Доступ предоставлен для: Guest
Портал Begell Электронная Бибилиотека e-Книги Журналы Справочники и Сборники статей Коллекции
Critical Reviews™ in Immunology
Импакт фактор: 1.404 5-летний Импакт фактор: 3.347 SJR: 0.706 SNIP: 0.55 CiteScore™: 2.19

ISSN Печать: 1040-8401
ISSN Онлайн: 2162-6472

Выпуски:
Том 40, 2020 Том 39, 2019 Том 38, 2018 Том 37, 2017 Том 36, 2016 Том 35, 2015 Том 34, 2014 Том 33, 2013 Том 32, 2012 Том 31, 2011 Том 30, 2010 Том 29, 2009 Том 28, 2008 Том 27, 2007 Том 26, 2006 Том 25, 2005 Том 24, 2004 Том 23, 2003 Том 22, 2002 Том 21, 2001 Том 20, 2000 Том 19, 1999 Том 18, 1998 Том 17, 1997 Том 16, 1996 Том 15, 1995 Том 14, 1994

Critical Reviews™ in Immunology

DOI: 10.1615/CritRevImmunol.2020033492
pages 157-166

The Antitumor Cytotoxic Response: If the Killer Cells Play the Music, the Microenvironmental Hypoxia Plays the Tune

Salem Chouaib
UMR1186, Integrative Tumor Immunology and Genetic Oncology, Gustave Roussy, Equipe Labellisée par La Ligue Contre Le Cancer, EPHE, Faculté de Médecine, Université Paris-Sud, Université Paris-Saclay, Villejuif, France; Thumbay Research Institute for Precision Medicine Gulf Medical University, Ajman, UAE; P.O. Box 4184, Ajman, United Arab Emirates

Краткое описание

The immune system is a potent defense mechanism regulating tumor development and progression. However, immune cells are often functionally compromised in cancer patients, and tumor rejection does not follow successful induction of a CTL response. This is, in part, due to the existing conflict between the tumor system and an unfavorable tumor microenvironment (TME) that is able to neutralize or paralyze the immune system of the host. The recent advances in the field of immune checkpoint inhibitors have changed the focus from targeting the tumor to targeting T lymphocytes. It has been well established that the TME and associated multiple factors contribute to the failures in cancer therapies, including immunotherapy. In this regard, hypoxia, which is a hallmark of solid tumors, is strongly associated with advanced disease stages and poor clinical outcomes. Hypoxia plays a crucial role in tumor promotion and immune escape by conferring tumor resistance, immunosuppression, and tumor heterogeneity, which contribute to the generation of diverse cancer invasion programs and enhanced stroma plasticity. Tumor hypoxic stress interferes with the mesenchymal transition EMT, conferring to cancer cells a high degree of plasticity and the capacity to escape from immune surveillance. Tumors have been also shown to take advantage of hypoxic conditions that impede normal cells. Thus, tumor progression may be mediated by hypoxia-induced phenotypic changes and subsequent clonal selection of malignant cells that overexpress hypoxia-responsive molecules, such as HIF-1α. Currently, the resistance of tumor cells to cell-mediated cytotoxicity remains a drawback in the immunotherapy of cancer, and its molecular basis is poorly understood. In this review, I focus on hypoxia as a key process that evolved in the TME, and I discuss how solid tumors use hypoxic stress as a potent saboteur of the antitumor immune reaction by shaping a compromised cytotoxic cell function through the alteration of tumor target susceptibility to cell-mediated cytotoxicity. Exploiting hypoxia-associated tumor escape capacities may hold promise for attenuating tumor heterogeneity and plasticity, overcoming alteration of antitumor cytotoxic response and improving its effectiveness in cancer patients.

Ключевые слова: tumor plasticity, tumor resistance, cytotoxicity, hypoxia

ЛИТЕРАТУРА

  1. Rivoltini L, Restifo NP, Rosenberg SA, Marincola FM. Enhancement of cellular immunity in melanoma patients immunized with a peptide from MART-1/Melan A. Cancer J Sci Am. 1997;3(1):37-44. .

  2. Jorritsma A, Schumacher TNM, Haanen JBAG. Immuno-therapeutic strategies: The melanoma example. Immunotherapy. 2009 Jul;1(4):679-90. .

  3. Raez LE, Fein S, Podack ER. Lung cancer immunotherapy. Clin Med Res. 2005 Nov;3(4):221-8. .

  4. Yasumoto K, Hanagiri T, Takenoyama M. Lung cancer-associated tumor antigens and the present status of immunotherapy against non-small-cell lung cancer. Gen Thorac Cardiovasc Surg. 2009 Sep;57(9):449-57. .

  5. Chouaib S, Janji B, Tittarelli A, Eggermont A, Thiery JP. Tumor plasticity interferes with anti-tumor immunity. Crit Rev Immunol. 2014;34(2):91-102. .

  6. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nature Rev Cancer. 2012;12:252-64. .

  7. Kalbasi A, Ribas A. Tumour-intrinsic resistance to immune checkpoint blockade. Nature Rev Immunol. 2020;20:25-39. .

  8. Brahmer JR, Tykodi SS, Chow LQM, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, Pitot HC, Hamid O, Bhatia S, Martins R, Eaton K, Chen S, Salay TM, Alaparthy S, Grosso JF, Korman AJ, Parker SM, Agrawal S, Goldberg SM, Pardoll DM, Gupta A, Wigginton JM. Safety and activity of anti-PD-Ll antibody in patients with advanced cancer. N Engl J Med. 2012 Jun 28;366(26):2455-65. .

  9. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, Leming PD, Spigel DR, Antonia SJ, Horn L, Drake CG, Pardoll DM, Chen L, Sharfman WH, Anders RA, Taube JM, McMiller TL, Xu H, Korman AJ, Jure-Kunkel M, Agrawal S, McDonald D, Kollia GD, Gupta A, Wigginton JM, Sznol M. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012 Jun 28;366(26):2443-54. .

  10. Laconi E. The evolving concept of tumor microenvironments. Bioessays. 2007 Aug;29(8):738-44. .

  11. Harris AL. Hypoxia-A key regulatory factor in tumour growth. Nat Rev Cancer. 2002;2:38-47. .

  12. Jain RK. Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science. 2005; 307:58-62. .

  13. Noman MZ, Messai Y, Carre T, Akalay I, Meron M, Janji B, Hasmim M, Chouaib S. Microenvironmental hypoxia orchestrating the cell stroma cross talk, tumor progression and antitumor response. Crit Rev Immunol. 2011;31(5):357-77. .

  14. Facciabene A, Peng X, Hagemann IS, Balint K, Barchetti A, Wang L-P, Gimotty PA, Gilks CB, Lal P, Zhang L, Coukos G. Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature. 2011 Jul 13;475(7355):226-30. .

  15. Hasmim M, Noman MZ, Messai Y, Bordereaux D, Gros G, Baud V, Chouaib S. Cutting edge: Hypoxia-induced Nanog favors the intratumoral infiltration of regulatory T cells and macrophages via direct regulation of TGF-pi. J Immunol. 2013 Dec 15;191(12):5802-6. .

  16. Noman MZ, Desantis G, Janji B, Hasmim M, Karray S, Dessen P, Bronte V, Chouaib S. PD-L1 is a novel direct target of HIF-la, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med. 2014 May 5;211(5):781-90. .

  17. Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell. 2007;129:465-72. .

  18. Chouaib S, Messai Y, Couve S, Escudier B, Hasmim M, Noman MZ. Hypoxia promotes tumor growth in linking angiogenesis to immune escape. Front Immunol. 2012; 3:21. .

  19. Chouaib S, Noman MZ, Kosmatopoulos K, Curran MA. Hypoxic stress: Obstacles and opportunities for innovative immunotherapy of cancer. Oncogene. 2017 Jan 26;36(4):439-45. .

  20. Noman MZ, Buart S, Van Pelt J, Richon C, Hasmim M, Leleu N, Suchorska WM, Jalil A, Lecluse Y, El Hage F, Giuliani M, Pichon C, Azzarone B, Mazure N, Romero P, Mami-Chouaib F, Chouaib S. The cooperative induction of hypoxia-inducible factor-1 alpha and STAT3 during hypoxia induced an impairment of tumor susceptibility to CTL-mediated cell lysis. J Immunol. 2009 Mar 15;182(6):3510-21. .

  21. Noman MZ, Janji B, Kaminska B, Van Moer K, Pierson S, Przanowski P, Buart S, Berchem G, Romero P, Mami-Chouaib F, Chouaib S. Blocking hypoxia-induced autophagy in tumors restores cytotoxic T-cell activity and promotes regression. Cancer Res. 2011 Sep 15;71(18):5976-86. .

  22. Noman MZ, Buart S, Romero P, Ketari S, Janji B, Mari B, Mami-Chouaib F, Chouaib S. Hypoxia-inducible miR-210 regulates the susceptibility of tumor cells to lysis by cytotoxic T cells. Cancer Res. 2012 Sep 15;72(18):4629-41. .

  23. Hasmim M, Noman MZ, Lauriol J, Benlalam H, Mallavialle A, Rosselli F, Mami-Chouaib F, Alcaide-Loridan C, Chouaib S. Hypoxia-dependent inhibition of tumor cell susceptibility to CTL-mediated lysis involves NANOG induction in target cells. J Immunol. 2011 Oct 15;187(8):4031-39. .

  24. Hasmim M, Janji B, Khaled M, Noman MZ, Louache F, Bordereaux D, Abderamane A, Baud V, Mami-Chouaib F, Chouaib S. Cutting edge: NANOG activates autophagy under hypoxic stress by binding to BNIP3L promoter. J Immunol. 2017;198(4):1423-28. .

  25. Farag SS, Fehniger TA, Ruggeri L, Velardi A, Caligiuri MA. Natural killer cell receptors: New biology and insights into the graft-versus-leukemia effect. Blood. 2002 Sep 15;100(6):1935-47. .

  26. Moretta L, Montaldo E, Vacca P, Del Zotto G, Moretta F, Merli P, Locatelli F, Mingari MC. Human natural killer cells: Origin, receptors, function, and clinical applications. Int Arch Allergy Immunol. 2014;164(4):253-64. .

  27. Parodi M, Raggi F, Cangelosi D, Manzini C, Balsamo M, Blengio F, Eva A, Varesio L, Pietra G, Moretta L, Mingari MC, Vitale M, Bosco MC. Hypoxia modifies the transcriptome of human NK cells, modulates their immunoregulatory profile, and influences NK cell subset migration. Front Immunol. 2018;9:2358. .

  28. Sarkar S, Germeraad WTV, Rouschop KMA, Steeghs EMP, van Gelder M, Bos GMJ, Wieten L. Hypoxia induced impairment of NK cell cytotoxicity against multiple myeloma can be overcome by IL-2 activation of the NK cells. PLoS One. 2013;8(5):e64835. .

  29. Krzywinska E, Kantari-Mimoun C, Kerdiles Y, Sobecki M, Isagawa T, Gotthardt D, Castells M, Haubold J, Millien C, Viel T, Tavitian B, Takeda N, Fandrey J, Vivier E, Sexl V, Stockmann C. Loss of HIF-1a in natural killer cells inhibits tumour growth by stimulating non-productive angiogenesis. Nat Commun. 2017;8(1):1597. .

  30. Ou Z-L, Luo Z, Wei W, Liang S, Gao T-L, Lu Y-B. Hypoxia-induced shedding of MICA and HIF1A-mediated immune escape of pancreatic cancer cells from NK cells: Role of circ_0000977/miR-153 axis. RNA Biol. 2019;16(11):1592-603. .

  31. Sufan RI, Jewett MAS, Ohh M. The role of von Hippel-Lindau tumor suppressor protein and hypoxia in renal clear cell carcinoma. Am J Physiol Renal Physiol. 2004 Jul;287(1):F1-6. .

  32. Kaelin WG. The von Hippel-Lindau tumor suppressor protein and clear cell renal carcinoma. Clin Cancer Res. 2007 Jan 15;13(2):680s-684s. .

  33. Messai Y, Noman MZ, Hasmim M, Janji B, Tittarelli A, Boutet M, Baud V, Viry E, Billot K, Nanbakhsh A, Ben Safta T, Richon C, Ferlicot S, Donnadieu E, Couve S, Gardie B, Orlanducci F, Albiges L, Thiery J, Olive D, Escudier B, Chouaib S. ITPR1 protects renal cancer cells against natural killer cells by inducing autophagy. Cancer Res. 2014 Dec 1;74(23):6820-32. .

  34. Chouaib S, Janji B, Tittarelli A, Eggermont A, Thiery JP. Tumor plasticity interferes with anti-tumor immunity. Crit Rev Immunol. 2014;34(2):91-102. .

  35. Abouzahr S, Bismuth G, Gaudin C, Caroll O, Van Endert P, Jalil A, Dausset J, Vergnon I, Richon C, Kauffmann A, Galon J, Raposo G, Mami-Chouaib F, Chouaib S. Identification of target actin content and polymerization status as a mechanism of tumor resistance after cytolytic T lymphocyte pressure. Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1428-33. .

  36. Hamai A, Meslin F, Benlalam H, Jalil A, Mehrpour M, Faure F, Lecluse Y, Vielh P, Avril M-F, Robert C, Chouaib S. ICAM-1 has a critical role in the regulation of meta-static melanoma tumor susceptibility to CTL lysis by interfering with PI3K/AKT pathway. Cancer Res. 2008 Dec 1;68(23):9854-64. .

  37. Akalay I, Janji B, Hasmim M, Noman MZ, Andre F, De Cremoux P, Bertheau P, Badoual C, Vielh P, Larsen AK, Sabbah M, Tan TZ, Keira JH, Hung NTY, Thiery JP, Mami-Chouaib F, Chouaib S. Epithelial-to-mesenchymal transition and autophagy induction in breast carcinoma promote escape from T-cell-mediated lysis. Cancer Res. 2013 Apr 15;73(8):2418-27. .

  38. Akalay I, Tan TZ, Kumar P, Janji B, Mami-Chouaib F, Charpy C, Vielh P, Larsen AK, Thiery JP, Sabbah M, Chouaib S. Targeting WNT1-inducible signaling pathway protein 2 alters human breast cancer cell susceptibility to specific lysis through regulation of KLF-4 and miR-7 ex-pression. Oncogene. 2015 Apr 23;34(17):2261-71. .

  39. Yuan S, Norgard RJ, Stanger BZ. Cellular plasticity in cancer. Cancer Discovery. 2019;9(7):837-51. .

  40. Terry S, Faouzi Zaarour R, Hassan Venkatesh G, Francis A, El-Sayed W, Buart S, Bravo P, Thiery J, Chouaib S. Role of hypoxic stress in regulating tumor immunogenicity, resis-tance and plasticity. Int J Mol Sci. 2018 Oct 6;19(10). .

  41. Terry S, Savagner P, Ortiz-Cuaran S, Mahjoubi L, Saintigny P, Thiery JP, Chouaib S. New insights into the role of EMT in tumor immune escape. Mol Oncol. 2017 Jul;11(7):824-46. .

  42. Akalay I, Janji B, Hasmim M, Noman MZ, Andre F, De Cremoux P, Bertheau P, Badoual C, Vielh P, Larsen AK, Sabbah M, Tan TZ, Keira JH, Hung NTY, Thiery JP, Mami-Chouaib F, Chouaib S. Epithelial-to-mesenchymal transition and autophagy induction in breast carcinoma promote escape from T-cell-mediated lysis. Cancer Res. 2013 Apr 15;73(8):2418-27. .

  43. DongreA, Rashidian M, Reinhardt F, BagnatoA, Keckesova Z, Ploegh HL, Weinberg RA. Epithelial-to-mesenchymal transition contributes to immunosuppression in breast carcinomas. Cancer Res. 2017 Aug 1;77(15):3982-89. .

  44. Noman MZ, Janji B, Abdou A, Hasmim M, Terry S, Tan TZ, Mami-Chouaib F, Thiery JP, Chouaib S. The immune checkpoint ligand PD-L1 is upregulated in EMT-activated human breast cancer cells by a mechanism involving ZEB-1 and miR-200. Oncoimmunology. 2017;6(1):e1263412. .

  45. MacFawn I, Wilson H, Selth LA, Leighton I, Serebriiskii I, Bleackley RC, Elzamzamy O, Farris J, Pifer PM, Richer J, Frisch SM. Grainyhead-like-2 confers NK-sensitivity through interactions with epigenetic modifiers. Mol Immunol. 2019;105:137-49. .

  46. Terry S, Buart S, Tan TZ, Gros G, Noman MZ, Lorens JB, Mami-Chouaib F, Thiery JP, Chouaib S. Acquisition of tumor cell phenotypic diversity along the EMT spectrum under hypoxic pressure: Consequences on susceptibility to cell-mediated cytotoxicity. Oncoimmunology. 2017;6(2):e1271858. .

  47. Palena C, Polev DE, Tsang KY, Fernando RI, Litzinger M, Krukovskaya LL, Baranova AV, Kozlov AP, Schlom J. The human T-box mesodermal transcription factor Brachyury is a candidate target for T-cell-mediated cancer immunotherapy. Clin Cancer Res. 2007;13(8):2471-78. .

  48. Terry S, Abdou A, Engelsen AST, Buart S, Dessen P, Corgnac S, Collares D, Meurice G, Gausdal G, Baud V, Saintigny P, Lorens JB, Thiery J-P, Mami-Chouaib F, Chouaib S. AXL targeting overcomes human lung cancer cell resistance to NK- and CTL-mediated cytotoxicity. Cancer Immunol Res. 2019;7(11):1789-802. .

  49. Khouzam RA, Hassan GV, Zaarour RF, Chamseddine NA, Amirtharaj F, Buart S, Terry S, Chouaib S. Integrating tumor hypoxic stress in novel and more adaptable strategies for cancer immunotherapy. Seminar Cancer Biol. 2020. In press. .

  50. Jayaprakash P, Ai M, Liu A, Budhani P, Bartkowiak T, Sheng J, Ager C, Nicholas C, Jaiswal AR, Sun Y, Shah K, Balasubramanyam S, Li N, Wang G, Ning J, Zal A, Zal T, Curran MA. Targeted hypoxia reduction restores T cell in-filtration and sensitizes prostate cancer to immunotherapy. J Clin Invest. 2018;128(11):5137-49. .


Articles with similar content:

Microenvironmental Hypoxia Orchestrating the Cell Stroma Cross Talk, Tumor Progression and Antitumor Response
Critical Reviews™ in Immunology, Vol.31, 2011, issue 5
Muhammad Zaeem Noman, Yosra Messai, Thibault Carre, Salem Chouaib, Bassam Janji, Meriem Hasmim, Intissar Akalay, Marine Meron
Tumor Hypoxia: A Key Determinant of Microenvironment Hostility and a Major Checkpoint during the Antitumor Response
Critical Reviews™ in Immunology, Vol.38, 2018, issue 6
Hussam H. Nawafleh, Stéphanie Buart, Rania Faouzi Zaarour, Stéphane Terry, Amirtharaj Francis, Prathibha Prasad, Nagwa Ahmed Zeinelabdin, Salem Chouaib, Goutham Hassan Venkatesh
Back to the Light Side: The Role of Mechanotransduction in the Paradoxical Response to Checkpoint Inhibitors in Cancer Patients
Critical Reviews™ in Immunology, Vol.39, 2019, issue 3
Eslam Abbas, Tamer Z. Salem
The ABL Genes in Normal and Abnormal Cell Development
Critical Reviews™ in Oncogenesis, Vol.7, 1996, issue 1-2
Siu-Wah Chung, Bryan Y. Wong, Rene Daniel, Peter M. C. Wong
Targeting the Overexpressed YY1 in Cancer Inhibits EMT and Metastasis
Critical Reviews™ in Oncogenesis, Vol.22, 2017, issue 1-2
Anne Arah Cho, Benjamin Bonavida