Axonal neuregulin 1 is a rate limiting but not essential factor for nerve remyelination

Brain

Volumn 136, Issue 7, 2013, Pages 2279-2297

  Fricker, Florence R ^a   Antunes Martins, Ana ^b   Galino, Jorge ^b   Paramsothy, Remi ^b   La Russa, Federica ^b   Perkins, James ^c   Goldberg, Rebecca ^b   Brelstaff, Jack ^b   Zhu, Ning ^a   McMahon, Stephen B ^b   Orengo, Christine ^c   Garratt, Alistair N ^d,e   Birchmeier, Carmen ^d,e   Bennett, David L H ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

injury; Nrg1; regeneration; remyelination; Schwann

Indexed keywords

CRE RECOMBINASE; MUTANT PROTEIN; MYELIN; NEU DIFFERENTIATION FACTOR; TAMOXIFEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CONVALESCENCE; ENZYME INDUCTION; GENE EXPRESSION; GENE LOSS; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; INJURY SEVERITY; MACROPHAGE; MOUSE; MYELINATION; NERVE ANASTOMOSIS; NERVE CRUSH; NERVE FIBER; NERVE FIBER REGENERATION; NERVE TRANSECTION; NONHUMAN; PRIORITY JOURNAL; REMYELINIZATION; SCHWANN CELL; SCIATIC NERVE INJURY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; WALLERIAN DEGENERATION;

EID: 84879974062     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt148     Document Type: Article

References (65)

1. Arthur-Farraj P, Wanek K, Hantke J, Davis CM, Jayakar A, Parkinson DB, et al. Mouse schwann cells need both NRG1 and cyclic AMP to myelinate. Glia 2011; 59: 750-33
2. Arthur-Farraj PJ, Latouche M, Wilton DK, Quintes S, Chabrol E, Banerjee A, et al. c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron 2012; 75: 633-47
3. Atanasoski S, Scherer SS, Sirkowski E, Leone D, Garratt AN, Birchmeier C, et al. ErbB2 signaling in schwann cells is mostly dispensable for maintenance of myelinated peripheral nerves and proliferation of adult schwann cells after injury. J Neurosci 2006; 26: 2124-31
4. Bain JR, Mackinnon SE, Hunter DA. Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plast Reconstr Surg 1989; 83: 129-38
5. Bermingham-McDonogh O, Xu YT, Marchionni MA, Scherer SS. Neuregulin expression in PNS neurons: Isoforms and regulation by target interactions. Mol Cell Neurosci 1997; 10: 184-95
6. Birchmeier C, Nave KA. Neuregulin-1, a key axonal signal that drives Schwann cell growth and differentiation. Glia 2008; 56: 1491-7
7. Bradley WG, Asbury AK. Duration of synthesis phase in neuilemma cells in mouse sciatic nerve during degeneration. Exp Neurol 1970; 26: 275-82
8. Bremer M, Frob F, Kichko T, Reeh P, Tamm ER, Suter U, et al. Sox10 is required for Schwann-cell homeostasis and myelin maintenance in the adult peripheral nerve. Glia 2011; 59: 1022-32
9. Brinkmann BG, Agarwal A, Sereda MW, Garratt AN, Muller T, Wende H, et al. Neuregulin-1/ErbB signaling serves distinct functions in myelination of the peripheral and central nervous system. Neuron 2008; 59: 581-95
10. Carroll SL, Miller ML, Frohnert PW, Kim SS, Corbett JA. Expression of neuregulins and their putative receptors, ErbB2 and ErbB3, is induced during Wallerian degeneration. J Neurosci 1997; 17: 1642-59
11. Chen LE, Liu K, Seaber AV, Katragadda S, Kirk C, Urbaniak Jr. Recombinant human glial growth factor 2 (rhGGF2) improves functional recovery of crushed peripheral nerve (a double-blind study). Neurochem Int 1998; 33: 341-51
12. Chen S, Rio C, Ji RR, Dikkes P, Coggeshall RE, Woolf CJ, et al. Disruption of ErbB receptor signaling in adult non-myelinating Schwann cells causes progressive sensory loss. Nat Neurosci 2003; 6: 1186-93
13. Chen S, Velardez MO, Warot X, Yu ZX, Miller SJ, Cros D, et al. Neuregulin 1-erbB signaling is necessary for normal myelination and sensory function. J Neurosci 2006; 26: 3079-86
14. Chen ZL, Yu WM, Strickland S. Peripheral regeneration. Annu Rev Neurosci 2007; 30: 209-33
15. Cohen JA, Yachnis AT, Arai M, Davis JG, Scherer SS. Expression of the neu proto-oncogene by Schwann cells during peripheral nerve development and Wallerian degeneration. J Neurosci Res 1992; 31: 622-34
16. Coleman MP, Freeman MR. Wallerian degeneration, wld(s), and nmnat. Annu Rev Neurosci 2010; 33: 245-67
17. Decker L, Desmarquet-Trin-Dinh C, Taillebourg E, Ghislain J, Vallat JM, Charnay P. Peripheral myelin maintenance is a dynamic process requiring constant Krox20 expression. J Neurosci 2006; 26: 9771-9
18. Dong Z, Brennan A, Liu N, Yarden Y, Lefkowitz G, Mirsky R, et al. Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 1995; 15: 585-96
19. Duncan D. A relation between axone diameter and myelination determined by measurement of myelinated spinal root fibers. J Comp Neurol 1934; 60: 437-71
20. Fancy SP, Chan JR, Baranzini SE, Franklin RJ, Rowitch DH. Myelin regeneration: A recapitulation of development? Ann Rev Neurosci 2011; 34: 21-43
21. Fricker FR, Bennett DL. The role of neuregulin-1 in the response to nerve injury. Future Neurol 2011; 6: 809-22
22. Fricker FR, Zhu N, Tsantoulas C, Abrahamsen B, Nassar MA, Thakur M, et al. Sensory axon-Derived neuregulin-1 is required for axoglial signaling and normal sensory function but not for long-Term axon maintenance. J Neurosci 2009; 29: 7667-78
23. Fricker FR, Lago N, Balarajah S, Tsantoulas C, Tanna S, Zhu N, et al. Axonally derived neuregulin-1 is required for remyelination and regeneration after nerve injury in adulthood. J Neurosci 2011; 31: 3225-33
24. Garratt AN, Voiculescu O, Topilko P, Charnay P, Birchmeier C. A dual role of erbB2 in myelination and in expansion of the schwann cell precursor pool. J Cell Biol 2000; 148: 1035-46
25. Griffin JW, Thompson WJ. Biology and pathology of nonmyelinating Schwann cells. Glia 2008; 56: 1518-31
26. Guy J, Gan J, Selfridge J, Cobb S, Bird A. Reversal of neurological defects in a mouse model of Rett syndrome. Science 2007; 315: 1143-7
27. Hayashi S, McMahon AP. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: A tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 2002; 244: 305-18
28. Hu X, Hicks CW, He W, Wong P, Macklin WB, Trapp BD, et al. Bace1 modulates myelination in the central and peripheral nervous system. Nat Neurosci 2006; 9: 1520-5
29. Hu X, He W, Diaconu C, Tang X, Kidd GJ, Macklin WB, et al. Genetic deletion of BACE1 in mice affects remyelination of sciatic nerves. FASEB J 2008; 22: 2970-80
30. Inserra MM, Bloch DA, Terris DJ. Functional indices for sciatic, peroneal, and posterior tibial nerve lesions in the mouse. Microsurgery 1998; 18: 119-24
31. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of affymetrix genechip probe level data. Nucleic Acids Res 2003; 31: E15
32. Jessen KR, Mirsky R. Negative regulation of myelination: Relevance for development, injury, and demyelinating disease. Glia 2008; 56: 1552-65
33. Joung I, Yoo M, Woo JH, Chang CY, Heo H, Kwon YK. Secretion of EGF-like domain of heregulinbeta promotes axonal growth and functional recovery of injured sciatic nerve. Mol Cells 2010; 30: 477-84
34. Kwon YK, Bhattacharyya A, Alberta JA, Giannobile WV, Cheon K, Stiles CD, et al. Activation of ErbB2 during wallerian degeneration of sciatic nerve. J Neurosci 1997; 17: 8293-9
35. Lauria G, Cornblath DR, Johansson O, McArthur JC, Mellgren SI, Nolano M, et al. EFNS guidelines on the use of skin biopsy in the diagnosis of peripheral neuropathy. Eur J Neurol 2005; 12: 747-58
36. Le N, Nagarajan R, Wang JY, Araki T, Schmidt RE, Milbrandt J. Analysis of congenital hypomyelinating Egr2Lo/Lo nerves identifies Sox2 as an inhibitor of Schwann cell differentiation and myelination. Proc Natl Acad Sci USA 2005; 102: 2596-601
37. Li L, Cleary S, Mandarano MA, Long W, Birchmeier C, Jones FE. The breast proto-oncogene, HRGalpha regulates epithelial proliferation and lobuloalveolar development in the mouse mammary gland. Oncogene 2002; 21: 4900-7
38. Mahanthappa NK, Anton ES, Matthew WD. Glial growth factor 2, a soluble neuregulin, directly increases Schwann cell motility and indirectly promotes neurite outgrowth. J Neurosci 1996; 16: 4673-83
39. Meyer D, Birchmeier C. Multiple essential functions of neuregulin in development. Nature 1995; 378: 386-90
40. Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B, Birchmeier C, et al. Axonal neuregulin-1 regulates myelin sheath thickness. Science 2004; 304: 700-3
41. Monk KR, Oshima K, Jors S, Heller S, Talbot WS. Gpr126 is essential for peripheral nerve development and myelination in mammals. Development 2011; 138: 2673-80
42. Monte-Raso VV, Barbieri CH, Mazzer N, Yamasita AC, Barbieri G. Is the Sciatic Functional Index always reliable and reproducible? J Neurosci Methods 2008; 170: 255-61
43. Morrissey TK, Levi AD, Nuijens A, Sliwkowski MX, Bunge RP. Axoninduced mitogenesis of human Schwann cells involves heregulin and p185erbB2. Proc Natl Acad Sci USA 1995; 92: 1431-5
44. Napoli I, Noon LA, Ribeiro S, Kerai AP, Parrinello S, Rosenberg LH, et al. A central role for the ERK-signaling pathway in controlling Schwann cell plasticity and peripheral nerve regeneration in vivo. Neuron 2012; 73: 729-42
45. Parkinson DB, Bhaskaran A, Droggiti A, Dickinson S, Dántonio M, Mirsky R, et al. Krox-20 inhibits Jun-NH2-Terminal kinase/c-Jun to control Schwann cell proliferation and death. J Cell Biol 2004; 164: 385-94
46. Pellegrino RG, Spencer PS. Schwann cell mitosis in response to regenerating peripheral axons in vivo. Brain Res 1985; 341: 16-25
47. Perlin JR, Lush ME, Stephens WZ, Piotrowski T, Talbot WS. Neuronal Neuregulin 1 type III directs Schwann cell migration. Development 2011; 138: 4639-48
48. Salzer JL, Williams AK, Glaser L, Bunge RP. Studies of Schwann cell proliferation. II. Characterization of the stimulation and specificity of the response to a neurite membrane fraction. J Cell Biol 1980; 84: 753-66
49. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004; 3. Article3
50. Stassart RM, Fledrich R, Velanac V, Brinkmann BG, Schwab MH, Meijer D, et al. A role for Schwann cell-Derived neuregulin-1 in remyelination. Nat Neurosci 2013; 16: 48-54
51. Stoll G, Muller HW. Nerve injury, axonal degeneration and neural regeneration: Basic insights. Brain Pathol 1999; 9: 313-25
52. Stoll G, Griffin JW, Li CY, Trapp BD. Wallerian degeneration in the peripheral nervous system: Participation of both Schwann cells and macrophages in myelin degradation. J Neurocytol 1989; 18: 671-83
53. Syed N, Reddy K, Yang DP, Taveggia C, Salzer JL, Maurel P, et al. Soluble neuregulin-1 has bifunctional, concentration-Dependent effects on Schwann cell myelination. J Neurosci 2010; 30: 6122-31
54. Taveggia C, Feltri ML, Wrabetz L. Signals to promote myelin formation and repair. Nat Rev Neurol 2010; 6: 276-87
55. Taveggia C, Zanazzi G, Petrylak A, Yano H, Rosenbluth J, Einheber S, et al. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 2055; 47: 681-94
56. Tawk M, Makoukji J, Belle M, Fonte C, Trousson A, Hawkins T, et al. Wnt/beta-catenin signaling is an essential and direct driver of myelin gene expression and myelinogenesis. J Neurosci 2011; 31: 3729-42
57. Terenghi G. Peripheral nerve regeneration and neurotrophic factors. J Anat 1999; 194 (Pt 1): 1-14
58. Theocharidis A, van Dongen S, Enright AJ, Freeman TC. Network visualization and analysis of gene expression data using BioLayout Express(3D). Nat Protoc 2009; 4: 1535-50
59. Voyvodic JT. Target size regulates calibre and myelination of sympathetic axons. Nature 1989; 342: 430-3
60. Willem M, Garratt AN, Novak B, Citron M, Kaufmann S, Rittger A, et al. Control of peripheral nerve myelination by the beta-secretase BACE1. Science 2006; 314: 664-6
61. Woodhoo A, Alonso MB, Droggiti A, Turmaine M, Dántonio M, Parkinson DB, et al. Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat Neurosci 2009; 12: 839-47
62. Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM, et al. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 2001; 30: 399-410
63. Yildiz M, Karlidag T, Yalcin S, Ozogul C, Keles E, Alpay HC, et al. Efficacy of glial growth factor and nerve growth factor on the recovery of traumatic facial paralysis. Eur Arch Otorhinolaryngol 2011; 268: 1127-33
64. Young P, Qiu L, Wang D, Zhao S, Gross J, Feng G. Single-neuron labeling with inducible Cre-mediated knockout in transgenic mice. Nat Neurosci 2008; 11: 721-8
65. Zanazzi G, Einheber S, Westreich R, Hannocks MJ, Bedell-Hogan D, Marchionni MA, et al. Glial growth factor/neuregulin inhibits Schwann cell myelination and induces demyelination. J Cell Biol 2001; 152: 1289-99