High IL-1R8 expression in breast tumors promotes tumor growth and contributes to impaired antitumor immunity

Oncotarget

Volumn 8, Issue 30, 2017, Pages 49470-49483

  Campesato, Luis Felipe ^a,b,c   Silva, Ana Paula M ^a   Cordeiro, Luna ^d   Correa, Bruna R ^b   Navarro, Fabio C P ^b   Zanin, Rafael F ^e   Marçola, Marina ^c   Inoue, Lilian T ^b   Duarte, Mariana L ^b   Molgora, Martina ^d   Pasqualini, Fabio ^d   Massara, Matteo ^d   Galante, Pedro ^b   Barroso Sousa, Romualdo ^f   Polentarutti, Nadia ^d   Riva, Federica ^g   Costa, Erico T ^a,b   Mantovani, Alberto ^d,h   Garlanda, Cecilia ^d   Camargo, Anamaria A ^a,b  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (Brazil)

^b HOSPITAL SÍRIO LIBANÊS   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^e PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^f DANA FARBER CANCER INSTITUTE   (United States)

^g UNIVERSITY OF MILAN   (Italy)

^h HUMANITAS UNIVERSITY   (Italy)

Author keywords

Breast cancer; Immune evasion; Innate immune sensing; SIGIRR IL 1R8; Toll IL 1 receptors

Indexed keywords

CD8 ANTIGEN; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR; PROTEIN IL 1R8; REGULATOR PROTEIN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; AUTACOID; SIGIRR PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CARCINOGENESIS; BREAST EPITHELIUM CELL; BREAST TUMOR; CD8+ T LYMPHOCYTE; CELL MOTILITY; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LYMPHOCYTE ACTIVATION; MACROPHAGE; METASTASIS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIMARY TUMOR; PROTEIN EXPRESSION; PROTEIN FAMILY; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; ANIMAL; DENDRITIC CELL; DISEASE MODEL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNITY; IMMUNOLOGY; IMMUNOMODULATION; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; TUMOR CELL LINE; TUMOR ESCAPE;

ANIMALS; BREAST NEOPLASMS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CYTOKINES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNITY; IMMUNITY, INNATE; IMMUNOMODULATION; INFLAMMATION MEDIATORS; KILLER CELLS, NATURAL; MICE; MICE, KNOCKOUT; NF-KAPPA B; RECEPTORS, INTERLEUKIN-1; TUMOR ESCAPE;

EID: 85025836267     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.17713     Document Type: Article

References (57)

1. Mantovani A, Mantovani A, Allavena P, Allavena P, Sica A, Sica A, Balkwill F, Balkwill F. Cancer-related inflammation. Nature. 2008; 454:436-44. doi: 10.1038/nature07205.
2. Elinav E, Nowarski R, Thaiss CA, Hu B, Jin C, Flavell RA. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev Cancer. 2013; 13:759-71. doi: 10.1038/nrc3611.
3. Grivennikov SI, Greten FR, Karin M. Immunity, Inflammation, and Cancer. Cell. 2011; 140:883-99. doi: 10.1016/j.cell.2010.01.025. Immunity.
4. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell. 2011. 646-74. doi: 10.1016/j.cell.2011.02.013.
5. Pandey S, Singh S, Anang V, Bhatt AN, Natarajan K, Dwarakanath BS. Pattern Recognition Receptors in Cancer Progression and Metastasis. Cancer Growth Metastasis. 2015; 8:25-34. doi: 10.4137/CGM.S24314.
6. Rakoff-Nahoum S, Medzhitov R. Toll-like receptors and cancer. Nat Rev Cancer. 2009; 9:57-63. doi: 10.1038/nrc2541.
7. Jinushi M. Yin and yang of tumor inflammation: How innate immune suppressors shape the tumor microenvironments. Int J Cancer. 2014; 135:1277-85. doi: 10.1002/ijc.28626.
8. Fuertes MB, Woo SR, Burnett B, Fu YX, Gajewski TF. Type I interferon response and innate immune sensing of cancer. Trends Immunol. 2013; 34:67-73. doi: 10.1016/j.it.2012.10.004.
9. Barton GM, Medzhitov R. Toll-like receptor signaling pathways. Science. 2003; 300:1524-5. doi: 10.1126/science.1085536.
10. Garlanda C, Dinarello CA, Mantovani A. The Interleukin-1 Family: Back to the Future. Immunity. 2013; 39:1003-18. doi: 10.1016/j.immuni.2013.11.010.
11. O'Neill LA. The interleukin-1 receptor/Toll-like receptor superfamily: 10 Years of progress. Immunol Rev. 2008; 226:10-8. doi: 10.1111/j.1600-065X.2008.00701.x.
12. Garlanda C, Anders HJ, Mantovani A. TIR8/SIGIRR: an IL-1R/TLR family member with regulatory functions in inflammation and T cell polarization. Trends in Immunology. 2009; 439-46. doi: 10.1016/j.it.2009.06.001.
13. Wald D, Qin J, Zhao Z, Qian Y, Naramura M, Tian L, Towne J, Sims JE, Stark GR, Li X. SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol. 2003; 4:920-7. doi: 10.1038/ni968.
14. Qin J, Qian Y, Yao J, Grace C, Li X. SIGIRR inhibits interleukin-1 receptor-and Toll-like receptor 4-mediated signaling through different mechanisms. J Biol Chem. 2005; 280:25233-41. doi: 10.1074/jbc. M501363200.
15. Bulek K, Swaidani S, Qin J, Lu Y, Gulen MF, Herjan T, Min B, Kastelein R a, Aronica M, Kosz-Vnenchak M, Li X. The essential role of single Ig IL-1 receptor-related molecule/Toll IL-1R8 in regulation of Th2 immune response. J Immunol. 2009; 182:2601-9. doi: 10.4049/jimmunol.0802729.
16. Nold-Petry CA, Lo CY, RudloffI, Elgass KD, Li S, Gantier MP, Lotz-Havla AS, Gersting SW, Cho SX, Lao JC, Ellisdon AM, Rotter B, Azam T, et al. IL-37 requires the receptors IL-18α and IL-1R8 (SIGIRR) to carry out its multifaceted anti-inflammatory program upon innate signal transduction. Nat Immunol. 2015; 8. doi: 10.1038/ni.3103.
17. Li S, NeffCP, Barber K, Hong J, Luo Y, Azam T, Palmer BE, Fujita M, Garlanda C, Mantovani A, Kim S, Dinarello CA. Extracellular forms of IL-37 inhibit innate inflammation in vitro and in vivo but require the IL-1 family decoy receptor IL-1R8. Proc Natl Acad Sci. 2015; 112: 201424626 doi: 10.1073/pnas.1424626112.
18. Blok DC, van Lieshout MH, Hoogendijk AJ, Florquin S, de Boer OJ, Garlanda C, Mantovani A, van't Veer C, de Vos AF, van der Poll T. Single immunoglobulin interleukin-1 receptor-related molecule impairs host defense during pneumonia and sepsis caused by Streptococcus pneumoniae. J Innate Immun. 2013; 542-52. doi: 10.1159/000358239.
19. Drexler SK, Kong P, Inglis J, Williams RO, Garlanda C, Mantovani A, Yazdi AS, Brennan F, Feldmann M, Foxwell BMJ. SIGIRR/TIR-8 is an inhibitor of toll-like receptor signaling in primary human cells and regulates inflammation in models of rheumatoid arthritis. Arthritis Rheum. 2010; 62:2249-61. doi: 10.1002/art.27517.
20. Lech M, Kulkarni OP, Pfeiffer S, Savarese E, Krug A, Garlanda C, Mantovani A, Anders HJ. Tir8/Sigirr prevents murine lupus by suppressing the immunostimulatory effects of lupus autoantigens. J Exp Med. 2008; 205:1879-88. doi: 10.1084/jem.20072646.
21. Lech M, Skuginna V, Kulkarni OP, Gong J, Wei T, Stark RW, Garlanda C, Mantovani A, Anders HJ. Lack of SIGIRR/TIR8 aggravates hydrocarbon oil-induced lupus nephritis. J Pathol. 2010; 220:596-607.
22. Garlanda C, Riva F, Polentarutti N, Buracchi C, Sironi M, De Bortoli M, Muzio M, Bergottini R, Scanziani E, Vecchi A, Hirsch E, Mantovani A. Intestinal inflammation in mice deficient in Tir8, an inhibitory member of the IL-1 receptor family. Proc Natl Acad Sci USA. 2004; 101:3522-6. doi: 10.1073/pnas.0308680101.
23. Xiao H, Gulen MF, Qin J, Yao J, Bulek K, Kish D, Altuntas CZ, Wald D, Ma C, Zhou H, Tuohy VK, Fairchild RL, de la Motte C, et al. The Toll-Interleukin-1 Receptor Member SIGIRR Regulates Colonic Epithelial Homeostasis, Inflammation, and Tumorigenesis. Immunity. 2007; 26:461-75. doi: 10.1016/j.immuni.2007.02.012.
24. Xiao H, Yin W, Khan MA, Gulen MF, Zhou H, Sham HP, Jacobson K, Vallance BA, Li X. Loss of single immunoglobulin interlukin-1 receptor-related molecule leads to enhanced colonic polyposis in Apcmin mice. Gastroenterology. 2010; 139:574-85. doi: 10.1053/j.gastro.2010.04.043.
25. Garlanda C, Riva F, Veliz T, Polentarutti N, Pasqualini F, Radaelli E, Sironi M, Nebuloni M, Zorini EO, Scanziani E, Mantovani A. Increased susceptibility to colitis-associated cancer of mice lacking TIR8, an inhibitory member of the interleukin-1 receptor family. Cancer Res. 2007; 67:6017-21. doi: 10.1158/0008-5472.CAN-07-0560.
26. Bertilaccio MTS, Simonetti G, Dagklis A, Rocchi M, Veliz Rodriguez T, Apollonio B, Mantovani A, Ponzoni M, Ghia P, Garlanda C, Caligaris-Cappio F, Muzio M. Lack of TIR8/SIGIRR triggers progression of chronic lymphocytic leukemia in mouse models. Blood. 2011; 118:660-9. doi: 10.1182/blood-2011-01-329870.
27. Harris RA, Eichholtz TJ, Hiles ID, Page MJ, O'Hare MJ. New model of erbB-2 over-expression in human mammary luminal epithelial cells. Int J Cancer. 1999; 80:477-84. doi: 10.1002/(SICI)1097-0215(19990129)80:3<477::AIDIJC23> 3.0.CO;2-W.
28. Dunne A, O'Neill LAJ. The interleukin-1 receptor/Tolllike receptor superfamily: signal transduction during inflammation and host defense. Sci STKE. 2003; 2003: re3. doi: 10.1126/stke.2003.171.re3.
29. DeNardo DG, Coussens LM. Inflammation and breast cancer. Balancing immune response: crosstalk between adaptive and innate immune cells during breast cancer progression. Breast Cancer Res. 2007; 9:212. doi: 10.1186/bcr1746.
30. Zamai L, Ponti C, Mirandola P, Gobbi G, Papa S, Galeotti L, Cocco L, Vitale M. NK cells and cancer. J Immunol. 2007; 178:4011-6. doi: 6606.
31. Mahmoud SMA, Paish EC, Powe DG, Macmillan RD, Grainge MJ, Lee AHS, Ellis IO, Green AR. Tumor-Infiltrating CD8+ Lymphocytes Predict Clinical Outcome in Breast Cancer. J Clin Oncol OffJ Am Soc Clin Oncol. 2011; 29:1949-55. doi: 10.1200/JCO.2010.30.5037.
32. Mantovani A, Schioppa T, Porta C, Allavena P, Sica A. Role of tumor-associated macrophages in tumor progression and invasion. Cancer and Metastasis Reviews. 2006; 315-22. doi: 10.1007/s10555-006-9001-7.
33. Laoui D, Van Overmeire E, Conza G Di, Aldeni C, Keirsse J, Morias Y, Movahedi K, Houbracken I, Schouppe E, Elkrim Y, Karroum O, Jordan B, Carmeliet P, et al. Tumor hypoxia does not drive differentiation of tumor-associated macrophages but rather fine-tunes the M2-like macrophage population. Cancer Res. 2014; 74:24-30. doi: 10.1158/0008-5472.CAN-13-1196.
34. Stossi F, Madak-Erdogan Z, Katzenellenbogen BS. Macrophage-Elicited Loss of Estrogen Receptor Alpha in Breast Cancer Cells via Involvement of MAPK and c-Jun at the ESR1 Genomic Locus. Oncogene. 2012; 29:997-1003. doi: 10.1016/j.biotechadv.2011.08.021. Secreted.
35. Carmi Y, Dotan S, Rider P, Kaplanov I, White MR, Baron R, Abutbul S, Huszar M, Dinarello CA, Apte RN, Voronov E. The role of IL-1β in the early tumor cell-induced angiogenic response. J Immunol. 2013; 190:3500-9. doi: 10.4049/jimmunol.1202769.
36. Bindea G, Mlecnik B, Tosolini M, Kirilovsky A, Waldner M, Obenauf AC, Angell H, Fredriksen T, Lafontaine L, Berger A, Bruneval P, Fridman WH, Becker C, et al. Spatiotemporal Dynamics of Intratumoral Immune Cells Reveal the Immune Landscape in Human Cancer. Immunity. 2013; 39:782-95. doi: 10.1016/j.immuni.2013.10.003.
37. Gajewski TF, Schreiber H, Fu YX. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol. 2013; 14:1014-22. doi: 10.1038/ni.2703.
38. Gajewski TF. The Next Hurdle in Cancer Immunotherapy: Overcoming the Non-T-Cell-Inflamed Tumor Microenvironment. Semin Oncol. 2015; 42:663-71. doi: 10.1053/j.seminoncol.2015.05.011.
39. Harlin H, Meng Y, Peterson AC, Zha Y, Tretiakova M, SlingluffC, McKee M, Gajewski TF. Chemokine Expression in Melanoma Metastases Associated with CD8+ T-Cell Recruitment. Cancer Res. 2009; 69:3077-85. doi: 10.1158/0008-5472.CAN-08-2281.
40. Takeda K, Akira S. TLR signaling pathways. Seminars in Immunology. 2004; 3-9. doi: 10.1016/j.smim.2003.10.003.
41. Li D, Zhang X, Chen B. SIGIRR participates in negative regulation of LPS response and tolerance in human bladder epithelial cells. BMC Immunol. BioMed Central. 2015; 16: 73. doi: 10.1186/s12865-015-0137-5.
42. Swann JB, Hayakawa Y, Zerafa N, Sheehan KCF, Scott B, Schreiber RD, Hertzog P, Smyth MJ. Type I IFN contributes to NK cell homeostasis, activation, and antitumor function. J Immunol. 2007; 178:7540-9.
43. Sica A, Mantovani A. Macrophage plasticity and polarization: In vivo veritas. Journal of Clinical Investigation. 2012; 122:787-95. doi: 10.1172/JCI59643.
44. Fleetwood AJ, Dinh H, Cook AD, Hertzog PJ, Hamilton JA. GM-CSF-and M-CSF-dependent macrophage phenotypes display differential dependence on type I interferon signaling. J Leukoc Biol. 2009; 86:411-21. doi: 10.1189/jlb.1108702.
45. Ambrosino E, Spadaro M, Iezzi M, Curcio C, Forni G, Musiani P, Wei WZ, Cavallo F. Immunosurveillance of Erbb2 carcinogenesis in transgenic mice is concealed by a dominant regulatory T-cell self-tolerance. Cancer Res. 2006; 66:7734-40. doi: 10.1158/0008-5472.CAN-06-1432.
46. Rolla S, Ria F, Occhipinti S, Di Sante G, Iezzi M, Spadaro M, Nicolò C, Ambrosino E, Merighi IF, Musiani P, Forni G, Cavallo F. Erbb2 DNA vaccine combined with regulatory T cell deletion enhances antibody response and reveals latent low-avidity T cells: potential and limits of its therapeutic efficacy. J Immunol. 2010; 184:6124-32. doi: 10.4049/jimmunol.0901215.
47. Zhao J, Bulek K, Gulen MF, Zepp JA, Karagkounis G, Martin BN, Zhou H, Yu M, Liu X, Huang E, Fox PL, Kalady MF, Markowitz SD, et al. Human Colon Tumors Express a Dominant-Negative Form of SIGIRR That Promotes Inflammation and Colitis-Associated Colon Cancer in Mice. Gastroenterology. 2015; 149:1860-1871.e8. doi: 10.1053/j.gastro.2015.08.051.
48. Ruffell B, Affara NI, Coussens LM. Differential macrophage programming in the tumor microenvironment. Trends Immunol. 2012; 33:119-26. doi: 10.1016/j.it.2011.12.001.
49. Salcedo R, Cataisson C, Hasan U, Yuspa SH, Trinchieri G. MyD88 and its divergent toll in carcinogenesis. Trends Immunol. 2013; 34:379-89. doi: 10.1016/j.it.2013.03.008.
50. Bauman TM, Becka AJ, Sehgal PD, Huang W, Ricke WA. SIGIRR/TIR8, an important regulator of TLR4 and IL-1R-mediated NF-κB activation, predicts biochemical recurrence after prostatectomy in low-grade prostate carcinomas. Hum Pathol. 2015; 46:1744-51. doi: 10.1016/j.humpath.2015.07.015.
51. Lawrence T, Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol. 2011; 11:750-61. doi: 10.1038/nri3088.
52. Gajewski TF, Louahed J, Brichard VG. Gene signature in melanoma associated with clinical activity: a potential clue to unlock cancer immunotherapy. Cancer J. 2010; 16:399-403. doi: 10.1097/PPO.0b013e3181eacbd8.
53. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJM, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V, West AN, Carmona M, Kivork C, et al. PD-1 Blockade Induces Responses by Inhibiting Adaptive Immune Resistance. Nature. 2015; 515:568-71. doi: 10.1038/nature13954.PD-1.
54. Ji RR, Chasalow SD, Wang L, Hamid O, Schmidt H, Cogswell J, Alaparthy S, Berman D, Jure-Kunkel M, Siemers NO, Jackson JR, Shahabi V. An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol Immunother. 2012; 61:1019-31. doi: 10.1007/s00262-011-1172-6.
55. Burnette B, Fu YX, Weichselbaum RR. The confluence of radiotherapy and immunotherapy. Front Oncol. 2012; 2:1-8. doi: 10.3389/fonc.2012.00143.
56. Corrales L, Gajewski TF. Molecular pathways: Targeting the Stimulator of Interferon Genes (STING) in the immunotherapy of cancer. Clin Cancer Res. 2015; 21:4774-9. doi: 10.1158/1078-0432.CCR-15-1362.
57. Ciriello G, Gatza ML, Beck AH, Wilkerson MD, Rhie SK, Pastore A, Zhang H, McLellan M, Yau C, Kandoth C, Bowlby R, Shen H, Hayat S, et al. Comprehensive Molecular Portraits of Invasive Lobular Breast Cancer. Cell. 2015; 163:506-19. doi: 10.1016/j.cell.2015.09.033.