The disorder of the iron metabolism as a possible mechanism for the development of neurodegeneration after new coronavirus infection of SARS-CoV-2
Igor V. Litvinenko , Igor V. Krasakov
Russian Military Medical Academy Reports ›› 2021, Vol. 40 ›› Issue (4) : 13 -24.
The disorder of the iron metabolism as a possible mechanism for the development of neurodegeneration after new coronavirus infection of SARS-CoV-2
The involvement of the nervous system in the pathological process that occurs when COVID-19 is infected is becoming more and more obvious. The question of the possibility of the debut or progression of the already developed Parkinsonism syndrome in patients who have undergone COVID-19 is regularly raised. A large number of hypotheses are put forward to explain this relationship. It is assumed that a violation of iron metabolism in the brain may underlie the development and progression of neurodegenerative diseases, including after the new coronavirus infection SARS-CoV-2. The analysis of stu dies on the possible influence of iron metabolism disorders on the occurrence and mechanism of development of neurodegenerative diseases after infection with SARS-CoV-2 has been carried out. The processes of physiological maintenance of iron homeostasis, as well as the influence of physiological aging on the accumulation of iron in the central nervous system are described. The relationship between hyperferritinemia occurring in COVID-19 and ferroptosis as the basis of the neurodegenerative process in Parkinson’s disease and Alzheimer’s disease is discussed. The main molecular mechanisms involved in ferroptosis are described. Examples of involvement of metal homeostasis disorders in the process of altering the structure of α-synuclein, synthesis of β-amyloid, hyperphosphorylated tau- protein are given. The causes of excessive iron accumulation in certain brain structures are discussed. The question of the possibility of using the assessment of changes in iron metabolism as a new biomarker of the progression of Parkinson’s disease is analyzed. (1 figure, bibliography: 62 refs)
Alzheimer’s disease / hyperferritinemia / iron / neurodegeneration / Parkinson’s disease / ferritin / ferroptosis / COVID-19 / SARS-CoV-2
| [1] |
Merello M, Bhatia KP, Obeso JA. SARS-CoV-2 and the risk of Parkinson’s disease: facts and fantasy. Lancet Neurol. 2021;20(2): 94–95. DOI: 10.1016/S1474-4422(20)30442-7 |
| [2] |
Merello M., Bhatia K.P., Obeso J.A. SARS-CoV-2 and the risk of Parkinson’s disease: facts and fantasy // Lancet Neurol. 2021. Vol. 20, No. 2. P. 94–95. DOI: 10.1016/S1474-4422(20)30442-7 |
| [3] |
Zaitsev AA, Chernov SA, Stets VV. et al. Algorithms for the management of patients with a new coronavirus COVID-19 infection in a hospital. Guidelines. Consilium Medicum. 2020;22(11):91–97. DOI: 10.26442/20751753.2020.11.200520 |
| [4] |
Зайцев А.А., Чернов С.А., Стец В.В., и др. Алгоритмы ведения пациентов с новой коронавирусной инфекцией COVID-19 в стационаре: Методические рекомендации // Consilium Medicum. 2020. Т. 22, № 11. С. 91–97. DOI: 10.26442/20751753.2020.11.200520 |
| [5] |
Orlov YuP, Dolgikh VT, Vereschagin EI, et al. Is there a connection between iron exchange and COVID-19? Bulletin of Anesthesiology and Reanimatology. 2020;17(4):6–13. (In Russ.) DOI: 10.21292/2078-5658-2020-17-4-6-13 |
| [6] |
Орлов Ю.П., Долгих В.Т., Верещагин Е.И., и др. Есть ли связь обмена железа с течением СOVID-19? // Вестник анестезиологии и реаниматологии. 2020. Т. 17, № 4. С. 6–13. DOI: 0.21292/2078-5658-2020-17-4-6-13 |
| [7] |
Polushin YuS, Shlyk IV, Gavrilova EG, et al. The role of ferritin in assessing COVID-19 severity. Bulletin of Anesthesiology and Reanimatology. 2021;18(4):20–28. (In Russ.) DOI: 10.21292/2078-5658-2021-18-4-20-28 |
| [8] |
Полушин Ю.С., Шлык И.В., Гаврилова Е.Г., и др. Роль ферритина в оценке тяжести COVID-19 // Вестник анестезиологии и реаниматологии. 2021. Т. 18, № 4. С. 20–28. DOI: 10.21292/2078-5658-2021-18-4-20-28 |
| [9] |
Vargas-Vargas M, Cortés-Rojo C. Ferritin levels and COVID-19. Rev Panam Salud Publica. 2020;44:72. DOI: 10.26633/RPSP.2020.72 |
| [10] |
Vargas-Vargas M., Cortés-Rojo C. Ferritin levels and COVID-19 // Rev. Panam. Salud. Publica. 2020. No. 44. Р. 72. DOI: 10.26633/RPSP.2020.72 |
| [11] |
Tsvetaeva NV, Levina AA, Mamukova UI. The basis of regulation of iron metabolism. Clinical oncohematology. 2010;3:278–283. (In Russ.) |
| [12] |
Цветаева Н.В., Левина А.А., Мамукова Ю.И. Основы регуляции обмена железа // Клиническая онкогематология. 2010. № 3. С. 278–283. |
| [13] |
Gordienko AV, Sakhin VT, Kryukov EV, et al. The importance of iron metabolism, hepcidine and soluble transferrin receptor in pathogenesis of anemia in patients with solid tumors. Bulletin of the Russian Military Medical Academy. 2018;3(63):91–94. (In Russ.) DOI: 10.17816/brmma12258 |
| [14] |
Гордиенко А.В., Сахин В.Т., Крюков Е.В., и др. Значение обмена железа, гепцидина и растворимого рецептора трансферрина в патогенезе анемии у пациентов, страдающих злокачественными новообразованиями // Вестник Российской Военно-медицинской академии. 2018. № 3 (63). С. 91–94. DOI: 10.17816/brmma12258 |
| [15] |
Ward RJ, Zucca FA, Duyn JH, et al. The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol. 2014;13(10): 1045–1060. DOI: 10.1016/S1474-4422(14)70117-6 |
| [16] |
Ward R.J., Zucca F.A., Duyn J.H., et al. The role of iron in brain ageing and neurodegenerative disorders // Lancet Neurol. 2014. Vol. 13, No. 10. P. 1045–1060. DOI: 10.1016/S1474-4422(14)70117-6 |
| [17] |
Lee P, Peng H, Gelbart T, Beutler E. The IL-6- and lipopolysaccharide-induced transcription of hepcidin in HFE-, transferrin receptor 2-, and beta 2-microglobulin-deficient hepatocytes. Proc Natl Acad Sci USA. 2004;101(25):9263–9265. DOI: 10.1073/pnas.0403108101 |
| [18] |
Lee P., Peng H., Gelbart T., Beutler E. The IL-6- and lipopolysaccharide-induced transcription of hepcidin in HFE-, transferrin receptor 2-, and beta 2-microglobulin-deficient hepatocytes // Proc. Natl. Acad. Sci. USA. 2004. Vol. 101, No. 25. P. 9263–9265. DOI: 10.1073/pnas.0403108101 |
| [19] |
Urrutia P, Aguirre P, Esparza A, et al. Inflammation alters the expression of DMT1, FPN1 and hepcidin, and it causes iron accumulation in central nervous system cells. J Neurochem. 2013;126(4): 541–549. DOI: 10.1111/jnc.12244 |
| [20] |
Urrutia P., Aguirre P., Esparza A., et al. Inflammation alters the expression of DMT1, FPN1 and hepcidin, and it causes iron accumulation in central nervous system cells // J. Neurochem. 2013. Vol. 126, No. 4. P. 541–549. DOI: 10.1111/jnc.12244 |
| [21] |
Farrall AJ, Wardlaw JM. Blood-brain barrier: ageing and microvascular disease – systematic review and meta-analysis. Neurobiol Aging. 2009;30(3):337–352. DOI: 10.1016/j.neurobiolaging.2007.07.015 |
| [22] |
Farrall A.J., Wardlaw J.M. Blood-brain barrier: ageing and microvascular disease – systematic review and meta-analysis // Neurobiol. Aging. 2009. Vol. 30, No. 3. P. 337–352. DOI: 10.1016/j.neurobiolaging.2007.07.015 |
| [23] |
Killilea DW, Wong SL, Cahaya HS, et al. Iron accumulation during cellular senescence. Ann N Y Acad Sci. 2004;1019:365–367. DOI: 10.1196/annals.1297.063 |
| [24] |
Killilea D.W., Wong S.L., Cahaya H.S., et al. Iron accumulation during cellular senescence // Ann. N. Y. Acad. Sci. 2004. No. 1019. P. 365–367. DOI: 10.1196/annals.1297.063 |
| [25] |
Xu J, Jia Z, Knutson MD, Leeuwenburgh C. Impaired iron status in aging research. Int J Mol Sci. 2012;13(2):2368–2386. DOI: 10.3390/ijms13022368 |
| [26] |
Xu J., Jia Z., Knutson M.D., Leeuwenburgh C. Impaired iron status in aging research // Int. J. Mol. Sci. 2012. Vol. 13, No. 2. P. 2368–2386. DOI: 10.3390/ijms13022368 |
| [27] |
Ramos P, Santos A, Pinto NR, et al. Iron levels in the human brain: a post-mortem study of anatomical region differences and age-related changes. J Trace Elem Med Biol. 2014;28(1):13–17. DOI: 10.1016/j.jtemb.2013.08.001 |
| [28] |
Ramos P., Santos A., Pinto N.R., et al. Iron levels in the human brain: a post-mortem study of anatomical region differences and age-related changes // J. Trace. Elem. Med. Biol. 2014. Vol. 28, No. 1. P. 13–17. DOI: 10.1016/j.jtemb.2013.08.001 |
| [29] |
House E, Esiri M, Forster G, et al. Aluminium, iron and copper in human brain tissues donated to the Medical Research Council’s Cognitive Function and Ageing Study. Metallomics. 2012;4(1):56–65. DOI: 10.1039/c1mt00139f |
| [30] |
House E., Esiri M., Forster G., et al. Aluminium, iron and copper in human brain tissues donated to the Medical Research Council’s Cognitive Function and Ageing Study // Metallomics. 2012. Vol. 4, No. 1. P. 56–65. DOI: 10.1039/c1mt00139f |
| [31] |
Bilgic B, Pfefferbaum A, Rohlfing T, et al. MRI estimates of brain iron concentration in normal aging using quantitative susceptibility mapping. Neuroimage. 2012;59(3):2625–2635. DOI: 10.1016/j.neuroimage.2011.08.077 |
| [32] |
Bilgic B., Pfefferbaum A., Rohlfing T., et al. MRI estimates of brain iron concentration in normal aging using quantitative susceptibility mapping // Neuroimage. 2012. Vol. 59, No. 3. P. 2625–2635. DOI: 10.1016/j.neuroimage.2011.08.077 |
| [33] |
Zecca L, Bellei C, Costi P, et al. New melanic pigments in the human brain that accumulate in aging and block environmental toxic metals. Proc Natl Acad Sci U S A. 2008;105(45):17567–17572. DOI: 10.1073/pnas.0808768105 |
| [34] |
Zecca L., Bellei C., Costi P., et al. New melanic pigments in the human brain that accumulate in aging and block environmental toxic metals // Proc. Natl. Acad. Sci. USA. 2008. Vol. 105, No. 45. P. 17567–17572. DOI: 10.1073/pnas.0808768105 |
| [35] |
Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8(1):57–69. DOI: 10.1038/nrn2038 |
| [36] |
Block M.L., Zecca L., Hong J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms // Nat. Rev. Neurosci. 2007. Vol. 8, No. 1. P. 57–69. DOI: 10.1038/nrn2038 |
| [37] |
Connor JR, Menzies SL, St Martin SM, Mufson EJ. Cellular distribution of transferrin, ferritin, and iron in normal and aged human brains. J Neurosci Res. 1990;27(4):595–611. DOI: 10.1002/jnr.490270421 |
| [38] |
Connor J.R., Menzies S.L., St Martin S.M., Mufson E.J. Cellular distribution of transferrin, ferritin, and iron in normal and aged human brains // J. Neurosci. Res. 1990. Vol. 27, No. 4. P. 595–611. DOI: 10.1002/jnr.490270421 |
| [39] |
Crichton R, Ward R, eds. Metal-Based Neurodegeneration: From Molecular Mechanisms to Therapeutic Strategies. 2nd ed. Chichester, West Sussex, U.K.: John Wiley & Sons Limited; 2014. |
| [40] |
Crichton R., Ward R., eds. Metal-Based Neurodegeneration: From Molecular Mechanisms to Therapeutic Strategies. 2nd ed. Chichester, West Sussex, U.K.: John Wiley & Sons Limited; 2014. |
| [41] |
Melis JP, van Steeg H, Luijten M. Oxidative DNA damage and nucleotide excision repair. Antioxid Redox Signal. 2013;18(18):2409–2419. DOI: 10.1089/ars.2012.5036 |
| [42] |
Melis J.P., van Steeg H., Luijten M. Oxidative DNA damage and nucleotide excision repair // Antioxid. Redox. Signal. 2013. Vol. 18, No. 18. P. 2409–2419. DOI: 10.1089/ars.2012.5036 |
| [43] |
Kwok JB. Role of epigenetics in Alzheimer’s and Parkinson’s disease. Epigenomics. 2010;2(5):671–682. DOI: 10.2217/epi.10.43 |
| [44] |
Kwok J.B. Role of epigenetics in Alzheimer’s and Parkinson’s disease // Epigenomics. 2010. Vol. 2, No. 5. P. 671–682. DOI: 10.2217/epi.10.43 |
| [45] |
Perluigi M, Coccia R, Butterfield DA. 4-Hydroxy-2-nonenal, a reactive product of lipid peroxidation, and neurodegenerative diseases: a toxic combination illuminated by redox proteomics studies. Antioxid Redox Signal. 2012;17(11):1590–1609. DOI:10.1089/ars.2011.4406 |
| [46] |
Perluigi M., Coccia R., Butterfield D.A. 4-Hydroxy-2-nonenal, a reactive product of lipid peroxidation, and neurodegenerative di seases: a toxic combination illuminated by redox proteomics stu dies // Antioxid. Redox. Signal. 2012. Vol. 17, No. 11. P. 1590–1609. DOI: 10.1089/ars.2011.4406 |
| [47] |
Horowitz MP, Greenamyre JT. Mitochondrial iron metabolism and its role in neurodegeneration. J Alzheimers Dis. 2010;20(2):551–568. DOI: 10.3233/JAD-2010-100354 |
| [48] |
Horowitz M.P., Greenamyre J.T. Mitochondrial iron metabolism and its role in neurodegeneration // J. Alzheimers. Dis. 2010. Vol. 20, No. 2. P. 551–568. DOI: 10.3233/JAD-2010-100354 |
| [49] |
Paris I, Martinez-Alvarado P, Cárdenas S, et al. Dopamine-dependent iron toxicity in cells derived from rat hypothalamus. Chem Res Toxicol. 2005;18(3):415–419. DOI: 10.1021/tx0497144 |
| [50] |
Paris I., Martinez-Alvarado P., Cárdenas S., et al. Dopamine-dependent iron toxicity in cells derived from rat hypothalamus // Chem. Res. Toxicol. 2005. Vol. 18, No. 3. P. 415–419. DOI: 10.1021/tx0497144 |
| [51] |
Di Monte DA, Schipper HM, Hetts S, Langston JW. Iron-mediated bioactivation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in glial cultures. Glia. 1995;15(2):203–206. DOI: 10.1002/glia.440150213 |
| [52] |
Di Monte D.A., Schipper H.M., Hetts S., Langston J.W. Iron-mediated bioactivation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in glial cultures // Glia. 1995. Vol. 15, No. 2. P. 203–206. DOI: 10.1002/glia.440150213 |
| [53] |
Yamamoto A, Shin RW, Hasegawa K, et al. Iron (III) induces aggregation of hyperphosphorylated tau and its reduction to iron (II) reverses the aggregation: implications in the formation of neurofibrillary tangles of Alzheimer’s disease. J Neurochem. 2002;82(5): 1137–1147. DOI: 10.1046/j.1471-4159.2002.t01-1-01061.x |
| [54] |
Yamamoto A., Shin R.W., Hasegawa K., et al. Iron (III) induces aggregation of hyperphosphorylated tau and its reduction to iron (II) reverses the aggregation: implications in the formation of neurofibrillary tangles of Alzheimer’s disease // J. Neurochem. 2002. Vol. 82, No. 5. P. 1137–1147. DOI: 10.1046/j.1471-4159.2002.t01-1-01061.x |
| [55] |
Ott M, Gogvadze V, Orrenius S, Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis. 2007;12(5):913–922. DOI: 10.1007/s10495-007-0756-2 |
| [56] |
Ott M., Gogvadze V., Orrenius S., Zhivotovsky B. Mitochondria, oxidative stress and cell death // Apoptosis. 2007. Vol. 12, No. 5. P. 913–922. DOI: 10.1007/s10495-007-0756-2 |
| [57] |
Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012;149(5): 1060–1072. DOI: 10.1016/j.cell.2012.03.042 |
| [58] |
Dixon S.J., Lemberg K.M., Lamprecht M.R., et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death // Cell. 2012. Vol. 149, No. 5. P. 1060–1072. DOI: 10.1016/j.cell.2012.03.042 |
| [59] |
Wu JR, Tuo QZ, Lei P. Ferroptosis, a Recent Defined Form of Critical Cell Death in Neurological Disorders. J Mol Neurosci. 2018;66(2):197–206. DOI: 10.1007/s12031-018-1155-6 |
| [60] |
Wu J.R., Tuo Q.Z., Lei P. Ferroptosis, a Recent Defined Form of Critical Cell Death in Neurological Disorders // J. Mol. Neurosci. 2018. Vol. 66, No. 2. P. 197–206. DOI: 10.1007/s12031-018-1155-6 |
| [61] |
Hirsch EC, Brandel JP, Galle P, et al. Iron and aluminum increase in the substantia nigra of patients with Parkinson’s di sease: an X-ray microanalysis. J Neurochem. 1991;56(2):446–451. DOI: 10.1111/j.1471-4159.1991.tb08170.x |
| [62] |
Hirsch E.C., Brandel J.P., Galle P., et al. Iron and aluminum increase in the substantia nigra of patients with Parkinson’s disease: an X-ray microanalysis // J. Neurochem. 1991. Vol. 56, No. 2. P. 446–451. DOI: 10.1111/j.1471-4159.1991.tb08170.x |
| [63] |
Gröger A, Berg D. Does structural neuroimaging reveal a disturbance of iron metabolism in Parkinson’s disease? Implications from MRI and TCS studies. J Neural Transm (Vienna). 2012;119(12): 1523–1528. DOI: 10.1007/s00702-012-0873-0 |
| [64] |
Gröger A., Berg D. Does structural neuroimaging reveal a disturbance of iron metabolism in Parkinson’s disease? Implications from MRI and TCS studies // J. Neural. Transm. (Vienna). 2012. Vol. 119, No. 12. P. 1523–1528. DOI: 10.1007/s00702-012-0873-0 |
| [65] |
Kortekaas R, Leenders KL, van Oostrom JC, et al. Blood-brain barrier dysfunction in parkinsonian midbrain in vivo. Ann Neurol. 2005;57(2):176–179. DOI: 10.1002/ana.20369 |
| [66] |
Kortekaas R., Leenders K.L., van Oostrom J.C., et al. Blood-brain barrier dysfunction in parkinsonian midbrain in vivo // Ann. Neurol. 2005. Vol. 57, No. 2. P. 176–179. DOI: 10.1002/ana.20369 |
| [67] |
Conde JR, Streit WJ. Microglia in the aging brain. J Neuropathol Exp Neurol. 2006;65(3):199–203. DOI: 10.1097/01.jnen.0000202887.22082.63 |
| [68] |
Conde J.R., Streit W.J. Microglia in the aging brain // J. Neuropathol. Exp. Neurol. 2006. Vol. 65, No. 3. P. 199–203. DOI: 10.1097/01.jnen.0000202887.22082.63 |
| [69] |
Litvinenko IV, Krasakov IV, Bisaga GN, et al. Modern conception of the pathogenesis of neurodegenerative diseases and therapeutic strategy. Neuroscience and Behavioral Physiology. 2017;117(6–2): 3–10. (In Russ.) DOI: 10.17116/jnevro2017117623-10 |
| [70] |
Литвиненко И.В., Красаков И.В., Бисага Г.Н., и др. Современная концепция патогенеза нейродегенеративных заболеваний и стратегия терапии // Журнал неврологии и психиатрии им. С.С. Корсакова. 2017. Т. 117, № 6 (2). С. 3–10. DOI: 10.17116/jnevro2017117623-10 |
| [71] |
Faucheux BA, Nillesse N, Damier P, et al. Expression of lactoferrin receptors is increased in the mesencephalon of patients with Parkinson disease. Proc Natl Acad Sci U S A. 1995;92(21):9603–9607. DOI: 10.1073/pnas.92.21.9603 |
| [72] |
Faucheux B.A., Nillesse N., Damier P., et al. Expression of lactoferrin receptors is increased in the mesencephalon of patients with Parkinson disease // Proc. Natl. Acad. Sci. USA. 1995. Vol. 92, No. 21. P. 9603–9607. DOI: 10.1073/pnas.92.21.9603 |
| [73] |
Salazar J, Mena N, Hunot S, et al Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of Parkinson’s disease. Proc Natl Acad Sci U S A. 2008;105(47):18578–18583. DOI: 10.1073/pnas.0804373105 |
| [74] |
Salazar J., Mena N., Hunot S., et al. Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of Parkinson’s disease // Proc. Natl. Acad. Sci. USA. 2008. Vol. 105, No. 47. P. 18578–18583. DOI: 10.1073/pnas.0804373105 |
| [75] |
Mastroberardino PG, Hoffman EK, Horowitz MP, et al. A novel transferrin/TfR2-mediated mitochondrial iron transport system is disrupted in Parkinson’s disease. Neurobiol Dis. 2009;34(3):417–431. DOI: 10.1016/j.nbd.2009.02.009 |
| [76] |
Mastroberardino P.G., Hoffman E.K., Horowitz M.P., et al. A novel transferrin/TfR2-mediated mitochondrial iron transport system is disrupted in Parkinson’s disease // Neurobiol. Dis. 2009. Vol. 34, No. 3. P. 417–431. DOI: 10.1016/j.nbd.2009.02.009 |
| [77] |
Guerreiro RJ, Bras JM, Santana I, et al. Association of HFE common mutations with Parkinson’s disease, Alzheimer’s disease and mild cognitive impairment in a Portuguese cohort. BMC Neurol. 2006;6:24. DOI: 10.1186/1471-2377-6-24 |
| [78] |
Guerreiro R.J., Bras J.M., Santana I., et al. Association of HFE common mutations with Parkinson’s disease, Alzheimer’s disease and mild cognitive impairment in a Portuguese cohort // BMC Neurol. 2006. No. 6, P. 24. DOI: 10.1186/1471-2377-6-24 |
| [79] |
Uversky VN, Li J, Fink AL. Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson’s disease and heavy metal exposure. J Biol Chem. 2001;276(47):44284–44296. DOI: 10.1074/jbc.M105343200 |
| [80] |
Uversky V.N., Li J., Fink A.L. Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson’s disease and heavy metal exposure // J. Biol. Chem. 2001. Vol. 276, No. 47. P. 44284–44296. DOI: 10.1074/jbc.M105343200 |
| [81] |
Connor JR, Snyder BS, Arosio P, et al. A quantitative analysis of isoferritins in select regions of aged, parkinsonian, and Alzheimer’s diseased brains. J Neurochem. 1995;65(2):717–724. DOI: 10.1046/j.1471-4159.1995.65020717.x |
| [82] |
Connor J.R., Snyder B.S., Arosio P., et al. A quantitative analysis of isoferritins in select regions of aged, parkinsonian, and Alzheimer’s diseased brains // J. Neurochem. 1995. Vol. 65, No. 2. P. 717–724. DOI: 10.1046/j.1471-4159.1995.65020717.x |
| [83] |
Castellani RJ, Siedlak SL, Perry G, Smith MA. Sequestration of iron by Lewy bodies in Parkinson’s disease. Acta Neuropathol. 2000;100(2):111–114. DOI: 10.1007/s004010050001 |
| [84] |
Castellani R.J., Siedlak S.L., Perry G., Smith M.A. Sequestration of iron by Lewy bodies in Parkinson’s disease // Acta Neuropathol. 2000. Vol. 100, No. 2. P. 111–114. DOI: 10.1007/s004010050001 |
| [85] |
Faucheux BA, Martin ME, Beaumont C, et al. Lack of up-regulation of ferritin is associated with sustained iron regulatory protein-1 binding activity in the substantia nigra of patients with Parkinson’s disease. J Neurochem. 2002;83(2):320–330. DOI: 10.1046/j.1471-4159.2002.01118.x |
| [86] |
Faucheux B.A., Martin M.E., Beaumont C., et al. Lack of up-regulation of ferritin is associated with sustained iron regulatory protein-1 binding activity in the substantia nigra of patients with Parkinson’s disease // J. Neurochem. 2002. Vol. 83, No. 2. P. 320–330. DOI: 10.1046/j.1471-4159.2002.01118.x |
| [87] |
Faucheux BA, Martin ME, Beaumont C, et al. Neuromelanin associated redox-active iron is increased in the substantia nigra of patients with Parkinson’s disease. J Neurochem. 2003;86(5): 1142–1148. DOI: 10.1046/j.1471-4159.2003.01923.x |
| [88] |
Faucheux B.A., Martin M.E., Beaumont C., et al. Neuromelanin associated redox-active iron is increased in the substantia nigra of patients with Parkinson’s disease // J. Neurochem. 2003. Vol. 86, No. 5. P. 1142–1148. DOI: 10.1046/j.1471-4159.2003.01923.x |
| [89] |
Langston JW, Forno LS, Tetrud J, et al. Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure. Ann Neurol. 1999;46(4):598–605. DOI: 10.1002/1531-8249(199910)46:4<598:: aid-ana7>3.0.co;2-f |
| [90] |
Langston J.W., Forno L.S., Tetrud J., et al. Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure // Ann. Neurol. 1999. Vol. 46, No. 4. P. 598–605. DOI: 10.1002/1531-8249(199910)46:4<598:: aid-ana7>3.0.co;2-f |
| [91] |
Zhang W, Phillips K, Wielgus AR, et al. Neuromelanin activates microglia and induces degeneration of dopaminergic neurons: implications for progression of Parkinson’s disease. Neurotox Res. 2011;19(1):63–72. DOI: 10.1007/s12640-009-9140-z |
| [92] |
Zhang W., Phillips K., Wielgus A.R., et al. Neuromelanin activates microglia and induces degeneration of dopaminergic neurons: implications for progression of Parkinson’s disease // Neurotox. Res. 2011. Vol. 19, No. 1. P. 63–72. DOI: 10.1007/s12640-009-9140-z |
| [93] |
Lewis MM, Du G, Kidacki M, et al. Higher iron in the red nucleus marks Parkinson’s dyskinesia. Neurobiol Aging. 2013;34(5): 1497–1503. DOI: 10.1016/j.neurobiolaging.2012.10.025 |
| [94] |
Lewis M.M., Du G., Kidacki M., et al. Higher iron in the red nucleus marks Parkinson’s dyskinesia // Neurobiol. Aging. 2013. Vol. 34, No. 5. P. 1497–1503. DOI: 10.1016/j.neurobiolaging.2012.10.025 |
| [95] |
Yu X, Du T, Song N, et al. Decreased iron levels in the temporal cortex in postmortem human brains with Parkinson disease. Neurology. 2013;80(5):492–495. DOI: 10.1212/WNL.0b013e31827f0ebb |
| [96] |
Yu X., Du T., Song N., et al. Decreased iron levels in the temporal cortex in postmortem human brains with Parkinson disease // Neurology. 2013. Vol. 80, No. 5. P. 492–495. DOI: 10.1212/WNL.0b013e31827f0ebb |
| [97] |
Olivieri S, Conti A, Iannaccone S, et al. Ceruloplasmin oxidation, a feature of Parkinson’s disease CSF, inhibits ferroxidase activity and promotes cellular iron retention. J Neurosci. 2011;31(50):18568–18577. DOI: 10.1523/JNEUROSCI.3768-11.2011 |
| [98] |
Olivieri S., Conti A., Iannaccone S., et al. Ceruloplasmin oxidation, a feature of Parkinson’s disease CSF, inhibits ferroxidase activity and promotes cellular iron retention // J. Neurosci. 2011. Vol. 31, No. 50. P. 18568–18577. DOI: 10.1523/JNEUROSCI.3768-11.2011 |
| [99] |
Boll MC, Sotelo J, Otero E, et al. Reduced ferroxidase activity in the cerebrospinal fluid from patients with Parkinson’s disease. Neurosci Lett. 1999;265(3):155–158. DOI: 10.1016/s0304-3940(99)00221-9 |
| [100] |
Boll M.C., Sotelo J., Otero E., et al. Reduced ferroxidase activity in the cerebrospinal fluid from patients with Parkinson’s disease // Neurosci. Lett. 1999. Vol. 265, No. 3. P. 155–158. DOI: 10.1016/s0304-3940(99)00221-9 |
| [101] |
Hochstrasser H, Bauer P, Walter U, et al. Ceruloplasmin gene variations and substantia nigra hyperechogenicity in Parkinson disease. Neurology. 2004;63(10):1912–1917. DOI: 10.1212/01.wnl.0000144276.29988.c3 |
| [102] |
Hochstrasser H., Bauer P., Walter U., et al. Ceruloplasmin gene variations and substantia nigra hyperechogenicity in Parkinson disease // Neurology. 2004. Vol. 63, No. 10. P. 1912–1917. DOI: 10.1212/01.wnl.0000144276.29988.c3 |
| [103] |
Song N, Wang J, Jiang H, Xie J. Ferroportin 1 but not hephaestin contributes to iron accumulation in a cell model of Parkinson’s disease. Free Radic Biol Med. 2010;48(2):332–341. DOI: 10.1016/j.freeradbiomed.2009.11.004 |
| [104] |
Song N., Wang J., Jiang H., Xie J. Ferroportin 1 but not hephaestin contributes to iron accumulation in a cell model of Parkinson’s disease // Free Radic. Biol. Med. 2010. Vol. 48, No. 2. P. 332–341. DOI: 10.1016/j.freeradbiomed.2009.11.004 |
| [105] |
Miyake Y, Tanaka K, Fukushima W, et al. Dietary intake of metals and risk of Parkinson’s disease: a case-control study in Japan. J Neurol Sci. 2011;306(1–2):98–102. DOI: 10.1016/j.jns.2011.03.035 |
| [106] |
Miyake Y., Tanaka K., Fukushima W., et al. Dietary intake of metals and risk of Parkinson’s disease: a case-control study in Japan // J. Neurol. Sci. 2011. Vol. 306, No. 1–2. P. 98–102. DOI: 10.1016/j.jns.2011.03.035 |
| [107] |
Levenson CW, Cutler RG, Ladenheim B, et al. Role of dietary iron restriction in a mouse model of Parkinson’s disease. Exp Neurol. 2004;190(2):506–514. DOI: 10.1016/j.expneurol.2004.08.014 |
| [108] |
Levenson C.W., Cutler R.G., Ladenheim B., et al. Role of dietary iron restriction in a mouse model of Parkinson’s disease // Exp. Neurol. 2004. Vol. 190, No. 2. P. 506–514. DOI: 10.1016/j.expneurol.2004.08.014 |
| [109] |
Maass F, Michalke B, Willkommen D, et al. Cerebrospinal Fluid Iron-Ferritin Ratio as a Potential Progression Marker for Parkinson’s Disease. Mov Disord. 2021. Online ahead of print. DOI: 10.1002/mds.28790 |
| [110] |
Maass F., Michalke B., Willkommen D., et al. Cerebrospinal Fluid Iron-Ferritin Ratio as a Potential Progression Marker for Parkinson’s Disease // Mov. Disord. 2021. Online ahead of print. DOI: 10.1002/mds.28790 |
| [111] |
Roberts BR, Ryan TM, Bush AI, et al. The role of metallobiology and amyloid-β peptides in Alzheimer’s disease. J Neurochem. 2012;120(Suppl 1):149–166. DOI: 10.1111/j.1471-4159.2011.07500.x |
| [112] |
Roberts B.R., Ryan T.M., Bush A.I., et al. The role of metallobiology and amyloid-β peptides in Alzheimer’s disease // J. Neurochem. 2012. No. 120, Suppl. 1. P. 149–166. DOI: 10.1111/j.1471-4159.2011.07500.x |
| [113] |
Sayre LM, Perry G, Harris PL, et al. In situ oxidative catalysis by neurofibrillary tangles and senile plaques in Alzheimer’s disease: a central role for bound transition metals. J Neurochem. 2000;74(1):270–279. DOI: 10.1046/j.1471-4159.2000.0740270.x |
| [114] |
Sayre L.M., Perry G., Harris P.L., et al. In situ oxidative catalysis by neurofibrillary tangles and senile plaques in Alzheimer’s disease: a central role for bound transition metals // J. Neurochem. 2000. Vol. 74, No. 1. P. 270–279. DOI: 10.1046/j.1471-4159.2000.0740270.x |
| [115] |
Perry G, Nunomura A, Hirai K, et al. Is oxidative damage the fundamental pathogenic mechanism of Alzheimer’s and other neurodegenerative diseases? Free Radic Biol Med. 2002;33(11):1475–1479. DOI: 10.1016/s0891-5849(02)01113-9 |
| [116] |
Perry G., Nunomura A., Hirai K., et al. Is oxidative damage the fundamental pathogenic mechanism of Alzheimer’s and other neurodegenerative diseases? // Free Radic. Biol. Med. 2002. Vol. 33, No. 11. P. 1475–1479. DOI: 10.1016/s0891-5849(02)01113-9 |
| [117] |
Altamura S, Muckenthaler MU. Iron toxicity in diseases of aging: Alzheimer’s disease, Parkinson’s disease and atherosclerosis. J Alzheimers Dis. 2009;16(4):879–895. DOI: 10.3233/JAD-2009-1010 |
| [118] |
Altamura S., Muckenthaler M.U. Iron toxicity in diseases of aging: Alzheimer’s disease, Parkinson’s disease and atherosclerosis // J. Alzheimers. Dis. 2009. Vol. 16, No. 4. P. 879–895. DOI: 10.3233/JAD-2009-1010 |
| [119] |
Guillemot J, Canuel M, Essalmani R, et al. Implication of the proprotein convertases in iron homeostasis: proprotein convertase 7 sheds human transferrin receptor 1 and furin activates hepcidin. Hepatology. 2013;57(6):2514–2524. DOI: 10.1002/hep.26297 |
| [120] |
Guillemot J., Canuel M., Essalmani R., et al. Implication of the proprotein convertases in iron homeostasis: proprotein convertase 7 sheds human transferrin receptor 1 and furin activates hepcidin // Hepatology. 2013. Vol. 57, No. 6. P. 2514–2524. DOI: 10.1002/hep.26297 |
| [121] |
Rogers JT, Randall JD, Cahill CM, et al. An iron-responsive element type II in the 5’-untranslated region of the Alzheimer’s amyloid precursor protein transcript. J Biol Chem. 2002;277(47):45518–45528. DOI: 10.1074/jbc.M207435200 |
| [122] |
Rogers J.T., Randall J.D., Cahill C.M., et al. An iron-responsive element type II in the 5’-untranslated region of the Alzheimer’s amyloid precursor protein transcript // J. Biol. Chem. 2002. Vol. 277, No. 47. P. 45518–45528. DOI: 10.1074/jbc.M207435200 |
| [123] |
Lei P, Ayton S, Finkelstein DI, et al. Tau deficiency induces parkinsonism with dementia by impairing APP-mediated iron export. Nat Med. 2012;18(2):291–295. DOI: 10.1038/nm.2613 |
| [124] |
Lei P., Ayton S., Finkelstein D.I., et al. Tau deficiency induces parkinsonism with dementia by impairing APP-mediated iron export // Nat. Med. 2012. Vol. 18, No. 2. P. 291–295. DOI: 10.1038/nm.2613 |
Litvinenko I.V., Krasakov I.V.
/
| 〈 |
|
〉 |