Sepsis inhibits tumor growth in mice with cancer through Toll-like receptor 4-associated enhanced Natural Killer cell activity

References

• Zuber B, Tran TC, Aegerter P, Grimaldi D, Charpentier J, Guidet B, Mira JP, Pène F. Impact of case volume on survival of septic shock in patients with malignancies. Crit Care Med. 2012;40:55–62. doi:10.1097/CCM.0b013e31822d74ba.
   PubMed Web of Science ®Google Scholar
• Venet F, Monneret G. Advances in the understanding and treatment of sepsis-induced immunosuppression. Nat Rev Nephrol. 2018;14:121–137. doi:10.1038/nrneph.2017.165.
   PubMed Web of Science ®Google Scholar
• Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140:883–899. doi:10.1016/j.cell.2010.01.025.
   PubMed Web of Science ®Google Scholar
• Hotchkiss RS, Moldawer LL. Parallels between cancer and infectious disease. N Engl J Med. 2014;371:380–383. doi:10.1056/NEJMcibr1404664.
   PubMed Web of Science ®Google Scholar
• Galluzzi L, Buque A, Kepp O, Zitvogel L, Kroemer G. Immunogenic cell death in cancer and infectious disease. Nat Rev Immunol. 2017;17:97–111. doi:10.1038/nri.2016.107.
   PubMed Web of Science ®Google Scholar
• Cavassani KA, Carson W, Moreira AP, Wen H, Schaller MA, Ishii M, Lindell DM, Dou Y, Lukacs NW, Keshamouni VG. The post sepsis-induced expansion and enhanced function of regulatory T cells create an environment to potentiate tumor growth. Blood. 2010;115:4403–4411. doi:10.1182/blood-2009-09-241083.
   PubMed Web of Science ®Google Scholar
• Mota JM, Leite CA, Souza LE, Melo PH, Nascimento DC, de-Deus-Wagatsuma VM, Temporal J, Figueiredo F, Noushmehr H, Alves-Filho JC. Post-sepsis state induces tumor-associated macrophage accumulation through CXCR4/CXCL12 and favors tumor progression in mice. Cancer Immunol Res. 2016;4:312–322. doi:10.1158/2326-6066.CIR-15-0170.
   PubMed Web of Science ®Google Scholar
• Chen L, He Z, Qin L, Li Q, Shi X, Zhao S, Chen L, Zhong N, Chen X. Antitumor effect of malaria parasite infection in a murine Lewis lung cancer model through induction of innate and adaptive immunity. PLoS One. 2011;6:e24407. doi:10.1371/journal.pone.0024407.
   PubMed Web of Science ®Google Scholar
• Zhang H, Diao H, Jia L, Yuan Y, Thamm DH, Wang H, Jin Y, Pei S, Zhou B, Yu F. Proteus mirabilis inhibits cancer growth and pulmonary metastasis in a mouse breast cancer model. PLoS One. 2017;12:e0188960. doi:10.1371/journal.pone.0188960.
   PubMed Web of Science ®Google Scholar
• Buzas K, Marton A, Vizler C, Gyukity-Sebestyen E, Harmati M, Nagy K, Zvara A, Katona RL, Tubak V, Endresz V, et al. Bacterial sepsis increases survival in metastatic melanoma: chlamydophila pneumoniae induces macrophage polarization and tumor regression. J Invest Dermatol. 2016;136:862–865. doi:10.1016/j.jid.2015.12.032.
   PubMed Web of Science ®Google Scholar
• Llitjos JF, Auffray C, Alby-Laurent F, Rousseau C, Merdji H, Bonilla N, Toubiana J, Belaidouni N, Mira JP, Lucas B, et al. Sepsis-induced expansion of granulocytic myeloid-derived suppressor cells promotes tumour growth through Toll-like receptor 4. J Pathol. 2016;239:473–483. doi:10.1002/path.4744.
   PubMed Web of Science ®Google Scholar
• Shu SY, Rosenberg SA. Adoptive immunotherapy of newly induced murine sarcomas. Cancer Res. 1985;45:1657–1662.
   PubMed Web of Science ®Google Scholar
• International Cell Line Authentification Committee [Internet]. https://iclac.org/databases/cross-contaminations/.[accessed 2019 Feb 4]
   Google Scholar
• National Center for Biotechnology Information, BioSample database. http://www.ncbi.nlm.nih.gov/biosample/?term=cell%20line%20status%20misidentified[Attribute]. [accessed 2019 Feb 4].
   Google Scholar
• Pène F, Zuber B, Courtine E, Rousseau C, Ouaaz F, Toubiana J, Tazi A, Mira JP, Chiche JD. Dendritic cells modulate lung response to Pseudomonas aeruginosa in a murine model of sepsis-induced immune dysfunction. J Immunol. 2008;181:8513–8520. doi:10.4049/jimmunol.181.12.8513.
   PubMed Web of Science ®Google Scholar
• de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, Plummer M. Global. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 2012;13:607–615. doi:10.1016/S1470-2045(12)70137-7.
   PubMed Web of Science ®Google Scholar
• Kristinsson SY, Bjorkholm M, Hultcrantz M, Derolf AR, Landgren O, Goldin LR. Chronic immune stimulation might act as a trigger for the development of acute myeloid leukemia or myelodysplastic syndromes. J Clin Oncol. 2011;29:2897–2903. doi:10.1200/JCO.2011.34.8540.
   PubMed Web of Science ®Google Scholar
• Titmarsh GJ, McMullin MF, McShane CM, Clarke M, Engels EA, Anderson LA. Community-acquired infections and their association with myeloid malignancies. Cancer Epidemiol. 2014;38:56–61. doi:10.1016/j.canep.2013.10.009.
   PubMed Web of Science ®Google Scholar
• Liu Z, Mahale P, Engels EA. Sepsis and risk of cancer among elderly adults in the United States. Clin Infect Dis. 2018.
   Web of Science ®Google Scholar
• Coley WB II. Contribution to the knowledge of sarcoma. Ann Surg. 1891;14:199–220. doi:10.1097/00000658-189112000-00015.
   PubMedGoogle Scholar
• Coley WB. The treatment of malignant tumors by repeated inoculations of erysipelas: with a report of ten original cases. Am J Med Sci. 1893;105:487–511. doi:10.1097/00000441-189305000-00001.
   Google Scholar
• Ifrah N, James JM, Viguie F, Marie JP, Zittoun R. Spontaneous remission in adult acute leukemia. Cancer. 1985;56:1187–1190. doi:10.1002/1097-0142(19850901)56:5<1187::aid-cncr2820560536>3.0.co;2-o.
   PubMed Web of Science ®Google Scholar
• Maywald O, Buchheidt D, Bergmann J, Schoch C, Ludwig WD, Reiter A, Hastka J, Lengfelder E, Hehlmann R. Spontaneous remission in adult acute myeloid leukemia in association with systemic bacterial infection-case report and review of the literature. Ann Hematol. 2004;83:189–194. doi:10.1007/s00277-003-0741-y.
   PubMed Web of Science ®Google Scholar
• Kostner AH, Johansen RF, Schmidt H, Molle I. Regression in cancer following fever and acute infection. Acta Oncol. 2013;52:455–457. doi:10.3109/0284186X.2012.711954.
   PubMed Web of Science ®Google Scholar
• Rankin EB, Yu D, Jiang J, Shen H, Pearce EJ, Goldschmidt MH, Levy DE, Golovkina TV, Hunter CA, Thomas-Tikhonenko A. An essential role of Th1 responses and interferon gamma in infection-mediated suppression of neoplastic growth. Cancer Biol Ther. 2003;2:687–693.
   PubMed Web of Science ®Google Scholar
• Hunter CA, Yu D, Gee M, Ngo CV, Sevignani C, Goldschmidt M, Golovkina TV, Evans S, Lee WF, Thomas-Tikhonenko A. Cutting edge: systemic inhibition of angiogenesis underlies resistance to tumors during acute toxoplasmosis. J Immunol. 2001;166:5878–5881. doi:10.4049/jimmunol.166.10.5878.
   PubMed Web of Science ®Google Scholar
• Saltzman D, Augustin L, Leonard A, Mertensotto M, Schottel J. Low dose chemotherapy combined with attenuated Salmonella decreases tumor burden and is less toxic than high dose chemotherapy in an autochthonous murine model of breast cancer. Surgery. 2018;163:509–514. doi:10.1016/j.surg.2017.09.036.
   PubMed Web of Science ®Google Scholar
• Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013;342:967–970. doi:10.1126/science.1240527.
   PubMed Web of Science ®Google Scholar
• Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillere R, Hannani D, Enot DP, Pfirschke C, Engblom C, Pittet MJ, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science. 2013;342:971–976. doi:10.1126/science.1240537.
   PubMed Web of Science ®Google Scholar
• Vetizou M, Pitt JM, Daillere R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350:1079–1084. doi:10.1126/science.aad1329.
   PubMed Web of Science ®Google Scholar
• Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillere R, Fluckiger A, Messaoudene M, Rauber C, Roberti MP, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 2017;359:91–97. doi:10.1126/science.aan3706.
   PubMed Web of Science ®Google Scholar
• Remick DG, Newcomb DE, Bolgos GL, Call DR. Comparison of the mortality and inflammatory response of two models of sepsis: lipopolysaccharide vs. cecal ligation and puncture. Shock. 2000;13:110–116.
   PubMed Web of Science ®Google Scholar
• Prakash H, Nadella V, Singh S, Schmitz-Winnenthal H. CD14/TLR4 priming potentially recalibrates and exerts anti-tumor efficacy in tumor associated macrophages in a mouse model of pancreatic carcinoma. Sci Rep. 2016;6:31490. doi:10.1038/srep31490.
   PubMed Web of Science ®Google Scholar
• Muller E, Christopoulos PF, Halder S, Lunde A, Beraki K, Speth M, Oynebraten I, Corthay A. Toll-like receptor ligands and interferon-gamma synergize for induction of antitumor m1 macrophages. Front Immunol. 2017;8:1383. doi:10.3389/fimmu.2017.01383.
   PubMed Web of Science ®Google Scholar
• Rakoff-Nahoum S, Medzhitov R. Toll-like receptors and cancer. Nat Rev Cancer. 2009;9:57–63. doi:10.1038/nrc2541.
   PubMed Web of Science ®Google Scholar
• Huang B, Zhao J, Shen S, Li H, He KL, Shen GX, Mayer L, Unkeless J, Li D, Yuan Y, et al. Listeria monocytogenes promotes tumor growth via tumor cell toll-like receptor 2 signaling. Cancer Res. 2007;67:4346–4352. doi:10.1158/0008-5472.CAN-06-4067.
   PubMed Web of Science ®Google Scholar
• Bohnhorst J, Rasmussen T, Moen SH, Flottum M, Knudsen L, Borset M, Espevik T, Sundan A. Toll-like receptors mediate proliferation and survival of multiple myeloma cells. Leukemia. 2006;20:1138–1144. doi:10.1038/sj.leu.2404225.
   PubMed Web of Science ®Google Scholar
• Yang H, Wang B, Wang T, Xu L, He C, Wen H, Yan J, Su H, Zhu X. et al. Toll-like receptor 4 prompts human breast cancer cells invasiveness via lipopolysaccharide stimulation and is overexpressed in patients with lymph node metastasis. PLoS One. 2014;9:e109980. doi:10.1371/journal.pone.0109980.
   PubMed Web of Science ®Google Scholar
• Pidgeon GP, Harmey JH, Kay E, Da Costa M, Redmond HP, Bouchier-Hayes DJ. The role of endotoxin/lipopolysaccharide in surgically induced tumour growth in a murine model of metastatic disease. Br J Cancer. 1999;81:1311–1317. doi:10.1038/sj.bjc.6694369.
   PubMed Web of Science ®Google Scholar
• Harmey JH, Bucana CD, Lu W, Byrne AM, McDonnell S, Lynch C, Bouchier-Hayes D, Dong Z. Lipopolysaccharide-induced metastatic growth is associated with increased angiogenesis, vascular permeability and tumor cell invasion. Int J Cancer. 2002;101:415–422. doi:10.1002/ijc.10632.
   PubMed Web of Science ®Google Scholar
• Standiford TJ, Kuick R, Bhan U, Chen J, Newstead M, Keshamouni VG. TGF-beta-induced IRAK-M expression in tumor-associated macrophages regulates lung tumor growth. Oncogene. 2011;30:2475–2484. doi:10.1038/onc.2010.619.
   PubMed Web of Science ®Google Scholar
• Sfondrini L, Rossini A, Besusso D, Merlo A, Tagliabue E, Menard S, Balsari A. Antitumor activity of the TLR-5 ligand flagellin in mouse models of cancer. J Immunol. 2006;176:6624–6630. doi:10.4049/jimmunol.176.11.6624.
   PubMed Web of Science ®Google Scholar
• Chang LS, Leng CH, Yeh YC, Wu CC, Chen HW, Huang HM, Liu SJ. Toll-like receptor 9 agonist enhances anti-tumor immunity and inhibits tumor-associated immunosuppressive cells numbers in a mouse cervical cancer model following recombinant lipoprotein therapy. Mol Cancer. 2014;13:60. doi:10.1186/1476-4598-13-60.
   PubMed Web of Science ®Google Scholar
• Dajon M, Iribarren K, Cremer I. Toll-like receptor stimulation in cancer: A pro- and anti-tumor double-edged sword. Immunobiology. 2017;222:89–100. doi:10.1016/j.imbio.2016.06.009.
   PubMed Web of Science ®Google Scholar
• Crowe NY, Smyth MJ, Godfrey DI. A critical role for natural killer T cells in immunosurveillance of methylcholanthrene-induced sarcomas. J Exp Med. 2002;196:119–127. doi:10.1084/jem.20020092.
   PubMed Web of Science ®Google Scholar
• Arias MA, Jimenez de Bagues MP, Aguilo N, Menao S, Hervas-Stubbs S, de Martino A, Alcaraz A, Simon MM, Froelich CJ, Pardo J. Elucidating sources and roles of granzymes A and B during bacterial infection and sepsis. Cell Rep. 2014;8:420–429. doi:10.1016/j.celrep.2014.06.012.
   PubMed Web of Science ®Google Scholar
• Garcia-Laorden MI, Stroo I, Blok DC, Florquin S, Medema JP, de Vos AF, van der Poll T. Granzymes A and B regulate the local inflammatory response during klebsiella pneumoniae pneumonia. J Innate Immun. 2016;8:258–268. doi:10.1159/000443401.
   PubMed Web of Science ®Google Scholar
• Chiossone L, Dumas PY, Vienne M, Vivier E. Natural killer cells and other innate lymphoid cells in cancer. Nat Rev Immunol. 2018;18:671–688. doi:10.1038/s41577-018-0061-z.
   PubMed Web of Science ®Google Scholar
• Cheney EE, Wise EL, Bui JD, Schreiber RD, Carayannopoulos LN, Spitzer D, Zafirova B, Polic B, Shaw AS, Markiewicz MA. A dual function of NKG2D ligands in NK-cell activation. Eur J Immunol. 2012;42:2452–2458. doi:10.1002/eji.201141849.
   PubMed Web of Science ®Google Scholar
• Deng W, Gowen BG, Zhang L, Wang L, Lau S, Iannello A, Xu J, Rovis TL, Xiong N, Raulet DH. Antitumor immunity. A shed NKG2D ligand that promotes natural killer cell activation and tumor rejection. Science. 2015;348:136–139. doi:10.1126/science.1258867.
   PubMed Web of Science ®Google Scholar
• Hasmim M, Messai Y, Ziani L, Thiery J, Bouhris JH, Noman MZ, Chouaib S. Critical role of tumor microenvironment in shaping NK cell functions: implication of hypoxic stress. Front Immunol. 2015;6:482. doi:10.3389/fimmu.2015.00482.
   PubMed Web of Science ®Google Scholar
• Guo Y, Patil NK, Luan L, Bohannon JK, Sherwood ER. The biology of natural killer cells during sepsis. Immunology. 2018;153:190–202. doi:10.1111/imm.12854.
   PubMed Web of Science ®Google Scholar
• Lee NC, Tsung K, Norton JA. Production of interferon-gamma by tumor-sensitized T cells is essential for interleukin-12-induced complete tumor eradication. Surgery. 2002;132:365–368.
   PubMed Web of Science ®Google Scholar
• Segal JG, Lee NC, Tsung YL, Norton JA, Tsung K. The role of IFN-gamma in rejection of established tumors by IL-12: source of production and target. Cancer Res. 2002;62:4696–4703.
   PubMed Web of Science ®Google Scholar
• Li Z, Pradera F, Kammertoens T, Li B, Liu S, Qin Z. Cross-talk between T cells and innate immune cells is crucial for IFN-gamma-dependent tumor rejection. J Immunol. 2007;179:1568–1576. doi:10.4049/jimmunol.179.3.1568.
   PubMed Web of Science ®Google Scholar
• Lucas M, Schachterle W, Oberle K, Aichele P, Diefenbach A. Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity. 2007;26:503–517. doi:10.1016/j.immuni.2007.03.006.
   PubMed Web of Science ®Google Scholar
• Guo Y, Luan L, Patil NK, Wang J, Bohannon JK, Rabacal W, Fensterheim BA, Hernandez A, Sherwood ER. IL-15 enables septic shock by maintaining NK cell integrity and function. J Immunol. 2017;198:1320–1333. doi:10.4049/jimmunol.1601486.
   PubMed Web of Science ®Google Scholar
• Kramer MG, Masner M, Ferreira FA, Hoffman RM. Bacterial therapy of cancer: promises, limitations, and insights for future directions. Front Microbiol. 2018;9:16. doi:10.3389/fmicb.2018.00016.
   PubMed Web of Science ®Google Scholar