Cytoplasmic retention of a nucleocytoplasmic protein TBC1D3 by microtubule network is required for enhanced EGFR signaling

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  He, Ze ^a   Tian, Tian ^a   Guo, Dan ^a   Wu, Huijuan ^a   Chen, Yang ^a   Zhang, Yongchen ^a   Wan, Qing ^a   Zhao, Huzi ^a   Wang, Congyang ^a   Shen, Hongjing ^b   Zhao, Lei ^a   Bu, Xiaodong ^a   Wan, Meiling ^a   Shen, Chuanlu ^a  

^a SOUTHEAST UNIVERSITY   (China)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; AMINO ACID; BETA TUBULIN; CYTOPLASM PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; NOCODAZOLE; PROTEIN TBC1D3; TUBULIN; UNCLASSIFIED DRUG; EGFR PROTEIN, HUMAN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; ONCOPROTEIN; TBC1D3 PROTEIN, HUMAN;

ARTICLE; CANCER CELL CULTURE; CARBOXY TERMINAL SEQUENCE; CARCINOMA CELL; CELL NUCLEUS; CELL PROLIFERATION ASSAY; CELL STRAIN SMMC7721; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; LIVER CELL CARCINOMA; MASS SPECTROMETRY; MICROTUBULE; NUCLEOTIDE SEQUENCE; ONCOGENE; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; TBC1D3 GENE; UBIQUITINATION; WESTERN BLOTTING; WILD TYPE; CELL PROLIFERATION; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL PROLIFERATION; CYTOPLASM; GTPASE-ACTIVATING PROTEINS; HUMANS; MICROTUBULES; PROTO-ONCOGENE PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TUBULIN;

EID: 84899464927     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094134     Document Type: Article

References (53)

1. Lemmon MA, Schlessinger J (2010) Cell signaling by receptor tyrosine kinases. Cell 141: 1117-1134.
2. Sibilia M, Kroismayr R, Lichtenberger BM, Natarajan A, Hecking M, et al. (2007) The epidermal growth factor receptor: from development to tumorigenesis. Differentiation 75: 770-787. (Pubitemid 350086174)
3. Blume-Jensen P, Hunter T (2001) Oncogenic kinase signalling. Nature 411: 355-365. (Pubitemid 32467045)
4. Levkowitz G, Waterman H, Zamir E, Kam Z, Oved S, et al. (1998) c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev 12: 3663-3674. (Pubitemid 29019647)
5. Schmidt MH, Dikic I (2005) The Cbl interactome and its functions. Nat Rev Mol Cell Biol 6: 907-918. (Pubitemid 41778710)
6. Levkowitz G, Waterman H, Ettenberg SA, Katz M, Tsygankov AY, et al. (1999) Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol Cell 4: 1029-1040. (Pubitemid 30054908)
7. Waterman H, Levkowitz G, Alroy I, Yarden Y (1999) The RING finger of c-Cbl mediates desensitization of the epidermal growth factor receptor. J Biol Chem 274: 22151-22154.
8. Waterman H, Katz M, Rubin C, Shtiegman K, Lavi S, et al. (2002) A mutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signaling. EMBO J 21: 303-313. (Pubitemid 34137292)
9. Umebayashi K, Stenmark H, Yoshimori T (2008) Ubc4/5 and c-Cbl continue to ubiquitinate EGF receptor after internalization to facilitate polyubiquitination and degradation. Mol Biol Cell 19: 3454-3462.
10. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A (2006) Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 21: 737-748. (Pubitemid 43376125)
11. Haglund K, Sigismund S, Polo S, Szymkiewicz I, Di Fiore PP, et al. (2003) Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol 5: 461-466. (Pubitemid 36592270)
12. Huang F, Goh LK, Sorkin A (2007) EGF receptor ubiquitination is not necessary for its internalization. Proc Natl Acad Sci U S A 104: 16904-16909. (Pubitemid 350210963)
13. Goh LK, Huang F, Kim W, Gygi S, Sorkin A (2010) Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor. J Cell Biol 189: 871-883.
14. Eden ER, Huang F, Sorkin A, Futter CE (2012) The role of EGF receptor ubiquitination in regulating its intracellular traffic. Traffic 13: 329-337.
15. Kim HJ, Bar-Sagi D (2004) Modulation of signalling by Sprouty: a developing story. Nat Rev Mol Cell Biol 5: 441-450. (Pubitemid 38745494)
16. Christofori G (2003) Split personalities: the agonistic antagonist Sprouty. Nat Cell Biol 5: 377-379.
17. Wu WJ, Tu S, Cerione RA (2003) Activated Cdc42 sequesters c-Cbl and prevents EGF receptor degradation. Cell 114: 715-725. (Pubitemid 37186766)
18. Okur MN, Ooi J, Fong CW, Martinez N, Garcia-Dominguez C, et al. (2012) Intersectin 1 enhances Cbl ubiquitylation of epidermal growth factor receptor through regulation of Sprouty2-Cbl interaction. Mol Cell Biol 32: 817-825.
19. Li X, Lu Y, Liang K, Hsu JM, Albarracin C, et al. (2012) Brk/PTK6 sustains activated EGFR signaling through inhibiting EGFR degradation and transactivating EGFR. Oncogene 31: 4372-4383.
20. Hatanaka H, Tsukui M, Takada S, Kurashina K, Choi YL, et al. (2010) Identification of transforming activity of free fatty acid receptor 2 by retroviral expression screening. Cancer Sci 101: 54-59.
21. Paulding CA, Ruvolo M, Haber DA (2003) The Tre2 (USP6) oncogene is a hominoid-specific gene. Proc Natl Acad Sci U S A 100: 2507-2511. (Pubitemid 36297529)
22. Pei L, Peng Y, Yang Y, Ling XB, Van Eyndhoven WG, et al. (2002) PRC17, a novel oncogene encoding a Rab GTPase-activating protein, is amplified in prostate cancer. Cancer Res 62: 5420-5424.
23. Hodzic D, Kong C, Wainszelbaum MJ, Charron AJ, Su X, et al. (2006) TBC1D3, a hominoid oncoprotein, is encoded by a cluster of paralogues located on chromosome 17q12. Genomics 88: 731-736. (Pubitemid 44739195)
24. Bernards A (2003) GAPs galore! A survey of putative Ras superfamily GTPase activating proteins in man and Drosophila. Biochim Biophys Acta 1603: 47-82.
25. Frittoli E, Palamidessi A, Pizzigoni A, Lanzetti L, Garre M, et al. (2008) The primate-specific protein TBC1D3 is required for optimal macropinocytosis in a novel ARF6-dependent pathway. Mol Biol Cell 19: 1304-1316. (Pubitemid 351805086)
26. Wainszelbaum MJ, Charron AJ, Kong C, Kirkpatrick DS, Srikanth P, et al. (2008) The hominoid-specific oncogene TBC1D3 activates Ras and modulates epidermal growth factor receptor signaling and trafficking. J Biol Chem 283: 13233-13242.
27. Wainszelbaum MJ, Liu J, Kong C, Srikanth P, Samovski D, et al. (2012) TBC1D3, a hominoid-specific gene, delays IRS-1 degradation and promotes insulin signaling by modulating p70 S6 kinase activity. PLoS One 7: e31225.
28. Kong C, Samovski D, Srikanth P, Wainszelbaum MJ, Charron AJ, et al. (2012) Ubiquitination and degradation of the hominoid-specific oncoprotein TBC1D3 is mediated by CUL7 E3 ligase. PLoS One 7: e46485.
29. Chen J, Lippincott-Schwartz J, Liu J (2012) Intracellular spatial localization regulated by the microtubule network. PLoS One 7: e34919.
30. Gundersen GG, Cook TA (1999) Microtubules and signal transduction. Curr Opin Cell Biol 11: 81-94. (Pubitemid 29084135)
31. Perdiz D, Mackeh R, Pous C, Baillet A (2011) The ins and outs of tubulin acetylation: more than just a post-translational modification? Cell Signal 23: 763-771.
32. Deribe YL, Wild P, Chandrashaker A, Curak J, Schmidt MH, et al. (2009) Regulation of epidermal growth factor receptor trafficking by lysine deacetylase HDAC6. Sci Signal 2: ra84.
33. Dompierre JP, Godin JD, Charrin BC, Cordelieres FP, King SJ, et al. (2007) Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J Neurosci 27: 3571-3583. (Pubitemid 46515140)
34. Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, et al. (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 16: 2166-2172. (Pubitemid 44692098)
35. Gao YS, Hubbert CC, Yao TP (2010) The microtubule-associated histone deacetylase 6 (HDAC6) regulates epidermal growth factor receptor (EGFR) endocytic trafficking and degradation. J Biol Chem 285: 11219-11226.
36. Purev E, Neff L, Horne WC, Baron R (2009) c-Cbl and Cbl-b act redundantly to protect osteoclasts from apoptosis and to displace HDAC6 from beta-tubulin, stabilizing microtubules and podosomes. Mol Biol Cell 20: 4021-4030.
37. Bowers K, Piper SC, Edeling MA, Gray SR, Owen DJ, et al. (2006) Degradation of endocytosed epidermal growth factor and virally ubiquitinated major histocompatibility complex class I is independent of mammalian ESCRTII. J Biol Chem 281: 5094-5105. (Pubitemid 43847775)
38. McCullough J, Clague MJ, Urbe S (2004) AMSH is an endosome-associated ubiquitin isopeptidase. J Cell Biol 166: 487-492. (Pubitemid 39097168)
39. Pareja F, Ferraro DA, Rubin C, Cohen-Dvashi H, Zhang F, et al. (2012) Deubiquitination of EGFR by Cezanne-1 contributes to cancer progression. Oncogene 31: 4599-4608.
40. Moseley GW, Lahaye X, Roth DM, Oksayan S, Filmer RP, et al. (2009) Dual modes of rabies P-protein association with microtubules: a novel strategy to suppress the antiviral response. J Cell Sci 122: 3652-3662.
41. Campbell EM, Hope TJ (2003) Role of the cytoskeleton in nuclear import. Adv Drug Deliv Rev 55: 761-771. (Pubitemid 36638688)
42. Carbonaro M, Escuin D, O'Brate A, Thadani-Mulero M, Giannakakou P (2012) Microtubules regulate hypoxia-inducible factor-1alpha protein trafficking and activity: implications for taxane therapy. J Biol Chem 287: 11859-11869.
43. Giannakakou P, Sackett DL, Ward Y, Webster KR, Blagosklonny MV, et al. (2000) p53 is associated with cellular microtubules and is transported to the nucleus by dynein. Nat Cell Biol 2: 709-717.
44. Lam MH, Thomas RJ, Loveland KL, Schilders S, Gu M, et al. (2002) Nuclear transport of parathyroid hormone (PTH)-related protein is dependent on microtubules. Mol Endocrinol 16: 390-401. (Pubitemid 34131233)
45. Mikenberg I, Widera D, Kaus A, Kaltschmidt B, Kaltschmidt C (2007) Transcription factor NF-kappaB is transported to the nucleus via cytoplasmic dynein/dynactin motor complex in hippocampal neurons. PLoS One 2: e589.
46. Moseley GW, Roth DM, DeJesus MA, Leyton DL, Filmer RP, et al. (2007) Dynein light chain association sequences can facilitate nuclear protein import. Mol Biol Cell 18: 3204-3213. (Pubitemid 47235323)
47. Rathinasamy K, Panda D (2008) Kinetic stabilization of microtubule dynamic instability by benomyl increases the nuclear transport of p53. Biochem Pharmacol 76: 1669-1680.
48. Roth DM, Moseley GW, Glover D, Pouton CW, Jans DA (2007) A microtubule-facilitated nuclear import pathway for cancer regulatory proteins. Traffic 8: 673-686. (Pubitemid 46785150)
49. Dohner K, Nagel CH, Sodeik B (2005) Viral stop-and-go along microtubules: taking a ride with dynein and kinesins. Trends Microbiol 13: 320-327. (Pubitemid 40884467)
50. Haller K, Rambaldi I, Daniels E, Featherstone M (2004) Subcellular localization of multiple PREP2 isoforms is regulated by actin, tubulin, and nuclear export. J Biol Chem 279: 49384-49394. (Pubitemid 39625824)
51. Malki S, Berta P, Poulat F, Boizet-Bonhoure B (2005) Cytoplasmic retention of the sex-determining factor SOX9 via the microtubule network. Exp Cell Res 309: 468-475. (Pubitemid 41317369)
52. Yamasaki C, Tashiro S, Nishito Y, Sueda T, Igarashi K (2005) Dynamic cytoplasmic anchoring of the transcription factor Bach1 by intracellular hyaluronic acid binding protein IHABP. J Biochem 137: 287-296. (Pubitemid 40628434)
53. Ziegler EC, Ghosh S (2005) Regulating inducible transcription through controlled localization. Sci STKE 2005: re6.