Neuregulin-induced expression of the acetylcholine receptor requires endocytosis of ErbB receptors

Molecular and Cellular Neuroscience

Volumn 28, Issue 2, 2005, Pages 335-346

  Yang, Xiao Li ^a   Huang, Yang Z ^a   Xiong, Wen C ^b,c   Mei, Lin ^a,c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINERGIC RECEPTOR; CLATHRIN; EPIDERMAL GROWTH FACTOR RECEPTOR; NEU DIFFERENTIATION FACTOR; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT;

EID: 13444252597     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2004.10.001     Document Type: Article

References (60)

1. S. Ahn, S. Maudsley, L.M. Luttrell, R.J. Lefkowitz, and Y. Daaka Src-mediated tyrosine phosphorylation of dynamin is required for beta2-adrenergic receptor internalization and mitogen-activated protein kinase signaling J. Biol. Chem. 274 1999 1185 1188
2. T. Akiyama, and H. Ogawara Use and specificity of genistein as inhibitor of protein-tyrosine kinases Methods Enzymol. 201 1991 362 370
3. N. Altiok, S. Altiok, and J.P. Changeux Heregulin-stimulated acetylcholine receptor gene expression in muscle: requirement for MAP kinase and evidence for a parallel inhibitory pathway independent of electrical activity EMBO J. (Europe) 16 1997 717 725
4. J. Baulida, M.H. Kraus, M. Alimandi, P.P. Di Fiore, and G. Carpenter All ErbB receptors other than the epidermal growth factor receptor are endocytosis impaired J. Biol. Chem. 271 1996 5251 5257
5. V. Besset, R.P. Scott, and C.F. Ibanez Signaling complexes and protein-protein interactions involved in the activation of the Ras and phosphatidylinositol 3-kinase pathways by the c-Ret receptor tyrosine kinase J. Biol. Chem. 275 2000 39159 39166
6. A.H. Bild, J. Turkson, and R. Jove Cytoplasmic transport of Stat3 by receptor-mediated endocytosis EMBO J. 21 2002 3255 3263
7. P. Burke, K. Schooler, and H.S. Wiley Regulation of epidermal growth factor receptor signaling by endocytosis and intracellular trafficking Mol. Biol. Cell 12 2001 1897 1910
8. G. Carpenter ErbB-4: mechanism of action and biology Exp. Cell Res. 284 2003 66 77
9. B.P. Ceresa, A.W. Kao, S.R. Santeler, and J.E. Pessin Inhibition of clathrin-mediated endocytosis selectively attenuates specific insulin receptor signal transduction pathways Mol. Cell. Biol. 18 1998 3862 3870
10. K.G. Chahine, W. Walke, and D. Goldman A 102 base pair sequence of the nicotinic acetylcholine receptor delta-subunit gene confers regulation by muscle electrical activity Development 115 1992 213 219
11. C.P. Chang, J.P. Kao, C.S. Lazar, B.J. Walsh, A. Wells, H.S. Wiley, G.N. Gill, and M.G. Rosenfeld Ligand-induced internalization and increased cell calcium are mediated via distinct structural elements in the carboxyl terminus of the epidermal growth factor receptor J. Biol. Chem. 266 1991 23467 23470
12. W.S. Chen, C.S. Lazar, K.A. Lund, J.B. Welsh, C.P. Chang, G.M. Walton, C.J. Der, H.S. Wiley, G.N. Gill, and M.G. Rosenfeld Functional independence of the epidermal growth factor receptor from a domain required for ligand-induced internalization and calcium regulation Cell 59 1989 33 43
13. Q.C. Cheng, O. Tikhomirov, W. Zhou, and G. Carpenter Ectodomain cleavage of ErbB-4: characterization of the cleavage site and m80 fragment J. Biol. Chem. 278 2003 38421 38427
14. G.C. Chu, L.M. Moscoso, M.X. Sliwkowski, and J.P. Merlie Regulation of the acetylcholine receptor epsilon subunit gene by recombinant ARIA: an in vitro model for transynaptic gene regulation Neuron 14 1995 329 339
15. J.L. Connolly, S.A. Green, and L.A. Greene Comparison of rapid changes in surface morphology and coated pit formation of PC12 cells in response to nerve growth factor, epidermal growth factor, and dibutyryl cyclic AMP J. Cell Biol. 98 1984 457 465
16. Y. Daaka, L.M. Luttrell, S. Ahn, G.J. Della Rocca, S.S. Ferguson, M.G. Caron, and R.J. Lefkowitz Essential role for G protein-coupled receptor endocytosis in the activation of mitogen-activated protein kinase J. Biol. Chem. 273 1998 685 688
17. H. Damke, T. Baba, D.E. Warnock, and S.L. Schmid Induction of mutant dynamin specifically blocks endocytic coated vesicle formation J. Cell Biol. 127 1994 915 934
18. D. Danino, and J.E. Hinshaw Dynamin family of mechanoenzymes Curr. Opin. Cell Biol. 13 2001 454 460
19. M.D. Ehlers Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting Neuron 28 2000 511 525
20. D.L. Falls Neuregulins and the neuromuscular system: 10 years of answers and questions J. Neurocytol. 32 2003 619 647
21. G.D. Fischbach, and K.M. Rosen ARIA: a neuromuscular junction neuregulin Annu. Rev. Neurosci. 20 1997 429 458
22. A.K. Fu, W.Y. Fu, J. Cheung, K.W. Tsim, F.C. Ip, J.H. Wang, and N.Y. Ip Cdk5 is involved in neuregulin-induced AChR expression at the neuromuscular junction Nat. Neurosci. 4 2001 374 381
23. L. Gilboa, R. Ben-Levy, Y. Yarden, and Y.I. Henis Roles for a cytoplasmic tyrosine and tyrosine kinase activity in the interactions of Neu receptors with coated pits J. Biol. Chem. 270 1995 7061 7067
24. M.L. Grimes, J. Zhou, E.C. Beattie, E.C. Yuen, D.E. Hall, J.S. Valletta, K.S. Topp, J.H. LaVail, N.W. Bunnett, and W.C. Mobley Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes J. Neurosci. 16 1996 7950 7964
25. H.T. Haigler, J.A. McKanna, and S. Cohen Direct visualization of the binding and internalization of a ferritin conjugate of epidermal growth factor in human carcinoma cells A-431 J. Cell Biol. 81 1979 382 395
26. W.E. Holmes, M.X. Slikowski, R.W. Akita, W.J. Kenzel, J. Lee, J.W. Park, D. Yansura, N. Abadi, H. Raab, G.D. Lewis, H.M. Shepard, W.J. Huang, W.J. Wood, D.V. Goeddel, and R.L. Vandlen Identification of heregulin, a specific activator of p185erbB2 Science (Washington) 256 1992 1205 1210
27. C.L. Howe, J.S. Valletta, A.S. Rusnak, and W.C. Mobley NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway Neuron 32 2001 801 814
28. Y.Z. Huang, S. Won, D.W. Ali, Q. Wang, M. Tanowitz, Q.S. Du, K.A. Pelkey, D.J. Yang, W.C. Xiong, M.W. Salter, and L. Mei Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses Neuron 26 2000 443 455
29. Y.Z. Huang, Q. Wang, W.C. Xiong, and L. Mei Erbin is a protein concentrated at postsynaptic membranes that interacts with PSD-95 J. Biol. Chem. 276 2001 19318 19326
30. T.M. Jessell, R.E. Siegel, and G.D. Fischbach Induction of acetylcholine receptors on cultured skeletal muscle by a factor extracted from brain and spinal cord Proc. Natl. Acad. Sci. U. S. A. 76 1979 5397 5401
31. J.T. Jones, M.D. Ballinger, P.I. Pisacane, J.A. Lofgren, V.D. Fitzpatrick, W.J. Fairbrother, J.A. Wells, and M.X. Sliwkowski Binding interaction of the heregulinbeta egf domain with ErbB3 and ErbB4 receptors assessed by alanine scanning mutagenesis J. Biol. Chem. 273 1998 11667 11674
32. B.N. Kholodenko MAP kinase cascade signaling and endocytic trafficking: a marriage of convenience? Trends Cell Biol. 12 2002 173 177
33. H.J. Lee, K.M. Jung, Y.Z. Huang, L.B. Bennett, J.S. Lee, L. Mei, and T.W. Kim Presenilin-dependent gamma-secretase-like intramembrane cleavage of ErbB4 J. Biol. Chem. 277 2002 6318 6323
34. G. Lemke Neuregulins in development Mol. Cell Neurosci. 7 1996 247 262
35. L.V. Lotti, C. Di Lazzaro, C. Zompetta, L. Frati, and M.R. Torrisi Surface distribution and internalization of ErbB-2 proteins Exp. Cell Res. 202 1992 274 280
36. J.C. Martinou, D.L. Falls, G.D. Fischbach, and J.P. Merlie Acetylcholine receptor-inducing activity stimulates expression of the epsilon-subunit gene of the muscle acetylcholine receptor Proc. Natl. Acad. Sci. U. S. A. 88 1991 7669 7673
37. U.J. McMahan, S.E. Horton, M.J. Werle, L.S. Honig, S. Kroger, M.A. Ruegg, and G. Escher Agrin isoforms and their role in synaptogenesis Curr. Opin. Cell Biol. 4 1992 869 874 (Review)
38. G.D. Plowman, J.M. Culouscou, G.S. Whitney, J.M. Green, G.W. Carlton, L. Foy, M.G. Neubauer, and M. Shoyab Ligand-specific activation of HER4/p180erbB4, a fourth member of the epidermal growth factor receptor family Proc. Natl. Acad. Sci. U. S. A. 90 1993 1746 1750
39. J. Sambrook, E.F. Fritsch, and T. Maniatis Molecular Cloning: A Laboratory Manual 1989 Cold Spring Harbor Laboratory Cold Spring Harbor, NY
40. A.W. Sandrock, S.E. Dryer, K.M. Rosen, S.N. Gozani, R. Kramer, L.E. Theill, and G.D. Fischbach Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo Science (Washington) 276 1997 599 603
41. J.R. Sanes, and J.W. Lichtman Induction, assembly, maturation and maintenance of a postsynaptic apparatus Nat. Rev. Neurosci. 2 2001 791 805
42. B.H. Shah, J. Alberto Olivares-Reyes, A. Yesilkaya, and K.J. Catt Independence of angiotensin II-induced MAP kinase activation from angiotensin type 1 receptor internalization in clone 9 hepatocytes Mol. Endocrinol. 16 2002 610 620
43. J. Si, Z. Luo, and L. Mei Induction of acetylcholine receptor gene expression by ARIA requires activation of mitogen-activated protein kinase J. Biol. Chem. 271 1996 19752 19759
44. J. Si, Q. Wang, and L. Mei Essential roles of c-JUN and c-JUN N-terminal kinase (JNK) in neuregulin-increased expression of the acetylcholine receptor epsilon-subunit J. Neurosci. 19 1999 8489 8508
45. J. Tang, S.A. Jo, and S.J. Burden Separate pathways for synapse-specific and electrical activity-dependent gene expression in skeletal muscle Development 120 1994 1799 1804
46. M. Tanowitz, J. Si, D.-H. Yu, G.-S. Feng, and L. Mei Regulation of neuregulin-mediated AChR synthesis by protein tyrosine phosphatase SHP2 J. Neuorsci. 19 1999 9426 9435
47. M.G. Tansey, G.C. Chu, and J.P. Merlie ARIA/HRG regulates AChR epsilon subunit gene expression at the neuromuscular synapse via activation of phosphatidylinositol 3-kinase and Ras/MAPK pathway J. Cell Biol. 134 1996 465 476
48. X.K. Tong, N.K. Hussain, A.G. Adams, J.P. O'Bryan, and P.S. McPherson Intersectin can regulate the Ras/MAP kinase pathway independent of its role in endocytosis J. Biol. Chem. 275 2000 29894 29899
49. T.B. Usdin, and G.D. Fischbach Purification and characterization of a polypeptide from chick brain that promotes the accumulation of acetylcholine receptors in chick myotubes J. Cell Biol. 103 1986 493 507
50. M. Vecchi, J. Baulida, and G. Carpenter Selective cleavage of the heregulin receptor ErbB-4 by protein kinase C activation J. Biol. Chem. 271 1996 18989 18995
51. A.V. Vieira, C. Lamaze, and S.L. Schmid Control of EGF receptor signaling by clathrin-mediated endocytosis Science 274 1996 2086 2089
52. Z. Wang, L. Zhang, T.K. Yeung, and X. Chen Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation Mol. Biol. Cell 10 1999 1621 1636
53. H. Waterman, and Y. Yarden Molecular mechanisms underlying endocytosis and sorting of ErbB receptor tyrosine kinases FEBS Lett. 490 2001 142 152
54. A. Wilde, E.C. Beattie, L. Lem, D.A. Riethof, S.H. Liu, W.C. Mobley, P. Soriano, and F.M. Brodsky EGF receptor signaling stimulates SRC kinase phosphorylation of clathrin, influencing clathrin redistribution and EGF uptake Cell 96 1999 677 687
55. H.S. Wiley Trafficking of the ErbB receptors and its influence on signaling Exp. Cell Res. 284 2003 78 88
56. H.S. Wiley, and P.M. Burke Regulation of receptor tyrosine kinase signaling by endocytic trafficking Traffic 2 2001 12 18
57. H.S. Wiley, J.J. Herbst, B.J. Walsh, D.A. Lauffenburger, M.G. Rosenfeld, and G.N. Gill The role of tyrosine kinase activity in endocytosis, compartmentation, and down-regulation of the epidermal growth factor receptor J. Biol. Chem. 266 1991 11083 11094
58. Y. Yarden Agonistic antibodies stimulate the kinase encoded by the neu protooncogene in living cells but the oncogenic mutant is constitutively active Proc. Natl. Acad. Sci. U. S. A. 87 1990 2569 2573
59. Y. Yarden The EGFR family and its ligands in human cancer. Signalling mechanisms and therapeutic opportunities Eur. J. Cancer 37 Suppl. 4 2001 S3 S8
60. W. Zhou, and G. Carpenter ErbB-4: a receptor tyrosine kinase Inflammation Res. 51 2002 91 101