Triggering HIV polyprotein processing by light using rapid photodegradation of a tight-binding protease inhibitor

Nature Communications

Volumn 6, Issue , 2015, Pages

  Schimer, Jirí ^a,b   Pávová, Marcela ^a   Anders, Maria ^c   Pachl, Petr ^a   Šácha, Pavel ^a,b   Cígler, Petr ^a   Weber, Jan ^a   Majer, Pavel ^a   Řezáčová, Pavlína ^a   Kräusslich, Hans Georg ^c,d   Müller, Barbara ^c,d   Konvalinka, Jan ^a,b  

^a INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^d Molecular Medicine Partnership Unit   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE INHIBITOR; POLYPROTEIN; AMINOCOUMARIN DERIVATIVE; CARBAMIC ACID DERIVATIVE; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; P55 GAG PRECURSOR PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; PROTEIN BINDING; PROTEIN PRECURSOR; THIAZOL-5-YLMETHYL (5-(2-AMINO-3-METHYLBUTANAMIDO)-3-HYDROXY-1,6-DIPHENYLHEXAN-2-YL)CARBAMATE; VALINE;

ENZYME ACTIVITY; HUMAN IMMUNODEFICIENCY VIRUS; INHIBITOR; MAGNITUDE; MATURATION; PHOTODEGRADATION; PROTEIN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DRUG DESIGN; DRUG INHIBITION; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVITY; IN VITRO STUDY; IRRADIATION; LIGHT; PHOTODEGRADATION; PROTEIN DEGRADATION; PROTEIN PROCESSING; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMISTRY; DRUG EFFECTS; HEK293 CELL LINE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; KINETICS; METABOLISM; MOLECULAR MODEL; PHOTOLYSIS; PHYSIOLOGY; RADIATION RESPONSE; SYNTHESIS; TIME FACTOR; VIRUS REPLICATION;

AMINOCOUMARINS; BINDING SITES; CARBAMATES; HEK293 CELLS; HIV PROTEASE; HIV PROTEASE INHIBITORS; HIV-1; HUMANS; KINETICS; LIGHT; MODELS, MOLECULAR; PHOTOLYSIS; PROTEIN BINDING; PROTEIN PRECURSORS; PROTEOLYSIS; TIME FACTORS; VALINE; VIRUS REPLICATION;

EID: 84924390132     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7461     Document Type: Article

References (37)

1. Krausslich, H. G. et al. Activity of purified biosynthetic proteinase of human immunodeficiency virus on natural substrates and synthetic peptides. Proc. Natl Acad. Sci. USA 86, 807-811 (1989).
2. Pokorna, J., Machala, L., Rezacova, P. & Konvalinka, J. Current and novel inhibitors of HIV protease. Viruses 1, 1209-1239 (2009).
3. Krausslich, H. G. Human immunodeficiency virus proteinase dimer as component of the viral polyprotein prevents particle assembly and viral infectivity. Proc. Natl Acad. Sci. USA 88, 3213-3217 (1991).
4. Wiegers, K. et al. Sequential steps in human immunodeficiency virus particle maturation revealed by alterations of individual Gag polyprotein cleavage sites. J. Virol. 72, 2846-2854 (1998).
5. Debouck, C. et al. Human immunodeficiency virus protease expressed in Escherichia coli exhibits autoprocessing and specific maturation of the gag precursor. Proc. Natl Acad. Sci. USA 84, 8903-8906 (1987).
6. Krausslich, H. G., Nicklin, M. J., Lee, C. K. & Wimmer, E. Polyprotein processing in picornavirus replication. Biochimie 70, 119-130 (1988).
7. Manchester, M., Everitt, L., Loeb, D. D., Hutchison, 3rd C. A. & Swanstrom, R. Identification of temperature-sensitive mutants of the human immunodeficiency virus type 1 protease through saturation mutagenesis. Amino acid side chain requirements for temperature sensitivity. J. Biol. Chem. 269, 7689-7695 (1994).
8. Konvalinka, J. Structural and molecular biology of protease function and inhibition. J. Cell Biochem. 56, 117-177 (1994).
9. Mattei, S. et al. Induced maturation of human immunodeficiency virus. J. Virol. 88, 13722-12731 (2014).
10. Engels, J. & Schlaeger, E. J. Synthesis, structure, and reactivity of adenosine cyclic 30,50-phosphate benzyl triesters. J. Med. Chem. 20, 907-911 (1977).
11. Kaplan, J. H., Forbush, 3rd B. & Hoffman, J. F. Rapid photolytic release of adenosine 5'-triphosphate from a protected analogue: Utilization by the Na:K pump of human red blood cell ghosts. Biochemistry 17, 1929-1935 (1978).
12. Ellis-Davies, G. C. Neurobiology with caged calcium. Chem. Rev. 108, 1603-1613 (2008).
13. Makings, L. R. & Tsien, R. Y. Caged nitric oxide. Stable organic molecules from which nitric oxide can be photoreleased. J. Biol. Chem. 269, 6282-6285 (1994).
14. Cruz, F. G., Koh, J. T. & Link, K. H. Light-activated gene expression. J. Am. Chem. Soc. 122, 8777-8778 (2000).
15. Lin, W., Albanese, C., Pestell, R. G. & Lawrence, D. S. Spatially discrete, light-driven protein expression. Chem. Biol. 9, 1347-1353 (2002).
16. Breitinger, H. G., Wieboldt, R., Ramesh, D., Carpenter, B. K. & Hess, G. P. Synthesis and characterization of photolabile derivatives of serotonin for chemical kinetic investigations of the serotonin 5-HT(3) receptor. Biochemistry 39, 5500-5508 (2000).
17. Callaway, E. M. & Yuste, R. Stimulating neurons with light. Curr. Opin. Neurobiol. 12, 587-592 (2002).
18. Mikat, V. & Heckel, A. Light-dependent RNA interference with nucleobasecaged siRNAs. RNA 13, 2341-2347 (2007).
19. Shah, S., Jain, P. K., Kala, A., Karunakaran, D. & Friedman, S. H. Lightactivated RNA interference using double-stranded siRNA precursors modified using a remarkable regiospecificity of diazo-based photolabile groups. Nucleic Acids Res. 37, 4508-4517 (2009).
20. Nadler, A. et al. The fatty acid composition of diacylglycerols determines local signaling patterns. Angew. Chem. Int. Ed. 52, 6330-6334 (2013).
21. Hiraoka, T. & Hamachi, I. Caged RNase: Photoactivation of the enzyme from perfect off-state by site-specific incorporation of 2-nitrobenzyl moiety. Bioorg. Med. Chem. Lett. 13, 13-15 (2003).
22. Chang, C. Y., Fernandez, T., Panchal, R. & Bayley, H. Caged catalytic subunit of cAMP-dependent protein kinase. J. Am. Chem. Soc. 120, 7661-7662 (1998).
23. Riggsbee, C. W. & Deiters, A. Recent advances in the photochemical control of protein function. Trends Biotechnol. 28, 468-475 (2010).
24. Brieke, C., Rohrbach, F., Gottschalk, A., Mayer, G. & Heckel, A. Lightcontrolled tools. Angew. Chem. Int. Ed. 51, 8446-8476 (2012).
25. Lee, H. M., Larson, D. R. & Lawrence, D. S. Illuminating the chemistry of life: Design, synthesis, and applications of "caged" and related photoresponsive compounds. ACS Chem. Biol. 4, 409-427 (2009).
26. Li, H., Hah, J. M. & Lawrence, D. S. Light-mediated liberation of enzymatic activity: "small molecule" caged protein equivalents. J. Am. Chem. Soc. 130, 10474-10475 (2008).
27. Porter, N. A., Bush, K. A. & Kinter, K. S. Photo-reversible binding of thrombin to avidin by means of a photolabile inhibitor. J. Photochem. Photobiol. B 38, 61-69 (1997).
28. Kempf, D. J. et al. ABT-538 is a potent inhibitor of human immunodeficiency virus protease and has high oral bioavailability in humans. Proc. Natl Acad. Sci. USA 92, 2484-2488 (1995).
29. Sundquist, W. I. & Krausslich, H. G. HIV-1 assembly, budding, and maturation. Cold Spring Harb. Symp. Quant. Biol. 2, a006924 (2012).
30. Muller, B. et al. HIV-1 Gag processing intermediates trans-dominantly interfere with HIV-1 infectivity. J. Biol. Chem. 284, 29692-29703 (2009).
31. Kaplan, A. H. et al. Partial inhibition of the human immunodeficiency virus type 1 protease results in aberrant virus assembly and the formation of noninfectious particles. J. Virol. 67, 4050-4055 (1993).
32. Konnyu, B. et al. Gag-Pol processing during HIV-1 virion maturation: A systems biology approach. PLoS Comput. Biol. 9, e1003103 (2013).
33. Dale, B. M. et al. Cell-to-cell transfer of HIV-1 via virological synapses leads to endosomal virion maturation that activates viral membrane fusion. Cell Host Microbe 10, 551-562 (2011).
34. Saskova, K. G. et al. Enzymatic and structural analysis of the I47A mutation contributing to the reduced susceptibility to HIV protease inhibitor lopinavir. Protein Sci. 17, 1555-1564 (2008).
35. Richards, A. D. et al. Sensitive, soluble chromogenic substrates for HIV-1 proteinase. J. Biol. Chem. 265, 7733-7736 (1990).
36. Adachi, A. et al. Production of acquired immunodeficiency syndromeassociated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59, 284-291 (1986).
37. Lampe, M. et al. Double-labelled HIV-1 particles for study of virus-cell interaction. Virology 360, 92-104 (2007).