Gut microbiota dependent anti-tumor immunity restricts melanoma growth in Rnf5 −/− mice

Nature Communications

Volumn 10, Issue 1, 2019, Pages

  Li, Yan ^a   Tinoco, Roberto ^a,n   Elmén, Lisa ^a   Segota, Igor ^a   Xian, Yibo ^b   Fujita, Yu ^a   Sahu, Avinash ^c   Zarecki, Raphy ^d   Marie, Kerrie ^e   Feng, Yongmei ^a   Khateb, Ali ^f   Frederick, Dennie T ^g   Ashkenazi, Shiri K ^f   Kim, Hyungsoo ^a   Perez, Eva Guijarro ^e   Day, Chi Ping ^e   Segura Muñoz, Rafael S ^b   Schmaltz, Robert ^b   Yooseph, Shibu ^h   Tam, Miguel A ⁱ   Zhang, Tongwu ^e   Avitan Hersh, Emily ^f,j   Tzur, Lihi ^j   Roizman, Shoshana ^j   Boyango, Ilanit ^j   Bar Sela, Gil ^f,j   Orian, Amir ^f   Kaufman, Randal J ^a   Bosenberg, Marcus ^k   Goding, Colin R ^l   Baaten, Bas ^a   Levesque, Mitchell P ^m   Dummer, Reinhard ^m   Brown, Kevin ^e   Merlino, Glenn ^e   Ruppin, Eytan ^c,d,e   Flaherty, Keith ^g   Ramer Tait, Amanda ^b   Long, Tao ^a   Peterson, Scott N ^a   Bradley, Linda M ^a   Ronai, Ze’ev A ^a,f   more..

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c Institute of Advanced Computer Science   (United States)

^d TEL AVIV UNIVERSITY   (Israel)

^e NATIONAL CANCER INSTITUTE   (United States)

^f TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^g HARVARD MEDICAL SCHOOL   (United States)

^h University of Central Florida   (United States)

ⁱ BIOLEGEND   (United States)

^j RAMBAM MEDICAL CENTER   (Israel)

^k YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^l UNIVERSITY OF OXFORD   (United Kingdom)

^m UNIVERSITY HOSPITAL ZURICH   (Switzerland)

ⁿ UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA1 INTERFERON; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INTERLEUKIN 1BETA; INTERLEUKIN 6; RANTES; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR; UBIQUITIN PROTEIN LIGASE; ANTIMICROBIAL CATIONIC PEPTIDE; MEMBRANE PROTEIN; RNF5 PROTEIN, MOUSE;

CELL; DIGESTIVE SYSTEM; ENZYME ACTIVITY; GENE EXPRESSION; IMMUNITY; INHIBITION; PHYSIOLOGY; PROTEIN; TUMOR;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CITROBACTER RODENTIUM; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FECES ANALYSIS; FLOW CYTOMETRY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; MELANOMA; MOUSE; NONHUMAN; PHENOTYPE; PROGRESSION FREE SURVIVAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR VOLUME; UNFOLDED PROTEIN RESPONSE; WESTERN BLOTTING; ANIMAL; BACTERIUM; C57BL MOUSE; CELL PROLIFERATION; CLASSIFICATION; DEFICIENCY; ENZYMOLOGY; GENETICS; IMMUNOLOGY; INTESTINE; ISOLATION AND PURIFICATION; KNOCKOUT MOUSE; MICROBIOLOGY; PATHOPHYSIOLOGY;

BACTERIA (MICROORGANISMS); MURINAE; MUS;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIA; CELL PROLIFERATION; GASTROINTESTINAL MICROBIOME; HUMANS; INTESTINES; MELANOMA; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; UBIQUITIN-PROTEIN LIGASES; UNFOLDED PROTEIN RESPONSE;

EID: 85063737545     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-019-09525-y     Document Type: Article

References (50)

1. Sharma, P. & Allison, J. P. Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell 161, 205–214 (2015).
2. Reddy, S. M., Reuben, A. & Wargo, J. A. Influences of BRAF inhibitors on the immune microenvironment and the rationale for combined molecular and immune targeted therapy. Curr. Oncol. Rep. 18, 42 (2016).
3. Sivan, A. et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350, 1084–1089 (2015).
4. Vetizou, M. et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350, 1079–1084 (2015).
5. Kuang, E., Qi, J. & Ronai, Z. Emerging roles of E3 ubiquitin ligases in autophagy. Trends Biochem. Sci. 38, 453–460 (2013).
6. Younger, J. M. et al. Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell 126, 571–582 (2006).
7. Jeon, Y. J. et al. Regulation of glutamine carrier proteins by RNF5 determines breast cancer response to ER stress-inducing chemotherapies. Cancer Cell. 27, 354–369 (2015).
8. Kuang, E. et al. Regulation of ATG4B stability by RNF5 limits basal levels of autophagy and influences susceptibility to bacterial infection. PLoS Genet. 8, e1003007 (2012).
9. Zhong, B. et al. The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA. Immunity 30, 397–407 (2009).
10. Corrales, L. et al. Direct activation of STING in the tumor microenvironment leads to potent and systemic tumor regression and immunity. Cell Rep. 11, 1018–1030 (2015).
11. Fu, J. et al. STING agonist formulated cancer vaccines can cure established tumors resistant to PD-1 blockade. Sci. Transl. Med 7, 283ra252 (2015).
12. Meeth, K., Wang, J. X., Micevic, G., Damsky, W. & Bosenberg, M. W. The YUMM lines: a series of congenic mouse melanoma cell lines with defined genetic alterations. Pigment. Cell. Melanoma Res. 29, 590–597 (2016).
13. Elinav, E. et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145, 745–757 (2011).
14. Couturier-Maillard, A. et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J. Clin. Invest. 123, 700–711 (2013).
15. Vanaja, S. K., Rathinam, V. A. & Fitzgerald, K. A. Mechanisms of inflammasome activation: recent advances and novel insights. Trends Cell Biol. 25, 308–315 (2015).
16. Kamada, N., Seo, S. U., Chen, G. Y. & Nunez, G. Role of the gut microbiota in immunity and inflammatory disease. Nat. Rev. Immunol. 13, 321–335 (2013).
17. Averous, J. et al. Induction of CHOP expression by amino acid limitation requires both ATF4 expression and ATF2 phosphorylation. J. Biol. Chem. 279, 5288–5297 (2004).
18. Roybal, C. N., Hunsaker, L. A., Barbash, O., Vander Jagt, D. L. & Abcouwer, S. F. The oxidative stressor arsenite activates vascular endothelial growth factor mRNA transcription by an ATF4-dependent mechanism. J. Biol. Chem. 280, 20331–20339 (2005).
19. Harding, H. P. et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11, 619–633 (2003).
20. Nesbeth, Y. C. et al. CD4+ T cells elicit host immune responses to MHC class II-negative ovarian cancer through CCL5 secretion and CD40-mediated licensing of dendritic cells. J. Immunol. 184, 5654–5662 (2010).
21. Goc, J. et al. Dendritic cells in tumor-associated tertiary lymphoid structures signal a Th1 cytotoxic immune contexture and license the positive prognostic value of infiltrating CD8+ T cells. Cancer Res. 74, 705–715 (2014).
22. Liu, Y. & Cao, X. Intratumoral dendritic cells in the anti-tumor immune response. Cell. Mol. Immunol. 12, 387–390 (2015).
23. Gururajan, M., Jacob, J. & Pulendran, B. Toll-like receptor expression and responsiveness of distinct murine splenic and mucosal B-cell subsets. PLoS One 2, e863 (2007).
24. Jang, M. H. et al. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J. Immunol. 176, 803–810 (2006).
25. Forster, R., Davalos-Misslitz, A. C. & Rot, A. CCR7 and its ligands: balancing immunity and tolerance. Nat. Rev. Immunol. 8, 362–371 (2008).
26. Salmon, H. et al. Expansion and activation of CD103(+) dendritic cell progenitors at the tumor site enhances tumor responses to therapeutic PD-L1 and BRAF inhibition. Immunity 44, 924–938 (2016).
27. Coombes, J. L. & Powrie, F. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8, 435–446 (2008).
28. Jung C., Hugot J. P., Barreau F. Peyer’s Patches: the immune sensors of the intestine. Int. J. Inflam. 2010, 823710 (2010).
29. Tcherpakov, M. et al. Regulation of endoplasmic reticulum-associated degradation by RNF5-dependent ubiquitination of JNK-associated membrane protein (JAMP). J. Biol. Chem. 284, 12099–12109 (2009).
30. Morito, D. et al. Gp78 cooperates with RMA1 in endoplasmic reticulum-associated degradation of CFTRDeltaF508. Mol. Biol. Cell 19, 1328–1336 (2008).
31. Lee, A. H., Iwakoshi, N. N. & Glimcher, L. H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23, 7448–7459 (2003).
32. Cubillos-Ruiz, J. R. et al. ER stress sensor XBP1 controls anti-tumor immunity by disrupting dendritic cell homeostasis. Cell 161, 1527–1538 (2015).
33. Kaser, A. et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134, 743–756 (2008).
34. Kaser, A. & Blumberg, R. S. Endoplasmic reticulum stress and intestinal inflammation. Mucosal Immunol. 3, 11–16 (2010).
35. Sun, H. et al. Inhibition of IRE1alpha-driven pro-survival pathways is a promising therapeutic application in acute myeloid leukemia. Oncotarget 7, 18736–18749 (2016).
36. Fujita, Y. et al. Regulation of S100A8 stability by RNF5 in intestinal epithelial cells determines intestinal inflammation and severity of colitis. Cell Rep. 24, 3296–3311 e3296 (2018).
37. Tschurtschenthaler, M. et al. Defective ATG16L1-mediated removal of IRE1alpha drives Crohn’s disease-like ileitis. J. Exp. Med. 214, 401–422 (2017).
38. Adolph, T. E. et al. Paneth cells as a site of origin for intestinal inflammation. Nature 503, 272–276 (2013).
39. Tsuchida, T. et al. The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 33, 765–776 (2010).
40. Zhang, J., Hu, M. M., Wang, Y. Y. & Shu, H. B. TRIM32 protein modulates type I interferon induction and cellular antiviral response by targeting MITA/STING protein for K63-linked ubiquitination. J. Biol. Chem. 287, 28646–28655 (2012).
41. Wang, Q. et al. The E3 ubiquitin ligase AMFR and INSIG1 bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 41, 919–933 (2014).
42. Xing, J. et al. Identification of a role for TRIM29 in the control of innate immunity in the respiratory tract. Nat. Immunol. 17, 1373–1380 (2016).
43. Delaunay, A. et al. The ER-bound RING finger protein 5 (RNF5/RMA1) causes degenerative myopathy in transgenic mice and is deregulated in inclusion body myositis. PLoS One 3, e1609 (2008).
44. Adachi, O. et al. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9, 143–150 (1998).
45. Gomes-Neto, J. C. et al. A real-time PCR assay for accurate quantification of the individual members of the Altered Schaedler Flora microbiota in gnotobiotic mice. J. Microbiol. Methods 135, 52–62 (2017).
46. Turner, S., Pryer, K. M., Miao, V. P. & Palmer, J. D. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J. Eukaryot. Microbiol. 46, 327–338 (1999).
47. Laukens, D., Brinkman, B. M., Raes, J., De Vos, M. & Vandenabeele, P. Heterogeneity of the gut microbiome in mice: guidelines for optimizing experimental design. FEMS Microbiol. Rev. 40, 117–132 (2016).
48. Bromberg, K. D. et al. Increased expression of the E3 ubiquitin ligase RNF5 is associated with decreased survival in breast cancer. Cancer Res. 67, 8172–8179 (2007).
49. Krieg, C. et al. High-dimensional single-cell analysis predicts response to anti-PD-1 immunotherapy. Nat. Med. 24, 144–153 (2018).
50. Ran, F. A. et al. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281–2308 (2013).