In vitro study of axonal migration and myelination of motor neurons in a three-dimensional tissue-engineered model

GLIA

Volumn 56, Issue 3, 2008, Pages 354-364

  Gingras, Marie ^a,b   Beaulieu, Marie Michèle ^a,b   Gagnon, Vicky ^a,b   Durham, Heather D ^c   Berthod, François ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Axon guidance; Biomaterial; Nerve regeneration; Peripheral nervous system; Schwann cells

Indexed keywords

MYELIN BASIC PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL SURVIVAL; COMPUTER MODEL; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; FIBROBLAST; IN VITRO STUDY; MOTOR NERVE; MOTOR NEURON DISEASE; MOUSE; MYELINATION; NERVE FIBER GROWTH; NERVE REGENERATION; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; SCHWANN CELL; SPINAL CORD MOTONEURON; TISSUE ENGINEERING;

EID: 38349098232     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20617     Document Type: Article

References (72)

1. Acheson A, Barker PA, Alderson RF, Miller FD, Murphy RA. 1991. Detection of brain-derived neurotrophic factor-like activity in fibroblasts and Schwann cells: Inhibition by antibodies to NGF. Neuron 7:265-275.
2. Arakawa Y, Sendtner M, Thoenen H. 1990. Survival effect of ciliary neurotrophic factor (CNTF) on chick embryonic motoneurons in culture: Comparison with other neurotrophic factors and cytokines. J Neurosci 10:3507-3515.
3. Arce V, Garces A, de Bovis B, Filippi P, Henderson C, Pettmann B, deLapeyriere O. 1999. Cardiotrophin-1 requires LIFRβ to promote survival of mouse motoneurons purified by a novel technique. J Neurosci Res 55:119-126.
4. Avossa D, Grandolfo M, Mazzarol F, Zatta M, Ballerini L. 2006. Early signs of motoneuron vulnerability in a disease model system: Characterization of transverse slice cultures of spinal cord isolated from embryonic ALS mice. Neuroscience 138:1179-1194.
5. Bearden SE, Segal SS. 2004. Microvessels promote motor nerve survival and regeneration through local VEGF release following ectopic reattachment. Microcirculation 11:633-644.
6. Becker E, Soler RM, Yuste VJ, Gine E, Sanz-Rodriguez C, Egea J, Martin-Zanca D, Comella JX. 1998. Development of survival responsiveness to brain-derived neurotrophic factor, neurotrophin 3 and neurotrophin 4/5, but not to nerve growth factor, in cultured motoneurons from chick embryo spinal cord. J Neurosci 18:7903-7911.
7. Berthod F, Germain L, Tremblay N, Auger FA. 2006. Extracellular matrix deposition by fibroblasts is necessary to promote capillary-like tube formation in vitro. J Cell Physiol 207:491-498.
8. Berthod F, Hayek D, Damour O, Collombel C. 1993. Collagen synthesis by fibroblasts cultured within a collagen sponge. Biomaterials 14:749-754.
9. Berthod F, Sahuc F, Hayek D, Damour O, Collombel C. 1996. Deposition of collagen fibril bundles by long-term culture of fibroblasts in a collagen sponge. J Biomed Mater Res 32:87-94.
10. Berthod F, Saintigny G, Chretien F, Hayek D, Collombel C, Damour O. 1994. Optimization of thickness, pore size and mechanical properties of a biomaterial designed for deep burn coverage. Clin Mater 15:259-265.
11. Bixby JL, Lilien J, Reichardt LF. 1988. Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. J Cell Biol 107:353-361.
12. Bohn MC. 2004. Motoneurons crave glial cell line-derived neurotrophic factor. Exp Neurol 190:263-275.
13. Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW. 2006. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312:1389-1392.
14. Braun S, Croizat B, Lagrange MC, Warter JM, Poindron P. 1996. Neurotrophins increase motoneurons' ability to innervate skeletal muscle fibers in rat spinal cord-human muscle cocultures. J Neurol Sci 136:17-23.
15. Bridge PM, Ball DJ, Mackinnon SE, Nakao Y, Brandt K, Hunter DA, Hertl C. 1994. Nerve crush injuries - A model for axonotmesis. Exp Neurol 127:284-290.
16. Bruijn LI, Miller TM, Cleveland DW. 2004. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu Rev Neurosci 27:723-749.
17. Bunge RP, Bunge MB, Bates M. 1989. Movements of the Schwann cell nucleus implicate progression of the inner (axon-related) Schwann cell process during myelination. J Cell Biol 109:273-284.
18. Caissie R, Gingras M, Champigny MF, Berthod F. 2006. In vivo enhancement of sensory perception recovery in a tissue-engineered skin enriched with laminin. Biomaterials 27:2988-2993.
19. Carden MJ, Trojanowski JQ, Schlaepfer WW, Lee VM. 1987. Two-stage expression of neurofilament polypeptides during rat neurogenesis with early establishment of adult phosphorylation patterns. J Neurosci 7:3489-3504.
20. Clark EA, Lee VM. 1991. Dynamics of mammalian high-molecular-weight neurofilament subunit phosphorylation in cultured rat sympathetic neurons. J Neurosci Res 30:116-123.
21. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, Rule M, McMahon AP, Doucette W, Siwek D, Ferrante RJ, Brown RH, JR, Julien JP, Goldstein LS, Cleveland DW. 2003. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302:113-117.
22. Coppe JP, Kauser K, Campisi J, Beausejour CM. 2006. Secretion of vascular endothelial growth factor by primary human fibroblasts at senescence. J Biol Chem 281:29568-29574.
23. Cullheim S, Carlstedt T, Risling M. 1999. Axon regeneration of spinal motoneurons following a lesion at the cord-ventral root interface. Spinal Cord 37:811-819.
24. D'Mello SR, Jiang C, Lamberti C, Martin SC, Heinrich G. 1992. Differential regulation of the nerve growth factor and brain-derived neurotrophic factor genes in L929 mouse fibroblasts. J Neurosci Res 33:519-526.
25. da Silva CF, Madison R, Dikkes P, Chiu TH, Sidman RL. 1985. An in vivo model to quantify motor and sensory peripheral nerve regeneration using bioresorbable nerve guide tubes. Brain Res 342:307-315.
26. Elliott JL. 1999. Experimental models of amyotrophic lateral sclerosis. Neurobiol Dis 6:310-320.
27. Germain L, Rouabhia M, Guignard R, Carrier L, Bouvard V, Auger FA. 1993. Improvement of human keratinocyte isolation and culture using thermolysin. Burns 19:99-104.
28. Gingras M, Bergeron J, Dery J, Durham HD, Berthod F. 2003. In vitro development of a tissue-engineered model of peripheral nerve regeneration to study neurite growth. FASEB J 17:2124-2126.
29. Gingras M, Gagnon V, Minotti S, Durham HD, Berthod F. 2007. Optimized protocols for isolation of primary motor neurons, astrocytes and microglia from embryonic mouse spinal cord. J Neurosci Methods 163:111-118.
30. Goodman CS. 1996. Mechanisms and molecules that control growth cone guidance. Annu Rev Neurosci 19:341-377.
31. Greensmith L, Vrbova G. 1997. Disturbances of neuromuscular interaction may contribute to muscle weakness in spinal muscular atrophy. Neuromuscul Disord 7:369-372.
32. Griffin JW, Sheikh K. 1999. Schwann cell-axon interactions in Charcot-Marie-Tooth disease. Ann N Y Acad Sci 883:77-90.
33. Guettier-Sigrist S, Coupin G, Braun S, Rogovitz D, Courdier I, Warter JM, Poindron P. 2001. On the possible role of muscle in the pathogenesis of spinal muscular atrophy. Fundam Clin Pharmacol 15:31-40.
34. Hanson MG Jr, Shen S, Wiemelt AP, McMorris FA, Barres BA. 1998. Cyclic AMP elevation is sufficient to promote the survival of spinal motor neurons in vitro. J Neurosci 18:7361-7371.
35. Koliatsos VE, Clatterbuck RE, Winslow JW, Cayouette MH, Price DL. 1993. Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron 10:359-367.
36. Komiyama T, Nakao Y, Toyama Y, Asou H, Vacanti CA, Vacanti MP. 2003. A novel technique to isolate adult Schwann cells for an artificial nerve conduit. J Neurosci Methods 122:195-200.
37. Kreider B, Zeller N, Lazzarini R, Shuman S, Pleasure D. 1988. Regulation of myelin P0 glycoprotein synthesis in cultured rat Schwann cells and continuous rat PNS cell lines. J Neurochem 51:566-571.
38. Lariviere RC, Julien JP. 2004. Functions of intermediate filaments in neuronal development and disease. J Neurobiol 58:131-148.
39. Lee HJ, Elliot GJ, Hammond DN, Lee VM, Wainer BH. 1991. Constitutive expression of the mature array of neurofilament proteins by a CNS neuronal cell line. Brain Res 558:197-208.
40. Maggi SP, Lowe JB III, Mackinnon SE. 2003. Pathophysiology of nerve injury. Clin Plast Surg 30:109-126.
41. Maier M, Berger P, Suter U. 2002. Understanding Schwann cell-neurone interactions: The key to Charcot-Marie-Tooth disease? J Anat 200:357-366.
42. Maki Y, Yoshizu T, Tsubokawa N. 2005. Selective regeneration of motor and sensory axons in an experimental peripheral nerve model without endorgans. Scand J Plast Reconstr Surg Hand Surg 39:257-260.
43. Maragakis NJ, Jackson M, Ganel R, Rothstein JD. 2003. Topiramate protects against motor neuron degeneration in organotypic spinal cord cultures but not in G93A SOD1 transgenic mice. Neurosci Lett 338:107-110.
44. Martini R, Carenini S. 1998. Formation and maintenance of the myelin sheath in the peripheral nerve: Roles of cell adhesion molecules and the gap junction protein connexin 32. Microsc Res Tech 41:403-415.
45. Martini R, Schachner M. 1986. Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and MAG) and their shared carbohydrate epitope and myelin basic protein in developing sciatic nerve. J Cell Biol 103 (6 Part 1):2439-2448.
46. Martini R, Schachner M. 1997. Molecular bases of myelin formation as revealed by investigations on mice deficient in glial cell surface molecules. Glia 19:298-310.
47. Monani UR. 2005. Spinal muscular atrophy: A deficiency in a ubiquitous protein; a motor neuron-specific disease. Neuron 48:885-896.
48. Oppenheim RW. 1996. Neurotrophic survival molecules for motoneurons: An embarrassment of riches. Neuron 17:195-197.
49. Oppenheim RW, Yin QW, Prevette D, Yan Q. 1992. Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature 360:755-757.
50. Padilla F, Marc Mege R, Sobel A, Nicolet M. 1999. Upregulation and redistribution of cadherins reveal specific glial and muscle cell phenotypes during wallerian degeneration and muscle denervation in the mouse. J Neurosci Res 58:270-283.
51. Patapoutian A, Backus C, Kispert A, Reichardt LF. 1999. Regulation of neurotrophin-3 expression by epithelial-mesenchymal interactions: The role of Wnt factors. Science 283:1180-1183.
52. Rakowicz WP, Staples CS, Milbrandt J, Brunstrom JE, Johnson EM Jr. 2002. Glial cell line-derived neurotrophic factor promotes the survival of early postnatal spinal motor neurons in the lateral and medial motor columns in slice culture. J Neurosci 22:3953-3962.
53. Robinson GA, Madison RD. 2006. Developmentally regulated changes in femoral nerve regeneration in the mouse and rat. Exp Neurol 197:341-346.
54. Schecterson LC, Bothwell M. 1992. Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9:449-463.
55. Sendtner M. 2001. Molecular mechanisms in spinal muscular atrophy: Models and perspectives. Curr Opin Neurol 14:629-634.
56. Sendtner M, Arakawa Y, Stockli KA, Kreutzberg GW, Thoenen H. 1991. Effect of ciliary neurotrophic factor (CNTF) on motoneuron survival. J Cell Sci Suppl 15:103-109.
57. Sendtner M, Holtmann B, Kolbeck R, Thoenen H, Barde YA. 1992. Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section. Nature 360:757-759.
58. Sherman DL, Brophy PJ. 2005. Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6:683-690.
59. Shy ME. 2004. Charcot-Marie-Tooth disease: An update. Curr Opin Neurol 17:579-585.
60. Sondell M, Lundborg G, Kanje M. 1999. Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci 19:5731-5740.
61. Stoll G, Muller HW. 1999. Nerve injury, axonal degeneration and neural regeneration: Basic insights. Brain Pathol 9:313-325.
62. Sugihara T, Kaul SC, Mitsui Y, Wadhwa R. 1994. Enhanced expression of multiple forms of VEGF is associated with spontaneous immortalization of murine fibroblasts. Biochim Biophys Acta 1224:365-370.
63. Tanaka Y, Hirokawa N. 2002. Mouse models of Charcot-Marie-Tooth disease. Trends Genet 18:S39-S44.
64. Terenghi G. 1999. Peripheral nerve regeneration and neurotrophic factors. J Anat 194 (Part 1):1-14.
65. Tessier-Lavigne M, Goodman CS. 1996. The molecular biology of axon guidance. Science 274:1123-1133.
66. Tomaselli KJ, Reichardt LF. 1988. Peripheral motoneuron interactions with laminin and Schwann cell-derived neurite-promoting molecules: Developmental regulation of laminin receptor function. J Neurosci Res 21:275-285.
67. Trupp M, Ryden M, Jornvall H, Funakoshi H, Timmusk T, Arenas E, Ibanez CF. 1995. Peripheral expression and biological activities of GDNF, a new neurotrophic factor for avian and mammalian peripheral neurons. J Cell Biol 130:137-148.
68. Urushitani M, Sik A, Sakurai T, Nukina N, Takahashi R, Julien JP. 2006. Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat Neurosci 9:108-118.
69. Willard M, Simon C. 1983. Modulations of neurofilament axonal transport during the development of rabbit retinal ganglion cells. Cell 35 (2 Part 1):551-559.
70. Wood SJ, Pritchard J, Sofroniew MV. 1990. Re-expression of nerve growth factor receptor after axonal injury recapitulates a developmental event in motor neurons: Differential regulation when regeneration is allowed or prevented. Eur J Neurosci 2:650-657.
71. Yan Q, Elliott J, Snider WD. 1992. Brain-derived neurotrophic factor rescues spinal motor neurons from axotomy-induced cell death. Nature 360:753-755.
72. Zorick TS, Lemke G. 1996. Schwann cell differentiation. Curr Opin Cell Biol 8:870-876.