Bunyamwera orthobunyavirus glycoprotein precursor is processed by cellular signal peptidase and signal peptide peptidase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 31, 2016, Pages 8825-8830

  Shi, Xiaohong ^a   Botting, Catherine H ^b   Li, Ping ^a   Niglas, Mark ^b   Brennan, Benjamin ^a   Shirran, Sally L ^b   Szemiel, Agnieszka M ^a   Elliott, Richard M ^a  

^a MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; GLYCOPROTEIN; GLYCOPROTEIN GC; GLYCOPROTEIN GN; PROTEIN PRECURSOR; SIGNAL PEPTIDASE; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; ASPARTIC PROTEINASE; MEMBRANE PROTEIN; SERINE PROTEINASE; SIGNAL PEPTIDE PEPTIDASE; TYPE I SIGNAL PEPTIDASE; VIRAL PROTEIN;

BUNYAMWERA VIRUS; CELL FUSION; CONFERENCE PAPER; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN PROCESSING; VIRUS REPLICATION; A-549 CELL LINE; ANIMAL; BINDING SITE; CELL LINE; CHLOROCEBUS AETHIOPS; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN DEGRADATION; TUMOR CELL LINE; VERO CELL LINE;

A549 CELLS; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; BINDING SITES; BUNYAMWERA VIRUS; CELL LINE; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; GLYCOPROTEINS; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; MEMBRANE PROTEINS; PROTEIN PRECURSORS; PROTEOLYSIS; SERINE ENDOPEPTIDASES; VERO CELLS; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84982683066     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1603364113     Document Type: Article

References (46)

1. Plyusnin A, Elliott RM, eds (2011) Bunyaviridae: Molecular and Cellular Biology (Caister Academic, Norfolk, U.K.).
2. Elliott RM, Schmaljohn CS (2013) Bunyaviridae. Fields Virology, eds Knipe DM, Howley PM (Wolters Kluwer, Philadelphia), 6th Ed, pp 1244-1282.
3. Shi X, van Mierlo JT, French A, Elliott RM (2010) Visualizing the replication cycle of bunyamwera orthobunyavirus expressing fluorescent protein-Tagged Gc glycoprotein. J Virol 84(17):8460-8469.
4. Shi X, Brauburger K, Elliott RM (2005) Role of N-linked glycans on bunyamwera virus glycoproteins in intracellular trafficking, protein folding, and virus infectivity. J Virol 79(21):13725-13734.
5. Bowden TA, et al. (2013) Orthobunyavirus ultrastructure and the curious tripodal glycoprotein spike. PLoS Pathog 9(5):e1003374.
6. Garry CE, Garry RF (2004) Proteomics computational analyses suggest that the carboxyl terminal glycoproteins of Bunyaviruses are class II viral fusion protein (betapenetrenes). Theor Biol Med Model 1:10.
7. Shi X, Kohl A, Li P, Elliott RM (2007) Role of the cytoplasmic tail domains of Bunyamwera orthobunyavirus glycoproteins Gn and Gc in virus assembly and morphogenesis. J Virol 81(18):10151-10160.
8. Shi X, et al. (2006) Requirement of the N-Terminal region of orthobunyavirus nonstructural protein NSm for virus assembly and morphogenesis. J Virol 80(16):8089-8099.
9. Fazakerley JK, et al. (1988) Organization of the middle RNA segment of snowshoe hare Bunyavirus. Virology 167(2):422-432.
10. Briese T, Rambaut A, Lipkin WI (2004) Analysis of the medium (M) segment sequence of Guaroa virus and its comparison to other orthobunyaviruses. J GenVirol 85(Pt 10):3071-3077.
11. Elliott RM, Blakqori G (2011) Molecular biology of Orthobunyaviruses. Bunyaviridae, eds Plyusnin A, Elliot RM (Caister Academic, Norfolk, U.K.), pp 1-39.
12. Auclair SM, Bhanu MK, Kendall DA (2012) Signal peptidase I: Cleaving the way to mature proteins. Protein Sci 21(1):13-25.
13. Golde TE, Wolfe MS, Greenbaum DC (2009) Signal peptide peptidases: A family of intramembrane-cleaving proteases that cleave type 2 transmembrane proteins. Semin Cell Dev Biol 20(2):225-230.
14. Lemberg MK (2011) Intramembrane proteolysis in regulated protein trafficking. Traffic 12(9):1109-1118.
15. Voss M, Schröder B, Fluhrer R (2013) Mechanism, specificity, and physiology of signal peptide peptidase (SPP) and SPP-like proteases. Biochim Biophys Acta Biomembranes (12):2828-2839.
16. Weihofen A, Martoglio B (2003) Intramembrane-cleaving proteases: Controlled liberation of proteins and bioactive peptides. Trends Cell Biol 13(2):71-78.
17. Friedmann E, et al. (2006) SPPL2a and SPPL2b promote intramembrane proteolysis of TNFalpha in activated dendritic cells to trigger IL-12 production. Nat Cell Biol 8(8):843-848.
18. Oliveira CC, et al. (2013) New role of signal peptide peptidase to liberate C-Terminal peptides for MHC class I presentation. J Immunol 191(8):4020-4028.
19. Lemberg MK, Bland FA, Weihofen A, Braud VM, Martoglio B (2001) Intramembrane proteolysis of signal peptides: An essential step in the generation of HLA-E epitopes. J Immunol 167(11):6441-6446.
20. McLauchlan J, Lemberg MK, Hope G, Martoglio B (2002) Intramembrane proteolysis promotes trafficking of hepatitis C virus core protein to lipid droplets. EMBO J 21(15): 3980-3988.
21. Bintintan I, Meyers G (2010) A new type of signal peptidase cleavage site identified in an RNA virus polyprotein. J Biol Chem 285(12):8572-8584.
22. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat Methods 8(10):785-786.
23. von Heijne G (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14(11):4683-4690.
24. Evnin LB, Vásquez JR, Craik CS (1990) Substrate specificity of trypsin investigated by using a genetic selection. Proc Natl Acad Sci USA 87(17):6659-6663.
25. Fontana J, López-Montero N, Elliott RM, Fernández JJ, Risco C (2008) The unique architecture of Bunyamwera virus factories around the Golgi complex. Cell Microbiol 10(10):2012-2028.
26. Lappin DF, Nakitare GW, Palfreyman JW, Elliott RM (1994) Localization of Bunyamwera bunyavirus G1 glycoprotein to the Golgi requires association with G2 but not with NSm. J Gen Virol 75(Pt 12):3441-3451.
27. Tilston-Lunel NL, Acrani GO, Randall RE, Elliott RM (2015) Generation of recombinant oropouche viruses lacking the nonstructural protein NSm or NSs. J Virol 90(5):2616-2627.
28. Thomas G (2002) Furin at the cutting edge: From protein traffic to embryogenesis and disease. Nat Rev Mol Cell Biol 3(10):753-766.
29. Seidah NG, Prat A (2012) The biology and therapeutic targeting of the proprotein convertases. Nat Rev Drug Discov 11(5):367-383.
30. Sanchez AJ, Vincent MJ, Erickson BR, Nichol ST (2006) Crimean-congo hemorrhagic fever virus glycoprotein precursor is cleaved by Furin-like and SKI-1 proteases to generate a novel 38-kilodalton glycoprotein. J Virol 80(1):514-525.
31. Bridge AJ, Pebernard S, Ducraux A, Nicoulaz AL, Iggo R (2003) Induction of an interferon response by RNAi vectors in mammalian cells. Nat Genet 34(3):263-264.
32. Whitehead KA, Dahlman JE, Langer RS, Anderson DG (2011) Silencing or stimulation? siRNA delivery and the immune system. Annu Rev Chem Biomol Eng 2(1):77-96.
33. Schrempf S, Froeschke M, Giroglou T, von Laer D, Dobberstein B (2007) Signal peptide requirements for lymphocytic choriomeningitis virus glycoprotein C maturation and virus infectivity. J Virol 81(22):12515-12524.
34. Bederka LH, Bonhomme CJ, Ling EL, Buchmeier MJ (2014) Arenavirus stable signal peptide is the keystone subunit for glycoprotein complex organization. MBio 5(6):e02063.
35. York J, Romanowski V, Lu M, Nunberg JH (2004) The signal peptide of the Junín arenavirus envelope glycoprotein is myristoylated and forms an essential subunit of the mature G1-G2 complex. J Virol 78(19):10783-10792.
36. Killip MJ, et al. (2013) Deep sequencing analysis of defective genomes of parainfluenza virus 5 and their role in interferon induction. J Virol 87(9):4798-4807.
37. Hale BG, et al. (2009) CDK/ERK-mediated phosphorylation of the human influenza A virus NS1 protein at threonine-215. Virology 383(1):6-11.
38. Buchholz UJ, Finke S, Conzelmann KK (1999) Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73(1):251-259.
39. Weber F, Dunn EF, Bridgen A, Elliott RM (2001) The Bunyamwera virus nonstructural protein NSs inhibits viral RNA synthesis in a minireplicon system. Virology 281(1):67-74.
40. Elliott RM, et al. (2013) Establishment of a reverse genetics system for Schmallenberg virus, a newly emerged orthobunyavirus in Europe. J Gen Virol 94(Pt 4):851-859.
41. Brennan B, Li P, Elliott RM (2011) Generation and characterization of a recombinant Rift Valley fever virus expressing a V5 epitope-Tagged RNA-dependent RNA polymerase. J Gen Virol 92(Pt 12):2906-2913.
42. Lowen AC, Noonan C, McLees A, Elliott RM (2004) Efficient bunyavirus rescue from cloned cDNA. Virology 330(2):493-500.
43. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68(5):850-858.
44. Naldini L, Blömer U, Gage FH, Trono D, Verma IM (1996) Efficient transfer, integration, and sustained long-Term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci USA 93(21):11382-11388.
45. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D (1997) Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 15(9):871-875.
46. Sugrue RJ, Brown C, Brown G, Aitken J, McL Rixon HW (2001) Furin cleavage of the respiratory syncytial virus fusion protein is not a requirement for its transport to the surface of virus-infected cells. J Gen Virol 82(Pt 6):1375-1386.