Neuroferritinopathy: From ferritin structure modification to pathogenetic mechanism

Neurobiology of Disease

Volumn 81, Issue , 2015, Pages 134-143

  Levi, Sonia ^a,b   Rovida, Ermanna ^c  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c Milan Unit   (Italy)

Author keywords

Ferritin; Iron; Neurodegenerative disorder; Neuroferritinopathy; Oxidative damage

Indexed keywords

FERRITIN; LIPOFUSCIN;

AMINO ACID SUBSTITUTION; CARBOXY TERMINAL SEQUENCE; CLINICAL FEATURE; EXON; EXPERIMENTAL MODEL; FIBROBLAST; FRAMESHIFT MUTATION; FTL1 GENE; GENETIC VARIABILITY; HETEROZYGOTE; HISTOPATHOLOGY; HUMAN; IN VITRO STUDY; IRON STORAGE; MOLECULAR MODEL; NERVE DEGENERATION; NEUROFERRITINOPATHY; NEUROPATHOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REVIEW; ANIMAL; BIOLOGY; BRAIN; CHEMISTRY; GENETICS; IRON METABOLISM DISORDER; METABOLISM; NEUROAXONAL DYSTROPHY; PATHOLOGY;

ANIMALS; BRAIN; COMPUTATIONAL BIOLOGY; FERRITINS; HUMANS; IRON METABOLISM DISORDERS; MODELS, MOLECULAR; NEUROAXONAL DYSTROPHIES;

EID: 84944399809     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.02.007     Document Type: Review

References (61)

1. Adzhubei I., Jordan D.M., Sunyaev S.R. Predicting functional effect of human missense mutations using PolyPhen-2. Current Protocols in Human Genetics/Editorial Board 2013, (Chapter 7, Unit7 20). J.L. Haines (Ed.).
2. Arosio P., Levi S. Cytosolic and mitochondrial ferritins in the regulation of cellular iron homeostasis and oxidative damage. Biochim. Biophys. Acta 2010, 1800:783-792.
3. Baraibar M.A., Barbeito A.G., Muhoberac B.B., Vidal R. Iron-mediated aggregation and a localized structural change characterize ferritin from a mutant light chain polypeptide that causes neurodegeneration. J. Biol. Chem. 2008, 283:31679-31689.
4. Baraibar M.A., Muhoberac B.B., Garringer H.J., Hurley T.D., Vidal R. Unraveling of the E-helices and disruption of 4-fold pores are associated with iron mishandling in a mutant ferritin causing neurodegeneration. J. Biol. Chem. 2010, 285:1950-1956.
5. Baraibar M.A., Barbeito A.G., Muhoberac B.B., Vidal R. A mutant light-chain ferritin that causes neurodegeneration has enhanced propensity toward oxidative damage. Free Radic. Biol. Med. 2012, 52:1692-1697.
6. Barbeito A.G., Garringer H.J., Baraibar M.A., Gao X., Arredondo M., Nunez M.T., Smith M.A., Ghetti B., Vidal R. Abnormal iron metabolism and oxidative stress in mice expressing a mutant form of the ferritin light polypeptide gene. J. Neurochem. 2009, 109:1067-1078.
7. Barbeito A.G., Levade T., Delisle M.B., Ghetti B., Vidal R. Abnormal iron metabolism in fibroblasts from a patient with the neurodegenerative disease hereditary ferritinopathy. Mol. Neurodegener. 2010, 5:50.
8. Behera R.K., Theil E.C. Moving Fe2+ from ferritin ion channels to catalytic OH centers depends on conserved protein cage carboxylates. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:7925-7930.
9. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., Shindyalov I.N., Bourne P.E. The Protein Data Bank. Nucleic Acids Res. 2000, 28:235-242.
10. Cazzola M. Hereditary hyperferritinaemia/ cataract syndrome. Best practice & research. Clin. Haematol. 2002, 15:385-398.
11. Chinnery P.F., Crompton D.E., Birchall D., Jackson M.J., Coulthard A., Lombes A., Quinn N., Wills A., Fletcher N., Mottershead J.P., Cooper P., Kellett M., Bates D., Burn J. Clinical features and natural history of neuroferritinopathy caused by the FTL1 460InsA mutation. Brain 2007, 130:110-119.
12. Chinnery P.F., Curtis A.R., Fey C., Coulthard A., Crompton D., Curtis A., Lombés A., Burn J. Neuroferritinopathy in a French family with late onset dominant dystonia. J Med Genet. 2003, 40. e69.
13. Connor J.R., Snyder B.S., Arosio P., Loeffler D.A., LeWitt P. A quantitative analysis of isoferritins in select regions of aged, parkinsonian, and Alzheimer's diseased brains. J. Neurochem. 1995, 65:717-724.
14. Cozzi A., Santambrogio P., Corsi B., Campanella A., Arosio P., Levi S. Characterization of the L-ferritin variant 460InsA responsible of a hereditary ferritinopathy disorder. Neurobiol. Dis. 2006, 23:644-652.
15. Cozzi A., Rovelli E., Frizzale G., Campanella A., Amendola M., Arosio P., Levi S. Oxidative stress and cell death in cells expressing L-ferritin variants causing neuroferritinopathy. Neurobiol. Dis. 2010, 37:77-85.
16. Crompton D.E., Chinnery P.F., Bates D., Walls T.J., Jackson M.J., Curtis A.J., Burn J. Spectrum of movement disorders in neuroferritinopathy. Mov Disord. 2005, 20:95-99.
17. Curtis A.R., Fey C., Morris C.M., Bindoff L.A., Ince P.G., Chinnery P.F., Coulthard A., Jackson M.J., Jackson A.P., McHale D.P., Hay D., Barker W.A., Markham A.F., Bates D., Curtis A., Burn J. Mutation in the gene encoding ferritin light polypeptide causes dominant adult-onset basal ganglia disease. Nat. Genet. 2001, 28:350-354.
18. den Dunnen J.T., Antonarakis S.E. Mutation nomenclature extensions and suggestions to describe complex mutations: a discussion. Hum. Mutat. 2000, 15:7-12.
19. Deng X., Vidal R., Englander E.W. Accumulation of oxidative DNA damage in brain mitochondria in mouse model of hereditary ferritinopathy. Neurosci. Lett. 2010, 479:44-48.
20. Devos D., Tchofo P.J., Vuillaume I., Destee A., Batey S., Burn J., Chinnery P.F. Clinical features and natural history of neuroferritinopathy caused by the 458dupA FTL mutation. Brain 2009, 132:e109.
21. Douglas T., Ripoll D.R. Calculated electrostatic gradients in recombinant human H-chain ferritin. Protein Sci. 1998, 7:1083-1091.
22. Ferrari F., Foglieni B., Arosio P., Camaschella C., Daraio F., Levi S., Garcia Erce J.A., Beaumont C., Cazzola M., Ferrari M., Cremonesi L. Microelectronic DNA chip for hereditary hyperferritinemia cataract syndrome, a model for large-scale analysis of disorders of iron metabolism. Hum. Mutat. 2006, 27:201-208.
23. Finazzi D., Arosio P. Biology of ferritin in mammals: an update on iron storage, oxidative damage and neurodegeneration. Arch. Toxicol. 2014, 88:1787-1802.
24. Girelli D., Olivieri O., De Franceschi L., Corrocher R., Bergamaschi G., Cazzola M. A linkage between hereditary hyperferritinaemia not related to iron overload and autosomal dominant congenital cataract. Br. J. Haematol. 1995, 90:931-934.
25. Graf E., Mahoney J.R., Bryant R.G., Eaton J.W. Iron-catalyzed hydroxyl radical formation. Stringent requirement for free iron coordination site. J. Biol. Chem. 1984, 259:3620-3624.
26. Hentze M.W., Muckenthaler M.U., Galy B., Camaschella C. Two to tango: regulation of Mammalian iron metabolism. Cell 2010, 142:24-38.
27. Hohn A., Grune T. Lipofuscin: formation, effects and role of macroautophagy. Redox Biol. 2013, 1:140-144.
28. Honig B., Nicholls A. Classical electrostatics in biology and chemistry. Science 1995, 268:1144-1149.
29. Keogh M.J., Jonas P., Coulthard A., Chinnery P.F., Burn J. Neuroferritinopathy: a new inborn error of iron metabolism. Neurogenetics 2012, 13:93-96.
30. Keogh M.J., Morris C.M., Chinnery P.F. Neuroferritinopathy. Int. Rev. Neurobiol. 2013, 110:91-123.
31. Kruer M.C., Boddaert N. Neurodegeneration with brain iron accumulation: a diagnostic algorithm. Semin. Pediatr. Neurol. 2012, 19:67-74.
32. Kubota A., Hida A., Ichikawa Y., Momose Y., Goto J., Igeta Y., Hashida H., Yoshida K., Ikeda S., Kanazawa I., Tsuji S. A novel ferritin light chain gene mutation in a Japanese family with neuroferritinopathy: description of clinical features and implications for genotype-phenotype correlations. Mov. Disord. 2009, 24:441-445.
33. Lawson D.M., Artymiuk P.J., Yewdall S.J., Smith J.M., Livingstone J.C., Treffry A., Luzzago A., Levi S., Arosio P., Cesareni G., et al. Solving the structure of human H ferritin by genetically engineering intermolecular crystal contacts. Nature 1991, 349:541-544.
34. Lehn A., Boyle R., Brown H., Airey C., Mellick G. Neuroferritinopathy. Parkinsonism Relat. Disord. 2012, 18:909-915.
35. Levi S., Finazzi D. Neurodegeneration with brain iron accumulation: update on pathogenic mechanisms. Front. Pharmacol. 2014, 5:99.
36. Levi S., Luzzago A., Cesareni G., Cozzi A., Franceschinelli F., Albertini A., Arosio P. Mechanism of ferritin iron uptake: activity of the H-chain and deletion mapping of the ferro-oxidase site. A study of iron uptake and ferro-oxidase activity of human liver, recombinant H-chain ferritins, and of two H-chain deletion mutants. J. Biol. Chem. 1988, 263:18086-18092.
37. Levi S., Santambrogio P., Cozzi A., Rovida E., Corsi B., Tamborini E., Spada S., Albertini A., Arosio P. The role of the L-chain in ferritin iron incorporation. Studies of homo and heteropolymers. J. Mol. Biol. 1994, 238:649-654.
38. Levi S., Girelli D., Perrone F., Pasti M., Beaumont C., Corrocher R., Albertini A., Arosio P. Analysis of ferritins in lymphoblastoid cell lines and in the lens of subjects with hereditary hyperferritinemia-cataract syndrome. Blood 1998, 91:4180-4187.
39. Levi S., Corsi B., Bosisio M., Invernizzi R., Volz A., Sanford D., Arosio P., Drysdale J. A human mitochondrial ferritin encoded by an intronless gene. J. Biol. Chem. 2001, 276:24437-24440.
40. Luscieti S., Santambrogio P., Langlois d'Estaintot B., Granier T., Cozzi A., Poli M., Gallois B., Finazzi D., Cattaneo A., Levi S., Arosio P. Mutant ferritin L-chains that cause neurodegeneration act in a dominant-negative manner to reduce ferritin iron incorporation. J. Biol. Chem. 2010, 285:11948-11957.
41. Luscieti S., Tolle G., Aranda J., Campos C.B., Risse F., Moran E., Muckenthaler M.U., Sanchez M. Novel mutations in the ferritin-L iron-responsive element that only mildly impair IRP binding cause hereditary hyperferritinaemia cataract syndrome. Orphanet J. Rare Dis. 2013, 8:30.
42. Maccarinelli F., Pagani A., Cozzi A., Codazzi F., Di Giacomo G., Capoccia S., Rapino S., Finazzi D., Politi L.S., Cirulli F., Giorgio M., Cremona O., Grohovaz F., Levi S. A novel neuroferritinopathy mouse model (FTL 498InsTC) shows progressive brain iron dysregulation, morphological signs of early neurodegeneration and motor coordination deficits. Neurobiol Dis. 2014, 10.1016/j.nbd.2014.10.023.
43. Maciel P., Cruz V.T., Constante M., Iniesta I., Costa M.C., Gallati S., Sousa N., Sequeiros J., Coutinho P., Santos M.M. Neuroferritinopathy: missense mutation in FTL causing early-onset bilateral pallidal involvement. Neurology 2005, 65:603-605.
44. Mancuso M., Davidzon G., Kurlan R.M., Tawil R., Bonilla E., Di Mauro S., Powers J.M. Hereditary ferritinopathy: a novel mutation, its cellular pathology, and pathogenetic insights. J. Neuropathol. Exp. Neurol. 2005, 64:280-294.
45. McNeill A., Birchall D., Hayflick S.J., Gregory A., Schenk J.F., Zimmerman E.A., Shang H., Miyajima H., Chinnery P.F. T2* and FSE MRI distinguishes four subtypes of neurodegeneration with brain iron accumulation. Neurology 2008, 70:1614-1619.
46. Mir P., Edwards M.J., Curtis A.R., Bhatia K.P., Quinn N.P. Adult-onset generalized dystonia due to a mutation in the neuroferritinopathy gene. Mov Disord. 2005, 20:243-245.
47. Moutton S., Fergelot P., Trocello J.M., Plante-Bordeneuve V., Houcinat N., Wenisch E., Larue V., Brugieres P., Clot F., Lacombe D., Arveiler B., Goizet C. A novel FTL mutation responsible for neuroferritinopathy with asymmetric clinical features and brain anomalies. Parkinsonism Relat. Disord. 2014, 20:935-937.
48. Muhoberac B.B., Vidal R. Abnormal iron homeostasis and neurodegeneration. Front. Aging Neurosci. 2013, 5:32.
49. Muhoberac B.B., Baraibar M.A., Vidal R. Iron loading-induced aggregation and reduction of iron incorporation in heteropolymeric ferritin containing a mutant light chain that causes neurodegeneration. Biochim. Biophys. Acta 2011, 1812:544-548.
50. Ng P.C., Henikoff S. SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res. 2003, 31:3812-3814.
51. Nishida K., Garringer H.J., Futamura N., Funakawa I., Jinnai K., Vidal R., Takao M. A novel ferritin light chain mutation in neuroferritinopathy with an atypical presentation. J. Neurol. Sci. 2014, 342:173-177.
52. Ohta E., Takiyama Y. MRI findings in neuroferritinopathy. Neurol. Res. Int. 2012, 2012:197438.
53. Ohta E., Nagasaka T., Shindo K., Toma S., Nagasaka K., Ohta K., Shiozawa Z. Neuroferritinopathy in a Japanese family with a duplication in the ferritin light chain gene. Neurology 2008, 70:1493-1494.
54. Roy A., Kucukural A., Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 2010, 5:725-738.
55. Santambrogio P., Levi S., Arosio P., Palagi L., Vecchio G., Lawson D.M., Yewdall S.J., Artymiuk P.J., Harrison P.M., Jappelli R., et al. Evidence that a salt bridge in the light chain contributes to the physical stability difference between heavy and light human ferritins. J. Biol. Chem. 1992, 267:14077-14083.
56. Storti E., Cortese F., Di Fabio R., Fiorillo C., Pierallini A., Tessa A., Valleriani A., Pierelli F., Santorelli F.M., Casali C. De novo FTL mutation: a clinical, neuroimaging, and molecular study. Mov. Disord. 2013, 28:252-253.
57. Vidal R., Delisle M.B., Rascol O., Ghetti B. Hereditary ferritinopathy. J. Neurol. Sci. 2003, 207:110-111.
58. Vidal R., Ghetti B., Takao M., Brefel-Courbon C., Uro-Coste E., Glazier B.S., Siani V., Benson M.D., Calvas P., Miravalle L., Rascol O., Delisle M.B. Intracellular ferritin accumulation in neural and extraneural tissue characterizes a neurodegenerative disease associated with a mutation in the ferritin light polypeptide gene. J. Neuropathol. Exp. Neurol. 2004, 63:363-380.
59. Vidal R., Miravalle L., Gao X., Barbeito A.G., Baraibar M.A., Hekmatyar S.K., Widel M., Bansal N., Delisle M.B., Ghetti B. Expression of a mutant form of the ferritin light chain gene induces neurodegeneration and iron overload in transgenic mice. J. Neurosci. 2008, 28:60-67.
60. Watt R.K., Hilton R.J., Graff D.M. Oxido-reduction is not the only mechanism allowing ions to traverse the ferritin protein shell. Biochim. Biophys. Acta 2010, 1800:745-759.
61. Wills A.J., Sawle G.V., Guilbert P.R., Curtis A.R. Palatal tremor and cognitive decline in neuroferritinopathy. J. Neurol. Neurosurg. Psychiatry 2002, 73:91-92.