Impaired axonal regeneration by isolectin B4-binding dorsal root ganglion neurons in vitro

Journal of Neuroscience

Volumn 27, Issue 5, 2007, Pages 1190-1199

  Leclere, Pascal G ^a   Norman, Emma ^a   Groutsi, Filitsa ^b   Coffin, Robert ^b   Mayer, Ulrike ^c   Pizzey, John ^a   Tonge, David ^a,d  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

7 integrin; Axonal regeneration; DRG; GAP 43; IB4; SPRR1A

Indexed keywords

ALPHA7 INTEGRIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; INTEGRIN; ISOLECTIN B4; LAMININ; LECTIN; NEUROTROPHIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; HERPES SIMPLEX VIRUS 1; IN VITRO STUDY; MOUSE; NERVE CELL; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL GANGLION;

ANIMALS; AXONS; CELL LINE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; CRICETINAE; FEMALE; GANGLIA, SPINAL; GRIFFONIA; HUMANS; MICE; NERVE REGENERATION; NEURONS; PLANT LECTINS; PROTEIN BINDING; RATS;

EID: 33846782783     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5089-06.2007     Document Type: Article

References (77)

1. Averill S, McMahon SB, Clary DO, Reichardt LF, Priestley JV (1995) Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur J Neurosci 7:1484-1494.
2. Bailey AL, Ribeiro-da-Silva A (2006) Transient loss of terminals from non-peptidergic nociceptive fibers in the substantia gelatinosa of spinal cord following chronic constriction injury of the sciatic nerve. Neuroscience 138:675-690.
3. Baloh RH, Enomoto H, Johnson Jr EM, Milbrandt J (2000) The GDNF family ligands and receptors: implications for neural development. Curr Opin Neurobiol 10:103-110.
4. Bao L, Wang HF, Cai HJ, Tong YG, Jin SX, Lu YJ, Grant G, Hokfelt T, Zhang X (2002) Peripheral axotomy induces only very limited sprouting of coarse myelinated afferents into inner lamina II of rat spinal cord. Eur J Neurosci 16:175-185.
5. Bar KJ, Saldanha GJ, Kennedy AJ, Facer P, Birch R, Carlstedt T, Anand P (1998) GDNF and its receptor component Ret in injured human nerves and dorsal root ganglia. NeuroReport 9:43-47.
6. Bates CA, Meyer RL (1997) The neurite-promoting effect of laminin is mediated by different mechanisms in embryonic and adult regenerating mouse optic axons in vitro. Dev Biol 181:91-101.
7. Baudet C, Mikaels A, Westphal H, Johansen J, Johansen TE, Ernfors P (2000) Positive and negative interactions of GDNF, NTN and ART in developing sensory neuron subpopulations, and their collaboration with neurotrophins. Development 127:4335-4344.
8. Bennett DL, Michael GJ, Ramachandran N, Munson JB, Averill S, Yan Q, McMahon SB, Priestley JV (1998) A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J Neurosci 18:3059-3072.
9. Bennett DL, Boucher TJ, Armanini MP, Poulsen KT, Michael GJ, Priestley JV, Phillips HS, McMahon SB, Shelton DL (2000) The glial cell line-derived neurotrophic factor family receptor components are differentially regulated within sensory neurons after nerve injury. J Neurosci 20:427-437.
10. Benowitz LI, Routenberg A (1997) GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 20:84-91.
11. Bomze HM, Bulsara KR, Iskandar BJ, Caroni P, Skene JH (2001) Spinal axon regeneration evoked by replacing two growth cone proteins in adult neurons. Nat Neurosci 4:38-43.
12. Bonilla IE, Tanabe K, Strittmatter SM (2002) Small proline-rich repeat protein 1A is expressed by axotomized neurons and promotes axonal outgrowth. J Neurosci 22:1303-1315.
13. Botchkareva NV, Botchkarev VA, Welker P, Airaksinen M, Roth W, Suvanto P, Muller-Rover S, Hadshiew IM, Peters C, Paus R (2000) New roles for glial cell line-derived neurotrophic factor and neurturin: involvement in hair cycle control. Am J Pathol 156:1041-1053.
14. Boucher TJ, McMahon SB (2001) Neurotrophic factors and neuropathic pain. Curr Opin Pharmacol 1:66-72.
15. Constantinou J, Reynolds ML, Woolf CJ, Safieh-Garabedian B, Fitzgerald M (1994) Nerve growth factor levels in developing rat skin: upregulation following skin wounding. NeuroReport 5:2281-2284.
16. Dethleffsen K, Morl K, Meyer M (2002) Control of local NGF mRNA synthesis by preformed factors rapidly released from peripheral nerves. Mol Cell Neurosci 20:503-514.
17. Diamond J, Holmes M, Coughlin M (1992) Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J Neurosci 12:1454-1466.
18. Doubell TP, Mannion RJ, Woolf CJ (1997) Intact sciatic myelinated primary afferent terminals collaterally sprout in the adult rat dorsal horn following section of a neighbouring peripheral nerve. J Comp Neurol 380:95-104.
19. Eble JA, Bruckner P, Mayer U (2003) Vipera lebetina venom contains two disintegrins inhibiting laminin-binding beta 1 integrins. J Biol Chem 278:26488-26496.
20. Edström A, Ekström PAR, Tonge D (1996) Axonal outgrowth and neuronal apoptosis in cultured adult mouse DRG preparations: effects of neurotrophins, of inhibition of neurotrophin actions, and of prior axotomy. Neuroscience 75:1165-1174.
21. Ekström PA, Mayer U, Panjwani A, Pountney D, Pizzey J, Tonge DA (2003) Involvement of alpha7beta1 integrin in the conditioning-lesion effect on sensory axon regeneration. Mol Cell Neurosci 22:383-395.
22. Ferguson IA, Williams R, Rush RA (1989) Chicken NGF and non-NGF trophic factor synthesis and release by sciatic nerves in vitro. J Neurosci Res 22:408-417.
23. Fine EG, Decosterd I, Papaloizos M, Zurn AD, Aebischer P (2002) GDNF and NGF released by synthetic guidance channels support sciatic nerve regeneration across a long gap. Eur J Neurosci 15:589-601.
24. Flecknell PA, Mitchell M (1984) Midazolam and fentanyl-fluanisone: assessment of anaesthetic effects in laboratory rodents and rabbits. Lab Anim 18:143-146.
25. Funakoshi H, Frisen J, Barbany G, Timmusk T, Zachrisson O, Verge VMK, Persson H (1993) Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J Cell Biol 123:455-465.
26. Gardiner NJ, Fernyhough P, Tomlinson DR, Mayer U, von der Mark H, Streuli CH (2005) Alpha7 integrin mediates neurite outgrowth of distinct populations of adult sensory neurons. Mol Cell Neurosci 28:229-240.
27. Gavazzi I, Kumar KD, McMahon SB, Cohen J (1999) Growth responses of different subpopulations of adult sensory neurons to neurotrophic factors in vitro. Eur J Neurosci 11:3405-3414.
28. Heumann R, Korsching S, Bandtlow C, Thoenen H (1987) Changes of nerve growth factor synthesis in non-neuronal cells in response to sciatic nerve transection. J Cell Biol 104:1623-1631.
29. Hoke A, Cheng C, Zochodne DW (2000) Expression of glial cell line-derived neurotrophic factor family of growth factors in peripheral nerve injury in rats. NeuroReport 11:1651-1654.
30. Hoke A, Gordon T, Zochodne DW, Sulaiman OA (2002) A decline in glial cell-line-derived neurotrophic factor expression is associated with impaired regeneration after long-term Schwann cell denervation. Exp Neurol 173:77-85.
31. Hu-Tsai M, Winter J, Emson PC, Woolf CJ (1994) Neurite outgrowth and GAP 43 expression in cultured adult rat dorsal root ganglion neurons: effects of NGF or prior peripheral axotomy. J Neurosci Res 39:634-645.
32. Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24:677-736.
33. Hughes DI, Scott DT, Todd AJ, Riddell JS (2003) Lack of evidence for sprouting of Abeta afferents into the superficial laminas of the spinal cord dorsal horn after nerve section. J Neurosci 23:9491-9499.
34. Hunt SP, Mantyh PW (2001) The molecular dynamics of pain control. Nat Rev Neurosci 2:83-91.
35. Ide C (1996) Peripheral nerve regeneration. Neurosci Res 25:101-121.
36. Kimpinski K, Campenot RB, Mearow K (1997) Effects of the neurotrophins nerve growth factor, neurotrophin-3, and brain-derived neurotrophic factor (BDNF) on neurite growth from adult sensory neurons in compartmented cultures. J Neurobiol 33:395-410.
37. Kuffler DP, Megwinoff O (1994) Neurotrophic influence of denervated sciatic nerve on adult dorsal root ganglion neurons. J Neurobiol 25:1267-1282.
38. Lankford KL, Waxman SG, Kocsis JD (1998) Mechanisms of enhancement of neurite regeneration in vitro following a conditioning sciatic nerve lesion. J Comp Neurol 391:11-29.
39. Leclere P, Ekström P, Edstrom A, Priestley J, Averill S, Tonge DA (1998) Effects of glial cell line-derived neurotrophic factor on axonal growth and apoptosis in adult mammalian sensory neurons in vitro. Neuroscience 82:545-558.
40. Leclere PG, Panjwani A, Docherty R, Berry M, Pizzey J, Tonge DA (2005) Effective gene delivery to adult neurons by a modified form of electroporation. J Neurosci Methods 142:137-143.
41. Lee YJ, Zachrisson O, Tonge DA, McNaughton PA (2002) Upregulation of bradykinin B2 receptor expression by neurotrophic factors and nerve injury in mouse sensory neurons. Mol Cell Neurosci 19:186-200.
42. Lilley CE, Groutsi F, Han Z, Palmer JA, Anderson PN, Latchman DS, Coffin RS (2001) Multiple immediate-early gene-deficient herpes simplex virus vectors allowing efficient gene delivery to neurons in culture and widespread gene delivery to the central nervous system in vivo. J Virol 75:4343-4356.
43. Lindsay RM (1988) Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurons. J Neurosci 8:2394-2408.
44. Liu RY, Snider WD (2001) Different signaling pathways mediate regenerative versus developmental sensory axon growth. J Neurosci 21:RC164(1-5).
45. Lu J, Zhou XF, Rush RA (2001) Small primary sensory neurons innervating epidermis and viscera display differential phenotype in the adult rat. Neurosci Res 41:355-363.
46. Luckenbill-Edds L (1997) Laminin and the mechanism of neuronal outgrowth. Brain Res Brain Res Rev 23:1-27.
47. Maddox DE, Shibata S, Goldstein IJ (1982) Stimulated macrophages express a new glycoprotein receptor reactive with Griffonia simplicifolia I-B4 isolectin. Proc Natl Acad Sci USA 79:166-170.
48. Malgrange B, Delree P, Rigo JM, Baron H, Moonen G (1994) Image analysis of neuritic regeneration by adult rat dorsal root ganglion neurons in culture: quantitation of the neurotoxicity of anticancer agents and of its prevention by nerve growth factor or basic fibroblast growth factor but not by brain-derived neurotrophic factor or neurotrophin-3. J Neurosci Methods 53:111-122.
49. McFarlane S (2003) Metalloproteases: carving out a role in axon guidance. Neuron 37:559-562.
50. McMahon SB, Armanini MP, Ling LH, Phillips HS (1994) Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12:1161-1171.
51. Meyer M, Matsuoka I, Wetmore C, Olsen L, Thoenen H (1992) Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J Cell Biol 119:45-54.
52. Mohiuddin L, Fernandez K, Tomlinson DR, Fernyhough P (1995) Nerve growth factor and neurotrophin-3 enhance neurite outgrowth and upregulate the levels of messenger RNA for growth-associated protein GAP-43 and Tα1 α-tubulin in cultured adult rat sensory neurons. Neurosci Lett 185:20-23.
53. Molliver DC, Snider WD (1997) Nerve growth factor receptor TrkA is down-regulated during postnatal development by a subset of dorsal root ganglion neurons. J Comp Neurol 19:428-438.
54. Molliver DC, Wright DE, Leitner ML, Parsadanian AS, Doster K, Wen D, Yan Q, Snider WD (1997) IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19:849-861.
55. Moskowitz PF, Oblinger MM (1995) Sensory neurons selectively upregulate synthesis and transport of the beta III-tubulin protein during axonal regeneration. J Neurosci 15:1545-1555.
56. Nanduri J, Vroegop SM, Buxser SE, Neet KE (1994) Immunological determinants of nerve growth factor involved in p140trk (Trk) receptor binding. J Neurosci Res 37:433-444.
57. Naveilhan P, ElShamy WM, Ernfors P (1997) Differential regulation of mRNAs for GDNF and its receptors Ret and GDNFR alpha after sciatic nerve lesion in the mouse. Eur J Neurosci 9:1450-1460.
58. Ramer MS, Priestley JV, McMahon SB (2000) Functional regeneration of sensory axons into the adult spinal cord. Nature 403:312-316.
59. Reynolds ML, Fitzgerald M (1995) Long-term sensory hyperinnervation following neonatal skin wounds. J Comp Neurol 358:487-498.
60. Richardson PM, Ebendal T (1982) Nerve growth activities in rat peripheral nerve. Brain Res 246:57-64.
61. Shehab SA, Spike RC, Todd AJ (2004) Do central terminals of intact myelinated primary afferents sprout into the superficial dorsal horn of rat spinal cord after injury to a neighboring peripheral nerve? J Comp Neurol 474:427-437.
62. Shu XQ, Mendell LM (1999) Neurotrophins and hyperalgesia. Proc Natl Acad Sci USA 96:7693-7696.
63. Smith DS, Pate Skene JH (1997) A transcription-dependent switch controls competence of adult neurons for distinct modes of axonal growth. J Neurosci 17:646-658.
64. Thomas SK, Lilley CE, Latchman DS, Coffin RS (1999) Equine herpesvirus 1 gene 12 can substitute for vmw65 in the growth of herpes simplex virus (HSV) type 1, allowing the generation of optimized cell lines for the propagation of HSV vectors with multiple immediate-early gene defects. J Virol 73:7399-7409.
65. Tonge DA, Aaronson OS, Golding JP, Jaggers D (1996) Cellular migration and axonal outgrowth from adult mammalian peripheral nerves in vitro. J Neurobiol 29:151-164.
66. Tonge D, Edstrom S, Ekström P (1998) Use of explant cultures of peripheral nerves of adult vertebrates to study axonal regeneration in vitro. Prog Neurobiol 54:459-480.
67. Trupp M, Rydén M, Jörnvall H, Funakoshi H, Timmusk T, Arenas E, Ibanéz 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. Ueda M, Hirose M, Takei N, Ibuki T, Naruse Y, Amaya F, Ibata Y, Tanaka M (2002) Nerve growth factor induces systemic hyperalgesia after thoracic burn injury in the rat. Neurosci Lett 328:97-100.
69. Vellani V, Zachrisson O, McNaughton PA (2004) Functional bradykinin B1 receptors are expressed in nociceptive neurones and are upregulated by the neurotrophin GDNF. J Physiol (Lond) 560:391-401.
70. Verge VM, Tetzlaff W, Richardson PM, Bisby MA (1990) Correlation between GAP43 and nerve growth factor receptors in rat sensory neurons. J Neurosci 10:926-934.
71. Wallquist W, Zelano J, Plantman S, Kaufman SJ, Cullheim S, Hammarberg H (2004) Dorsal root ganglion neurons up-regulate the expression of laminin-associated integrins after peripheral but not central axotomy. J Comp Neurol 480:162-169.
72. Werner A, Willem M, Jones LL, Kreutzberg GW, Mayer U, Raivich G (2000) Impaired axonal regeneration in α7 integrin-deficient mice. J Neurosci 20:1822-1830.
73. White FA, Bennett-Clarke CA, Macdonald GJ, Enfiejian HL, Chiaia NL, Rhoades RW (1990) Neonatal infraorbital nerve transection in the rat: comparison of effects on substance P immunoreactive primary afferents and those recognized by the lectin Bandierea simplicifolia-I. J Comp Neurol 300:249-262.
74. Wiklund P, Ekström PA (2000) Axonal outgrowth from adult mouse no-dose ganglia in vitro is stimulated by neurotrophin-4 in a Trk receptor and mitogen-activated protein kinase-dependent way. J Neurobiol 45:142-151.
75. Wilson POG, Barber PC, Hamid QA, Power BF, Dhillon AP, Rhode J, Day INM, Thompson RJ, Polak JM (1988) Immunolocalization of protein gene product 9.5 using rabbit polyclonal and mouse monoclonal antibodies. Br J Exp Pathol 69:91-104.
76. Windebank AJ, Poduslo JF (1986) Neuronal growth factors produced by adult peripheral nerve after injury. Brain Res 385:197-200.
77. Zhang Y, Bo X, Schoepfer R, Holtmaat AJ, Verhaagen J, Emson PC, Lieberman AR, Anderson PN (2005) Growth-associated protein GAP-43 and L1 act synergistically to promote regenerative growth of Purkinje cell axons in vivo. Proc Natl Acad Sci USA 102:14883-14888.