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Onco Therapeutics

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Hypoxia as a Potential Inducer of Immune Tolerance and a Driver of Tumor Mutational Burden: Impact on Cancer Immunotherapy

Volume 8, Edição 1, 2021, pp. 1-9
DOI: 10.1615/ForumImmunDisTher.2021041436
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Salem Chouaib
Thumbay Research Institute for Precision Medicine, Gulf Medical University, Ajman-4184, United Arab Emirates; INSERM UMR 1186, Integrative Tumor Immunology and Immunotherapy, Gustave Roussy, Faculty of Medicine, University Paris-Saclay, Research Building 1, 114, rue Vaillant Couturier, Villejuif F-94805, France

RESUMO

In cancer patients, immune cells are often functionally compromised due to the immunosuppressive features of the tumor microenvironment (TME) which contributes to the failures in cancer therapies, including immunotherapy. Targeting immune systems can benefit patients across a wide range of tumors and immune checkpoint blockers drive current revolution in immunotherapy across multiple tumor types. Nevertheless, most cancer patients do not respond, and the determinants of response and resistance are not well understood. To survive, developing tumors adapt to the immunological environment and create a local microenvironment that inhibits immune function by inducing immune tolerance and invasion. The TME is an integral part of tumor physiology that nurtures the malignant process. In this context, microenvironmental hypoxia, which is a hallmark of solid tumors, may result in pleiotropic effects contributing significantly to tumor aggressiveness and therapy resistance. It controls tumor resistance and plasticity and promotes the differentiation and expansion of immune-suppressive stromal cells. More importantly, hypoxia also drives genomic instability in cancer cells, and it may hinder the DNA damage response and DNA repair. Recent advances place hypoxia as a potential driver of tumor mutational burden. Here, we review the current knowledge on how hypoxic stress in the TME impacts on the tumor heterogeneity, plasticity and immune resistance, with a special interest in tumor immunogenicity. A detailed and integrated understanding of the dual effect of hypoxia might lead to innovative approaches for accurately exploiting hypoxia-associated pathways in the clinical setting.

Palavras-chave: hypoxic stress, antitumor immunity, immune evasion, tumor immunogenicity
Referências

  1. Vaupel P. Tumor microenvironmental physiology and its implications for radiation oncology. Semin Radiat Oncol. 2004;14(3):198-206.

  2. Schwartz DL, Powis G, Thitai-Kumar A, He Y, Bankson J, Williams R, Lemos R, Oh J, Volgin A, Soghomonyan S, Nishii R, Alauddin M, Mukhopadhay U, Peng Z, Bornmann W, Gelovani J. The selective hypoxia inducible factor-1 inhibitor PX-478 provides in vivo radiosensitization through tumor stromal effects. Mol Cancer Ther. 2009;8(4):947-58.

  3. Dengler VL, Galbraith M, Espinosa JM. Transcriptional regulation by hypoxia inducible factors. Crit Rev Biochem Mol Biol. 2014;49(1):1-15.

  4. Cao J, Li J, Sun L, Qin T, Xiao Y, Chen K, Qian W, Duan W, Lei J, Ma J, Ma Q, Han L. Hypoxia-driven paracrine osteopontin/integrin avp3 signaling promotes pancreatic cancer cell epithelial-mesenchymal transition and cancer stem cell-like properties by modulating forkhead box protein M1. Mol Oncol. 2019;13(2):228-45.

  5. Rathmell WK, Chen S. VHL inactivation in renal cell carcinoma: Implications for diagnosis, prognosis and treatment. Expert Rev Anticancer Ther. 2008;8(1):63-73.

  6. 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;182(6):3510-21.

  7. Baginska J, Viry E, Berchem G, Poli A, Noman MZ, van Moer K, Medves S, Zimmer J, Oudin A, Niclou SP, Bleackley RC, Goping IS, Chouaib S, Janji B. Granzyme B degradation by autophagy decreases tumor cell susceptibility to natural killer-mediated lysis under hypoxia. Proc Natl Acad Sci U S A. 2013;110(43):17450-5.

  8. Scanlon SE, Glazer PM. Multifaceted control of DNA repair pathways by the hypoxic tumor microenvironment. DNA Repair. 2015;32:180-9.

  9. Luoto KR, Kumareswaran R, Bristow RG. Tumor hypoxia as a driving force in genetic instability. Genome Integr. 2013;4(1):5.

  10. Anderson KG, Stromnes IM, Greenberg PD. Obstacles posed by the tumor microenvironment to T cell activity: A case for synergistic therapies. Cancer Cell. 2017;31(3):311-25.

  11. Noman MZ, Hasmim M, Messai Y, Terry S, Kieda C, Janji B, Chouaib S. Hypoxia: A key player in antitumor immune response. a review in the theme: Cellular responses to hypoxia. Am J Physiol Cell Physiol. 2015;309(9):C569-79.

  12. Vaupel P, Mayer A. Hypoxia in cancer: Significance and impact on clinical outcome. Cancer Metastasis Rev. 2007;26(2):225-39.

  13. 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;11(7):824-46.

  14. Williams ED, Gao D, Redfern A, Thompson EW. Contro-versies around epithelial-mesenchymal plasticity in cancer metastasis. Nat Rev Cancer. 2019;19(12):716-32.

  15. Chen X, Iliopoulos D, Zhang Q, Tang Q, Greenblatt MB, Hatziapostolou M, Lim E, Tam WL, Ni M, Chen Y, Mai J, Shen H, Hu DZ, Adoro S, Hu B, Song M, Tan C, Landis MD, Ferrari M, Shin SJ, Brown M, Chang JC, Liu XS, Glimcher LH. XBP1 promotes triple-negative breast cancer by controlling the HIFla pathway. Nature. 2014;508(7494):103-7.

  16. Zhou J, Huang S, Wang L, Yuan X, Dong Q, Zhang D, Wang X. Clinical and prognostic significance of HIF-1a overexpression in oral squamous cell carcinoma: A meta-analysis. World J Surg Oncol. 2017;15(1):104.

  17. Buart S, Terry S, Noman MZ, Lanoy E, Boutros C, Fogel P, Dessen P, Meurice G, Gaston-Mathe Y, Vielh P, Roy S, Routier E, Marty V, Ferlicot S, Legres L, Bouchtaoui ME, Kamsu-Kom N, Muret J, Deutsch E, Eggermont A, Soria JC, Robert C, Chouaib S. Transcriptional response to hypoxic stress in melanoma and prognostic potential of GBE1 and BNIP3. Oncotarget. 2017;8(65):108786-801.

  18. LaGory EL, Giaccia AJ. The ever-expanding role of HIF in tumour and stromal biology. Nat Cell Biol. 2016;18(4):356-65.

  19. Yang MH, Wu MZ, Chiou SH, Chen PM, Chang SY, Liu CJ, Teng SC, Wu KJ. Direct regulation of TWIST by HIF-1 alpha promotes metastasis. Nat Cell Biol. 2008;10(3):295-305.

  20. Wong CC, Gilkes DM, Zhang H, Chen J, Wei H, Chaturvedi P, Fraley SI, Wong CM, Khoo US, Ng IO, Wirtz D, Semenza GL. Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc Natl Acad Sci U S A. 2011;108(39):16369-74.

  21. Liao D, Corle C, Seagroves TN, Johnson RS. Hypoxia-inducible factor-1alpha is a key regulator of metastasis in a transgenic model of cancer initiation and progression. Cancer Res. 2007;67(2):563-72.

  22. Semenza GL. Hypoxia-inducible factors: Mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci. 2012;33(4):207-14.

  23. Lee CT, Mace T, Repasky EA. Hypoxia-driven immunosuppression: A new reason to use thermal therapy in the treatment of cancer? Int J Hyperthermia. 2010; 26(3):232-46.

  24. 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;191(12):5802-6.

  25. 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.

  26. 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;182(6):3510-21.

  27. Hasmim M, Noman MZ, Lauriol J, Benlalam H, Malla-vialle 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;187(8): 4031-9.

  28. 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 NT, 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;73(8):2418-27.

  29. Baginska J, Viry E, Berchem G, Poli A, Noman MZ, van Moer K, Medves S, Zimmer J, Oudin A, Niclou SP, Bleackley RC, Goping IS, Chouaib S, Janji B. Granzyme B degradation by autophagy decreases tumor cell susceptibility to natural killer-mediated lysis under hypoxia. Proc Natl Acad Sci U S A. 2013;110(43):17450-5.

  30. Sitkovsky MV, Lukashev D, Apasov S, Kojima H, Koshiba M, Caldwell C, Ohta A, Thiel M. Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu Rev Immunol. 2004;22:657-82.

  31. Hoskin DW, Mader JS, Furlong SJ, Conrad DM, Blay J. Inhibition of T cell and natural killer cell function by adenosine and its contribution to immune evasion by tumor cells. Int J Oncol. 2008;32(3):527-35.

  32. Sitkovsky MV, Kjaergaard J, Lukashev D, Ohta A. Hypoxia-adenosinergic immunosuppression: Tumor protection by T regulatory cells and cancerous tissue hypoxia. Clin Cancer Res. 2008;14(19):5947-52.

  33. Hielscher A, Gerecht S. Hypoxia and free radicals: Role in tumor progression and the use of engineering-based platforms to address these relationships. Free Radic Biol Med. 2015;79:281-91.

  34. Kasic T, Colombo P, Soldani C, Wang CM, Miranda E, Roncalli M, Bronte V, Viola A. Modulation of human T-cell functions by reactive nitrogen species. Eur J Immunol. 2011;41(7):1843-9.

  35. da Silva-Diz V, Lorenzo-Sanz L, Bernat-Peguera A, Lopez-Cerda M, Munoz P. Cancer cell plasticity: Impact on tumor progression and therapy response. Semin Cancer Biol. 2018;53:48-58.

  36. Nieto MA, Huang RY, Jackson RA, Thiery JP. EMT: 2016. Cell. 2016;166(1):21-45.

  37. Byles V, Zhu L, Lovaas JD, Chmilewski LK, Wang J, Faller DV, Dai Y. SIRT1 induces EMT by cooperating with EMT transcription factors and enhances prostate cancer cell migration and metastasis. Oncogene. 2012;31(43): 4619-29.

  38. Balamurugan K. HIF-1 at the crossroads ofhypoxia, inflammation, and cancer. Int J Cancer. 2016;138(5):1058-66.

  39. Tsubaki M, Komai M, Fujimoto S, Itoh T, Imano M, Sakamoto K, Shimaoka H, Takeda T, Ogawa N, Mashimo K, Fujiwara D, Mukai J, Sakaguchi K, Satou T, Nishida S. Activation of NF-KB by the RANKL/RANK system up-regulates snail and twist expressions and induces epithelial-to-mesenchymal transition in mammary tumor cell lines. J Exp Clin Cancer Res. 2013;32(1):62.

  40. Paolicchi E, Gemignani F, Krstic-Demonacos M, Dedhar S, Mutti L, Landi S. Targeting hypoxic response for cancer therapy. Oncotarget. 2016;7(12):13464-78.

  41. 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.

  42. Yang MH, Wu KJ. TWIST activation by hypoxia inducible factor-1 (HIF-1): Implications in metastasis and de-velopment. Cell Cycle. 2008;7(14):2090-6.

  43. Hotz B, Arndt M, Dullat S, Bhargava S, Buhr HJ, Hotz HG. Epithelial to mesenchymal transition: Expression of the regulators snail, slug, and twist in pancreatic cancer. Clin Cancer Res. 2007;13(16):4769-76.

  44. Zhang H, Lu H, Xiang L, Bullen JW, Zhang C, Samanta D, Gilkes DM, He J, Semenza GL. HIF-1 regulates CD47 expression in breast cancer cells to promote evasion of phagocytosis and maintenance of cancer stem cells. Proc Natl Acad Sci U S A. 2015;112(45):E6215-23.

  45. Noman MZ, Van Moer K, Marani V, Gemmill RM, Tranchevent LC, Azuaje F, Muller A, Chouaib S, Thiery JP, Berchem G, Janji B. CD47 is a direct target of SNAI1 and ZEB1 and its blockade activates the phagocytosis of breast cancer cells undergoing EMT. Oncoimmunology. 2018;7(4):e1345415.

  46. Luoto KR, Kumareswaran R, Bristow RG. Tumor hypoxia as a driving force in genetic instability. Genome Integr. 2013;4(1):5.

  47. Bristow RG, Hill RP. Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer. 2008;8(3):180-92.

  48. Bindra RS, Crosby ME, Glazer PM. Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Rev. 2007;26(2):249-60.

  49. Luoto KR, Kumareswaran R, Bristow RG. Tumor hypoxia as a driving force in genetic instability. Genome Integr. 2013;4(1):5.

  50. Tang M, Bolderson E, O'Byrne KJ, Richard DJ. Tumor hypoxia drives genomic instability. Front Cell Dev Biol. 2021;9:626229.

  51. Hassan Venkatesh G, Bravo P, Shaaban Moustafa Elsayed W, Amirtharaj F, Wojtas B, Abou Khouzam R, Hussein Nawafleh H, Mallya S, Satyamoorthy K, Dessen P, Rosselli F, Thiery J, Chouaib S. Hypoxia increases mutational load of breast cancer cells through frameshift mutations. Oncoimmunology. 2020;9(1):1750750.

  52. Abou Khouzam R, Rao SP, Venkatesh GH, Zeinelabdin NA, Buart S, Meylan M, Nimmakayalu M, Terry S, Chouaib S. An eight-gene hypoxia signature predicts survival in pancreatic cancer and is associated with an immunosuppressed tumor microenvironment. Front Immunol. 2021;12:680435.

  53. Bader SB, Ma TS, Simpson CJ, Liang J, Maezono SEB, Olcina MM, Buffa FM, Hammond EM. Replication catastrophe induced by cyclic hypoxia leads to increased APOBEC3B activity. Nucleic Acids Res. 2021;49(13):7492-506.

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