The NLRP3 inflammasome functions as a driver of the myelodysplastic syndrome phenotype

Blood

Volumn 128, Issue 25, 2016, Pages 2960-2975

  Basiorka, Ashley A ^a   McGraw, Kathy L ^a   Eksioglu, Erika A ^a   Chen, Xianghong ^a   Johnson, Joseph ^a   Zhang, Ling ^a   Zhang, Qing ^a   Irvine, Brittany A ^a   Cluzeau, Thomas ^b,c,d,e   Sallman, David A ^a   Padron, Eric ^a   Komrokji, Rami ^a   Sokol, Lubomir ^a   Coll, Rebecca C ^f   Robertson, Avril A B ^f   Cooper, Matthew A ^f   Cleveland, John L ^a   O'Neill, Luke A ^g   Wei, Sheng ^a   List, Alan F ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY HOSPITAL OF NICE   (France)

^c UNIVERSITÉ CÔTE D'AZUR   (France)

^d CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

^e French Group of Myelodysplasia   (France)

^f UNIVERSITY OF QUEENSLAND   (Australia)

^g TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ALARMIN; BETA CATENIN; CALGRANULIN B; CATION; CATION CHANNEL; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ION CHANNEL; NLRP3 PROTEIN, HUMAN;

ARTICLE; BONE MARROW; CELL SWELLING; ENZYME ACTIVATION; GENE MUTATION; GENOTYPE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; IN VIVO STUDY; MYELODYSPLASTIC SYNDROME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PYROPTOSIS; SIGNAL TRANSDUCTION; SOMATIC MUTATION; ANIMAL; CELL SIZE; CFU COUNTING; CHANNEL GATING; GENETICS; HUMAN; METABOLISM; MUTATION; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; BETA CATENIN; CALGRANULIN B; CELL SIZE; COLONY-FORMING UNITS ASSAY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; INFLAMMASOMES; ION CHANNEL GATING; ION CHANNELS; MICE, TRANSGENIC; MUTATION; MYELODYSPLASTIC SYNDROMES; NADPH OXIDASE; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; PHENOTYPE; PYROPTOSIS; REACTIVE OXYGEN SPECIES;

EID: 85010214978     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-07-730556     Document Type: Article

References (62)

1. List A, Kurtin S, Roe DJ, et al. Efficacy of lenalidomide in myelodysplastic syndromes. N Engl J Med. 2005;352(6):549-557.
2. Span LF, Rutten E, Gemmink A, Boezeman JB, Raymakers RA, de Witte T. Bone marrow mononuclear cells of MDS patients are characterized by in vitro proliferation and increased apoptosis independently of stromal interactions. Leuk Res. 2007;31(12):1659-1667.
3. Garcia-Manero G. Myelodysplastic syndromes: 2014 update on diagnosis, risk-stratification, and management. Am J Hematol. 2014;89(1):97-108.
4. Bejar R, Levine R, Ebert BL. Unraveling the molecular pathophysiology of myelodysplastic syndromes. J Clin Oncol. 2011;29(5):504-515.
5. Yoshida K, Sanada M, Shiraishi Y, et al. Frequent pathway mutations of splicing machinery in myelodysplasia. Nature. 2011;478(7367):64-69.
6. Raza A, Gezer S, Mundle S, et al. Apoptosis in bone marrow biopsy samples involving stromal and hematopoietic cells in 50 patients with myelodysplastic syndromes. Blood. 1995;86(1):268-276.
7. Parker JE, Mufti GJ, Rasool F, Mijovic A, Devereux S, Pagliuca A. The role of apoptosis, proliferation, and the Bcl-2-related proteins in the myelodysplastic syndromes and acute myeloid leukemia secondary to MDS. Blood. 2000;96(12):3932-3938.
8. Tehranchi R, Fadeel B, Forsblom AM, et al. Granulocyte colony-stimulating factor inhibits spontaneous cytochrome c release and mitochondria-dependent apoptosis of myelodysplastic syndrome hematopoietic progenitors. Blood. 2003;101(3):1080-1086.
9. Takizawa H, Boettcher S, Manz MG. Demand-adapted regulation of early hematopoiesis in infection and inflammation. Blood. 2012;119(13):2991-3002.
10. Mundle SD, Venugopal P, Cartlidge JD, et al. Indication of an involvement of interleukin-1 beta converting enzyme-like protease in intramedullary apoptotic cell death in the bone marrow of patients with myelodysplastic syndromes. Blood. 1996;88(7):2640-2647.
11. Chen X, Eksioglu EA, Zhou J, et al. Induction of myelodysplasia by myeloid-derived suppressor cells. J Clin Invest. 2013;123(11):4595-4611.
12. Vogl T, Tenbrock K, Ludwig S, et al. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med. 2007;13(9):1042-1049.
13. Ehrchen JM, Sunderkötter C, Foell D, Vogl T, Roth J. The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J Leukoc Biol. 2009;86(3):557-566.
14. Maratheftis CI, Andreakos E, Moutsopoulos HM, Voulgarelis M. Toll-like receptor-4 is up-regulated in hematopoietic progenitor cells and contributes to increased apoptosis in myelodysplastic syndromes. Clin Cancer Res. 2007;13(4):1154-1160.
15. Rhyasen GW, Bolanos L, Fang J, et al. Targeting IRAK1 as a therapeutic approach for myelodysplastic syndrome. Cancer Cell. 2013;24(1):90-104.
16. Hofmann WK, de Vos S, Komor M, Hoelzer D, Wachsman W, Koeffler HP. Characterization of gene expression of CD34+ cells from normal and myelodysplastic bone marrow. Blood. 2002;100(10):3553-3560.
17. Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol. 2009;7(2):99-109.
18. Brennan MA, Cookson BT. Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol. 2000;38(1):31-40.
19. Kessel C, Holzinger D, Foell D. Phagocyte-derived S100 proteins in autoinflammation: putative role in pathogenesis and usefulness as biomarkers. Clin Immunol. 2013;147(3):229-241.
20. Cookson BT, Brennan MA. Pro-inflammatory programmed cell death. Trends Microbiol. 2001;9(3):113-114.
21. Fantuzzi G, Dinarello CA. Interleukin-18 and interleukin-1 beta: two cytokine substrates for ICE (caspase-1). J Clin Immunol. 1999;19(1):1-11.
22. Lim SY, Raftery MJ, Goyette J, Hsu K, Geczy CL. Oxidative modifications of S100 proteins: functional regulation by redox. J Leukoc Biol. 2009;86(3):577-587.
23. Simard JC, Cesaro A, Chapeton-Montes J, et al. S100A8 and S100A9 induce cytokine expression and regulate the NLRP3 inflammasome via ROS-dependent activation of NF-κB(1.). PLoS One. 2013;8(8):e72138.
24. Sester DP, Thygesen SJ, Sagulenko V, et al. A novel flow cytometric method to assess inflammasome formation. J Immunol. 2015;194(1):455-462.
25. Franklin BS, Bossaller L, De Nardo D, et al. The adaptor ASC has extracellular and 'prionoid' activities that propagate inflammation. Nat Immunol. 2014;15(8):727-737.
26. Velegraki M, Papakonstanti E, Mavroudi I, et al. Impaired clearance of apoptotic cells leads to HMGB1 release in the bone marrow of patients with myelodysplastic syndromes and induces TLR4-mediated cytokine production. Haematologica. 2013;98(8):1206-1215.
27. Chirico V, Lacquaniti A, Salpietro V, et al. High-mobility group box 1 (HMGB1) in childhood: from bench to bedside. Eur J Pediatr. 2014;173(9):1123-1136.
28. Fink SL, Cookson BT. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol. 2006;8(11):1812-1825.
29. Tzur A, Moore JK, Jorgensen P, Shapiro HM, Kirschner MW. Optimizing optical flow cytometry for cell volume-based sorting and analysis. PLoS One. 2011;6(1):e16053.
30. Ali A, Mundle SD, Ragasa D, et al. Sequential activation of caspase-1 and caspase-3-like proteases during apoptosis in myelodysplastic syndromes. J Hematother Stem Cell Res. 1999;8(4):343-356.
31. Coll RC, Robertson AA, Chae JJ, et al. A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. Nat Med. 2015;21(3):248-255.
32. Rharass T, Lemcke H, Lantow M, Kuznetsov SA, Weiss DG, Panáková D. Ca2+-mediated mitochondrial reactive oxygen species metabolism augments Wnt/b-catenin pathway activation to facilitate cell differentiation. J Biol Chem. 2014;289(40):27937-27951.
33. Kajla S, Mondol AS, Nagasawa A, et al. A crucial role for Nox 1 in redox-dependent regulation of Wnt-β-catenin signaling. FASEB J. 2012;26(5):2049-2059.
34. Xu J, Suzuki M, Niwa Y, et al. Clinical significance of nuclear non-phosphorylated beta-catenin in acute myeloid leukaemia and myelodysplastic syndrome. Br J Haematol. 2008;140(4):394-401.
35. Masala E, Valencia A, Buchi F, et al. Hypermethylation of Wnt antagonist gene promoters and activation of Wnt pathway in myelodysplastic marrow cells. Leuk Res. 2012;36(10):1290-1295.
36. Bello E, Pellagatti A, Shaw J, et al. CSNK1A1 mutations and gene expression analysis in myelodysplastic syndromes with del(5q) [published online ahead of print 8 June 2015]. Br J Haematol.
37. Obeng EA, McConkey ME, Campagna D, et al. Mutant splicing factor 3b subunit 1 (SF3B1) causes dysregulated erythropoiesis and a stem cell disadvantage. Blood. 2014;124(21):828.
38. Abdel-Wahab O, Gao J, Adli M, et al. Deletion of Asxl1 results in myelodysplasia and severe developmental defects in vivo. J Exp Med. 2013;210(12):2641-2659.
39. Moran-Crusio K, Reavie L, Shih A, et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell. 2011;20(1):11-24.
40. Shirai CL, Ley JN, White BS, et al. Mutant U2AF1 expression alters hematopoiesis and Pre-mRNA splicing in vivo. Cancer Cell. 2015;27(5):631-643.
41. Kim E, Ilagan JO, Liang Y, et al. SRSF2 mutations contribute to myelodysplasia by mutant-specific effects on exon recognition. Cancer Cell. 2015;27(5):617-630.
42. Graubert TA, Shen D, Ding L, et al. Recurrent mutations in the U2AF1 splicing factor in myelodysplastic syndromes. Nat Genet. 2011;44(1):53-57.
43. Pellagatti A, Cazzola M, Giagounidis A, et al. Deregulated gene expression pathways in myelodysplastic syndrome hematopoietic stem cells. Leukemia. 2010;24(4):756-764.
44. Liao PC, Chao LK, Chou JC, et al. Lipopolysaccharide/adenosine triphosphate-mediated signal transduction in the regulation of NLRP3 protein expression and caspase-1-mediated interleukin-1β secretion. Inflamm Res. 2013;62(1):89-96.
45. Heid ME, Keyel PA, Kamga C, Shiva S, Watkins SC, Salter RD. Mitochondrial reactive oxygen species induces NLRP3-dependent lysosomal damage and inflammasome activation. J Immunol. 2013;191(10):5230-5238.
46. Bauernfeind F, Bartok E, Rieger A, Franchi L, Núñez G, Hornung V. Cutting edge: reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J Immunol. 2011;187(2):613-617.
47. Doussiere J, Bouzidi F, Vignais PV. The S100A8/A9 protein as a partner for the cytosolic factors of NADPH oxidase activation in neutrophils. Eur J Biochem. 2002;269(13):3246-3255.
48. Kerkhoff C, Nacken W, Benedyk M, Dagher MC, Sopalla C, Doussiere J. The arachidonic acid-binding protein S100A8/A9 promotes NADPH oxidase activation by interaction with p67phox and Rac-2. FASEB J. 2005;19(3):467-469.
49. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87(1):245-313.
50. Coant N, Ben Mkaddem S, Pedruzzi E, et al. NADPH oxidase 1 modulates WNT and NOTCH1 signaling to control the fate of proliferative progenitor cells in the colon. Mol Cell Biol. 2010;30(11):2636-2650.
51. Wu X, Tu X, Joeng KS, Hilton MJ, Williams DA, Long F. Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell. 2008;133(2):340-353.
52. Schneider RK, Schenone M, Ferreira MV, et al. Rps14 haploinsufficiency causes a block in erythroid differentiation mediated by S100A8 and S100A9. Nat Med. 2016;22(3):288-297.
53. Lee SC, Dvinge H, Kim E, et al. Modulation of splicing catalysis for therapeutic targeting of leukemia with mutations in genes encoding spliceosomal proteins. Nat Med. 2016;22(6):672-678.
54. Yang Y, Akada H, Nath D, Hutchison RE, Mohi G. Loss of Ezh2 cooperates with Jak2V617F in the development of myelofibrosis in a mouse model of myeloproliferative neoplasm. Blood. 2016;127(26):3410-3423.
55. Baroja-Mazo A, Martín-Sánchez F, Gomez AI, et al. The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response. Nat Immunol. 2014;15(8):738-748.
56. Kashio M, Sokabe T, Shintaku K, et al. Redox signal-mediated sensitization of transient receptor potential melastatin 2 (TRPM2) to temperature affects macrophage functions. Proc Natl Acad Sci USA. 2012;109(17):6745-6750.
57. Zhong Z, Zhai Y, Liang S, et al. TRPM2 links oxidative stress to NLRP3 inflammasome activation. Nat Commun. 2013;4:1611.
58. Yamamoto S, Shimizu S, Kiyonaka S, et al. TRPM2-mediated Ca2+ influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration. Nat Med. 2008;14(7):738-747.
59. Kühn FJ, Heiner I, Lückhoff A. TRPM2: a calcium influx pathway regulated by oxidative stress and the novel second messenger ADP-ribose. Pflugers Arch. 2005;451(1):212-219.
60. Sallmyr A, Fan J, Rassool FV. Genomic instability in myeloid malignancies: increased reactive oxygen species (ROS), DNA double strand breaks (DSBs) and error-prone repair. Cancer Lett. 2008;270(1):1-9.
61. Rassool FV, Gaymes TJ, Omidvar N, et al. Reactive oxygen species, DNA damage, and error-prone repair: a model for genomic instability with progression in myeloid leukemia? Cancer Res. 2007;67(18):8762-8771.
62. Funato Y, Michiue T, Asashima M, Miki H. The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-beta-catenin signalling through dishevelled. Nat Cell Biol. 2006;8(5):501-508.