Upregulation of Mitochondrial Ferritin by Proinflammatory Cytokines: Implications for a Role in Alzheimer's Disease

Journal of Alzheimer's Disease

Volumn 45, Issue 3, 2015, Pages 797-811

  Yang, Hongkuan ^a,b   Guan, Hongpeng ^a,b   Yang, Mingchun ^a,b   Liu, Ziyi ^a,b   Takeuchi, Shigeko ^a   Yanagisawa, Daijiro ^a   Vincent, Steven R ^a,c   Zhao, Shiguang ^b   Tooyama, Ikuo ^a  

^a SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^b HARBIN MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Alzheimer's disease; amyloid ; inflammation; iron; mitochondrial ferritin; NF B

Indexed keywords

BETA SECRETASE; CYTOKINE; FERRITIN; GAMMA SECRETASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; IRON; MESSENGER RNA; PROTEIN PRECURSOR; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR ALPHA; 3-(4-METHYLPHENYLSULFONYL)-2-PROPENENITRILE; AMYLOID BETA PROTEIN; ASPARTIC PROTEINASE; BACE1 PROTEIN, HUMAN; CYCLOHEXIMIDE; FTH1 PROTEIN, HUMAN; MITOCHONDRIAL FERRITIN, HUMAN; MITOCHONDRIAL PROTEIN; NITRILE; PROTEIN SYNTHESIS INHIBITOR; SECRETASE; SMALL INTERFERING RNA; SULFONE; TRANSCRIPTION FACTOR RELA;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; CELL CULTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; ANTAGONISTS AND INHIBITORS; CELL LINE; DOSE RESPONSE; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; METABOLISM; TIME;

AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; APOPTOSIS; ASPARTIC ACID ENDOPEPTIDASES; CELL LINE; CYCLOHEXIMIDE; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; FERRITINS; HUMANS; MITOCHONDRIAL PROTEINS; NF-KAPPA B; NITRILES; PROTEIN SYNTHESIS INHIBITORS; RNA, MESSENGER; RNA, SMALL INTERFERING; SULFONES; TIME FACTORS; TRANSCRIPTION FACTOR RELA; TRANSFECTION; UP-REGULATION;

EID: 84925702106     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-142595     Document Type: Article

References (48)

1. Querfurth HW, LaFerla FM (2011) Alzheimer's disease. N Engl J Med 362, 329-344.
2. Rubio-Perez JM, Morillas-Ruiz JM (2012) A review: Inflammatory process in Alzheimer's disease, role of cytokines. ScientificWorldJournal 2012, 756357.
3. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Machenzie IR, McGeer PL, O'Banion MK, Pachter J, Pasinetti G, Plata-Salaman C, Rogers J, Rydel R, Shen Y, Streit W, Strohmeyer R, Tooyama I, Van Muiswinkel FL, Veerhuis R, Walker D, Webster S, Wegrzyniak B, Wenk G, Wyss-Coray T (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21, 383-421.
4. Heneka MT, O'Banion MK (2007) Inflammatory processes in Alzheimer's disease. J Neuroimmunol 184, 69-91.
5. Ham D, Schipper HM (2000) Heme oxygenase-1 induction and mitochondrial iron sequestration in astroglia exposed to amyloid peptides. Cell Mol Biol (Noisy-le-grand) 46, 587-596.
6. Christen Y (2000) Oxidative stress and Alzheimer disease. Am J Clin Nutr 71, 621S-629S.
7. Oshiro S, Morioka MS, Kikuchi M (2011) Dysregulation of iron metabolism in Alzheimer's disease, Parkinson's disease, and amyotrophic lateral sclerosis. Adv Pharmacol Sci 2011, 378278.
8. Crichton RR, Dexter DT, Ward RJ (2011) Brain iron metabolism and its perturbation in neurological diseases. J Neural Transm 118, 301-314.
9. Levi S, Corsi B, Bosisio M, Invernizzi R, Volz A, Sanford D, Arosio P, Drysdale J (2001) A human mitochondrial ferritin encoded by an intronless gene. J Biol Chem 276, 24437-24440.
10. Corsi B, Cozzi A, Arosio P, Drysdale J, Santambrogio P, Campanella A, Biasiotto G, Albertini A, Levi S (2002) Human mitochondrial ferritin expressed in HeLa cells incorporates iron and affects cellular iron metabolism. J Biol Chem 277, 22430-22437.
11. Drysdale J, Arosio P, Invernizzi R, Cazzola M, Volz A, Corsi B, Biasiotto G, Levi S (2002) Mitochondrial ferritin: A new player in iron metabolism. Blood Cells Mol Dis 29, 376-383.
12. Levi S, Arosio P (2004) Mitochondrial ferritin. Int J Biochem Cell Biol 36, 1887-1889.
13. Nie G, Sheftel AD, Kim SF, Ponka P (2005) Overexpression of mitochondrial ferritin causes cytosolic iron depletion and changes cellular iron homeostasis. Blood 105, 2161-2167.
14. Bou-Abdallah F, Santambrogio P, Levi S, Arosio P, Chasteen ND (2005) Unique iron binding and oxidation properties of human mitochondrial ferritin: A comparative analysis with Human H-chain ferritin. J Mol Biol 347, 543-554.
15. Gao G, Chang YZ (2014) Mitochondrial ferritin in the regulation of brain iron homeostasis and neurodegenerative diseases. Front Pharmacol 5, 19.
16. Yang H, Yang M, Guan H, Liu Z, Zhao S, Takeuchi S, Yanagisawa D, Tooyama I (2013) Mitochondrial ferritin in neurodegenerative diseases. Neurosci Res 77, 1-7.
17. Shi ZH, Nie G, Duan XL, Rouault T, Wu WS, Ning B, Zhang N, Chang YZ, Zhao BL (2010) Neuroprotective mechanism of mitochondrial ferritin on 6-hydroxydopamine-induced dopaminergic cell damage: Implication for neuroprotection in Parkinson's disease. Antioxid Redox Signal 13, 783-796.
18. Snyder AM, Wang X, Patton SM, Arosio P, Levi S, Earley CJ, Allen RP, Connor JR (2009) Mitochondrial ferritin in the substantia nigra in restless legs syndrome. J Neuropathol Exp Neurol 68, 1193-1199.
19. Campanella A, Rovelli E, Santambrogio P, Cozzi A, Taroni F, Levi S (2009) Mitochondrial ferritin limits oxidative damage regulating mitochondrial iron availability: Hypothesis for a protective role in Friedreich ataxia. Hum Mol Genet 18, 1-11.
20. Stenirri S, Santambrogio P, Setaccioli M, Erba BG, Pia Manitto M, Rovida E, Ferrari M, Levi S, Cremonesi L (2012) Study of FTMT and ABCA4 genes in a patient affected by age-related macular degeneration: Identification and analysis of new mutations. Clin Chem Lab Med 50, 1021-1029.
21. Wang L, Yang H, Zhao S, Sato H, Konishi Y, Beach TG, Abdelalim EM, Bisem NJ, Tooyama I (2011) Expression and localization of mitochondrial ferritin mRNA in Alzheimer's disease cerebral cortex. PLoS One 6, e22325.
22. Wu WS, Zhao YS, Shi ZH, Chang SY, Nie GJ, Duan XL, Zhao SM, Wu Q, Yang ZL, Zhao BL, Chang YZ (2013) Mitochondrial ferritin attenuates β-amyloid-induced neurotoxicity: Reduction in oxidative damage through the Erk/P38 mitogen-activated protein kinase pathways. Antioxid Redox Signal 18, 158-169.
23. Rogers JT, Randall JD, Cahill CM, Eder PS, Huang X, Gunshin H, Leiter L, McPhee J, Sarang SS, Utsuki T, Greig NH, Lahiri DK, Tanzi RE, Bush AI, Giordano T, Gullans SR (2002) An iron-responsive element type II in the 5'-untranslated region of the Alzheimer's amyloid precursor protein transcript. J Biol Chem 277, 45518-45528.
24. Chami L, Buggia-Prévot V, Duplan E, Delprete D, Chami M, Peyron JF, Checler F (2012) Nuclear factor-κB regulates βAPP and β- and γ-secretases differently at physiological and supraphysiological Aβ concentrations. J Biol Chem 287, 24573-24584.
25. Torti FM, Torti SV (2002) Regulation of ferritin genes and protein. Blood 99, 3505-3516.
26. Ruddell RG, Hoang-Le D, Barwood JM, Rutherford PS, Piva TJ, Watters DJ, Santambrogio P, Arosio P, Ramm GA (2009) Ferritin functions as a proinflammatory cytokine via iron-independent protein kinase C zeta/nuclear factor kappaB-regulated signaling in rat hepatic stellate cells. Hepatology 49, 887-900.
27. Thomson AM, Cahill CM, Cho HH, Kassachau KD, Epis MR, Bridges KR, Leedman PJ, Rogers JT (2005) The acute box cis-element in human heavy ferritin mRNA 5′-untranslated region is a unique translation enhancer that binds poly(C)-binding proteins. J Biol Chem 280, 30032-30045.
28. Rogers JT (1996) Ferritin translation by interleukin-1 and interleukin-6: The role of sequences upstream of the start codons of the heavy and light subunit genes. Blood 87, 2525-2537.
29. Fahmy M, Young SP (1993) Modulation of iron metabolism in monocyte cell line U937 by inflammatory cytokines: Changes in transferrin uptake, iron handling and ferritin mRNA. Biochem J 296, 175-181.
30. Gilmore TD (2006) Introduction to NF-kappaB: Players, pathways, perspectives. Oncogene 25, 6680-6684.
31. Miyamoto S, Maki M, Schmitt MJ, Hatanaka M, Verma IM (1994) Tumor necrosis factor alpha-induced phosphorylation of I kappa B alpha is a signal for its degradation but not dissociation from NF-kappa B. Proc Natl Acad Sci U S A 91, 12740-12744.
32. Kwak EL, Larochelle DA, Beaumont C, Torti SV, Torti FM (1995) Role for NF-kappa B in the regulation of ferritin H by tumor necrosis factor-alpha. J Biol Chem 270, 15285-15293.
33. Pham CG, Bubici C, Zazzeroni F, Papa S, Jones J, Alvarez K, Jayawardena S, De Smaele E, Cong R, Beaumont C, Torti FM, Tori SV, Franzoso G (2004) Ferritin heavy chain upregulation by NF-kappaB inhibits TNFalpha-induced apoptosis by suppressing reactive oxygen species. Cell 119, 529-542.
34. Yang L, Lindholm K, Konishi Y, Li R, Shen Y (2002) Target depletion of distinct tumor necrosis factor receptor subtypes reveals hippocampal neuron death and survival through different signal transduction pathways. J Neurosci 22, 3025-3032.
35. Boldyrev A, Koudinov A, Berezov T, Carpenter DO (2004) Amyloid-beta induced cell death is independent of free radicals. J Alzheimers Dis 6, 633-638.
36. Mattson MP, Camandola S (2001) NF-kappaB in neuronal plasticity and neurodegenerative disorders. J Clin Invest 107, 247-254.
37. Shimohama S (2000) Apoptosis in Alzheimer's disease-an update. Apoptosis 5, 9-16.
38. Behl C (2000) Apoptosis and Alzheimer's disease. J Neural Transm 107, 1325-1344.
39. Varfolomeev EE, Ashkenazi A (2004) Tumor necrosis factor: An apoptosis JuNKie? Cell 116, 491-497.
40. Hsu H, Xiong J, Goeddel DV (1995) The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 81, 495-504.
41. Delhalle S, Deregowski V, Benoit V, Merville MP, Bours V (2002) NF-kappaB-dependent MnSOD expression protects adenocarcinoma cells from TNF-alpha-induced apoptosis. Oncogene 21, 3917-3924.
42. Javelaud D, Besanc¸on F (2001) NF-kappa B activation results in rapid inactivation of JNK in TNF alpha-treated Ewing sarcoma cells: A mechanism for the anti-apoptotic effect of NF-kappa B. Oncogene 20, 4365-4372.
43. Tang G, Minemoto Y, Dibling B, Purcell NH, Li Z, Karin M, Lin A (2001) Inhibition of JNK activation through NF-kappaB target genes. Nature 414, 313-317.
44. Garg AK, Aggarwal BB (2002) Reactive oxygen intermediates in TNF signaling. Mol Immunol 39, 509-517.
45. Sakon S, Xue X, Takekawa M, Sasazuki T, Okazaki T, Kojima Y, Piao JH, Yagita H, Okumura K, Doi T, Nakano H (2003) NF-kappaB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J 22, 3898-3909.
46. Karin M, Lin A (2002) NF-kappaB at the crossroads of life and death. Nat Immunol 3, 221-227.
47. Liu G, Men P, Perry G, Smith MA (2010) Nanoparticle and iron chelators as a potential novel Alzheimer therapy. Methods Mol Biol 610, 123-144.
48. Crapper McLachlan DR, Dalton AJ, Kruck TP, Bell MY, Smith WL, Kalow W, Andrews DF (1991) Intramuscular desferrioxamine in patients with Alzheimer's disease. Lancet 337, 1304-1308.