KUPROPTOZ; BAKIR İLİŞKİLİ HÜCRE ÖLÜM YOLAĞI
Year 2023,
, 764 - 770, 30.12.2023
Ebru Nur Aksu
,
Esin Sakallı
Abstract
Farklı organlarda ve metabolik süreçlerde yer alan enzimler için bir kofaktör olan bakır (Cu), hücresel ve fizyolojik insan sağlığı için gerekli olan önemli mikro besinlerden biridir. Son yıllarda hücrelerde biriken bakırın mitokondriyal solunum ve lipoik asit (LA) yolu ile ilişkili ve proteotoksik stres ile karakterize, “kuproptoz” olarak adlandırılan yeni bir programlı ölüm şekli tanımlanmıştır. Kuproptoz mekanizmasının daha iyi anlaşılmasına yönelik çalışmalar devam etmekle birlikte birçok araştırmacı da kuproptoz ve kanserin farklı özellikleri arasındaki ilişkiyi ortaya koymak amacıyla araştırmalarını sürdürmektedir. Bu derleme hücresel ve fizyolojik Cu metabolizmasına, kuproptoz mekanizmasına ve çeşitli kanser türleri ile olan ilişkisine odaklanmaktadır.
Ethical Statement
Bu makale, insan veya hayvanlar üzerinde herhangi bir çalışma içermemektedir.
Supporting Institution
Bu araştırma, kamu, ticari veya kar amacı gütmeyen sektörlerdeki finansman kuruluşlarından herhangi bir finansal destek almamıştır.
References
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- 3. Tsvetkov P, Coy S, Petrova B, Dreishpoon M, Verma A, Abdusamad M, et al. Copper induces cell death by targeting lipoylated TCA cycle proteins. Science 2022;375(6586):1254.
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- 5. Bost M, Houdart S, Oberli M, Kalonji E, Huneau JF, Margaritis I. Dietary copper and human health: Current evidence and unresolved issues. Journal of Trace Elements in Medicine and Biology 2016;35:107-15.
- 6. Lönnerdal B. Intestinal regulation of copper homeostasis: a developmental perspective. The American Journal of Clinical Nutrition 2008;88(3):846S-850S.
- 7. Kidane TZ, Farhad R, Lee KJ, Santos A, Russo E, Linder MC. Uptake of copper from plasma proteins in cells where expression of CTR1 has been modulated. Biometals 2012;25(4):697-709.
- 8. Migocka M. Copper-transporting ATPases: The evolutionarily conserved machineries for balancing copper in living systems. IUBMB Life 2015;67(10):737-45.
- 9. Cabrera A, Alonzo E, Sauble E, Chu YL, Linder MC, Sato DS, et al. Copper binding components of blood plasma and organs, and their responses to influx of large doses of 65Cu, in the mouse. Biometals 2008;21(5):525-43.
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- 11. Bertinato J, L’Abbé MR. Copper modulates the degradation of copper chaperone for Cu,Zn superoxide dismutase by the 26 S proteosome. J Biol Chem. 2003;278(37):35071-8.
- 12. Wong PC, Waggoner D, Subramaniam JR, Tessarollo L, Bartnikas TB, Culotta VC, et al. Copper chaperone for superoxide dismutase is essential to activate mammalian Cu/Zn superoxide dismutase. Proc Natl Acad Sci U S A. 2000;97(6):2886-91.
- 13. Nývltová E, Dietz JV, Seravalli J, Khalimonchuk O, Barrientos A. Coordination of metal center biogenesis in human cytochrome c oxidase. Nat Commun. 2022;13:3615.
- 14. Prohaska JR. Role of copper transporters in copper homeostasis. Am J Clin Nutr. 2008;88(3):826S-829S.
- 15. Itoh S, Kim HW, Nakagawa O, Ozumi K, Lessner SM, Aoki H, et al. Novel Role of Antioxidant-1 (Atox1) as a Copper-dependent Transcription Factor Involved in Cell Proliferation. J Biol Chem. 2008;283(14):9157-67.
- 16. Chen J, Jiang Y, Shi H, Peng Y, Fan X, Li C. The molecular mechanisms of copper metabolism and its roles in human diseases. Pflugers Arch - Eur J Physiol. 2020;472(10):1415-29.
- 17. Hernandez S, Tsuchiya Y, García–Ruiz JP, Lalioti V, Nielsen S, Cassio D, et al. ATP7B Copper-Regulated Traffic and Association With the Tight Junctions: Copper Excretion Into the Bile. Gastroenterology. 2008;134(4):1215-23.
- 18. Palmgren MG, Nissen P. P-type ATPases. Annu Rev Biophys. 2011;40:243-66.
- 19. Lutsenko S, Barnes NL, Bartee MY, Dmitriev OY. Function and Regulation of Human Copper-Transporting ATPases. Physiological Reviews 2007;87(3):1011-46.
- 20. Shim H, Harris ZL. Genetic Defects in Copper Metabolism. The Journal of Nutrition. 2003;133(5):1527S-1531S.
- 21. Møller LB, Mogensen M, Horn N. Molecular diagnosis of Menkes disease: Genotype–phenotype correlation. Biochimie 2009;91(10):1273-7.
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- 23. Czlonkowska A, Litwin T, Dusek P, Ferenci P, Lutsenko S, Medici V, et al. Nature Reviews Disease Primers article: Wilson disease. Nat Rev Dis Primers. 2018;4(1):21.
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- 25. Przybyłkowski A, Gromadzka G, Chabik G, Wierzchowska A, Litwin T, Członkowska A. Liver cirrhosis in patients newly diagnosed with neurological phenotype of Wilson’s disease. Funct Neurol. 2014;29(1):23-9.
- 26. Factor SM, Cho S, Sternlieb I, Scheinberg IH, Goldfischer S. The cardiomyopathy of Wilson’s disease. Virchows Arch A Path Anat and Histol. 1982;397(3):301-11.
- 27. Misra A, Biswas A, Ganguly G, Ghosh A, Das S, Roy T. Arthropathic presentation of Wilson’s disease. The Journal of the Association of Physicians of India 2004;52:246-8.
- 28. Squitti R, Lupoi D, Pasqualetti P, Dal Forno G, Vernieri F, Chiovenda P, et al. Elevation of serum copper levels in Alzheimer’s disease. Neurology 2002;59(8):1153.
- 29. Fox JH, Kama JA, Lieberman G, Chopra R, Dorsey K, Chopra V, et al. Mechanisms of Copper Ion Mediated Huntington’s Disease Progression. PLoS One 2007;2(3):e334.
- 30. Ford ES. Serum Copper Concentration and Coronary Heart Disease among US Adults. American Journal of Epidemiology. 2000;151(12):1182-8.
- 31. Sheftel AD, Stehling O, Pierik AJ, Elsässer HP, Mühlenhoff U, Webert H, et al. Humans possess two mitochondrial ferredoxins, Fdx1 and Fdx2, with distinct roles in steroidogenesis, heme, and Fe/S cluster biosynthesis. Proc Natl Acad Sci. 2010;107(26):11775-80.
- 32. Py B, Barras F. Building Fe–S proteins: bacterial strategies. Nat Rev Microbiol. 2010;8(6):436-46.
- 33. Shanbhag VC, Gudekar N, Jasmer K, Papageorgiou C, Singh K, Petris MJ. Copper metabolism as a unique vulnerability in cancer. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 2021;1868(2):118893.
- 34. He F, Chang C, Liu B, Li Z, Li H, Cai N, et al. Copper (II) Ions Activate Ligand-Independent Receptor Tyrosine Kinase (RTK) Signaling Pathway. BioMed Research International 2019;2019:e4158415.
- 35. Qiu L, Ding X, Zhang Z, Kang YJ. Copper Is Required for Cobalt-Induced Transcriptional Activity of Hypoxia-Inducible Factor-1. J Pharmacol Exp Ther. 2012;342(2):561-7.
- 36. Ostrakhovitch EA, Lordnejad MR, Schliess F, Sies H, Klotz LO. Copper ions strongly activate the phosphoinositide-3-kinase/Akt pathway independent of the generation of reactive oxygen species. Arch Biochem Biophys. 2002;397(2):232-9.
- 37. Guo J, Cheng J, Zheng N, Zhang X, Dai X, Zhang L, et al. Copper Promotes Tumorigenesis by Activating the PDK1-AKT Oncogenic Pathway in a Copper Transporter 1 Dependent Manner. Advanced Science 2021;8(18):2004303.
- 38. Walter PL, Kampkötter A, Eckers A, Barthel A, Schmoll D, Sies H, et al. Modulation of FoxO signaling in human hepatoma cells by exposure to copper or zinc ions. Arch Biochem Biophys. 2006;454(2):107-13.
- 39. Baldari S, Di Rocco G, Heffern MC, Su TA, Chang CJ, Toietta G. Effects of Copper Chelation on BRAFV600E Positive Colon Carcinoma Cells. Cancers 2019;11(5):659.
- 40. Turski ML, Brady DC, Kim HJ, Kim BE, Nose Y, Counter CM, et al. A Novel Role for Copper in Ras/Mitogen-Activated Protein Kinase Signaling. Molecular and Cellular Biology 2012;32(7):1284-95.
- 41. Ge EJ, Bush AI, Casini A, Cobine PA, Cross JR, DeNicola GM, et al. Connecting copper and cancer: from transition metal signalling to metalloplasia. Nat Rev Cancer 2022;22(2):102-13.
- 42. Tsang T, Posimo JM, Gudiel AA, Cicchini M, Feldser DM, Brady DC. Copper is an essential regulator of the autophagic kinases ULK1/2 to drive lung adenocarcinoma. Nat Cell Biol. 2020;22(4):412-24.
- 43. Yun CW, Lee SH. The Roles of Autophagy in Cancer. Int J Mol Sci. 2018;19(11):3466.
- 44. Parr-Sturgess CA, Tinker CL, Hart CA, Brown MD, Clarke NW, Parkin ET. Copper Modulates Zinc Metalloproteinase-Dependent Ectodomain Shedding of Key Signaling and Adhesion Proteins and Promotes the Invasion of Prostate Cancer Epithelial Cells. Molecular Cancer Research 2012;10(10):1282-93.
- 45. McAuslan BR, Reilly W. Endothelial cell phagokinesis in response to specific metal ions. Experimental Cell Research 1980;130(1):147-57.
- 46. Li Y. Copper homeostasis: Emerging target for cancer treatment. IUBMB Life 2020;72(9):1900-8.
- 47. Suska F, Esposito M, Gretzer C, Källtorp M, Tengvall P, Thomsen P. IL-1α, IL-1β and TNF-α secretion during in vivo/ex vivo cellular interactions with titanium and copper. Biomaterials 2003;24(3):461-8.
- 48. Soncin F, Guitton JD, Cartwright T, Badet J. Interaction of Human Angiogenin with Copper Modulates Angiogenin Binding to Endothelial Cells. Biochemical and Biophysical Research Communications 1997;236(3):604-10.
- 49. Kohno T, Urao N, Ashino T, Sudhahar V, McKinney RD, Hamakubo T, et al. Novel Role of Copper Transport Protein Antioxidant-1 in Neointimal Formation After Vascular Injury. Arteriosclerosis, Thrombosis, and Vascular Biology 2013;33(4):805-13.
- 50. Zhang C, Zeng Y, Guo X, Shen H, Zhang J, Wang K, et al. Pan-cancer analyses confirmed the cuproptosis-related gene FDX1 as an immunotherapy predictor and prognostic biomarker. Frontiers in Genetics 2022;13:947372.
- 51. Xiao C, Yang L, Jin L, Lin W, Zhang F, Huang S, et al. Prognostic and immunological role of cuproptosis-related protein FDX1 in pan-cancer. Frontiers in Genetics 2022;13:962028.
- 52. Cai Y, He Q, Liu W, Liang Q, Peng B, Li J, et al. Comprehensive analysis of the potential cuproptosis-related biomarker LIAS that regulates prognosis and immunotherapy of pan-cancers. Frontiers in Oncology 2022;12:952129.
- 53. Zhang H, Shi Y, Yi Q, Wang C, Xia Q, Zhang Y, et al. A novel defined cuproptosis-related gene signature for predicting the prognosis of lung adenocarcinoma. Front Genet. 2022;13:975185.
- 54. Deng L, Jiang A, Zeng H, Peng X, Song L. Comprehensive analyses of PDHA1 that serves as a predictive biomarker for immunotherapy response in cancer. Frontiers in Pharmacology 2022;13:947372.
- 55. Chen Y, Chen X, Wang X. Identification of a prognostic model using cuproptosis-related genes in uveal melanoma. Frontiers in Cell and Developmental Biology 2022;10:973073.
- 56. Lv H, Liu X, Zeng X, Liu Y, Zhang C, Zhang Q, et al. Comprehensive Analysis of Cuproptosis-Related Genes in Immune Infiltration and Prognosis in Melanoma. Front Pharmacol. 2022;13:930041.
- 57. Chen Y. Identification and Validation of Cuproptosis-Related Prognostic Signature and Associated Regulatory Axis in Uterine Corpus Endometrial Carcinoma. Front Genet. 2022;13:912037.
- 58. Hu Q, Wang R, Ma H, Zhang Z, Xue Q. Cuproptosis predicts the risk and clinical outcomes of lung adenocarcinoma. Frontiers in Oncology 2022;12:922332.
- 59. Ye Z, Zhang S, Cai J, Ye L, Gao L, Wang Y, et al. Development and validation of cuproptosis-associated prognostic signatures in WHO 2/3 glioma. Front Oncol. 2022;12:967159.
- 60. Du Y, Lin Y, Wang B, Li Y, Xu D, Gan L, et al. Cuproptosis patterns and tumor immune infiltration characterization in colorectal cancer. Front Genet. 2022;13:976007.
- 61. Fu J, Wang S, Li Z, Qin W, Tong Q, Liu C, et al. Comprehensive multiomics analysis of cuproptosis-related gene characteristics in hepatocellular carcinoma. Frontiers in Genetics 2022;12:942387.
CUPROPTOSIS; COPPER ASSOCIATED CELL DEATH PATHWAY
Year 2023,
, 764 - 770, 30.12.2023
Ebru Nur Aksu
,
Esin Sakallı
Abstract
Copper (Cu) is an essential micronutrient for human cellular and physiological health since it acts as a cofactor for enzymes involved in various metabolic processes throughout different organs in the body. Recently, a new type of programmed cell death, known as "cuproptosis," has been discovered and linked to mitochondrial respiration and the lipoic acid (LA) pathway. Cuproptosis is characterised by proteotoxic stress resulting from the gradual accumulation of copper in cells. Although researchers continue to study the mechanism of cuproptosis, the relationship between cuproptosis and different features of cancer is still being explored. This review examines cellular and physiological copper metabolism, the cuproptosis mechanism, and its associations with various types of cancer.
References
- 1. Balamurugan K, Schaffner W. Copper homeostasis in eukaryotes: Teetering on a tightrope. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 2006;1763(7):737-46.
- 2. Walshe JM. Wilson’s disease. The Lancet 2007;369(9565):902.
- 3. Tsvetkov P, Coy S, Petrova B, Dreishpoon M, Verma A, Abdusamad M, et al. Copper induces cell death by targeting lipoylated TCA cycle proteins. Science 2022;375(6586):1254.
- 4. Maung MT, Carlson A, Olea-Flores M, Elkhadragy L, Schachtschneider KM, Navarro-Tito N, et al. The molecular and cellular basis of copper dysregulation and its relationship with human pathologies. The FASEB Journal 2021;35(9):e21810.
- 5. Bost M, Houdart S, Oberli M, Kalonji E, Huneau JF, Margaritis I. Dietary copper and human health: Current evidence and unresolved issues. Journal of Trace Elements in Medicine and Biology 2016;35:107-15.
- 6. Lönnerdal B. Intestinal regulation of copper homeostasis: a developmental perspective. The American Journal of Clinical Nutrition 2008;88(3):846S-850S.
- 7. Kidane TZ, Farhad R, Lee KJ, Santos A, Russo E, Linder MC. Uptake of copper from plasma proteins in cells where expression of CTR1 has been modulated. Biometals 2012;25(4):697-709.
- 8. Migocka M. Copper-transporting ATPases: The evolutionarily conserved machineries for balancing copper in living systems. IUBMB Life 2015;67(10):737-45.
- 9. Cabrera A, Alonzo E, Sauble E, Chu YL, Linder MC, Sato DS, et al. Copper binding components of blood plasma and organs, and their responses to influx of large doses of 65Cu, in the mouse. Biometals 2008;21(5):525-43.
- 10. Robinson NJ, Winge DR. Copper Metallochaperones. Annual Review of Biochemistry 2010;79(1):537-62.
- 11. Bertinato J, L’Abbé MR. Copper modulates the degradation of copper chaperone for Cu,Zn superoxide dismutase by the 26 S proteosome. J Biol Chem. 2003;278(37):35071-8.
- 12. Wong PC, Waggoner D, Subramaniam JR, Tessarollo L, Bartnikas TB, Culotta VC, et al. Copper chaperone for superoxide dismutase is essential to activate mammalian Cu/Zn superoxide dismutase. Proc Natl Acad Sci U S A. 2000;97(6):2886-91.
- 13. Nývltová E, Dietz JV, Seravalli J, Khalimonchuk O, Barrientos A. Coordination of metal center biogenesis in human cytochrome c oxidase. Nat Commun. 2022;13:3615.
- 14. Prohaska JR. Role of copper transporters in copper homeostasis. Am J Clin Nutr. 2008;88(3):826S-829S.
- 15. Itoh S, Kim HW, Nakagawa O, Ozumi K, Lessner SM, Aoki H, et al. Novel Role of Antioxidant-1 (Atox1) as a Copper-dependent Transcription Factor Involved in Cell Proliferation. J Biol Chem. 2008;283(14):9157-67.
- 16. Chen J, Jiang Y, Shi H, Peng Y, Fan X, Li C. The molecular mechanisms of copper metabolism and its roles in human diseases. Pflugers Arch - Eur J Physiol. 2020;472(10):1415-29.
- 17. Hernandez S, Tsuchiya Y, García–Ruiz JP, Lalioti V, Nielsen S, Cassio D, et al. ATP7B Copper-Regulated Traffic and Association With the Tight Junctions: Copper Excretion Into the Bile. Gastroenterology. 2008;134(4):1215-23.
- 18. Palmgren MG, Nissen P. P-type ATPases. Annu Rev Biophys. 2011;40:243-66.
- 19. Lutsenko S, Barnes NL, Bartee MY, Dmitriev OY. Function and Regulation of Human Copper-Transporting ATPases. Physiological Reviews 2007;87(3):1011-46.
- 20. Shim H, Harris ZL. Genetic Defects in Copper Metabolism. The Journal of Nutrition. 2003;133(5):1527S-1531S.
- 21. Møller LB, Mogensen M, Horn N. Molecular diagnosis of Menkes disease: Genotype–phenotype correlation. Biochimie 2009;91(10):1273-7.
- 22. Tümer Z, Møller LB. Menkes disease. Eur J Hum Genet. 2010;18(5):511-8.
- 23. Czlonkowska A, Litwin T, Dusek P, Ferenci P, Lutsenko S, Medici V, et al. Nature Reviews Disease Primers article: Wilson disease. Nat Rev Dis Primers. 2018;4(1):21.
- 24. Ferenci P, Caca K, Loudianos G, Mieli-Vergani G, Tanner S, Sternlieb I, et al. Diagnosis and phenotypic classification of Wilson disease 1: Diagnosis and phenotypic classification of Wilson disease. Liver International 2003;23(3):139-42.
- 25. Przybyłkowski A, Gromadzka G, Chabik G, Wierzchowska A, Litwin T, Członkowska A. Liver cirrhosis in patients newly diagnosed with neurological phenotype of Wilson’s disease. Funct Neurol. 2014;29(1):23-9.
- 26. Factor SM, Cho S, Sternlieb I, Scheinberg IH, Goldfischer S. The cardiomyopathy of Wilson’s disease. Virchows Arch A Path Anat and Histol. 1982;397(3):301-11.
- 27. Misra A, Biswas A, Ganguly G, Ghosh A, Das S, Roy T. Arthropathic presentation of Wilson’s disease. The Journal of the Association of Physicians of India 2004;52:246-8.
- 28. Squitti R, Lupoi D, Pasqualetti P, Dal Forno G, Vernieri F, Chiovenda P, et al. Elevation of serum copper levels in Alzheimer’s disease. Neurology 2002;59(8):1153.
- 29. Fox JH, Kama JA, Lieberman G, Chopra R, Dorsey K, Chopra V, et al. Mechanisms of Copper Ion Mediated Huntington’s Disease Progression. PLoS One 2007;2(3):e334.
- 30. Ford ES. Serum Copper Concentration and Coronary Heart Disease among US Adults. American Journal of Epidemiology. 2000;151(12):1182-8.
- 31. Sheftel AD, Stehling O, Pierik AJ, Elsässer HP, Mühlenhoff U, Webert H, et al. Humans possess two mitochondrial ferredoxins, Fdx1 and Fdx2, with distinct roles in steroidogenesis, heme, and Fe/S cluster biosynthesis. Proc Natl Acad Sci. 2010;107(26):11775-80.
- 32. Py B, Barras F. Building Fe–S proteins: bacterial strategies. Nat Rev Microbiol. 2010;8(6):436-46.
- 33. Shanbhag VC, Gudekar N, Jasmer K, Papageorgiou C, Singh K, Petris MJ. Copper metabolism as a unique vulnerability in cancer. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 2021;1868(2):118893.
- 34. He F, Chang C, Liu B, Li Z, Li H, Cai N, et al. Copper (II) Ions Activate Ligand-Independent Receptor Tyrosine Kinase (RTK) Signaling Pathway. BioMed Research International 2019;2019:e4158415.
- 35. Qiu L, Ding X, Zhang Z, Kang YJ. Copper Is Required for Cobalt-Induced Transcriptional Activity of Hypoxia-Inducible Factor-1. J Pharmacol Exp Ther. 2012;342(2):561-7.
- 36. Ostrakhovitch EA, Lordnejad MR, Schliess F, Sies H, Klotz LO. Copper ions strongly activate the phosphoinositide-3-kinase/Akt pathway independent of the generation of reactive oxygen species. Arch Biochem Biophys. 2002;397(2):232-9.
- 37. Guo J, Cheng J, Zheng N, Zhang X, Dai X, Zhang L, et al. Copper Promotes Tumorigenesis by Activating the PDK1-AKT Oncogenic Pathway in a Copper Transporter 1 Dependent Manner. Advanced Science 2021;8(18):2004303.
- 38. Walter PL, Kampkötter A, Eckers A, Barthel A, Schmoll D, Sies H, et al. Modulation of FoxO signaling in human hepatoma cells by exposure to copper or zinc ions. Arch Biochem Biophys. 2006;454(2):107-13.
- 39. Baldari S, Di Rocco G, Heffern MC, Su TA, Chang CJ, Toietta G. Effects of Copper Chelation on BRAFV600E Positive Colon Carcinoma Cells. Cancers 2019;11(5):659.
- 40. Turski ML, Brady DC, Kim HJ, Kim BE, Nose Y, Counter CM, et al. A Novel Role for Copper in Ras/Mitogen-Activated Protein Kinase Signaling. Molecular and Cellular Biology 2012;32(7):1284-95.
- 41. Ge EJ, Bush AI, Casini A, Cobine PA, Cross JR, DeNicola GM, et al. Connecting copper and cancer: from transition metal signalling to metalloplasia. Nat Rev Cancer 2022;22(2):102-13.
- 42. Tsang T, Posimo JM, Gudiel AA, Cicchini M, Feldser DM, Brady DC. Copper is an essential regulator of the autophagic kinases ULK1/2 to drive lung adenocarcinoma. Nat Cell Biol. 2020;22(4):412-24.
- 43. Yun CW, Lee SH. The Roles of Autophagy in Cancer. Int J Mol Sci. 2018;19(11):3466.
- 44. Parr-Sturgess CA, Tinker CL, Hart CA, Brown MD, Clarke NW, Parkin ET. Copper Modulates Zinc Metalloproteinase-Dependent Ectodomain Shedding of Key Signaling and Adhesion Proteins and Promotes the Invasion of Prostate Cancer Epithelial Cells. Molecular Cancer Research 2012;10(10):1282-93.
- 45. McAuslan BR, Reilly W. Endothelial cell phagokinesis in response to specific metal ions. Experimental Cell Research 1980;130(1):147-57.
- 46. Li Y. Copper homeostasis: Emerging target for cancer treatment. IUBMB Life 2020;72(9):1900-8.
- 47. Suska F, Esposito M, Gretzer C, Källtorp M, Tengvall P, Thomsen P. IL-1α, IL-1β and TNF-α secretion during in vivo/ex vivo cellular interactions with titanium and copper. Biomaterials 2003;24(3):461-8.
- 48. Soncin F, Guitton JD, Cartwright T, Badet J. Interaction of Human Angiogenin with Copper Modulates Angiogenin Binding to Endothelial Cells. Biochemical and Biophysical Research Communications 1997;236(3):604-10.
- 49. Kohno T, Urao N, Ashino T, Sudhahar V, McKinney RD, Hamakubo T, et al. Novel Role of Copper Transport Protein Antioxidant-1 in Neointimal Formation After Vascular Injury. Arteriosclerosis, Thrombosis, and Vascular Biology 2013;33(4):805-13.
- 50. Zhang C, Zeng Y, Guo X, Shen H, Zhang J, Wang K, et al. Pan-cancer analyses confirmed the cuproptosis-related gene FDX1 as an immunotherapy predictor and prognostic biomarker. Frontiers in Genetics 2022;13:947372.
- 51. Xiao C, Yang L, Jin L, Lin W, Zhang F, Huang S, et al. Prognostic and immunological role of cuproptosis-related protein FDX1 in pan-cancer. Frontiers in Genetics 2022;13:962028.
- 52. Cai Y, He Q, Liu W, Liang Q, Peng B, Li J, et al. Comprehensive analysis of the potential cuproptosis-related biomarker LIAS that regulates prognosis and immunotherapy of pan-cancers. Frontiers in Oncology 2022;12:952129.
- 53. Zhang H, Shi Y, Yi Q, Wang C, Xia Q, Zhang Y, et al. A novel defined cuproptosis-related gene signature for predicting the prognosis of lung adenocarcinoma. Front Genet. 2022;13:975185.
- 54. Deng L, Jiang A, Zeng H, Peng X, Song L. Comprehensive analyses of PDHA1 that serves as a predictive biomarker for immunotherapy response in cancer. Frontiers in Pharmacology 2022;13:947372.
- 55. Chen Y, Chen X, Wang X. Identification of a prognostic model using cuproptosis-related genes in uveal melanoma. Frontiers in Cell and Developmental Biology 2022;10:973073.
- 56. Lv H, Liu X, Zeng X, Liu Y, Zhang C, Zhang Q, et al. Comprehensive Analysis of Cuproptosis-Related Genes in Immune Infiltration and Prognosis in Melanoma. Front Pharmacol. 2022;13:930041.
- 57. Chen Y. Identification and Validation of Cuproptosis-Related Prognostic Signature and Associated Regulatory Axis in Uterine Corpus Endometrial Carcinoma. Front Genet. 2022;13:912037.
- 58. Hu Q, Wang R, Ma H, Zhang Z, Xue Q. Cuproptosis predicts the risk and clinical outcomes of lung adenocarcinoma. Frontiers in Oncology 2022;12:922332.
- 59. Ye Z, Zhang S, Cai J, Ye L, Gao L, Wang Y, et al. Development and validation of cuproptosis-associated prognostic signatures in WHO 2/3 glioma. Front Oncol. 2022;12:967159.
- 60. Du Y, Lin Y, Wang B, Li Y, Xu D, Gan L, et al. Cuproptosis patterns and tumor immune infiltration characterization in colorectal cancer. Front Genet. 2022;13:976007.
- 61. Fu J, Wang S, Li Z, Qin W, Tong Q, Liu C, et al. Comprehensive multiomics analysis of cuproptosis-related gene characteristics in hepatocellular carcinoma. Frontiers in Genetics 2022;12:942387.