Cell susceptibility to baculovirus transduction and echovirus infection is modified by protein kinase C phosphorylation and vimentin organization

Journal of Virology

Volumn 87, Issue 17, 2013, Pages 9822-9835

  Turkki, Paula ^a   Makkonen, Kaisa Emilia ^b   Huttunen, Moona ^a   Laakkonen, Johanna P ^b   Ylä Herttuala, Seppo ^b,c   Airenne, Kari J ^b   Marjomäki, Varpu ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C EPSILON; SYNDECAN 1; SYNTENIN; VIMENTIN; VIRUS RECEPTOR;

ARTICLE; BACULOVIRUS; CELL SPECIFICITY; CELL STRAIN HEPG2; CELL SURFACE; CONTROLLED STUDY; CULTURE MEDIUM; ECHO VIRUS; ECHO VIRUS 1; ECHOVIRUS INFECTION; ENZYME ACTIVATION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; INFECTION RATE; INFECTION SENSITIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS ENTRY;

ANIMALS; BACULOVIRIDAE; CELL LINE; CULTURE MEDIA; ENTEROVIRUS B, HUMAN; HEK293 CELLS; HEP G2 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTEGRIN ALPHA2BETA1; MICE; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN KINASE C-ALPHA; PROTEIN KINASE C-EPSILON; RECEPTORS, VIRUS; SYNDECAN-1; TRANSDUCTION, GENETIC; VIMENTIN; VIRULENCE; VIRUS INTERNALIZATION;

EID: 84883307565     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01004-13     Document Type: Article

References (60)

1. Chen CY, Lin CY, Chen GY, Hu YC. 2011. Baculovirus as a gene delivery vector: recent understandings of molecular alterations in transduced cells and latest applications. Biotechnol. Adv. 29:618-631.
2. Airenne KJ, Hu YC, Kost TA, Smith RH, Kotin RM, Ono C, Matsuura Y, Wang S, Yla-Herttuala S. 2013. Baculovirus: an insect-derived vector for diverse gene transfer applications. Mol. Ther. doi:10.1038/mt.2012 .286.
3. Airenne KJ, Makkonen KE, Mahonen AJ, Yla-Herttuala S. 2010. In vivo application and tracking of baculovirus. Curr. Gene Ther. 10:187-194.
4. Kost TA, Condreay JP. 2002. Recombinant baculoviruses as mammalian cell gene-delivery vectors. Trends Biotechnol. 20:173-180.
5. Kost TA, Condreay JP, Jarvis DL. 2005. Baculovirus as versatile vectors for protein expression in insect and mammalian cells. Nat. Biotechnol. 23:567-575.
6. Kukkonen SP, Airenne KJ, Marjomaki V, Laitinen OH, Lehtolainen P, Kankaanpaa P, Mahonen AJ, Raty JK, Nordlund HR, Oker-Blom C, Kulomaa MS, Yla-Herttuala S. 2003. Baculovirus capsid display: a novel tool for transduction imaging. Mol. Ther. 8:853-862.
7. Airenne KJ, Laitinen OH, Mahonen AJ, Yla-Herttuala S. 2009. Transduction of vertebrate cells with recombinant baculovirus. Cold Spring Harb. Protoc. 2009:pdb.prot5182. doi:10.1101/pdb.prot5182.
8. Mahonen AJ, Airenne KJ, Purola S, Peltomaa E, Kaikkonen MU, Riekkinen MS, Heikura T, Kinnunen K, Roschier MM, Wirth T, Yla-Herttuala S. 2007. Post-transcriptional regulatory element boosts baculovirus-mediated gene expression in vertebrate cells. J. Biotechnol. 131: 1-8.
9. Boyce FM, Bucher NL. 1996. Baculovirus-mediated gene transfer into mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 93:2348-2352.
10. Hofmann C, Sandig V, Jennings G, Rudolph M, Schlag P, Strauss M. 1995. Efficient gene transfer into human hepatocytes by baculovirus vectors. Proc. Natl. Acad. Sci. U. S. A. 92:10099-10103.
11. Song SU, Shin SH, Kim SK, Choi GS, Kim WC, Lee MH, Kim SJ, Kim IH, Choi MS, Hong YJ, Lee KH. 2003. Effective transduction of osteogenic sarcoma cells by a baculovirus vector. J. Gen. Virol. 84:697-703.
12. Mahonen AJ, Makkonen KE, Laakkonen JP, Ihalainen TO, Kukkonen SP, Kaikkonen MU, Vihinen-Ranta M, Yla-Herttuala S, Airenne KJ. 2010. Culture medium induced vimentin reorganization associates with enhanced baculovirus-mediated gene delivery. J. Biotechnol. 145:111-119.
13. Tuthill TJ, Groppelli E, Hogle JM, Rowlands DJ. 2010. Picornaviruses. Curr. Top. Microbiol. Immunol. 343:43-89.
14. Sawyer MH. 2002. Enterovirus infections: diagnosis and treatment. Semin. Pediatr. Infect. Dis. 13:40-47.
15. Muir P, Kammerer U, Korn K, Mulders MN, Poyry T, Weissbrich B, Kandolf R, Cleator GM, van Loon AM. 1998. Molecular typing of enteroviruses: current status and future requirements. The European Union Concerted Action on Virus Meningitis and Encephalitis. Clin. Microbiol. Rev. 11:202-227.
16. Whitton JL, Cornell CT, Feuer R. 2005. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 3:765-776.
17. Mizejewski GJ. 1999. Role of integrins in cancer: survey of expression patterns. Proc. Soc. Exp. Biol. Med. 222:124-138.
18. Upla P, Marjomaki V, Kankaanpaa P, Ivaska J, Hyypia T, Van Der Goot FG, Heino J. 2004. Clustering induces a lateral redistribution of alpha 2 beta 1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. Mol. Biol. Cell 15:625-636.
19. Karjalainen M, Kakkonen E, Upla P, Paloranta H, Kankaanpaa P, Liberali P, Renkema GH, Hyypia T, Heino J, Marjomaki V. 2008. ARaft-derived, Pak1-regulated entry participates in alpha2beta1 integrindependent sorting to caveosomes. Mol. Biol. Cell 19:2857-2869.
20. Teng YH, Aquino RS, Park PW. 2012. Molecular functions of syndecan-1 in disease. Matrix Biol. 31:3-16.
21. Couchman JR. 2010. Transmembrane signaling proteoglycans. Annu. Rev. Cell Dev. Biol. 26:89-114.
22. Rapraeger A, Jalkanen M, Bernfield M. 1986. Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells. J. Cell Biol. 103:2683-2696.
23. Carey DJ, Stahl RC, Tucker B, Bendt KA, Cizmeci-Smith G. 1994. Aggregation-induced association of syndecan-1 with microfilaments mediated by the cytoplasmic domain. Exp. Cell Res. 214:12-21.
24. Choi Y, Chung H, Jung H, Couchman JR, Oh ES. 2011. Syndecans as cell surface receptors: unique structure equates with functional diversity. Matrix Biol. 30:93-99.
25. Chen Y, Gotte M, Liu J, Park PW. 2008. Microbial subversion of heparan sulfate proteoglycans. Mol. Cells 26:415-426.
26. Stewart PL, Nemerow GR. 2007. Cell integrins: commonly used receptors for diverse viral pathogens. Trends Microbiol. 15:500-507.
27. Fears CY, Woods A. 2006. The role of syndecans in disease and wound healing. Matrix Biol. 25:443-456.
28. Marjomaki V, Pietiainen V, Matilainen H, Upla P, Ivaska J, Nissinen L, Reunanen Huttunen HP, Hyypia T, Heino J. 2002. Internalization of echovirus 1 in caveolae. J. Virol. 76:1856-1865.
29. Laakkonen JP, Makela AR, Kakkonen E, Turkki P, Kukkonen S, Peranen J, Yla-Herttuala S, Airenne KJ, Oker-Blom C, Vihinen-Ranta M, Marjomaki V. 2009. Clathrin-independent entry of baculovirus triggers uptake of E. coli in non-phagocytic human cells. PLoS One 4:e5093. doi: 10.1371/journal.pone.0005093.
30. Kankaanpaa P, Paavolainen L, Tiitta S, Karjalainen M, Paivarinne J, Nieminen J, Marjomaki V, Heino J, White DJ. 2012. BioImageXD: an open, general-purpose and high-throughput image-processing platform. Nat. Methods 9:683-689.
31. Karjalainen M, Rintanen N, Lehkonen M, Kallio K, Maki A, Hellstrom K, Siljamaki V, Upla P, Marjomaki V. 2011. Echovirus 1 infection depends on biogenesis of novel multivesicular bodies. Cell. Microbiol. 13:1975-1995.
32. Ohkawa T, Volkman LE, Welch MD. 2010. Actin-based motility drives baculovirus transit to the nucleus and cell surface. J. Cell Biol. 190:187-195.
33. Tkachenko E, Lutgens E, Stan RV, Simons M. 2004. Fibroblast growth factor 2 endocytosis in endothelial cells proceed via syndecan-4-dependent activation of Rac1 and a Cdc42-dependent macropinocytic pathway. J. Cell Sci. 117:3189-3199.
34. Fuki IV, Kuhn KM, Lomazov IR, Rothman VL, Tuszynski GP, Iozzo RV, Swenson TL, Fisher EA, Williams KJ. 1997. The syndecan family of proteoglycans. Novel receptors mediating internalization of atherogenic lipoproteins in vitro. J. Clin. Invest. 100:1611-1622.
35. Zimmermann P, Zhang Z, Degeest G, Mortier E, Leenaerts I, Coomans C, Schulz J, N'Kuli F, Courtoy PJ, David G. 2005. Syndecan recycling is controlled by syntenin-PIP2 interaction and Arf. Dev. Cell 9:377-388.
36. Ng T, Shima D, Squire A, Bastiaens PI, Gschmeissner S, Humphries MJ, Parker PJ. 1999. PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J. 18: 3909-3923.
37. Ivaska J, Vuoriluoto K, Huovinen T, Izawa I, Inagaki M, Parker PJ. 2005. PKCepsilon-mediated phosphorylation of vimentin controls integrin recycling and motility. EMBO J. 24:3834-3845.
38. Ivaska J, Whelan RD, Watson R, Parker PJ. 2002. PKC controls the traffic of ε1 integrins in motile cells. EMBO J. 21:3608-3619.
39. Freeley M, Kelleher D, Long A. 2011. Regulation of protein kinase C function by phosphorylation on conserved and non-conserved sites. Cell. Signal. 23:753-762.
40. Steinberg SF. 2008. Structural basis of protein kinase C isoform function. Physiol. Rev. 88:1341-1378.
41. Hwangbo C, Kim J, Lee JJ, Lee JH. 2010. Activation of the integrin effector kinase focal adhesion kinase in cancer cells is regulated by crosstalk between protein kinase Calpha and the PDZ adapter protein mda-9/ Syntenin. Cancer Res. 70:1645-1655.
42. Fuki IV, Meyer ME, Williams KJ. 2000. Transmembrane and cytoplasmic domains of syndecan mediate a multi-step endocytic pathway involving detergent-insoluble membrane rafts. Biochem. J. 351:607-612.
43. Powelka AM, Sun J, Li J, Gao M, Shaw LM, Sonnenberg A, Hsu VW. 2004. Stimulation-dependent recycling of integrin beta1 regulated by ARF6 and Rab11. Traffic 5:20-36.
44. Stefanovic S, Windsor M, Nagata KI, Inagaki M, Wileman T. 2005. Vimentin rearrangement during African swine fever virus infection involves retrograde transport along microtubules and phosphorylation of vimentin by calcium calmodulin kinase II. J. Virol. 79:11766-11775.
45. Ferreira LR, Moussatche N, Moura Neto V. 1994. Rearrangement of intermediate filament network of BHK-21 cells infected with vaccinia virus. Arch. Virol. 138:273-285.
46. Snasel J, Shoeman R, Horejsi M, Hruskova-Heidingsfeldova O, Sedlacek J, Ruml T, Pichova I. 2000. Cleavage of vimentin by different retroviral proteases. Arch. Biochem. Biophys. 377:241-245.
47. Belin MT, Boulanger P. 1987. Processing of vimentin occurs during the early stages of adenovirus infection. J. Virol. 61:2559-2566.
48. Nuesch JP, Lachmann S, Rommelaere J. 2005. Selective alterations of the host cell architecture upon infection with parvovirus minute virus of mice. Virology 331:159-174.
49. Kanlaya R, Pattanakitsakul SN, Sinchaikul S, Chen ST, Thongboonkerd V. 2010. Vimentin interacts with heterogeneous nuclear ribonucleoproteins and dengue nonstructural protein 1 and is important for viral replication and release. Mol. Biosyst. 6:795-806.
50. Das S, Ravi V, Desai A. 2011. Japanese encephalitis virus interacts with vimentin to facilitate its entry into porcine kidney cell line. Virus Res. 160:404-408.
51. Liang JJ, Yu CY, Liao CL, Lin YL. 2011. Vimentin binding is critical for infection by the virulent strain of Japanese encephalitis virus. Cell. Microbiol. 13:1358-1370.
52. Miller MS, Hertel L. 2009. Onset of human cytomegalovirus replication in fibroblasts requires the presence of an intact vimentin cytoskeleton. J. Virol. 83:7015-7028.
53. Ghosh S, Ahrens WA, Phatak SU, Hwang S, Schrum LW, Bonkovsky HL. 2011. Association of filamin A and vimentin with hepatitis C virus proteins in infected human hepatocytes. J. Viral Hepat. 18:e568 -77. doi: 10.1111/j.1365-2893.2011.01487.x.
54. Armer H, Moffat K, Wileman T, Belsham GJ, Jackson T, Duprex WP, Ryan M, Monaghan P. 2008. Foot-and-mouth disease virus, but not bovine enterovirus, targets the host cell cytoskeleton via the nonstructural protein 3Cpro. J. Virol. 82:10556-10566.
55. Eriksson JE, Brautigan DL, Vallee R, Olmsted J, Fujiki H, Goldman RD. 1992. Cytoskeletal integrity in interphase cells requires protein phosphatase activity. Proc. Natl. Acad. Sci. U. S. A. 89:11093-11097.
56. Keum E, Kim Y, Kim J, Kwon S, Lim Y, Han I, Oh ES. 2004. Syndecan-4 regulates localization, activity and stability of protein kinase C-alpha. Biochem. J. 378:1007-1014.
57. Lim ST, Longley RL, Couchman JR, Woods A. 2003. Direct binding of syndecan-4 cytoplasmic domain to the catalytic domain of protein kinase C alpha (PKC alpha) increases focal adhesion localization of PKC alpha. J. Biol. Chem. 278:13795-13802.
58. Horowitz A, Simons M. 1998. Phosphorylation of the cytoplasmic tail of syndecan-4 regulates activation of protein kinase Calpha. J. Biol. Chem. 273:25548-25551.
59. Simons M, Horowit A. 2001. Syndecan-4-mediated signalling. Cell. Signal. 13:855-862.
60. Eriksson JE, He T, Trejo-Skalli AV, Harmala-Brasken AS, Hellman J, Chou YH, Goldman RD. 2004. Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J. Cell Sci. 117:919-932.