Gem-Induced Cytoskeleton Remodeling Increases Cellular Migration of HTLV-1-Infected Cells, Formation of Infected-to-Target T-Cell Conjugates and Viral Transmission

PLoS Pathogens

Volumn 10, Issue 2, 2014, Pages

  Chevalier, Sébastien A ^a   Turpin, Jocelyn ^a   Cachat, Anne ^a   Afonso, Philippe V ^b   Gessain, Antoine ^b   Brady, John N ^c   Pise Masison, Cynthia A ^c   Mahieux, Renaud ^a  

^a UNIVERSITÉ DE LYON   (France)

^b INSTITUT PASTEUR   (France)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYTOSKELETON PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN GEM; STROMAL CELL DERIVED FACTOR 1; TAX PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CONTACT; CELL MIGRATION; CHEMOTAXIS; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; IMMUNOFLUORESCENCE TEST; NONHUMAN; PROMOTER REGION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; UPREGULATION; VIRUS TRANSMISSION; WESTERN BLOTTING; WOUND HEALING;

CELL LINE; CHEMOTAXIS, LEUKOCYTE; CHROMATIN IMMUNOPRECIPITATION; CYTOSKELETON; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, VIRAL; GENE PRODUCTS, TAX; HUMAN T-LYMPHOTROPIC VIRUS 1; IMMUNOBLOTTING; MONOMERIC GTP-BINDING PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TRANSCRIPTIONAL ACTIVATION; TRANSDUCTION, GENETIC;

EID: 84895727884     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003917     Document Type: Article

References (48)

1. Gessain A, Cassar O, (2012) Epidemiological Aspects and World Distribution of HTLV-1 Infection. Front Microbiol 3: 388.
2. Uchiyama T, Yodoi J, Sagawa K, Takatsuki K, Uchino H, (1977) Adult T-cell leukemia: clinical and hematologic features of 16 cases. Blood 50: 481-492.
3. Gessain A, Barin F, Vernant JC, Gout O, Maurs L, et al. (1985) Antibodies to human T-lymphotropic virus type-I in patients with tropical spastic paraparesis. Lancet 2: 407-410.
4. Osame M, Usuku K, Izumo S, Ijichi N, Amitani H, et al. (1986) HTLV-I associated myelopathy, a new clinical entity. Lancet 1: 1031-1032.
5. Boxus M, Willems L, (2009) Mechanisms of HTLV-1 persistence and transformation. Br J Cancer 101: 1497-1501.
6. Currer R, Van Duyne R, Jaworski E, Guendel I, Sampey G, et al. (2012) HTLV tax: a fascinating multifunctional co-regulator of viral and cellular pathways. Front Microbiol 3: 406.
7. Journo C, Douceron E, Mahieux R, (2009) HTLV gene regulation: because size matters, transcription is not enough. Future Microbiol 4: 425-440.
8. Bellon M, Baydoun HH, Yao Y, Nicot C, (2010) HTLV-I Tax-dependent and-independent events associated with immortalization of human primary T lymphocytes. Blood 115: 2441-2448.
9. Hasegawa H, Sawa H, Lewis MJ, Orba Y, Sheehy N, et al. (2006) Thymus-derived leukemia-lymphoma in mice transgenic for the Tax gene of human T-lymphotropic virus type I. Nat Med 12: 466-472.
10. Derse D, Hill SA, Lloyd PA, Chung H, Morse BA, (2001) Examining human T-lymphotropic virus type 1 infection and replication by cell-free infection with recombinant virus vectors. J Virol 75: 8461-8468.
11. Pique C, Jones KS, (2012) Pathways of cell-cell transmission of HTLV-1. Front Microbiol 3: 378.
12. Igakura T, Stinchcombe JC, Goon PK, Taylor GP, Weber JN, et al. (2003) Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton. Science 299: 1713-1716.
13. Pais-Correia AM, Sachse M, Guadagnini S, Robbiati V, Lasserre R, et al. (2010) Biofilm-like extracellular viral assemblies mediate HTLV-1 cell-to-cell transmission at virological synapses. Nat Med 16: 83-89.
14. Nejmeddine M, Barnard AL, Tanaka Y, Taylor GP, Bangham CR, (2005) Human T-lymphotropic virus, type 1, tax protein triggers microtubule reorientation in the virological synapse. J Biol Chem 280: 29653-29660.
15. Nejmeddine M, Negi VS, Mukherjee S, Tanaka Y, Orth K, et al. (2009) HTLV-1-Tax and ICAM-1 act on T-cell signal pathways to polarize the microtubule-organizing center at the virological synapse. Blood 114: 1016-1025.
16. Majorovits E, Nejmeddine M, Tanaka Y, Taylor GP, Fuller SD, et al. (2008) Human T-lymphotropic virus-1 visualized at the virological synapse by electron tomography. PLoS One 3: e2251.
17. Chevalier SA, Durand S, Dasgupta A, Radonovich M, Cimarelli A, et al. (2012) The transcription profile of Tax-3 is more similar to Tax-1 than Tax-2: insights into HTLV-3 potential leukemogenic properties. PLoS One 7: e41003.
18. Ward Y, Kelly K, (2006) Gem protein signaling and regulation. Methods Enzymol 407: 468-483.
19. Kelly K, (2005) The RGK family: a regulatory tail of small GTP-binding proteins. Trends Cell Biol 15: 640-643.
20. Opatowsky Y, Sasson Y, Shaked I, Ward Y, Chomsky-Hecht O, et al. (2006) Structure-function studies of the G-domain from human gem, a novel small G-protein. FEBS Lett 580: 5959-5964.
21. Correll RN, Pang C, Niedowicz DM, Finlin BS, Andres DA, (2008) The RGK family of GTP-binding proteins: regulators of voltage-dependent calcium channels and cytoskeleton remodeling. Cell Signal 20: 292-300.
22. Maguire J, Santoro T, Jensen P, Siebenlist U, Yewdell J, et al. (1994) Gem: an induced, immediate early protein belonging to the Ras family. Science 265: 241-244.
23. Hatzoglou A, Ader I, Splingard A, Flanders J, Saade E, et al. (2007) Gem associates with Ezrin and acts via the Rho-GAP protein Gmip to down-regulate the Rho pathway. Mol Biol Cell 18: 1242-1252.
24. Suyama E, Kawasaki H, Nakajima M, Taira K, (2003) Identification of genes involved in cell invasion by using a library of randomized hybrid ribozymes. Proc Natl Acad Sci U S A 100: 5616-5621.
25. Kress AK, Kalmer M, Rowan AG, Grassmann R, Fleckenstein B, (2011) The tumor marker Fascin is strongly induced by the Tax oncoprotein of HTLV-1 through NF-kappaB signals. Blood 117: 3609-3612.
26. Ng PW, Iha H, Iwanaga Y, Bittner M, Chen Y, et al. (2001) Genome-wide expression changes induced by HTLV-1 Tax: evidence for MLK-3 mixed lineage kinase involvement in Tax-mediated NF-kappaB activation. Oncogene 20: 4484-4496.
27. Pise-Masison CA, Radonovich M, Mahieux R, Chatterjee P, Whiteford C, et al. (2002) Transcription profile of cells infected with human T-cell leukemia virus type I compared with activated lymphocytes. Cancer Res 62: 3562-3571.
28. Conkright MD, Guzman E, Flechner L, Su AI, Hogenesch JB, et al. (2003) Genome-wide analysis of CREB target genes reveals a core promoter requirement for cAMP responsiveness. Mol Cell 11: 1101-1108.
29. Kwok RP, Laurance ME, Lundblad JR, Goldman PS, Shih H, et al. (1996) Control of cAMP-regulated enhancers by the viral transactivator Tax through CREB and the co-activator CBP. Nature 380: 642-646.
30. Ward Y, Yap SF, Ravichandran V, Matsumura F, Ito M, et al. (2002) The GTP binding proteins Gem and Rad are negative regulators of the Rho-Rho kinase pathway. J Cell Biol 157: 291-302.
31. Mitchison TJ, Cramer LP, (1996) Actin-based cell motility and cell locomotion. Cell 84: 371-379.
32. Varrin-Doyer M, Nicolle A, Marignier R, Cavagna S, Benetollo C, et al. (2012) Human T lymphotropic virus type 1 increases T lymphocyte migration by recruiting the cytoskeleton organizer CRMP2. J Immunol 188: 1222-1233.
33. Afonso PV, Ozden S, Prevost MC, Schmitt C, Seilhean D, et al. (2007) Human blood-brain barrier disruption by retroviral-infected lymphocytes: role of myosin light chain kinase in endothelial tight-junction disorganization. J Immunol 179: 2576-2583.
34. Van Prooyen N, Gold H, Andresen V, Schwartz O, Jones K, et al. (2010) Human T-cell leukemia virus type 1 p8 protein increases cellular conduits and virus transmission. Proc Natl Acad Sci U S A 107: 20738-20743.
35. Riento K, Ridley AJ, (2003) Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol 4: 446-456.
36. Wu Y, Yoder A, Yu D, Wang W, Liu J, et al. (2008) Cofilin activation in peripheral CD4 T cells of HIV-1 infected patients: a pilot study. Retrovirology 5: 95.
37. Yoder A, Yu D, Dong L, Iyer SR, Xu X, et al. (2008) HIV envelope-CXCR4 signaling activates cofilin to overcome cortical actin restriction in resting CD4 T cells. Cell 134: 782-792.
38. Arimura N, Inagaki N, Chihara K, Menager C, Nakamura N, et al. (2000) Phosphorylation of collapsin response mediator protein-2 by Rho-kinase. Evidence for two separate signaling pathways for growth cone collapse. J Biol Chem 275: 23973-23980.
39. Jayo A, Parsons M, Adams JC, (2012) A novel Rho-dependent pathway that drives interaction of fascin-1 with p-Lin-11/Isl-1/Mec-3 kinase (LIMK) 1/2 to promote fascin-1/actin binding and filopodia stability. BMC Biol 10: 72.
40. Li Q, Lu F, Wang K, (2012) Modeling of HIV-1 infection: insights to the role of monocytes/macrophages, latently infected T4 cells, and HAART regimes. PLoS One 7: e46026.
41. Nagata K, Ohtani K, Nakamura M, Sugamura K, (1989) Activation of endogenous c-fos proto-oncogene expression by human T-cell leukemia virus type I-encoded p40tax protein in the human T-cell line, Jurkat. J Virol 63: 3220-3226.
42. Ward Y, Spinelli B, Quon MJ, Chen H, Ikeda SR, et al. (2004) Phosphorylation of critical serine residues in Gem separates cytoskeletal reorganization from down-regulation of calcium channel activity. Mol Cell Biol 24: 651-661.
43. Meertens L, Chevalier S, Weil R, Gessain A, Mahieux R, (2004) A 10-amino acid domain within human T-cell leukemia virus type 1 and type 2 tax protein sequences is responsible for their divergent subcellular distribution. J Biol Chem 279: 43307-43320.
44. Cho SJ, Lee SS, Kim YJ, Park BD, Choi JS, et al. (2010) Xylocydine, a novel Cdk inhibitor, is an effective inducer of apoptosis in hepatocellular carcinoma cells in vitro and in vivo. Cancer Lett 287: 196-206.
45. Zhou M, Lu H, Park H, Wilson-Chiru J, Linton R, et al. (2006) Tax interacts with P-TEFb in a novel manner to stimulate human T-lymphotropic virus type 1 transcription. J Virol 80: 4781-4791.
46. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676-682.
47. Journo C, Bonnet A, Favre-Bonvin A, Turpin J, Vinera J, et al. (2013) Human T cell leukemia virus type 2 tax-mediated NF-kappaB activation involves a mechanism independent of Tax conjugation to ubiquitin and SUMO. J Virol 87: 1123-1136.
48. Astier-Gin T, Portail JP, Lafond F, Guillemain B, (1995) Identification of HTLV-I- or HTLV-II-producing cells by cocultivation with BHK-21 cells stably transfected with a LTR-lacZ gene construct. J Virol Methods 51: 19-29.