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Peripheral Sensory Axon Growth: From Receptor Binding to Cellular Signaling

Published online by Cambridge University Press:  02 December 2014

Budd A. Tucker  and
Karen M. Mearow
Budd A. Tucker
Affiliation:
Department of Ophthalmology, Schepens Eye Research Institute, Harvard Medical School, Boston, MA, USA
Karen M. Mearow*
Affiliation:
Division of BioMedical Sciences, Memorial University of Newfoundland, St. John's, NL, Canada
*
Div BioMedical Sciences – M5352, Faculty of Medicine, Memorial University of Newfoundland, 300 Prince Philip Dr, St. John's, Newfoundland, A1B 3V6, Canada.
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Abstract

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Regeneration following axonal injury of the adult peripheral sensory nervous system is heavily influenced by factors located in a neuron's extracellular environment. These factors include neurotrophins, such as Nerve Growth Factor (NGF) and the extracellular matrix, such as laminin. The presence of these molecules in the peripheral nervous system (PNS) is a major contributing factor for the dichotomy between regenerative capacities of central vs. peripheral neurons. Although PNS neurons are capable of spontaneous regeneration, this response is critically dependent on many different factors including the type, location and severity of the injury. In this article, we will focus on the plasticity of adult dorsal root ganglion (DRG) sensory neurons and how trophic factors and the extracellular environment stimulate the activation of intracellular signaling cascades that promote axonal growth in adult dorsal root ganglion neurons.

Résumé:

RÉSUMÉ:

La régénérescence axonale suite à une lésion du système nerveux sensitif chez l'adulte est très influencée par des facteurs localisés dans l'environnement extracellulaire du neurone, dont les neurotropines comme le facteur de croissance nerveuse (NGF) et la matrice extracellulaire comme la laminine. La présence de ces molécules dans le système nerveux périphérique (SNP) est un facteur majeur contribuant à la dichotomie entre la capacité de régénérescence des neurones centraux et périphériques. Bien que les neurones du SNP soient capables de régénérescence spontanée, cette réponse est intimement dépendante de plusieurs facteurs différents, dont le type, la localisation et la sévérité de la lésion. Dans cet article nous traitons de la plasticité des neurones sensitifs du ganglion de la racine postérieure chez l'adulte et de la façon dont les facteurs trophiques et l'environnement extracellulaire stimulent l'activation des cascades de signalisation intracellulaire qui activent la croissance axonale dans les neurones des ganglions de la racine postérieure chez l'adulte.

Type
Review Article
Information
Canadian Journal of Neurological Sciences , Volume 35 , Issue 5 , November 2008 , pp. 551 - 566
Copyright
Copyright © The Canadian Journal of Neurological 2008

References

1. Meiners, S, Mercado, ML. Functional peptide sequences derived from extracellular matrix glycoproteins and their receptors: strategies to improve neuronal regeneration. Mol Neurobiol. 2003;27(2):177–96.Google Scholar
2. Nakamoto, T, Kain, KH, Ginsberg, MH. Neurobiology: new connections between integrins and axon guidance. Curr Biol. 2004;14(3):R121–3.CrossRefGoogle ScholarPubMed
3. Lemons, ML, Condic, ML. Integrin signaling is integral to regeneration. Exp Neurol. 2008;209:343–52.CrossRefGoogle ScholarPubMed
4. Hoke, A. Mechanisms of disease: what factors limit the success of peripheral nerve regeneration in humans? Nat Clin Pract Neurol. 2006;2(8):448–54.Google Scholar
5. Fenrich, K, Gordon, T. Canadian Association of Neuroscience review: axonal regeneration in the peripheral and central nervous systems-current issues and advances. Can J Neurol Sci. 2004;31(2):142–56.Google Scholar
6. Lundborg, G, Rosen, B. Hand function after nerve repair. Acta Physiol (Oxf). 2007;189(2):207–17.CrossRefGoogle ScholarPubMed
7. Navarro, X, Vivo, M, Valero-Cabre, A. Neural plasticity after peripheral nerve injury and regeneration. Prog Neurobiol. 2007;82(4):163–201.CrossRefGoogle ScholarPubMed
8. Aguayo, AJ, David, S, Bray, GM. Influences of the glial environment on the elongation of axons after injury: transplantation studies in adult rodents. J Exp Biol. 1981;95:231–40.CrossRefGoogle ScholarPubMed
9. Aguayo, AJ, Rasminsky, M, Bray, GM, Carbonetto, S, McKerracher, L, Villegas-Perez, MP, et al. Degenerative and regenerative responses of injured neurons in the central nervous system of adult mammals. Philos Trans R Soc Lond B Biol Sci. 1991;331(1261):337–43.Google Scholar
10. David, S, Aguayo, AJ. Axonal elongation into peripheral nervous system “bridges” after central nervous system injury in adult rats. Science. 1981;214(4523):931–3.CrossRefGoogle ScholarPubMed
11. Filbin, MT. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci. 2003;4(9): 703–13.Google Scholar
12. McKerracher, L, David, S, Jackson, DL, Kottis, V, Dunn, RJ, Braun, PE. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron. 1994;13(4): 805–11.CrossRefGoogle Scholar
13. Chen, MS, Huber, AB, van der Haar, ME, Frank, M, Schnell, L, Spillmann, AA, et al. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature. 2000;403(6768):434–9.Google Scholar
14. GrandPre, T, Nakamura, F, Vartanian, T, Strittmatter, SM. Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature. 2000;403(6768):439–44.CrossRefGoogle ScholarPubMed
15. Cafferty, WB, Yang, SH, Duffy, PJ, Li, S, Strittmatter, SM. Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J Neurosci. 2007;27(9):2176–85.Google Scholar
16. Galtrey, CM, Fawcett, JW. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev. 2007;54(1):1–18.CrossRefGoogle ScholarPubMed
17. Liu, BP, Cafferty, WB, Budel, SO, Strittmatter, SM. Extracellular regulators of axonal growth in the adult central nervous system. Philos Trans R Soc Lond B Biol Sci. 2006;361(1473):1593–610.CrossRefGoogle ScholarPubMed
18. Lemons, ML, Barua, S, Abanto, ML, Halfter, W, Condic, ML. Adaptation of sensory neurons to hyalectin and decorin proteoglycans. J Neurosci. 2005;25(20):4964–73.CrossRefGoogle ScholarPubMed
19. David, S, Braun, PE, Jackson, DL, Kottis, V, McKerracher, L. Laminin overrides the inhibitory effects of peripheral nervous system and central nervous system myelin-derived inhibitors of neurite growth. J Neurosci Res. 1995;42(4):594–602.Google Scholar
20. Grimpe, B, Silver, J. The extracellular matrix in axon regeneration. Prog Brain Res. 2002;137:333–49.CrossRefGoogle ScholarPubMed
21. Fu, SY, Gordon, T. The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol. 1997;14(1-2):67–116.CrossRefGoogle ScholarPubMed
22. McKerracher, L, Chamoux, M, Arregui, CO. Role of laminin and integrin interactions in growth cone guidance. Mol Neurobiol. 1996;12(2):95–116.Google Scholar
23. Vogelezang, MG, Liu, Z, Relvas, JB, Raivich, G, Scherer, SS, ffrench-Constant, C. Alpha4 integrin is expressed during peripheral nerve regeneration and enhances neurite outgrowth. J Neurosci. 2001;21(17):6732–44.CrossRefGoogle ScholarPubMed
24. Vogelezang, MG, Scherer, SS, Fawcett, JW, ffrench-Constant, C. Regulation of fibronectin alternative splicing during peripheral nerve repair. J Neurosci Res. 1999;56(4):323–33.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
25. Kim, SM, Lee, SK, Lee, JH. Peripheral nerve regeneration using a three dimensionally cultured schwann cell conduit. J Craniofac Surg. 2007;18(3):475–88.Google Scholar
26. Dornseifer, U, Matiasek, K, Fichter, MA, Rupp, A, Henke, J, Weidner, N, et al. Surgical therapy of peripheral nerve lesions: current status and new perspectives. Zentralbl Neurochir. 2007;68(3): 101–10.Google Scholar
27. Yang, Y, Ding, F, Wu, J, Hu, W, Liu, W, Liu, J, et al. Development and evaluation of silk fibroin-based nerve grafts used for peripheral nerve regeneration. Biomaterials. 2007;28(36):5526–35.CrossRefGoogle ScholarPubMed
28. Haastert, K, Grothe, C. Gene therapy in peripheral nerve reconstruction approaches. Curr Gene Ther. 2007;7(3):221–8.Google Scholar
29. Devor, M. Unexplained peculiarities of the dorsal root ganglion. Pain. 1999;Suppl 6:S27–35.Google Scholar
30. Priestley, JV, Michael, GJ, Averill, S, Liu, M, Willmott, N. Regulation of nociceptive neurons by nerve growth factor and glial cell line derived neurotrophic factor. Can J Physiol Pharmacol. 2002;80(5):495–505.Google Scholar
31. Petruska, JC, Napaporn, J, Johnson, RD, Gu, JG, Cooper, BY. Subclassified acutely dissociated cells of rat DRG: histochemistry and patterns of capsaicin-, proton-, and ATP-activated currents. J Neurophysiol. 2000;84(5):2365–79.CrossRefGoogle ScholarPubMed
32. Gavazzi, I, Kumar, RD, McMahon, SB, Cohen, J. Growth responses of different subpopulations of adult sensory neurons to neurotrophic factors in vitro. Eur J Neurosci. 1999;11(10): 3405–14.Google Scholar
33. Averill, S, McMahon, SB, Clary, DO, Reichardt, LF, Priestley, JV. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur J Neurosci. 1995;7(7):1484–94.Google Scholar
34. Ishikawa, T, Miyagi, M, Ohtori, S, Aoki, Y, Ozawa, T, Doya, H, et al. Characteristics of sensory DRG neurons innervating the lumbar facet joints in rats. Eur Spine J. 2005;14(6):559–64.CrossRefGoogle ScholarPubMed
35. Tucker, BA, Rahimtula, M, Mearow, KM. Laminin and growth factor receptor activation stimulates differential growth responses in subpopulations of adult DRG neurons. Eur J Neurosci. 2006;24(3):676–90.CrossRefGoogle ScholarPubMed
36. Ramer, MS, Bradbury, EJ, Michael, GJ, Lever, IJ, McMahon, SB. Glial cell line-derived neurotrophic factor increases calcitonin gene-related peptide immunoreactivity in sensory and motoneurons in vivo. Eur J Neurosci. 2003;18(10):2713–21.Google Scholar
37. Molliver, DC, Wright, DE, Leitner, ML, Parsadanian, AS, Doster, K, Wen, D, et al. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron. 1997;19(4): 849–61.CrossRefGoogle ScholarPubMed
38. Bennett, DL, Michael, GJ, Ramachandran, N, Munson, JB, Averill, S, Yan, Q, et al. A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J Neurosci. 1998;18(8):3059–72.Google Scholar
39. Kashiba, H, Uchida, Y, Senba, E. Distribution and colocalization of NGF and GDNF family ligand receptor mRNAs in dorsal root and nodose ganglion neurons of adult rats. Brain Res Mol Brain Res. 2003;110(1):52–62.Google Scholar
40. Karchewski, LA, Kim, FA, Johnston, J, McKnight, RM, Verge, VM. Anatomical evidence supporting the potential for modulation by multiple neurotrophins in the majority of adult lumbar sensory neurons. J Comp Neurol. 1999;413(2):327–41.Google Scholar
41. Kashiba, H, Noguchi, K, Ueda, Y, Senba, E. Coexpression of trk family members and low-affinity neurotrophin receptors in rat dorsal root ganglion neurons. Brain Res Mol Brain Res. 1995;30(1):158–64.Google Scholar
42. Kashiba, H, Ueda, Y, Ueyama, T, Nemoto, K, Senba, E. Relationship between BDNF- and trk-expressing neurones in rat dorsal root ganglion: an analysis by in situ hybridization. Neuroreport. 1997;8(5):1229–34.Google Scholar
43. McMahon, SB, Armanini, MP, Ling, LH, Phillips, HS. Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron. 1994;12(5):1161–71.Google Scholar
44. Kimpinski, K, Campenot, RB, Mearow, K. Effects of the neurotrophins nerve growth factor, neurotrophin-3, and brainderived neurotrophic factor (BDNF) on neurite growth from adult sensory neurons in compartmented cultures. J Neurobiol. 1997;33(4):395–410.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
45. Lee, R, Kermani, P, Teng, KK, Hempstead, BL. Regulation of cell survival by secreted proneurotrophins. Science. 2001;294(5548): 1945–8.Google Scholar
46. Bandtlow, C, Dechant, G. From cell death to neuronal regeneration, effects of the p75 neurotrophin receptor depend on interactions with partner subunits. Sci STKE. 2004;2004(235):pe24.Google Scholar
47. Barker, PA. p75NTR is positively promiscuous: novel partners and new insights. Neuron. 2004;42(4):529–33.Google Scholar
48. Hasegawa, Y, Yamagishi, S, Fujitani, M, Yamashita, T. p75 Neurotrophin receptor signaling in the nervous system. Biotechnol Annu Rev. 2004;10:123–49.CrossRefGoogle ScholarPubMed
49. Hennigan, A, O’Callaghan, RM, Kelly, AM. Neurotrophins and their receptors: roles in plasticity, neurodegeneration and neuroprotection. Biochem Soc Trans. 2007;35(Pt 2):424–7.Google Scholar
50. Lu, B, Pang, PT, Woo, NH. The yin and yang of neurotrophin action. Nat Rev Neurosci. 2005;6(8):603–14.Google Scholar
51. Twiss, JL, Chang, JH, Schanen, NC. Pathophysiological mechanisms for actions of the neurotrophins. Brain Pathol. 2006;16(4): 320–32.Google Scholar
52. Airaksinen, MS, Saarma, M. The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci. 2002;3(5):383–94.Google Scholar
53. Runeberg-Roos, P, Saarma, M. Neurotrophic factor receptor RET: structure, cell biology, and inherited diseases. Ann Med. 2007: 39:572–80.Google Scholar
54. McMahon, SB, Priestley, JV. Peripheral neuropathies and neurotrophic factors: animal models and clinical perspectives. Curr Opin Neurobiol. 1995;5(5):616–24.Google Scholar
55. Durbec, P, Marcos-Gutierrez, CV, Kilkenny, C, Grigoriou, M, Wartiowaara, K, Suvanto, P, et al. GDNF signalling through the Ret receptor tyrosine kinase. Nature. 1996;381(6585):789–93.CrossRefGoogle ScholarPubMed
56. Treanor, JJ, Goodman, L, de Sauvage, F, Stone, DM, Poulsen, KT, Beck, CD, et al. Characterization of a multicomponent receptor for GDNF. Nature. 1996;382(6586):80–3.Google Scholar
57. Trupp, M, Arenas, E, Fainzilber, M, Nilsson, AS, Sieber, BA, Grigoriou, M, et al. Functional receptor for GDNF encoded by the c-ret proto-oncogene. Nature. 1996;381(6585):785–9.Google Scholar
58. Tonge, D, Edstrom, A, Ekstrom, P. Use of explant cultures of peripheral nerves of adult vertebrates to study axonal regeneration in vitro. Prog Neurobiol. 1998;54(4):459–80.Google Scholar
59. Delree, P, Ribbens, C, Martin, D, Rogister, B, Lefebvre, PP, Rigo, JM, et al. Plasticity of developing and adult dorsal root ganglion neurons as revealed in vitro. Brain Res Bull. 1993;30(3-4): 231–7.Google Scholar
60. Tucker, BA, Rahimtula, M, Mearow, KM. A procedure for selecting and culturing subpopulations of neurons from rat dorsal root ganglia using magnetic beads. Brain Res Brain Res Protoc. 2005; 16(1-3):50–7.Google Scholar
61. Smith, DS, Skene, JH. A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth. J Neurosci. 1997; 17(2):646–58.Google Scholar
62. Lankford, KL, Waxman, SG, Kocsis, JD. Mechanisms of enhancement of neurite regeneration in vitro following a conditioning sciatic nerve lesion. J Comp Neurol. 1998; 391(1): 11–29.Google Scholar
63. White, FA, Keller-Peck, CR, Knudson, CM, Korsmeyer, SJ, Snider, WD. Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J Neurosci. 1998; 18(4):1428–39.Google Scholar
64. Lindsay, RM. Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurons. J Neurosci. 1988;8(7):2394–405.Google Scholar
65. Williams, KL, Rahimtula, M, Mearow, KM. Heat shock protein 27 is involved in neurite extension and branching of dorsal root ganglion neurons in vitro. J Neurosci Res. 2006;84(4):716–23.Google Scholar
66. Dodge, ME, Rahimtula, M, Mearow, KM. Factors contributing to neurotrophin-independent survival of adult sensory neurons. Brain Res. 2002;953(1-2):144–56.CrossRefGoogle ScholarPubMed
67. Chen, ZL, Yu, WM, Strickland, S. Peripheral regeneration. Annu Rev Neurosci. 2007;30:209–33.Google Scholar
68. Lykissas, MG, Batistatou, AK, Charalabopoulos, KA, Beris, AE. The role of neurotrophins in axonal growth, guidance, and regeneration. Curr Neurovasc Res. 2007;4(2):143–51.CrossRefGoogle ScholarPubMed
69. Ekstrom, AR, Kanje, M, Skottner, A. Nerve regeneration and serum levels of insulin-like growth factor-I in rats with streptozotocininduced insulin deficiency. Brain Res. 1989;496(1-2):141–7.Google Scholar
70. Jones, DM, Tucker, BA, Rahimtula, M, Mearow, KM. The synergistic effects of NGF and IGF-1 on neurite growth in adult sensory neurons: convergence on the PI 3-kinase signaling pathway. J Neurochem. 2003;86(5):1116–28.Google Scholar
71. Kimpinski, K, Mearow, K. Neurite growth promotion by nerve growth factor and insulin-like growth factor-1 in cultured adult sensory neurons: role of phosphoinositide 3-kinase and mitogen activated protein kinase. J Neurosci Res. 2001;63(6):486–99.Google Scholar
72. Haastert, K, Lipokatic, E, Fischer, M, Timmer, M, Grothe, C. Differentially promoted peripheral nerve regeneration by grafted Schwann cells over-expressing different FGF-2 isoforms. Neurobiol Dis. 2006;21(1):138–53.CrossRefGoogle ScholarPubMed
73. Malgrange, B, Delree, P, Rigo, JM, Baron, H, Moonen, G. Image analysis of neuritic regeneration by adult rat dorsal root ganglion neurons in culture: quantification of the neurotoxicity of anticancer agents and of its prevention by nerve growth factor or basic fibroblast growth factor but not brain-derived neurotrophic factor or neurotrophin-3. J Neurosci Methods. 1994;53(1):111–22.Google Scholar
74. Mohiuddin, L, Fernyhough, P, Tomlinson, DR. Acidic fibroblast growth factor enhances neurite outgrowth and stimulates expression of GAP-43 and T alpha 1 alpha-tubulin in cultured neurones from adult rat dorsal root ganglia. Neurosci Lett. 1996;215(2):111–4.CrossRefGoogle Scholar
75. Sondell, M, Sundler, F, Kanje, M. Vascular endothelial growth factor is a neurotrophic factor which stimulates axonal outgrowth through the flk-1 receptor. Eur J Neurosci. 2000;12(12):4243–54.Google Scholar
76. Nilsson, A, Kanje, M. Amphiregulin acts as an autocrine survival factor for adult sensory neurons. Neuroreport. 2005;16(3):213–8.Google Scholar
77. Chalazonitis, A, Kalberg, J, Twardzik, DR, Morrison, RS, Kessler, JA. Transforming growth factor beta has neurotrophic actions on sensory neurons in vitro and is synergistic with nerve growth factor. Dev Biol. 1992;152(1):121–32.Google Scholar
78. Niwa, H, Hayakawa, K, Yamamoto, M, Itoh, T, Mitsuma, T, Sobue, G. Differential age-dependent trophic responses of nodose, sensory, and sympathetic neurons to neurotrophins and GDNF: potencies for neurite extension in explant culture. Neurochem Res. 2002;27(6):485–96.CrossRefGoogle ScholarPubMed
79. Kimpinski, K, Jelinski, S, Mearow, K. The anti-p75 antibody, MC192, and brain-derived neurotrophic factor inhibit nerve growth factor-dependent neurite growth from adult sensory neurons. Neuroscience. 1999;93(1):253–263.Google Scholar
80. Kaplan, DR, Miller, FD. Signal transduction by the neurotrophin receptors. Curr Opin Cell Biol. 1997;9(2):213–21.Google Scholar
81. Kaplan, DR, Miller, FD. Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol. 2000;10(3):381–91.Google Scholar
82. Markus, A, Patel, TD, Snider, WD. Neurotrophic factors and axonal growth. Curr Opin Neurobiol. 2002;12(5):523–31.Google Scholar
83. Reichardt, LF. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci. 2006;361(1473):1545–64.Google Scholar
84. Atwal, JK, Massie, B, Miller, FD, Kaplan, DR. The TrkB-Shc site signals neuronal survival and local axon growth via MEK and P13-kinase. Neuron. 2000;27(2):265–77.Google Scholar
85. Cafferty, WB, Gardiner, NJ, Gavazzi, I, Powell, J, McMahon, SB, Heath, JK, et al. Leukemia inhibitory factor determines the growth status of injured adult sensory neurons. J Neurosci. 2001;21(18):7161–70.Google Scholar
86. Edstrom, A, Ekstrom, PA. Role of phosphatidylinositol 3-kinase in neuronal survival and axonal outgrowth of adult mouse dorsal root ganglia explants. J Neurosci Res. 2003;74(5):726–35.Google Scholar
87. Liu, RY, Snider, WD. Different signaling pathways mediate regenerative versus developmental sensory axon growth. J Neurosci. 2001;21(17):RC164.Google Scholar
88. Wiklund, P, Ekstrom, PA, Edbladh, M, Tonge, D, Edstrom, A. Protein kinase C and mouse sciatic nerve regeneration. Brain Res. 1996;715(1-2):145–54.CrossRefGoogle ScholarPubMed
89. Wiklund, P, Ekstrom, PA, Edstrom, A. Mitogen-activated protein kinase inhibition reveals differences in signalling pathways activated by neurotrophin-3 and other growth-stimulating conditions of adult mouse dorsal root ganglia neurons. J Neurosci Res. 2002;67(1):62–8.Google Scholar
90. Edstrom, A, Ekstrom, PA, Tonge, D. Axonal outgrowth and neuronal apoptosis in cultured adult mouse dorsal root ganglion preparations: effects of neurotrophins, of inhibition of neurotrophin actions and of prior axotomy. Neuroscience. 1996;75(4):1165–74.Google Scholar
91. Eickholt, BJ, Ahmed, AI, Davies, M, Papakonstanti, EA, Pearce, W, Starkey, ML, et al. Control of axonal growth and regeneration of sensory neurons by the p110delta PI 3-Kinase. PLoS ONE. 2007;2(9):e869.Google Scholar
92. Tucker, BA, Rahimtula, M, Mearow, KM. Integrin activation and neurotrophin signaling cooperate to enhance neurite outgrowth in sensory neurons. J Comp Neurol. 2005;486(3):267–80.Google Scholar
93. Tucker, BA, Rahimtula, M, Mearow, KM. Src and FAK are key early signalling intermediates required for neurite growth in NGF-responsive adult DRG neurons. Cell Signal. 2008;20(1):241–57.Google Scholar
94. Ganju, P, O’Bryan, JP, Der, C, Winter, J, James, IF. Differential regulation of SHC proteins by nerve growth factor in sensory neurons and PC12 cells. Eur J Neurosci. 1998;10(6):1995–2008.Google Scholar
95. Seijffers, R, Mills, CD, Woolf, CJ. ATF3 increases the intrinsic growth state of DRG neurons to enhance peripheral nerve regeneration. J Neurosci. 2007;27(30):7911–20.Google Scholar
96. Lindwall, C, Kanje, M. The Janus role of c-Jun: cell death versus survival and regeneration of neonatal sympathetic and sensory neurons. Exp Neurol. 2005;196(1):184–94.CrossRefGoogle ScholarPubMed
97. Stam, FJ, MacGillavry, HD, Armstrong, NJ, de Gunst, MC, Zhang, Y, van Kesteren, RE, et al. Identification of candidate transcriptional modulators involved in successful regeneration after nerve injury. Eur J Neurosci. 2007;25(12):3629–37.Google Scholar
98. Chen, ZL, Strickland, S. Laminin gamma1 is critical for Schwann cell differentiation, axon myelination, and regeneration in the peripheral nerve. J Cell Biol. 2003;163(4):889–99.Google Scholar
99. Liuzzi, FJ, Tedeschi, B. Peripheral nerve regeneration. Neurosurg Clin N Am. 1991;2(1):31–42.Google Scholar
100. Matesz, C, Modis, L, Halasi, G, Szigeti, ZM, Felszeghy, S, Bacskai, T, et al. Extracellular matrix molecules and their possible roles in the regeneration of frog nervous system. Brain Res Bull. 2005;66(4-6):526–31.CrossRefGoogle ScholarPubMed
101. Loers, G, Schachner, M. Recognition molecules and neural repair. J Neurochem. 2007;101(4):865–82.Google Scholar
102. Yamaguchi, Y. Heparan sulfate proteoglycans in the nervous system: their diverse roles in neurogenesis, axon guidance, and synaptogenesis. Semin Cell Dev Biol. 2001;12(2):99–106.Google Scholar
103. Luckenbill-Edds, L. Laminin and the mechanism of neuronal outgrowth. Brain Res Brain Res Rev. 1997;23(1-2):1–27.Google Scholar
104. Colognato, H, ffrench-Constant, C, Feltri, ML. Human diseases reveal novel roles for neural laminins. Trends Neurosci. 2005;28(9):480–6.Google Scholar
105. Bunge, RP, Bunge, MB, Eldridge, CF. Linkage between axonal ensheathment and basal lamina production by Schwann cells. Annu Rev Neurosci. 1986;9:305–28.Google Scholar
106. Ekstrom, PA, Mayer, U, Panjwani, A, Pountney, D, Pizzey, J, Tonge, DA. Involvement of alpha7beta1 integrin in the conditioning-lesion effect on sensory axon regeneration. Mol Cell Neurosci. 2003;22(3):383–95.CrossRefGoogle ScholarPubMed
107. Tonge, DA, Golding, JP, Edbladh, M, Kroon, M, Ekstrom, PE, Edstrom, A. Effects of extracellular matrix components on axonal outgrowth from peripheral nerves of adult animals in vitro. Exp Neurol. 1997;146(1):81–90.Google Scholar
108. Carbonetto, S, Cochard, P. In vitro studies on the control of nerve fiber growth by the extracellular matrix of the nervous system. J Physiol (Paris). 1987;82(4):258–70.Google Scholar
109. Itoh, T, Sobue, G, Yasuda, T, Mitsuma, T, Takahashi, A, Kimata, K. Geometry of adult rat sensory neurons in culture; its modulation by laminin. Neurosci Lett. 1991;123(2):212–6.Google Scholar
110. Kohno, K, Kawakami, T, Hiruma, H. Effects of soluble laminin on organelle transport and neurite growth in cultured mouse dorsal root ganglion neurons: difference between primary neurites and branches. J Cell Physiol. 2005;205(2):253–61.Google Scholar
111. Unsicker, K, Skaper, SD, Davis, GE, Manthorpe, M, Varon, S. Comparison of the effects of laminin and the polyornithine-binding neurite promoting factor from RN22 Schwannoma cells on neurite regeneration from cultured newborn and adult rat dorsal root ganglion neurons. Brain Res. 1985;349(1-2):304–8.Google Scholar
112. Williams, KL, Rahimtula, M, Mearow, KM. Hsp27 and axonal growth in adult sensory neurons in vitro. BMC Neurosci. 2005;6(1):24.Google Scholar
113. Paveliev, M, Lume, M, Velthut, A, Phillips, M, Arumae, U, Saarma, M. Neurotrophic factors switch between two signaling pathways that trigger axonal growth. J Cell Sci. 2007;120(Pt 15):2507–16.Google Scholar
114. Deister, C, Aljabari, S, Schmidt, CE. Effects of collagen 1, fibronectin, laminin and hyaluronic acid concentration in multi-component gels on neurite extension. J Biomater Sci Polym Ed. 2007;18(8):983–97.Google Scholar
115. Gardiner, NJ, Moffatt, S, Fernyhough, P, Humphries, MJ, Streuli, CH, Tomlinson, DR. Preconditioning injury-induced neurite outgrowth of adult rat sensory neurons on fibronectin is mediated by mobilisation of axonal alpha5 integrin. Mol Cell Neurosci. 2007;35(2):249–60.Google Scholar
116. Giancotti, FG, Tarone, G. Positional control of cell fate through joint integrin/receptor protein kinase signaling. Annu Rev Cell Dev Biol. 2003;19:173–206.Google Scholar
117. Giancotti, FG. A structural view of integrin activation and signaling. Dev Cell. 2003;4(2):149–51.Google Scholar
118. Guo, W, Giancotti, FG. Integrin signalling during tumour progression. Nat Rev Mol Cell Biol. 2004;5(10):816–26.Google Scholar
119. Giancotti, FG, Ruoslahti, E. Integrin signaling. Science 1999;285(5430):1028–32.Google Scholar
120. Hynes, RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002;110(6):673–87.Google Scholar
121. Previtali, SC, Feltri, ML, Archelos, JJ, Quattrini, A, Wrabetz, L, Hartung, H. Role of integrins in the peripheral nervous system. Prog Neurobiol. 2001;64(1):35–49.Google Scholar
122. Archelos, JJ, Previtali, SC, Hartung, HP. The role of integrins in immune-mediated diseases of the nervous system. Trends Neurosci. 1999;22(1):30–8.Google Scholar
123. Hynes, RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 1992;69(1):11–25.Google Scholar
124. Eble, JA, Haier, J. Integrins in cancer treatment. Curr Cancer Drug Targets. 2006;6(2):89–105.Google Scholar
125. Lenz, HJ. Antiangiogenic agents in cancer therapy. Oncology (Williston Park). 2005;19(4 Suppl 3):17–25.Google ScholarPubMed
126. Serini, G, Valdembri, D, Bussolino, F. Integrins and angiogenesis: a sticky business. Exp Cell Res. 2006;312(5):651–8.Google Scholar
127. Caswell, PT, Norman, JC. Integrin trafficking and the control of cell migration. Traffic. 2006;7(1):14–21.CrossRefGoogle ScholarPubMed
128. Condic, ML. Adult neuronal regeneration induced by transgenic integrin expression. J Neurosci. 2001;21(13):4782–8.Google Scholar
129. Tomaselli, KJ, Doherty, P, Emmett, CJ, Damsky, CH, Walsh, FS, Reichardt, LF. Expression of beta 1 integrins in sensory neurons of the dorsal root ganglion and their functions in neurite outgrowth on two laminin isoforms. J Neurosci. 1993;13(11):4880–8.Google Scholar
130. Gardiner, NJ, Fernyhough, P, Tomlinson, DR, Mayer, U, von der Mark, H, Streuli, CH. Alpha7 integrin mediates neurite outgrowth of distinct populations of adult sensory neurons. Mol Cell Neurosci. 2005;28(2):229–40.Google Scholar
131. Condic, ML, Letourneau, PC. Ligand-induced changes in integrin expression regulate neuronal adhesion and neurite outgrowth. Nature. 1997;389(6653):852–6.Google Scholar
132. Guan, W, Puthenveedu, MA, Condic, ML. Sensory neuron subtypes have unique substratum preference and receptor expression before target innervation. J Neurosci 2003;23(5):1781–91.Google Scholar
133. Leclere, PG, Norman, E, Groutsi, F, Coffin, R, Mayer, U, Pizzey, J, et al. Impaired axonal regeneration by isolectin B4-binding dorsal root ganglion neurons in vitro. J Neurosci. 2007;27(5):1190–9.Google Scholar
134. Wallquist, W, Zelano, J, Plantman, S, Kaufman, SJ, Cullheim, S, Hammarberg, H. Dorsal root ganglion neurons up-regulate the expression of laminin-associated integrins after peripheral but not central axotomy. J Comp Neurol. 2004;480(2):162–9.Google Scholar
135. Arnaout, MA, Goodman, SL, Xiong, JP. Structure and mechanics of integrin-based cell adhesion. Curr Opin Cell Biol. 2007;19(5):495–507.Google Scholar
136. Aplin, AE, Howe, AK, Juliano, RL. Cell adhesion molecules, signal transduction and cell growth. Curr Opin Cell Biol. 1999;11(6):737–44.Google Scholar
137. Travis, MA, Humphries, JD, Humphries, MJ. An unraveling tale of how integrins are activated from within. Trends Pharmacol Sci. 2003;24(4):192–7.Google Scholar
138. Ginsberg, MH, Partridge, A, Shattil, SJ. Integrin regulation. Curr Opin Cell Biol. 2005;17(5):509–16.Google Scholar
139. Chen, HC, Appeddu, PA, Isoda, H, Guan, JL. Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding phosphatidylinositol 3-kinase. J Biol Chem. 1996;271(42):26329–34.Google Scholar
140. Wary, KK, Mainiero, F, Isakoff, SJ, Marcantonio, EE, Giancotti, FG. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell. 1996;87(4):733–43.Google Scholar
141. Wary, KK, Mariotti, A, Zurzolo, C, Giancotti, FG. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell. 1998;94(5):625–34.Google Scholar
142. Hannigan, GE, Leung-Hagesteijn, C, Fitz-Gibbon, L, Coppolino, MG, Radeva, G, Filmus, J, et al. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature. 1996;379(6560):91–6.Google Scholar
143. Kornberg, L, Earp, HS, Parsons, JT, Schaller, M, Juliano, RL. Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase. J Biol Chem. 1992;267(33):23439–42.Google Scholar
144. Schaller, MD, Parsons, JT. Focal adhesion kinase and associated proteins. Curr Opin Cell Biol. 1994;6(5):705–10.Google Scholar
145. Howe, A, Aplin, AE, Alahari, SK, Juliano, RL. Integrin signaling and cell growth control. Curr Opin Cell Biol. 1998;10(2):220–31.Google Scholar
146. Alam, N, Goel, HL, Zarif, MJ, Butterfield, JE, Perkins, HM, Sansoucy, BG, et al. The integrin-growth factor receptor duet. J Cell Physiol. 2007;213(3):649–53.Google Scholar
147. Delcroix, JD, Valletta, JS, Wu, C, Hunt, SJ, Kowal, AS, Mobley, WC. NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals. Neuron. 2003;39(1):69–84.Google Scholar
148. Mills, J, Digicaylioglu, M, Legg, AT, Young, CE, Young, SS, Barr, AM, et al. Role of integrin-linked kinase in nerve growth factor-stimulated neurite outgrowth. J Neurosci. 2003;23(5):1638–48.Google Scholar
149. Markus, A, Zhong, J, Snider, WD. Raf and akt mediate distinct aspects of sensory axon growth. Neuron. 2002;35(1):65–76.Google Scholar
150. Zhou, FQ, Zhou, J, Dedhar, S, Wu, YH, Snider, WD. NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron. 2004;42(6):897–912.Google Scholar
151. Higuchi, M, Onishi, K, Masuyama, N, Gotoh, Y. The phosphatidylinositol-3 kinase (PI3K)-Akt pathway suppresses neurite branch formation in NGF-treated PC12 cells. Genes Cells. 2003;8(8):657–69.Google Scholar
152. Kamata, Y, Shiraga, H, Tai, A, Kawamoto, Y, Gohda, E. Induction of neurite outgrowth in PC12 cells by the medium-chain fatty acid octanoic acid. Neuroscience. 2007;146(3):1073–81.CrossRefGoogle ScholarPubMed
153. Gary, DS, Mattson, MP. Integrin signaling via the PI3-kinase-Akt pathway increases neuronal resistance to glutamate-induced apoptosis. J Neurochem. 2001;76(5):1485–96.Google Scholar
154. Koul, D, Shen, R, Bergh, S, Lu, Y, de Groot, JF, Liu, TJ, et al. Targeting integrin-linked kinase inhibits Akt signaling pathways and decreases tumor progression of human glioblastoma. Mol Cancer Ther. 2005;4(11):1681–8.Google Scholar
155. Dey, N, Howell, BW, De, PK, Durden, DL. CSK negatively regulates nerve growth factor induced neural differentiation and augments AKT kinase activity. Exp Cell Res. 2005;307(1):1–14.Google Scholar
156. Schlaepfer, DD, Hunter, T. Integrin signalling and tyrosine phosphorylation: just the FAKs? Trends Cell Biol. 1998;8(4):151–7.Google Scholar
157. Dikic, I, Tokiwa, G, Lev, S, Courtneidge, SA, Schlessinger, J. A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature. 1996;383(6600):547–50.Google Scholar
158. Clark, EA, Brugge, JS. Integrins and signal transduction pathways: the road taken. Science. 1995;268(5208):233–9.Google Scholar
159. da Silva, JS, Dotti, CG. Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci. 2002;3(9):694–704.CrossRefGoogle ScholarPubMed
160. Hall, A. Rho GTPases and the control of cell behaviour. Biochem Soc Trans. 2005;33(Pt 5):891–5.Google Scholar
161. Huang, TY, DerMardirossian, C, Bokoch, GM. Cofilin phosphatases and regulation of actin dynamics. Curr Opin Cell Biol. 2006;18(1):26–31.Google Scholar
162. Sarmiere, PD, Bamburg, JR. Regulation of the neuronal actin cytoskeleton by ADF/cofilin. J Neurobiol. 2004;58(1):103–17.Google Scholar
163. Gallo, G, Letourneau, PC. Regulation of growth cone actin filaments by guidance cues. J Neurobiol. 2004;58(1):92–102.Google Scholar
164. Toshima, J, Toshima, JY, Amano, T, Yang, N, Narumiya, S, Mizuno, K. Cofilin phosphorylation by protein kinase testicular protein kinase 1 and its role in integrin-mediated actin reorganization and focal adhesion formation. Mol Biol Cell. 2001;12(4):1131–45.Google Scholar
165. Ohashi, K, Nagata, K, Maekawa, M, Ishizaki, T, Narumiya, S, Mizuno, K. Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J Biol Chem. 2000;275(5):3577–82.Google Scholar
166. Yang, N, Higuchi, O, Ohashi, K, Nagata, K, Wada, A, Kangawa, K, et al. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature. 1998;393(6687):809–12.Google Scholar
167. Ohta, Y, Kousaka, K, Nagata-Ohashi, K, Ohashi, K, Muramoto, A, Shima, Y, et al. Differential activities, subcellular distribution and tissue expression patterns of three members of Slingshot family phosphatases that dephosphorylate cofilin. Genes Cells. 2003;8(10):811–24.Google Scholar
168. Costigan, M, Mannion, RJ, Kendall, G, Lewis, SE, Campagna, JA, Coggeshall, RE, et al. Heat shock protein 27: developmental regulation and expression after peripheral nerve injury. J Neurosci. 1998;18(15):5891–900.Google Scholar
169. Guay, J, Lambert, H, Gingras-Breton, G, Lavoie, JN, Huot, J, Landry, J. Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J Cell Sci. 1997;110 (Pt 3):357–68.Google Scholar
170. Pichon, S, Bryckaert, M, Berrou, E. Control of actin dynamics by p38 MAP kinase - Hsp27 distribution in the lamellipodium of smooth muscle cells. J Cell Sci. 2004;117(Pt 12):2569–77.Google Scholar
171. Mounier, N, Arrigo, AP. Actin cytoskeleton and small heat shock proteins: how do they interact? Cell Stress Chaperones. 2002;7(2):167–76.Google Scholar
172. During, RL, Gibson, BG, Li, W, Bishai, EA, Sidhu, GS, Landry, J, et al. Anthrax lethal toxin paralyzes actin-based motility by blocking Hsp27 phosphorylation. Embo J. 2007;26(9):2240–50.Google Scholar
173. Ackerley, S, James, PA, Kalli, A, French, S, Davies, KE, Talbot, K. A mutation in the small heat-shock protein HSPB1 leading to distal hereditary motor neuronopathy disrupts neurofilament assembly and the axonal transport of specific cellular cargoes. Hum Mol Genet. 2006;15(2):347–54.Google Scholar
174. Evgrafov, OV, Mersiyanova, I, Irobi, J, Van Den Bosch, L, Dierick, I, Leung, CL, et al. Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy. Nat Genet. 2004;36(6):602–6.Google Scholar
175. Dent, EW, Gertler, FB. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron. 2003;40(2):209–27.Google Scholar
176. Gallo, G, Letourneau, PC. Neurotrophins and the dynamic regulation of the neuronal cytoskeleton. J Neurobiol. 2000;44(2):159–73.Google Scholar
177. Gordon-Weeks, PR. Microtubules and growth cone function. J Neurobiol. 2004;58(1):70–83.Google Scholar
178. Ketschek, AR, Jones, SL, Gallo, G. Axon extension in the fast and slow lanes: substratum-dependent engagement of myosin II functions. Dev Neurobiol. 2007;67(10):1305–20.Google Scholar
179. Dehmelt, L, Halpain, S. Actin and microtubules in neurite initiation: are MAPs the missing link? J Neurobiol. 2004;58(1):18–33.Google Scholar
180. Halpain, S, Dehmelt, L. The MAP1 family of microtubule-associated proteins. Genome Biol. 2006;7(6):224.Google Scholar
181. Ahmed, Z, Mazibrada, G, Seabright, RJ, Dent, RG, Berry, M, Logan, A. TACE-induced cleavage of NgR and p75NTR in dorsal root ganglion cultures disinhibits outgrowth and promotes branching of neurites in the presence of inhibitory CNS myelin. Faseb J. 2006;20(11):1939–41.Google Scholar
182. Hiraga, A, Kuwabara, S, Doya, H, Kanai, K, Fujitani, M, Taniguchi, J, et al. Rho-kinase inhibition enhances axonal regeneration after peripheral nerve injury. J Peripher Nerv Syst. 2006;11(3):217–24.Google Scholar
183. Gaillard, S, Nasarre, C, Gonthier, B, Bagnard, D. [The cellular and molecular basis of axonal growth]. Rev Neurol (Paris). 2005;161(2):153–72.Google Scholar
184. Gungabissoon, RA, Bamburg, JR. Regulation of growth cone actin dynamics by ADF/cofilin. J Histochem Cytochem. 2003;51(4):411–20.Google Scholar
185. Lundquist, EA. Rac proteins and the control of axon development. Curr Opin Neurobiol. 2003;13(3):384–90.Google Scholar
186. Ng, J, Luo, L. Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron. 2004;44(5):779–93.Google Scholar
187. Sandvig, A, Berry, M, Barrett, LB, Butt, A, Logan, A. Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration. Glia. 2004;46(3):225–51.Google Scholar
188. Huber, AB, Kolodkin, AL, Ginty, DD, Cloutier, JF. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci. 2003;26:509–63.Google Scholar
189. Loudon, RP, Silver, LD, Yee, HF Jr., Gallo, G. RhoA-kinase and myosin II are required for the maintenance of growth cone polarity and guidance by nerve growth factor. J Neurobiol. 2006;66(8):847–67.Google Scholar
190. Ren, XD, Kiosses, WB, Sieg, DJ, Otey, CA, Schlaepfer, DD, Schwartz, MA. Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J Cell Sci. 2000;113 (Pt 20):3673–8.Google Scholar
191. Fernyhough, P, Willars, GB, Lindsay, RM, Tomlinson, DR. Insulin and insulin-like growth factor I enhance regeneration in cultured adult rat sensory neurones. Brain Res. 1993;607(1-2):117–24.Google Scholar
192. Akahori, Y, Horie, H. IGF-I enhances neurite regeneration but is not required for its survival in adult DRG explant. Neuroreport. 1997;8(9-10):2265–9.CrossRefGoogle Scholar