Granzyme M targets host cell hnRNP K that is essential for human cytomegalovirus replication

Cell Death and Differentiation

Volumn 20, Issue 3, 2013, Pages 419-429

  Van Domselaar, R ^a   De Poot, S A H ^a   Remmerswaal, E B M ^b   Lai, K W ^a   Ten Berge, I J M ^b   Bovenschen, N ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

cytomegalovirus; cytotoxic lymphocyte; granzyme M; hnRNP K; transplantation

Indexed keywords

GRANZYME; GRANZYME M; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN K; UNCLASSIFIED DRUG; VIRUS IMMEDIATE EARLY 2; VIRUS PROTEIN;

ARTICLE; CD8+ T LYMPHOCYTE; CELL VIABILITY; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; HOST CELL; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRUS REPLICATION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; GRANZYMES; HEK293 CELLS; HELA CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN K; HUMANS; IMMEDIATE-EARLY PROTEINS; JURKAT CELLS; MICE; MUTAGENESIS; RNA; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; T-LYMPHOCYTES, CYTOTOXIC; TRANS-ACTIVATORS; VIRUS REPLICATION;

CYTOMEGALOVIRUS; HUMAN HERPESVIRUS 5; MURINAE; MUS;

EID: 84873703591     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2012.132     Document Type: Article

References (42)

1. Mocarski ES, Shenk T, Pass RF. Cytomegaloviruses. In: Knipe PM, Howley DE, Griffin DE, Lamb RA, Martin MA, Roizman B et al. (eds) Fields Virology. 5th edn., Vol. 2 Lippincott Williams & Wilkins: Philadelphia, PA, 2007, pp 2701-2772.
2. Crough T, Khanna R. Immunobiology of human cytomegalovirus: from bench to bedside. Clin Microbiol Rev 2009; 22: 76-98.
3. Moss P, Rickinson A. Cellular immunotherapy for viral infection after HSC transplantation. Nat Rev Immunol 2005; 5: 9-20.
4. Wathen MW, Stinski MF. Temporal patterns of human cytomegalovirus transcription: mapping the viral RNAs synthesized at immediate early, early, and late times after infection. J Virol 1982; 41: 462-477.
5. Gamadia LE, Remmerswaal EB, Weel JF, Bemelman F, van Lier RA, Ten Berge IJ. Primary immune responses to human CMV: a critical role for IFN-gamma-producing CD4 T cells in protection against CMV disease. Blood 2003; 101: 2686-2692.
6. van Leeuwen EM, de Bree GJ, ten Berge IJ, van Lier RA. Human virus-specific CD8 T cells: diversity specialists. Immunol Rev 2006; 211: 225-235.
7. Barry M, Bleackley RC. Cytotoxic T lymphocytes: all roads lead to death. Nat Rev Immunol 2002; 2: 401-409.
8. Chowdhury D, Lieberman J. Death by a thousand cuts: granzyme pathways of programmed cell death. Annu Rev Immunol 2008; 26: 389-420.
9. Bovenschen N, Kummer JA. Orphan granzymes find a home. Immunol Rev 2010; 235: 117-127.
10. Trapani JA, Smyth MJ. Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol 2002; 2: 735-747.
11. Mahrus S, Craik CS. Selective chemical functional probes of granzymes A and B reveal granzyme B is a major effector of natural killer cell-mediated lysis of target cells. Chem Biol 2005; 12: 567-577.
12. van Domselaar R, Bovenschen N. Cell death-independent functions of granzymes: hit viruses where it hurts. Rev Med Virol 2011; 21: 301-314.
13. Knickelbein JE, Khanna KM, Yee MB, Baty CJ, Kinchington PR, Hendricks RL. Noncytotoxic lytic granule-mediated CD8 T cell inhibition of HSV-1 reactivation from neuronal latency. Science 2008; 322: 268-271.
14. Romero V, Fellows E, Jenne DE, Andrade F. Cleavage of La protein by granzyme H induces cytoplasmic translocation and interferes with La-mediated HCV-IRES translational activity. Cell Death Differ 2009; 16: 340-348.
15. Zhong C, Li C, Wang X, Toyoda T, Gao G, Fan Z. Granzyme K inhibits replication of influenza virus through cleaving the nuclear transport complex importin alpha1/beta dimer of infected host cells. Cell Death Differ 2011; 19: 882-890.
16. Tang H, Li C, Wang L, Zhang H, Fan Z. Granzyme H of cytotoxic lymphocytes is required for clearance of the hepatitis B virus through cleavage of the hepatitis B virus X protein. J Immunol 2011; 19: 882-890.
17. van Domselaar R, Philippen LE, Quadir R, Wiertz EJ, Kummer JA, Bovenschen N. Noncytotoxic inhibition of cytomegalovirus replication through NK cell protease granzyme M-mediated cleavage of viral phosphoprotein 71. J Immunol 2010; 185: 7605-7613.
18. Pao LI, Sumaria N, Kelly JM, van Dommelen S, Cretney E, Wallace ME et al. Functional analysis of granzyme M and its role in immunity to infection. J Immunol 2005; 175: 3235-3243.
19. Bresnahan WA, Shenk TE. UL82 virion protein activates expression of immediate early viral genes in human cytomegalovirus-infected cells. Proc Natl Acad Sci USA 2000; 97: 14506-14511.
20. van Leeuwen EM, ten Berge IJ, van Lier RA. Induction and maintenance of CD8 T cells specific for persistent viruses. Adv Exp Med Biol 2007; 590: 121-137.
21. de Poot SA, Westgeest M, Hostetter DR, Van Damme P, Plasman K, Demeyer K et al. Human and mouse granzyme M display divergent and species-specific substrate specificities. Biochem J 2011; 437: 431-442.
22. Schmidt T, Striebinger H, Haas J, Bailer SM. The heterogeneous nuclear ribonucleoprotein K is important for Herpes simplex virus-1 propagation. FEBS Lett 2010; 584: 4361-4365.
23. Ng LF, Chan M, Chan SH, Cheng PC, Leung EH, Chen WN et al. Host heterogeneous ribonucleoprotein K (hnRNP K) as a potential target to suppress hepatitis B virus replication. PLoS Med 2005; 2: e163.
24. Bomsztyk K, Denisenko O, Ostrowski J. hnRNP K: one protein multiple processes. BioEssays 2004; 26: 629-638.
25. Paziewska A, Wyrwicz LS, Bujnicki JM, Bomsztyk K, Ostrowski J. Cooperative binding of the hnRNP K three KH domains to mRNA targets. FEBS Lett 2004; 577: 134-140.
26. Heider JA, Bresnahan WA, Shenk TE. Construction of a rationally designed human cytomegalovirus variant encoding a temperature-sensitive immediate-early 2 protein. Proc Natl Acad Sci USA 2002; 99: 3141-3146.
27. White EA, Clark CL, Sanchez V, Spector DH. Small internal deletions in the human cytomegalovirus IE2 gene result in nonviable recombinant viruses with differential defects in viral gene expression. J Virol 2004; 78: 1817-1830.
28. Stenberg RM, Depto AS, Fortney J, Nelson JA. Regulated expression of early and late RNAs and proteins from the human cytomegalovirus immediate-early gene region. J Virol 1989; 63: 2699-2708.
29. White EA, Del Rosario CJ, Sanders RL, Spector DH. The IE2 60-kilodalton and 40- kilodalton proteins are dispensable for human cytomegalovirus replication but are required for efficient delayed early and late gene expression and production of infectious virus. J Virol 2007; 81: 2573-2583.
30. Kaspari M, Tavalai N, Stamminger T, Zimmermann A, Schilf R, Bogner E. Proteasome inhibitor MG132 blocks viral DNA replication and assembly of human cytomegalovirus. FEBS Lett 2008; 582: 666-672.
31. Lin JY, Li ML, Huang PN, Chien KY, Horng JT, Shih SR. Heterogeneous nuclear ribonuclear protein K interacts with the enterovirus 71 50 untranslated region and participates in virus replication. J Gen Virol 2008; 89: 2540-2549.
32. Liu Y, Szaro BG. hnRNP K post-transcriptionally co-regulates multiple cytoskeletal genes needed for axonogenesis. Development 2011; 138: 3079-3090.
33. Laursen LS, Chan CW, Ffrench-Constant C. Translation of myelin basic protein mRNA in oligodendrocytes is regulated by integrin activation and hnRNP-K. J Cell Biol 2011; 192: 797-811.
34. Bovenschen N, de Koning PJ, Quadir R, Broekhuizen R, Damen JM, Froelich CJ et al. NK cell protease granzyme M targets alpha-tubulin and disorganizes the microtubule network. J Immunol 2008; 180: 8184-8191.
35. Bovenschen N, Quadir R, van den Berg AL, Brenkman AB, Vandenberghe I, Devreese B et al. Granzyme K displays highly restricted substrate specificity that only partially overlaps with granzyme A. J Biol Chem 2009; 284: 3504-3512.
36. Bredemeyer AJ, Lewis RM, Malone JP, Davis AE, Gross J, Townsend RR et al. A proteomic approach for the discovery of protease substrates. Proc Natl Acad Sci USA 2004; 101: 11785-11790.
37. Van Damme P, Maurer-Stroh S, Hao H, Colaert N, Timmerman E, Eisenhaber F et al. The substrate specificity profile of human granzyme A. Biol Chem 2010; 391: 983-997.
38. Van Damme P, Staes A, Bronsoms S, Helsens K, Colaert N, Timmerman E et al. Complementary positional proteomics for screening substrates of endo- and exoproteases. Nat Methods 2010; 7: 512-515.
39. Delmas S, Brousset P, Clement D, Le Roy E, Davignon JL. Anti-IE1 CD4 T-cell clones kill peptide-pulsed, but not human cytomegalovirus-infected, target cells. J Gen Virol 2007; 88: 2441-2449.
40. Besold K, Wills M, Plachter B. Immune evasion proteins gpUS2 and gpUS11 of human cytomegalovirus incompletely protect infected cells from CD8 T cell recognition. Virology 2009; 391: 5-19.
41. de Koning PJ, Tesselaar K, Bovenschen N, Colak S, Quadir R, Volman TJ et al. The cytotoxic protease granzyme M is expressed by lymphocytes of both the innate and adaptive immune system. Mol Immunol 2010; 47: 903-911.
42. Shen W, Westgard E, Huang L, Ward MD, Osborn JL, Chau NH et al. Nuclear trafficking of the human cytomegalovirus pp71 (ppUL82) tegument protein. Virology 2008; 376: 42-52.