Thick collagen-based 3D matrices including growth factors to induce neurite outgrowth

Acta Biomaterialia

Volumn 8, Issue 9, 2012, Pages 3302-3312

  Labour, M N ^a,b,c   Banc, A ^a,b   Tourrette, A ^a,b   Cunin, F ^b   Verdier, J M ^a,c   Devoisselle, J M ^b   Marcilhac, A ^a,c   Belamie, E ^a,b  

^a PSL RESEARCH UNIVERSITY   (France)

^b INSTITUT CHARLES GERHARDT   (France)

^c University of Montpellier   (France)

Author keywords

3D scaffold; Compartmentation; Coupling; Growth factor; Neurite outgrowth

Indexed keywords

COLLAGEN; CROSSLINKING; CYTOLOGY; MOLECULAR BIOLOGY; SCAFFOLDS (BIOLOGY);

3D SCAFFOLDS; ACTIVE AREA; CELL BIOLOGY; CELLULARS; COMPARTMENTATION; GROWTH FACTOR; MATRIX; MICROENVIRONMENTS; NEURAL CELLS; NEURITE OUTGROWTH;

CELLS;

BRAIN DERIVED NEUROTROPHIC FACTOR; COLLAGEN TYPE 1; GLASS; NERVE GROWTH FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALIBRATION; CELL DIFFERENTIATION; CELL LINE; CELL STRAIN; CELL TYPE; CONFOCAL MICROSCOPY; CONJUGATION; HUMAN; HUMAN CELL; NERVE CELL; NERVE FIBER GROWTH; NEURITE; NONHUMAN; PRIORITY JOURNAL; RAT; SCANNING ELECTRON MICROSCOPY;

EID: 84864413380     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2012.05.015     Document Type: Article

References (74)

1. M.P. Lutolf, P.M. Gilbert, and H.M. Blau Designing materials to direct stem-cell fate Nature 462 2009 433 441
2. R. Perez-Castillejos Replication of the 3D architecture of tissues Mater Today 13 2010 32 41
3. B.L. MacInnis, and R.B. Campenot Retrograde support of neuronal survival without retrograde transport of nerve growth factor Science 295 2002 1536 1539 (Pubitemid 34174011)
4. R.B. Campenot, and B.L. MacInnis Retrograde transport of neurotrophins: fact and function J Neurobiol 58 2004 217 229 (Pubitemid 38173720)
5. M.S. Song, and L. Saavedra Posse de Chaves EI. Apoptosis is secondary to non-apoptotic axonal degeneration in neurons exposed to Aβ in distal axons Neurobiol Aging 27 2006 1224 1238 (Pubitemid 44088575)
6. D.H. Kim, H. Lee, Y.K. Lee, J.M. Nam, and A. Levchenko Biomimetic nanopatterns as enabling tools for analysis and control of live cells Adv Mater 22 2010 4551 4566
7. W.J. Rosoff, R. McAllister, M.A. Esrick, G.J. Goodhill, and J.S. Urbach Generating controlled molecular gradients in 3D gels Biotechnol Bioeng 91 2005 754 759 (Pubitemid 41283868)
8. X. Cao, and M.S. Shoichet Defining the concentration gradient of nerve growth factor for guided neurite outgrowth Neuroscience 103 2001 831 840 (Pubitemid 32239344)
9. N. Gomez, Y. Lu, S. Chen, and C.E. Schmidt Immobilized nerve growth factor and microtopography have distinct effects on polarization versus axon elongation in hippocampal cells in culture Biomaterials 28 2007 271 284 (Pubitemid 44537382)
10. C.K. Yeung, L. Lauer, A. Offenhäusser, and W. Knoll Modulation of the growth and guidance of rat brain stem neurons using patterned extracellular matrix proteins Neurosci Lett 301 2001 147 150 (Pubitemid 32206707)
11. G.J. Liu WW, N.L. Jeon, and L.W. Enquist A microfluidic chamber for analysis of neuron-to-cell spread and axonal transport of an alpha-herpesvirus PLoS ONE 2008
12. S.L. Bechara, A. Judson, and K.C. Popat Template synthesized poly(epsilon-caprolactone) nanowire surfaces for neural tissue engineering Biomaterials 31 2010 3492 3501
13. R.B. Campenot Local control of neurite development by nerve growth factor Proc Natl Acad Sci 74 1977 4516 4519 (Pubitemid 8225155)
14. M.W. Hayman, K.H. Smith, N.R. Cameron, and S.A. Przyborski Enhanced neurite outgrowth by human neurons grown on solid three-dimensional scaffolds Biochem Biophys Res Commun 314 2004 483 488 (Pubitemid 38084743)
15. C.A. Brayfield, K.G. Marra, J.P. Leonard, X. Tracy Cui, and J.C. Gerlach Excimer laser channel creation in polyethersulfone hollow fibers for compartmentalized in vitro neuronal cell culture scaffolds Acta Biomater 4 2008 244 255 (Pubitemid 351218105)
16. A.M. Taylor, S.W. Rhee, C.H. Tu, D.H. Cribbs, C.W. Cotman, and N.L. Jeon Microfluidic multicompartment device for neuroscience research Langmuir 19 2002 1551 1556
17. A.M. Taylor, M. Blurton-Jones, S.W. Rhee, D.H. Cribbs, C.W. Cotman, and N.L. Jeon A microfluidic culture platform for CNS axonal injury, regeneration and transport Nat Methods 2 2005 599 605 (Pubitemid 41086851)
18. A.M. Taylor, D.C. Dieterich, H.T. Ito, S.A. Kim, and E.M. Schuman Microfluidic local perfusion chambers for the visualization and manipulation of synapses Neuron 66 2010 57 68
19. M.S. Cohen, C.B. Orth, H.J. Kim, N.L. Jeon, and S.R. Jaffrey Neurotrophin-mediated dendrite-to-nucleus signaling revealed by microfluidic compartmentalization of dendrites Proc Natl Acad Sci 108 2011 11246 11251
20. E. Torre, and O. Steward Demonstration of local protein synthesis within dendrites using a new cell culture system that permits the isolation of living axons and dendrites from their cell bodies J Neurosci 12 1992 762 772
21. M. Nakajima, T. Ishimuro, K. Kato, I.K. Ko, I. Hirata, and Y. Arima Combinatorial protein display for the cell-based screening of biomaterials that direct neural stem cell differentiation Biomaterials 28 2007 1048 1060 (Pubitemid 44809416)
22. A. Singh, and J. Elisseeff Biomaterials for stem cell differentiation J Mater Chem 20 2010 8832
23. A. Engler, L. Bacakova, C. Newman, A. Hategan, M. Griffin, and D. Discher Substrate compliance versus ligand density in cell on gel responses Biophys J 86 2004 617 628 (Pubitemid 38067491)
24. L. Besseau, B. Coulomb, C. Lebreton-Decoster, and M.-M. Giraud-Guille Production of ordered collagen matrices for three-dimensional cell culture Biomaterials 23 2001 27 36
25. C. Helary, L. Ovtracht, B. Coulomb, G. Godeau, and M.M. Giraud-Guille Dense fibrillar collagen matrices: a model to study myofibroblast behavior during wound healing Biomaterials 27 2006 4443 4452 (Pubitemid 43732455)
26. S. Vigier, C. Helary, O. Fromigué, P.J. Marie, and M.-M. Giraud-Guille Dense fibrillar collagen matrices and sponges for bone repair. Comparative study of structure and long-term culture of a human osteoblast cell line J Biomed Mater Res 94 2010 556 567
27. L.A. Flanagan, Y.E. Ju, B. Marg, M. Osterfield, and P.A. Janmey Neurite branching on deformable substrates Neuroreport 13 2002 2411 2415 (Pubitemid 36143534)
28. E. Bell, B. Ivarsson, and C. Merrill Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro Proc Natl Acad Sci USA 76 1979 1274 1278 (Pubitemid 9143722)
29. A. Banerjee, M. Arha, S. Choudhary, R.S. Ashton, S.R. Bhatia, and D.V. Schaffer The influence of hydrogel modulus on the proliferation and differentiation of encapsulated neural stem cells Biomaterials 30 2009 4695 4699
30. K. Brannvall, K. Bergman, U. Wallenquist, S. Svahn, T. Bowden, and J. Hilborn Enhanced neuronal differentiation in a three-dimensional collagen-hyaluronan matrix J Neurosci Res 85 2007 2138 2146 (Pubitemid 47172145)
31. J. Lee, M.J. Cuddihy, and N.A. Kotov Three-dimensional cell culture matrices: state of the art Tissue Eng Part B Rev 14 2008 61 86
32. W. Ma, T. Tavakoli, S. Chen, D. Maric, J.L. Liu, and T.J. O'Shaughnessy Reconstruction of functional cortical-like tissues from neural stem and progenitor cells Tissue Eng Part A 14 2008 1673 1686
33. S.C. Owen, and M.S. Shoichet Design of three-dimensional biomimetic scaffolds J Biomed Mater Res A 94 2010 1321 1331
34. L.A. Greene, and A.S. Tischler Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor Proc Natl Acad Sci 73 1976 2424 2428
35. J.L. Biedler, S. Roffler-Tarlov, M. Schachner, and L.S. Freedman Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones Cancer Res 38 1978 3751 3757 (Pubitemid 9045201)
36. F. Gobeaux, G. Mosser, A. Anglo, P. Panine, P. Davidson, and M.M. Giraud-Guille Fibrillogenesis in dense collagen solutions: a physicochemical study J Mol Biol 376 2008 1509 1522
37. I. Bergman, and R. Loxley Two improved and simplified methods for the spectrophotometric determination of hydroxyproline Anal Chem 35 1963 1961 1965
38. T. Buffeteau, B. Desbat, and J.M. Turlet Polarization modulation FT-IR spectroscopy of surfaces and ultra-thin films - experimental procedure and quantitative analysis Appl Spectrosc 45 1991 380 389
39. D. Blaudez, J.M. Turlet, J. Dufourcq, T. Buffeteau, and B. Desbat Investigation at the air/water interface using polarization modulation IR spectroscopy J chem Soc Faraday Trans 92 1996 525 530 (Pubitemid 126836712)
40. B. Brodsky Doyle, E.G. Bendit, and E.R. Blout Infrared spectroscopy of collagen and collagen-like polypeptides Biopolymers 14 1975 937 957
41. B. Brodsky, and J.A.M. Ramshaw The collagen triple-helix structure Matrix Biol 15 1997 545 554 (Pubitemid 27190029)
42. L. Besseau, B. Coulomb, C. Lebreton-Decoster, and M.M. Giraud-Guille Production of ordered collagen matrices for three-dimensional cell culture Biomaterials 23 2002 27 36 (Pubitemid 33041338)
43. D.L. Christiansen, E.K. Huang, and F.H. Silver Assembly of type I collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties Matrix Biol 19 2000 409 420
44. M.T. Sheu, J.C. Huang, G.C. Yeh, and H.O. Ho Characterization of collagen gel solutions and collagen matrices for cell culture Biomaterials 22 2001 1713 1719
45. D.K. Fujii, S.L. Massoglia, N. Savion, and D. Gospodarowicz Neurite outgrowth and protein synthesis by PC12 cells as a function of substratum and nerve growth factor J Neurosci 2 1982 1157 1175 (Pubitemid 13252043)
46. L. Greene Nerve growth factor prevents the death and stimulates the neuronal differentiation of clonal PC12 pheochromocytoma cells in serum-free medium J Cell Biol 78 1978 747 755 (Pubitemid 9007417)
47. C.E. Beaty, and W.M. Saltzman Controlled growth factor delivery induces differential neurite outgrowth in three-dimensional cell cultures Anglais 24 1993 15 23 (Pubitemid 23161318)
48. S.M. Willerth, P.J. Johnson, D.J. Maxwell, S.R. Parsons, M.E. Doukas, and S.E. Sakiyama-Elbert Rationally designed peptides for controlled release of nerve growth factor from fibrin matrices J Biomed Mater Res A 80 2007 13 23 (Pubitemid 44913329)
49. S. Doleski, L. Yao, A. Pandit, and C. Elvira NGF release from thermo-responsive collagen-poly NIPAam polymer networks supports neuronal cell growth and differentiation J Biomed Mater Res A 94 2010 457 465
50. S.H. Bhang, T.J. Lee, J.M. Lim, J.S. Lim, A.M. Han, and C.Y. Choi The effect of the controlled release of nerve growth factor from collagen gel on the efficiency of neural cell culture Biomaterials 30 2009 126 132
51. W. Sun, H. Lin, B. Chen, W. Zhao, Y. Zhao, and Z. Xiao Collagen scaffolds loaded with collagen-binding NGF-beta accelerate ulcer healing J Biomed Mater Res A 92 2010 887 895
52. A. Al Ahmad, B. Lee, J. Stack, C. Parham, J. Campbell, and D. Clarke Endostatin binds nerve growth factor and thereby inhibits neurite outgrowth and neuronal migration in-vitro Brain Res 1360 2010 28 39
53. C.B. Nguyen, É. Szönyi, M.D. Sadick, T.E. Hotaling, J.-L. Mendoza-Ramirez, and E. Escandón Stability and interactions of recombinant human nerve growth factor in different biological matrices: in vitro and in vivo studies Drug Metab Dispos 28 2000 590 597 (Pubitemid 30238520)
54. I. Katzir, J. Shani, K. Regev, D. Shabashov, and P. Lazarovici A quantitative bioassay for nerve growth factor, using PC12 clones expressing different levels of trkA receptors J Mol Neurosci 18 2002 251 264 (Pubitemid 34569416)
55. J. Schimmelpfeng, K.F. Weibezahn, and H. Dertinger Quantification of NGF-dependent neuronal differentiation of PC-12 cells by means of neurofilament-L mRNA expression and neuronal outgrowth J Neurosci Methods 139 2004 299 306 (Pubitemid 39370856)
56. T.A. Kapur, and M.S. Shoichet Immobilized concentration gradients of nerve growth factor guide neurite outgrowth J Biomed Mater Res Part A 68A 2004 235 243 (Pubitemid 38524717)
57. Y.H. Shen, M.S. Shoichet, and M. Radisic Vascular endothelial growth factor immobilized in collagen scaffold promotes penetration and proliferation of endothelial cells Acta Biomater 4 2008 477 489
58. M.J.B. Wissink, R. Beernink, J.S. Pieper, A.A. Poot, G.H.M. Engbers, and T. Beugeling Immobilization of heparin to EDC/NHS-crosslinked collagen. Characterization and in vitro evaluation Biomaterials 22 2001 151 163
59. L.M. Yu, F.D. Miller, and M.S. Shoichet The use of immobilized neurotrophins to support neuron survival and guide nerve fiber growth in compartmentalized chambers Biomaterials 31 2010 6987 6999
60. T.L. Pohl, J.H. Boergermann, G.K. Schwaerzer, P. Knaus, and E.A. Cavalcanti-Adam Surface immobilization of bone morphogenetic protein 2 via a self-assembled monolayer formation induces cell differentiation Acta Biomater 2011
61. A. Minato, H. Ise, M. Goto, and T. Akaike Cardiac differentiation of embryonic stem cells by substrate immobilization of insulin-like growth factor binding protein 4 with elastin-like polypeptides Biomaterials 33 2012 515 523
62. X. Cao, and M.S. Shoichet Investigating the synergistic effect of combined neurotrophic factor concentration gradients to guide axonal growth Neuroscience 122 2003 381 389 (Pubitemid 37410168)
63. J. Mai, L. Fok, H. Gao, X. Zhang, and M.M. Poo Axon initiation and growth cone turning on bound protein gradients J Neurosci 29 2009 7450 7458
64. D. Paris, D. Beaulieu-Abdelahad, C. Bachmeier, J. Reed, G. Ait-Ghezala, and A. Bishop Anatabine lowers Alzheimer's Abeta production in vitro and in vivo Eur J Pharmacol 2011
65. C.-Y. Wang, T. Wang, W. Zheng, B.-L. Zhao, G. Danscher, and Y.-H. Chen Zinc overload enhances app cleavage and aβ deposition in the Alzheimer mouse brain PLoS ONE 5 2010 e15349
66. W.J. Callahan, L.O. Narhi, A.A. Kosky, and M.J. Treuheit Sodium chloride enhances the storage and conformational stability of BDNF and PEG-BDNF Pharm Res 18 2001 261 266 (Pubitemid 32595811)
67. M. Encinas, M. Iglesias, N. Llecha, and J.X. Comella Extracellular- regulated kinases and phosphatidylinositol 3-kinase are involved in brain-derived neurotrophic factor-mediated survival and neuritogenesis of the neuroblastoma cell line SH-SY5Y J Neurochem 73 1999 1409 1421 (Pubitemid 29440140)
68. M. Encinas, M. Iglesias, Y. Liu, H. Wang, A. Muhaisen, and V. Ceña Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells J Neurochem 75 2000 991 1003 (Pubitemid 30660487)
69. K. Matsumoto, R.K. Wada, J.M. Yamashiro, D.R. Kaplan, and C.J. Thiele Expression of brain-derived neurotrophic factor and p145TrkB affects survival, differentiation, and invasiveness of human neuroblastoma cells Cancer Res 55 1995 1798 1806
70. D.R. Kaplan, K. Matsumoto, E. Lucarelli, and C.J. Thielet Induction of TrkB by retinoic acid mediates biologic responsiveness to BDNF and differentiation of human neuroblastoma cells Neuron 11 1993 321 331 (Pubitemid 23250349)
71. S. Påhlman, A.-I. Ruusala, L. Abrahamsson, M.E.K. Mattsson, and T. Esscher Retinoic acid-induced differentiation of cultured human neuroblastoma cells: a comparison with phorbolester-induced differentiation Cell Differ 14 1984 135 144 (Pubitemid 14089031)
72. R.B. Knowles, C. Wyart, S.V. Buldyrev, L. Cruz, B. Urbanc, and M.E. Hasselmo Plaque-induced neurite abnormalities: implications for disruption of neural networks in Alzheimer's disease Proc Natl Acad Sci 96 1999 5274 5279 (Pubitemid 29214573)
73. T.C. Dickson, and J.C. Vickers The morphological phenotype of β-amyloid plaques and associated neuritic changes in Alzheimer's disease Neuroscience 105 2001 99 107 (Pubitemid 32722097)
74. C. Duyckaerts, B. Delatour, and M.C. Potier Classification and basic pathology of Alzheimer disease Acta Neuropathol 118 2009 5 36