A cholesterol recognition amino acid consensus domain in GP64 fusion protein facilitates anchoring of baculovirus to mammalian cells

Journal of Virology

Volumn 87, Issue 21, 2013, Pages 11894-11907

  Luz Madrigal, Agustin ^a,b   Asanov, Alexander ^c   Camacho Zarco, Aldo R ^d   Sampieri, Alicia ^e   Vaca, Luis ^a,e  

^a UNIVERSITY OF DAYTON   (United States)

^b MIAMI UNIVERSITY   (United States)

^c TIRF Labs   (United States)

^d MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^e INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CHOLESTEROL; CLATHRIN; DYNAMIN; PROTEIN GP64; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS FUSION PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACULOVIRUS; BACULOVIRUS EXPRESSION SYSTEM; BINDING SITE; CELL MEMBRANE; CONSENSUS SEQUENCE; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; HUMAN; HUMAN CELL; INTERNALIZATION; MAMMAL CELL; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; VIRUS ATTACHMENT; VIRUS CELL INTERACTION;

AMINO ACID MOTIFS; BACULOVIRIDAE; CELL LINE; CHOLESTEROL; ENDOCYTOSIS; HUMANS; VIRAL FUSION PROTEINS; VIRUS ATTACHMENT;

EID: 84886888625     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01356-13     Document Type: Article

References (54)

1. Marsh M, Helenius A. 1989. Virus entry into animal cells. Adv. Virus Res. 36:107-151.
2. Kalia M, Jameel S. 2011. Virus entry paradigms. Amino Acids 41:1147-1157.
3. Jehle JA, Blissard GW, Bonning BC, Cory JS, Herniou EA, Rohrmann GF, Theilmann DA, Thiem SM, Vlak JM. 2006. On the classification and nomenclature of baculoviruses: a proposal for revision. Arch. Virol. 151: 1257-1266.
4. Caron AW, Archambault J, Massie B. 1990. High-level recombinant protein production in bioreactors using the baculovirus-insect cell expression system. Biotechnol. Bioeng. 36:1133-1140.
5. Elias CB, Jardin B, Kamen A. 2007. Recombinant protein production in large-scale agitated bioreactors using the baculovirus expression vector system. Methods Mol. Biol. 388:225-246.
6. McIntosh AH, Shamy R. 1980. Biological studies of a baculovirus in a mammalian cell line. Intervirology 13:331-341.
7. Wang KC, Wu JC, Chung YC, Ho YC, Chang MD, Hu YC. 2005. Baculovirus as a highly efficient gene delivery vector for the expression of hepatitis delta virus antigens in mammalian cells. Biotechnol. Bioeng. 89: 464-473.
8. Condreay JP, Witherspoon SM, Clay WC, Kost TA. 1999. Transient and stable gene expression in mammalian cells transduced with a recombinant baculovirus vector. Proc. Natl. Acad. Sci. U. S. A. 96:127-132.
9. Luz-Madrigal A, Clapp C, Aranda J, Vaca L. 2007. In vivo transcriptional targeting into the retinal vasculature using recombinant baculovirus carrying the human flt-1 promoter. Virol.doi:10.1186/1743-422X-4-88.J. 4:88.
10. Hefferon KL, Oomens AG, Monsma SA, Finnerty CM, Blissard GW. 1999. Host cell receptor binding by baculovirus GP64 and kinetics of virion entry. Virology 258:455-468.
11. Tani H, Nishijima M, Ushijima H, Miyamura T, Matsuura Y. 2001. Characterization of cell-surface determinants important for baculovirus infection. Virology 279:343-353.
12. Duisit G, Saleun S, Douthe S, Barsoum J, Chadeuf G, Moullier P. Baculovirus vector requires electrostatic interactions including heparan sulfate for efficient gene transfer in mammalian cells. J Gene Med. 1:93-102.
13. Kataoka C, Kaname Y, Taguwa S, Abe T, Fukuhara T, Tani H, Moriishi K, Matsuura Y. 2012. Baculovirus GP64-mediated entry into mammalian cells. J. Virol. 86:2610-2620.
14. 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. 10.1371/journal.pone.0005093.4:e5093.
15. Matilainen H, Rinne J, Gilbert L, Marjomaki V, Reunanen H, Oker-Blom C. 2005. Baculovirus entry into human hepatoma cells. J. Virol. 79:15452-15459.
16. Kadlec J, Loureiro S, Abrescia NG, Stuart DI, Jones IM. 2008. The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat. Struct. Mol. Biol. 15:1024-1030.
17. Wiejak J, Wyroba E. 2002. Dynamin: characteristics, mechanism of action and function. Cell. Mol. Biol. Lett. 7:1073-1080.
18. Bonifacino JS, Marks MS, Ohno H, Kirchhausen T. 1996. Mechanisms of signal-mediated protein sorting in the endocytic and secretory pathways. Proc. Assoc. Am. Physician 108:285-295.
19. Laude AJ, Prior IA. 2004. Plasma membrane microdomains: organization, function and trafficking. Mol. Membr. Biol. 21:193-205.
20. Krauss M, Haucke V. 2011. Shaping membranes for endocytosis. Rev. Physiol. Biochem. Pharmacol. 161:45-66.
21. Lung O, Westenberg M, Vlak JM, Zuidema D, Blissard GW. 2002. Pseudotyping Autographa californica multicapsid nucleopolyhedrovirus (AcMNPV): F proteins from group II NPVs are functionally analogous to AcMNPV GP64. 76:5729-5736.
22. Moreno C, Sampieri A, Vivas O, Pena-Segura C, Vaca L. 2012. STIM1 and Orai1 mediate thrombin-induced Ca(2) influx in rat cortical astrocytes. Cell Calcium 52:457-467.
23. Asanov A, Zepeda A, Vaca L. 2010. A novel form of total internal reflection fluorescence microscopy (LG-TIRFM) reveals different and independent lipid raft domains in living cells. Biochim. Biophys. Acta 1801:147-155.
24. Alfonso S, Benito O, Alicia S, Angelica Z, Patricia G, Diana K, Vaca L. 2008. Regulation of the cellular localization and function of human transient receptor potential channel 1 by other members of the TRPC family. Cell Calcium 43:375-387.
25. McIntosh AL, Atshaves BP, Huang H, Gallegos AM, Kier AB, Schroeder F. 2008. Fluorescence techniques using dehydroergosterol to study cholesterol trafficking. Lipids 43:1185-1208.
26. Valdes VJ, Athie A, Salinas LS, Navarro RE, Vaca L. 2012. CUP-1 is a novel protein involved in dietary cholesterol uptake in Caenorhabditis elegans. PLoS One 7:e33962. doi:10.1371/journal.pone.0033962.
27. Manders EMM, Verbeek FJ, Aten JA. 1993. Measurement of colocalization of objects in dual-colour confocal images. J. Microsc. 169: 375-382.
28. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comp. Chem. 25:1605-1612.
29. Ernst WJ, Spenger A, Toellner L, Katinger H, Grabherr RM. 2000. Expanding baculovirus surface display. Modification of the native coat protein gp64 of Autographa californica NPV. Eur. J. Biochem. 267:4033-4039.
30. Asanov A, Zepeda A, Vaca L. 2012. A platform for combined DNA and protein microarrays based on total internal reflection fluorescence. Sensors 12:1800-1815.
31. Ohkubo S, Nakahata N. 2007. Role of lipid rafts in trimeric G proteinmediated signal transduction. Yakugaku Zasshi 127:27-40. (In Japanese.)
32. Simons K, Toomre D. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-39.
33. Zidovetzki R, Levitan I. 2007. Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochim. Biophys. Acta 1768:1311-1324.
34. Li H, Papadopoulos V. 1998. Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern. Endocrinology 139:4991-4997.
35. Schroeder C. 2010. Cholesterol-binding viral proteins in virus entry and morphogenesis. Subcell. Biochem. 51:77-108.
36. Kwon HJ, Abi-Mosleh L, Wang ML, Deisenhofer J, Goldstein JL, Brown MS, Infante RE. 2009. Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 137: 1213-1224.
37. Corbin J, Wang HH, Blanton MP. 1998. Identifying the cholesterol binding domain in the nicotinic acetylcholine receptor with [125I]azidocholesterol. Biochim. Biophys. Acta 1414:65-74.
38. Jafurulla M, Tiwari S, Chattopadhyay A. 2011. Identification of cholesterol recognition amino acid consensus (CRAC) motif in G-protein coupled receptors. Biochem. Biophys. Res. Commun. 404:569-573.
39. Hanson MA, Cherezov V, Griffith MT, Roth CB, Jaakola VP, Chien EY, Velasquez J, Kuhn P, Stevens RC. 2008. A specific cholesterol binding site is established by the 2.8 A structure of the human beta2-adrenergic receptor. Structure 16:897-905.
40. Pfeifer TA, Hegedus DD, Grigliatti TA, Theilmann DA. 1997. Baculovirus immediate-early promoter-mediated expression of the Zeocin resistance gene for use as a dominant selectable marker in dipteran and lepidopteran insect cell lines. Gene 188:183-190.
41. Mercer J, Helenius A. 2009. Virus entry by macropinocytosis. Nat. Cell Biol. 11:510-520.
42. Boyce FM, Bucher NL. 1996. Baculovirus-mediated gene transfer into mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 93:2348-2352.
43. Garry CE, Garry RF. 2009. Proteomics computational analyses suggestthat the bornavirus glycoprotein is a class III viral fusion protein (gamma penetrene). Virol. doi:10.1186/1743-422X-6-145.J. 6:145.
44. Nayak DP, Barman S. 2002. Role of lipid rafts in virus assembly and budding. Adv. Virus Res. 58:1-28.
45. Umashankar. M, Sánchez-San Martín C, Liao M, Reilly B, Guo A, Taylor G, Kielian M. 2008. Differential cholesterol binding by class II fusion proteins determines membrane fusion properties. J. Virol. 82:9245-9253.
46. Phalen T, Kielian M. 1991. Cholesterol is required for infection by Semliki Forest virus. J. Cell Biol. 112:615-623.
47. Roussel A, Lescar J, Vaney M-C, Wengler G, Wengler G, Rey FA. 2006. Structure and interactions at the viral surface of the envelope protein E1 of Semliki Forest virus. Structure 14:75-86.
48. Connolly SA, Longnecker R. 2012. Residues within the C-terminal arm of the herpes simplex virus 1 glycoprotein B ectodomain contribute to its refolding during the fusion step of virus entry. J. Virol. 86:6386-6393.
49. Sáez-Cirión A, Nir S, Lorizate M, Agirre A, Cruz A, Pérez-Gil J, Nieva JL. 2002. Sphingomyelin and cholesterol promote HIV-1 gp41 pretransmembrane sequence surface aggregation and membrane restructuring. J. Biol. Chem. 277:21776-21785.
50. Simons K, Ikonen E. 1997. Functional rafts in cell membranes. Nature 387:569-572.
51. Ares GR, Ortiz PA. 2012. Dynamin2, clathrin, and lipid rafts mediate endocytosis of the apical Na/K/2Cl cotransporter NKCC2 in thick ascending limbs. J. Biol. Chem. 287:37824-37834.
52. Masuyama N, Kuronita T, Tanaka R, Muto T, Hirota Y, Takigawa A, Fujita H, Aso Y, Amano J, Tanaka Y. 2009. HM1.24 is internalized from lipid rafts by clathrin-mediated endocytosis through interaction with alpha-adaptin. J. Biol. Chem. 284:15927-15941.
53. Dong S, Blissard GW. 2012. Functional analysis of the Autographa californica multiple nucleopolyhedrovirus GP64 terminal fusion loops and interactions with membranes. J. Virol. 86:9617-9628.
54. van Loo ND, Fortunati E, Ehlert E, Rabelink M, Grosveld F, Scholte BJ. 2001. Baculovirus infection of nondividing mammalian cells: mechanisms of entry and nuclear transport of capsids. J. Virol. 75:961-970.