Epstein-barr virus-encoded LMP1 interacts with FGD4 to activate Cdc42 and thereby promote migration of nasopharyngeal carcinoma cells

PLoS Pathogens

Volumn 8, Issue 5, 2012, Pages

  Liu, Hao Ping ^a   Chen, Chia Chun ^a   Wu, Chih Ching ^a   Huang, Yi Chuan ^a   Liu, Shu Chen ^a   Liang, Ying ^a   Chang, Kai Ping ^b   Chang, Yu Sun ^a  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; LATENT MEMBRANE PROTEIN 1; PROTEIN CDC42; PROTEIN FGD4; UNCLASSIFIED DRUG; EBV ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN BARR VIRUS; EBV-ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN-BARR VIRUS; FGD4 PROTEIN, HUMAN; INTERLEUKIN 1ALPHA; MATRIX PROTEIN; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA;

ACTIN FILAMENT; ARTICLE; CARCINOGENESIS; CARCINOMA CELL; CASE REPORT; CELL LYSATE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; EPITHELIUM CELL; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; NASOPHARYNX CARCINOMA; NONHUMAN; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR GROWTH; BIOSYNTHESIS; CELL MOTION; CELL STRAIN HEK293; EPSTEIN BARR VIRUS INFECTION; GENETICS; METABOLISM; NASOPHARYNX TUMOR; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

HUMAN HERPESVIRUS 4;

ACTIN CYTOSKELETON; CDC42 GTP-BINDING PROTEIN; CELL LINE, TUMOR; CELL MOVEMENT; EPSTEIN-BARR VIRUS INFECTIONS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HERPESVIRUS 4, HUMAN; HUMANS; INTERLEUKIN-1ALPHA; MICROFILAMENT PROTEINS; NASOPHARYNGEAL NEOPLASMS; RAC1 GTP-BINDING PROTEIN; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; VIRAL MATRIX PROTEINS;

EID: 84863670351     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002690     Document Type: Article

References (70)

1. Niedobitek G, Herbst H, Young LS, Rowe M, Dienemann D, et al. (1992) Epstein-Barr virus and carcinomas. Expression of the viral genome in an undifferentiated gastric carcinoma. Diagn Mol Pathol 1: 103-108.
2. Hsu MM, Tu SM, (1983) Nasopharyngeal carcinoma in Taiwan. Clinical manifestations and results of therapy. Cancer 52: 362-368.
3. Tsao SW, Tramoutanis G, Dawson CW, Lo AK, Huang DP, (2002) The significance of LMP1 expression in nasopharyngeal carcinoma. Semin Cancer Biol 12: 473-487.
4. Baichwal VR, Sugden B, (1988) Transformation of Balb 3T3 cells by the BNLF-1 gene of Epstein-Barr virus. Oncogene 2: 461-467.
5. Wang D, Liebowitz D, Kieff E, (1985) An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells. Cell 43: 831-840.
6. Fahraeus R, Rymo L, Rhim JS, Klein G, (1990) Morphological transformation of human keratinocytes expressing the LMP gene of Epstein-Barr virus. Nature 345: 447-449.
7. Li HP, Chang YS, (2003) Epstein-Barr virus latent membrane protein 1: structure and functions. J Biomed Sci 10: 490-504.
8. Devergne O, Hatzivassiliou E, Izumi KM, Kaye KM, Kleijnen MF, et al. (1996) Association of TRAF1, TRAF2, and TRAF3 with an Epstein-Barr virus LMP1 domain important for B-lymphocyte transformation: role in NF-kappaB activation. Mol Cell Biol 16: 7098-7108.
9. Gires O, Kohlhuber F, Kilger E, Baumann M, Kieser A, et al. (1999) Latent membrane protein 1 of Epstein-Barr virus interacts with JAK3 and activates STAT proteins. EMBO J 18: 3064-3073.
10. Eliopoulos AG, Young LS, (1998) Activation of the cJun N-terminal kinase (JNK) pathway by the Epstein-Barr virus-encoded latent membrane protein 1 (LMP1). Oncogene 16: 1731-1742.
11. Higuchi M, Izumi KM, Kieff E, (2001) Epstein-Barr virus latent-infection membrane proteins are palmitoylated and raft-associated: protein 1 binds to the cytoskeleton through TNF receptor cytoplasmic factors. Proc Natl Acad Sci U S A 98: 4675-4680.
12. Coffin WF 3rd, Geiger TR, Martin JM, (2003) Transmembrane domains 1 and 2 of the latent membrane protein 1 of Epstein-Barr virus contain a lipid raft targeting signal and play a critical role in cytostasis. J Virol 77: 3749-3758.
13. Kaykas A, Worringer K, Sugden B, (2001) CD40 and LMP-1 both signal from lipid rafts but LMP-1 assembles a distinct, more efficient signaling complex. EMBO J 20: 2641-2654.
14. Gires O, Zimber-Strobl U, Gonnella R, Ueffing M, Marschall G, et al. (1997) Latent membrane protein 1 of Epstein-Barr virus mimics a constitutively active receptor molecule. EMBO J 16: 6131-6140.
15. Eliopoulos AG, Rickinson AB, (1998) Epstein-Barr virus: LMP1 masquerades as an active receptor. Curr Biol 8: R196-198.
16. Lam N, Sugden B, (2003) CD40 and its viral mimic, LMP1: similar means to different ends. Cell Signal 15: 9-16.
17. Puls A, Eliopoulos AG, Nobes CD, Bridges T, Young LS, et al. (1999) Activation of the small GTPase Cdc42 by the inflammatory cytokines TNF(alpha) and IL-1, and by the Epstein-Barr virus transforming protein LMP1. J Cell Sci 112 (Pt 17): 2983-2992.
18. Etienne-Manneville S, Hall A, (2002) Rho GTPases in cell biology. Nature 420: 629-635.
19. Musch A, Cohen D, Kreitzer G, Rodriguez-Boulan E, (2001) cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network. EMBO J 20: 2171-2179.
20. Wu H, Rossi G, Brennwald P, (2008) The ghost in the machine: small GTPases as spatial regulators of exocytosis. Trends Cell Biol 18: 397-404.
21. Harris KP, Tepass U, (2010) Cdc42 and Vesicle Trafficking in Polarized Cells. Traffic 11: 1272-9.
22. Rossman KL, Der CJ, Sondek J, (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 6: 167-180.
23. Schmidt A, Hall A, (2002) Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev 16: 1587-1609.
24. Haddad E, Zugaza JL, Louache F, Debili N, Crouin C, et al. (2001) The interaction between Cdc42 and WASP is required for SDF-1-induced T-lymphocyte chemotaxis. Blood 97: 33-38.
25. Dovas A, Gevrey JC, Grossi A, Park H, Abou-Kheir W, et al. (2009) Regulation of podosome dynamics by WASp phosphorylation: implication in matrix degradation and chemotaxis in macrophages. J Cell Sci 122: 3873-3882.
26. White CD, Brown MD, Sacks DB, (2009) IQGAPs in cancer: a family of scaffold proteins underlying tumorigenesis. FEBS Lett 583: 1817-1824.
27. Kreis P, Barnier JV, (2009) PAK signalling in neuronal physiology. Cell Signal 21: 384-393.
28. Sinha S, Yang W, (2008) Cellular signaling for activation of Rho GTPase Cdc42. Cell Signal 20: 1927-1934.
29. Stendel C, Roos A, Deconinck T, Pereira J, Castagner F, et al. (2007) Peripheral nerve demyelination caused by a mutant Rho GTPase guanine nucleotide exchange factor, frabin/FGD4. Am J Hum Genet 81: 158-164.
30. Obaishi H, Nakanishi H, Mandai K, Satoh K, Satoh A, et al. (1998) Frabin, a novel FGD1-related actin filament-binding protein capable of changing cell shape and activating c-Jun N-terminal kinase. J Biol Chem 273: 18697-18700.
31. Pasteris NG, Gorski JL, (1999) Isolation, characterization, and mapping of the mouse and human Fgd2 genes, faciogenital dysplasia (FGD1; Aarskog syndrome) gene homologues. Genomics 60: 57-66.
32. Pasteris NG, Nagata K, Hall A, Gorski JL, (2000) Isolation, characterization, and mapping of the mouse Fgd3 gene, a new Faciogenital Dysplasia (FGD1; Aarskog Syndrome) gene homologue. Gene 242: 237-247.
33. Zheng Y, Fischer DJ, Santos MF, Tigyi G, Pasteris NG, et al. (1996) The faciogenital dysplasia gene product FGD1 functions as a Cdc42Hs-specific guanine-nucleotide exchange factor. J Biol Chem 271: 33169-33172.
34. Delague V, Jacquier A, Hamadouche T, Poitelon Y, Baudot C, et al. (2007) Mutations in FGD4 encoding the Rho GDP/GTP exchange factor FRABIN cause autosomal recessive Charcot-Marie-Tooth type 4H. Am J Hum Genet 81: 1-16.
35. Nakanishi H, Takai Y, (2008) Frabin and other related Cdc42-specific guanine nucleotide exchange factors couple the actin cytoskeleton with the plasma membrane. J Cell Mol Med 12: 1169-1176.
36. Vandenabeele P, Declercq W, Beyaert R, Fiers W, (1995) Two tumour necrosis factor receptors: structure and function. Trends Cell Biol 5: 392-399.
37. Estrada L, Caron E, Gorski JL, (2001) Fgd1, the Cdc42 guanine nucleotide exchange factor responsible for faciogenital dysplasia, is localized to the subcortical actin cytoskeleton and Golgi membrane. Hum Mol Genet 10: 485-495.
38. Kim Y, Ikeda W, Nakanishi H, Tanaka Y, Takekuni K, et al. (2002) Association of frabin with specific actin and membrane structures. Genes Cells 7: 413-420.
39. Kintscher C, Groemping Y, (2009) Characterisation of the nucleotide exchange factor ITSN1L: evidence for a kinetic discrimination of GEF-stimulated nucleotide release from Cdc42. J Mol Biol 387: 270-283.
40. Yang J, Zhang Z, Roe SM, Marshall CJ, Barford D, (2009) Activation of Rho GTPases by DOCK exchange factors is mediated by a nucleotide sensor. Science 325: 1398-1402.
41. Ikeda W, Nakanishi H, Tanaka Y, Tachibana K, Takai Y, (2001) Cooperation of Cdc42 small G protein-activating and actin filament-binding activities of frabin in microspike formation. Oncogene 20: 3457-3463.
42. Rebecchi MJ, Scarlata S, (1998) Pleckstrin homology domains: a common fold with diverse functions. Annu Rev Biophys Biomol Struct 27: 503-528.
43. Lemmon MA, Ferguson KM, (2001) Molecular determinants in pleckstrin homology domains that allow specific recognition of phosphoinositides. Biochem Soc Trans 29: 377-384.
44. Ono Y, Nakanishi H, Nishimura M, Kakizaki M, Takahashi K, et al. (2000) Two actions of frabin: direct activation of Cdc42 and indirect activation of Rac. Oncogene 19: 3050-3058.
45. Gruenheid S, Finlay BB, (2003) Microbial pathogenesis and cytoskeletal function. Nature 422: 775-781.
46. Sallee NA, Rivera GM, Dueber JE, Vasilescu D, Mullins RD, et al. (2008) The pathogen protein EspF(U) hijacks actin polymerization using mimicry and multivalency. Nature 454: 1005-1008.
47. Oliver AW, He X, Borthwick K, Donne AJ, Hampson L, et al. (2011) The HPV16 E6 binding protein Tip-1 interacts with ARHGEF16, which activates Cdc42. Br J Cancer 104: 324-331.
48. Rauch S, Pulkkinen K, Saksela K, Fackler OT, (2008) Human immunodeficiency virus type 1 Nef recruits the guanine exchange factor Vav1 via an unexpected interface into plasma membrane microdomains for association with p21-activated kinase 2 activity. J Virol 82: 2918-2929.
49. Takenawa T, Miki H, (2001) WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J Cell Sci 114: 1801-1809.
50. Liu HP, Wu CC, Chang YS, (2006) PRA1 promotes the intracellular trafficking and NF-kappaB signaling of EBV latent membrane protein 1. EMBO J 25: 4120-4130.
51. Lam N, Sugden B, (2003) LMP1, a viral relative of the TNF receptor family, signals principally from intracellular compartments. EMBO J 22: 3027-3038.
52. Rothenberger S, Rousseaux M, Knecht H, Bender FC, Legler DF, et al. (2002) Association of the Epstein-Barr virus latent membrane protein 1 with lipid rafts is mediated through its N-terminal region. Cell Mol Life Sci 59: 171-180.
53. Yasui T, Luftig M, Soni V, Kieff E, (2004) Latent infection membrane protein transmembrane FWLY is critical for intermolecular interaction, raft localization, and signaling. Proc Natl Acad Sci U S A 101: 278-283.
54. Hart MJ, Jiang X, Kozasa T, Roscoe W, Singer WD, et al. (1998) Direct stimulation of the guanine nucleotide exchange activity of p115 RhoGEF by Galpha13. Science 280: 2112-2114.
55. Kawasaki Y, Senda T, Ishidate T, Koyama R, Morishita T, et al. (2000) Asef, a link between the tumor suppressor APC and G-protein signaling. Science 289: 1194-1197.
56. Anborgh PH, Qian X, Papageorge AG, Vass WC, DeClue JE, et al. (1999) Ras-specific exchange factor GRF: oligomerization through its Dbl homology domain and calcium-dependent activation of Raf. Mol Cell Biol 19: 4611-4622.
57. Chen XM, Splinter PL, Tietz PS, Huang BQ, Billadeau DD, et al. (2004) Phosphatidylinositol 3-kinase and frabin mediate Cryptosporidium parvum cellular invasion via activation of Cdc42. J Biol Chem 279: 31671-31678.
58. Dawson CW, Tramountanis G, Eliopoulos AG, Young LS, (2003) Epstein-Barr virus latent membrane protein 1 (LMP1) activates the phosphatidylinositol 3-kinase/Akt pathway to promote cell survival and induce actin filament remodeling. J Biol Chem 278: 3694-3704.
59. Osmani N, Peglion F, Chavrier P, Etienne-Manneville S, (2010) Cdc42 localization and cell polarity depend on membrane traffic. J Cell Biol 191: 1261-1269.
60. Luna A, Matas OB, Martinez-Menarguez JA, Mato E, Duran JM, et al. (2002) Regulation of protein transport from the Golgi complex to the endoplasmic reticulum by CDC42 and N-WASP. Mol Biol Cell 13: 866-879.
61. Erickson JW, Zhang C, Kahn RA, Evans T, Cerione RA, (1996) Mammalian Cdc42 is a brefeldin A-sensitive component of the Golgi apparatus. J Biol Chem 271: 26850-26854.
62. Egorov MV, Capestrano M, Vorontsova OA, Di Pentima A, Egorova AV, et al. (2009) Faciogenital dysplasia protein (FGD1) regulates export of cargo proteins from the golgi complex via Cdc42 activation. Mol Biol Cell 20: 2413-2427.
63. Houlden H, Hammans S, Katifi H, Reilly MM, (2009) A novel Frabin (FGD4) nonsense mutation p.R275X associated with phenotypic variability in CMT4H. Neurology 72: 617-620.
64. Vallat JM, Ouvrier RA, Pollard JD, Magdelaine C, Zhu D, et al. (2008) Histopathological findings in hereditary motor and sensory neuropathy of axonal type with onset in early childhood associated with mitofusin 2 mutations. J Neuropathol Exp Neurol 67: 1097-1102.
65. Ayala I, Giacchetti G, Caldieri G, Attanasio F, Mariggio S, et al. (2009) Faciogenital dysplasia protein Fgd1 regulates invadopodia biogenesis and extracellular matrix degradation and is up-regulated in prostate and breast cancer. Cancer Res 69: 747-752.
66. Lin CT, Wong CI, Chan WY, Tzung KW, Ho JK, et al. (1990) Establishment and characterization of two nasopharyngeal carcinoma cell lines. Lab Invest 62: 713-724.
67. Lin CT, Chan WY, Chen W, Huang HM, Wu HC, et al. (1993) Characterization of seven newly established nasopharyngeal carcinoma cell lines. Lab Invest 68: 716-727.
68. Tsao SW, Wang X, Liu Y, Cheung YC, Feng H, et al. (2002) Establishment of two immortalized nasopharyngeal epithelial cell lines using SV40 large T and HPV16E6/E7 viral oncogenes. Biochim Biophys Acta 1590: 150-158.
69. Liu HP, Wu CC, Kao HY, Huang YC, Liang Y, et al. (2011) Proteome-wide dysregulation by PRA1 depletion delineates a role of PRA1 in lipid transport and cell migration. Mol Cell Proteomics 10: M900641MCP9200.
70. Ravn V, Rasmussen BB, Hojholt L, Barfoed M, Heiberg I, et al. (1993) Reproducibility of subjective immunohistochemical estrogen- and progesterone receptor determination in human endometrium. Pathol Res Pract 189: 1015-1022.