Mitochondrial DNA sensing by STING signaling participates in inflammation, cancer and beyond

International Journal of Cancer

Volumn 139, Issue 4, 2016, Pages 736-741

  Liu, Song ^a   Feng, Min ^a   Guan, Wenxian ^a  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

Author keywords

cancer; inflammation; mitochondria DNA; STING; transfer

Indexed keywords

MEMBRANE PROTEIN; MITOCHONDRIAL DNA; STIMULATOR OF INTERFERON GENE PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; AUTOPHAGY; BACTERIUM; CANCER GROWTH; CARCINOGENESIS; EXTRACELLULAR TRAP; HUMAN; IMMUNITY; INFECTION; INFLAMMATION; MOLECULAR RECOGNITION; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SOMATIC CELL; TUMOR CELL; VIRUS;

EID: 84976541127     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.30074     Document Type: Review

References (61)

1. O'Neill LA, Golenbock D, Bowie AG. The history of Toll-like receptors - redefining innate immunity. Nat Rev Immunol 2013; 13:453–60.
2. Chen GY, Nunez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol 2010; 10:826–37.
3. West AP, Shadel GS, Ghosh S. Mitochondria in innate immune responses. Nat Rev Immunol 2011; 11:389–402.
4. Hemmi H, Takeuchi O, Kawai T, et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000; 408:740–5.
5. Bauer S, Kirschning CJ, Hacker H, et al. Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc Natl Acad Sci USA 2001; 98:9237–42.
6. Shin MS, Kang Y, Lee N, et al. Self double-stranded (ds)DNA induces IL-1beta production from human monocytes by activating NLRP3 inflammasome in the presence of anti-dsDNA antibodies. J Immunol 2013; 190:1407–15.
7. Shimada K, Crother TR, Karlin J, et al. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 2012; 36:401–14.
8. Fernandes-Alnemri T, Yu JW, Datta P, et al. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 2009; 458:509–13.
9. Hornung V, Ablasser A, Charrel-Dennis M, et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 2009; 458:514–18.
10. Roberts TL, Idris A, Dunn JA, et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 2009; 323:1057–60.
11. Karki R, Man SM, Malireddi RK, et al. Concerted activation of the AIM2 and NLRP3 inflammasomes orchestrates host protection against Aspergillus infection. Cell Host Microbe 2015; 17:357–68.
12. Man SM, Zhu Q, Zhu L, et al. Critical role for the DNA sensor AIM2 in stem cell proliferation and cancer. Cell 2015; 162:45–58.
13. Wilson JE, Petrucelli AS, Chen L, et al. Inflammasome-independent role of AIM2 in suppressing colon tumorigenesis via DNA-PK and Akt. Nat Med 2015; 21:906–13.
14. Liu S, Zhang Y, Ren J, et al. Microbial DNA recognition by cGAS-STING and other sensors in dendritic cells in inflammatory bowel diseases. Inflamm Bowel Dis 2015; 21:901–11.
15. Sun L, Wu J, Du F, et al. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013; 339:786–91.
16. Wu J, Sun L, Chen X, et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 2013; 339:826–30.
17. Li XD, Wu J, Gao D, et al. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 2013; 341:1390–4.
18. Gao D, Wu J, Wu YT, et al. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 2013; 341:903–6.
19. Barber GN. STING-dependent cytosolic DNA sensing pathways. Trends Immunol 2014; 35:88–93.
20. Rongvaux A, Jackson R, Harman CC, et al. Apoptotic caspases prevent the induction of type I interferons by mitochondrial DNA. Cell 2014; 159:1563–77.
21. White MJ, McArthur K, Metcalf D, et al. Apoptotic caspases suppress mtDNA-induced STING-mediated type I IFN production. Cell 2014; 159:1549–62.
22. West AP, Khoury-Hanold W, Staron M, et al. Mitochondrial DNA stress primes the antiviral innate immune response. Nature 2015; 520:553–7.
23. Yousefi S, Gold JA, Andina N, et al. Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med 2008; 14:949–53.
24. Meller S, Di Domizio J, Voo KS, et al. TH17 cells promote microbial killing and innate immune sensing of DNA via interleukin 26. Nat Immunol 2015; 16:970–9.
25. Lee JS, Cua DJ. IL-26 AMPs up the TH17 arsenal. Nat Immunol 2015; 16:897–8.
26. Lande R, Gregorio J, Facchinetti V, et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007; 449:564–9.
27. Collins LV, Hajizadeh S, Holme E, et al. Endogenously oxidized mitochondrial DNA induces in vivo and in vitro inflammatory responses. J Leukoc Biol 2004; 75:995–1000.
28. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303:1532–5.
29. Yousefi S, Mihalache C, Kozlowski E, et al. Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ 2009; 16:1438–44.
30. McIlroy DJ, Jarnicki AG, Au GG, et al. Mitochondrial DNA neutrophil extracellular traps are formed after trauma and subsequent surgery. J Crit Care 2014; 29:1133e1–5.
31. Zhang Q, Raoof M, Chen Y, et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 2010; 464:104–7.
32. Itagaki K, Kaczmarek E, Lee YT, et al. Mitochondrial DNA released by trauma induces neutrophil extracellular traps. PLoS One 2015; 10:e0120549.
33. Marino G, Niso-Santano M, Baehrecke EH, et al. Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol 2014; 15:81–94.
34. Minton K. Cell death. Silencing the immune response of apoptotic cells. Nat Rev Immunol 2015; 15:68–9.
35. Petrasek J, Iracheta-Vellve A, Csak T, et al. STING-IRF3 pathway links endoplasmic reticulum stress with hepatocyte apoptosis in early alcoholic liver disease. Proc Natl Acad Sci USA 2013; 110:16544–9.
36. Liu Y, Jesus AA, Marrero B, et al. Activated STING in a vascular and pulmonary syndrome. N Engl J Med 2014; 371:507–18.
37. Onuora S. Autoinflammation: a new STING-associated monogenic autoinflammatory disease. Nat Rev Rheumatol 2014; 10:512
38. Liang Q, Seo GJ, Choi YJ, et al. Autophagy side of MB21D1/cGAS DNA sensor. Autophagy 2014; 10:1146–7.
39. Watson RO, Manzanillo PS, Cox JS. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 2012; 150:803–15.
40. Watson RO, Bell SL, MacDuff DA, et al. The cytosolic sensor cGAS detects Mycobacterium tuberculosis DNA to induce type I interferons and activate autophagy. Cell Host Microbe 2015; 17:811–19.
41. Wassermann R, Gulen MF, Sala C, et al. Mycobacterium tuberculosis differentially activates cGAS- and inflammasome-dependent intracellular immune responses through ESX-1. Cell Host Microbe 2015; 17:799–810.
42. Collins AC, Cai H, Li T, et al. Cyclic GMP-AMP synthase is an innate immune DNA sensor for Mycobacterium tuberculosis. Cell Host Microbe 2015; 17:820–8.
43. Liang Q, Seo GJ, Choi YJ, et al. Crosstalk between the cGAS DNA sensor and Beclin-1 autophagy protein shapes innate antimicrobial immune responses. Cell Host Microbe 2014; 15:228–38.
44. Rustom A, Saffrich R, Markovic I, et al. Nanotubular highways for intercellular organelle transport. Science 2004; 303:1007–10.
45. Acquistapace A, Bru T, Lesault PF, et al. Human mesenchymal stem cells reprogram adult cardiomyocytes toward a progenitor-like state through partial cell fusion and mitochondria transfer. Stem Cells 2011; 29:812–24.
46. Vallabhaneni KC, Haller H, Dumler I. Vascular smooth muscle cells initiate proliferation of mesenchymal stem cells by mitochondrial transfer via tunneling nanotubes. Stem Cells Dev 2012; 21:3104–13.
47. Spees JL, Olson SD, Whitney MJ, Prockop DJ. Mitochondrial transfer between cells can rescue aerobic respiration. Proc Natl Acad Sci USA America 2006; 103:1283–8.
48. Wang X, Gerdes HH. Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells. Cell Death Differ 2015; 22:1181–91.
49. Rebbeck CA, Leroi AM, Burt A. Mitochondrial capture by a transmissible cancer. Science 2011; 331:303.
50. Villanueva T. Metabolism: the mitochondria that wag the dog. Nat Rev Cancer 2011; 11:155.
51. Tan AS, Baty JW, Dong LF, et al. Mitochondrial genome acquisition restores respiratory function and tumorigenic potential of cancer cells without mitochondrial DNA. Cell Metab 2015; 21:81–94.
52. Berridge MV, Dong L, Neuzil J. Mitochondrial DNA in tumor initiation, progression, and metastasis: role of horizontal mtDNA transfer. Cancer Res 2015; 75:3203–8.
53. Pasquier J, Guerrouahen BS, Al Thawadi H, et al. Preferential transfer of mitochondria from endothelial to cancer cells through tunneling nanotubes modulates chemoresistance. J Transl Med 2013; 11:94.
54. Zhang Q, Itagaki K, Hauser CJ. Mitochondrial DNA is released by shock and activates neutrophils via p38 map kinase. Shock 2010; 34:55–9.
55. Timmermans K, Kox M, Gerretsen J, et al. The involvement of danger-associated molecular patterns in the development of immunoparalysis in cardiac arrest patients. Crit Care Med 2015; 43:2332–8.
56. Liu X, Pu Y, Cron K, et al. CD47 blockade triggers T cell-mediated destruction of immunogenic tumors. Nat Med 2015; 21:1209–15.
57. Ishikawa K, Takenaga K, Akimoto M, et al. ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 2008; 320:661–4.
58. Sabharwal SS, Schumacker PT. Mitochondrial ROS in cancer: initiators, amplifiers or an Achilles' heel? Nat Rev Cancer 2014; 14:709–21.
59. Wallace DC. Mitochondria and cancer. Nat Rev Cancer 2012; 12:685–98.
60. Caicedo A, Fritz V, Brondello JM, et al. MitoCeption as a new tool to assess the effects of mesenchymal stem/stromal cell mitochondria on cancer cell metabolism and function. Sci Rep 2015; 5:9073.
61. Gao D, Li T, Li XD, et al. Activation of cyclic GMP-AMP synthase by self-DNA causes autoimmune diseases. Proc Natl Acad Sci USA 2015; 112:E5699–705.