The Tao of Copper Metabolism: From Physiology to Pathology


Cite item

Full Text

Abstract

:As a transitional metal, copper plays a crucial role in maintaining the normal physiological activities of mammals. The intracellular copper concentration is meticulously regulated to maintain extremely low levels through homeostatic regulation. Excessive accumulation of free copper in cells can have deleterious effects, as observed in conditions such as Wilson’s disease. Moreover, data accumulated over the past few decades have revealed a crucial role of copper imbalance in tumorigenesis, progression and metastasis. Recently, cuproptosis, also known as copper-induced cell death, has been proposed as a novel form of cell death. This discovery offers new prospects for treating copperrelated diseases and provides a promising avenue for developing copper-responsive therapies, particularly in cancer treatment. We present a comprehensive overview of the Yin– Yang equilibrium in copper metabolism, particularly emphasising its pathophysiological alterations and their relevance to copper-related diseases and malignancies.

About the authors

Shan Gao

Department of Gastroenterology, The Second Xiangya Hospital, Central South University

Email: info@benthamscience.net

Mei Zhou

Department of Gastroenterology, The Second Xiangya Hospital, Central South University

Email: info@benthamscience.net

Zhenchu Tang

Department of Neurology, The Second Xiangya Hospital, Central South University

Author for correspondence.
Email: info@benthamscience.net

References

  1. Festa, R.A.; Thiele, D.J. Copper: An essential metal in biology. Curr. Biol., 2011, 21(21), R877-R883. doi: 10.1016/j.cub.2011.09.040 PMID: 22075424
  2. Myint, Z.W.; Oo, T.H.; Thein, K.Z.; Tun, A.M.; Saeed, H. Copper deficiency anemia: Review article. Ann. Hematol., 2018, 97(9), 1527-1534. doi: 10.1007/s00277-018-3407-5 PMID: 29959467
  3. Tsang, T.; Davis, C.I.; Brady, D.C. Copper biology. Curr. Biol., 2021, 31(9), R421-R427. doi: 10.1016/j.cub.2021.03.054 PMID: 33974864
  4. Lin, C.; Zhang, Z.; Wang, T.; Chen, C.; James Kang, Y. Copper uptake by DMT1: A compensatory mechanism for CTR1 deficiency in human umbilical vein endothelial cells. Metallomics, 2015, 7(8), 1285-1289. doi: 10.1039/c5mt00097a PMID: 26067577
  5. Song, I.S.; Chen, H.H.W.; Aiba, I.; Hossain, A.; Liang, Z.D.; Klomp, L.W.J.; Kuo, M.T. Transcription factor Sp1 plays an important role in the regulation of copper homeostasis in mammalian cells. Mol. Pharmacol., 2008, 74(3), 705-713. doi: 10.1124/mol.108.046771 PMID: 18483225
  6. Liang, Z.D.; Tsai, W.B.; Lee, M.Y.; Savaraj, N.; Kuo, M.T. Specificity protein 1 (sp1) oscillation is involved in copper homeostasis maintenance by regulating human high-affinity copper transporter 1 expression. Mol. Pharmacol., 2012, 81(3), 455-464. doi: 10.1124/mol.111.076422 PMID: 22172574
  7. Petris, M.J.; Smith, K.; Lee, J.; Thiele, D.J. Copper-stimulated endocytosis and degradation of the human copper transporter, hCtr1. J. Biol. Chem., 2003, 278(11), 9639-9646. doi: 10.1074/jbc.M209455200 PMID: 12501239
  8. Ohgami, R.S.; Campagna, D.R.; McDonald, A.; Fleming, M.D. The Steap proteins are metalloreductases. Blood, 2006, 108(4), 1388-1394. doi: 10.1182/blood-2006-02-003681 PMID: 16609065
  9. Batzios, S.; Tal, G.; DiStasio, A.T.; Peng, Y.; Charalambous, C.; Nicolaides, P.; Kamsteeg, E.J.; Korman, S.H.; Mandel, H.; Steinbach, P.J.; Yi, L.; Fair, S.R.; Hester, M.E.; Drousiotou, A.; Kaler, S.G. Newly identified disorder of copper metabolism caused by variants in CTR1, a high-affinity copper transporter. Hum. Mol. Genet., 2022, 31(24), 4121-4130. doi: 10.1093/hmg/ddac156 PMID: 35913762
  10. Wyman, S.; Simpson, R.J.; McKie, A.T.; Sharp, P.A. Dcytb (Cybrd1) functions as both a ferric and a cupric reductase in vitro. FEBS Lett., 2008, 582(13), 1901-1906. doi: 10.1016/j.febslet.2008.05.010 PMID: 18498772
  11. 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., 2020, 472(10), 1415-1429. doi: 10.1007/s00424-020-02412-2 PMID: 32506322
  12. Rozensztrauch, A.; Dzien, I.; Śmigiel, R. Health-related quality of life and family functioning of primary caregivers of children with menkes disease. J. Clin. Med., 2023, 12(5), 1769. doi: 10.3390/jcm12051769 PMID: 36902556
  13. De Feyter, S.; Beyens, A.; Callewaert, B. ATP7A‐related copper transport disorders: A systematic review and definition of the clinical subtypes. J. Inherit. Metab. Dis., 2023, 46(2), 163-173. doi: 10.1002/jimd.12590 PMID: 36692329
  14. Yang, G.M.; Xu, L.; Wang, R.M.; Tao, X.; Zheng, Z.W.; Chang, S.; Ma, D.; Zhao, C.; Dong, Y.; Wu, S.; Guo, J.; Wu, Z.Y. Structures of the human Wilson disease copper transporter ATP7B. Cell Rep., 2023, 42(5), 112417. doi: 10.1016/j.celrep.2023.112417 PMID: 37074913
  15. Ge, E.J.; Bush, A.I.; Casini, A.; Cobine, P.A.; Cross, J.R.; DeNicola, G.M.; Dou, Q.P.; Franz, K.J.; Gohil, V.M.; Gupta, S.; Kaler, S.G.; Lutsenko, S.; Mittal, V.; Petris, M.J.; Polishchuk, R.; Ralle, M.; Schilsky, M.L.; Tonks, N.K.; Vahdat, L.T.; Van Aelst, L.; Xi, D.; Yuan, P.; Brady, D.C.; Chang, C.J. Connecting copper and cancer: From transition metal signalling to metalloplasia. Nat. Rev. Cancer, 2022, 22(2), 102-113. doi: 10.1038/s41568-021-00417-2 PMID: 34764459
  16. Lutsenko, S. Human copper homeostasis: A network of interconnected pathways. Curr. Opin. Chem. Biol., 2010, 14(2), 211-217. doi: 10.1016/j.cbpa.2010.01.003 PMID: 20117961
  17. Luo, Q.; Song, Y.; Kang, J.; Wu, Y.; Wu, F.; Li, Y.; Dong, Q.; Wang, J.; Song, C.; Guo, H. mtROS-mediated Akt/AMPK/mTOR pathway was involved in Copper-induced autophagy and it attenuates copper-induced apoptosis in RAW264.7 mouse monocytes. Redox Biol., 2021, 41, 101912. doi: 10.1016/j.redox.2021.101912 PMID: 33706171
  18. Yang, F.; Pei, R.; Zhang, Z.; Liao, J.; Yu, W.; Qiao, N.; Han, Q.; Li, Y.; Hu, L.; Guo, J.; Pan, J.; Tang, Z. Copper induces oxidative stress and apoptosis through mitochondria-mediated pathway in chicken hepatocytes. Toxicol. In Vitro, 2019, 54, 310-316. doi: 10.1016/j.tiv.2018.10.017 PMID: 30389602
  19. Nagai, M.; Vo, N.H.; Shin Ogawa, L.; Chimmanamada, D.; Inoue, T.; Chu, J.; Beaudette-Zlatanova, B.C.; Lu, R.; Blackman, R.K.; Barsoum, J.; Koya, K.; Wada, Y. The oncology drug elesclomol selectively transports copper to the mitochondria to induce oxidative stress in cancer cells. Free Radic. Biol. Med., 2012, 52(10), 2142-2150. doi: 10.1016/j.freeradbiomed.2012.03.017 PMID: 22542443
  20. Shimada, K.; Reznik, E.; Stokes, M.E.; Krishnamoorthy, L.; Bos, P.H.; Song, Y.; Quartararo, C.E.; Pagano, N.C.; Carpizo, D.R.; deCarvalho, A.C.; Lo, D.C.; Stockwell, B.R. Copper-binding small molecule induces oxidative stress and cell-cycle arrest in glioblastoma-patient-derived cells. Cell Chem. Biol., 2018, 25(5), 585-594.e7. doi: 10.1016/j.chembiol.2018.02.010 PMID: 29576531
  21. Yip, N.C.; Fombon, I.S.; Liu, P.; Brown, S.; Kannappan, V.; Armesilla, A.L.; Xu, B.; Cassidy, J.; Darling, J.L.; Wang, W. Disulfiram modulated ROS–MAPK and NFκB pathways and targeted breast cancer cells with cancer stem cell-like properties. Br. J. Cancer, 2011, 104(10), 1564-1574. doi: 10.1038/bjc.2011.126 PMID: 21487404
  22. Chen, D.; Cui, Q.C.; Yang, H.; Dou, Q.P. Disulfiram, a clinically used anti-alcoholism drug and copper-binding agent, induces apoptotic cell death in breast cancer cultures and xenografts via inhibition of the proteasome activity. Cancer Res., 2006, 66(21), 10425-10433. doi: 10.1158/0008-5472.CAN-06-2126 PMID: 17079463
  23. Liu, N.; Huang, H.; Dou, Q.P.; Liu, J. Inhibition of 19S proteasome-associated deubiquitinases by metal-containing compounds. Oncoscience, 2015, 2(5), 457-466. doi: 10.18632/oncoscience.167 PMID: 26097878
  24. Skrott, Z.; Mistrik, M.; Andersen, K.K.; Friis, S.; Majera, D.; Gursky, J.; Ozdian, T.; Bartkova, J.; Turi, Z.; Moudry, P.; Kraus, M.; Michalova, M.; Vaclavkova, J.; Dzubak, P.; Vrobel, I.; Pouckova, P.; Sedlacek, J.; Miklovicova, A.; Kutt, A.; Li, J.; Mattova, J.; Driessen, C.; Dou, Q.P.; Olsen, J.; Hajduch, M.; Cvek, B.; Deshaies, R.J.; Bartek, J. Alcohol-abuse drug disulfiram targets cancer via p97 segregase adaptor NPL4. Nature, 2017, 552(7684), 194-199. doi: 10.1038/nature25016 PMID: 29211715
  25. Tsvetkov, P.; Detappe, A.; Cai, K.; Keys, H.R.; Brune, Z.; Ying, W.; Thiru, P.; Reidy, M.; Kugener, G.; Rossen, J.; Kocak, M.; Kory, N.; Tsherniak, A.; Santagata, S.; Whitesell, L.; Ghobrial, I.M.; Markley, J.L.; Lindquist, S.; Golub, T.R. Mitochondrial metabolism promotes adaptation to proteotoxic stress. Nat. Chem. Biol., 2019, 15(7), 681-689. doi: 10.1038/s41589-019-0291-9 PMID: 31133756
  26. Tardito, S.; Bassanetti, I.; Bignardi, C.; Elviri, L.; Tegoni, M.; Mucchino, C.; Bussolati, O.; Franchi-Gazzola, R.; Marchiò, L. Copper binding agents acting as copper ionophores lead to caspase inhibition and paraptotic cell death in human cancer cells. J. Am. Chem. Soc., 2011, 133(16), 6235-6242. doi: 10.1021/ja109413c PMID: 21452832
  27. Tardito, S.; Barilli, A.; Bassanetti, I.; Tegoni, M.; Bussolati, O.; Franchi-Gazzola, R.; Mucchino, C.; Marchiò, L. Copper-dependent cytotoxicity of 8-hydroxyquinoline derivatives correlates with their hydrophobicity and does not require caspase activation. J. Med. Chem., 2012, 55(23), 10448-10459. doi: 10.1021/jm301053a PMID: 23170953
  28. Tsvetkov, P.; Coy, S.; Petrova, B.; Dreishpoon, M.; Verma, A.; Abdusamad, M.; Rossen, J.; Joesch-Cohen, L.; Humeidi, R.; Spangler, R.D.; Eaton, J.K.; Frenkel, E.; Kocak, M.; Corsello, S.M.; Lutsenko, S.; Kanarek, N.; Santagata, S.; Golub, T.R. Copper induces cell death by targeting lipoylated TCA cycle proteins. Science, 2022, 375(6586), 1254-1261. doi: 10.1126/science.abf0529 PMID: 35298263
  29. Hunsaker, E.W.; Franz, K.J. Emerging opportunities to manipulate metal trafficking for therapeutic benefit. Inorg. Chem., 2019, 58(20), 13528-13545. doi: 10.1021/acs.inorgchem.9b01029 PMID: 31247859
  30. Hasinoff, B.B.; Yadav, A.A.; Patel, D.; Wu, X. The cytotoxicity of the anticancer drug elesclomol is due to oxidative stress indirectly mediated through its complex with Cu(II). J. Inorg. Biochem., 2014, 137, 22-30. doi: 10.1016/j.jinorgbio.2014.04.004 PMID: 24798374
  31. Kirshner, J.R.; He, S.; Balasubramanyam, V.; Kepros, J.; Yang, C.Y.; Zhang, M.; Du, Z.; Barsoum, J.; Bertin, J. Elesclomol induces cancer cell apoptosis through oxidative stress. Mol. Cancer Ther., 2008, 7(8), 2319-2327. doi: 10.1158/1535-7163.MCT-08-0298 PMID: 18723479
  32. Elmore, S. Apoptosis: A review of programmed cell death. Toxicol. Pathol., 2007, 35(4), 495-516. doi: 10.1080/01926230701320337 PMID: 17562483
  33. Dzieżyc-Jaworska, K.; Litwin, T.; Członkowska, A. Clinical manifestations of Wilson disease in organs other than the liver and brain. Ann. Transl. Med., 2019, 7(S2)(Suppl. 2), S62. doi: 10.21037/atm.2019.03.30 PMID: 31179299
  34. Poujois, A.; Woimant, F. Challenges in the diagnosis of wilson disease. Ann. Transl. Med., 2019, 7(S2)(Suppl. 2), S67. doi: 10.21037/atm.2019.02.10 PMID: 31179304
  35. Sandahl, T.D.; Laursen, T.L.; Munk, D.E.; Vilstrup, H.; Weiss, K.H.; Ott, P. The prevalence of Wilson’s disease: An update. Hepatology, 2020, 71(2), 722-732. doi: 10.1002/hep.30911 PMID: 31449670
  36. European Association for Study of Liver. EASL clinical practice guidelines: Wilson’s disease. J. Hepatol., 2012, 56(3), 671-685. doi: 10.1016/j.jhep.2011.11.007 PMID: 22340672
  37. Lo, C.; Bandmann, O. Epidemiology and introduction to the clinical presentation of Wilson disease. Handb. Clin. Neurol., 2017, 142, 7-17. doi: 10.1016/B978-0-444-63625-6.00002-1 PMID: 28433111
  38. Coffey, A.J.; Durkie, M.; Hague, S.; McLay, K.; Emmerson, J.; Lo, C.; Klaffke, S.; Joyce, C.J.; Dhawan, A.; Hadzic, N.; Mieli-Vergani, G.; Kirk, R.; Elizabeth Allen, K.; Nicholl, D.; Wong, S.; Griffiths, W.; Smithson, S.; Giffin, N.; Taha, A.; Connolly, S.; Gillett, G.T.; Tanner, S.; Bonham, J.; Sharrack, B.; Palotie, A.; Rattray, M.; Dalton, A.; Bandmann, O. A genetic study of Wilson’s disease in the United Kingdom. Brain, 2013, 136(5), 1476-1487. doi: 10.1093/brain/awt035 PMID: 23518715
  39. Dong, Y.; Wang, R.M.; Yang, G.M.; Yu, H.; Xu, W.Q.; Xie, J.J.; Zhang, Y.; Chen, Y.C.; Ni, W.; Wu, Z.Y. Role for biochemical assays and kayser-fleischer rings in diagnosis of Wilson’s disease. Clin. Gastroenterol. Hepatol., 2021, 19(3), 590-596. doi: 10.1016/j.cgh.2020.05.044 PMID: 32485301
  40. Wu, Z.Y.; Wang, N.; Lin, M.T.; Fang, L.; Murong, S.X.; Yu, L. Mutation analysis and the correlation between genotype and phenotype of Arg778Leu mutation in chinese patients with Wilson disease. Arch. Neurol., 2001, 58(6), 971-976. doi: 10.1001/archneur.58.6.971 PMID: 11405812
  41. Cheng, N.; Wang, H.; Wu, W.; Yang, R.; Liu, L.; Han, Y.; Guo, L.; Hu, J.; Xu, L.; Zhao, J.; Han, Y.; Liu, Q.; Li, K.; Wang, X.; Chen, W. Spectrum of ATP7B mutations and genotype-phenotype correlation in large-scale Chinese patients with Wilson disease. Clin. Genet., 2017, 92(1), 69-79. doi: 10.1111/cge.12951 PMID: 27982432
  42. Dong, Y.; Ni, W.; Chen, W.J.; Wan, B.; Zhao, G.X.; Shi, Z.Q.; Zhang, Y.; Wang, N.; Yu, L.; Xu, J.F.; Wu, Z.Y. Spectrum and classification of ATP7B variants in a large cohort of Chinese patients with Wilson’s disease guides genetic diagnosis. Theranostics, 2016, 6(5), 638-649. doi: 10.7150/thno.14596 PMID: 27022412
  43. Li, X.; Lu, Z.; Lin, Y.; Lu, X.; Xu, Y.; Cheng, J.; Shao, Y.; Su, X.; Liu, Z.; Sheng, H.; Cai, Y.; Li, T.; Zhou, Z.; Tan, J.; Liu, H.; Huang, Y.; Liu, L.; Zeng, C. Clinical features and mutational analysis in 114 young children with Wilson disease from South China. Am. J. Med. Genet. A., 2019, 179(8), ajmg.a.61254. doi: 10.1002/ajmg.a.61254 PMID: 31172689
  44. Merle, U.; Weiss, K.H.; Eisenbach, C.; Tuma, S.; Ferenci, P.; Stremmel, W. Truncating mutations in the Wilson disease gene ATP7B are associated with very low serum ceruloplasmin oxidase activity and an early onset of Wilson disease. BMC Gastroenterol., 2010, 10(1), 8. doi: 10.1186/1471-230X-10-8 PMID: 20082719
  45. Okada, T.; Shiono, Y.; Kaneko, Y.; Miwa, K.; Hasatani, K.; Hayashi, Y.; Mibayashi, H.; Aoyagi, H.; Tsuji, S.; Yoshimitsu, M.; Hayashi, H.; Yamagishi, M. High prevalence of fulminant hepatic failure among patients with mutant alleles for truncation of ATP7B in Wilson’s disease. Scand. J. Gastroenterol., 2010, 45(10), 1232-1237. doi: 10.3109/00365521.2010.492527 PMID: 20491539
  46. Kluska, A.; Kulecka, M.; Litwin, T.; Dziezyc, K.; Balabas, A.; Piatkowska, M.; Paziewska, A.; Dabrowska, M.; Mikula, M.; Kaminska, D.; Wiernicka, A.; Socha, P.; Czlonkowska, A.; Ostrowski, J. Whole-exome sequencing identifies novel pathogenic variants across the ATP7B gene and some modifiers of Wilson’s disease phenotype. Liver Int., 2019, 39(1), 177-186. doi: 10.1111/liv.13967 PMID: 30230192
  47. Litwin, T.; Gromadzka, G.; Członkowska, A. Apolipoprotein E gene (APOE) genotype in Wilson’s disease: Impact on clinical presentation. Parkinsonism Relat. Disord., 2012, 18(4), 367-369. doi: 10.1016/j.parkreldis.2011.12.005 PMID: 22221592
  48. Członkowska, A.; Litwin, T.; Dusek, P.; Ferenci, P.; Lutsenko, S.; Medici, V.; Rybakowski, J.K.; Weiss, K.H.; Schilsky, M.L. Wilson disease. Nat. Rev. Dis. Primers, 2018, 4(1), 21. doi: 10.1038/s41572-018-0018-3 PMID: 30190489
  49. Ferenci, P.; Stremmel, W.; Członkowska, A.; Szalay, F.; Viveiros, A.; Stättermayer, A.F.; Bruha, R.; Houwen, R.; Pop, T.L.; Stauber, R.; Gschwantler, M.; Pfeiffenberger, J.; Yurdaydin, C.; Aigner, E.; Steindl-Munda, P.; Dienes, H.P.; Zoller, H.; Weiss, K.H. Age and sex but not ATP7B genotype effectively influence the clinical phenotype of wilson disease. Hepatology, 2019, 69(4), 1464-1476. doi: 10.1002/hep.30280 PMID: 30232804
  50. Członkowska, A.; Gromadzka, G.; Chabik, G. Monozygotic female twins discordant for phenotype of Wilson’s disease. Mov. Disord., 2009, 24(7), 1066-1069. doi: 10.1002/mds.22474 PMID: 19306278
  51. Kegley, K.M.; Sellers, M.A.; Ferber, M.J.; Johnson, M.W.; Joelson, D.W.; Shrestha, R. Fulminant Wilson’s disease requiring liver transplantation in one monozygotic twin despite identical genetic mutation. Am. J. Transplant., 2010, 10(5), 1325-1329. doi: 10.1111/j.1600-6143.2010.03071.x PMID: 20346064
  52. Takeshita, Y.; Shimizu, N.; Yamaguchi, Y.; Nakazono, H.; Saitou, M.; Fujikawa, Y.; Aoki, T. Two families with Wilson disease in which siblings showed different phenotypes. J. Hum. Genet., 2002, 47(10), 0543-0547. doi: 10.1007/s100380200082 PMID: 12376745
  53. Medici, V.; Shibata, N.M.; Kharbanda, K.K.; LaSalle, J.M.; Woods, R.; Liu, S.; Engelberg, J.A.; Devaraj, S.; Török, N.J.; Jiang, J.X.; Havel, P.J.; Lönnerdal, B.; Kim, K.; Halsted, C.H. Wilson’s disease: Changes in methionine metabolism and inflammation affect global DNA methylation in early liver disease. Hepatology, 2013, 57(2), 555-565. doi: 10.1002/hep.26047 PMID: 22945834
  54. Guo, X.; Schrag, M.; Ghoshal, S.; Schilsky, M.; Beslow, L.; Schindler, E. Neuropsychiatric presentation of wilson disease in an adolescent male. Neuropediatrics, 2016, 47(5), 346-347. doi: 10.1055/s-0036-1586225 PMID: 27490186
  55. Ye, X.N.; Mao, L.P.; Lou, Y.J.; Tong, H.Y. Hemolytic anemia as first presentation of Wilson’s disease with uncommon ATP7B mutation. Int. J. Clin. Exp. Med., 2015, 8(3), 4708-4711. PMID: 26064408
  56. Cleymaet, S.; Nagayoshi, K.; Gettings, E.; Faden, J. A review and update on the diagnosis and treatment of neuropsychiatric Wilson disease. Expert Rev. Neurother., 2019, 19(11), 1117-1126. doi: 10.1080/14737175.2019.1645009 PMID: 31314605
  57. Antos, A.; Litwin, T.; Skowrońska, M.; Kurkowska-Jastrzębska, I.; Członkowska, A. Pitfalls in diagnosing Wilson’s Disease by genetic testing alone: The case of a 47-year-old woman with two pathogenic variants of the ATP7B gene. Neurol. Neurochir. Pol., 2020, 54(5), 478-480. doi: 10.5603/PJNNS.a2020.0063 PMID: 32808274
  58. Tümer, Z.; Møller, L.B. Menkes disease. Eur. J. Hum. Genet., 2010, 18(5), 511-518. doi: 10.1038/ejhg.2009.187 PMID: 19888294
  59. Vairo, F.P.; Chwal, B.C.; Perini, S.; Ferreira, M.A.P.; de Freitas Lopes, A.C.; Saute, J.A.M. A systematic review and evidence-based guideline for diagnosis and treatment of Menkes disease. Mol. Genet. Metab., 2019, 126(1), 6-13. doi: 10.1016/j.ymgme.2018.12.005 PMID: 30594472
  60. Boullata, J.; Muthukumaran, G.; Piarulli, A.; Labarre, J.; Compher, C. Oral copper absorption in men with morbid obesity. J. Trace Elem. Med. Biol., 2017, 44, 146-150. doi: 10.1016/j.jtemb.2017.07.005 PMID: 28965570
  61. Choi, E.H.; Strum, W. Hypocupremia-related myeloneuropathy following gastrojejunal bypass surgery. Ann. Nutr. Metab., 2010, 57(3-4), 190-192. doi: 10.1159/000321519 PMID: 21088385
  62. Yarandi, S.S.; Griffith, D.P.; Sharma, R.; Mohan, A.; Zhao, V.M.; Ziegler, T.R. Optic neuropathy, myelopathy, anemia, and neutropenia caused by acquired copper deficiency after gastric bypass surgery. J. Clin. Gastroenterol., 2014, 48(10), 862-865. doi: 10.1097/MCG.0000000000000092 PMID: 24583748
  63. Tisato, F.; Marzano, C.; Porchia, M.; Pellei, M.; Santini, C. Copper in diseases and treatments, and copper-based anticancer strategies. Med. Res. Rev., 2010, 30(4), 708-749. PMID: 19626597
  64. Prohaska, J.R. Impact of copper deficiency in humans. Ann. N. Y. Acad. Sci., 2014, 1314(1), 1-5. doi: 10.1111/nyas.12354 PMID: 24517364
  65. Lopez, J.; Ramchandani, D.; Vahdat, L. Copper depletion as a therapeutic strategy in cancer. Met. Ions Life Sci., 2019, 19, 303-330. doi: 10.1515/9783110527872-012 PMID: 30855113
  66. Ishida, S.; Andreux, P.; Poitry-Yamate, C.; Auwerx, J.; Hanahan, D. Bioavailable copper modulates oxidative phosphorylation and growth of tumors. Proc. Natl. Acad. Sci. USA, 2013, 110(48), 19507-19512. doi: 10.1073/pnas.1318431110 PMID: 24218578
  67. Wooton-Kee, C.R.; Robertson, M.; Zhou, Y.; Dong, B.; Sun, Z.; Kim, K.H.; Liu, H.; Xu, Y.; Putluri, N.; Saha, P.; Coarfa, C.; Moore, D.D.; Nuotio-Antar, A.M. Metabolic dysregulation in the Atp7b−/− Wilson’s disease mouse model. Proc. Natl. Acad. Sci. USA, 2020, 117(4), 2076-2083. doi: 10.1073/pnas.1914267117 PMID: 31924743
  68. Hao, Y.N.; Zhang, W.X.; Gao, Y.R.; Wei, Y.N.; Shu, Y.; Wang, J.H. State-of-the-art advances of copper-based nanostructures in the enhancement of chemodynamic therapy. J. Mater. Chem. B Mater. Biol. Med., 2021, 9(2), 250-266. doi: 10.1039/D0TB02360D PMID: 33237121
  69. Ngamchuea, K.; Batchelor-McAuley, C.; Compton, R.G. The Copper(II)-catalyzed oxidation of glutathione. Chemistry, 2016, 22(44), 15937-15944. doi: 10.1002/chem.201603366 PMID: 27649691
  70. Bansal, A.; Simon, M.C. Glutathione metabolism in cancer progression and treatment resistance. J. Cell Biol., 2018, 217(7), 2291-2298. doi: 10.1083/jcb.201804161 PMID: 29915025
  71. Laws, K.; Bineva-Todd, G.; Eskandari, A.; Lu, C.; O’Reilly, N.; Suntharalingam, K.A. Copper(II) phenanthroline metallopeptide that targets and disrupts mitochondrial function in breast cancer stem cells. Angew. Chem. Int. Ed., 2018, 57(1), 287-291. doi: 10.1002/anie.201710910 PMID: 29144008
  72. Rochford, G.; Molphy, Z.; Kavanagh, K.; McCann, M.; Devereux, M.; Kellett, A.; Howe, O. Cu(II) phenanthroline–phenazine complexes dysregulate mitochondrial function and stimulate apoptosis. Metallomics, 2020, 12(1), 65-78. doi: 10.1039/c9mt00187e PMID: 31720645
  73. Angelé-Martínez, C.; Nguyen, K.V.T.; Ameer, F.S.; Anker, J.N.; Brumaghim, J.L. Reactive oxygen species generation by copper(II) oxide nanoparticles determined by DNA damage assays and EPR spectroscopy. Nanotoxicology, 2017, 11(2), 278-288. doi: 10.1080/17435390.2017.1293750 PMID: 28248593
  74. Jomova, K.; Hudecova, L.; Lauro, P.; Simunková, M.; Barbierikova, Z.; Malcek, M.; Alwasel, S.H.; Alhazza, I.M.; Rhodes, C.J.; Valko, M. The effect of luteolin on DNA damage mediated by a copper catalyzed fenton reaction. J. Inorg. Biochem., 2022, 226, 111635. doi: 10.1016/j.jinorgbio.2021.111635 PMID: 34717250
  75. Tsang, T.; Posimo, J.M.; Gudiel, A.A.; Cicchini, M.; Feldser, D.M.; Brady, D.C. Copper is an essential regulator of the autophagic kinases ULK1/2 to drive lung adenocarcinoma. Nat. Cell Biol., 2020, 22(4), 412-424. doi: 10.1038/s41556-020-0481-4 PMID: 32203415
  76. Santoro, A.M.; Monaco, I.; Attanasio, F.; Lanza, V.; Pappalardo, G.; Tomasello, M.F.; Cunsolo, A.; Rizzarelli, E.; De Luigi, A.; Salmona, M.; Milardi, D. Copper(II) ions affect the gating dynamics of the 20S proteasome: A molecular and in cell study. Sci. Rep., 2016, 6(1), 33444. doi: 10.1038/srep33444 PMID: 27633879
  77. Zhang, Z.; Wang, H.; Yan, M.; Wang, H.; Zhang, C. Novel copper complexes as potential proteasome inhibitors for cancer treatment. Mol. Med. Rep., 2017, 15(1), 3-11. doi: 10.3892/mmr.2016.6022 PMID: 27959411
  78. Antoniades, V.; Sioga, A.; Dietrich, E.M.; Meditskou, S.; Ekonomou, L.; Antoniades, K. Is copper chelation an effective anti-angiogenic strategy for cancer treatment? Med. Hypotheses, 2013, 81(6), 1159-1163. doi: 10.1016/j.mehy.2013.09.035 PMID: 24210000
  79. Cucci, L.M.; Satriano, C.; Marzo, T.; La Mendola, D. Angiogenin and copper crossing in wound healing. Int. J. Mol. Sci., 2021, 22(19), 10704. doi: 10.3390/ijms221910704 PMID: 34639045
  80. Brewer, G.J.; Dick, R.D.; Grover, D.K.; LeClaire, V.; Tseng, M.; Wicha, M.; Pienta, K.; Redman, B.G.; Jahan, T.; Sondak, V.K.; Strawderman, M.; LeCarpentier, G.; Merajver, S.D. Treatment of metastatic cancer with tetrathiomolybdate, an anticopper, antiangiogenic agent: Phase I study. Clin. Cancer Res., 2000, 6(1), 1-10. PMID: 10656425
  81. Sen, C.K.; Khanna, S.; Venojarvi, M.; Trikha, P.; Ellison, E.C.; Hunt, T.K.; Roy, S. Copper-induced vascular endothelial growth factor expression and wound healing. Am. J. Physiol. Heart Circ. Physiol., 2002, 282(5), H1821-H1827. doi: 10.1152/ajpheart.01015.2001 PMID: 11959648
  82. Das, A.; Ash, D.; Fouda, A.Y.; Sudhahar, V.; Kim, Y.M.; Hou, Y.; Hudson, F.Z.; Stansfield, B.K.; Caldwell, R.B.; McMenamin, M.; Littlejohn, R.; Su, H.; Regan, M.R.; Merrill, B.J.; Poole, L.B.; Kaplan, J.H.; Fukai, T.; Ushio-Fukai, M. Cysteine oxidation of copper transporter CTR1 drives VEGFR2 signalling and angiogenesis. Nat. Cell Biol., 2022, 24(1), 35-50. doi: 10.1038/s41556-021-00822-7 PMID: 35027734
  83. Chan, N.; Willis, A.; Kornhauser, N.; Ward, M.M.; Lee, S.B.; Nackos, E.; Seo, B.R.; Chuang, E.; Cigler, T.; Moore, A.; Donovan, D.; Vallee Cobham, M.; Fitzpatrick, V.; Schneider, S.; Wiener, A.; Guillaume-Abraham, J.; Aljom, E.; Zelkowitz, R.; Warren, J.D.; Lane, M.E.; Fischbach, C.; Mittal, V.; Vahdat, L. Influencing the tumor microenvironment: A phase II study of copper depletion using tetrathiomolybdate in patients with breast cancer at high risk for recurrence and in preclinical models of lung metastases. Clin. Cancer Res., 2017, 23(3), 666-676. doi: 10.1158/1078-0432.CCR-16-1326 PMID: 27769988
  84. Jiao, Y.; Hannafon, B.N.; Ding, W.Q. Disulfiram’s anticancer activity: Evidence and mechanisms. Anticancer. Agents Med. Chem., 2016, 16(11), 1378-1384. doi: 10.2174/1871520615666160504095040 PMID: 27141876
  85. Huang, J.; Campian, J.L.; Gujar, A.D.; Tran, D.D.; Lockhart, A.C.; DeWees, T.A.; Tsien, C.I.; Kim, A.H. A phase I study to repurpose disulfiram in combination with temozolomide to treat newly diagnosed glioblastoma after chemoradiotherapy. J. Neurooncol., 2016, 128(2), 259-266. doi: 10.1007/s11060-016-2104-2 PMID: 26966095
  86. O’Day, S.; Gonzalez, R.; Lawson, D.; Weber, R.; Hutchins, L.; Anderson, C.; Haddad, J.; Kong, S.; Williams, A.; Jacobson, E. Phase II, randomized, controlled, double-blinded trial of weekly elesclomol plus paclitaxel versus paclitaxel alone for stage IV metastatic melanoma. J. Clin. Oncol., 2009, 27(32), 5452-5458. doi: 10.1200/JCO.2008.17.1579 PMID: 19826135
  87. O’Day, S.J.; Eggermont, A.M.M.; Chiarion-Sileni, V.; Kefford, R.; Grob, J.J.; Mortier, L.; Robert, C.; Schachter, J.; Testori, A.; Mackiewicz, J.; Friedlander, P.; Garbe, C.; Ugurel, S.; Collichio, F.; Guo, W.; Lufkin, J.; Bahcall, S.; Vukovic, V.; Hauschild, A. Final results of phase III SYMMETRY study: Randomized, double-blind trial of elesclomol plus paclitaxel versus paclitaxel alone as treatment for chemotherapy-naive patients with advanced melanoma. J. Clin. Oncol., 2013, 31(9), 1211-1218. doi: 10.1200/JCO.2012.44.5585 PMID: 23401447
  88. Gohil, V.M. Repurposing elesclomol, an investigational drug for the treatment of copper metabolism disorders. Expert Opin. Investig. Drugs, 2021, 30(1), 1-4. doi: 10.1080/13543784.2021.1840550 PMID: 33081534
  89. Krishnamoorthy, L.; Cotruvo, J.A., Jr; Chan, J.; Kaluarachchi, H.; Muchenditsi, A.; Pendyala, V.S.; Jia, S.; Aron, A.T.; Ackerman, C.M.; Wal, M.N.V.; Guan, T.; Smaga, L.P.; Farhi, S.L.; New, E.J.; Lutsenko, S.; Chang, C.J. Copper regulates cyclic-AMP-dependent lipolysis. Nat. Chem. Biol., 2016, 12(8), 586-592. doi: 10.1038/nchembio.2098 PMID: 27272565
  90. Michniewicz, F.; Saletta, F.; Rouaen, J.R.C.; Hewavisenti, R.V.; Mercatelli, D.; Cirillo, G.; Giorgi, F.M.; Trahair, T.; Ziegler, D.; Vittorio, O. Copper: An intracellular achilles’ heel allowing the targeting of epigenetics, kinase pathways, and cell metabolism in cancer therapeutics. ChemMedChem, 2021, 16(15), 2315-2329. doi: 10.1002/cmdc.202100172 PMID: 33890721
  91. He, F.; Chang, C.; Liu, B.; Li, Z.; Li, H.; Cai, N.; Wang, H.H. Copper (II) ions activate ligand-independent receptor tyrosine kinase (RTK) signaling pathway. BioMed Res. Int., 2019, 2019, 1-8. doi: 10.1155/2019/4158415 PMID: 31218225
  92. Turski, M.L.; Brady, D.C.; Kim, H.J.; Kim, B.E.; Nose, Y.; Counter, C.M.; Winge, D.R.; Thiele, D.J. A novel role for copper in Ras/mitogen-activated protein kinase signaling. Mol. Cell. Biol., 2012, 32(7), 1284-1295. doi: 10.1128/MCB.05722-11 PMID: 22290441
  93. Brady, D.C.; Crowe, M.S.; Turski, M.L.; Hobbs, G.A.; Yao, X.; Chaikuad, A.; Knapp, S.; Xiao, K.; Campbell, S.L.; Thiele, D.J.; Counter, C.M. Copper is required for oncogenic BRAF signalling and tumorigenesis. Nature, 2014, 509(7501), 492-496. doi: 10.1038/nature13180 PMID: 24717435
  94. Aubert, L.; Nandagopal, N.; Steinhart, Z.; Lavoie, G.; Nourreddine, S.; Berman, J.; Saba-El-Leil, M.K.; Papadopoli, D.; Lin, S.; Hart, T.; Macleod, G.; Topisirovic, I.; Gaboury, L.; Fahrni, C.J.; Schramek, D.; Meloche, S.; Angers, S.; Roux, P.P. Copper bioavailability is a KRAS-specific vulnerability in colorectal cancer. Nat. Commun., 2020, 11(1), 3701. doi: 10.1038/s41467-020-17549-y PMID: 32709883
  95. Blockhuys, S.; Celauro, E.; Hildesjö, C.; Feizi, A.; Stål, O.; Fierro-González, J.C.; Wittung-Stafshede, P. Defining the human copper proteome and analysis of its expression variation in cancers. Metallomics, 2017, 9(2), 112-123. doi: 10.1039/C6MT00202A PMID: 27942658
  96. Kamiya, T. Copper in the tumor microenvironment and tumor metastasis. J. Clin. Biochem. Nutr., 2022, 71(1), 22-28. doi: 10.3164/jcbn.22-9 PMID: 35903604
  97. Polishchuk, E.V.; Merolla, A.; Lichtmannegger, J.; Romano, A.; Indrieri, A.; Ilyechova, E.Y.; Concilli, M.; De Cegli, R.; Crispino, R.; Mariniello, M.; Petruzzelli, R.; Ranucci, G.; Iorio, R.; Pietrocola, F.; Einer, C.; Borchard, S.; Zibert, A.; Schmidt, H.H.; Di Schiavi, E.; Puchkova, L.V.; Franco, B.; Kroemer, G.; Zischka, H.; Polishchuk, R.S. Activation of autophagy, observed in liver tissues from patients with wilson disease and from ATP7B-deficient animals, protects hepatocytes from copper-induced apoptosis. Gastroenterology, 2019, 156(4), 1173-1189.e5. doi: 10.1053/j.gastro.2018.11.032 PMID: 30452922
  98. Kang, J.; Lin, C.; Chen, J.; Liu, Q. Copper induces histone hypoacetylation through directly inhibiting histone acetyltransferase activity. Chem. Biol. Interact., 2004, 148(3), 115-123. doi: 10.1016/j.cbi.2004.05.003 PMID: 15276868

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2024 Bentham Science Publishers