Increased alveolar epithelial TRAF6 via autophagy-dependent TRIM37 degradation mediates particulate matter-induced lung metastasis

References

• Cohen AJ, Brauer M, Burnett R, et al. Estimates and 25-year trends of the global burden of disease attributable to ambient air pollution: an analysis of data from the Global Burden of Diseases Study 2015. Lancet. 2017;389(10082):1907–1918.
   PubMed Web of Science ®Google Scholar
• Liu C, Chen R, Sera F, et al. Ambient particulate air pollution and daily mortality in 652 cities. N Engl J Med. 2019;381:705–715.
   PubMed Web of Science ®Google Scholar
• Eckel SP, Cockburn M, Shu YH, et al. Air pollution affects lung cancer survival. Thorax. 2016;71:891–898.
   PubMed Web of Science ®Google Scholar
• Lippi G, Mattiuzzi C. Particulate matter pollution and lung cancer: a worldwide perspective. Clin Respir J. 2020;14:179–180.
   PubMed Web of Science ®Google Scholar
• Tseng CH, Tsuang BJ, Chiang CJ, et al. The relationship between air pollution and lung cancer in nonsmokers in Taiwan. J Thorac Oncol. 2019;14:784–792.
   PubMed Web of Science ®Google Scholar
• Zhang ZY, Zhu DW, Cui B, et al. Association between particulate matter air pollution and lung cancer. Thorax. 2020;75:85–87.
   PubMed Web of Science ®Google Scholar
• Lee KK, Bing R, Kiang J, et al. Adverse health effects associated with household air pollution: a systematic review, meta-analysis, and burden estimation study. Lancet Glob Health. 2020;8:e1427–e34.
   PubMed Web of Science ®Google Scholar
• Asgharian B, Price OT, Oldham M, et al. Computational modeling of nanoscale and microscale particle deposition, retention and dosimetry in the mouse respiratory tract. Inhal Toxicol. 2014;26:829–842.
   PubMed Web of Science ®Google Scholar
• Zhao QJ, Chen H, Yang T, et al. Direct effects of airborne PM2.5 exposure on macrophage polarizations. BBA-Gen Subj. 2016;1860:2835–2843.
   PubMed Web of Science ®Google Scholar
• Thevenot PT, Saravia J, Jin N, et al. Radical-containing ultrafine particulate matter initiates epithelial-to-mesenchymal transitions in airway epithelial cells. Am J Respir Cell Mol Biol. 2013;48(2):188–197.
   PubMed Web of Science ®Google Scholar
• Wang PL, Thevenot P, Saravia J, et al. Radical-containing particles activate dendritic cells and enhance Th17 inflammation in a mouse model of asthma. Am J Resp Cell Mol. 2011;45(5):977–983.
   PubMed Web of Science ®Google Scholar
• Deng X, Zhang F, Rui W, et al. PM2.5-induced oxidative stress triggers autophagy in human lung epithelial A549 cells. Toxicol In Vitro. 2013;27(6):1762–1770.
   PubMed Web of Science ®Google Scholar
• Xu X, Wang H, Liu S, et al. Aodengqimuge, et al. TP53-dependent autophagy links the ATR-CHEK1 axis activation to proinflammatory VEGFA production in human bronchial epithelial cells exposed to fine particulate matter (PM2.5). Autophagy. 2016;12:1832–1848.
   PubMed Web of Science ®Google Scholar
• Li XB, Lv Y, Gao N, et al. microRNA-802/Rnd3 pathway imposes on carcinogenesis and metastasis of fine particulate matter exposure. Oncotarget. 2016;7:35026–35043.
   PubMedGoogle Scholar
• Lu YY, Lin Y, Ding DX, et al. MiR-26a functions as a tumor suppressor in ambient particulate matter-bound metal-triggered lung cancer cell metastasis by targeting LIN28B-IL6-STAT3 axis. Arch Toxicol. 2018;92:1023–1035.
   PubMed Web of Science ®Google Scholar
• Chen ZH, Wu YF, Wang PL, et al. Autophagy is essential for ultrafine particle-induced inflammation and mucus hyperproduction in airway epithelium. Autophagy. 2016;12:297–311.
   PubMed Web of Science ®Google Scholar
• Deng X, Zhang F, Wang L, et al. Airborne fine particulate matter induces multiple cell death pathways in human lung epithelial cells. Apoptosis. 2014;19:1099–1112.
   PubMed Web of Science ®Google Scholar
• Deng XB, Feng NN, Zheng M, et al. PM2.5 exposure-induced autophagy is mediated by lncRNA loc146880 which also promotes the migration and invasion of lung cancer cells. BBA-Gen Subj. 2017;1861:112–125.
   PubMed Web of Science ®Google Scholar
• Onorati AV, Dyczynski M, Ojha R, et al. Targeting autophagy in cancer. Cancer. 2018;124:3307–3318.
   PubMed Web of Science ®Google Scholar
• Rao S, Tortola L, Perlot T, et al. A dual role for autophagy in a murine model of lung cancer. Nat Commun. 2014;5:3056.
   PubMed Web of Science ®Google Scholar
• White E. The role for autophagy in cancer. J Clin Invest. 2015;125:42–46.
   PubMed Web of Science ®Google Scholar
• Sosa MS, Bragado P, Aguirre-Ghiso JA. Mechanisms of disseminated cancer cell dormancy: an awakening field. Nat Rev Cancer. 2014;14:611–622.
   PubMed Web of Science ®Google Scholar
• Peng YF, Shi YH, Shen YH, et al. Promoting colonization in metastatic HCC cells by modulation of autophagy. PLoS One. 2013;8:e74407.
   PubMed Web of Science ®Google Scholar
• Ishida T, Mizushima S, Azuma S, et al. Identification of TRAF6, a novel tumor necrosis factor receptor-associated factor protein that mediates signaling from an amino-terminal domain of the CD40 cytoplasmic region. J Biol Chem. 1996;271:28745–28748.
   PubMed Web of Science ®Google Scholar
• Cao Z, Xiong J, Takeuchi M, et al. TRAF6 is a signal transducer for interleukin-1. Nature. 1996;383:443–446.
   PubMed Web of Science ®Google Scholar
• Zhan Z, Xie X, Cao H, et al. Autophagy facilitates TLR4- and TLR3-triggered migration and invasion of lung cancer cells through the promotion of TRAF6 ubiquitination. Autophagy. 2014;10:257–268.
   PubMed Web of Science ®Google Scholar
• Wu H, Lu XX, Wang JR, et al. TRAF6 inhibits colorectal cancer metastasis through regulating selective autophagic CTNNB1/β-catenin degradation and is targeted for GSK3B/GSK3β-mediated phosphorylation and degradation. Autophagy. 2019;15:1506–1522.
   PubMed Web of Science ®Google Scholar
• Rezaeian AH, Li CF, Wu CY, et al. A hypoxia-responsive TRAF6-ATM-H2AX signalling axis promotes HIF1α activation, tumorigenesis and metastasis. Nat Cell Biol. 2017;19:38–51.
   PubMed Web of Science ®Google Scholar
• Paget S. The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev. 1989;8:98–101.
   PubMed Web of Science ®Google Scholar
• Wu CF, Andzinski L, Kasnitz N, et al. The lack of type I interferon induces neutrophil-mediated pre-metastatic niche formation in the mouse lung. Int J Cancer. 2015;137:837–847.
   PubMed Web of Science ®Google Scholar
• Scherz-Shouval R, Santagata S, Mendillo ML, et al. The reprogramming of tumor stroma by HSF1 is a potent enabler of malignancy. Cell. 2014;158:564–578.
   PubMed Web of Science ®Google Scholar
• Yamamura Y, Asai N, Enomoto A, et al. Akt-Girdin signaling in cancer-associated fibroblasts contributes to tumor progression. Cancer Res. 2015;75:813–823.
   PubMed Web of Science ®Google Scholar
• Liu Y, Cao X. Characteristics and significance of the pre-metastatic niche. Cancer Cell. 2016;30:668–681.
   PubMed Web of Science ®Google Scholar
• Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013;19:1423–1437.
   PubMed Web of Science ®Google Scholar
• Marigo I, Dolcetti L, Serafini P, et al. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev. 2008;222:162–179.
   PubMed Web of Science ®Google Scholar
• Cella CA, Minucci S, Spada F, et al. Dual inhibition of mTOR pathway and VEGF signalling in neuroendocrine neoplasms: from bench to bedside. Cancer Treat Rev. 2015;41:754–760.
   PubMed Web of Science ®Google Scholar
• Ruan J, Hajjar K, Rafii S, et al. Angiogenesis and antiangiogenic therapy in non-Hodgkin’s lymphoma. Ann Oncol. 2009;20:413–424.
   PubMed Web of Science ®Google Scholar
• Coffelt SB, Kersten K, Doornebal CW, et al. IL-17-producing γδ T cells and neutrophils conspire to promote breast cancer metastasis. Nature. 2015;522:345–348.
   PubMed Web of Science ®Google Scholar
• Liu Y, Gu Y, Han Y, et al. Tumor exosomal RNAs promote lung pre-metastatic niche formation by activating alveolar epithelial TLR3 to recruit neutrophils. Cancer Cell. 2016;30:243–256.
   PubMed Web of Science ®Google Scholar
• Albrengues J, Shields MA, Ng D, et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science. 2018;361:eaao4227.
   Google Scholar
• Quail DF, Olson OC, Bhardwaj P, et al. Obesity alters the lung myeloid cell landscape to enhance breast cancer metastasis through IL5 and GM-CSF. Nat Cell Biol. 2017;19:974–987.
   Google Scholar
• Ruiz-Irastorza G, Ramos-Casals M, Brito-Zeron P, et al. Clinical efficacy and side effects of antimalarials in systemic lupus erythematosus: a systematic review. Ann Rheum Dis. 2010;69:20–28.
   PubMed Web of Science ®Google Scholar
• Olsen NJ, Schleich MA, Karp DR. Multifaceted effects of hydroxychloroquine in human disease. Semin Arthritis Rheum. 2013;43:264–272.
   PubMed Web of Science ®Google Scholar
• Balakrishna S, Lomnicki S, McAvey KM, et al. Environmentally persistent free radicals amplify ultrafine particle mediated cellular oxidative stress and cytotoxicity. Part Fibre Toxicol. 2009;6:11.
   PubMed Web of Science ®Google Scholar
• Lin WJ, Kuang HY. Oxidative stress induces autophagy in response to multiple noxious stimuli in retinal ganglion cells. Autophagy. 2014;10:1692–1701.
   PubMed Web of Science ®Google Scholar
• Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci. 2011;36:30–38.
   PubMed Web of Science ®Google Scholar
• Arthur JS, Ley SC. Mitogen-activated protein kinases in innate immunity. Nat Rev Immunol. 2013;13:679–692.
   PubMed Web of Science ®Google Scholar
• Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell. 2008;132:344–362.
   PubMed Web of Science ®Google Scholar
• Hu HB, Sun SC. Ubiquitin signaling in immune responses. Cell Res. 2016;26:457–483.
   PubMed Web of Science ®Google Scholar
• Harhaj EW, Dixit VM. Deubiquitinases in the regulation of NF-κB signaling. Cell Res. 2011;21:22–39.
   PubMed Web of Science ®Google Scholar
• Zhao W, Wang L, Zhang M, et al. E3 ubiquitin ligase tripartite motif 38 negatively regulates TLR-mediated immune responses by proteasomal degradation of TNF receptor-associated factor 6 in macrophages. J Immunol. 2012;188:2567–2574.
   PubMed Web of Science ®Google Scholar
• Donohue E, Balgi AD, Komatsu M, et al. Induction of covalently crosslinked p62 oligomers with reduced binding to polyubiquitinated proteins by the autophagy inhibitor verteporfin. PLoS One. 2014;9:e114964.
   PubMed Web of Science ®Google Scholar
• McAllister SS, Weinberg RA. The tumour-induced systemic environment as a critical regulator of cancer progression and metastasis. Nat Cell Biol. 2014;16:717–727.
   PubMed Web of Science ®Google Scholar
• Peinado H, Zhang H, Matei IR, et al. Pre-metastatic niches: organ-specific homes for metastases. Nat Rev Cancer. 2017;17:302–317.
   PubMed Web of Science ®Google Scholar
• Wculek SK, Malanchi I. Neutrophils support lung colonization of metastasis-initiating breast cancer cells. Nature. 2015;528:413–417.
   PubMed Web of Science ®Google Scholar
• Kuznik A, Bencina M, Svajger U, et al. Mechanism of endosomal TLR inhibition by antimalarial drugs and imidazoquinolines. J Immunol. 2011;186:4794–4804.
   PubMed Web of Science ®Google Scholar
• Lamphier M, Zheng W, Latz E, et al. Novel small molecule inhibitors of TLR7 and TLR9: mechanism of action and efficacy in vivo. Mol Pharmacol. 2014;85:429–440.
   PubMed Web of Science ®Google Scholar
• Rybstein MD, Bravo-San Pedro JM, Kroemer G, et al. The autophagic network and cancer. Nat Cell Biol. 2018;20:243–251.
   PubMed Web of Science ®Google Scholar
• Wu YF, Li ZY, Dong LL, et al. Inactivation of MTOR promotes autophagy-mediated epithelial injury in particulate matter-induced airway inflammation. Autophagy. 2020;16:435–450.
   PubMed Web of Science ®Google Scholar
• Ovrevik J, Refsnes M, Lag M, et al. Triggering mechanisms and inflammatory effects of combustion exhaust particles with implication for carcinogenesis. Basic Clin Pharmacol Toxicol. 2017;121(Suppl 3):55–62.
   PubMed Web of Science ®Google Scholar
• Ovrevik J, Refsnes M, Lag M, et al. Activation of proinflammatory responses in cells of the airway mucosa by particulate matter: oxidant- and non-oxidant-mediated triggering mechanisms. Biomolecules. 2015;5:1399–1440.
   PubMed Web of Science ®Google Scholar
• Ubellacker JM, Tasdogan A, Ramesh V, et al. Lymph protects metastasizing melanoma cells from ferroptosis. Nature. 2020;585:113–118.
   Google Scholar
• Liou GY, Storz P. Reactive oxygen species in cancer. Free Radic Res. 2010;44:479–496.
   PubMed Web of Science ®Google Scholar
• Piskounova E, Agathocleous M, Murphy MM, et al. Oxidative stress inhibits distant metastasis by human melanoma cells. Nature. 2015;527:186–191.
   PubMed Web of Science ®Google Scholar
• Gao P, Zhang H, Dinavahi R, et al. HIF-dependent antitumorigenic effect of antioxidants in vivo. Cancer Cell. 2007;12:230–238.
   PubMed Web of Science ®Google Scholar
• Gorrini C, Harris IS, Mak TW. Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discov. 2013;12:931–947.
   PubMed Web of Science ®Google Scholar
• Skaug B, Jiang X, Chen ZJ. The role of ubiquitin in NF-kappaB regulatory pathways. Annu Rev Biochem. 2009;78:769–796.
   PubMed Web of Science ®Google Scholar
• Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol. 2013;13:722–737.
   PubMed Web of Science ®Google Scholar
• Senft D, Qi J, Ronai ZA. Ubiquitin ligases in oncogenic transformation and cancer therapy. Nat Rev Cancer. 2018;18:69–88.
   PubMed Web of Science ®Google Scholar
• Wu G, Song L, Zhu J, et al. An ATM/TRIM37/NEMO axis counteracts genotoxicity by activating nuclear-to-cytoplasmic NF-kappaB signaling. Cancer Res. 2018;78:6399–6412.
   PubMed Web of Science ®Google Scholar
• Meitinger F, Ohta M, Lee KY, et al. TRIM37 controls cancer-specific vulnerability to PLK4 inhibition. Nature. 2020;585:440–446.
   PubMed Web of Science ®Google Scholar
• Yeow ZY, Lambrus BG, Marlow R, et al. Targeting TRIM37-driven centrosome dysfunction in 17q23-amplified breast cancer. Nature. 2020;585:447–452.
   PubMed Web of Science ®Google Scholar
• Ding X, Lucas T, Gp M, et al. Distinct functions of epidermal and myeloid-derived VEGF-A in skin tumorigenesis mediated by HPV8. Cancer Res. 2015;75:330–343.
   PubMed Web of Science ®Google Scholar