Expression of an activated integrin promotes long-distance sensory axon regeneration in the spinal cord

Journal of Neuroscience

Volumn 36, Issue 27, 2016, Pages 7283-7297

  Cheah, Menghon ^a   Andrews, Melissa R ^b   Chew, Daniel J ^a   Moloney, Elizabeth B ^c   Verhaagen, Joost ^c   Fässler, Reinhard ^d   Fawcett, James W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^d MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Adeno associated virus; Alpha9 integrin; Axon regeneration; Dorsal root ganglion; Kindlin 1; Spinal cord

Indexed keywords

ALPHA9 INTEGRIN; INTEGRIN; KINDLIN 1 PROTEIN; PROTEOCHONDROITIN SULFATE; REGULATOR PROTEIN; TENASCIN; UNCLASSIFIED DRUG; CALCITONIN GENE RELATED PEPTIDE; KINDLIN-1 PROTEIN, RAT; NERVE PROTEIN;

ADENO ASSOCIATED VIRUS; ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPIFLUORESCENCE MICROSCOPY; EXPERIMENTAL LOCOMOTOR ACTIVITY TEST; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPINAL CORD; SPINAL GANGLION; ANIMAL; AXON; CELL CULTURE; CYTOLOGY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HEMISPHERIC DOMINANCE; METABOLISM; NERVE REGENERATION; NEURITE; PATHOPHYSIOLOGY; PHYSIOLOGY; PRESSURE; SPINAL CORD INJURY; SPRAGUE DAWLEY RAT; WALKING;

ANIMALS; AXONS; CALCITONIN GENE-RELATED PEPTIDE; CELLS, CULTURED; CHONDROITIN SULFATE PROTEOGLYCANS; DISEASE MODELS, ANIMAL; FEMALE; FUNCTIONAL LATERALITY; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; INTEGRINS; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEURITES; PRESSURE; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SPINAL CORD INJURIES; WALKING;

EID: 84977543684     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0901-16.2016     Document Type: Article

References (58)

1. Alto LT, Havton LA, Conner JM, Hollis ER 2nd, Blesch A, Tuszynski MH (2009) Chemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury. Nat Neurosci 12:1106-1113. CrossRef Medline
2. Anderson KD (2004) Targeting recovery: priorities of the spinal cordinjured population. J Neurotrauma 21:1371-1383. CrossRef Medline
3. Andrews MR, Czvitkovich S, Dassie E, Vogelaar CF, Faissner A, Blits B, Gage FH, ffrench-Constant C, Fawcett JW (2009) Alpha9 integrin promotes neurite outgrowth on tenascin-C and enhances sensory axon regeneration. J Neurosci 29:5546-5557. CrossRef Medline
4. Arthur WT, Petch LA, Burridge K (2000) Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr Biol 10:719-722. CrossRef Medline
5. 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. CrossRef Medline
6. Bonner JF, Connors TM, Silverman WF, Kowalski DP, Lemay MA, Fischer I (2011) Grafted neural progenitors integrate and restore synaptic connectivity across the injured spinal cord. J Neurosci 31:4675-4686. CrossRef Medline
7. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640. CrossRef Medline
8. Cafferty WB, Yang SH, Duffy PJ, Li S, Strittmatter SM (2007) Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J Neurosci 27:2176-2185. CrossRef Medline
9. Carulli D, Rhodes KE, Brown DJ, Bonnert TP, Pollack SJ, Oliver K, Strata P, Fawcett JW (2006) Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components. J Comp Neurol 494:559-577. CrossRef Medline
10. Carulli D, Pizzorusso T, Kwok JC, Putignano E, Poli A, Forostyak S, Andrews MR, Deepa SS, Glant TT, Fawcett JW (2010) Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133:2331-2347. CrossRef Medline
11. Chiu IM, Barrett LB, Williams EK, Strochlic DE, Lee S, Weyer AD, Lou S, Bryman GS, Roberson DP, Ghasemlou N, Piccoli C, Ahat E, Wang V, Cobos EJ, Stucky CL, Ma Q, Liberles SD, Woolf CJ (2014) Transcriptional profiling at whole population and single cell levels reveals somatosensory neuron molecular diversity. Elife 3. CrossRef Medline
12. Condic ML (2001) Adult neuronal regeneration induced by transgenic integrin expression. J Neurosci 21:4782-4788. Medline
13. 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. CrossRef Medline
14. Eva R, Dassie E, Caswell PT, Dick G, ffrench-Constant C, Norman JC, Fawcett JW (2010) Rab11 and its effector Rab coupling protein contribute to the trafficking of β1 integrins during axon growth in adult dorsal root ganglion neurons and PC12 cells. J Neurosci 30:11654-11669. CrossRef Medline
15. Eva R, Crisp S, Marland JR, Norman JC, Kanamarlapudi V, ffrench-Constant C, Fawcett JW (2012) ARF6 directs axon transport and traffic of integrins and regulates axon growth in adult DRG neurons. J Neurosci 32: 10352-10364. CrossRef Medline
16. Fagoe ND, Attwell CL, Kouwenhoven D, Verhaagen J, Mason MR (2015) Overexpression of ATF3 or the combination of ATF3, c-Jun, STAT3 and Smad1 promotes regeneration of the central axon branch of sensory neurons but without synergistic effects. Hum Mol Genet 24:6788-6800. CrossRef Medline
17. Franssen EH, Zhao RR, Koseki H, Kanamarlapudi V, Hoogenraad CC, Eva R, Fawcett JW (2015) Exclusion of integrins from CNS axons is regulated by Arf6 activation and the AIS. J Neurosci 35:8359-8375. CrossRef Medline
18. Friedlander DR, Milev P, Karthikeyan L, Margolis RK, Margolis RU, Grumet M (1994) The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J Cell Biol 125:669-680. CrossRef Medline
19. 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. CrossRef Medline
20. Gardiner NJ, Moffatt S, Fernyhough P, Humphries MJ, Streuli CH, Tomlinson DR (2007) Preconditioning injury-induced neurite outgrowth of adult rat sensory neurons on fibronectin is mediated by mobilisation of axonal alpha5 integrin. Mol Cell Neurosci 35:249-260. CrossRef Medline
21. Hammarberg H, Wallquist W, Piehl F, Risling M, Cullheim S (2000) Regulation of laminin-associated integrin subunit mRNAs in rat spinal motoneurons during postnatal development and after axonal injury. J Comp Neurol 428:294-304. CrossRef Medline
22. Heintz TG, Heller JP, Zhao R, Caceres A, Eva R, Fawcett JW (2014) Kinesin KIF4A transports integrin beta1 in developing axons of cortical neurons. Mol Cell Neurosci 63:60-71. CrossRef Medline
23. Hermens WT, ter Brake O, Dijkhuizen PA, Sonnemans MA, Grimm D, Kleinschmidt JA, Verhaagen J (1999) Purification of recombinant adenoassociated virus by iodixanol gradient ultracentrifugation allows rapid and reproducible preparation of vector stocks for gene transfer in the nervous system. Hum Gene Ther 10:1885-1891. CrossRef Medline
24. Hu F, Strittmatter SM (2008) The N-terminal domain of Nogo-A inhibits cell adhesion and axonal outgrowth by an integrin-specific mechanism. J Neurosci 28:1262-1269. CrossRef Medline
25. Joester A, Faissner A (1999) Evidence for combinatorial variability of tenascin-C isoforms and developmental regulation in the mouse central nervous system. J Biol Chem 274:17144-17151. CrossRef Medline
26. Kwok JC, Yang S, Fawcett JW (2014) Neural ECM in regeneration and rehabilitation. Prog Brain Res 214:179-192. CrossRef Medline
27. Lein PJ, Higgins D, Turner DC, Flier LA, Terranova VP (1991) The NC1 domain of type IV collagen promotes axonal growth in sympathetic neurons through interaction with the alpha 1 beta 1 integrin. J Cell Biol 113:417-428. CrossRef Medline
28. Lundell A, Olin AI, Mörgelin M, al-Karadaghi S, Aspberg A, Logan DT (2004) Structural basis for interactions between tenascins and lectican C-type lectin domains: evidence for a crosslinking role for tenascins. Structure 12:1495-1506. CrossRef Medline
29. Luo X, Salgueiro Y, Beckerman SR, Lemmon VP, Tsoulfas P, Park KK (2013) Three-dimensional evaluation of retinal ganglion cell axon regeneration and pathfinding in whole mouse tissue after injury. Exp Neurol 247:653-662. CrossRef Medline
30. Mason MR, Ehlert EM, Eggers R, Pool CW, Hermening S, Huseinovic A, Timmermans E, Blits B, Verhaagen J (2010) Comparison of AAV serotypes for gene delivery to dorsal root ganglion neurons. Mol Ther 18: 715-724. CrossRef Medline
31. McPhail LT, Borisoff JF, Tsang B, Hwi LP, Kwiecien JM, Ramer MS (2007) Protracted myelin clearance hinders central primary afferent regeneration following dorsal rhizotomy and delayed neurotrophin-3 treatment. Neurosci Lett 411:206-211. CrossRef Medline
32. Mercado ML, Nur-e-Kamal A, Liu HY, Gross SR, Movahed R, Meiners S (2004) Neurite outgrowth by the alternatively spliced region of human tenascin-C is mediated by neuronal alpha7beta1 integrin. J Neurosci 24: 238-247. CrossRef Medline
33. Milev P, Fischer D, Häring M, Schulthess T, Margolis RK, Chiquet-Ehrismann R, Margolis RU (1997) The fibrinogen-like globe of tenascin-C mediates its interactions with neurocan and phosphacan/ protein-tyrosine phosphatase-zeta/beta. J Biol Chem 272:15501-15509. CrossRef Medline
34. Monnier PP, Sierra A, Schwab JM, Henke-Fahle S, Mueller BK (2003) The Rho/ROCK pathway mediates neurite growth-inhibitory activity associated with the chondroitin sulfate proteoglycans of the CNS glial scar. Mol Cell Neurosci 22:319-330. CrossRef Medline
35. Moon LD, Asher RA, Rhodes KE, Fawcett JW (2001) Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat Neurosci 4:465-466. Medline
36. Moser M, Legate KR, Zent R, Fässler R (2009) The tail of integrins, talin, and kindlins. Science 324:895-899. CrossRef Medline
37. Neugebauer KM, Emmett CJ, Venstrom KA, Reichardt LF (1991) Vitronectin and thrombospondin promote retinal neurite outgrowth: developmental regulation and role of integrins. Neuron 6:345-358. CrossRef Medline
38. Niederöst B, Oertle T, Fritsche J, McKinney RA, Bandtlow CE (2002) Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Rac1. J Neurosci 22: 10368-10376. Medline
39. Novak A, Hsu SC, Leung-Hagesteijn C, Radeva G, Papkoff J, Montesano R, Roskelley C, Grosschedl R, Dedhar S (1998) Cell adhesion and the integrin-linked kinase regulate the LEF-1 and beta-catenin signaling pathways. Proc Natl Acad Sci USA 95:4374-4379. CrossRef Medline
40. Pasterkamp RJ, Verhaagen J (2006) Semaphorins in axon regeneration: developmental guidance molecules gone wrong? Philos Trans R Soc Lond B Biol Sci 361:1499-1511. CrossRef Medline
41. Probstmeier R, Pesheva P (1999) Tenascin-C inhibits beta1 integrindependent cell adhesion and neurite outgrowth on fibronectin by a disialoganglioside-mediated signaling mechanism. Glycobiology 9: 101-114. CrossRef Medline
42. Probstmeier R, Braunewell K, Pesheva P (2000) Involvement of chondroitin sulfates on brain-derived tenascin-R in carbohydrate-dependent interac-tions with fibronectin and tenascin-C. Brain Res 863:42-51. CrossRef Medline
43. Rogalski TM, Mullen GP, Gilbert MM, Williams BD, Moerman DG (2000) The UNC-112 gene in Caenorhabditis elegans encodes a novel component of cell-matrix adhesion structures required for integrin localization in the muscle cell membrane. J Cell Biol 150:253-264. CrossRef Medline
44. Rognoni E, Ruppert R, Fässler R (2016) The kindlin family: functions, signaling properties and implications for human disease. J Cell Sci 129: 17-27. CrossRef Medline
45. Schaller MD, Otey CA, Hildebrand JD, Parsons JT (1995) Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains. J Cell Biol 130:1181-1187. CrossRef Medline
46. Staniszewska I, Sariyer IK, Lecht S, Brown MC, Walsh EM, Tuszynski GP, Safak M, Lazarovici P, Marcinkiewicz C (2008) Integrin alpha9 beta1 is a receptor for nerve growth factor and other neurotrophins. J Cell Sci 121:504-513. CrossRef Medline
47. Takahashi Y, Nakajima Y (1996) Dermatomes in the rat limbs as determined by antidromic stimulation of sensory C-fibers in spinal nerves. Pain 67:197-202. CrossRef Medline
48. Tan CL, Kwok JC, Patani R, Ffrench-Constant C, Chandran S, Fawcett JW (2011) Integrin activation promotes axon growth on inhibitory chondroitin sulfate proteoglycans by enhancing integrin signaling. J Neurosci 31:6289-6295. CrossRef Medline
49. Tan CL, Andrews MR, Kwok JC, Heintz TG, Gumy LF, Fässler R, Fawcett JW (2012) Kindlin-1 enhances axon growth on inhibitory chondroitin sulfate proteoglycans and promotes sensory axon regeneration. J Neurosci 32:7325-7335. CrossRef Medline
50. Tan CL, Kwok JC, Heller JP, Zhao R, Eva R, Fawcett JW (2015) Full length talin stimulates integrin activation and axon regeneration. Mol Cell Neurosci 68:1-8. CrossRef Medline
51. Theodosiou M, Widmaier M, Bottcher RT, Rognoni E, Veelders M, Bharadwaj M, Lambacher A, Austen K, Muller DJ, Zent R, Fassler R (2016) Kindlin-2 cooperates with talin to activate integrins and induces cell spreading by directly binding paxillin. Elife 5. CrossRef Medline
52. Tucker RP, Chiquet-Ehrismann R (2015) Tenascin-C: its functions as an integrin ligand. Int J Biochem Cell Biol 65:165-168. CrossRef Medline
53. Ussar S, Wang HV, Linder S, Fässler R, Moser M (2006) The Kindlins: subcellular localization and expression during murine development. Exp Cell Res 312:3142-3151. CrossRef Medline
54. Vogelezang MG, Liu Z, Relvas JB, Raivich G, Scherer SS, ffrench-Constant C (2001) Alpha4 integrin is expressed during peripheral nerve regeneration and enhances neurite outgrowth. J Neurosci 21:6732-6744. Medline
55. 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. CrossRef Medline
56. Wang R, King T, Ossipov MH, Rossomando AJ, Vanderah TW, Harvey P, Cariani P, Frank E, Sah DW, Porreca F (2008) Persistent restoration of sensory function by immediate or delayed systemic artemin after dorsal root injury. Nat Neurosci 11:488-496. CrossRef Medline
57. Wong LE, Gibson ME, Arnold HM, Pepinsky B, Frank E (2015) Artemin promotes functional long-distance axonal regeneration to the brainstem after dorsal root crush. Proc Natl Acad Sci USA 112:6170-6175. CrossRef Medline
58. Wu A, Lauschke JL, Morris R, Waite PM (2009) Characterization of rat forepaw function in two models of cervical dorsal root injury. J Neurotrauma 26:17-29. CrossRef Medline