst Biol Med 3, 107, 2011.
13. Discher, D.E., Mooney, D.J., and Zandstra, P.W. Growth factors, matrices, and forces combine and control stem cells. Science 324, 1673, 2009.
14. Potter, W., Kalil, R.E., and Kao, W.J. Biomimetic material systems for neural progenitor cell-based therapy. Front Biosci 13, 806, 2008.
15. Zurita, M., Otero, L., Aguayo, C., Bonilla, C., Ferreira, E., Parajon, A., and Vaquero, J. Cell therapy for spinal cord repair: optimization of biologic scaffolds for survival and neural differentiation of human bone marrow stromal cells. Cytotherapy 12, 522, 2010.
16. Song, J.J., and Ott, H.C. Organ engineering based on decellularized matrix scaffolds. Trends Mol Med 17, 424, 2011.
17. Guo, S.Z., Ren, X.J., Wu, B., and Jiang, T. Preparation of the acellular scaffold of the spinal cord and the study of biocompatibility. Spinal Cord 48, 576, 2010.
18. Dequach, J.A., Yuan, S.H., Goldstein, L.S., and Christman, K.L. Decellularized porcine brain matrix for cell culture and tissue engineering scaffolds. Tissue Eng Part A 17, 2583, 2011.
19. Crapo, P.M., Medberry, C.J., Reing, J.E., Tottey, S., van der Merwe, Y., Jones, K.E., and Badylak, S.F. Biologic scaffolds composed of central nervous system extracellular matrix. Biomaterials 33, 3539, 2012.
20. Medberry, C.J., Crapo, P.M., Siu, B.F., Carruthers, C.A., Wolf, M.T., Nagarkar, S.P., Agrawal, V., Jones, K.E., Kelly, J., Johnson, S.A., Velankar, S.S., Watkins, S.C., Modo, M., and Badylak, S.F. Hydrogels derived from central nervous system extracellular matrix. Biomaterials 34, 1033, 2013.
21. Brown, B.N., Londono, R., Tottey, S., Zhang, L., Kukla, K.A., Wolf, M.T., Daly, K.A., Reing, J.E., and Badylak, S.F. Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials. Acta Biomater 8, 978, 2012.
22. Keane, T.J., Londono, R., Turner, N.J., and Badylak, S.F. Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials 33, 1771, 2012.
23. Ariganello, M.B., Simionescu, D.T., Labow, R.S., and Lee, J.M. Macrophage differentiation and polarization on a decellularized pericardial biomaterial. Biomaterials 32, 439, 2011.
24. Wong, M.L., Leach, J.K., Athanasiou, K.A., and Griffiths, L.G. The role of protein solubilization in antigen removal from xenogeneic tissue for heart valve tissue engineering. Biomaterials 32, 8129, 2011.
25. Sayk, F., Bos, I., Schubert, U., Wedel, T., and Sievers, H.H. Histopathologic findings in a novel decellularized pulmonary homograft: an autopsy study. Ann Thorac Surg 79, 1755, 2005.
26. Ruzmetov, M., Shah, J.J., Geiss, D.M., and Fortuna, R.S. Decellularized versus standard cryopreserved valve allografts for right ventricular outflow tract reconstruction: a single-institution comparison. J Thorac Cardiovasc Surg 143, 543, 2012.
27. Badylak, S.F., Hoppo, T., Nieponice, A., Gilbert, T.W., Davison, J.M., and Jobe, B.A. Esophageal preservation in five male patients after endoscopic inner-layer circumferential resection in the setting of superficial cancer: a regenerative medicine approach with a biologic scaffold. Tissue Eng Part A 17, 1643, 2011.
28. Mase, V.J., Jr., Hsu, J.R., Wolf, S.E., Wenke, J.C., Baer, D.G., Owens, J., Badylak, S.F., and Walters, T.J. Clinical application of an acellular biologic scaffold for surgical repair of a large, traumatic quadriceps femoris muscle defect. Orthopedics 33, 511, 2011.
29. Faleris, J.A., Hernandez, R.M., Wetzel, D., Dodds, R., and Greenspan, D.C. In-vivo and in-vitro histological evaluation of two commercially available acellular dermal matrices. Hernia 15, 147, 2011.
30. Bejjani, G.K., and Zabramski, J. Safety and efficacy of the porcine small intestinal submucosa dural substitute: results of a prospective multicenter study and literature review. J Neurosurg 106, 1028, 2007.
31. Hoell, T., Hohaus, C., Huschak, G., Beier, A., and Meisel, H.J. Total dura substitute in the spine: double layer dural substitute made from polylactide layer and bovine pericardium. Acta Neurochir (Wien) 149, 1259, 2007.
32. Shah, A.R., Pearlman, A.N., O'Grady, K.M., Bhattacharyya, T.K., and Toriumi, D.M. Combined use of fibrin tissue adhesive and acellular dermis in dural repair. Am J Rhinol 21, 619, 2007.
33. Agrawal, V., Brown, B.N., Beattie, A.J., Gilbert, T.W., and Badylak, S.F. Evidence of innervation following extracellular matrix scaffold-mediated remodelling of muscular tissues. J Tissue Eng Regen Med 3, 590, 2009.
34. Karabekmez, F.E., Duymaz, A., and Moran, S.L. Early clinical outcomes with the use of decellularized nerve allograft for repair of sensory defects within the hand. Hand (NY) 4, 245, 2009.
35. Zhang, Y., He, Y., Bharadwaj, S., Hammam, N., Carnagey, K., Myers, R., Atala, A., and Van Dyke, M. Tissue-specific extracellular matrix coatings for the promotion of cell proliferation and maintenance of cell phenotype. Biomaterials 30, 4021, 2009.
36. Sellaro, T.L., Ranade, A., Faulk, D.M., McCabe, G.P., Dorko, K., Badylak, S.F., and Strom, S.C. Maintenance of human hepatocyte function in vitro by liver-derived extracellular matrix gels. Tissue Eng Part A 16, 1075, 2010.
37. Ott, H.C., Clippinger, B., Conrad, C., Schuetz, C., Pomerantseva, I., Ikonomou, L., Kotton, D., and Vacanti, J.P. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med 16, 927, 2010.
38. Uygun, B.E., Soto-Gutierrez, A., Yagi, H., Izamis, M.L., Guzzardi, M.A., Shulman, C., Milwid, J., Kobayashi, N., Tilles, A., Berthiaume, F., Hertl, M., Nahmias, Y., Yarmush, M.L., and Uygun, K. Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix. Nat Med 16, 814, 2010.
39. Petersen, T.H., Calle, E.A., Zhao, L., Lee, E.J., Gui, L., Raredon, M.B., Gavrilov, K., Yi, T., Zhuang, Z.W., Breuer, C., Herzog, E., and Niklason, L.E. Tissue-engineered lungs for in vivo implantation. Science 329, 538, 2010.
40. Ott, H.C., Matthiesen, T.S., Goh, S.K., Black, L.D., Kren, S.M., Netoff, T.I., and Taylor, D.A. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 14, 213, 2008.
41. Freytes, D.O., Badylak, S.F., Webster, T.J., Geddes, L.A., and Rundell, A.E. Biaxial strength of multilaminated extracellular matrix scaffolds. Biomaterials 25, 2353, 2004.
42. Donato, R., Miljan, E.A., Hines, S.J., Aouabdi, S., Pollock, K., Patel, S., Edwards, F.A., and Sinden, J.D. Differential development of neuronal physiological responsiveness in two human neural stem cell lines. BMC Neurosci 8, 36, 2007.
43. Pollock, K., Stroemer, P., Patel, S., Stevanato, L., Hope, A., Miljan, E., Dong, Z., Hodges, H., Price, J., and Sinden, J.D. A conditionally immortal clonal stem cell line from human cortical neuroepithelium for the treatment of ischemic stroke. Exp Neurol 199, 143, 2006.
44. Crisan, M., Yap, S., Casteilla, L., Chen, C.W., Corselli, M., Park, T.S., Andriolo, G., Sun, B., Zheng, B., Zhang, L., Norotte, C., Teng, P.N., Traas, J., Schugar, R., Deasy, B.M., Badylak, S., Buhring, H.J., Giacobino, J.P., Lazzari, L., Huard, J., and Peault, B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3, 301, 2008.
45. Mack, G.S. ReNeuron and StemCells get green light for neural stem cell trials. Nat Biotechnol 29, 95, 2011.
46. Hofstetter, C.P., Holmstrom, N.A., Lilja, J.A., Schweinhardt, P., Hao, J., Spenger, C., Wiesenfeld-Hallin, Z., Kurpad, S.N., Frisen, J., and Olson, L. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat Neurosci 8, 346, 2005.
47. Sharp, K.G., Dickson, A.R., Marchenko, S.A., Yee, K.M., Emery, P.N., Laidmae, I., Uibo, R., Sawyer, E.S., Steward, O., and Flanagan, L.A. Salmon fibrin treatment of spinal cord injury promotes functional recovery and density of serotonergic innervation. Exp Neurol 235, 345, 2012.
48. Adams, R.A., Bauer, J., Flick, M.J., Sikorski, S.L., Nuriel, T., Lassmann, H., Degen, J.L., and Akassoglou, K. The fibrinderived gamma377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J Exp Med 204, 571, 2007.
49. Tottey, S., Corselli, M., Jeffries, E.M., Londono, R., Peault, B., and Badylak, S.F. Extracellular matrix degradation products and low-oxygen conditions enhance the regenerative potential of perivascular stem cells. Tissue Eng Part A 17, 37, 2011.
50. Tottey, S., Johnson, S.A., Crapo, P.M., Reing, J.E., Zhang, L., Jiang, H., Medberry, C.J., Reines, B., and Badylak, S.F. The effect of source animal age upon extracellular matrix scaffold properties. Biomaterials 32, 128, 2011.
51. Douet, V., Kerever, A., Arikawa-Hirasawa, E., and Mercier, F. Fractone-heparan sulphates mediate FGF-2 stimulation of cell proliferation in the adult subventricular zone. Cell Prolif 46, 137, 2013.
52. Preston, M., and Sherman, L.S. Neural stem cell niches: roles for the hyaluronan-based extracellular matrix. Front Biosci (Schol Ed) 3, 1165, 2011.
53. Purushothaman, A., Sugahara, K., and Faissner, A. Chondroitin sulfate "wobble motifs" modulate maintenance and differentiation of neural stem cells and their progeny. J Biol Chem 287, 2935, 2012.
54. Herculano-Houzel, S., Collins, C.E., Wong, P., and Kaas, J.H. Cellular scaling rules for primate brains. Proc Natl Acad Sci U S A 104, 3562, 2007.
55. Herculano-Houzel, S., Mota, B., and Lent, R. Cellular scaling rules for rodent brains. Proc Natl Acad Sci U S A 103, 12138, 2006.
56. Jehee, J.F., and Murre, J.M. The scalable mammalian brain: emergent distributions of glia and neurons. Biol Cybern 98, 439, 2008.
57. Azevedo, F.A., Carvalho, L.R., Grinberg, L.T., Farfel, J.M., Ferretti, R.E., Leite, R.E., Jacob Filho, W., Lent, R., and Herculano-Houzel, S. Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol 513, 532, 2009.
58. Beattie, A.J., Gilbert, T.W., Guyot, J.P., Yates, A.J., and Badylak, S.F. Chemoattraction of progenitor cells by remodeling extracellular matrix scaffolds. Tissue Eng 5, 1119, 2009.
59. Agrawal, V., Tottey, S., Johnson, S.A., Freund, J.M., Siu, B.F., and Badylak, S.F. Recruitment of progenitor cells by an extracellular matrix cryptic peptide in a mouse model of digit amputation. Tissue Eng Part A 17, 2435, 2011.
60. Agrawal, V., Kelly, J., Tottey, S., Daly, K.A., Johnson, S.A., Siu, B.F., Reing, J., and Badylak, S.F. An isolated cryptic Peptide influences osteogenesis and bone remodeling in an adult Mammalian model of digit amputation. Tissue Eng Part A 17, 3033, 2011.
61. O'Reilly, M.S., Holmgren, L., Shing, Y., Chen, C., Rosenthal, R.A., Moses, M., Lane, W.S., Cao, Y., Sage, E.H., and Folkman, J. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79, 315, 1994.
62. Harder, J., Bartels, J., Christophers, E., and Schroder, J.M. Isolation and characterization of human beta -defensin-3, a novel human inducible peptide antibiotic. J Biol Chem 276, 5707, 2001.