NLRC4 suppresses melanoma tumor progression independently of inflammasome activation

Journal of Clinical Investigation

Volumn 126, Issue 10, 2016, Pages 3917-3928

  Janowski, Ann M ^a,b   Colegio, Oscar R ^c   Hornick, Emma E ^a,b   McNiff, Jennifer M ^c   Martin, Matthew D ^b,d   Badovinac, Vladimir P ^b,d   Norian, Lyse A ^e   Zhang, Weizhou ^b,d   Cassel, Suzanne L ^a,b,d   Sutterwala, Fayyaz S ^a,b,d  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF IOWA   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASC PROTEIN; BINDING PROTEIN; GAMMA INTERFERON; INFLAMMASOME; INTERLEUKIN 1BETA CONVERTING ENZYME; NLRC4 PROTEIN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; CHEMOKINE; IPAF PROTEIN, MOUSE; STAT3 PROTEIN; STAT3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B16F10 CELL LINE; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MACROPHAGE; MELANOMA; MELANOMA CELL LINE; MOUSE; NLRC4 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TUMOR ASSOCIATED LEUKOCYTE; ANIMAL; C57BL MOUSE; CANCER TRANSPLANTATION; DISEASE COURSE; EXPERIMENTAL MELANOMA; IMMUNOLOGY; KNOCKOUT MOUSE; MAPK SIGNALING; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR MICROENVIRONMENT; TUMOR VOLUME;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CALCIUM-BINDING PROTEINS; CASPASE 1; CHEMOKINES; DISEASE PROGRESSION; FEMALE; HUMANS; INFLAMMASOMES; LYMPHOCYTES, TUMOR-INFILTRATING; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MELANOMA, EXPERIMENTAL; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASM TRANSPLANTATION; STAT3 TRANSCRIPTION FACTOR; TUMOR BURDEN; TUMOR MICROENVIRONMENT;

EID: 84991608477     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI86953     Document Type: Article

References (67)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66(1):7-30.
2. Eggermont AM, Spatz A, Robert C. Cutaneous melanoma. Lancet. 2014;383(9919):816-827.
3. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140(6):883-899.
4. Lawrence MS, et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature. 2013;499(7457):214-218.
5. Karachaliou N, et al. Melanoma: oncogenic drivers and the immune system. Ann Transl Med. 2015;3(18):265.
6. Krelin Y, et al. Interleukin-1beta-driven inflammation promotes the development and invasiveness of chemical carcinogen-induced tumors. Cancer Res. 2007;67(3):1062-1071.
7. Saijo Y, et al. Proinflammatory cytokine IL-1 beta promotes tumor growth of Lewis lung carcinoma by induction of angiogenic factors: in vivo analysis of tumor-stromal interaction. J Immunol. 2002;169(1):469-475.
8. Voronov E, et al. IL-1 is required for tumor invasiveness and angiogenesis. Proc Natl Acad Sci U S A. 2003;100(5):2645-2650.
9. Guo H, Callaway JB, Ting JP. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med. 2015;21(7):677-687.
10. Lamkanfi M, Dixit VM. Mechanisms and functions of inflammasomes. Cell. 2014;157(5):1013-1022.
11. Poyet JL, Srinivasula SM, Tnani M, Razmara M, Fernandes-Alnemri T, Alnemri ES. Identification of Ipaf, a human caspase-1-activating protein related to Apaf-1. J Biol Chem. 2001;276(30):28309-28313.
12. Zhao Y, Shao F. The NAIP-NLRC4 inflammasome in innate immune detection of bacterial flagellin and type III secretion apparatus. Immunol Rev. 2015;265(1):85-102.
13. Mariathasan S, et al. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature. 2004;430(6996):213-218.
14. Franchi L, Stoolman J, Kanneganti TD, Verma A, Ramphal R, Nunez G. Critical role for Ipaf in Pseudomonas aeruginosa-induced caspase-1 acti-vation. Eur J Immunol. 2007;37(11):3030-3039.
15. Sutterwala FS, Mijares LA, Li L, Ogura Y, Kazmierczak BI, Flavell RA. Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J Exp Med. 2007;204(13):3235-3245.
16. Cai S, Batra S, Wakamatsu N, Pacher P, Jeyaseelan S. NLRC4 inflammasome-mediated production of IL-1β modulates mucosal immunity in the lung against gram-negative bacterial infection. J Immunol. 2012;188(11):5623-5635.
17. Amer A, et al. Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J Biol Chem. 2006;281(46):35217-35223.
18. Zamboni DS, et al. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat Immunol. 2006;7(3):318-325.
19. Lightfield KL, et al. Differential requirements for NAIP5 in activation of the NLRC4 inflammasome. Infect Immun. 2011;79(4):1606-1614.
20. Miao EA, et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol. 2006;7(6):569-575.
21. Miao EA, et al. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci U S A. 2010;107(7):3076-3080.
22. Zhao Y, et al. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature. 2011;477(7366):596-600.
23. Franchi L, et al. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol. 2006;7(6):576-582.
24. Kofoed EM, Vance RE. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature. 2011;477(7366):592-595.
25. Rayamajhi M, Zak DE, Chavarria-Smith J, Vance RE, Miao EA. Cutting edge: Mouse NAIP1 detects the type III secretion system needle protein. J Immunol. 2013;191(8):3986-3989.
26. Yang J, Zhao Y, Shi J, Shao F. Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. Proc Natl Acad Sci U S A. 2013;110(35):14408-14413.
27. Hu B, et al. Inflammation-induced tumorigenesis in the colon is regulated by caspase-1 and NLRC4. Proc Natl Acad Sci U S A. 2010;107(50):21635-21640.
28. Nordlander S, Pott J, Maloy KJ. NLRC4 expression in intestinal epithelial cells mediates protection against an enteric pathogen. Mucosal Immunol. 2014;7(4):775-785.
29. Gajewski TF, Schreiber H, Fu YX. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol. 2013;14(10):1014-1022.
30. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6(5):392-401.
31. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer. 2004;4(7):540-550.
32. Kakinuma T, Hwang ST. Chemokines, chemokine receptors, and cancer metastasis. J Leukoc Biol. 2006;79(4):639-651.
33. Harlin H, et al. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 2009;69(7):3077-3085.
34. Mullins IM, et al. CXC chemokine receptor 3 expression by activated CD8+ T cells is associated with survival in melanoma patients with stage III disease. Cancer Res. 2004;64(21):7697-7701.
35. Walser TC, Ma X, Kundu N, Dorsey R, Goloubeva O, Fulton AM. Immune-mediated modulation of breast cancer growth and metastasis by the chemokine Mig (CXCL9) in a murine model. J Immunother. 2007;30(5):490-498.
36. Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity. 2014;41(1):49-61.
37. Biswas SK, et al. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood. 2006;107(5):2112-2122.
38. Ostuni R, Natoli G. Transcriptional control of macrophage diversity and specialization. Eur J Immunol. 2011;41(9):2486-2490.
39. Allen IC, et al. NLRP12 suppresses colon inflammation and tumorigenesis through the negative regulation of noncanonical NF-κB signaling. Immunity. 2012;36(5):742-754.
40. Anand PK, et al. NLRP6 negatively regulates innate immunity and host defence against bacterial pathogens. Nature. 2012;488(7411):389-393.
41. Lich JD, et al. Monarch-1 suppresses non-canonical NF-kappaB activation and p52-dependent chemokine expression in monocytes. J Immunol. 2007;178(3):1256-1260.
42. Zaki MH, et al. The NOD-like receptor NLRP12 attenuates colon inflammation and tumorigenesis. Cancer Cell. 2011;20(5):649-660.
43. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009;9(11):798-809.
44. Kaplan DH, et al. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci U S A. 1998;95(13):7556-7561.
45. Man SM, et al. Critical Role for the DNA Sensor AIM2 in Stem Cell Proliferation and Cancer. Cell. 2015;162(1):45-58.
46. Wilson JE, et al. Inflammasome-independent role of AIM2 in suppressing colon tumorigenesis via DNA-PK and Akt. Nat Med. 2015;21(8):906-913.
47. Eyking A, et al. Toll-like receptor 4 variant D299G induces features of neoplastic progression in Caco-2 intestinal cells and is associated with advanced human colon cancer. Gastroenterology. 2011;141(6):2154-2165.
48. Herrmann A, et al. TLR9 is critical for glioma stem cell maintenance and targeting. Cancer Res. 2014;74(18):5218-5228.
49. Tye H, et al. STAT3-driven upregulation of TLR2 promotes gastric tumorigenesis independent of tumor inflammation. Cancer Cell. 2012;22(4):466-478.
50. Junttila MR, et al. p38alpha and p38delta mitogen-activated protein kinase isoforms regulate invasion and growth of head and neck squamous carcinoma cells. Oncogene. 2007;26(36):5267-5279.
51. Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer. 2009;9(8):537-549.
52. Lautz K, et al. NLRP10 enhances Shigella-induced pro-inflammatory responses. Cell Microbiol. 2012;14(10):1568-1583.
53. Wang L, et al. PYPAF7, a novel PYRIN-containing Apaf1-like protein that regulates activation of NF-kappa B and caspase-1-dependent cytokine processing. J Biol Chem. 2002;277(33):29874-29880.
54. Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science. 1996;271(5256):1734-1736.
55. Freeman GJ, et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med. 2000;192(7):1027-1034.
56. Topalian SL, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012;366(26):2443-2454.
57. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252-264.
58. Hodi FS, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711-723.
59. Arthur JC, et al. Cutting edge: NLRP12 controls dendritic and myeloid cell migration to affect contact hypersensitivity. J Immunol. 2010;185(8):4515-4519.
60. Elinav E, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell. 2011;145(5):745-757.
61. Kuida K, et al. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science. 1995;267(5206):2000-2003.
62. Lara-Tejero M, et al. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J Exp Med. 2006;203(6):1407-1412.
63. Sutterwala FS, et al. Critical role for NALP3/ CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity. 2006;24(3):317-327.
64. Sutterwala FS, Noel GJ, Clynes R, Mosser DM. Selective suppression of interleukin-12 induction after macrophage receptor ligation. J Exp Med. 1997;185(11):1977-1985.
65. Joly S, et al. Cutting edge: Nlrp10 is essential for protective antifungal adaptive immunity against Candida albicans. J Immunol. 2012;189(10):4713-4717.
66. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101-1108.
67. Colegio OR, et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature. 2014;513(7519):559-563.