2,862
Views
3
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Immune suppressive function of IL-1α release in the tumor microenvironment regulated by calpain 1

, , , , , , , , , , & show all
Article: 2088467 | Received 24 Nov 2021, Accepted 07 Jun 2022, Published online: 15 Jun 2022

References

  • Dinarello CA. Overview of the IL-1 family in innate inflammation and acquired immunity. Immunol Rev. 2018;281(1):8–14. doi:10.1111/imr.12621.
  • Chiu JW, Binte Hanafi Z, Chew LCY, Mei Y, Liu H. IL-1alpha processing, signaling and its role in cancer progression. Cells. 2021;10(1):92. doi:10.3390/cells10010092.
  • Buryskova M, Pospisek M, Grothey A, Simmet T, Burysek L. Intracellular interleukin-1alpha functionally interacts with histone acetyltransferase complexes. J Biol Chem. 2004;279(6):4017–4026. doi:10.1074/jbc.M306342200.
  • Yano S, Banno T, Walsh R, Blumenberg M. Transcriptional responses of human epidermal keratinocytes to cytokine interleukin-1. J Cell Physiol. 2008;214(1):1–13. doi:10.1002/jcp.21300.
  • Brody DT, Durum SK. Membrane IL-1: IL-1 alpha precursor binds to the plasma membrane via a lectin-like interaction. J Immunol. 1989;143:1183–1187.
  • Lin D, Lei L, Liu Y, Zhang Y, Hu B, Bao G, Song Y, Jin Z, Liu C, Mei Y, et al. Membrane IL1alpha inhibits the development of hepatocellular carcinoma via promoting T- and NK-cell activation. Cancer Res. 2016;76(11):3179–3188. doi:10.1158/0008-5472.CAN-15-2658.
  • Afonina IS, Tynan GA, Logue SE, Cullen SP, Bots M, Luthi AU, Reeves EP, McElvaney NG, Medema JP, Lavelle EC, et al. Granzyme B-dependent proteolysis acts as a switch to enhance the proinflammatory activity of IL-1alpha. Mol Cell. 2011;44(2):265–278. doi:10.1016/j.molcel.2011.07.037.
  • Xu D, Mu R, Wei X. The roles of IL-1 family cytokines in the pathogenesis of systemic sclerosis. Front Immunol. 2019;10:2025. doi:10.3389/fimmu.2019.02025.
  • Rider P, Kaplanov I, Romzova M, Bernardis L, Braiman A, Voronov E, Apte RN. The transcription of the alarmin cytokine interleukin-1 alpha is controlled by hypoxia inducible factors 1 and 2 alpha in hypoxic cells. Front Immunol. 2012;3:290. doi:10.3389/fimmu.2012.00290.
  • Di Paolo NC, Shayakhmetov DM. Interleukin 1 alpha and the inflammatory process. Nat Immunol. 2016;17(8):906–913. doi:10.1038/ni.3503.
  • Thornton P, McColl BW, Greenhalgh A, Denes A, Allan SM, Rothwell NJ. Platelet interleukin-1alpha drives cerebrovascular inflammation. Blood. 2010;115(17):3632–3639. doi:10.1182/blood-2009-11-252643.
  • Dinarello CA, Ikejima T, Warner SJ, Orencole SF, Lonnemann G, Cannon JG, Libby P. Interleukin 1 induces interleukin 1. I. Induction of circulating interleukin 1 in rabbits in vivo and in human mononuclear cells in vitro. J Immunol. 1987;139:1902–1910.
  • Menghini P, Corridoni D, Butto LF, Osme A, Shivaswamy S, Lam M, Bamias G, Pizarro TT, Rodriguez-Palacios A, Dinarello CA, et al. 2019. Neutralization of IL-1alpha ameliorates Crohn’s disease-like ileitis by functional alterations of the gut microbiome. Proc Natl Acad Sci U S A. 116(52): 26717–26726.
  • Gabay C, Lamacchia C, Palmer G. IL-1 pathways in inflammation and human diseases. Nat Rev Rheumatol. 2010;6(4):232–241. doi:10.1038/nrrheum.2010.4.
  • Greten FR, Grivennikov SI. Inflammation and cancer: triggers, mechanisms, and consequences. Immunity. 2019;51(1):27–41. doi:10.1016/j.immuni.2019.06.025.
  • Xiao Z, Singh S, Singh M. Improving cancer immunotherapy by targeting IL-1. Oncoimmunology. 2021;10(1):2008111. doi:10.1080/2162402X.2021.2008111.
  • Leon X, Bothe C, Garcia J, Parreno M, Alcolea S, Quer M, Vila L, Camacho M. Expression of IL-1alpha correlates with distant metastasis in patients with head and neck squamous cell carcinoma. Oncotarget. 2015;6(35):37398–37409. doi:10.18632/oncotarget.6054.
  • Charbonneau B,MS, Block WR, Bamlet RA, Vierkant KR, Kalli Z, Fogarty DN, Rider TA, Sellers SS, Tworoger E, Poole HA, et al. Risk of ovarian cancer and the NF-κB pathway: genetic association with IL1A and TNFSF10. Cancer Res. 2014;74(3):852–861. doi:10.1158/0008-5472.CAN-13-1051.
  • Kuan EL, Ziegler SF. A tumor-myeloid cell axis, mediated via the cytokines IL-1alpha and TSLP, promotes the progression of breast cancer. Nat Immunol. 2018;19(4):366–374. doi:10.1038/s41590-018-0066-6.
  • Dvorkin T, Song X, Argov S, White RM, Zoller M, Segal S, Dinarello CA, Voronov E, Apte RN. Immune phenomena involved in the in vivo regression of fibrosarcoma cells expressing cell-associated IL-1alpha. J Leukoc Biol. 2006;80(1):96–106. doi:10.1189/jlb.0905509.
  • Song X, Voronov E, Dvorkin T, Fima E, Cagnano E, Benharroch D, Shendler Y, Bjorkdahl O, Segal S, Dinarello CA, et al. Differential effects of IL-1 alpha and IL-1 beta on tumorigenicity patterns and invasiveness. J Immunol. 2003;171(12):6448–6456. doi:10.4049/jimmunol.171.12.6448.
  • Voronov E, Weinstein Y, Benharroch D, Cagnano E, Ofir R, Dobkin M, White RM, Zoller M, Barak V, Segal S, et al. Antitumor and immunotherapeutic effects of activated invasive T lymphoma cells that display short-term interleukin 1alpha expression. Cancer Res. 1999;59:1029–1035.
  • Ben-Sasson SZ, Hogg A, Hu-Li J, Wingfield P, Chen X, Crank M, Caucheteux S, Ratner-Hurevich M, Berzofsky JA, Nir-Paz R, et al. IL-1 enhances expansion, effector function, tissue localization, and memory response of antigen-specific CD8 T cells. J Exp Med. 2013;210(3):491–502. doi:10.1084/jem.20122006.
  • Abdel-Wahab N, Safa H, Abudayyeh A, Johnson DH, Trinh VA, Zobniw CM, Lin H, Wong MK, Abdelrahim M, Gaber AO, et al. Checkpoint inhibitor therapy for cancer in solid organ transplantation recipients: an institutional experience and a systematic review of the literature. J Immunother Cancer. 2019;7(1):106. doi:10.1186/s40425-019-0585-1.
  • Smith MA, Schnellmann RG. Calpains, mitochondria, and apoptosis. Cardiovasc Res. 2012;96(1):32–37. doi:10.1093/cvr/cvs163.
  • Starling S. Innate immunity: revealing the secrets of IL-1 secretion. Nat Rev Immunol. 2017;18(1):2–3. doi:10.1038/nri.2017.155.
  • Hickish T, Andre T, Wyrwicz L, Saunders M, Sarosiek T, Kocsis J, Nemecek R, Rogowski W, Lesniewski-Kmak K, Petruzelka L, et al. MABp1 as a novel antibody treatment for advanced colorectal cancer: a randomised, double-blind, placebo-controlled, phase 3 study. Lancet Oncol. 2017;18(2):192–201. doi:10.1016/S1470-2045(17)30006-2.
  • Liu Y, Song Y, Lin D, Lei L, Mei Y, Jin Z, Gong H, Zhu Y, Hu B, Zhang Y, et al. NCR(-) group 3 innate lymphoid cells orchestrate IL-23/IL-17 axis to promote hepatocellular carcinoma development. EBioMedicine. 2019;41:333–344. doi:10.1016/j.ebiom.2019.02.050.
  • Hu B, Bao G, Zhang Y, Lin D, Wu Y, Wu D, Liu H. Donor NK Cells and IL-15 promoted engraftment in nonmyeloablative allogeneic bone marrow transplantation. The Journal of Immunology. 2012;189(4):1661–1670. doi:10.4049/jimmunol.1103199.
  • Lee CR, Kwak Y, Yang T, Han JH, Park SH, Ye MB, Lee W, Sim KY, Kang JA, Kim YC, et al. Myeloid-Derived suppressor cells are controlled by regulatory T cells via TGF-beta during murine colitis. Cell Rep. 2016;17(12):3219–3232. doi:10.1016/j.celrep.2016.11.062.
  • Suzuki E, Kapoor V, Jassar AS, Kaiser LR, Albelda SM. Gemcitabine selectively eliminates splenic Gr-1 + /CD11b + myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin Cancer Res. 2005;11(18):6713–6721. doi:10.1158/1078-0432.CCR-05-0883.
  • Veglia F, Sanseviero E, Gabrilovich DI. Myeloid-derived suppressor cells in the era of increasing myeloid cell diversity. Nat Rev Immunol. 2021;21(8):485–498. doi:10.1038/s41577-020-00490-y.
  • Lin D, Lei L, Zhang Y, Hu B, Bao G, Liu Y, Song Y, Liu C, Wu Y, Zhao L, et al. Secreted IL-1α promotes T-cell activation and expansion of CD11b + Gr1 + cells in carbon tetrachloride-induced liver injury in mice. Eur J Immunol. 2015;45(7):2084–2098. doi:10.1002/eji.201445195.
  • Newman AM, Steen CB, Liu CL, Gentles AJ, Chaudhuri AA, Scherer F, Khodadoust MS, Esfahani MS, Luca BA, Steiner D, et al. Determining cell type abundance and expression from bulk tissues with digital cytometry. Nat Biotechnol. 2019;37(7):773–782. doi:10.1038/s41587-019-0114-2.
  • Mantovani A, Barajon I, Garlanda C. IL-1 and IL-1 regulatory pathways in cancer progression and therapy. Immunol Rev. 2018;281(1):57–61. doi:10.1111/imr.12614.
  • Keenan BP, Fong L, Kelley RK. Immunotherapy in hepatocellular carcinoma: the complex interface between inflammation, fibrosis, and the immune response. J ImmunoTher Cancer. 2019;7(1):267. doi:10.1186/s40425-019-0749-z.
  • Refolo MG, Messa C, Guerra V, Carr BI, D’Alessandro R. Inflammatory mechanisms of HCC development. Cancers. 2020;12(3):641. doi:10.3390/cancers12030641.
  • Apte RN, Voronov E. Immunotherapeutic approaches of IL-1 neutralization in the tumor microenvironment. J Leukoc Biol. 2017;102(2):293–306. doi:10.1189/jlb.3MR1216-523R.
  • Gehrke N, Hovelmeyer N, Waisman A, Straub BK, Weinmann-Menke J, Worns MA, Galle PR, Schattenberg JM. Hepatocyte-specific deletion of IL1-RI attenuates liver injury by blocking IL-1 driven autoinflammation. J Hepatol. 2018;68(5):986–995. doi:10.1016/j.jhep.2018.01.008.
  • Kasprzak A, Zabel M, Wysocki J, Seidel J, Surdyk-Zasada J, Filipiak B. Expression of mRNA for cytokines (TNF-alpha and IL-1alpha) in human cytomegalovirus (HCMV) and hepatitis B virus (HBV) infections. Folia Histochemica Et Cytobiologica. 2002;40:63–68.
  • Steuerwald NM, Foureau DM, Norton HJ, Zhou J, Parsons JC, Chalasani N, Fontana RJ, Watkins PB, Lee WM, Reddy KR, et al. Profiles of serum cytokines in acute drug-induced liver injury and their prognostic significance. PloS one. 2013;8:e81974.
  • Olteanu S, Kandel-Kfir M, Shaish A, Almog T, Shemesh S, Barshack I, Apte RN, Harats D, Kamari Y. Lack of interleukin-1alpha in Kupffer cells attenuates liver inflammation and expression of inflammatory cytokines in hypercholesterolaemic mice. Digestive and Liver Disease: Official Journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver. 2014;46(5):433–439. doi:10.1016/j.dld.2014.01.156.
  • Kamari Y, Shaish A, Vax E, Shemesh S, Kandel-Kfir M, Arbel Y, Olteanu S, Barshack I, Dotan S, Voronov E, et al. Lack of interleukin-1alpha or interleukin-1beta inhibits transformation of steatosis to steatohepatitis and liver fibrosis in hypercholesterolemic mice. J Hepatol. 2011;55(5):1086–1094. doi:10.1016/j.jhep.2011.01.048.
  • Sakurai T, He G, Matsuzawa A, Yu GY, Maeda S, Hardiman G, Karin M. Hepatocyte necrosis induced by oxidative stress and IL-1 alpha release mediate carcinogen-induced compensatory proliferation and liver tumorigenesis. Cancer Cell. 2008;14(2):156–165. doi:10.1016/j.ccr.2008.06.016.
  • Zhang M, Liu L, Lin X, Wang Y, Li Y, Guo Q, Li S, Sun Y, Tao X, Zhang D, et al. A Translocation Pathway for Vesicle-Mediated Unconventional Protein Secretion. Cell. 2020;181(3):637–652 e615. doi:10.1016/j.cell.2020.03.031.
  • Tsuchiya K, Hosojima S, Hara H, Kushiyama H, Mahib MR, Kinoshita T, Suda T. Gasdermin D mediates the maturation and release of IL-1alpha downstream of inflammasomes. Cell Rep. 2021;34(12):108887. doi:10.1016/j.celrep.2021.108887.
  • Pietras EM, Mirantes-Barbeito C, Fong S, Loeffler D, Kovtonyuk LV, Zhang S, Lakshminarasimhan R, Chin CP, Techner JM, Will B, et al. Chronic interleukin-1 exposure drives haematopoietic stem cells towards precocious myeloid differentiation at the expense of self-renewal. Nat Cell Biol. 2016;18(6):607–618. doi:10.1038/ncb3346.
  • Law AMK, Valdes-Mora F, Gallego-Ortega D. Myeloid-Derived suppressor cells as a therapeutic target for cancer. Cells. 2020;9(3):561. doi:10.3390/cells9030561.
  • Lu LC, Chang CJ, Hsu CH. Targeting myeloid-derived suppressor cells in the treatment of hepatocellular carcinoma: current state and future perspectives. J Hepatocellular Carcinoma. 2019;6:71–84. doi:10.2147/JHC.S159693.
  • Afonina IS, Muller C, Martin SJ, Beyaert R. Proteolytic processing of interleukin-1 family cytokines: variations on a common theme. Immunity. 2015;42(6):991–1004. doi:10.1016/j.immuni.2015.06.003.
  • England H, Summersgill HR, Edye ME, Rothwell NJ, Brough D. Release of interleukin-1alpha or interleukin-1beta depends on mechanism of cell death. J Biol Chem. 2014;289(23):15942–15950. doi:10.1074/jbc.M114.557561.
  • Kimura Y, Koga H, Araki N, Mugita N, Fujita N, Takeshima H, Nishi T, Yamashima T, Saido TC, Yamasaki T, et al. The involvement of calpain-dependent proteolysis of the tumor suppressor NF2 (merlin) in schwannomas and meningiomas. Nat Med. 1998;4(8):915–922. doi:10.1038/nm0898-915.
  • Shapovalov I, Harper D, Greer PA. Calpain as a therapeutic target in cancer. Expert Opin Ther Targets. 2022;26(3):217–231. doi:10.1080/14728222.2022.2047178.
  • Ono Y, Saido TC, Sorimachi H. Calpain research for drug discovery: challenges and potential. Nat Rev Drug Discov. 2016;15(12):854–876. doi:10.1038/nrd.2016.212.