Mitochondria-related signaling pathways involved in breast cancer regulate ferroptosis

Xinrui Dong; Ye Li; Xiaonan Sheng; Weihang Zhou; Aijun Sun; Huijuan Dai

doi:10.1016/j.gendis.2023.03.019

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Mitochondria-related signaling pathways involved in breast cancer regulate ferroptosis

Review Articles | 更新时间：2024-02-04

- Mitochondria-related signaling pathways involved in breast cancer regulate ferroptosis
- Mitochondria-related signaling pathways involved in breast cancer regulate ferroptosis
- Genes & Diseases 2024年1卷第1期页码：358-366
- 作者机构：
  
  1. Department of Breast Surgery, Renji Hospital, School of Medicine, Shanghai Jiaotong University,Shanghai,China,200127
  2. Department of Thyroid and Breast Oncological Surgery, Xuzhou Medical College Affiliated Huaian Hospital,Jiangsu,Huai'an,China,223001
- 作者简介：
- 基金信息：
- DOI：10.1016/j.gendis.2023.03.019
  中图分类号：
- 纸质出版日期：2024，
  
  网络出版日期：2024-1-1，
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Mitochondria-related signaling pathways involved in breast cancer regulate ferroptosis[J]. Genes & Diseases, 2024,1(1):358-366.

Xinrui Dong, Ye Li, Xiaonan Sheng, et al. Mitochondria-related signaling pathways involved in breast cancer regulate ferroptosis[J]. Genes & Diseases, 2024,1(1):358-366.
Mitochondria-related signaling pathways involved in breast cancer regulate ferroptosis[J]. Genes & Diseases, 2024,1(1):358-366. DOI： 10.1016/j.gendis.2023.03.019.

Xinrui Dong, Ye Li, Xiaonan Sheng, et al. Mitochondria-related signaling pathways involved in breast cancer regulate ferroptosis[J]. Genes & Diseases, 2024,1(1):358-366. DOI： 10.1016/j.gendis.2023.03.019.

摘要

Abstract

Ferroptosis is a novel form of regulated cell death characterized by iron-dependent excessive lipid peroxidation. The core organelle involved in ferroptosis is mitochondria. Mitochondria undergoing ferroptosis are distinct from normal mitochondria in terms of morphology

biochemistry

gene expression

and energy metabolism. An increasing number of studies have shown that mitochondria and their associated metabolic pathways mediate ferroptosis in the development and progression of breast cancer. In this review

we discuss the relevant research about ferroptosis in breast cancer and provide a comprehensive summary of mitochondrial regulation in ferroptosis from the perspective of lipid metabolism

oxidative phosphorylation

ion metabolism

glycometabolism

and nucleotide metabolism. We also summarize the application of mitochondrial metabolism-related pathways as ferroptosis treatment targets. Here we provide new insights into the relationship between mitochondria

ferroptosis

and breast cancer treatment.

关键词

Keywords

Breast cancerCancer treatmentFerroptosisLipid metabolismMitochondriaOxidative phosphorylation

references

1 S.J. Dixon, K.M. Lemberg, M.R. Lamprecht, et al.Ferroptosis: an iron-dependent form of nonapoptotic cell death Cell, 149 (5) (2012), pp. 1060-1072

2 X. Chen, R. Kang, G. Kroemer, et al.Broadening horizons: the role of ferroptosis in cancer Nat Rev Clin Oncol, 18 (5) (2021), pp. 280-296

3 A.R. Bogdan, M. Miyazawa, K. Hashimoto, et al.Regulators of iron homeostasis: new players in metabolism, cell death, and disease Trends Biochem Sci, 41 (3) (2016), pp. 274-286

4 S. Doll, B. Proneth, Y.Y. Tyurina, et al.ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition Nat Chem Biol, 13 (1) (2017), pp. 91-98

5 B.R. Stockwell, J.P. Friedmann Angeli, H. Bayir, et al.Ferroptosis: a regulated cell death nexus linking metabolism, redox biology, and disease Cell, 171 (2) (2017), pp. 273-285

6 D. Tang, G. KroemerFerroptosis Curr Biol., 30 (21) (2020), pp. R1292-R1297

7 D.E. Handy, J. LoscalzoRedox regulation of mitochondrial function Antioxidants Redox Signal, 16 (11) (2012), pp. 1323-1367

8 H. Sato, M. Tamba, T. Ishii, et al.Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins J Biol Chem, 274 (17) (1999), pp. 11455-11458

9 A. MeisterGlutathione metabolism Methods Enzymol, 251 (1995), pp. 3-7

10 A. Seiler, M. Schneider, H. Förster, et al.Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death Cell Metabol, 8 (3) (2008), pp. 237-248

11 G. de Jong, J.P. van Dijk, H.G. van EijkThe biology of transferrin Clin Chim Acta, 190 (1–2) (1990), pp. 1-46

12 Z. Tang, P. Zhao, H. Wang, et al.Biomedicine meets Fenton chemistry Chem Rev, 121 (4) (2021), pp. 1981-2019

13 M. Conrad, D.A. PrattThe chemical basis of ferroptosis Nat Chem Biol, 15 (12) (2019), pp. 1137-1147

14 D.B. Zorov, M. Juhaszova, S.J. SollottMitochondrial reactive oxygen species (ROS) and ROS-induced ROS release Physiol Rev, 94 (3) (2014), pp. 909-950

15 Z. Shen, J. Song, B.C. Yung, et al.Emerging strategies of cancer therapy based on ferroptosis Adv Mater, 30 (12) (2018), Article e1704007

16 L.J. Su, J.H. Zhang, H. Gomez, et al.Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis Oxid Med Cell Longev, 2019 (2019), p. 5080843

17 W.S. Yang, B.R. StockwellFerroptosis: death by lipid peroxidation Trends Cell Biol, 26 (3) (2016), pp. 165-176

18 W.D. Bao, P. Pang, X.T. Zhou, et al.Loss of ferroportin induces memory impairment by promoting ferroptosis in Alzheimer's disease Cell Death Differ, 28 (5) (2021), pp. 1548-1562

19 X. Fang, Z. Cai, H. Wang, et al.Loss of cardiac ferritin H facilitates cardiomyopathy via Slc7a11-mediated ferroptosis Circ Res, 127 (4) (2020), pp. 486-501

20 B.R. Stockwell, X. Jiang, W. GuEmerging mechanisms and disease relevance of ferroptosis Trends Cell Biol, 30 (6) (2020), pp. 478-490

21 R. Lill, S.A. FreibertMechanisms of mitochondrial iron-sulfur protein biogenesis Annu Rev Biochem, 89 (2020), pp. 471-499

22 D. SpeijerOxygen radicals shaping evolution: why fatty acid catabolism leads to peroxisomes while neurons do without it: FADH₂/NADH flux ratios determining mitochondrial radical formation were crucial for the eukaryotic invention of peroxisomes and catabolic tissue differentiation Bioessays, 33 (2) (2011), pp. 88-94

23 M.C. Hunt, V. Tillander, S.E.H. AlexsonRegulation of peroxisomal lipid metabolism: the role of acyl-CoA and coenzyme A metabolizing enzymes Biochimie, 98 (2014), pp. 45-55

24 L. Tesfay, B.T. Paul, A. Konstorum, et al.Stearoyl-CoA desaturase 1 protects ovarian cancer cells from ferroptotic cell death Cancer Res, 79 (20) (2019), pp. 5355-5366

25 A.R. BrashLipoxygenases: occurrence, functions, catalysis, and acquisition of substrate J Biol Chem, 274 (34) (1999), pp. 23679-23682

26 S. Pallast, K. Arai, X. Wang, et al.12/15-Lipoxygenase targets neuronal mitochondria under oxidative stress J Neurochem, 111 (3) (2009), pp. 882-889

27 D.A. Stoyanovsky, Y.Y. Tyurina, I. Shrivastava, et al.Iron catalysis of lipid peroxidation in ferroptosis: regulated enzymatic or random free radical reaction? Free Radic Biol Med, 133 (2019), pp. 153-161

28 V.E. Kagan, G. Mao, F. Qu, et al.Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis Nat Chem Biol, 13 (1) (2017), pp. 81-90

29 L. Magtanong, P.J. Ko, M. To, et al.Exogenous monounsaturated fatty acids promote a ferroptosis-resistant cell state Cell Chem Biol, 26 (3) (2019), pp. 420-432.e9

30 H. Miess, B. Dankworth, A.M. Gouw, et al.The glutathione redox system is essential to prevent ferroptosis caused by impaired lipid metabolism in clear cell renal cell carcinoma Oncogene, 37 (40) (2018), pp. 5435-5450

31 M.P. MurphyHow mitochondria produce reactive oxygen species Biochem J, 417 (1) (2009), pp. 1-13

32 M. Gao, J. Yi, J. Zhu, et al.Role of mitochondria in ferroptosis Mol Cell, 73 (2) (2019), pp. 354-363.e3

33 K. Shimada, M. Hayano, N. Pagano, et al.Cell-line selectivity improves the predictive power of pharmacogenomic analyses and helps identify NADPH as biomarker for ferroptosis sensitivity Cell Chem Biol, 23 (2) (2016), pp. 225-235

34 K. Bersuker, J.M. Hendricks, Z. Li, et al.The CoQ oxidoreductase FSP1 acts parallel to GPX4 to inhibit ferroptosis Nature, 575 (7784) (2019), pp. 688-692

35 S. Doll, F.P. Freitas, R. Shah, et al.FSP1 is a glutathione-independent ferroptosis suppressor Nature, 575 (7784) (2019), pp. 693-698

36 S.M. Kanzok, A. Fechner, H. Bauer, et al.Substitution of the thioredoxin system for glutathione reductase in Drosophila melanogaster Science, 291 (5504) (2001), pp. 643-646

37 H. Wu, F. Wang, N. Ta, et al.The multifaceted regulation of mitochondria in ferroptosis Life, 11 (3) (2021), p. 222

38 D.N. Douda, M.A. Khan, H. Grasemann, et al.SK3 channel and mitochondrial ROS mediate NADPH oxidase-independent NETosis induced by calcium influx Proc Natl Acad Sci U S A, 112 (9) (2015), pp. 2817-2822

39 D.N. DeHart, D. Fang, K. Heslop, et al.Opening of voltage dependent anion channels promotes reactive oxygen species generation, mitochondrial dysfunction and cell death in cancer cells Biochem Pharmacol, 148 (2018), pp. 155-162

40 M. Gao, P. Monian, N. Quadri, et al.Glutaminolysis and transferrin regulate ferroptosis Mol Cell, 59 (2) (2015), pp. 298-308

41 E.E. Mon, F.Y. Wei, R.N.R. Ahmad, et al.Regulation of mitochondrial iron homeostasis by sideroflexin 2 J Physiol Sci, 69 (2) (2019), pp. 359-373

42 X. Fang, H. Wang, D. Han, et al.Ferroptosis as a target for protection against cardiomyopathy Proc Natl Acad Sci U S A, 116 (7) (2019), pp. 2672-2680

43 G. Gao, Y.Z. ChangMitochondrial ferritin in the regulation of brain iron homeostasis and neurodegenerative diseases Front Pharmacol, 5 (2014), p. 19

44 L. Zecca, M.B.H. Youdim, P. Riederer, et al.Iron, brain ageing and neurodegenerative disorders Nat Rev Neurosci, 5 (11) (2004), pp. 863-873

45 S. Gleitze, A. Paula-Lima, M.T. Núñez, et al.The calcium–iron connection in ferroptosis-mediated neuronal death Free Radic Biol Med, 175 (2021), pp. 28-41

46 M.T. Núñez, C. HidalgoNoxious iron-calcium connections in neurodegeneration Front Neurosci, 13 (2019), p. 48

47 A. Görlach, K. Bertram, S. Hudecova, et al.Calcium and ROS: a mutual interplay Redox Biol, 6 (2015), pp. 260-271

48 C.H. Lipper, O. Karmi, Y.S. Sohn, et al.Structure of the human monomeric NEET protein MiNT and its role in regulating iron and reactive oxygen species in cancer cells Proc Natl Acad Sci U S A, 115 (2) (2018), pp. 272-277

49 B. Do Van, F. Gouel, A. Jonneaux, et al.Ferroptosis, a newly characterized form of cell death in Parkinson's disease that is regulated by PKC Neurobiol Dis, 94 (2016), pp. 169-178

50 P. Santambrogio, M. Ripamonti, C. Paolizzi, et al.Harmful iron-calcium relationship in pantothenate kinase associated neurodegeneration Int J Mol Sci, 21 (10) (2020), p. 3664

51 X. Wang, S. Lu, C. He, et al.RSL3 induced autophagic death in glioma cells via causing glycolysis dysfunction Biochem Biophys Res Commun, 518 (3) (2019), pp. 590-597

52 D. Gincel, S.D. Silberberg, V. Shoshan-BarmatzModulation of the voltage-dependent anion channel (VDAC) by Glutamate1 J Bioenerg Biomembr, 32 (6) (2000), pp. 571-583

53 T. Rostovtseva, M. ColombiniVDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function Biophys J, 72 (5) (1997), pp. 1954-1962

54 W. Kang, M. Suzuki, T. Saito, et al.Emerging role of TCA cycle-related enzymes in human diseases Int J Mol Sci, 22 (23) (2021), p. 13057

55 R.J. DeBerardinis, A. Mancuso, E. Daikhin, et al.Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis Proc Natl Acad Sci U S A, 104 (49) (2007), pp. 19345-19350

56 H. Lee, F. Zandkarimi, Y. Zhang, et al.Energy-stress-mediated AMPK activation inhibits ferroptosis Nat Cell Biol, 22 (2) (2020), pp. 225-234

57 J. Guo, L. Duan, X. He, et al.A combined model of human iPSC-derived liver organoids and hepatocytes reveals ferroptosis in DGUOK mutant mtDNA depletion syndrome Adv Sci, 8 (10) (2021), p. 2004680

58 C. Li, Y. Zhang, J. Liu, et al.Mitochondrial DNA stress triggers autophagy-dependent ferroptotic death Autophagy, 17 (4) (2021), pp. 948-960

59 S. Toyokuni, F. Ito, K. Yamashita, et al.Iron and thiol redox signaling in cancer: an exquisite balance to escape ferroptosis Free Radic Biol Med, 108 (2017), pp. 610-626

60 C.W. Brown, J.J. Amante, H.L. Goel, et al.The α6β4 integrin promotes resistance to ferroptosis J Cell Biol, 216 (12) (2017), pp. 4287-4297

61 F. Yang, Y. Xiao, J.H. Ding, et al.Ferroptosis heterogeneity in triple-negative breast cancer reveals an innovative immunotherapy combination strategy Cell Metabol, 35 (1) (2023), pp. 84-100.e8

62 M.A. Dattilo, Y. Benzo, L.M. Herrera, et al.Regulatory mechanisms leading to differential Acyl-CoA synthetase 4 expression in breast cancer cells Sci Rep, 9 (2019), p. 10324

63 F.L. Sarmiento-Salinas, A. Delgado-Magallón, J.B. Montes-Alvarado, et al.Breast cancer subtypes present a differential production of reactive oxygen species (ROS) and susceptibility to antioxidant treatment Front Oncol, 9 (2019), p. 480

64 S. Müller, F. Sindikubwabo, T. Cañeque, et al.CD44 regulates epigenetic plasticity by mediating iron endocytosis Nat Chem, 12 (10) (2020), pp. 929-938

65 W. Liu, B. Chakraborty, R. Safi, et al.Dysregulated cholesterol homeostasis results in resistance to ferroptosis increasing tumorigenicity and metastasis in cancer Nat Commun, 12 (2021), p. 5103

66 H. Li, P. Yang, J. Wang, et al.HLF regulates ferroptosis, development and chemoresistance of triple-negative breast cancer by activating tumor cell-macrophage crosstalk J Hematol Oncol, 15 (2022), p. 2

67 Z. Li, L. Chen, C. Chen, et al.Targeting ferroptosis in breast cancer Biomark Res, 8 (2020), p. 58

68 Y. Ding, X. Chen, C. Liu, et al.Identification of a small molecule as inducer of ferroptosis and apoptosis through ubiquitination of GPX4 in triple negative breast cancer cells J Hematol Oncol, 14 (2021), p. 19

69 G. Luis, A. Godfroid, S. Nishiumi, et al.Tumor resistance to ferroptosis driven by stearoyl-CoA desaturase-1 (SCD1) in cancer cells and fatty acid binding protein-4 (FABP4) in tumor microenvironment promote tumor recurrence Redox Biol, 43 (2021), p. 102006

70 L. Sun, H. Wang, S. Yu, et al.Herceptin induces ferroptosis and mitochondrial dysfunction in H9c2 cells Int J Mol Med, 49 (2) (2022), p. 17

71 L.A. MacMillan-Crow, J.A. ThompsonTyrosine modifications and inactivation of active site manganese superoxide dismutase mutant (Y34F) by peroxynitrite Arch Biochem Biophys, 366 (1) (1999), pp. 82-88

72 P.C. Hart, M. Mao, A.L.P. de Abreu, et al.MnSOD upregulation sustains the Warburg effect via mitochondrial ROS and AMPK-dependent signalling in cancer Nat Commun, 6 (2015), p. 6053

73 S. Ma, X. Fu, L. Liu, et al.Iron-dependent autophagic cell death induced by radiation in MDA-MB-231 breast cancer cells Front Cell Dev Biol, 9 (2021), p. 723801

74 C.W. Wu, P.H. Yin, W.Y. Hung, et al.Mitochondrial DNA mutations and mitochondrial DNA depletion in gastric cancer Genes Chromosomes Cancer, 44 (1) (2005), pp. 19-28

75 H. Nie, G. Chen, J. He, et al.Mitochondrial common deletion is elevated in blood of breast cancer patients mediated by oxidative stress Mitochondrion, 26 (2016), pp. 104-112

76 S. Sui, S. Xu, D. PangEmerging role of ferroptosis in breast cancer: new dawn for overcoming tumor progression Pharmacol Ther, 232 (2022), p. 107992

77 Y.S. Sohn, S. Tamir, L. Song, et al.NAF-1 and mitoNEET are central to human breast cancer proliferation by maintaining mitochondrial homeostasis and promoting tumor growth Proc Natl Acad Sci U S A, 110 (36) (2013), pp. 14676-14681

78 F. Bai, F. Morcos, Y.S. Sohn, et al.The Fe-S cluster-containing NEET proteins mitoNEET and NAF-1 as chemotherapeutic targets in breast cancer Proc Natl Acad Sci U S A, 112 (12) (2015), pp. 3698-3703

79 C. Louandre, Z. Ezzoukhry, C. Godin, et al.Iron-dependent cell death of hepatocellular carcinoma cells exposed to sorafenib Int J Cancer, 133 (7) (2013), pp. 1732-1742

80 M. Sang, R. Luo, Y. Bai, et al.Mitochondrial membrane anchored photosensitive nano-device for lipid hydroperoxides burst and inducing ferroptosis to surmount therapy-resistant cancer Theranostics, 9 (21) (2019), pp. 6209-6223

81 X. Yao, R. Xie, Y. Cao, et al.Simvastatin induced ferroptosis for triple-negative breast cancer therapy J Nanobiotechnol, 19 (2021), p. 311

82 K. Li, C. Lin, M. Li, et al.Multienzyme-like reactivity cooperatively impairs glutathione peroxidase 4 and ferroptosis suppressor protein 1 pathways in triple-negative breast cancer for sensitized ferroptosis therapy ACS Nano, 16 (2) (2022), pp. 2381-2398

83 Y. Zou, J. Xie, S. Zheng, et al.Leveraging diverse cell-death patterns to predict the prognosis and drug sensitivity of triple-negative breast cancer patients after surgery Int J Surg, 107 (2022), p. 106936

84 R. Sha, Y. Xu, C. Yuan, et al.Predictive and prognostic impact of ferroptosis-related genes ACSL4 and GPX4 on breast cancer treated with neoadjuvant chemotherapy EBioMedicine, 71 (2021), p. 103560

85 X. Song, X. Wang, Z. Liu, et al.Role of GPX4-mediated ferroptosis in the sensitivity of triple negative breast cancer cells to gefitinib Front Oncol, 10 (2020), p. 597434

86 A.L. Turcu, A. Versini, N. Khene, et al.DMT1 inhibitors kill cancer stem cells by blocking lysosomal iron translocation Chemistry, 26 (33) (2020), pp. 7369-7373

87 Y. Zou, S. Zheng, X. Xie, et al.N6-methyladenosine regulated FGFR4 attenuates ferroptotic cell death in recalcitrant HER2-positive breast cancer Nat Commun, 13 (2022), p. 2672

88 J.K. Eaton, L. Furst, R.A. Ruberto, et al.Selective covalent targeting of GPX4 using masked nitrile-oxide electrophiles Nat Chem Biol, 16 (5) (2020), pp. 497-506

89 Y. Zou, S.L. SchreiberProgress in understanding ferroptosis and challenges in its targeting for therapeutic benefit Cell Chem Biol, 27 (4) (2020), pp. 463-471

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