A nuclear variant of ErbB3 receptor tyrosine Kinase regulates ezrin distribution and schwann cell myelination

Journal of Neuroscience

Volumn 31, Issue 13, 2011, Pages 5106-5119

  Adilakshmi, Tadepalli ^a   Ness Myers, Jennifer ^a   Madrid Aliste, Carlos ^b   Fiser, Andras ^b   Tapinos, Nikos ^a  

^a WEIS CENTER FOR RESEARCH   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 3; EZRIN; HIGH MOBILITY GROUP B1 PROTEIN; NEU DIFFERENTIATION FACTOR;

ANIMAL CELL; ARTICLE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; MYELINATION; NEUROMODULATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN VARIANT; RANVIER NODE; RAT; SCHWANN CELL; SIGNAL TRANSDUCTION; SPINAL GANGLION; TISSUE DISTRIBUTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

ALTERNATIVE SPLICING; ANIMALS; ANIMALS, NEWBORN; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; COCULTURE TECHNIQUES; COS CELLS; CYTOSKELETAL PROTEINS; FEMALE; GENETIC VARIATION; MALE; MYELIN SHEATH; RATS; RECEPTOR, ERBB-3; SCHWANN CELLS;

EID: 79955745746     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5635-10.2011     Document Type: Article

References (54)

1. Ahmad S, Gromiha MM, Sarai A (2004) Analysis and prediction of DNAbinding proteins and their binding residues based on composition, sequence and structural information. Bioinformatics 20:477-486.
2. Bednenko J, Cingolani G, Gerace L (2003) Nucleocytoplasmic transport: navigating the channel. Traffic 4:127-135.
3. Berryman M, Franck Z, Bretscher A (1993) Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cells whereas moesin is found primarily in endothelial cells. J Cell Sci 105:1025-1043.
4. Cao X, Südhof TC (2001) A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293:115-120.
5. Carey DJ, Todd MS (1987) Schwann cell myelination in a chemically defined medium: demonstration of a requirement for additives that promote Schwann cell extracellular matrix formation. Brain Res 429:95-102.
6. Carpenter G (2003) Nuclear localization and possible functions of receptor tyrosine kinases. Curr Opin Cell Biol 15:143-148.
7. Chen N, Ye XC, Chu K, Navone NM, Sage EH, Yu-Lee LY, Logothetis CJ, Lin SH (2007) A secreted isoform of ErbB3 promotes osteonectin expression in bone and enhances the invasiveness of prostate cancer cells. Cancer Res 67:6544-6548.
8. Citri A, Skaria KB, Yarden Y (2003) The deaf and the dumb: the biology of ErbB-2 and ErbB-3. Exp Cell Res 284:54-65.
9. Cokol M, Nair R, Rost B (2000) Finding nuclear localization signals. EMBO Rep 1:411-415.
10. Corfas G, Rosen KM, Aratake H, Krauss R, Fischbach GD (1995) Differential expression of ARIA isoforms in the rat brain. Neuron 14:103-115.
11. Davies AM (1998) Neuronal survival: early dependence on Schwann cells. Curr Biol 8:R15-R18.
12. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4:P3.
13. Dong Z, Brennan A, Liu N, Yarden Y, Lefkowitz G, Mirsky R, Jessen KR (1995) Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15:585-596.
14. Einheber S, Milner TA, Giancotti F, Salzer JL (1993) Axonal regulation of Schwann cell integrin expression suggests a role for alpha 6 beta 4 in myelination. J Cell Biol 123:1223-1236.
15. Elenius K, Corfas G, Paul S, Choi CJ, Rio C, Plowman GD, Klagsbrun M (1997) A novel juxtamembrane domain isoform of HER4/ErbB4. Isoform-specific tissue distribution and differential processing in response to phorbol ester. J Biol Chem 272:26761-26768.
16. Erickson SL, O'Shea KS, Ghaboosi N, Loverro L, Frantz G, Bauer M, Lu LH, Moore MW (1997) ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice. Development 124:4999-5011.
17. Frade JM (2005) Nuclear translocation of the p75 neurotrophin receptor cytoplasmic domain in response to neurotrophin binding. J Neurosci 25:1407-1411.
18. Garratt AN, Britsch S, Birchmeier C (2000) Neuregulin, a factor with many functions in the life of a Schwann cell. Bioessays 22:987-996.
19. Ishigaki Y, Li X, Serin G, Maquat LE (2001) Evidence for a pioneer round of mRNAtranslation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106:607- 617.
20. Koumakpayi IH, Diallo JS, Le Page C, Lessard L, Gleave M, Bégin LR, Mes-Masson AM, Saad F (2006) Expression and nuclear localization of ErbB3 in prostate cancer. Clin Cancer Res 12:2730-2737.
21. Koumakpayi IH, Diallo JS, Le Page C, Lessard L, Filali-Mouhim A, Bégin LR, Mes-Masson AM, Saad F (2007) Low nuclear ErbB3 predicts biochemical recurrence in patients with prostate cancer. BJU Int 100:303-309.
22. Lallemand D, Manent J, Couvelard A, Watilliaux A, Siena M, Chareyre F, Lampin A, Niwa-Kawakita M, Kalamarides M, Giovannini M (2009) Merlin regulates transmembrane receptor accumulation and signaling at the plasma membrane in primary mouse Schwann cells and in human schwannomas. Oncogene 28:854-865.
23. Lee HJ, Jung KM, Huang YZ, Bennett LB, Lee JS, Mei L, Kim TW (2002) Presenilin-dependent gamma-secretase-like intramembrane cleavage of ErbB4. J Biol Chem 277:6318-6323.
24. Lee KF, Simon H, Chen H, Bates B, Hung MC, Hauser C (1995) Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378:394-398.
25. Levi AD, Bunge RP, Lofgren JA, Meima L, Hefti F, Nikolics K, Sliwkowski MX (1995) The influence of heregulins on human Schwann cell proliferation. J Neurosci 15:1329-1340.
26. Li W, Jaroszewski L, Godzik A (2001) Clustering of highly homologous sequences to reduce the size of large protein databases. Bioinformatics 17:282-283.
27. Maquat LE (1995) When cells stop making sense: effects of nonsense codons on RNA metabolism in vertebrate cells. RNA 1:453-465.
28. Maquat LE, Carmichael GG (2001) Quality control of mRNA function. Cell 104:173-176.
29. Melendez-Vasquez CV, Rios JC, Zanazzi G, Lambert S, Bretscher A, Salzer JL (2001) Nodes of Ranvier form in association with ezrin-radixin-moesin (ERM)-positive Schwann cell processes. Proc Natl Acad Sci U S A 98:1235-1240.
30. Meyer D, Birchmeier C (1995) Multiple essential functions of neuregulin in development. Nature 378:386-390.
31. Meyer D, Yamaai T, Garratt A, Riethmacher-Sonnenberg E, Kane D, Theill LE, Birchmeier C (1997) Isoform-specific expression and function of neuregulin. Development 124:3575-3586.
32. Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B, Birchmeier C, Role L, Lai C, Schwab MH, Nave KA (2004) Axonal neuregulin-1 regulates myelin sheath thickness. Science 304:700-703.
33. Morris JK, Lin W, Hauser C, Marchuk Y, Getman D, Lee KF (1999) Rescue of the cardiac defect in ErbB2 mutant mice reveals essential roles of ErbB2 in peripheral nervous system development. Neuron 23:273-283.
34. Morrissey TK, Levi AD, Nuijens A, Sliwkowski MX, Bunge RP (1995) Axoninduced mitogenesis of human Schwann cells involves heregulin and p185erbB2. Proc Natl Acad Sci U S A 92:1431-1435.
35. Muraoka-Cook RS, Sandahl M, Husted C, Hunter D, Miraglia L, Feng SM, Elenius K, Earp HS 3rd (2006) The intracellular domain of ErbB4 induces differentiation of mammary epithelial cells. Mol Biol Cell 17:4118-4129.
36. Ni CY, Murphy MP, Golde TE, Carpenter G (2001) gamma-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294:2179-2181.
37. Offterdinger M, Schöfer C, Weipoltshammer K, Grunt TW (2002) c-erbB-3: a nuclear protein in mammary epithelial cells. J Cell Biol 157:929-939.
38. Prigent SA, Lemoine NR, Hughes CM, Plowman GD, Selden C, Gullick WJ (1992) Expression of the c-erbB-3 protein in normal human adult and fetal tissues. Oncogene 7:1273-1278.
39. Raabe TD, Deadwyler G, Varga JW, Devries GH (2004) Localization of neuregulin isoforms and erbB receptors in myelinating glial cells. Glia 45:197-207.
40. Riethmacher D, Sonnenberg-Riethmacher E, Brinkmann V, Yamaai T, Lewin GR, Birchmeier C (1997) Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 389:725-730.
41. Sardi SP, Murtie J, Koirala S, Patten BA, Corfas G (2006) Presenilin dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 127:185-197.
42. Scherer SS, Xu T, Crino P, Arroyo EJ, Gutmann DH (2001) Ezrin, radixin, and moesin are components of Schwann cell microvilli. J Neurosci Res 65:150-164.
43. Steiner H, Haass C (2000) Intramembrane proteolysis by presenilins. Nat Rev Mol Cell Biol 1:217-224.
44. Sweet DJ, Gerace L (1995) Taking from the cytoplasm and giving to the pore: soluble transport factors in nuclear protein import. Trends Cell Biol 5:444-447.
45. Syroid DE, Maycox PR, Burrola PG, Liu N, Wen D, Lee KF, Lemke G, Kilpatrick TJ (1996) Cell death in the Schwann cell lineage and its regulation by neuregulin. Proc Natl Acad Sci U S A 93:9229-9234.
46. Taveggia C, Zanazzi G, Petrylak A, Yano H, Rosenbluth J, Einheber S, Xu X, Esper RM, Loeb JA, Shrager P, Chao MV, Falls DL, Role L, Salzer JL (2005) Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47:681-694.
47. Thompson M, Lauderdale S, Webster MJ, Chong VZ, McClintock B, Saunders R, Weickert CS (2007) Widespread expression of ErbB2, ErbB3 and ErbB4 in non-human primate brain. Brain Res 1139:95-109.
48. Vecchi M, Carpenter G (1997) Constitutive proteolysis of the ErbB-4 receptor tyrosine kinase by a unique, sequential mechanism. J Cell Biol 139:995-1003.
49. Weinmann AS, Farnham PJ (2002) Identification of unknown target genes of human transcription factors using chromatin immunoprecipitation. Methods 26:37-47.
50. Windebank AJ, Wood P, Bunge RP, Dyck PJ (1985) Myelination determines the caliber of dorsal root ganglion neurons in culture. J Neurosci 5:1563-1569.
51. Woldeyesus MT, Britsch S, Riethmacher D, Xu L, Sonnenberg-Riethmacher E, Abou-Rebyeh F, Harvey R, Caroni P, Birchmeier C (1999) Peripheral nervous system defects in erbB2 mutants following genetic rescue of heart development. Genes Dev 13:2538-2548.
52. Xu L, Massagué J (2004) Nucleocytoplasmic shuttling of signal transducers. Nat Rev Mol Cell Biol 5:209-219.
53. Xue C, Liang F, Mahmood R, Vuolo M, Wyckoff J, Qian H, Tsai KL, Kim M, Locker J, Zhang ZY, Segall JE (2006) ErbB3-dependent motility and intravasation in breast cancer metastasis. Cancer Res 66:1418-1426.
54. Yamauchi J, Miyamoto Y, Chan JR, Tanoue A (2008) ErbB2 directly activates the exchange factor Dock7 to promote Schwann cell migration. J Cell Biol 181:351-365.