Mouse granzyme A induces a novel death with writhing morphology that is mechanistically distinct from granzyme B-induced apoptosis

Cell Death and Differentiation

Volumn 20, Issue 9, 2013, Pages 1183-1193

  Susanto, O ^a,b   Stewart, S E ^c   Voskoboinik, I ^a,b   Brasacchio, D ^a,b   Hagn, M ^a,b   Ellis, S ^a   Asquith, S ^a   Sedelies, K A ^a,b   Bird, P I ^c   Waterhouse, N J ^d,e,f   Trapani, J A ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d MATER MEDICAL RESEARCH INSTITUTE   (Australia)

^e UNIVERSITY OF QUEENSLAND   (Australia)

^f QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

cell death; cytoskeleton; cytotoxic lymphocyte; granzyme; natural killer cells

Indexed keywords

CASPASE; GRANZYME A; GRANZYME B; LATRUNCULIN B; LIPOCORTIN 5; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; APOPTOSIS; ARTICLE; ATHETOSIS; CELL DEATH; CELL DISRUPTION; CELL KINETICS; CELL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXIC LYMPHOCYTE; CYTOTOXICITY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MITOCHONDRION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; STAINING; TARGET CELL; TIME-LAPSE VIDEO MICROSCOPY;

MUS;

ACTIN CYTOSKELETON; ANIMALS; APOPTOSIS; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL LINE, TUMOR; GRANZYMES; HELA CELLS; HUMANS; KILLER CELLS, NATURAL; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; OXAZOLES; PERFORIN; THIAZOLIDINES; TIME-LAPSE IMAGING;

EID: 84882271744     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.59     Document Type: Article

References (44)

1. Smyth MJ, Thia KY, Street SEA, MacGregor D, Godfrey DI, Trapani JA. Perforin-mediated cytotoxicity if critical for surveillance of spontaneous lymphoma. J Exp Med 2000; 192: 755-760.
2. Kagi D, Ledermann B, Burki K, Seiler P, Odermatt B, Olsen KJ et al. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 1994; 369: 31-37.
3. Trapani JA, Klein JL, White PC, Dupont B. Molecular cloning of an inducible serine esterase gene from human cytotoxic lymphocytes. Proc Natl Acad Sci USA 1988; 85: 6924-6928.
4. Beresford PJ, Xia Z, Greenberg AH, Lieberman J. Granzyme A loading induces rapid cytolysis and a novel form of dna damage independently of caspase activation. Immunity 1999; 10: 585-594.
5. Martinvalet D, Zhu P, Lieberman JL. Granzyme A induces caspase-independent mitochondrial damage, a required first step for apoptosis. Immunity 2005; 22: 355-370.
6. Martinvalet D, Dykxhoorn DM, Ferrini R, Lieberman J. Granzyme A cleaves a mitochondrial complex I protein to initiate caspase-independent cell death. Cell 2008; 133: 681-692.
7. Beresford PJ, Zhang D, Oh DY, Fan Z, Greer EL, Russo ML et al. Granzyme A activates an endoplasmic reticulum-associated caspase-independent nuclease to induce singlestranded DNA nicks. J Biol Chem 2001; 276: 43285-43293.
8. Metkar SS, Menaa C, Pardo J, Wang B, Wallich R, Freudenberg M et al. Human and Mouse Granzyme A Induce a Proinflammatory Cytokine Response. Immunity 2008; 29: 720-733.
9. Joeckel LT, Wallich R, Martin P, Sanchez-Martinez D, Weber FC, Martin SF et al. Mouse granzyme K has pro-inflammatory potential. Cell Death Differ 2011; 18: 1112-1119.
10. Kaiserman D, Bird CH, Sun J, Matthews A, Ung K, Whisstock JC et al. The major human and mouse granzymes are structurally and functionally divergent. J Cell Biol 2006; 175: 619-630.
11. Shresta S, Russell JH, Ley TJ. Mechanisms responsible for Granzyme B-Independent Cytotoxicity. Blood 1997; 89: 4085-4091.
12. Pardo J, Bosque A, Brehm R, Wallich R, Naval J, Mullbacher A et al. Apoptotic pathways are selectively activated by granzyme A and/or granzyme B in CTL-mediated target cell lysis. J Cell Biol 2004; 167: 457-468.
13. Waterhouse NJ, Sutton VR, Sedelies KA, Ciccone A, Jenkins M, Turner SJ et al. Cytotoxic T lymphocyte-induced killing in the absence of granzymes A and B is unique and distinct from both apoptosis and perforin-dependent lysis. J Cell Biol 2006; 173: 133-144.
14. Yoshikawa Y, Hirayasu H, Tsuzuki S, Fushiki T. Granzyme A causes detachment of alveolar epithelial A549 cells accompanied by promotion of interleukin-8 release. Biosci Biotechnol Biochem 2008; 72: 2481-2484.
15. Simon MM, Kramer MD, Prester M, Gay S. Mouse T-cell associated serine proteinase 1 degrades collagen type IV: a structural basis for the migration of lymphocytes through vascular basement membranes. Immunology 1991; 73: 117-119.
16. Buzza MS, Bird PI. Extracellular granzymes: current perspectives. Biol Chem 2006; 387: 827-837.
17. Lopez JA, Susanto O, Jenkins MR, Lukoyanova N, Sutton VR, Law RH et al. Perforin forms transient pores on the target cell plasma membrane to facilitate rapid access of granzymes during killer cell attack. Blood 2013; 121: 2659-2668.
18. Sutton VR, Wowk ME, Cancilla M, Trapani JA. Caspase activation by granzyme B is indirect, and caspase autoprocessing requires the release of proapoptotic mitochondrial factors. Immunity 2003; 18: 319-329.
19. Sebbagh M, Hamelin J, Bertoglio J, Solary E, Breard J. Direct cleavage of ROCK II by granzyme B induces target cell membrane blebbing in a caspase-independent manner. J Exp Med 2005; 201: 465-471.
20. Degterev A, Hitomi J, Germscheid M, Ch'en IL, Korkina O, Teng X et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 2008; 4: 313-321.
21. Van Damme P, Maurer-Stroh S, Hao H, Colaert N, Timmerman E, Eisenhabler F et al. The substrate specificity profile of human granzyme A. Biol Chem 2010; 391: 983-997.
22. Luders J, Stearns T. Microtubule-organizing centres: a re-evaluation. Nat Rev Mol Cell Biol 2007; 8: 161-167.
23. Bornens M. Is the centriole bound to the nuclear membrane? Nature 1977; 270: 80-82.
24. Anthony DA, Andrews DM, Chow M, Watt SV, House C, Akira S et al. A role for granzyme M in TLR4-driven inflammation and endotoxicosis. J Immunol 2010; 185: 1794-1803.
25. Fan Z, Beresford PJ, Zhang D, Xu Z, Novina CD, Yoshida A et al. Cleaving the oxidative repair protein Ape1 enhances cell death mediated by granzyme A. Nat Immunol 2003; 4: 145-153.
26. Gourlay CW, Carpp LN, Timpson P, Winder SJ, Ayscough KR. A role for the actin cytoskeleton in cell death and aging in yeast. J Cell Biol 2004; 164: 803-809.
27. Wilson CA, Tsuchida MA, Allen GM, Barnhardt EL, Applegate KT, Yam PT et al. Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature 2010; 465: 373-379.
28. Shresta S, MacIvor DM, Heusel JW, Russell JH, Ley TJ. Natural killer and lymphokineactivated killer cells require granzyme B for the rapid induction of apoptosis in susceptible target cells. Proc Natl Acad Sci USA 1995; 92: 5679-5683.
29. Mullbacher A, Waring P, Hla RT, Tran T, Chin S, Stehle T et al. Granzymes are the essential downstream effector molecules for the control of primary virus infections by cytolytic leukocytes. Proc Natl Acad Sci USA 1999; 96: 13950-13955.
30. Sedelies KA, Ciccone A, Clarke CJP, Oliaro J, Sutton VR, Scott FL et al. Blocking granulemediated death by primary human NK cells requires both protection of mitochondria and inhibition of caspase activity. Cell Death Differ 2008; 15: 708-717.
31. Pegram HJ, Haynes NM, Smyth MJ, Kershaw MH, Darcy PK. Characterizing the anti-tumor function of adoptively transferred NK cells in vivo. Cancer Immunol Immunother 2010; 59: 1235-1246.
32. Ebnet K, Hausmann M, Lehmann-Grube F, Mullbacher A, Kopf M, Lamers M et al. Granzyme A-deficient mice retain potent cell-mediated cytotoxicity. EMBO J 1995; 14: 4230-4239.
33. Heusel JW, Wesselschmidt RL, Shresta S, Russell JH, Ley TJ. Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 1994; 76: 977-987.
34. Simon MM, Hausmann M, Tran T, Ebnet K, Tschopp J, ThaHla R et al. In vitro-and ex vivo-derived cytolytic leukocytes from granzyme a x b double knockout mice are defective in granule-mediated apoptosis but not lysis of target cells. J Exp Med 1997; 186: 1781-1786.
35. Kagi D, Ledermann B, Burki K, Hengartner H, Zinkernagel RM. CD8\+ T cell-mediated protection against an intracellular bacterium by perforin-dependent cytotoxicity. Eur J Immunol 1994; 24: 3068-3072.
36. Sun J, Bird CH, Buzza MS, McKee KE, Whisstock JC, Bird PI. Expression and purification of recombinant human granzyme B from Pichia pastoris. Biochem Biophys Res Commun 1999; 261: 251-255.
37. Sun J, Bird CH, Thia KY, Matthews AY, Trapani JA, Bird PI. Granzyme B encoded by the commonly ocurring human RAH allele retains pro-apoptotic activity. J Biol Chem 2004; 279: 16907-16911.
38. Sutton VR, Waterhouse NJ, Baran K, Browne KA, Voskoboinik I, Trapani JA. Measuring cell death mediated by cytotoxic lymphocytes or their granule effector molecules. Methods 2008; 44: 241-249.
39. Bird CH, Sun J, Ung K, Karambalis D, Whisstock JC, Trapani JA et al. Cationic sites on granyzme B contribute to cytotoxicity by promoting its uptake into target cells. Mol Cell Biol 2005; 25: 7854-7867.
40. Voskoboinik I, Thia MC, Fletcher J, Ciccone A, Browne KA, Smyth MJ et al. Calciumdependent plasma membrane binding and cell lysis by perforin are mediated through its C2 domain: a critical role for aspartate residues 429, 435, 483, and 485 but not 491. J Biol Chem 2005; 280: 8426-8434.
41. Voskoboinik I, Thia MC, De Bono A, Browne KA, Cretney E, Jackson JT et al. The functional basis for hemophagocytic lymphohistiocytosis in a patient with co-inherited missense mutations in the perforin (PFN1) gene. J Exp Med 2004; 200: 811-816.
42. Schuh M. An actin-dependent mechanism for long-range vesicle transport. Nat Cell Biol 2011; 13: 1431-1436.
43. Strickland L, von Dassow G, Ellenberg J, Foe V, Lenart P, Burgess D. Light microscopy of echinoderm embryos. Methods Cell Biol 2004; 74: 371-409.
44. Jenkins MR, Tsun A, Stinchcombe JC, Griffiths GM. The strength of T cell receptor signal controls the polarization of cytotoxic machinery to the immunological synapse. Immunity 2009; 31: 621-631.