Ukr.Biochem.J. 2024; Том 96, № 6, листопад-грудень, c. 5-16

doi: https://doi.org/10.15407/ubj96.06.005

Біохімічні та клітинні механізми імуногенної загибелі клітин

М. Кліщ, Н. Скорохід, Р. Панчук, Р. Стойка*

Інститут біології клітини НАН України, Львів;
*e-mail: stoika@cellbiol.lviv.ua; stoika.rostyslav@gmail.com

Отримано: 21 квітня 2024; Виправлено: 11 вересня 2024;
Затверджено: 21 листопада 2024; Доступно онлайн: 17 грудня 2024

Імуногенна загибель клітин (ІЗК) – це режим запрограмованої клітинної загибелі, що призводить до активації протипухлинної імунної відповіді та визначає довгостроковий успіх протиракової терапії. Тут ми надаємо огляд відомих молекулярних і клітинних механізмів ІЗК. Зазвичай у дослідженнях ІЗК використовуються експериментальні моделі солідних пухлин. Проте моделі асцитних пухлин можуть мати деякі переваги перед ними. У статті наведено результати нашого дослідження з апробації мишачої лімфоми Немет-Келнера як експериментальної моделі асцитних пухлин для досліджень ІЗК.

Ключові слова: , , , , ,


Посилання:

  1. Serrano-Del Valle A, Anel A, Naval J, Marzo I. Immunogenic Cell Death and Immunotherapy of Multiple Myeloma. Front Cell Dev Biol. 2019;7:50. PubMed, PubMedCentral, CrossRef
  2. Fucikova J, Kepp O, Kasikova L, Petroni G, Yamazaki T, Liu P, Zhao L, Spisek R, Kroemer G, Galluzzi L. Detection of immunogenic cell death and its relevance for cancer therapy. Cell Death Dis. 2020;11(11):1013. PubMed, PubMedCentral, CrossRef
  3. Green DR, Ferguson T, Zitvogel L, Kroemer G. Immunogenic and tolerogenic cell death. Nat Rev Immunol. 2009;9(5):353-363. PubMed, PubMedCentral, CrossRef
  4. Galluzzi L, Buqué A, Kepp O, Zitvogel L, Kroemer G. Immunogenic cell death in cancer and infectious disease. Nat Rev Immunol. 2017;17(2):97-111. PubMed, CrossRef
  5. Choi M, Shin J, Lee CE, Chung JY, Kim M, Yan X, Yang WH, Cha JH. Immunogenic cell death in cancer immunotherapy. BMB Rep. 2023;56(5):275-286. PubMed, PubMedCentral, CrossRef
  6. Zhou J, Wang G, Chen Y, Wang H, Hua Y, Cai Z. Immunogenic cell death in cancer therapy: Present and emerging inducers. J Cell Mol Med. 2019;23(8):4854-4865. PubMed, PubMedCentral, CrossRef
  7. Rodriguez-Ruiz ME, Vitale I, Harrington KJ, Melero I, Galluzzi L. Immunological impact of cell death signaling driven by radiation on the tumor microenvironment. Nat Immunol. 2020;21(2):120-134. PubMed, CrossRef
  8. Tatsuno K, Yamazaki T, Hanlon D, Han P, Robinson E, Sobolev O, Yurter A, Rivera-Molina F, Arshad N, Edelson RL, Galluzzi L. Extracorporeal photochemotherapy induces bona fide immunogenic cell death. Cell Death Dis. 2019;10(8):578. PubMed, PubMedCentral, CrossRef
  9. Krombach J, Hennel R, Brix N, Orth M, Schoetz U, Ernst A, Schuster J, Zuchtriegel G, Reichel CA, Bierschenk S, Sperandio M, Vogl T, Unkel S, Belka C, Lauber K. Priming anti-tumor immunity by radiotherapy: Dying tumor cell-derived DAMPs trigger endothelial cell activation and recruitment of myeloid cells. Oncoimmunology. 2018;8(1):e1523097. PubMed, PubMedCentral, CrossRef
  10. Zitvogel L, Kepp O, Senovilla L, Menger L, Chaput N, Kroemer G. Immunogenic tumor cell death for optimal anticancer therapy: the calreticulin exposure pathway. Clin Cancer Res. 2010;16(12):3100-3104. PubMed, CrossRef
  11. Chen GY, Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol. 2010;10(12):826-837. PubMed, PubMedCentral, CrossRef
  12. Krysko DV, Garg AD, Kaczmarek A, Krysko O, Agostinis P, Vandenabeele P. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer. 2012 Dec;12(12):860-875. PubMed, CrossRef
  13. Fucikova J, Spisek R, Kroemer G, Galluzzi L. Calreticulin and cancer. Cell Res. 2021;31(1):5-16. PubMed, PubMedCentral, CrossRef
  14. Ahmed A, Tait SWG. Targeting immunogenic cell death in cancer. Mol Oncol. 2020;14(12):2994-3006. PubMed, PubMedCentral, CrossRef
  15. Liu Z, Xu X, Liu K, Zhang J, Ding D, Fu R. Immunogenic Cell Death in Hematological Malignancy Therapy. Adv Sci (Weinh). 2023;10(13):e2207475. PubMed, PubMedCentral, CrossRef
  16. Kazama H, Ricci JE, Herndon JM, Hoppe G, Green DR, Ferguson TA. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein. Immunity. 2008;29(1):21-32. PubMed, PubMedCentral, CrossRef
  17. Garg AD, Agostinis P. Cell death and immunity in cancer: From danger signals to mimicry of pathogen defense responses. Immunol Rev. 2017;280(1):126-148. PubMed, CrossRef
  18. Galluzzi L, Vitale I, Warren S, Adjemian S, Agostinis P, Martinez AB, Chan TA, Coukos G, Demaria S, Deutsch E. et al. Consensus guidelines for the definition, detection and interpretation of immunogenic cell death. J Immunother Cancer. 2020;8(1):e000337. PubMed, PubMedCentral, CrossRef
  19. Johnson S, Michalak M, Opas M, Eggleton P. The ins and outs of calreticulin: from the ER lumen to the extracellular space. Trends Cell Biol. 2001;11(3):122-129. PubMed, CrossRef
  20. Michalak M, Groenendyk J, Szabo E, Gold LI, Opas M. Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem J. 2009;417(3):651-666. PubMed, CrossRef
  21. Pandya UM, Egbuta C, Abdullah Norman TM, Chiang CE, Wiersma VR, Panchal RG, Bremer E, Eggleton P, Gold LI. The Biophysical Interaction of the Danger-Associated Molecular Pattern (DAMP) Calreticulin with the Pattern-Associated Molecular Pattern (PAMP) Lipopolysaccharide. Int J Mol Sci. 2019;20(2):408. PubMed, PubMedCentral, CrossRef
  22. Menger L, Vacchelli E, Adjemian S, Martins I, Ma Y, Shen S, Yamazaki T, Sukkurwala AQ, Michaud M, Mignot G, Schlemmer F, Sulpice E, Locher C, Gidrol X, Ghiringhelli F, Modjtahedi N, Galluzzi L, André F, Zitvogel L, Kepp O, Kroemer G. Cardiac glycosides exert anticancer effects by inducing immunogenic cell death. Sci Transl Med. 2012;4(143):143ra99. PubMed, CrossRef
  23. Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol. 2013;31:51-72. PubMed, CrossRef
  24. Schcolnik-Cabrera A, Oldak B, Juárez M, Cruz-Rivera M, Flisser A, Mendlovic F. Calreticulin in phagocytosis and cancer: opposite roles in immune response outcomes. Apoptosis. 2019;24(3-4):245-255. PubMed, CrossRef
  25. Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, Murphy-Ullrich JE, Bratton DL, Oldenborg PA, Michalak M, Henson PM. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell. 2005;123(2):321-334. PubMed, CrossRef
  26. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, Castedo M, Mignot G, Panaretakis T, Casares N, Métivier D, Larochette N, van Endert P, Ciccosanti F, Piacentini M, Zitvogel L, Kroemer G. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med. 2007;13(1):54-61. PubMed, CrossRef
  27. Panaretakis T, Kepp O, Brockmeier U, Tesniere A, Bjorklund AC, Chapman DC, Durchschlag M, Joza N, Pierron G, van Endert P, Yuan J, Zitvogel L, Madeo F, Williams DB, Kroemer G. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J. 2009;28(5):578-590. PubMed, PubMedCentral, CrossRef
  28. Byrne JC, Ní Gabhann J, Stacey KB, Coffey BM, McCarthy E, Thomas W, Jefferies CA. Bruton’s tyrosine kinase is required for apoptotic cell uptake via regulating the phosphorylation and localization of calreticulin. J Immunol. 2013;190(10):5207-5215. PubMed, CrossRef
  29. Fucikova J, Kasikova L, Truxova I, Laco J, Skapa P, Ryska A, Spisek R. Relevance of the chaperone-like protein calreticulin for the biological behavior and clinical outcome of cancer. Immunol Lett. 2018;193:25-34. PubMed, CrossRef
  30. Stoll G, Iribarren K, Michels J, Leary A, Zitvogel L, Cremer I, Kroemer G. Calreticulin expression: Interaction with the immune infiltrate and impact on survival in patients with ovarian and non-small cell lung cancer. Oncoimmunology. 2016;5(7):e1177692. PubMed, PubMedCentral, CrossRef
  31. Truxova I, Kasikova L, Salek C, Hensler M, Lysak D, Holicek P, Bilkova P, Holubova M, Chen X, Mikyskova R, Reinis M, Kovar M, Tomalova B, Kline JP, Galluzzi L, Spisek R, Fucikova J. Calreticulin exposure on malignant blasts correlates with improved natural killer cell-mediated cytotoxicity in acute myeloid leukemia patients. Haematologica. 2020;105(7):1868-1878. PubMed, PubMedCentral, CrossRef
  32. Müller S, Ronfani L, Bianchi ME. Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function. J Intern Med. 2004;255(3):332-343. PubMed, CrossRef
  33. Yang H, Wang H, Chavan SS, Andersson U. High Mobility Group Box Protein 1 (HMGB1): The Prototypical Endogenous Danger Molecule. Mol Med. 2015;21(Suppl 1):S6-S12. PubMed, PubMedCentral, CrossRef
  34. Zhu X, Messer JS, Wang Y, Lin F, Cham CM, Chang J, Billiar TR, Lotze MT, Boone DL, Chang EB. Cytosolic HMGB1 controls the cellular autophagy/apoptosis checkpoint during inflammation. J Clin Invest. 2015;125(3):1098-1110. PubMed, PubMedCentral, CrossRef
  35. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 2002;418(6894):191-195. PubMed, CrossRef
  36. Li L, Lu YQ. The Regulatory Role of High-Mobility Group Protein 1 in Sepsis-Related Immunity. Front Immunol. 2021;11:601815. PubMed, PubMedCentral, CrossRef
  37. Ge Y, Huang M, Yao YM. The Effect and Regulatory Mechanism of High Mobility Group Box-1 Protein on Immune Cells in Inflammatory Diseases. Cells. 2021;10(5):1044. PubMed, PubMedCentral, CrossRef
  38. Klune JR, Dhupar R, Cardinal J, Billiar TR, Tsung A. HMGB1: endogenous danger signaling. Mol Med. 2008;14(7-8):476-484. PubMed, PubMedCentral, CrossRef
  39. Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol. 2011;29:139-162. PubMed, PubMedCentral, CrossRef
  40. Venereau E, Casalgrandi M, Schiraldi M, Antoine DJ, Cattaneo A, De Marchis F, Liu J, Antonelli A, Preti A, Raeli L, Shams SS, Yang H, Varani L, Andersson U, Tracey KJ, Bachi A, Uguccioni M, Bianchi ME. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med. 2012;209(9):1519-1528. PubMed, PubMedCentral, CrossRef
  41. Galluzzi L, Aaronson SA, Abrams J, Alnemri ES, Andrews DW, Baehrecke EH, Bazan NG, Blagosklonny MV, Blomgren K, Borner C. et al. Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ. 2009;16(8):1093-1107. PubMed, PubMedCentral, CrossRef
  42. Bell CW, Jiang W, Reich CF 3rd, Pisetsky DS. The extracellular release of HMGB1 during apoptotic cell death. Am J Physiol Cell Physiol. 2006;291(6):C1318-C1325. PubMed, CrossRef
  43. ims GP, Rowe DC, Rietdijk ST, Herbst R, Coyle AJ. HMGB1 and RAGE in inflammation and cancer. Annu Rev Immunol. 2010;28:367-388. PubMed, CrossRef
  44. Gay NJ, Symmons MF, Gangloff M, Bryant CE. Assembly and localization of Toll-like receptor signalling complexes. Nat Rev Immunol. 2014;14(8):546-558. PubMed, CrossRef
  45. Vigneron C, Mirouse A, Merdji H, Rousseau C, Cousin C, Alby-Laurent F, Mira JP, Chiche JD, Llitjos JF, Pène F. Sepsis inhibits tumor growth in mice with cancer through Toll-like receptor 4-associated enhanced Natural Killer cell activity. Oncoimmunology. 2019;8(11):e1641391. PubMed, PubMedCentral, CrossRef
  46. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, Mignot G, Maiuri MC, Ullrich E, Saulnier P, Yang H. et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med. 2007;13(9):1050-1059. PubMed, CrossRef
  47. Saenz R, Futalan D, Leutenez L, Eekhout F, Fecteau JF, Sundelius S, Sundqvist S, Larsson M, Hayashi T, Minev B, Carson D, Esener S, Messmer B, Messmer D. TLR4-dependent activation of dendritic cells by an HMGB1-derived peptide adjuvant. J Transl Med. 2014;12:211. PubMed, PubMedCentral, CrossRef
  48. Nayagom B, Amara I, Habiballah M, Amrouche F, Beaune P, de Waziers I. Immunogenic cell death in a combined synergic gene- and immune-therapy against cancer. Oncoimmunology. 2019;8(12):e1667743. PubMed, PubMedCentral, CrossRef
  49. Martins I, Wang Y, Michaud M, Ma Y, Sukkurwala AQ, Shen S, Kepp O, Métivier D, Galluzzi L, Perfettini JL, Zitvogel L, Kroemer G. Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ. 2014;21(1):79-91. PubMed, PubMedCentral, CrossRef
  50. Garg AD, Dudek AM, Ferreira GB, Verfaillie T, Vandenabeele P, Krysko DV, Mathieu C, Agostinis P. ROS-induced autophagy in cancer cells assists in evasion from determinants of immunogenic cell death. Autophagy. 2013;9(9):1292-1307. PubMed, CrossRef
  51. Vénéreau E, Ceriotti C, Bianchi ME. DAMPs from Cell Death to New Life. Front Immunol. 2015;6:422. PubMed, PubMedCentral, CrossRef
  52. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev. 2007;87(2):659-797. PubMed, CrossRef
  53. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M, Sharma P, Lysiak JJ, Harden TK, Leitinger N, Ravichandran KS. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature. 2009;461(7261):282-286. PubMed, PubMedCentral, CrossRef
  54. Swanson KV, Deng M, Ting JP. The NLRP3 inflammasome: molecular activation and regulation to therapeutics. Nat Rev Immunol. 2019;19(8):477-489.  PubMed, PubMedCentral, CrossRef
  55.  Amores-Iniesta J, Barberà-Cremades M, Martínez CM, Pons JA, Revilla-Nuin B, Martínez-Alarcón L, Di Virgilio F, Parrilla P, Baroja-Mazo A, Pelegrín P. Extracellular ATP Activates the NLRP3 Inflammasome and Is an Early Danger Signal of Skin Allograft Rejection. Cell Rep. 2017;21(12):3414-3426. PubMed, PubMedCentral, CrossRef
  56. Ghiringhelli F, Apetoh L, Tesniere A, Aymeric L, Ma Y, Ortiz C, Vermaelen K, Panaretakis T, Mignot G, Ullrich E, Perfettini JL. et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med. 2009;15(10):1170-1178. PubMed, CrossRef
  57. Kepp O, Bezu L, Yamazaki T, Di Virgilio F, Smyth MJ, Kroemer G, Galluzzi L. ATP and cancer immunosurveillance. EMBO J. 2021;40(13):e108130. PubMed, PubMedCentral, CrossRef
  58. Ohta A, Sitkovsky M. Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage.
    Nature. 2001;414(6866):916-920. PubMed, CrossRef
  59. Stagg J, Beavis PA, Divisekera U, Liu MC, Möller A, Darcy PK, Smyth MJ. CD73-deficient mice are resistant to carcinogenesis. Cancer Res. 2012;72(9):2190-2196. PubMed, CrossRef
  60. Allard B, Allard D, Buisseret L, Stagg J. The adenosine pathway in immuno-oncology. Nat Rev Clin Oncol. 2020;17(10):611-629. PubMed, CrossRef
  61. Zitvogel L, Apetoh L, Ghiringhelli F, André F, Tesniere A, Kroemer G. The anticancer immune response: indispensable for therapeutic success? J Clin Invest. 2008;118(6):1991-2001. PubMed, PubMedCentral, CrossRef
  62. Zitvogel L, Kepp O, Kroemer G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol. 2011;8(3):151-160. PubMed, CrossRef
  63. West NR, Milne K, Truong PT, Macpherson N, Nelson BH, Watson PH. Tumor-infiltrating lymphocytes predict response to anthracycline-based chemotherapy in estrogen receptor-negative breast cancer. Breast Cancer Res. 2011;13(6):R126. PubMed, PubMedCentral, CrossRef
  64. Michaud M, Martins I, Sukkurwala AQ, Adjemian S, Ma Y, Pellegatti P, Shen S, Kepp O, Scoazec M, Mignot G, Rello-Varona S, Tailler M, Menger L, Vacchelli E, Galluzzi L, Ghiringhelli F, di Virgilio F, Zitvogel L, Kroemer G. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science. 2011;334(6062):1573-1577. PubMed, CrossRef
  65. Ma Y, Aymeric L, Locher C, Mattarollo SR, Delahaye NF, Pereira P, Boucontet L, Apetoh L, Ghiringhelli F, Casares N, Lasarte JJ, Matsuzaki G, Ikuta K, Ryffel B, Benlagha K, Tesnière A, Ibrahim N, Déchanet-Merville J, Chaput N, Smyth MJ, Kroemer G, Zitvogel L. Contribution of IL-17-producing gamma delta T cells to the efficacy of anticancer chemotherapy. J Exp Med. 2011;208(3):491-503. PubMed, PubMedCentral, CrossRef
  66. Ganassin R, Oliveira GRT, Oliveira da Rocha MC, Morais JAV, Rodrigues MC, Motta FN, Azevedo RB, Muehlmann LA. Curcumin induces immunogenic cell death in murine colorectal carcinoma CT26 cells. Pharmacol Res Modern Chinese Med. 2022;2:100046. CrossRef
  67. Lootsik MD, Lutsyk MM, Stoika RS. Nemeth-Kellner Lymphoma Is a Valid Experimental Model in Testing Chemical Agents for Anti-Lymphoproliferative Activity. Open J Blood Dis. 2013;3(3A):1-6. CrossRef

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License.