A Novel Two-Tag System for Monitoring Transport and Cleavage through the Classical Secretory Pathway - Adaptation to HIV Envelope Processing

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Stolp, Zachary D ^a   Stotland, Aleksandr ^a   Diaz, Samantha ^a   Hilton, Brett J ^a   Burford, Wesley ^a   Wolkowicz, Roland ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; EPITOPE; FURIN; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; SCAFFOLD PROTEIN; SERINE PROTEINASE; GLYCOPROTEIN GP 160;

ARTICLE; CELL ASSAY; CELL COMPARTMENTALIZATION; CELL SURFACE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EXTRACELLULAR MATRIX; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SECRETORY PATHWAY; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS; TRANS GOLGI NETWORK; VIRUS ENVELOPE; CELL LINE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; PROTEIN DEGRADATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CELL LINE; FLOW CYTOMETRY; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP160; HIV-1; HUMANS; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; PROTEOLYSIS;

EID: 84879249086     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068835     Document Type: Article

References (36)

1. Fisher JM, Scheller RH, (1988) Prohormone processing and the secretory pathway. J Biol Chem 263: 16515-16518. PubMed: 3053690.
2. Checkley MA, Luttge BG, Freed EO, (2011) HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. J Mol Biol 410: 582-608. doi:10.1016/j.jmb.2011.04.042. PubMed: 21762802.
3. Simon SM, Aderem A, (1992) Myristoylation of proteins in the yeast secretory pathway. J Biol Chem 267: 3922-3931. PubMed: 1740440.
4. Rocks O, Gerauer M, Vartak N, Koch S, Huang Z-P, et al. (2010) The Palmitoylation Machinery Is a Spatially Organizing System for Peripheral Membrane Proteins. Cell 141: 458-471. doi:10.1016/j.cell.2010.04.007. PubMed: 20416930.
5. Dalbey RE, Von Heijne G, (1992) Signal peptidases in prokaryotes and eukaryotes--a new protease family. Trends Biochem Sci 17: 474-478. doi:10.1016/0968-0004(92)90492-R. PubMed: 1455520.
6. Seidah NG, Prat A, (2012) The biology and therapeutic targeting of the proprotein convertases. Nat Rev Drug Discov 11: 367-383. doi:10.1038/nrd3699. PubMed: 22679642.
7. Pène V, Hernandez C, Vauloup-Fellous C, Garaud-Aunis J, Rosenberg AR, (2009) Sequential processing of hepatitis C virus core protein by host cell signal peptidase and signal peptide peptidase: a reassessment. J Viral Hepat 16: 705-715. doi:10.1111/j.1365-2893.2009.01118.x. PubMed: 19281487.
8. Seidah NG, (2011) The proprotein convertases, 20 years later. Methods Mol Biol 768: 23-57. doi:10.1007/978-1-61779-204-5_3. PubMed: 21805237.
9. Bennett BD, Denis P, Haniu M, Teplow DB, Kahn S, et al. (2000) A furin-like convertase mediates propeptide cleavage of BACE, the Alzheimer's beta-secretase. J Biol Chem 275: 37712-37717. doi:10.1074/jbc.M005339200. PubMed: 10956649.
10. Davids BJ, Gilbert MA, Liu Q, Reiner DS, Smith AJ, et al. (2011) An Atypical Proprotein Convertase in Giardia lamblia Differentiation. Mol Biochem Parasitol 175: 169-180. doi:10.1016/j.molbiopara.2010.11.008. PubMed: 21075147.
11. Molloy SS, Bresnahan PA, Leppla SH, Klimpel KR, Thomas G, (1992) Human furin is a calcium-dependent serine endoprotease that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J Biol Chem 267: 16396-16402. PubMed: 1644824.
12. Decroly E, Benjannet S, Savaria D, Seidah NG, (1997) Comparative functional role of PC7 and furin in the processing of the HIV envelope glycoprotein gp160. FEBS Lett 405: 68-72. doi:10.1016/S0014-5793(97)00156-7. PubMed: 9094426.
13. Yu I-M, Zhang W, Holdaway HA, Li L, Kostyuchenko VA, et al. (2008) Structure of the Immature Dengue Virus at Low pH Primes Proteolytic Maturation. Science 319: 1834-1837. doi:10.1126/science.1153264. PubMed: 18369148.
14. Stadler K, Allison SL, Schalich J, Heinz FX, (1997) Proteolytic activation of tick-borne encephalitis virus by furin. J Virol 71: 8475-8481. PubMed: 9343204.
15. Tian S, Huajun W, Wu J, (2012) Computational prediction of furin cleavage sites by a hybrid method and understanding mechanism underlying diseases. Sci Rep 2: 261. doi:10.1038/srep00261.
16. Tian S, Huang Q, Fang Y, Wu J, (2011) FurinDB: A Database of 20-Residue Furin Cleavage Site Motifs, Substrates and Their Associated Drugs. Int J Mol Sci 12: 1060-1065. doi:10.3390/ijms12021060. PubMed: 21541042.
17. Thomas G, (2002) Furin at the Cutting Edge: From Protein Traffic to Embryoenesis and Disease. Nat Rev Mol Cell Biol 3: 753-766. doi:10.1038/nrm934. PubMed: 12360192.
18. Didigu CA, Doms RW, (2012) Novel Approaches to Inhibit HIV Entry. Viruses 4: 309-324. doi:10.3390/v4020309. PubMed: 22470838.
19. McCune JM, Rabin LB, Feinberg MB, Lieberman M, Kosek JC, et al. (1988) Endoproteolytic cleavage of gp160 is required for the activation of human immunodeficiency virus. Cell 53: 55-67. doi:10.1016/0092-8674(88)90487-4. PubMed: 2450679.
20. Crooks ET, Tong T, Osawa K, Binley JM, (2011) Enzyme digests eliminate nonfunctional Env from HIV-1 particle surfaces, leaving native Env trimers intact and viral infectivity unaffected. J Virol 85: 5825-5839. doi:10.1128/JVI.00154-11. PubMed: 21471242.
21. Tong T, Crooks ET, Osawa K, Binley JM, (2012) HIV-1 virus-like particles bearing pure env trimers expose neutralizing epitopes but occlude nonneutralizing epitopes. J Virol 86: 3574-3587. doi:10.1128/JVI.06938-11. PubMed: 22301141.
22. Pasquato A, Dettin M, Basak A, Gambaretto R, Tonin L, et al. (2007) Heparin enhances the furin cleavage of HIV-1 gp160 peptides. FEBS Letters 581: 5807-5813. doi:10.1016/j.febslet.2007.11.050.
23. Klasse PJ, (2012) The molecular basis of HIV entry. Cell Microbiol 14: 1183-1192. doi:10.1111/j.1462-5822.2012.01812.x. PubMed: 22583677.
24. Kantanen ML, Leinikki P, Kuismanen E, (1995) Endoproteolytic cleavage of HIV-1 gp160 envelope precursor occurs after exit from the trans-Golgi network (TGN). Arch Virol 140: 1441-1449. doi:10.1007/BF01322670. PubMed: 7661695.
25. Earl PL, Doms RW, Moss B, (1990) Oligomeric structure of the human immunodeficiency virus type 1 envelope glycoprotein. PNAS 87: 648-652. doi:10.1073/pnas.87.2.648. PubMed: 2300552.
26. Molloy SS, Thomas L, VanSlyke JK, Stenberg PE, Thomas G, (1994) Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO J 13: 18-33. PubMed: 7508380.
27. Wang X, Pei D, (2001) Shedding of Membrane Type Matrix Metalloproteinase 5 by a Furin-type Convertase: a Potential Mechanism for Down-regulation. J Biol Chem 276: 35953-35960. doi:10.1074/jbc.M103680200. PubMed: 11470782.
28. Basak A, Chrétien M, Seidah NG, (2002) A rapid fluorometric assay for the proteolytic activity of SKI-1/S1P based on the surface glycoprotein of the hemorrhagic fever Lassa virus. FEBS Lett 514: 333-339. doi:10.1016/S0014-5793(02)02394-3. PubMed: 11943176.
29. Coppola JM, Hamilton CA, Bhojani MS, Larsen MJ, Ross BD, et al. (2007) Identification of inhibitors using a cell-based assay for monitoring Golgi-resident protease activity. Anal Biochem 364: 19-29. doi:10.1016/j.ab.2007.01.013. PubMed: 17316541.
30. Wolkowicz R, Jager GC, Nolan GP, (2005) A random peptide library fused to CCR5 for selection of mimetopes expressed on the mammalian cell surface via retroviral vectors. J Biol Chem 280: 15195-15201. doi:10.1074/jbc.M500254200. PubMed: 15657029.
31. Wolkowicz R, Nolan GP, (2003) Retroviral technology--applications for expressed peptide libraries. Front Biosci 8: d603-d619. doi:10.2741/952. PubMed: 12700115.
32. Hobson JP, Liu S, Rønø B, Leppla SH, Bugge TH, (2006) Imaging specific cell-surface proteolytic activity in single living cells. Nat Methods 3: 259-261. doi:10.1038/nmeth862. PubMed: 16554829.
33. Bosch V, Pawlita M, (1990) Mutational analysis of the human immunodeficiency virus type 1 env gene product proteolytic cleavage site. J Virol 64: 2337-2344. PubMed: 2182911.
34. Hilton BJ, Wolkowicz R, (2010) An assay to monitor HIV-1 protease activity for the identification of novel inhibitors in T-cells. PLOS ONE 5: e10940. doi:10.1371/journal.pone.0010940. PubMed: 20532177.
35. Rajakuberan C, Hilton BJ, Wolkowicz R, (2012) Protocol for a mammalian cell-based assay for monitoring the HIV-1 protease activity. Methods Mol Biol 903: 393-405. doi:10.1007/978-1-61779-937-2_27. PubMed: 22782834.
36. Swift S, Lorens J, Achacoso P, Nolan GP, (2001) Rapid production of retroviruses for efficient gene delivery to mammalian cells using 293T cell-based systems. Curr Protoc Immunol Chapter 10Unit 10.17C. doi:10.1002/0471142735.im1017cs31. PubMed: 18432682.