Small molecule-driven mitophagy-mediated NLRP3 inflammasome inhibition is responsible for the prevention of colitis-associated cancer

Autophagy

Volumn 10, Issue 6, 2014, Pages 972-985

  Guo, Wenjie ^a,b   Sun, Yang ^a   Liu, Wen ^a   Wu, Xingxin ^a   Guo, Lele ^a   Cai, Peifen ^c   Wu, Xuefeng ^a   Wu, Xudong ^a   Shen, Yan ^a   Shu, Yongqian ^c   Gu, Yanhong ^c   Xu, Qiang ^a  

^a NANJING UNIVERSITY   (China)

^b JIANGSU UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Andrographolide; Colitis; Inflammasome; Inflammation associated cancer; Mitophagy

Indexed keywords

ANDROGRAPHOLIDE; AZOXYMETHANE; DEXTRAN SULFATE; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MAMMALIAN TARGET OF RAPAMYCIN; NLR FAMILY PYRIN DOMAIN CONTAINING 3; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; S6 KINASE; SALAZOSULFAPYRIDINE; UNCLASSIFIED DRUG; CARRIER PROTEIN; CIAS1 PROTEIN, MOUSE; DITERPENE; IL1B PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER PREVENTION; CANCER RISK; COLITIS ASSOCIATED COLORECTAL CANCER; COLON CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE COURSE; DOWN REGULATION; EXPERIMENTAL COLITIS; EXPERIMENTAL NEOPLASM; IMMUNOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOPHAGY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SINGLE DRUG DOSE; TUMOR VOLUME; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL LINE; COLITIS; COLORECTAL NEOPLASMS; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; HUMAN; METABOLISM; PATHOLOGY;

ANIMALS; CARRIER PROTEINS; CASPASE 1; CELL LINE; COLITIS; COLORECTAL NEOPLASMS; DISEASE MODELS, ANIMAL; DITERPENES; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICE, INBRED C57BL; MITOCHONDRIAL DEGRADATION;

EID: 84903599695     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.28374     Document Type: Article

References (58)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61:69-90; PMID:21296855; http://dx.doi.org/ 10.3322/caac.20107
2. Weir HK, Thun MJ, Hankey BF, Ries LA, Howe HL, Wingo PA, Jemal A, Ward E, Anderson RN, Edwards BK. Annual report to the nation on the status of cancer, 1975-2000, featuring the uses of surveillance data for cancer prevention and control. J Natl Cancer Inst 2003; 95:1276-99; PMID:12953083; http://dx.doi.org/10.1093/jnci/djg040 (Pubitemid 37160862)
3. Fearon ER. Molecular genetics of colorectal cancer. Annu Rev Pathol 2011; 6:479-507; PMID:21090969; http://dx.doi.org/10.1146/annurev-pathol-011110- 130235
4. Pancione M, Remo A, Colantuoni V. Genetic and epigenetic events generate multiple pathways in colorectal cancer progression. Patholog Res Int 2012; 2012:509348; PMID:22888469; http://dx.doi.org/10.1155/2012/509348
5. Grivennikov SI. Inflammation and colorectal cancer: colitis-associated neoplasia. Semin Immunopathol 2013; 35:229-44; PMID:23161445; http://dx.doi.org/10.1007/s00281-012-0352-6
6. Rogler G. Inflammatory bowel disease cancer risk, detection and surveillance. Dig Dis 2012; 30(Suppl 2):48-54; PMID:23207932; http://dx.doi.org/10.1159/000341893
7. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 2009; 30:1073-81; PMID:19468060; http://dx.doi.org/10.1093/ carcin/bgp127
8. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j. cell.2011.02.013
9. Terzić J, Grivennikov S, Karin E, Karin M. Inflammation and colon cancer. Gastroenterology 2010; 138:2101-14, e5; PMID:20420949; http://dx.doi.org/10.1053/j.gastro.2010.01.058
10. Fantini MC, Pallone F. Cytokines: from gut inflammation to colorectal cancer. Curr Drug Targets 2008; 9:375-80; PMID:18473765; http://dx.doi.org/10. 2174/138945008784221206 (Pubitemid 352025211)
11. Bernstein CN, Blanchard JF, Kliewer E, Wajda A. Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer 2001; 91:854-62; PMID:11241255; http://dx.doi.org/10.1002/1097-0142(20010215)91: 4<854::AIDCNCR1073> 3.0.CO;2-Z (Pubitemid 32173312)
12. Triantafillidis JK, Nasioulas G, Kosmidis PA. Colorectal cancer and inflammatory bowel disease: epidemiology, risk factors, mechanisms of carcinogenesis and prevention strategies. Anticancer Res 2009; 29:2727-37; PMID:19596953
13. Farrell RJ, Peppercorn MA. Ulcerative colitis. Lancet 2002; 359:331-40; PMID:11830216; http://dx.doi.org/10.1016/S0140-6736(02)07499-8 (Pubitemid 34119301)
14. Gross O, Thomas CJ, Guarda G, Tschopp J. The inflammasome: an integrated view. Immunol Rev 2011; 243:136-51; PMID:21884173; http://dx.doi.org/10.1111/j. 1600-065X.2011.01046.x
15. Nunes T, de Souza HS. Inflammasome in intestinal inflammation and cancer. Mediators Inflamm 2013; 2013:654963; PMID:23606794; http://dx.doi.org/10.1155/ 2013/654963
16. Ding WX, Yin XM. Mitophagy: mechanisms, pathophysiological roles, and analysis. Biol Chem 2012; 393:547-64; PMID:22944659; http://dx.doi.org/10.1515/ hsz-2012-0119
17. Lupfer C, Thomas PG, Anand PK, Vogel P, Milasta S, Martinez J, Huang G, Green M, Kundu M, Chi H, et al. Receptor interacting protein kinase 2-mediated mitophagy regulates inflammasome activation during virus infection. Nat Immunol 2013; 14:480-8; PMID:23525089; http://dx.doi.org/10.1038/ni.2563
18. Wiart C, Kumar K, Yusof MY, Hamimah H, Fauzi ZM, Sulaiman M. Antiviral properties of entlabdene diterpenes of Andrographis paniculata nees, inhibitors of herpes simplex virus type 1. Phytother Res 2005; 19:1069-70; PMID:16372376; http://dx.doi.org/10.1002/ptr.1765 (Pubitemid 43133467)
19. Abu-Ghefreh AA, Canatan H, Ezeamuzie CI. In vitro and in vivo anti-inflammatory effects of andrographolide. Int Immunopharmacol 2009; 9:313-8; PMID:19110075; http://dx.doi.org/10.1016/j.intimp.2008.12.002
20. Chan SJ, Wong WS, Wong PT, Bian JS. Neuroprotective effects of andrographolide in a rat model of permanent cerebral ischaemia. Br J Pharmacol 2010; 161:668-79; PMID:20880404; http://dx.doi.org/10.1111/j.1476-5381.2010. 00906.x
21. Rajagopal S, Kumar RA, Deevi DS, Satyanarayana C, Rajagopalan R. Andrographolide, a potential cancer therapeutic agent isolated from Andrographis paniculata. J Exp Ther Oncol 2003; 3:147-58; PMID:14641821; http://dx.doi.org/10.1046/j.1359-4117.2003.01090.x (Pubitemid 37153001)
22. Ricciotti E, Fitz Gerald GA. Prostaglandins and inflammation. Arterioscler Thromb Vasc Biol 2011; 31:986-1000; PMID:21508345; http://dx.doi.org/10.1161/ATVBAHA.110.207449
23. Jobin C, Sartor RB. NF-kappaB signaling proteins as therapeutic targets for inflammatory bowel diseases. Inflamm Bowel Dis 2000; 6:206-13; PMID:10961593; http://dx.doi.org/10.1097/00054725-200008000-00007
24. Shimada K, Crother TR, Karlin J, Dagvadorj J, Chiba N, Chen S, Ramanujan VK, Wolf AJ, Vergnes L, Ojcius DM, et al. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 2012; 36:401-14; PMID:22342844; http://dx.doi.org/10.1016/j.immuni.2012.01.009
25. Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011; 469:221-5; PMID:21124315; http://dx.doi.org/10.1038/nature09663
26. Nathan C, Ding A. Nonresolving inflammation. Cell 2010; 140:871-82; PMID:20303877; http://dx.doi.org/10.1016/j.cell.2010.02.029
27. Ligumsky M, Simon PL, Karmeli F, Rachmilewitz D. Role of interleukin 1 in inflammatory bowel disease-enhanced production during active disease. Gut 1990; 31:686-9; PMID:2379873; http://dx.doi.org/10.1136/gut.31.6.686
28. Gionchetti P, Campieri M, Belluzzi A, Boni P, Brignola C, Ferretti H, Iannone P, Miglioli M, Barbara L. Interleukin 1 in ulcerative colitis. Gut 1991; 32:338; PMID:2013435; http://dx.doi.org/10.1136/gut.32.3.338-a
29. Reinecker HC, Steffen M, Witthoeft T, Pflueger I, Schreiber S, MacDermott RP, Raedler A. Enhanced secretion of tumour necrosis factor-alpha, IL-6, and IL-1 beta by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn's disease. Clin Exp Immunol 1993; 94:174-81; PMID:8403503; http://dx.doi.org/10.1111/j.1365-2249.1993.tb05997.x (Pubitemid 23308385)
30. McAlindon ME, Hawkey CJ, Mahida YR. Expression of interleukin 1 β and interleukin 1 β converting enzyme by intestinal macrophages in health and inflammatory bowel disease. Gut 1998; 42:214-9; PMID:9536946; http://dx.doi.org/10.1136/gut.42.2.214 (Pubitemid 28212176)
31. Coccia M, Harrison OJ, Schiering C, Asquith MJ, Becher B, Powrie F, Maloy KJ. IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4(+) Th17 cells. J Exp Med 2012; 209:1595-609; PMID:22891275; http://dx.doi.org/10.1084/jem. 20111453
32. Dinarello CA. Biologic basis for interleukin-1 in disease. Blood 1996; 87:2095-147; PMID:8630372 (Pubitemid 26086851)
33. Ben-Sasson SZ, Hu-Li J, Quiel J, Cauchetaux S, Ratner M, Shapira I, Dinarello CA, Paul WE. IL-1 acts directly on CD4 T cells to enhance their antigendriven expansion and differentiation. Proc Natl Acad Sci U S A 2009; 106:7119-24; PMID:19359475; http://dx.doi.org/10.1073/pnas.0902745106
34. Sutton C, Brereton C, Keogh B, Mills KH, Lavelle EC. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J Exp Med 2006; 203:1685-91; PMID:16818675; http://dx.doi.org/10.1084/jem.20060285 (Pubitemid 44036274)
35. Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002; 10:417-26; PMID:12191486; http://dx.doi.org/10.1016/S1097-2765(02) 00599-3 (Pubitemid 35007355)
36. Zaki MH, Boyd KL, Vogel P, Kastan MB, Lamkanfi M, Kanneganti TD. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 2010; 32:379-91; PMID:20303296; http://dx.doi.org/10.1016/j.immuni.2010.03.003
37. Allen IC, TeKippe EM, Woodford RM, Uronis JM, Holl EK, Rogers AB, Herfarth HH, Jobin C, Ting JP. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitisassociated cancer. J Exp Med 2010; 207:1045-56; PMID:20385749; http://dx.doi.org/10.1084/jem.20100050
38. Bauer C, Duewell P, Mayer C, Lehr HA, Fitzgerald KA, Dauer M, Tschopp J, Endres S, Latz E, Schnurr M. Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut 2010; 59:1192-9; PMID:20442201; http://dx.doi.org/10.1136/gut.2009.197822
39. Arai Y, Takanashi H, Kitagawa H, Okayasu I. Involvement of interleukin-1 in the development of ulcerative colitis induced by dextran sulfate sodium in mice. Cytokine 1998; 10:890-6; PMID:9878126; http://dx.doi.org/10.1006/cyto. 1998.0355 (Pubitemid 29002742)
40. Siegmund B, Lehr H-A, Fantuzzi G, Dinarello CA. IL-1 β -converting enzyme (caspase-1) in intestinal inflammation. Proc Natl Acad Sci U S A 2001; 98:13249-54; PMID:11606779; http://dx.doi.org/10.1073/pnas.231473998 (Pubitemid 33051348)
41. Bauer C, Duewell P, Lehr HA, Endres S, Schnurr M. Protective and aggravating effects of Nlrp3 inflammasome activation in IBD models: influence of genetic and environmental factors. Dig Dis 2012; 30(Suppl 1):82-90; PMID:23075874; http://dx.doi.org/10.1159/000341681
42. Siegmund B, Fantuzzi G, Rieder F, Gamboni-Robertson F, Lehr HA, Hartmann G, Dinarello CA, Endres S, Eigler A. Neutralization of interleukin-18 reduces severity in murine colitis and intestinal IFNgamma and TNF-alpha production. Am J Physiol Regul Integr Comp Physiol 2001; 281:R1264-73; PMID:11557635
43. Sivakumar PV, Westrich GM, Kanaly S, Garka K, Born TL, Derry JM, Viney JL. Interleukin 18 is a primary mediator of the inflammation associated with dextran sulphate sodium induced colitis: blocking interleukin 18 attenuates intestinal damage. Gut 2002; 50:812-20; PMID:12010883; http://dx.doi.org/10. 1136/gut.50.6.812 (Pubitemid 34539043)
44. Bauer C, Loher F, Dauer M, Mayer C, Lehr HA, Schönharting M, Hallwachs R, Endres S, Eigler A. The ICE inhibitor pralnacasan prevents DSS-induced colitis in C57BL/6 mice and suppresses IP-10 mRNA but not TNF-alpha mRNA expression. Dig Dis Sci 2007; 52:1642-52; PMID:17393315; http://dx.doi.org/10.1007/s10620-007-9802-8 (Pubitemid 46870573)
45. Loher F, Bauer C, Landauer N, Schmall K, Siegmund B, Lehr HA, Dauer M, Schoenharting M, Endres S, Eigler A. The interleukin-1 beta-converting enzyme inhibitor pralnacasan reduces dextran sulfate sodium-induced murine colitis and T helper 1 T-cell activation. J Pharmacol Exp Ther 2004; 308:583-90; PMID:14610233; http://dx.doi.org/10.1124/jpet.103.057059 (Pubitemid 38134220)
46. Thomas TK, Will PC, Srivastava A, Wilson CL, Harbison M, Little J, Chesonis RS, Pignatello M, Schmolze D, Symington J, et al. Evaluation of an interleukin-1 receptor antagonist in the rat acetic acid-induced colitis model. Agents Actions 1991; 34:187-90; PMID:1838896; http://dx.doi.org/10.1007/ BF01993274
47. Coll RC, O'Neill LA. The cytokine release inhibitory drug CRID3 targets ASC oligomerisation in the NLRP3 and AIM2 inflammasomes. PLoS One 2011; 6:e29539; PMID:22216309; http://dx.doi.org/10.1371/journal.pone.0029539
48. Lee KC, Chang HH, Chung YH, Lee TY. Andrographolide acts as an anti-inflammatory agent in LPS-stimulated RAW264.7 macrophages by inhibiting STAT3-mediated suppression of the NF-κB pathway. J Ethnopharmacol 2011; 135:678-84; PMID:21497192; http://dx.doi.org/10.1016/j. jep.2011.03.068
49. Hsieh CY, Hsu MJ, Hsiao G, Wang YH, Huang CW, Chen SW, Jayakumar T, Chiu PT, Chiu YH, Sheu JR. Andrographolide enhances nuclear factor-kappaB subunit p65 Ser536 dephosphorylation through activation of protein phosphatase 2A in vascular smooth muscle cells. J Biol Chem 2011; 286:5942-55; PMID:21169355; http://dx.doi.org/10.1074/jbc. M110.123968
50. Martinon F. Dangerous liaisons: mitochondrial DNA meets the NLRP3 inflammasome. Immunity 2012; 36:313-5; PMID:22444626; http://dx.doi.org/10.1016/ j.immuni.2012.03.005
51. Kepp O, Galluzzi L, Kroemer G. Mitochondrial control of the NLRP3 inflammasome. Nat Immunol 2011; 12:199-200; PMID:21321591; http://dx.doi.org/10. 1038/ni0311-199
52. Schroder K, Tschopp J. The inflammasomes. Cell 2010; 140:821-32; PMID:20303873; http://dx.doi.org/10.1016/j.cell.2010.01.040
53. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011; 12:222-30; PMID:21151103; http://dx.doi.org/10.1038/ni.1980
54. Chen W, Feng L, Nie H, Zheng X. Andrographolide induces autophagic cell death in human liver cancer cells through cyclophilin D-mediated mitochondrial permeability transition pore. Carcinogenesis 2012; 33:2190-8; PMID:22869602; http://dx.doi.org/10.1093/carcin/bgs264
55. Zhou J, Hu SE, Tan SH, Cao R, Chen Y, Xia D, Zhu X, Yang XF, Ong CN, Shen HM. Andrographolide sensitizes cisplatin-induced apoptosis via suppression of autophagosome-lysosome fusion in human cancer cells. Autophagy 2012; 8:338-49; PMID:22302005; http://dx.doi.org/10.4161/auto.18721
56. Malik M, Jividen K, Padmakumar VC, Cataisson C, Li L, Lee J, Howard OM, Yuspa SH. Inducible NOS-induced chloride intracellular channel 4 (CLIC4) nuclear translocation regulates macrophage deactivation. Proc Natl Acad Sci U S A 2012; 109:6130-5; PMID:22474389; http://dx.doi.org/10.1073/pnas.1201351109
57. Wirtz S, Neufert C, Weigmann B, Neurath MF. Chemically induced mouse models of intestinal inflammation. Nat Protoc 2007; 2:541-6; PMID:17406617; http://dx.doi.org/10.1038/nprot.2007.41 (Pubitemid 47040018)
58. Guo WJ, Zhang YM, Zhang L, Huang B, Tao FF, Chen W, Guo ZJ, Xu Q, Sun Y. Novel monofunctional platinum (II) complex Mono-Pt induces apoptosisindependent autophagic cell death in human ovarian carcinoma cells, distinct from cisplatin. Autophagy 2013; 9:996-1008; PMID:23580233; http://dx.doi.org/10.4161/auto.24407