Vaccinia Virus Protein Complex F12/E2 Interacts with Kinesin Light Chain Isoform 2 to Engage the Kinesin-1 Motor Complex

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Viruses often hijack the cellular transport systems to facilitate their movement within and between cells. Vaccinia virus (VACV), the smallpox vaccine, is very adept at this and exploits cellular transport machinery at several stages during its life cycle. For instance, during transport of new virus particles to the cell surface VACV interacts with a protein motor complex called kinesin-1 that moves cargo on microtubules. However, details of the cellular and viral components needed and the molecular mechanisms involved remain poorly understood. Hitherto, only the VACV protein A36 has been shown to interact with kinesin-1, however viruses lacking A36 still reach the cell surface, albeit at reduced efficiency, indicating other factors are involved. Here we describe an interaction between kinesin-1 and a complex of VACV proteins F12 and E2, which are both needed for virus transport. The F12/E2 complex associates with a subset of kinesin-1 molecules (kinesin light chain isoform 2) with a region thought to be involved in modulation of cargo binding and kinesin-1 motor activity. Further study of this interaction will enhance understanding of the VACV life cycle and of the roles of different kinesin-1 subtypes in cellular processes and the mechanisms that regulate them.

Vyšlo v časopise: Vaccinia Virus Protein Complex F12/E2 Interacts with Kinesin Light Chain Isoform 2 to Engage the Kinesin-1 Motor Complex. PLoS Pathog 11(3): e32767. doi:10.1371/journal.ppat.1004723
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004723

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Zdroje

1. Moss B (2013) Poxviridae. In: Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA et al., editors. Fields Virology. Philadelphia, Baltimore, New York, London, Buenos Aires, Hong Kong, Sydney, Tokyo: Wolters Kluwer/Lippincott Williams & Wilkins.

2. Fenner F, Anderson DA, Arita I, Jezek Z, Ladnyi ID (1988) Smallpox and its Eradication. Geneva: World Health Organisation.

3. Roberts KL, Smith GL (2008) Vaccinia virus morphogenesis and dissemination. Trends Microbiol 16 : 472–479. doi: 10.1016/j.tim.2008.07.009 18789694

4. Smith GL, Vanderplasschen A, Law M (2002) The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83 : 2915–2931. 12466468

5. Liu L, Cooper T, Howley PM, Hayball JD (2014) From crescent to mature virion: vaccinia virus assembly and maturation. Viruses 6 : 3787–3808. doi: 10.3390/v6103787 25296112

6. Dales S, Mosbach EH (1968) Vaccinia as a model for membrane biogenesis. Virology 35 : 564–583. 5677800

7. Hollinshead M, Vanderplasschen A, Smith GL, Vaux DJ (1999) Vaccinia virus intracellular mature virions contain only one lipid membrane. J Virol 73 : 1503–1517. 9882356

8. Hollinshead M, Rodger G, Van Eijl H, Law M, Hollinshead R, et al. (2001) Vaccinia virus utilizes microtubules for movement to the cell surface. J Cell Biol 154 : 389–402. 11470826

9. Newsome TP, Weisswange I, Frischknecht F, Way M (2006) Abl collaborates with Src family kinases to stimulate actin-based motility of vaccinia virus. Cell Microbiol 8 : 233–241. 16441434

10. Humphries AC, Dodding MP, Barry DJ, Collinson LM, Durkin CH, et al. (2012) Clathrin potentiates vaccinia-induced actin polymerization to facilitate viral spread. Cell Host Microbe 12 : 346–359. doi: 10.1016/j.chom.2012.08.002 22980331

11. Frischknecht F, Moreau V, Rottger S, Gonfloni S, Reckmann I, et al. (1999) Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401 : 926–929. 10553910

12. Cudmore S, Cossart P, Griffiths G, Way M (1995) Actin-based motility of vaccinia virus. Nature 378 : 636–638. 8524400

13. Cudmore S, Reckmann I, Griffiths G, Way M (1996) Vaccinia virus: a model system for actin-membrane interactions. J Cell Sci 109 1739–1747. 8832396

14. Doceul V, Hollinshead M, Breiman A, Laval K, Smith GL (2012) Protein B5 is required on extracellular enveloped vaccinia virus for repulsion of superinfecting virions. J Gen Virol 93 : 1876–1886. doi: 10.1099/vir.0.043943-0 22622330

15. Doceul V, Hollinshead M, van der Linden L, Smith GL (2010) Repulsion of superinfecting virions: a mechanism for rapid virus spread. Science 327 : 873–876. doi: 10.1126/science.1183173 20093437

16. Carter GC, Law M, Hollinshead M, Smith GL (2005) Entry of the vaccinia virus intracellular mature virion and its interactions with glycosaminoglycans. J Gen Virol 86 : 1279–1290. 15831938

17. Law M, Carter GC, Roberts KL, Hollinshead M, Smith GL (2006) Ligand-induced and nonfusogenic dissolution of a viral membrane. Proc Natl Acad Sci U S A 103 : 5989–5994. 16585508

18. Vanderplasschen A, Hollinshead M, Smith GL (1998) Intracellular and extracellular vaccinia virions enter cells by different mechanisms. J Gen Virol 79 877–887. 9568984

19. Moss B (2006) Poxvirus entry and membrane fusion. Virology 344 : 48–54. 16364735

20. Carter GC, Rodger G, Murphy BJ, Law M, Krauss O, et al. (2003) Vaccinia virus cores are transported on microtubules. J Gen Virol 84 : 2443–2458. 12917466

21. Ward BM (2005) Visualization and characterization of the intracellular movement of vaccinia virus intracellular mature virions. J Virol 79 : 4755–4763. 15795261

22. Sanderson CM, Hollinshead M, Smith GL (2000) The vaccinia virus A27L protein is needed for the microtubule-dependent transport of intracellular mature virus particles. J Gen Virol 81 : 47–58. 10640541

23. Geada MM, Galindo I, Lorenzo MM, Perdiguero B, Blasco R (2001) Movements of vaccinia virus intracellular enveloped virions with GFP tagged to the F13L envelope protein. J Gen Virol 82 : 2747–2760. 11602786

24. Rietdorf J, Ploubidou A, Reckmann I, Holmstrom A, Frischknecht F, et al. (2001) Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nat Cell Biol 3 : 992–1000. 11715020

25. Ward BM, Moss B (2001) Vaccinia virus intracellular movement is associated with microtubules and independent of actin tails. J Virol 75 : 11651–11663. 11689647

26. Ward BM, Moss B (2001) Visualization of intracellular movement of vaccinia virus virions containing a green fluorescent protein-B5R membrane protein chimera. J Virol 75 : 4802–4813. 11312352

27. Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10 : 682–696. doi: 10.1038/nrm2774 19773780

28. Palacios IM, St Johnston D (2002) Kinesin light chain-independent function of the kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte. Development 129 : 5473–5485. 12403717

29. Kanai Y, Okada Y, Tanaka Y, Harada A, Terada S, et al. (2000) KIF5C, a novel neuronal kinesin enriched in motor neurons. J Neurosci 20 : 6374–6384. 10964943

30. Rice SE, Gelfand VI (2006) Paradigm lost: milton connects kinesin heavy chain to miro on mitochondria. J Cell Biol 173 : 459–461. 16717123

31. Rahman A, Friedman DS, Goldstein LS (1998) Two kinesin light chain genes in mice. Identification and characterization of the encoded proteins. J Biol Chem 273 : 15395–15403. 9624122

32. Junco A, Bhullar B, Tarnasky HA, van der Hoorn FA (2001) Kinesin light-chain KLC3 expression in testis is restricted to spermatids. Biol Reprod 64 : 1320–1330. 11319135

33. Engelstad M, Smith GL (1993) The vaccinia virus 42-kDa envelope protein is required for the envelopment and egress of extracellular virus and for virus virulence. Virology 194 : 627–637. 8503178

34. Blasco R, Moss B (1991) Extracellular vaccinia virus formation and cell-to-cell virus transmission are prevented by deletion of the gene encoding the 37,000-Dalton outer envelope protein. J Virol 65 : 5910–5920. 1920620

35. Wolffe EJ, Isaacs SN, Moss B (1993) Deletion of the vaccinia virus B5R gene encoding a 42-kilodalton membrane glycoprotein inhibits extracellular virus envelope formation and dissemination. J Virol 67 : 4732–4741. 8331727

36. van Eijl H, Hollinshead M, Rodger G, Zhang WH, Smith GL (2002) The vaccinia virus F12L protein is associated with intracellular enveloped virus particles and is required for their egress to the cell surface. J Gen Virol 83 : 195–207. 11752717

37. Morgan GW, Hollinshead M, Ferguson BJ, Murphy BJ, Carpentier DC, et al. (2010) Vaccinia protein F12 has structural similarity to kinesin light chain and contains a motor binding motif required for virion export. PLoS Pathog 6: e1000785. doi: 10.1371/journal.ppat.1000785 20195521

38. van Eijl H, Hollinshead M, Smith GL (2000) The vaccinia virus A36R protein is a type Ib membrane protein present on intracellular but not extracellular enveloped virus particles. Virology 271 : 26–36. 10814567

39. Scaplehorn N, Holmstrom A, Moreau V, Frischknecht F, Reckmann I, et al. (2002) Grb2 and Nck act cooperatively to promote actin-based motility of vaccinia virus. Curr Biol 12 : 740–745. 12007418

40. Ward BM, Moss B (2004) Vaccinia virus A36R membrane protein provides a direct link between intracellular enveloped virions and the microtubule motor kinesin. J Virol 78 : 2486–2493. 14963148

41. Herrero-Martinez E, Roberts KL, Hollinshead M, Smith GL (2005) Vaccinia virus intracellular enveloped virions move to the cell periphery on microtubules in the absence of the A36R protein. J Gen Virol 86 : 2961–2968. 16227217

42. Konecna A, Frischknecht R, Kinter J, Ludwig A, Steuble M, et al. (2006) Calsyntenin-1 docks vesicular cargo to kinesin-1. Mol Biol Cell 17 : 3651–3663. 16760430

43. Dodding MP, Mitter R, Humphries AC, Way M (2011) A kinesin-1 binding motif in vaccinia virus that is widespread throughout the human genome. EMBO J 30 : 4523–4538. doi: 10.1038/emboj.2011.326 21915095

44. Yutin N, Faure G, Koonin EV, Mushegian AR (2014) Chordopoxvirus protein F12 implicated in enveloped virion morphogenesis is an inactivated DNA polymerase. Biol Direct 9 : 22. doi: 10.1186/1745-6150-9-22 25374149

45. Johnston SC, Ward BM (2009) Vaccinia virus protein F12 associates with intracellular enveloped virions through an interaction with A36. J Virol 83 : 1708–1717. doi: 10.1128/JVI.01364-08 19052096

46. Dodding MP, Newsome TP, Collinson LM, Edwards C, Way M (2009) An E2-F12 complex is required for intracellular enveloped virus morphogenesis during vaccinia infection. Cell Microbiol 11 : 808–824. doi: 10.1111/j.1462-5822.2009.01296.x 19207726

47. Zhang WH, Wilcock D, Smith GL (2000) Vaccinia virus F12L protein is required for actin tail formation, normal plaque size, and virulence. J Virol 74 : 11654–11662. 11090164

48. Domi A, Weisberg AS, Moss B (2008) Vaccinia virus E2L null mutants exhibit a major reduction in extracellular virion formation and virus spread. J Virol 82 : 4215–4226. doi: 10.1128/JVI.00037-08 18287229

49. Chen RA, Jacobs N, Smith GL (2006) Vaccinia virus strain Western Reserve protein B14 is an intracellular virulence factor. J Gen Virol 87 : 1451–1458. 16690909

50. Chen RA, Ryzhakov G, Cooray S, Randow F, Smith GL (2008) Inhibition of IkappaB kinase by vaccinia virus virulence factor B14. PLoS Pathog 4: e22. doi: 10.1371/journal.ppat.0040022 18266467

51. Stenoien DL, Brady ST (1997) Immunochemical analysis of kinesin light chain function. Mol Biol Cell 8 : 675–689. 9247647

52. Vagnoni A, Rodriguez L, Manser C, De Vos KJ, Miller CC (2011) Phosphorylation of kinesin light chain 1 at serine 460 modulates binding and trafficking of calsyntenin-1. J Cell Sci 124 : 1032–1042. doi: 10.1242/jcs.075168 21385839

53. Ploubidou A, Moreau V, Ashman K, Reckmann I, Gonzalez C, et al. (2000) Vaccinia virus infection disrupts microtubule organization and centrosome function. EMBO J 19 : 3932–3944. 10921875

54. Parkinson JE, Smith GL (1994) Vaccinia virus gene A36R encodes a M(r) 43–50 K protein on the surface of extracellular enveloped virus. Virology 204 : 376–390. 8091668

55. Brum LM, Turner PC, Devick H, Baquero MT, Moyer RW (2003) Plasma membrane localization and fusion inhibitory activity of the cowpox virus serpin SPI-3 require a functional signal sequence and the virus encoded hemagglutinin. Virology 306 : 289–302. 12642102

56. McCart AE, Mahony D, Rothnagel JA (2003) Alternatively spliced products of the human kinesin light chain 1 (KNS2) gene. Traffic 4 : 576–580. 12839500

57. Kamal A, Goldstein LS (2002) Principles of cargo attachment to cytoplasmic motor proteins. Curr Opin Cell Biol 14 : 63–68. 11792546

58. Gyoeva FK, Sarkisov DV, Khodjakov AL, Minin AA (2004) The tetrameric molecule of conventional kinesin contains identical light chains. Biochemistry 43 : 13525–13531. 15491159

59. Maliga Z, Junqueira M, Toyoda Y, Ettinger A, Mora-Bermudez F, et al. (2013) A genomic toolkit to investigate kinesin and myosin motor function in cells. Nat Cell Biol 15 : 325–334. doi: 10.1038/ncb2689 23417121

60. Johnson C, Tinti M, Wood NT, Campbell DG, Toth R, et al. (2011) Visualization and biochemical analyses of the emerging mammalian 14-3-3-phosphoproteome. Mol Cell Proteomics 10: M110 005751.

61. Gyoeva FK, Bybikova EM, Minin AA (2000) An isoform of kinesin light chain specific for the Golgi complex. J Cell Sci 113 2047–2054. 10806115

62. Wozniak MJ, Allan VJ (2006) Cargo selection by specific kinesin light chain 1 isoforms. EMBO J 25 : 5457–5468. 17093494

63. Morfini G, Szebenyi G, Elluru R, Ratner N, Brady ST (2002) Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J 21 : 281–293. 11823421

64. Ichimura T, Wakamiya-Tsuruta A, Itagaki C, Taoka M, Hayano T, et al. (2002) Phosphorylation-dependent interaction of kinesin light chain 2 and the 14–3–3 protein. Biochemistry 41 : 5566–5572. 11969417

65. Hammond JW, Griffin K, Jih GT, Stuckey J, Verhey KJ (2008) Co-operative versus independent transport of different cargoes by Kinesin-1. Traffic 9 : 725–741. doi: 10.1111/j.1600-0854.2008.00722.x 18266909

66. Zhu H, Lee HY, Tong Y, Hong BS, Kim KP, et al. (2012) Crystal structures of the tetratricopeptide repeat domains of kinesin light chains: insight into cargo recognition mechanisms. PLoS One 7: e33943. doi: 10.1371/journal.pone.0033943 22470497

67. Pernigo S, Lamprecht A, Steiner RA, Dodding MP (2013) Structural basis for kinesin-1:cargo recognition. Science 340 : 356–359. doi: 10.1126/science.1234264 23519214

68. Krauss O, Hollinshead R, Hollinshead M, Smith GL (2002) An investigation of incorporation of cellular antigens into vaccinia virus particles. J Gen Virol 83 : 2347–2359. 12237415

69. Morihara T, Hayashi N, Yokokoji M, Akatsu H, Silverman MA, et al. (2014) Transcriptome analysis of distinct mouse strains reveals kinesin light chain-1 splicing as an amyloid-beta accumulation modifier. Proc Natl Acad Sci U S A 111 : 2638–2643. doi: 10.1073/pnas.1307345111 24497505

70. Gan KJ, Morihara T, Silverman MA (2014) Atlas stumbled: Kinesin light chain-1 variant E triggers a vicious cycle of axonal transport disruption and amyloid-beta generation in Alzheimer's disease. Bioessays.

71. Manser C, Guillot F, Vagnoni A, Davies J, Lau KF, et al. (2012) Lemur tyrosine kinase-2 signalling regulates kinesin-1 light chain-2 phosphorylation and binding of Smad2 cargo. Oncogene 31 : 2773–2782. doi: 10.1038/onc.2011.437 21996745

72. Higuchi R, Krummel B, Saiki RK (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res 16 : 7351–7367. 3045756

73. Unterholzner L, Sumner RP, Baran M, Ren H, Mansur DS, et al. (2011) Vaccinia virus protein C6 is a virulence factor that binds TBK-1 adaptor proteins and inhibits activation of IRF3 and IRF7. PLoS Pathog 7: e1002247. doi: 10.1371/journal.ppat.1002247 21931555

74. Falkner FG, Moss B (1990) Transient dominant selection of recombinant vaccinia viruses. J Virol 64 : 3108–3111. 2159565

75. Schmelz M, Sodeik B, Ericsson M, Wolffe EJ, Shida H, et al. (1994) Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans Golgi network. J Virol 68 : 130–147. 8254722

76. Law M, Smith GL (2004) Studying the binding and entry of the intracellular and extracellular enveloped forms of vaccinia virus. Methods Mol Biol 269 : 187–204. 15114017