Research progress of mitochondrial quality control in leukemia_West China Medical Journal

Authors：

WEI Jing ^1,2 , CHEN Xingbiao ^1,2 ,  LU Ziyuan ¹

1. Department of Hematology, Guangdong Provincial Key Laboratory of Major Obstetric Diseases; Guangdong Provincial Clinical Research Center for Obstetrics and Gynecology; the Third Affiliated Hospital, Guangzhou Medical University, Guangzhou, Guangdong 510150, P. R. China;
2. Department of Clinical Medicine, Guangzhou Medical University, Guangzhou, Guangdong 510150, P. R. China;

Corresponding author：

LU Ziyuan, Email: lzo19880306@126.com

Keywords：

Mitochondrial quality control; leukemia; immunomodulation; immunotherapy

DOI：

10.7507/1002-0179.202408274

Video：

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Abstract Full text Figures/Tables Video References Cited by

Mitochondrial quality control includes mechanisms such as mitochondria-derived vesicles, fusion / fission and autophagy. These processes rely on the collaboration of a variety of key proteins in the inner and outer membranes of mitochondria to jointly regulate the morphological structure and functional integrity of mitochondria, repair mitochondrial damage, and maintain the homeostasis of their internal environment. The imbalance of mitochondrial quality control is associated with leukemia. Therefore, by exploring the mechanisms related to mitochondrial quality control of various leukemia cells and their interactions with immune cells and immune microenvironment, this article sought possible targets in the treatment of leukemia, providing new ideas for the immunotherapy of leukemia.

Citation： WEI Jing, CHEN Xingbiao, LU Ziyuan. Research progress of mitochondrial quality control in leukemia. West China Medical Journal, 2024, 39(12): 1970-1977. doi: 10.7507/1002-0179.202408274 Copy

1.	Banoth B, Cassel SL. Mitochondria in innate immune signaling. Transl Res, 2018, 202: 52-68.
2.	Bonawitz ND, Clayton DA, Shadel GS. Initiation and beyond: multiple functions of the human mitochondrial transcription machinery. Mol Cell, 2006, 24(6): 813-825.
3.	吴昀紫, 郗博洲, 马亮亮, 等. 线粒体质量控制与肿瘤研究进展. 中国医学前沿杂志(电子版), 2024, 16(2): 78-87.
4.	Ta N, Qu C, Wu H, et al. Mitochondrial outer membrane protein FUNDC2 promotes ferroptosis and contributes to doxorubicin-induced cardiomyopathy. Proc Natl Acad Sci U S A, 2022, 119(36): e2117396119.
5.	吉士俊, 刘楠. 线粒体能量代谢相关铁死亡在肿瘤治疗中的研究进展. 药物生物技术, 2023, 30(5): 525-530.
6.	Koppenol WH, Bounds PL, Dang CV. Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer, 2011, 11(5): 325-337.
7.	Vander heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science, 2009, 324(5930): 1029-1033.
8.	Del Principe MI, Del Poeta G, Venditti A, et al. Apoptosis and immaturity in acute myeloid leukemia. Hematology, 2005, 10(1): 25-34.
9.	Chan DC. Mitochondrial dynamics and its involvement in disease. Annu Rev Pathol, 2020, 15: 235-259.
10.	李静, 徐平龙, 陈莎莎. 线粒体调控肿瘤免疫的研究进展. 浙江大学学报 (医学版), 2024, 53(1): 1-14.
11.	Ho GT, Theiss AL. Mitochondria and inflammatory bowel diseases: toward a stratified therapeutic intervention. Annu Rev Physiol, 2022, 84: 435-459.
12.	Sugiura A, McLelland GL, Fon EA, et al. A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. EMBO J, 2014, 33(19): 2142-2156.
13.	Towers CG, Wodetzki DK, Thorburn J, et al. Mitochondrial-derived vesicles compensate for loss of LC3-mediated mitophagy. Dev Cell, 2021, 56(14): 2029-2042. e5.
14.	Ni HM, Williams JA, Ding WX. Mitochondrial dynamics and mitochondrial quality control. Redox Biol, 2015, 4: 6-13.
15.	Wang R, Li Y, Dehaen W. Antiproliferative effect of mitochondria-targeting allobetulin 1, 2, 3-triazolium salt derivatives and their mechanism of inducing apoptosis of cancer cells. Eur J Med Chem, 2020, 207: 112737.
16.	Lenaers G, Neutzner A, Le Dantec Y, et al. Dominant optic atrophy: culprit mitochondria in the optic nerve. Prog Retin Eye Res, 2021, 83: 100935.
17.	Rasmussen ML, Gama V. A connection in life and death: the BCL-2 family coordinates mitochondrial network dynamics and stem cell fate. Int Rev Cell Mol Biol, 2020, 353: 255-284.
18.	Wang X, Wen Y, Zhang J, et al. MFN2 interacts with nuage-associated proteins and is essential for male germ cell development by controlling mRNA fate during spermatogenesis. Development, 2021, 148(7): dev196295.
19.	Vezza T, Díaz-Pozo P, Canet F, et al. The role of mitochondrial dynamic dysfunction in age-associated type 2 diabetes. World J Mens Health, 2022, 40(3): 399-411.
20.	Giacomello M, Pyakurel A, Glytsou C, et al. The cell biology of mitochondrial membrane dynamics. Nat Rev Mol Cell Biol, 2020, 21(4): 204-224.
21.	Herkenne S, Scorrano L. OPA1, a new mitochondrial target in cancer therapy. Aging (Albany NY), 2020, 12(21): 20931-20933.
22.	Chuang KC, Chang CR, Chang SH, et al. Imiquimod-induced ROS production disrupts the balance of mitochondrial dynamics and increases mitophagy in skin cancer cells. J Dermatol Sci, 2020, 98(3): 152-162.
23.	Hernández-Alvarez MI, Zorzano A. Mitochondrial dynamics and liver cancer. Cancers (Basel), 2021, 13(11): 2571.
24.	司雨平, 殷学伟, 魏文健, 等. 线粒体动力学在白血病中的研究进展. 中国实验血液学杂志, 2023, 31(4): 1224-1228.
25.	Ma Y, Wang L, Jia R. The role of mitochondrial dynamics in human cancers. Am J Cancer Res, 2020, 10(5): 1278-1293.
26.	Yin CF, Chang YW, Huang HC, et al. Targeting protein interaction networks in mitochondrial dynamics for cancer therapy. Drug Discov Today, 2022, 27(4): 1077-1087.
27.	Ng MYW, Wai T, Simonsen A. Quality control of the mitochondrion. Dev Cell, 2021, 56(7): 881-905.
28.	Song C, Pan S, Zhang J, et al. Mitophagy: a novel perspective for insighting into cancer and cancer treatment. Cell Prolif, 2022, 55(12): e13327.
29.	Panigrahi DP, Praharaj PP, Bhol CS, et al. The emerging, multifaceted role of mitophagy in cancer and cancer therapeutics. Semin Cancer Biol, 2020, 66: 45-58.
30.	Lazarini M, Machado-Neto JA, Duarte AD, et al. BNIP3L in myelodysplastic syndromes and acute myeloid leukemia: impact on disease outcome and cellular response to decitabine. Haematologica, 2016, 101(11): e445-e448.
31.	Pei S, Minhajuddin M, Adane B, et al. AMPK/FIS1-mediated mitophagy is required for self-renewal of human AML stem cells. Cell stem cell, 2018, 23(1): 86-100. e6.
32.	Mattes K, Vellenga E, Schepers H. Differential redox-regulation and mitochondrial dynamics in normal and leukemic hematopoietic stem cells: a potential window for leukemia therapy. Crit Rev Oncol Hematol, 2019, 144: 102814.
33.	Nguyen TD, Shaid S, Vakhrusheva O, et al. Loss of the selective autophagy receptor p62 impairs murine myeloid leukemia progression and mitophagy. Blood, 2019, 133(2): 168-179.
34.	Folkerts H, Wierenga AT, van den Heuvel FA, et al. Elevated VMP1 expression in acute myeloid leukemia amplifies autophagy and is protective against venetoclax-induced apoptosis. Cell Death Dis, 2019, 10(6): 421.
35.	Xu Y, Tran L, Tang J, et al. FBP1-altered carbohydrate metabolism reduces leukemic viability through activating P53 and Modulating the mitochondrial quality control system in vitro. Int J Mol Sci, 2022, 23(19): 11387.
36.	Cai J, Wang J, Huang Y, et al. ERK/Drp1-dependent mitochondrial fission is involved in the MSC-induced drug resistance of T-cell acute lymphoblastic leukemia cells. Cell Death Dis, 2016, 7(11): e2459.
37.	Matthijssens F, Sharma ND, Nysus M, et al. RUNX2 regulates leukemic cell metabolism and chemotaxis in high-risk T cell acute lymphoblastic leukemia. J Clin Invest, 2021, 131(6): e141566.
38.	Singh R, Jain A, Palanichamy JK, et al. Ultrastructural changes in cristae of lymphoblasts in acute lymphoblastic leukemia parallel alterations in biogenesis markers. Appl Microsc, 2021, 51(1): 20.
39.	Dubois A, Ginet C, Furstoss N, et al. Differentiation inducing factor 3 mediates its anti-leukemic effect through ROS-dependent DRP1-mediated mitochondrial fission and induction of caspase-independent cell death. Oncotarget, 2016, 7(18): 26120-26136.
40.	Maggi F, Morelli MB, Tomassoni D, et al. The effects of cannabidiol via TRPV2 channel in chronic myeloid leukemia cells and its combination with imatinib. Cancer Sci, 2022, 113(4): 1235-1249.
41.	Penter L, Gohil SH, Lareau C, et al. Longitudinal single-cell dynamics of chromatin accessibility and mitochondrial mutations in chronic lymphocytic leukemia mirror disease history. Cancer Discov, 2021, 11(12): 3048-3063.
42.	Gavriilidis GI, Ntoufa S, Papakonstantinou N, et al. Stem cell factor is implicated in microenvironmental interactions and cellular dynamics of chronic lymphocytic leukemia. Haematologica, 2021, 106(3): 692-700.
43.	Scharping NE, Menk AV, Moreci RS, et al. The tumor microenvironment represses t cell mitochondrial biogenesis to drive intratumoral T cell metabolic insufficiency and dysfunction. Immunity, 2016, 45(2): 374-388.
44.	van Bruggen JAC, Martens AWJ, Fraietta JA, et al. Chronic lymphocytic leukemia cells impair mitochondrial fitness in CD8⁺ T cells and impede CAR T-cell efficacy. Blood, 2019, 134(1): 44-58.
45.	WEI J, LONG L, ZHENG W, et al. Targeting REGNASE-1 programs long-lived effector T cells for cancer therapy. Nature, 2019, 576(7787): 471-476.
46.	Zheng W, Wei J, Zebley CC, et al. Regnase-1 suppresses TCF-1⁺ precursor exhausted T-cell formation to limit CAR-T-cell responses against ALL. Blood, 2021, 138(2): 122-135.
47.	王利, 王科进. 骨髓微环境在白血病发病机制中的研究进展. 实用肿瘤学杂志, 2023, 37(6): 524-528.
48.	宋建新, 欧阳红梅, 闻艳, 等. 急性白血病相关巨噬细胞的性质及 rhIFN-γ对其影响的研究. 重庆医学, 2019, 48(19): 3292-3296, 3302.
49.	Ganapathy-kanniappan S. Linking tumor glycolysis and immune evasion in cancer: emerging concepts and therapeutic opportunities. Biochim Biophys Acta Rev Cancer, 2017, 1868(1): 212-220.
50.	Xu B, Hu R, Liang Z, et al. Metabolic regulation of the bone marrow microenvironment in leukemia. Blood Rev, 2021, 48: 100786.
51.	Klein K, He K, Younes AI, et al. Role of mitochondria in cancer immune evasion and potential therapeutic approaches. Front Immunol, 2020, 11: 573326.
52.	李凤, 杨斐斐, 徐燕丽. 白血病微环境免疫异质性最新研究进展. 中国实验血液学杂志, 2023, 31(5): 1569-1573.
53.	Spiegel JY, Patel S, Muffly L, et al. CAR T cells with dual targeting of CD19 and CD22 in adult patients with recurrent or refractory B cell malignancies: a phase 1 trial. Nat Med, 2021, 27(8): 1419-1431.
54.	Dai H, Wu Z, Jia H, et al. Bispecific CAR-T cells targeting both CD19 and CD22 for therapy of adults with relapsed or refractory B cell acute lymphoblastic leukemia. J Hematol Onco, 2020, 13(1): 53.
55.	Melenhorst JJ, Chen GM, Wang M, et al. Decade-long leukaemia remissions with persistence of CD4⁺ CAR T cells. Nature, 2022, 602(7897): 503-509.
56.	Chamoto K, Chowdhury PS, Kumar A, et al. Mitochondrial activation chemicals synergize with surface receptor PD-1 blockade for T cell-dependent antitumor activity. Proc Natl Acad Sci U S A, 2017, 114(5): E761-E770.
57.	Bengsch B, Johnson AL, Kurachi M, et al. Bioenergetic insufficiencies due to metabolic alterations regulated by the inhibitory receptor PD-1 are an early driver of CD8(+) T cell exhaustion. Immunity, 2016, 45(2): 358-373.
58.	Kouidhi S, Ben Ayed F, Benammar Elgaaied A. Targeting tumor metabolism: a new challenge to improve immunotherapy. Front Immunol, 2018, 9: 353.

1. Banoth B, Cassel SL. Mitochondria in innate immune signaling. Transl Res, 2018, 202: 52-68.
2. Bonawitz ND, Clayton DA, Shadel GS. Initiation and beyond: multiple functions of the human mitochondrial transcription machinery. Mol Cell, 2006, 24(6): 813-825.
3. 吴昀紫, 郗博洲, 马亮亮, 等. 线粒体质量控制与肿瘤研究进展. 中国医学前沿杂志(电子版), 2024, 16(2): 78-87.
4. Ta N, Qu C, Wu H, et al. Mitochondrial outer membrane protein FUNDC2 promotes ferroptosis and contributes to doxorubicin-induced cardiomyopathy. Proc Natl Acad Sci U S A, 2022, 119(36): e2117396119.
5. 吉士俊, 刘楠. 线粒体能量代谢相关铁死亡在肿瘤治疗中的研究进展. 药物生物技术, 2023, 30(5): 525-530.
6. Koppenol WH, Bounds PL, Dang CV. Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer, 2011, 11(5): 325-337.
7. Vander heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science, 2009, 324(5930): 1029-1033.
8. Del Principe MI, Del Poeta G, Venditti A, et al. Apoptosis and immaturity in acute myeloid leukemia. Hematology, 2005, 10(1): 25-34.
9. Chan DC. Mitochondrial dynamics and its involvement in disease. Annu Rev Pathol, 2020, 15: 235-259.
10. 李静, 徐平龙, 陈莎莎. 线粒体调控肿瘤免疫的研究进展. 浙江大学学报 (医学版), 2024, 53(1): 1-14.
11. Ho GT, Theiss AL. Mitochondria and inflammatory bowel diseases: toward a stratified therapeutic intervention. Annu Rev Physiol, 2022, 84: 435-459.
12. Sugiura A, McLelland GL, Fon EA, et al. A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. EMBO J, 2014, 33(19): 2142-2156.
13. Towers CG, Wodetzki DK, Thorburn J, et al. Mitochondrial-derived vesicles compensate for loss of LC3-mediated mitophagy. Dev Cell, 2021, 56(14): 2029-2042. e5.
14. Ni HM, Williams JA, Ding WX. Mitochondrial dynamics and mitochondrial quality control. Redox Biol, 2015, 4: 6-13.
15. Wang R, Li Y, Dehaen W. Antiproliferative effect of mitochondria-targeting allobetulin 1, 2, 3-triazolium salt derivatives and their mechanism of inducing apoptosis of cancer cells. Eur J Med Chem, 2020, 207: 112737.
16. Lenaers G, Neutzner A, Le Dantec Y, et al. Dominant optic atrophy: culprit mitochondria in the optic nerve. Prog Retin Eye Res, 2021, 83: 100935.
17. Rasmussen ML, Gama V. A connection in life and death: the BCL-2 family coordinates mitochondrial network dynamics and stem cell fate. Int Rev Cell Mol Biol, 2020, 353: 255-284.
18. Wang X, Wen Y, Zhang J, et al. MFN2 interacts with nuage-associated proteins and is essential for male germ cell development by controlling mRNA fate during spermatogenesis. Development, 2021, 148(7): dev196295.
19. Vezza T, Díaz-Pozo P, Canet F, et al. The role of mitochondrial dynamic dysfunction in age-associated type 2 diabetes. World J Mens Health, 2022, 40(3): 399-411.
20. Giacomello M, Pyakurel A, Glytsou C, et al. The cell biology of mitochondrial membrane dynamics. Nat Rev Mol Cell Biol, 2020, 21(4): 204-224.
21. Herkenne S, Scorrano L. OPA1, a new mitochondrial target in cancer therapy. Aging (Albany NY), 2020, 12(21): 20931-20933.
22. Chuang KC, Chang CR, Chang SH, et al. Imiquimod-induced ROS production disrupts the balance of mitochondrial dynamics and increases mitophagy in skin cancer cells. J Dermatol Sci, 2020, 98(3): 152-162.
23. Hernández-Alvarez MI, Zorzano A. Mitochondrial dynamics and liver cancer. Cancers (Basel), 2021, 13(11): 2571.
24. 司雨平, 殷学伟, 魏文健, 等. 线粒体动力学在白血病中的研究进展. 中国实验血液学杂志, 2023, 31(4): 1224-1228.
25. Ma Y, Wang L, Jia R. The role of mitochondrial dynamics in human cancers. Am J Cancer Res, 2020, 10(5): 1278-1293.
26. Yin CF, Chang YW, Huang HC, et al. Targeting protein interaction networks in mitochondrial dynamics for cancer therapy. Drug Discov Today, 2022, 27(4): 1077-1087.
27. Ng MYW, Wai T, Simonsen A. Quality control of the mitochondrion. Dev Cell, 2021, 56(7): 881-905.
28. Song C, Pan S, Zhang J, et al. Mitophagy: a novel perspective for insighting into cancer and cancer treatment. Cell Prolif, 2022, 55(12): e13327.
29. Panigrahi DP, Praharaj PP, Bhol CS, et al. The emerging, multifaceted role of mitophagy in cancer and cancer therapeutics. Semin Cancer Biol, 2020, 66: 45-58.
30. Lazarini M, Machado-Neto JA, Duarte AD, et al. BNIP3L in myelodysplastic syndromes and acute myeloid leukemia: impact on disease outcome and cellular response to decitabine. Haematologica, 2016, 101(11): e445-e448.
31. Pei S, Minhajuddin M, Adane B, et al. AMPK/FIS1-mediated mitophagy is required for self-renewal of human AML stem cells. Cell stem cell, 2018, 23(1): 86-100. e6.
32. Mattes K, Vellenga E, Schepers H. Differential redox-regulation and mitochondrial dynamics in normal and leukemic hematopoietic stem cells: a potential window for leukemia therapy. Crit Rev Oncol Hematol, 2019, 144: 102814.
33. Nguyen TD, Shaid S, Vakhrusheva O, et al. Loss of the selective autophagy receptor p62 impairs murine myeloid leukemia progression and mitophagy. Blood, 2019, 133(2): 168-179.
34. Folkerts H, Wierenga AT, van den Heuvel FA, et al. Elevated VMP1 expression in acute myeloid leukemia amplifies autophagy and is protective against venetoclax-induced apoptosis. Cell Death Dis, 2019, 10(6): 421.
35. Xu Y, Tran L, Tang J, et al. FBP1-altered carbohydrate metabolism reduces leukemic viability through activating P53 and Modulating the mitochondrial quality control system in vitro. Int J Mol Sci, 2022, 23(19): 11387.
36. Cai J, Wang J, Huang Y, et al. ERK/Drp1-dependent mitochondrial fission is involved in the MSC-induced drug resistance of T-cell acute lymphoblastic leukemia cells. Cell Death Dis, 2016, 7(11): e2459.
37. Matthijssens F, Sharma ND, Nysus M, et al. RUNX2 regulates leukemic cell metabolism and chemotaxis in high-risk T cell acute lymphoblastic leukemia. J Clin Invest, 2021, 131(6): e141566.
38. Singh R, Jain A, Palanichamy JK, et al. Ultrastructural changes in cristae of lymphoblasts in acute lymphoblastic leukemia parallel alterations in biogenesis markers. Appl Microsc, 2021, 51(1): 20.
39. Dubois A, Ginet C, Furstoss N, et al. Differentiation inducing factor 3 mediates its anti-leukemic effect through ROS-dependent DRP1-mediated mitochondrial fission and induction of caspase-independent cell death. Oncotarget, 2016, 7(18): 26120-26136.
40. Maggi F, Morelli MB, Tomassoni D, et al. The effects of cannabidiol via TRPV2 channel in chronic myeloid leukemia cells and its combination with imatinib. Cancer Sci, 2022, 113(4): 1235-1249.
41. Penter L, Gohil SH, Lareau C, et al. Longitudinal single-cell dynamics of chromatin accessibility and mitochondrial mutations in chronic lymphocytic leukemia mirror disease history. Cancer Discov, 2021, 11(12): 3048-3063.
42. Gavriilidis GI, Ntoufa S, Papakonstantinou N, et al. Stem cell factor is implicated in microenvironmental interactions and cellular dynamics of chronic lymphocytic leukemia. Haematologica, 2021, 106(3): 692-700.
43. Scharping NE, Menk AV, Moreci RS, et al. The tumor microenvironment represses t cell mitochondrial biogenesis to drive intratumoral T cell metabolic insufficiency and dysfunction. Immunity, 2016, 45(2): 374-388.
44. van Bruggen JAC, Martens AWJ, Fraietta JA, et al. Chronic lymphocytic leukemia cells impair mitochondrial fitness in CD8⁺ T cells and impede CAR T-cell efficacy. Blood, 2019, 134(1): 44-58.
45. WEI J, LONG L, ZHENG W, et al. Targeting REGNASE-1 programs long-lived effector T cells for cancer therapy. Nature, 2019, 576(7787): 471-476.
46. Zheng W, Wei J, Zebley CC, et al. Regnase-1 suppresses TCF-1⁺ precursor exhausted T-cell formation to limit CAR-T-cell responses against ALL. Blood, 2021, 138(2): 122-135.
47. 王利, 王科进. 骨髓微环境在白血病发病机制中的研究进展. 实用肿瘤学杂志, 2023, 37(6): 524-528.
48. 宋建新, 欧阳红梅, 闻艳, 等. 急性白血病相关巨噬细胞的性质及 rhIFN-γ对其影响的研究. 重庆医学, 2019, 48(19): 3292-3296, 3302.
49. Ganapathy-kanniappan S. Linking tumor glycolysis and immune evasion in cancer: emerging concepts and therapeutic opportunities. Biochim Biophys Acta Rev Cancer, 2017, 1868(1): 212-220.
50. Xu B, Hu R, Liang Z, et al. Metabolic regulation of the bone marrow microenvironment in leukemia. Blood Rev, 2021, 48: 100786.
51. Klein K, He K, Younes AI, et al. Role of mitochondria in cancer immune evasion and potential therapeutic approaches. Front Immunol, 2020, 11: 573326.
52. 李凤, 杨斐斐, 徐燕丽. 白血病微环境免疫异质性最新研究进展. 中国实验血液学杂志, 2023, 31(5): 1569-1573.
53. Spiegel JY, Patel S, Muffly L, et al. CAR T cells with dual targeting of CD19 and CD22 in adult patients with recurrent or refractory B cell malignancies: a phase 1 trial. Nat Med, 2021, 27(8): 1419-1431.
54. Dai H, Wu Z, Jia H, et al. Bispecific CAR-T cells targeting both CD19 and CD22 for therapy of adults with relapsed or refractory B cell acute lymphoblastic leukemia. J Hematol Onco, 2020, 13(1): 53.
55. Melenhorst JJ, Chen GM, Wang M, et al. Decade-long leukaemia remissions with persistence of CD4⁺ CAR T cells. Nature, 2022, 602(7897): 503-509.
56. Chamoto K, Chowdhury PS, Kumar A, et al. Mitochondrial activation chemicals synergize with surface receptor PD-1 blockade for T cell-dependent antitumor activity. Proc Natl Acad Sci U S A, 2017, 114(5): E761-E770.
57. Bengsch B, Johnson AL, Kurachi M, et al. Bioenergetic insufficiencies due to metabolic alterations regulated by the inhibitory receptor PD-1 are an early driver of CD8(+) T cell exhaustion. Immunity, 2016, 45(2): 358-373.
58. Kouidhi S, Ben Ayed F, Benammar Elgaaied A. Targeting tumor metabolism: a new challenge to improve immunotherapy. Front Immunol, 2018, 9: 353.

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