Nrg1/ErbB signaling networks in Schwann cell development and myelination

Seminars in Cell and Developmental Biology

Volumn 21, Issue 9, 2010, Pages 922-928

  Newbern, Jason ^a   Birchmeier, Carmen ^b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Erbin; Erk; Myelination; Neuregulin; Shp2

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FOCAL ADHESION KINASE; G PROTEIN COUPLED RECEPTOR; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEU DIFFERENTIATION FACTOR; NOTCH RECEPTOR; PROTEIN CDC42; RAC1 PROTEIN;

CELL LINEAGE; DEVELOPMENTAL STAGE; HUMAN; IN VIVO STUDY; MYELINATION; NERVE CELL GROWTH; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; REVIEW; SCHWANN CELL; SIGNAL TRANSDUCTION;

EID: 78449298649     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2010.08.008     Document Type: Review

References (92)

1. Bargmann C.I., Hung M.C., Weinberg R.A. The neu oncogene encodes an epidermal growth factor receptor-related protein. Nature 1986, 319(6050):226-230.
2. Downward J., Yarden Y., Mayes E., Scrace G., Totty N., Stockwell P., et al. Close similarity of epidermal growth factor receptor and v-erb-B oncogene protein sequences. Nature 1984, 307(5951):521-527.
3. Zhang H., Berezov A., Wang Q., Zhang G., Drebin J., Murali R., et al. ErbB receptors: from oncogenes to targeted cancer therapies. J Clin Invest 2007, 117(8):2051-2058.
4. Yarden Y.M.X., Sliwkowski Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001, 2(2):127-137.
5. Burgess A.W., Cho H.S., Eigenbrot C., Ferguson K.M., Garrett T.P., Leahy D.J., et al. An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol Cell 2003, 12(3):541-552.
6. Pawson T. Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 2004, 116(2):191-203.
7. Jones R.B., Gordus A., Krall J.A., MacBeath G. A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature 2006, 439(7073):168-174.
8. Birchmeier C., Nave K.A. Neuregulin-1, a key axonal signal that drives Schwann cell growth and differentiation. Glia 2008, 56(14):1491-1497.
9. Citri A., Skaria K.B., Yarden Y. The deaf and the dumb: the biology of ErbB-2 and ErbB-3. Exp Cell Res 2003, 284(1):54-65.
10. Meyer D., Yamaai T., Garratt A., Riethmacher-Sonnenberg E., Kane D., Theill L.E., et al. Isoform-specific expression and function of neuregulin. Development 1997, 124(18):3575-3586.
11. 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 2005, 47(5):681-694.
12. Jessen K.R., Mirsky R. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 2005, 6(9):671-682.
13. Shah N.M., Marchionni M.A., Isaacs I., Stroobant P., Anderson D.J. Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 1994, 77(3):349-360.
14. Aquino J.B., Hjerling-Leffler J., Koltzenburg M., Edlund T., Villar M.J., Ernfors P. In vitro and in vivo differentiation of boundary cap neural crest stem cells into mature Schwann cells. Exp Neurol 2006, 198(2):438-449.
15. Dong Z., Sinanan A., Parkinson D., Parmantier E., Mirsky R., Jessen K.R. Schwann cell development in embryonic mouse nerves. J Neurosci Res 1999, 56(4):334-348.
16. Meyer D., Birchmeier C. Multiple essential functions of neuregulin in development. Nature 1995, 378(6555):386-390.
17. Riethmacher D., Sonnenberg-Riethmacher E., Brinkmann V., Yamaai T., Lewin G.R., Birchmeier C. Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 1997, 389(6652):725-730.
18. Morris J.K., Lin W., Hauser C., Marchuk Y., Getman D., Lee K.F. Rescue of the cardiac defect in ErbB2 mutant mice reveals essential roles of ErbB2 in peripheral nervous system development. Neuron 1999, 23(2):273-283.
19. Woldeyesus M.T., Britsch S., Riethmacher D., Xu L., Sonnenberg-Riethmacher E., Abou-Rebyeh F., et al. Peripheral nervous system defects in erbB2 mutants following genetic rescue of heart development. Genes Dev 1999, 13(19):2538-2548.
20. Lin W., Sanchez H.B., Deerinck T., Morris J.K., Ellisman M., Lee K.F. Aberrant development of motor axons and neuromuscular synapses in erbB2-deficient mice. Proc Natl Acad Sci USA 2000, 97(3):1299-1304.
21. Britsch S., Li L., Kirchhoff S., Theuring F., Brinkmann V., Birchmeier C., et al. The ErbB2 and ErbB3 receptors and their ligand, neuregulin-1, are essential for development of the sympathetic nervous system. Genes Dev 1998, 12(12):1825-1836.
22. Lyons D.A., Pogoda H.M., Voas M.G., Woods I.G., Diamond B., Nix R., et al. erbb3 and erbb2 are essential for schwann cell migration and myelination in zebrafish. Curr Biol 2005, 15(6):513-524.
23. Leimeroth R., Lobsiger C., Lussi A., Taylor V., Suter U., Sommer L. Membrane-bound neuregulin1 type III actively promotes Schwann cell differentiation of multipotent Progenitor cells. Dev Biol 2002, 246(2):245-258.
24. Murphy P., Topilko P., Schneider-Maunoury S., Seitanidou T., Baron-Van Evercooren A., Charnay P. The regulation of Krox-20 expression reveals important steps in the control of peripheral glial cell development. Development 1996, 122(9):2847-2857.
25. Garratt A.N., 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(5):1035-1046.
26. Michailov G.V., Sereda M.W., Brinkmann B.G., Fischer T.M., Haug B., Birchmeier C., et al. Axonal neuregulin-1 regulates myelin sheath thickness. Science 2004, 304(5671):700-703.
27. Chen S., Velardez M.O., Warot X., Yu Z.X., Miller S.J., Cros D., et al. Neuregulin 1-erbB signaling is necessary for normal myelination and sensory function. J Neurosci 2006, 26(12):3079-3086.
28. Smith K.J., Blakemore W.F., Murray J.A., Patterson R.C. Internodal myelin volume and axon surface area. A relationship determining myelin thickness?. J Neurol Sci 1982, 55(2):231-246.
29. Fricker F.R., Zhu N., Tsantoulas C., Abrahamsen B., Nassar M.A., 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(24):7667-7678.
30. Chen S., Rio C., Ji R.R., Dikkes P., Coggeshall R.E., Woolf C.J., et al. Disruption of ErbB receptor signaling in adult non-myelinating Schwann cells causes progressive sensory loss. Nat Neurosci 2003, 6(11):1186-1193.
31. Cohen J.A., Yachnis A.T., Arai M., Davis J.G., Scherer S.S. Expression of the neu proto-oncogene by Schwann cells during peripheral nerve development and Wallerian degeneration. J Neurosci Res 1992, 31(4):622-634.
32. Chen M.S., Bermingham-McDonogh O., Danehy F.T., Nolan C., Scherer S.S., Lucas J., et al. Expression of multiple neuregulin transcripts in postnatal rat brains. J Comp Neurol 1994, 349(3):389-400.
33. Grinspan J.B., Marchionni M.A., Reeves M., Coulaloglou M., Scherer S.S. Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: neuregulin receptors and the role of neuregulins. J Neurosci 1996, 16(19):6107-6118.
34. Trachtenberg J.T., Thompson W.J. Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor. Nature 1996, 379(6561):174-177.
35. Atanasoski S., Scherer S.S., Sirkowski E., Leone D., Garratt A.N., 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(7):2124-2131.
36. Tapinos N., Ohnishi M., Rambukkana A. ErbB2 receptor tyrosine kinase signaling mediates early demyelination induced by leprosy bacilli. Nat Med 2006, 12(8):961-966.
37. Hippenmeyer S., Shneider N.A., Birchmeier C., Burden S.J., Jessell T.M., Arber S. A role for neuregulin1 signaling in muscle spindle differentiation. Neuron 2002, 36(6):1035-1049.
38. Vassar R., Bennett B.D., Babu-Khan S., Kahn S., Mendiaz E.A., Denis P., et al. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 1999, 286(5440):735-741.
39. Willem M., Garratt A.N., Novak B., Citron M., Kaufmann S., Rittger A., et al. Control of peripheral nerve myelination by the beta-secretase BACE1. Science 2006, 314(5799):664-666.
40. Hu X., Hicks C.W., He W., Wong P., Macklin W.B., Trapp B.D., et al. Bace1 modulates myelination in the central and peripheral nervous system. Nat Neurosci 2006, 9(12):1520-1525.
41. Blobel C.P. ADAMs: key components in EGFR signalling and development. Nat Rev Mol Cell Biol 2005, 6(1):32-43.
42. Daub H., Weiss F.U., Wallasch C., Ullrich A. Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 1996, 379(6565):557-560.
43. Montero J.C., Yuste L., Diaz-Rodriguez E., Esparis-Ogando A., Pandiella A. Differential shedding of transmembrane neuregulin isoforms by the tumor necrosis factor-alpha-converting enzyme. Mol Cell Neurosci 2000, 16(5):631-648.
44. Shirakabe K., Wakatsuki S., Kurisaki T., Fujisawa-Sehara A. Roles of Meltrin beta/ADAM19 in the processing of neuregulin. J Biol Chem 2001, 276(12):9352-9358.
45. Wang J.Y., Miller S.J., Falls D.L. The N-terminal region of neuregulin isoforms determines the accumulation of cell surface and released neuregulin ectodomain. J Biol Chem 2001, 276(4):2841-2851.
46. Ohno M., Hiraoka Y., Matsuoka T., Tomimoto H., Takao K., Miyakawa T., et al. Nardilysin regulates axonal maturation and myelination in the central and peripheral nervous system. Nat Neurosci 2009, 12(12):1506-1513.
47. Kaech S.M., Whitfield C.W., Kim S.K. The LIN-2/LIN-7/LIN-10 complex mediates basolateral membrane localization of the C. elegans EGF receptor LET-23 in vulval epithelial cells. Cell 1998, 94(6):761-771.
48. Borg J.P., Marchetto S., Le Bivic A., Ollendorff V., Jaulin-Bastard F., Saito H., et al. ERBIN: a basolateral PDZ protein that interacts with the mammalian ERBB2/HER2 receptor. Nat Cell Biol 2000, 2(7):407-414.
49. Arikkath J., Israely I., Tao Y., Mei L., Liu X., Reichardt L.F. Erbin controls dendritic morphogenesis by regulating localization of delta-catenin. J Neurosci 2008, 28(28):7047-7056.
50. Dai F., Chang C., Lin X., Dai P., Mei L., Feng X.H. Erbin inhibits transforming growth factor beta signaling through a novel Smad-interacting domain. Mol Cell Biol 2007, 27(17):6183-6194.
51. 2+ channels through relief of an autoinhibitory domain in the Ca(v)1.3 alpha1 subunit. J Neurosci 2007, 27(6):1374-1385.
52. Favre B., Fontao L., Koster J., Shafaatian R., Jaunin F., Saurat J.H., et al. The hemidesmosomal protein bullous pemphigoid antigen 1 and the integrin beta 4 subunit bind to ERBIN. Molecular cloning of multiple alternative splice variants of ERBIN and analysis of their tissue expression. J Biol Chem 2001, 276(35):32427-32436.
53. Tao Y., Dai P., Liu Y., Marchetto S., Xiong W.C., Borg J.P., et al. Erbin regulates NRG1 signaling and myelination. Proc Natl Acad Sci USA 2009, 106(23):9477-9482.
54. Kim H.A., DeClue J.E., Ratner N. cAMP-dependent protein kinase A is required for Schwann cell growth: interactions between the cAMP and neuregulin/tyrosine kinase pathways. J Neurosci Res 1997, 49(2):236-247.
55. Li Y., Tennekoon G.I., Birnbaum M., Marchionni M.A., Rutkowski J.L. Neuregulin signaling through a PI3K/Akt/Bad pathway in Schwann cell survival. Mol Cell Neurosci 2001, 17(4):761-767.
56. Ogata T., Iijima S., Hoshikawa S., Miura T., Yamamoto S., Oda H., et al. Opposing extracellular signal-regulated kinase and Akt pathways control Schwann cell myelination. J Neurosci 2004, 24(30):6724-6732.
57. Maurel P., Salzer J.L. Axonal regulation of Schwann cell proliferation and survival and the initial events of myelination requires PI 3-kinase activity. J Neurosci 2000, 20(12):4635-4645.
58. Vartanian T., Goodearl A., Lefebvre S., Park S.K., Fischbach G. Neuregulin induces the rapid association of focal adhesion kinase with the erbB2-erbB3 receptor complex in schwann cells. Biochem Biophys Res Commun 2000, 271(2):414-417.
59. Kao S.C., Wu H., Xie J., Chang C.P., Ranish J.A., Graef I.A., et al. Calcineurin/NFAT signaling is required for neuregulin-regulated Schwann cell differentiation. Science 2009, 323(5914):651-654.
60. Grove M., Komiyama N.H., Nave K.A., Grant S.G., Sherman D.L., Brophy P.J. FAK is required for axonal sorting by Schwann cells. J Cell Biol 2007, 176(3):277-282.
61. Mohi M.G., Neel B.G. The role of Shp2 (PTPN11) in cancer. Curr Opin Genet Dev 2007, 17(1):23-30.
62. Perkins L.A., Larsen I., Perrimon N. Corkscrew encodes a putative protein tyrosine phosphatase that functions to transduce the terminal signal from the receptor tyrosine kinase torso. Cell 1992, 70(2):225-236.
63. Herbst R., Carroll P.M., Allard J.D., Schilling J., Raabe T., Simon M.A. Daughter of sevenless is a substrate of the phosphotyrosine phosphatase Corkscrew and functions during sevenless signaling. Cell 1996, 85(6):899-909.
64. Yang W., Klaman L.D., Chen B., Araki T., Harada H., Thomas S.M., et al. An Shp2/SFK/Ras/Erk signaling pathway controls trophoblast stem cell survival. Dev Cell 2006, 10(3):317-327.
65. Tartaglia M., Mehler E.L., Goldberg R., Zampino G., Brunner H.G., Kremer H., et al. Mutations in PTPN11, encoding the protein tyrosine phosphatase SHP-2, cause Noonan syndrome. Nat Genet 2001, 29(4):465-468.
66. Grossmann K.S., Wende H., Paul F.E., Cheret C., Garratt A.N., Zurborg S., et al. The tyrosine phosphatase Shp2 (PTPN11) directs neuregulin-1/ErbB signaling throughout Schwann cell development. Proc Natl Acad Sci USA 2009, 106(39):16704-16709.
67. Harrisingh M.C., Perez-Nadales E., Parkinson D.B., Malcolm D.S., Mudge A.W., Lloyd A.C. The Ras/Raf/ERK signalling pathway drives Schwann cell dedifferentiation. Embo J 2004, 23(15):3061-3071.
68. Newbern J., Zhong J., Wickramasinghe R.S., Li X., Wu Y., Samuels I., et al. Mouse and human phenotypes indicate a critical conserved role for ERK2 signaling in neural crest development. Proc Natl Acad Sci USA 2008, 105(44):17115-17120.
69. Yamauchi J., Miyamoto Y., Chan J.R., Tanoue A. ErbB2 directly activates the exchange factor Dock7 to promote Schwann cell migration. J Cell Biol 2008, 181(2):351-365.
70. Benninger Y., Thurnherr T., Pereira J.A., Krause S., Wu X., Chrostek-Grashoff A., et al. Essential and distinct roles for cdc42 and rac1 in the regulation of Schwann cell biology during peripheral nervous system development. J Cell Biol 2007, 177(6):1051-1061.
71. Nodari A., Zambroni D., Quattrini A., Court F.A., D'Urso A., Recchia A., et al. Beta1 integrin activates Rac1 in Schwann cells to generate radial lamellae during axonal sorting and myelination. J Cell Biol 2007, 177(6):1063-1075.
72. Coso O.A., Chiariello M., Yu J.C., Teramoto H., Crespo P., Xu N., et al. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 1995, 81(7):1137-1146.
73. Minden A., Lin A., Claret F.X., Abo A., Karin M. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 1995, 81(7):1147-1157.
74. Parkinson D.B., Bhaskaran A., Arthur-Farraj P., Noon L.A., Woodhoo A., Lloyd A.C., et al. c-Jun is a negative regulator of myelination. J Cell Biol 2008, 181(4):625-637.
75. Fragoso G., Robertson J., Athlan E., Tam E., Almazan G., Mushynski W.E. Inhibition of p38 mitogen-activated protein kinase interferes with cell shape changes and gene expression associated with Schwann cell myelination. Exp Neurol 2003, 183(1):34-46.
76. Haines J.D., Fragoso G., Hossain S., Mushynski W.E., Almazan G. p38 Mitogen-activated protein kinase regulates myelination. J Mol Neurosci 2008, 35(1):23-33.
77. Woodhoo A., Alonso M.B., Droggiti A., Turmaine M., D'Antonio M., Parkinson D.B., et al. Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat Neurosci 2009, 12(7):839-847.
78. Chan J.R., Watkins T.A., Cosgaya J.M., Zhang C., Chen L., Reichardt L.F., et al. NGF controls axonal receptivity to myelination by Schwann cells or oligodendrocytes. Neuron 2004, 43(2):183-191.
79. Hoke A., Ho T., Crawford T.O., LeBel C., Hilt D., Griffin J.W. Glial cell line-derived neurotrophic factor alters axon schwann cell units and promotes myelination in unmyelinated nerve fibers. J Neurosci 2003, 23(2):561-567.
80. Pietri T., Eder O., Breau M.A., Topilko P., Blanche M., Brakebusch C., et al. Conditional beta1-integrin gene deletion in neural crest cells causes severe developmental alterations of the peripheral nervous system. Development 2004, 131(16):3871-3883.
81. Morgan L., Jessen K.R., Mirsky R. The effects of cAMP on differentiation of cultured Schwann cells: progression from an early phenotype (04+) to a myelin phenotype (P0+, GFAP-, N-CAM-, NGF-receptor-) depends on growth inhibition. J Cell Biol 1991, 112(3):457-467.
82. Salzer J.L., Bunge R.P. Studies of Schwann cell proliferation. I. An analysis in tissue culture of proliferation during development, Wallerian degeneration, and direct injury. J Cell Biol 1980, 84(3):739-752.
83. Monk K.R., Naylor S.G., Glenn T.D., Mercurio S., Perlin J.R., Dominguez C., et al. A G protein-coupled receptor is essential for Schwann cells to initiate myelination. Science 2009, 325(5946):1402-1405.
84. Brinkmann B.G., Agarwal A., Sereda M.W., Garratt A.N., 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(4):581-595.
85. Garratt A.N., Ozcelik C., Birchmeier C. ErbB2 pathways in heart and neural diseases. Trends Cardiovasc Med 2003, 13(2):80-86.
86. Leu M., Bellmunt E., Schwander M., Farinas I., Brenner H.R., Muller U. Erbb2 regulates neuromuscular synapse formation and is essential for muscle spindle development. Development 2003, 130(11):2291-2301.
87. Walsh T., McClellan J.M., McCarthy S.E., Addington A.M., Pierce S.B., Cooper G.M., et al. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science 2008, 320(5875):539-543.
88. Stefansson H., Sigurdsson E., Steinthorsdottir V., Bjornsdottir S., Sigmundsson T., Ghosh S., et al. Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 2002, 71(4):877-892.
89. Mei L., Xiong W.C. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 2008, 9(6):437-452.
90. Lopez-Bendito G., Cautinat A., Sanchez J.A., Bielle F., Flames N., Garratt A.N., et al. Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 2006, 125(1):127-142.
91. Flames N., Long J.E., Garratt A.N., Fischer T.M., Gassmann M., Birchmeier C., et al. Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 2004, 44(2):251-261.
92. Wen L., Lu Y.S., Zhu X.H., Li X.M., Woo R.S., Chen Y.J., et al. Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc Natl Acad Sci USA 2010, 107(3):1211-1216.