NK cell intrinsic regulation of MIP-1α by granzyme M

Cell Death and Disease

Volumn 5, Issue 3, 2014, Pages

  Baschuk, N ^a   Wang, N ^b   Watt, S V ^a   Halse, H ^a   House, C ^a   Bird, P I ^c   Strugnell, R ^b   Trapani, J A ^a,b   Smyth, M J ^a,b,d,e   Andrews, D M ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^e UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Granzyme M; Listeria monocytogenes infection; MIP 1 ; NK cells

Indexed keywords

ALANINE AMINOTRANSFERASE; GRANZYME; GRANZYME M; INTERLEUKIN 12; INTERLEUKIN 12P70; INTERLEUKIN 15; INTERLEUKIN 18; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL LOAD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; INFECTION SENSITIVITY; INNATE IMMUNITY; LISTERIOSIS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; REAL TIME POLYMERASE CHAIN REACTION; SPLEEN CELL;

ANIMALS; CELLS, CULTURED; CHEMOKINE CCL3; CHEMOTAXIS, LEUKOCYTE; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; GRANZYMES; HUMANS; IMMUNITY, INNATE; INTERLEUKINS; KILLER CELLS, NATURAL; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; MICE, KNOCKOUT; TIME FACTORS;

EID: 84897390586     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.74     Document Type: Article

References (63)

1. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol 2008; 9: 503-510.
2. Trinchieri G. Biology of natural killer cells. Adv Immunol 1989; 47: 187-376.
3. Trapani JA, Smyth MJ. Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol 2002; 2: 735-747.
4. Andrews DM, Estcourt MJ, Andoniou CE, Wikstrom ME, Khong A, Voigt V et al. Innate immunity defines the capacity of antiviral T cells to limit persistent infection. J Exp Med 2010; 207: 1333-1343.
5. Narni-Mancinelli E, Jaeger BN, Bernat C, Fenis A, Kung S, De Gassart A et al. Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science 2012; 335: 344-348.
6. Newman KC, Riley EM. Whatever turns you on: accessory-cell-dependent activation of NK cells by pathogens. Nat Rev Immunol 2007; 7: 279-291.
7. Rukamp BJ, Kam CM, Natarajan S, Bolton BW, Smyth MJ, Kelly JM et al. Subsite specificities of granzyme M: a study of inhibitors and newly synthesized thiobenzyl ester substrates. Arch Biochem Biophys 2004; 422: 9-22.
8. Smyth MJ, Sayers TJ, Wiltrout T, Powers JC, Trapani JA. Met-ase: cloning and distinct chromosomal location of a serine protease preferentially expressed in human natural killer cells. J Immunol 1993; 151: 6195-6205.
9. Sayers TJ, Lloyd AR, McVicar DW, O'Connor MD, Kelly JM, Carter CR et al. Cloning and expression of a second human natural killer cell granule tryptase, HNK-Tryp-2/granzyme 3. J Leukoc Biol 1996; 59: 763-768.
10. Krenacs L, Smyth MJ, Bagdi E, Krenacs T, Kopper L, Rudiger T et al. The serine protease granzyme M is preferentially expressed in NK-cell, gamma delta T-cell, and intestinal T-cell lymphomas: evidence of origin from lymphocytes involved in innate immunity. Blood 2003; 101: 3590-3593.
11. Sayers TJ, Brooks AD, Ward JM, Hoshino T, Bere WE, Wiegand GW et al. The restricted expression of granzyme M in human lymphocytes. J Immunol 2001; 166: 765-771.
12. deKoning 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.
13. van Domselaar R, de Poot SA, Remmerswaal EB, Lai KW, ten Berge IJ, Bovenschen N. Granzyme M targets host cell hnRNP K that is essential for human cytomegalovirus replication. Cell Death Differ 2013; 20: 419-429.
14. Kelly JM, Waterhouse NJ, Cretney E, Browne KA, Ellis S, Trapani JA et al. Granzyme M mediates a novel form of perforin-dependent cell death. J Biol Chem 2004; 279: 22236-22242.
15. Lieberman J. The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat Rev Immunol 2003; 3: 361-370.
16. Smyth MJ, Street SE, Trapani JA. Cutting edge: granzymes A and B are not essential for perforin-mediated tumor rejection. J Immunol 2003; 171: 515-518.
17. Hu D, Liu S, Shi L, Li C, Wu L, Fan Z. Cleavage of survivin by Granzyme M triggers degradation of the survivin-X-linked inhibitor of apoptosis protein (XIAP) complex to free caspase activity leading to cytolysis of target tumor cells. J Biol Chem 2010; 285: 18326-18335.
18. Wang S, Xia P, Shi L, Fan Z. FADD cleavage by NK cell granzyme M enhances its selfassociation to facilitate procaspase-8 recruitment for auto-processing leading to caspase cascade. Cell Death Differ 2012; 19: 605-615.
19. de Poot SA, Lai KW, van der Wal L, Plasman K, Van Damme P, Porter AC et al. Granzyme M targets topoisomerase II alpha to trigger cell cycle arrest and caspasedependent apoptosis. Cell Death Differ 2013; 21: 416-426.
20. 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.
21. Humann J, Lenz LL. Activation of naive NK cells in response to Listeria monocytogenes requires IL-18 and contact with infected dendritic cells. J Immunol 2010; 184(9): 5172-5178.
22. Wang N, Strugnell R, Wijburg O, Brodnicki T. Measuring bacterial load and immune responses in mice infected with Listeria monocytogenes. J Vis Exp 2011 3076.
23. Maghazachi AA, al-Aoukaty A, Schall TJ. C-C chemokines induce the chemotaxis of NK and IL-2-activated NK cells. Role for G proteins. J Immunol 1994; 153: 4969-4977.
24. Taub DD, Sayers TJ, Carter CR, Ortaldo JR. Alpha and beta chemokines induce NK cell migration and enhance NK-mediated cytolysis. J Immunol 1995; 155: 3877-3888.
25. Loetscher P, Seitz M, Clark-Lewis I, Baggiolini M, Moser B. Activation of NK cells by CC chemokines. Chemotaxis, Ca2+ mobilization, and enzyme release. J Immunol 1996; 156: 322-327.
26. Salazar-Mather TP, Lewis CA, Biron CA. Type I interferons regulate inflammatory cell trafficking and macrophage inflammatory protein 1alpha delivery to the liver. J Clin Invest 2002; 110: 321-330.
27. Salazar-Mather TP, Orange JS, Biron CA. Early murine cytomegalovirus (MCMV) infection induces liver natural killer (NK) cell inflammation and protection through macrophage inflammatory protein 1alpha (MIP-1alpha)-dependent pathways. J Exp Med 1998; 187: 1-14.
28. Maurer M, von Stebut E. Macrophage inflammatory protein-1. Int J Biochem Cell Biol 2004; 36: 1882-1886.
29. Koch AE, Kunkel SL, Harlow LA, Mazarakis DD, Haines GK, Burdick MD et al. Macrophage inflammatory protein-1 alpha. A novel chemotactic cytokine for macrophages in rheumatoid arthritis. J Clin Invest 1994; 93: 921-928.
30. Fauriat C, Long EO, Ljunggren HG, Bryceson YT. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood 2010; 115: 2167-2176.
31. Bluman EM, Bartynski KJ, Avalos BR, Caligiuri MA. Human natural killer cells produce abundant macrophage inflammatory protein-1 alpha in response to monocyte-derived cytokines. J Clin Invest 1996; 97: 2722-2727.
32. 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.
33. Chiossone L, Chaix J, Fuseri N, Roth C, Vivier E, Walzer T. Maturation of mouse NK cells is a 4-stage developmental program. Blood 2009; 113: 5488-5496.
34. Silva A, Andrews DM, Brooks AG, Smyth MJ, Hayakawa Y. Application of CD27 as a marker for distinguishing human NK cell subsets. Int Immunol 2008; 20: 625-630.
35. Fehniger TA, Shah MH, Turner MJ, VanDeusen JB, Whitman SP, Cooper MA et al. Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J Immunol 1999; 162: 4511-4520.
36. Ferlazzo G, Munz C. NK cell compartments and their activation by dendritic cells. J Immunol 2004; 172: 1333-1339.
37. Wagner L, Yang OO, Garcia-Zepeda EA, Ge Y, Kalams SA, Walker BD et al. Betachemokines are released from HIV-1-specific cytolytic T-cell granules complexed to proteoglycans. Nature 1998; 391: 908-911.
38. Menten P, Wuyts A, Van Damme J. Macrophage inflammatory protein-1. Cytokine Growth Factor Rev 2002; 13: 455-481.
39. Proost P, Menten P, Struyf S, Schutyser E, De Meester I, Van Damme J. Cleavage by CD26/dipeptidyl peptidase IV converts the chemokine LD78beta into a most efficient monocyte attractant and CCR1 agonist. Blood 2000; 96: 1674-1680.
40. Anthony DA, Andrews DM, Watt SV, Trapani JA, Smyth MJ. Functional dissection of the granzyme family: cell death and inflammation. Immunol Rev 2010; 235: 73-92.
41. Henkart PA, Berrebi GA, Takayama H, Munger WE, Sitkovsky MV. Biochemical and functional properties of serine esterases in acidic cytoplasmic granules of cytotoxic T lymphocytes. J Immunol 1987; 139: 2398-2405.
42. 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.
43. Salti SM, Hammelev EM, Grewal JL, Reddy ST, Zemple SJ, Grossman WJ et al. Granzyme B regulates antiviral CD8+ T cell responses. J Immunol 2011; 187: 6301-6309.
44. Mullbacher A, Ebnet K, Blanden RV, Hla RT, Stehle T, Museteanu C et al. Granzyme A is critical for recovery of mice from infection with the natural cytopathic viral pathogen, ectromelia. Proc Natl Acad Sci USA 1996; 93: 5783-5787.
45. 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.
46. Cohen J. The immunopathogenesis of sepsis. Nature 2002; 420: 885-891.
47. Harrison C. Sepsis: calming the cytokine storm. Nat Rev Drug Discov 2010; 9: 360-361.
48. Remick DG. Pathophysiology of sepsis. Am J Pathol 2007; 170: 1435-1444.
49. Horowitz A, Stegmann KA, Riley EM. Activation of natural killer cells during microbial infections. Front Immunol 2011; 2: 88.
50. Costantini C, Cassatella MA. The defensive alliance between neutrophils and NK cells as a novel arm of innate immunity. J Leukoc Biol 2011; 89: 221-233.
51. Thoren FB, Riise RE, Ousback J, Della Chiesa M, Alsterholm M, Marcenaro E et al. Human NK Cells induce neutrophil apoptosis via an NKp46- and Fas-dependent mechanism. J Immunol 2012; 188: 1668-1674.
52. Zeng X, Moore TA, Newstead MW, Hernandez-Alcoceba R, Tsai WC, Standiford TJ. Intrapulmonary expression of macrophage inflammatory protein 1alpha (CCL3) induces neutrophil and NK cell accumulation and stimulates innate immunity in murine bacterial pneumonia. Infect Immun 2003; 71: 1306-1315.
53. 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.
54. 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.
55. Lapaque N, Walzer T, Meresse S, Vivier E, Trowsdale J. Interactions between human NK cells and macrophages in response to Salmonella infection. J Immunol 2009; 182: 4339-4348.
56. Walzer T, Dalod M, Robbins SH, Zitvogel L, Vivier E. Natural-killer cells and dendritic cells: "l'union fait la force". Blood 2005; 106: 2252-2258.
57. Andrews DM, Estcourt MJ, Andoniou CE, Wikstrom ME, Khong A, Voigt V et al. Innate immunity defines the capacity of antiviral T cells to limit persistent infection. J Exp Med 2010; 207: 1333-1343.
58. Chaix J, Tessmer MS, Hoebe K, Fuséri N, Ryffel B, Dalod M et al. Cutting edge: priming of NK cells by IL-18. J Immunol 2008; 181: 1627-1631.
59. Fehniger TA, Cai SF, Cao X, Bredemeyer AJ, Presti RM, French AR et al. Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 2007; 26: 798-811.
60. Murphy WJ, Parham P, Miller JS. NK cells-from bench to clinic. Biol Blood Marrow Transplant 2012; 18(1 Suppl): S2-S7.
61. 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.
62. 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.
63. Wessel D, Flugge UI. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 1984; 138: 141-143.