Kupffer Cell-Derived Tnf Triggers Cholangiocellular Tumorigenesis through JNK due to Chronic Mitochondrial Dysfunction and ROS

Cancer Cell

Volumn 31, Issue 6, 2017, Pages 771-789.e6

  Yuan, Detian ^a,b   Huang, Shan ^b   Berger, Emanuel ^a   Liu, Lei ^a   Gross, Nina ^c   Heinzmann, Florian ^d,e   Ringelhan, Marc ^a,c   Connor, Tracy O ^a,b   Stadler, Mira ^b   Meister, Michael ^b   Weber, Julia ^c   Öllinger, Rupert ^c   Simonavicius, Nicole ^a   Reisinger, Florian ^a   Hartmann, Daniel ^a   Meyer, Rüdiger ^f   Reich, Maria ^g   Seehawer, Marco ^d,e   Leone, Valentina ^a   Höchst, Bastian ^c   Wohlleber, Dirk ^c   Jörs, Simone ^c   Prinz, Marco ^h   Spalding, Duncan ⁱ   Protzer, Ulrike ^a   Luedde, Tom ^j   Terracciano, Luigi ^k   Matter, Matthias ^k   Longerich, Thomas ^l   Knolle, Percy ^c   Ried, Thomas ^f   Keitel, Verena ^g   Geisler, Fabian ^c   Unger, Kristian ^m   Cinnamon, Einat ⁿ   Pikarsky, Eli ^n,o   Hüser, Norbert ^a   Davis, Roger J ^p   Tschaharganeh, Darjus F ^b   Rad, Roland ^c   Weber, Achim ^q   Zender, Lars ^b,d,e   Haller, Dirk ^a   Heikenwalder, Mathias ^a,b   more..

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^g HEINRICH HEINE UNIVERSITY   (Germany)

^h UNIVERSITY OF FREIBURG   (Germany)

ⁱ IMPERIAL COLLEGE LONDON   (United Kingdom)

^j RWTH AACHEN UNIVERSITY   (Germany)

^k UNIVERSITY HOSPITAL BASEL   (Switzerland)

^l UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^m INSTITUTE OF EPIDEMIOLOGY   (Germany)

ⁿ HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^o HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^p UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^q UNIVERSITY HOSPITAL ZURICH   (Switzerland)

more..

Author keywords

cholastasis; intrahepatic cholangiocarcinoma; JNK; Kupffer cell; mitochondrial dysfunction; pro inflammatory niche; reactive oxygen species; Tnf; unfolded protein response

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BUTYLATED HYDROXYANISOLE; CHAPERONIN 60; JANUS KINASE; JANUS KINASE 1; JANUS KINASE 2; JNK 6O; JNK IN 8; K RAS PROTEIN; NOTCH RECEPTOR; PROTEIN C JUN; PROTEIN KINASE B; PROTEIN P53; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG; TUMOR NECROSIS FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT CARCINOMA; CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHOLANGIOCYTE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG TARGETING; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; FETUS; GENE DELETION; HUMAN; HUMAN CELL; HUMAN TISSUE; KUPFFER CELL; LIVER CELL; LIVER INJURY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; BILE DUCT TUMOR; CELL TRANSFORMATION; DRUG EFFECTS; GENETICS; LIVER; METABOLISM; MITOCHONDRION; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

ANIMALS; BILE DUCT NEOPLASMS; BUTYLATED HYDROXYANISOLE; CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CHOLANGIOCARCINOMA; HUMANS; KUPFFER CELLS; LIVER; MAP KINASE SIGNALING SYSTEM; MICE; MITOCHONDRIA; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85020666393     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2017.05.006     Document Type: Article

References (62)

1. Ariizumi, S.I., Yamamoto, M., Intrahepatic cholangiocarcinoma and cholangiolocellular carcinoma in cirrhosis and chronic viral hepatitis. Surg. Today 45 (2014), 682–687.
2. Arnott, C.H., Scott, K.A., Moore, R.J., Robinson, S.C., Thompson, R.G., Balkwill, F.R., Expression of both TNF-alpha receptor subtypes is essential for optimal skin tumour development. Oncogene 23 (2004), 1902–1910.
3. Berger, E., Yuan, D., Waldschmitt, N., Rath, E., Allgäuer, M., Staszewski, O., Kober, O., Lobner, E., Schöttl, T., Prinz, M., et al. Mitochondrial function controls epithelial stemness and proliferation in the intestine independent of unfolded protein response signaling mechanisms. Nat. Commun., 7, 2016, 13171.
4. Boulter, L., Govaere, O., Bird, T.G., Radulescu, S., Ramachandran, P., Pellicoro, A., Ridgway, R.A., Seo, S.S., Spee, B., Van Rooijen, N., et al. Macrophage-derived Wnt opposes Notch signaling to specify hepatic progenitor cell fate in chronic liver disease. Nat. Med. 18 (2012), 572–579.
5. Boulter, L., Guest, R.V., Kendall, T.J., Wilson, D.H., Wojtacha, D., Robson, A.J., Ridgway, R.A., Samuel, K., Van Rooijen, N., Barry, S.T., et al. WNT signaling drives cholangiocarcinoma growth and can be pharmacologically inhibited. J. Clin. Invest. 125 (2015), 1269–1285.
6. Cubero, F.J., Zhao, G., Nevzorova, Y.A., Hatting, M., Al Masaoudi, M., Verdier, J., Peng, J., Schaefer, F.M., Hermanns, N., Boekschoten, M.V., et al. Haematopoietic cell-derived Jnk1 is crucial for chronic inflammation and carcinogenesis in an experimental model of liver injury. J. Hepatol. 62 (2015), 140–149.
7. Das, M., Garlick, D.S., Greiner, D.L., Davis, R.J., The role of JNK in the development of hepatocellular carcinoma. Genes Dev. 25 (2011), 634–645.
8. Espin-Palazon, R., Stachura, D.L., Campbell, C.A., Garcia-Moreno, D., Del Cid, N., Kim, A.D., Candel, S., Meseguer, J., Mulero, V., Traver, D., Proinflammatory signaling regulates hematopoietic stem cell emergence. Cell 159 (2014), 1070–1085.
9. Fan, B., Malato, Y., Calvisi, D.F., Naqvi, S., Razumilava, N., Ribback, S., Gores, G.J., Dombrowski, F., Evert, M., Chen, X., et al. Cholangiocarcinomas can originate from hepatocytes in mice. J. Clin. Invest. 122 (2012), 2911–2915.
10. Fujimoto, A., Furuta, M., Shiraishi, Y., Gotoh, K., Kawakami, Y., Arihiro, K., Nakamura, T., Ueno, M., Ariizumi, S., Hai Nguyen, H., et al. Whole-genome mutational landscape of liver cancers displaying biliary phenotype reveals hepatitis impact and molecular diversity. Nat. Commun., 6, 2015, 6120.
11. Gatto, M., Alvaro, D., New insights on cholangiocarcinoma. World J. Gastrointest. Oncol. 2 (2010), 136–145.
12. Guest, R.V., Boulter, L., Kendall, T.J., Minnis-Lyons, S.E., Walker, R., Wigmore, S.J., Sansom, O.J., Forbes, S.J., Cell lineage tracing reveals a biliary origin of intrahepatic cholangiocarcinoma. Cancer Res. 74 (2014), 1005–1010.
13. Guichard, C., Amaddeo, G., Imbeaud, S., Ladeiro, Y., Pelletier, L., Maad, I.B., Calderaro, J., Bioulac-Sage, P., Letexier, M., Degos, F., et al. Integrated analysis of somatic mutations and focal copy-number changes identifies key genes and pathways in hepatocellular carcinoma. Nat. Genet. 44 (2012), 694–698.
14. Han, M.S., Barrett, T., Brehm, M.A., Davis, R.J., Inflammation mediated by JNK in myeloid cells promotes the development of hepatitis and hepatocellular carcinoma. Cell Rep. 15 (2016), 19–26.
15. Haybaeck, J., Zeller, N., Wolf, M.J., Weber, A., Wagner, U., Kurrer, M.O., Bremer, J., Iezzi, G., Graf, R., Clavien, P.A., et al. A lymphotoxin-driven pathway to hepatocellular carcinoma. Cancer Cell 16 (2009), 295–308.
16. Hefetz-Sela, S., Stein, I., Klieger, Y., Porat, R., Sade-Feldman, M., Zreik, F., Nagler, A., Pappo, O., Quagliata, L., Dazert, E., et al. Acquisition of an immunosuppressive protumorigenic macrophage phenotype depending on c-Jun phosphorylation. Proc. Natl. Acad. Sci. USA 111 (2014), 17582–17587.
17. Huang, J., Deng, Q., Wang, Q., Li, K.Y., Dai, J.H., Li, N., Zhu, Z.D., Zhou, B., Liu, X.Y., Liu, R.F., et al. Exome sequencing of hepatitis B virus-associated hepatocellular carcinoma. Nat. Genet. 44 (2012), 1117–1121.
18. Huang, H., Chen, H.W., Evankovich, J., Yan, W., Rosborough, B.R., Nace, G.W., Ding, Q., Loughran, P., Beer-Stolz, D., Billiar, T.R., et al. Histones activate the NLRP3 inflammasome in Kupffer cells during sterile inflammatory liver injury. J. Immunol. 191 (2013), 2665–2679.
19. Hui, L., Bakiri, L., Mairhorfer, A., Schweifer, N., Haslinger, C., Kenner, L., Komnenovic, V., Scheuch, H., Beug, H., Wagner, E.F., p38alpha suppresses normal and cancer cell proliferation by antagonizing the JNK-c-Jun pathway. Nat. Genet. 39 (2007), 741–749.
20. Hui, L., Zatloukal, K., Scheuch, H., Stepniak, E., Wagner, E.F., Proliferation of human HCC cells and chemically induced mouse liver cancers requires JNK1-dependent p21 downregulation. J. Clin. Invest. 118 (2008), 3943–3953.
21. Iannelli, F., Collino, A., Sinha, S., Radaelli, E., Nicoli, P., D'Antiga, L., Sonzogni, A., Faivre, J., Buendia, M.A., Sturm, E., et al. Massive gene amplification drives paediatric hepatocellular carcinoma caused by bile salt export pump deficiency. Nat. Commun., 5, 2014, 3850.
22. Jhunjhunwala, S., Jiang, Z., Stawiski, E.W., Gnad, F., Liu, J., Mayba, O., Du, P., Diao, J., Johnson, S., Wong, K.F., et al. Diverse modes of genomic alteration in hepatocellular carcinoma. Genome Biol., 15, 2014, 436.
23. Jiao, Y., Pawlik, T.M., Anders, R.A., Selaru, F.M., Streppel, M.M., Lucas, D.J., Niknafs, N., Guthrie, V.B., Maitra, A., Argani, P., et al. Exome sequencing identifies frequent inactivating mutations in BAP1, ARID1A and PBRM1 in intrahepatic cholangiocarcinomas. Nat. Genet. 45 (2013), 1470–1473.
24. Jors, S., Jeliazkova, P., Ringelhan, M., Thalhammer, J., Durl, S., Ferrer, J., Sander, M., Heikenwalder, M., Schmid, R.M., Siveke, J.T., et al. Lineage fate of ductular reactions in liver injury and carcinogenesis. J. Clin. Invest. 125 (2015), 2445–2457.
25. Kamata, H., Honda, S., Maeda, S., Chang, L., Hirata, H., Karin, M., Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120 (2005), 649–661.
26. Kang, L.I., Mars, W.M., Michalopoulos, G.K., Signals and cells involved in regulating liver regeneration. Cells 1 (2012), 1261–1292.
27. Keitel, V., Ullmer, C., Haussinger, D., The membrane-bound bile acid receptor TGR5 (Gpbar-1) is localized in the primary cilium of cholangiocytes. Biol. Chem. 391 (2010), 785–789.
28. Liu, B., Zupan, B., Laird, E., Klein, S., Gleason, G., Bozinoski, M., Gal Toth, J., Toth, M., Maternal hematopoietic TNF, via milk chemokines, programs hippocampal development and memory. Nat. Neurosci. 17 (2014), 97–105.
29. Livet, J., Weissman, T.A., Kang, H., Draft, R.W., Lu, J., Bennis, R.A., Sanes, J.R., Lichtman, J.W., Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450 (2007), 56–62.
30. Lu, W.Y., Bird, T.G., Boulter, L., Tsuchiya, A., Cole, A.M., Hay, T., Guest, R.V., Wojtacha, D., Man, T.Y., Mackinnon, A., et al. Hepatic progenitor cells of biliary origin with liver repopulation capacity. Nat. Cell Biol. 17 (2015), 971–983.
31. Maeda, S., Kamata, H., Luo, J.L., Leffert, H., Karin, M., IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 121 (2005), 977–990.
32. Malato, Y., Naqvi, S., Schurmann, N., Ng, R., Wang, B., Zape, J., Kay, M.A., Grimm, D., Willenbring, H., Fate tracing of mature hepatocytes in mouse liver homeostasis and regeneration. J. Clin. Invest. 121 (2011), 4850–4860.
33. Matter, M.S., Marquardt, J.U., Andersen, J.B., Quintavalle, C., Korokhov, N., Stauffer, J.K., Kaji, K., Decaens, T., Quagliata, L., Elloumi, F., et al. Oncogenic driver genes and the inflammatory microenvironment dictate liver tumor phenotype. Hepatology 63 (2016), 1888–1899.
34. Nakagawa, H., Umemura, A., Taniguchi, K., Font-Burgada, J., Dhar, D., Ogata, H., Zhong, Z., Valasek, M.A., Seki, E., Hidalgo, J., et al. ER stress cooperates with hypernutrition to trigger TNF-dependent spontaneous HCC development. Cancer Cell 26 (2014), 331–343.
35. Nishikawa, Y., Sone, M., Nagahama, Y., Kumagai, E., Doi, Y., Omori, Y., Yoshioka, T., Tokairin, T., Yoshida, M., Yamamoto, Y., et al. Tumor necrosis factor-alpha promotes bile ductular transdifferentiation of mature rat hepatocytes in vitro. J. Cell Biochem. 114 (2013), 831–843.
36. Nitou, M., Sugiyama, Y., Ishikawa, K., Shiojiri, N., Purification of fetal mouse hepatoblasts by magnetic beads coated with monoclonal anti-e-cadherin antibodies and their in vitro culture. Exp. Cell Res. 279 (2002), 330–343.
37. Ohsawa, S., Sato, Y., Enomoto, M., Nakamura, M., Betsumiya, A., Igaki, T., Mitochondrial defect drives non-autonomous tumour progression through Hippo signalling in Drosophila. Nature 490 (2012), 547–551.
38. Pikarsky, E., Porat, R.M., Stein, I., Abramovitch, R., Amit, S., Kasem, S., Gutkovich-Pyest, E., Urieli-Shoval, S., Galun, E., Ben-Neriah, Y., NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 431 (2004), 461–466.
39. Postic, C., Shiota, M., Niswender, K.D., Jetton, T.L., Chen, Y., Moates, J.M., Shelton, K.D., Lindner, J., Cherrington, A.D., Magnuson, M.A., Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J. Biol. Chem. 274 (1999), 305–315.
40. Rizvi, S., Eaton, J.E., Gores, G.J., Primary sclerosing cholangitis as a premalignant biliary tract disease: surveillance and management. Clin. Gastroenterol. Hepatol. 13 (2015), 2152–2165.
41. Roberts, R.A., Ganey, P.E., Ju, C., Kamendulis, L.M., Rusyn, I., Klaunig, J.E., Role of the Kupffer cell in mediating hepatic toxicity and carcinogenesis. Toxicol. Sci. 96 (2007), 2–15.
42. Rougemont, A.L., Genevay, M., McKee, T.A., Gremaud, M., Mentha, G., Rubbia-Brandt, L., Extensive biliary intraepithelial neoplasia (BilIN) and multifocal early intrahepatic cholangiocarcinoma in non-biliary cirrhosis. Virchows Arch. 456 (2010), 711–717.
43. Saha, S.K., Parachoniak, C.A., Ghanta, K.S., Fitamant, J., Ross, K.N., Najem, M.S., Gurumurthy, S., Akbay, E.A., Sia, D., Cornella, H., et al. Mutant IDH inhibits HNF-4alpha to block hepatocyte differentiation and promote biliary cancer. Nature 513 (2014), 110–114.
44. Sakurai, T., Maeda, S., Chang, L., Karin, M., Loss of hepatic NF-kappa B activity enhances chemical hepatocarcinogenesis through sustained c-Jun N-terminal kinase 1 activation. Proc. Natl. Acad. Sci. USA 103 (2006), 10544–10551.
45. Scheeren, F.A., Kuo, A.H., van Weele, L.J., Cai, S., Glykofridis, I., Sikandar, S.S., Zabala, M., Qian, D., Lam, J.S., Johnston, D., et al. A cell-intrinsic role for TLR2-MYD88 in intestinal and breast epithelia and oncogenesis. Nat. Cell Biol. 16 (2014), 1238–1248.
46. Schulze, K., Imbeaud, S., Letouze, E., Alexandrov, L.B., Calderaro, J., Rebouissou, S., Couchy, G., Meiller, C., Shinde, J., Soysouvanh, F., et al. Exome sequencing of hepatocellular carcinomas identifies new mutational signatures and potential therapeutic targets. Nat. Genet. 47 (2015), 505–511.
47. Shi, Y., Evans, J.E., Rock, K.L., Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425 (2003), 516–521.
48. Szabo, G., Petrasek, J., Inflammasome activation and function in liver disease. Nat. Rev. Gastroenterol. Hepatol. 12 (2015), 387–400.
49. Taniguchi, K., Wu, L.W., Grivennikov, S.I., de Jong, P.R., Lian, I., Yu, F.X., Wang, K., Ho, S.B., Boland, B.S., Chang, J.T., et al. A gp130-Src-YAP module links inflammation to epithelial regeneration. Nature 519 (2015), 57–62.
50. Tarlow, B.D., Pelz, C., Naugler, W.E., Wakefield, L., Wilson, E.M., Finegold, M.J., Grompe, M., Bipotential adult liver progenitors are derived from chronically injured mature hepatocytes. Cell Stem Cell 15 (2014), 605–618.
51. Tschaharganeh, D.F., Xue, W., Calvisi, D.F., Evert, M., Michurina, T.V., Dow, L.E., Banito, A., Katz, S.F., Kastenhuber, E.R., Weissmueller, S., et al. p53-dependent Nestin regulation links tumor suppression to cellular plasticity in liver cancer. Cell 158 (2014), 579–592.
52. Tyson, G.L., El-Serag, H.B., Risk factors for cholangiocarcinoma. Hepatology 54 (2011), 173–184.
53. Vucur, M., Reisinger, F., Gautheron, J., Janssen, J., Roderburg, C., Cardenas, D.V., Kreggenwinkel, K., Koppe, C., Hammerich, L., Hakem, R., et al. RIP3 inhibits inflammatory hepatocarcinogenesis but promotes cholestasis by controlling caspase-8- and JNK-dependent compensatory cell proliferation. Cell Rep 4 (2013), 776–790.
54. Weber, J., Ollinger, R., Friedrich, M., Ehmer, U., Barenboim, M., Steiger, K., Heid, I., Mueller, S., Maresch, R., Engleitner, T., et al. CRISPR/Cas9 somatic multiplex-mutagenesis for high-throughput functional cancer genomics in mice. Proc. Natl. Acad. Sci. USA 112 (2015), 13982–13987.
55. Wolf, M.J., Adili, A., Piotrowitz, K., Abdullah, Z., Boege, Y., Stemmer, K., Ringelhan, M., Simonavicius, N., Egger, M., Wohlleber, D., et al. Metabolic activation of intrahepatic CD8+ T cells and NKT cells causes nonalcoholic steatohepatitis and liver cancer via cross-talk with hepatocytes. Cancer Cell 26 (2014), 549–564.
56. Woodworth, C.D., McMullin, E., Iglesias, M., Plowman, G.D., Interleukin 1 alpha and tumor necrosis factor alpha stimulate autocrine amphiregulin expression and proliferation of human papillomavirus-immortalized and carcinoma-derived cervical epithelial cells. Proc. Natl. Acad. Sci. USA 92 (1995), 2840–2844.
57. Yanger, K., Knigin, D., Zong, Y., Maggs, L., Gu, G., Akiyama, H., Pikarsky, E., Stanger, B.Z., Adult hepatocytes are generated by self-duplication rather than stem cell differentiation. Cell Stem Cell 15 (2014), 340–349.
58. Yimlamai, D., Christodoulou, C., Galli, G.G., Yanger, K., Pepe-Mooney, B., Gurung, B., Shrestha, K., Cahan, P., Stanger, B.Z., Camargo, F.D., Hippo pathway activity influences liver cell fate. Cell 157 (2014), 1324–1338.
59. Zender, S., Nickeleit, I., Wuestefeld, T., Sorensen, I., Dauch, D., Bozko, P., El-Khatib, M., Geffers, R., Bektas, H., Manns, M.P., et al. A critical role for notch signaling in the formation of cholangiocellular carcinomas. Cancer Cell 23 (2013), 784–795.
60. Zhang, F., Chen, X.P., Zhang, W., Dong, H.H., Xiang, S., Zhang, W.G., Zhang, B.X., Combined hepatocellular cholangiocarcinoma originating from hepatic progenitor cells: immunohistochemical and double-fluorescence immunostaining evidence. Histopathology 52 (2008), 224–232.
61. Zhu, H.Z., Ruan, Y.B., Wu, Z.B., Zhang, C.M., Kupffer cell and apoptosis in experimental HCC. World J. Gastroenterol. 6 (2000), 405–407.
62. Zou, S., Li, J., Zhou, H., Frech, C., Jiang, X., Chu, J.S., Zhao, X., Li, Y., Li, Q., Wang, H., et al. Mutational landscape of intrahepatic cholangiocarcinoma. Nat. Commun., 5, 2014, 5696.