Gut microbiota promotes obesity-associated liver cancer through pge2-mediated suppression of antitumor immunity

Cancer Discovery

Volumn 7, Issue 5, 2017, Pages 522-538

  Loo, Tze Mun ^a   Kamachi, Fumitaka ^a   Watanabe, Yoshihiro ^a   Yoshimoto, Shin ^b,c   Kanda, Hiroaki ^b   Arai, Yuriko ^a,b   Nakajima Takagi, Yaeko ^d   Iwama, Atsushi ^d   Koga, Tomoaki ^e   Sugimoto, Yukihiko ^e   Ozawa, Takayuki ^a   Nakamura, Masaru ^a   Kumagai, Miho ^a   Watashi, Koichi ^f,g   Taketo, Makoto M ^h   Aoki, Tomohiro ^h   Narumiya, Shuh ^h,i   Oshima, Masanobu ^i,j   Arita, Makoto ^g,k,l,m   Hara, Eiji ^b,i,n   Ohtani, Naoko ^a,g,o   more..

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

^b CANCER INSTITUTE   (Japan)

^c LSI MEDIENCE CORPORATION   (Japan)

^d CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e KUMAMOTO UNIVERSITY   (Japan)

^f NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^g JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^h KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

ⁱ JAPAN AGENCY FOR MEDICAL RESEARCH AND DEVELOPMENT   (Japan)

^j KANAZAWA UNIVERSITY   (Japan)

^k RIKEN Center for Integrative Medical Sciences   (Japan)

^l YOKOHAMA CITY UNIVERSITY   (Japan)

^m KEIO UNIVERSITY   (Japan)

ⁿ OSAKA UNIVERSITY   (Japan)

^o OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CYCLOOXYGENASE 2; DEOXYCHOLIC ACID; LIPOTEICHOIC ACID; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN E2; RNA 16S; TOLL LIKE RECEPTOR 2; VANCOMYCIN; LIPOPOLYSACCHARIDE; TEICHOIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL ISOLATION; CELL STIMULATION; CONTROLLED STUDY; DIET INDUCED OBESITY; FLOW CYTOMETRY; GENE OVEREXPRESSION; HEPATIC STELLATE CELL; HISTOLOGY; HUMAN; IMMUNOFLUORESCENCE; INTESTINE FLORA; LIPID DIET; LIPIDOMICS; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; LIVER CANCER; MALE; MICROENVIRONMENT; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; PHENOTYPE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR IMMUNITY; TUMOR VOLUME; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; COMPLICATION; FEMALE; IMMUNOLOGY; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; TUMOR ESCAPE; TUMOR MICROENVIRONMENT;

ANIMALS; CARCINOMA, HEPATOCELLULAR; DINOPROSTONE; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; LIPOPOLYSACCHARIDES; LIVER NEOPLASMS; MALE; MICE, INBRED C57BL; OBESITY; TEICHOIC ACIDS; TUMOR ESCAPE; TUMOR MICROENVIRONMENT;

EID: 85017373900     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-16-0932     Document Type: Article

References (50)

1. Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer 2004;4: 579–91.
2. Deng T, Lyon CJ, Bergin S, Caligiuri MA, Hsueh WA. Obesity, inflammation, and cancer. Annu Rev Pathol 2016;11:421–49.
3. Font-Burgada J, Sun B, Karin M. Obesity and cancer: the oil that feeds the flame. Cell Metab 2016;23:48–62.
4. Yoshimoto S, Loo TM, Atarashi K, Kanda H, Sato S, Oyadomari S, et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 2013;499:97–101.
5. Forner A, Llovet JM, Bruix J. Hepatocellular carcinoma. Lancet 2012; 379:1245–55.
6. Michelotti GA, Machado MV, Diehl AM. NAFLD, NASH and liver cancer. Nat Rev Gastroenterol Hepatol 2013;10:656–65.
7. Rodier F, Campisi J. Four faces of cellular senescence. J Cell Biol 2011;192:547–56.
8. Campisi J, Andersen JK, Kapahi P, Melov S. Cellular senescence: a link between cancer and age-related degenerative disease? Semin Cancer Biol 2011;21:354–9.
9. Collado M, Serrano M. Senescence in tumours: evidence from mice and humans. Nat Rev Cancer 2010;10:51–7.
10. Munoz-Espin D, Canamero M, Maraver A, Gomez-Lopez G, Contreras J, Murillo-Cuesta S, et al. Programmed cell senescence during mammalian embryonic development. Cell 2013;155:1104–18.
11. Storer M, Mas A, Robert-Moreno A, Pecoraro M, Ortells MC, Di Giacomo V, et al. Senescence is a developmental mechanism that contributes to embryonic growth and patterning. Cell 2013;155:1119–30.
12. Kang TW, Yevsa T, Woller N, Hoenicke L, Wuestefeld T, Dauch D, et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 2011;479:547–51.
13. Krizhanovsky V, Yon M, Dickins RA, Hearn S, Simon J, Miething C, et al. Senescence of activated stellate cells limits liver fibrosis. Cell 2008;134:657–67.
14. Tasdemir N, Banito A, Roe JS, Alonso-Curbelo D, Camiolo M, Tschaharganeh DF, et al. BRD4 connects enhancer remodeling to senescence immune surveillance. Cancer Discov 2016;6:612–29.
15. Demaria M, Ohtani N, Youssef SA, Rodier F, Toussaint W, Mitchell JR, et al. An essential role for senescent cells in optimal wound healing through secretion of PDGF-AA. Dev Cell 2014;31:722–33.
16. Jun JI, Lau LF. The matricellular protein CCN1 induces fibroblast senescence and restricts fibrosis in cutaneous wound healing. Nat Cell Biol 2010;12:676–85.
17. Acosta JC, Banito A, Wuestefeld T, Georgilis A, Janich P, Morton JP, et al. A complex secretory program orchestrated by the inflammasome controls paracrine senescence. Nat Cell Biol 2013;15:978–90.
18. Pribluda A, Elyada E, Wiener Z, Hamza H, Goldstein RE, Biton M, et al. A senescence-inflammatory switch from cancer-inhibitory to cancer-promoting mechanism. Cancer Cell 2013;24:242–56.
19. Cichowski K, Hahn WC. Unexpected pieces to the senescence puzzle. Cell 2008;133:958–61.
20. Kang C, Xu Q, Martin TD, Li MZ, Demaria M, Aron L, et al. The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. Science 2015;349:aaa5612.
21. Kaplon J, Zheng L, Meissl K, Chaneton B, Selivanov VA, Mackay G, et al. A key role for mitochondrial gatekeeper pyruvate dehydrogenase in oncogene-induced senescence. Nature 2013;498:109–12.
22. Rai TS, Cole JJ, Nelson DM, Dikovskaya D, Faller WJ, Vizioli MG, et al. HIRA orchestrates a dynamic chromatin landscape in senescence and is required for suppression of neoplasia. Genes Dev 2014;28:2712–25.
23. Takahashi A, Imai Y, Yamakoshi K, Kuninaka S, Ohtani N, Yoshimoto S, et al. DNA damage signaling triggers degradation of histone methyltransferases through APC/C(Cdh1) in senescent cells. Mol Cell 2012;45:123–31.
24. Vigneron A, Vousden KH. p53, ROS and senescence in the control of aging. Aging 2010;2:471–4.
25. Davalos AR, Kawahara M, Malhotra GK, Schaum N, Huang J, Ved U, et al. p53-dependent release of Alarmin HMGB1 is a central mediator of senescent phenotypes. J Cell Biol 2013;201:613–29.
26. Dapito DH, Mencin A, Gwak GY, Pradere JP, Jang MK, Mederacke I, et al. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. Cancer Cell 2012;21:504–16.
27. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 2006;444:1022–3.
28. Fukui H. Gut-liver axis in liver cirrhosis: How to manage leaky gut and endotoxemia. World J Hepatol 2015;7:425–42.
29. Goodman ZD. The impact of obesity on liver histology. Clin Liver Dis 2014;18:33–40.
30. Arita M. Mediator lipidomics in acute inflammation and resolution. J Biochem 2012;152:313–9.
31. Morita M, Kuba K, Ichikawa A, Nakayama M, Katahira J, Iwamoto R, et al. The lipid mediator protectin D1 inhibits influenza virus replication and improves severe influenza. Cell 2013;153:112–25.
32. Schwab JM, Chiang N, Arita M, Serhan CN. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 2007;447:869–74.
33. Castellone MD, Teramoto H, Williams BO, Druey KM, Gutkind JS. Prostaglandin E2 promotes colon cancer cell growth through a Gs-axin-beta-catenin signaling axis. Science 2005;310:1504–10.
34. Oshima H, Matsunaga A, Fujimura T, Tsukamoto T, Taketo MM, Oshima M. Carcinogenesis in mouse stomach by simultaneous activation of the Wnt signaling and prostaglandin E2 pathway. Gastroenterology 2006;131:1086–95.
35. Wang D, Dubois RN. Eicosanoids and cancer. Nat Rev Cancer 2010; 10:181–93.
36. Harris SG, Padilla J, Koumas L, Ray D, Phipps RP. Prostaglandins as modulators of immunity. Trends Immunol 2002;23:144–50.
37. Chen JH, Perry CJ, Tsui YC, Staron MM, Parish IA, Dominguez CX, et al. Prostaglandin E2 and programmed cell death 1 signaling coordinately impair CTL function and survival during chronic viral infection. Nat Med 2015;21:327–34.
38. Soontrapa K, Honda T, Sakata D, Yao C, Hirata T, Hori S, et al. Prostaglandin E2-prostaglandin E receptor subtype 4 (EP4) signaling mediates UV irradiation-induced systemic immunosuppression. Proc Natl Acad Sci U S A 2011;108:6668–73.
39. Fuertes MB, Kacha AK, Kline J, Woo SR, Kranz DM, Murphy KM, et al. Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8+ dendritic cells. J Exp Med 2011;208:2005–16.
40. Zelenay S, van der Veen AG, Bottcher JP, Snelgrove KJ, Rogers N, Acton SE, et al. Cyclooxygenase-dependent tumor growth through evasion of immunity. Cell 2015;162:1257–70.
41. Perumpail RB, Wong RJ, Ahmed A, Harrison SA. Hepatocellular carcinoma in the setting of non-cirrhotic nonalcoholic fatty liver disease and the metabolic syndrome: US Experience. Dig Dis Sci 2015;60:3142–8.
42. Takuma Y, Nouso K. Nonalcoholic steatohepatitis-associated hepatocellular carcinoma: our case series and literature review. World J Gastroenterol 2010;16:1436–41.
43. Forman D, Ferlay J. The global and regional burden of cancer. In: Stewart Bernard W, Wild Christpher L, editors. World Cancer Report 2014. World Health Organization; 2014. p.16–53.
44. Sawey ET, Chanrion M, Cai C, Wu G, Zhang J, Zender L, et al. Identification of a therapeutic strategy targeting amplified FGF19 in liver cancer by Oncogenomic screening. Cancer Cell 2011;19:347–58.
45. Wang L, Fouts DE, Starkel P, Hartmann P, Chen P, Llorente C, et al. Intestinal REG3 lectins protect against alcoholic steatohepatitis by reducing mucosa-associated microbiota and preventing bacterial translocation. Cell Host Microbe 2016;19:227–39.
46. Miura K, Ohnishi H. Role of gut microbiota and Toll-like receptors in nonalcoholic fatty liver disease. World J Gastroenterol 2014; 20:7381–91.
47. Bauer CA, Kim EY, Marangoni F, Carrizosa E, Claudio NM, Mempel TR. Dynamic Treg interactions with intratumoral APCs promote local CTL dysfunction. J Clin Invest 2014;124:2425–40.
48. Joyce JA, Fearon DT. T cell exclusion, immune privilege, and the tumor microenvironment. Science 2015;348:74–80.
49. Okumura Y, Yamagishi T, Nukui S, Nakao K. Discovery of AAT-008, a novel, potent, and selective prostaglandin EP4 receptor antagonist. Bioorg Med Chem Lett 2017;27:1186–92.
50. Kurtova AV, Xiao J, Mo Q, Pazhanisamy S, Krasnow R, Lerner SP, et al. Blocking PGE2-induced tumour repopulation abrogates bladder cancer chemoresistance. Nature 2015;517:209–13.