Brain transcriptome perturbations in the transferrin receptor 2 mutant mouse support the case for brain changes in iron loading disorders, including effects relating to long-term depression and long-term potentiation

Neuroscience

Volumn 235, Issue , 2013, Pages 119-128

  Acikyol, B ^a,b   Graham, R M ^c,d,e,f   Trinder, D ^c,d   House, M J ^g   Olynyk, J K ^f,h,j   Scott, R J ^a,b,k   Milward, E A ^a,b   Johnstone, D M ^a,b,i  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b HUNTER MEDICAL RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e CURTIN UNIVERSITY   (Australia)

^f CURTIN UNIVERSITY   (Australia)

^g UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^h FREMANTLE HOSPITAL   (Australia)

ⁱ UNIVERSITY OF SYDNEY   (Australia)

^j MURDOCH UNIVERSITY   (Australia)

^k JOHN HUNTER HOSPITAL   (Australia)

more..

Author keywords

Hemochromatosis; Iron; Long term depression; Microarray; Mouse model; Transferrin receptor 2

Indexed keywords

IRON; TRANSCRIPTOME; TRANSFERRIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE MODEL; GENETIC TRANSCRIPTION; HEMOCHROMATOSIS; IRON THERAPY; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MEMORY; MICROARRAY ANALYSIS; MOLECULAR BIOLOGY; MOUSE; MOUSE STRAIN; MUTANT; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPSE;

ANIMALS; BLOTTING, WESTERN; BRAIN CHEMISTRY; FERRITINS; GLIOMA; HEMOCHROMATOSIS; HISTOCOMPATIBILITY ANTIGENS CLASS I; IRON; IRON, DIETARY; LIVER; LONG-TERM POTENTIATION; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; MUTATION; MUTATION, MISSENSE; NEURONAL PLASTICITY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, TRANSFERRIN; SPECTROPHOTOMETRY, ATOMIC; TRANSCRIPTOME;

EID: 84873933182     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.01.014     Document Type: Article

References (66)

1. Ajioka R.S., Levy J.E., Andrews N.C., Kushner J.P. Regulation of iron absorption in Hfe mutant mice. Blood 2002, 100:1465-1469.
2. Allen K.J., Gurrin L.C., Constantine C.C., Osborne N.J., Delatycki M.B., Nicoll A.J., McLaren C.E., Bahlo M., Nisselle A.E., Vulpe C.D., Anderson G.J., Southey M.C., Giles G.G., English D.R., Hopper J.L., Olynyk J.K., Powell L.W., Gertig D.M. Iron-overload-related disease in HFE hereditary hemochromatosis. N Engl J Med 2008, 358:221-230.
3. Ayonrinde O.T., Milward E.A., Chua A.C., Trinder D., Olynyk J.K. Clinical perspectives on hereditary hemochromatosis. Crit Rev Clin Lab Sci 2008, 45:451-484.
4. Bartzokis G., Beckson M., Hance D.B., Marx P., Foster J.A., Marder S.R. MR evaluation of age-related increase of brain iron in young adult and older normal males. Magn Reson Imaging 1997, 15:29-35.
5. Bartzokis G., Lu P.H., Tingus K., Peters D.G., Amar C.P., Tishler T.A., Finn J.P., Villablanca P., Altshuler L.L., Mintz J., Neely E., Connor J.R. Gender and iron genes may modify associations between brain iron and memory in healthy aging. Neuropsychopharmacology 2011, 36:1375-1384.
6. Bastin J.M., Jones M., O'Callaghan C.A., Schimanski L., Mason D.Y., Townsend A.R. Kupffer cell staining by an HFE-specific monoclonal antibody: implications for hereditary haemochromatosis. Br J Haematol 1998, 103:931-941.
7. Berg D., Hoggenmuller U., Hofmann E., Fischer R., Kraus M., Scheurlen M., Becker G. The basal ganglia in haemochromatosis. Neuroradiology 2000, 42:9-13.
8. Boes C.J., Black D.F., Dodick D.W. Pathophysiology and management of transformed migraine and medication overuse headache. Semin Neurol 2006, 26:232-241.
9. Bondy C.A., Cheng C.M. Signaling by insulin-like growth factor 1 in brain. Eur J Pharmacol 2004, 490:25-31.
10. Bridle K.R., Frazer D.M., Wilkins S.J., Dixon J.L., Purdie D.M., Crawford D.H., Subramaniam V.N., Powell L.W., Anderson G.J., Ramm G.A. Disrupted hepcidin regulation in HFE-associated haemochromatosis and the liver as a regulator of body iron homoeostasis. Lancet 2003, 361:669-673.
11. Brigman J.L., Wright T., Talani G., Prasad-Mulcare S., Jinde S., Seabold G.K., Mathur P., Davis M.I., Bock R., Gustin R.M., Colbran R.J., Alvarez V.A., Nakazawa K., Delpire E., Lovinger D.M., Holmes A. Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning. J Neurosci 2010, 30:4590-4600.
12. Brissot P., Moirand R., Jouanolle A.M., Guyader D., Le Gall J.Y., Deugnier Y., David V. A genotypic study of 217 unrelated probands diagnosed as " genetic hemochromatosis" on " classical" phenotypic criteria. J Hepatol 1999, 30:588-593.
13. Calzolari A., Larocca L.M., Deaglio S., Finisguerra V., Boe A., Raggi C., Ricci-Vitani L., Pierconti F., Malavasi F., De Maria R., Testa U., Pallini R. Transferrin receptor 2 is frequently and highly expressed in glioblastomas. Transl Oncol 2010, 3:123-134.
14. Calzolari A., Oliviero I., Deaglio S., Mariani G., Biffoni M., Sposi N.M., Malavasi F., Peschle C., Testa U. Transferrin receptor 2 is frequently expressed in human cancer cell lines. Blood Cells Mol Dis 2007, 39:82-91.
15. Camaschella C., Roetto A., Cali A., De Gobbi M., Garozzo G., Carella M., Majorano N., Totaro A., Gasparini P. The gene TFR2 is mutated in a new type of haemochromatosis mapping to 7q22. Nat Genet 2000, 25:14-15.
16. Chua A.C., Delima R.D., Morgan E.H., Herbison C.E., Tirnitz-Parker J.E., Graham R.M., Fleming R.E., Britton R.S., Bacon B.R., Olynyk J.K., Trinder D. Iron uptake from plasma transferrin by a transferrin receptor 2 mutant mouse model of haemochromatosis. J Hepatol 2010, 52:425-431.
17. Chua A.C., Herbison C.E., Drake S.F., Graham R.M., Olynyk J.K., Trinder D. The role of Hfe in transferrin-bound iron uptake by hepatocytes. Hepatology 2008, 47:1737-1744.
18. Collingridge G.L., Peineau S., Howland J.G., Wang Y.T. Long-term depression in the CNS. Nat Rev Neurosci 2010, 11:459-473.
19. Connor J.R., Milward E.A., Moalem S., Sampietro M., Boyer P., Percy M.E., Vergani C., Scott R.J., Chorney M. Is hemochromatosis a risk factor for Alzheimer's disease?. J Alzheimers Dis 2001, 3:471-477.
20. De Gobbi M., Barilaro M.R., Garozzo G., Sbaiz L., Alberti F., Camaschella C. TFR2 Y250X mutation in Italy. Br J Haematol 2001, 114:243-244.
21. Delima R.D., Chua A.C., Tirnitz-Parker J.E., Gan E.K., Croft K.D., Graham R.M., Olynyk J.K., Trinder D. Disruption of hemochromatosis protein and transferrin receptor 2 causes iron-induced liver injury in mice. Hepatology 2012, 56:585-593.
22. Drake S.F., Morgan E.H., Herbison C.E., Delima R., Graham R.M., Chua A.C., Leedman P.J., Fleming R.E., Bacon B.R., Olynyk J.K., Trinder D. Iron absorption and hepatic iron uptake are increased in a transferrin receptor 2 (Y245X) mutant mouse model of hemochromatosis type 3. Am J Physiol Gastrointest Liver Physiol 2007, 292:G323-G328.
23. Ducros A., Denier C., Joutel A., Vahedi K., Michel A., Darcel F., Madigand M., Guerouaou D., Tison F., Julien J., Hirsch E., Chedru F., Bisgard C., Lucotte G., Despres P., Billard C., Barthez M.A., Ponsot G., Bousser M.G., Tournier-Lasserve E. Recurrence of the T666M calcium channel CACNA1A gene mutation in familial hemiplegic migraine with progressive cerebellar ataxia. Am J Hum Genet 1999, 64:89-98.
24. Feder J.N., Gnirke A., Thomas W., Tsuchihashi Z., Ruddy D.A., Basava A., Dormishian F., Domingo R., Ellis M.C., Fullan A., Hinton L.M., Jones N.L., Kimmel B.E., Kronmal G.S., Lauer P., Lee V.K., Loeb D.B., Mapa F.A., McClelland E., Meyer N.C., Mintier G.A., Moeller N., Moore T., Morikang E., Wolff R.K., et al. A novel MHC class I-like gene is mutated in patients with hereditary haemochromatosis. Nat Genet 1996, 13:399-408.
25. Fleming R.E., Ahmann J.R., Migas M.C., Waheed A., Koeffler H.P., Kawabata H., Britton R.S., Bacon B.R., Sly W.S. Targeted mutagenesis of the murine transferrin receptor-2 gene produces hemochromatosis. Proc Natl Acad Sci U S A 2002, 99:10653-10658.
26. Gao J., Chen J., Kramer M., Tsukamoto H., Zhang A.S., Enns C.A. Interaction of the hereditary hemochromatosis protein HFE with transferrin receptor 2 is required for transferrin-induced hepcidin expression. Cell Metab 2009, 9:217-227.
27. Gaul C., Krummernerl P., Tamke B., Kornhuber M. Chronic daily headache in hereditary hemochromatosis treated by venesection. Headache 2007, 47:926-928.
28. Griffiths S., Scott H., Glover C., Bienemann A., Ghorbel M.T., Uney J., Brown M.W., Warburton E.C., Bashir Z.I. Expression of long-term depression underlies visual recognition memory. Neuron 2008, 58:186-194.
29. Hagen K., Stovner L.J., Asberg A., Thorstensen K., Bjerve K.S., Hveem K. High headache prevalence among women with hemochromatosis: the Nord-Trondelag health study. Ann Neurol 2002, 51:786-789.
30. Hallgren B., Sourander P. The effect of age on the non-haemin iron in the human brain. J Neurochem 1958, 3:41-51.
31. Hanninen M.M., Haapasalo J., Haapasalo H., Fleming R.E., Britton R.S., Bacon B.R., Parkkila S. Expression of iron-related genes in human brain and brain tumors. BMC Neurosci 2009, 10:36.
32. Hans M., Luvisetto S., Williams M.E., Spagnolo M., Urrutia A., Tottene A., Brust P.F., Johnson E.C., Harpold M.M., Stauderman K.A., Pietrobon D. Functional consequences of mutations in the human alpha1A calcium channel subunit linked to familial hemiplegic migraine. J Neurosci 1999, 19:1610-1619.
33. Hentze M.W., Kuhn L.C. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci U S A 1996, 93:8175-8182.
34. Hill J.M., Switzer R.C. The regional distribution and cellular localization of iron in the rat brain. Neuroscience 1984, 11:595-603.
35. Huang da W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13.
36. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
37. Huser M., Luckett J., Chiloeches A., Mercer K., Iwobi M., Giblett S., Sun X.M., Brown J., Marais R., Pritchard C. MEK kinase activity is not necessary for Raf-1 function. EMBO J 2001, 20:1940-1951.
38. Johnson L., Greenbaum D., Cichowski K., Mercer K., Murphy E., Schmitt E., Bronson R.T., Umanoff H., Edelmann W., Kucherlapati R., Jacks T. K-ras is an essential gene in the mouse with partial functional overlap with N-ras. Genes Dev 1997, 11:2468-2481.
39. Johnstone D., Milward E.A. Genome-wide microarray analysis of brain gene expression in mice on a short-term high iron diet. Neurochem Int 2010, 56:856-863.
40. Johnstone D., Milward E.A. Molecular genetic approaches to understanding the roles and regulation of iron in brain health and disease. J Neurochem 2010, 113:1387-1402.
41. -/- mouse model of genetic iron loading. Brain Res 2012, 1448:144-152.
42. Johnstone D.M., Graham R.M., Trinder D., Riveros C., Olynyk J.K., Scott R.J., Moscato P., Milward E.A. Changes in brain transcripts related to Alzheimer's disease in a model of HFE hemochromatosis are not consistent with increased Alzheimer's disease risk. J Alzheimers Dis 2012, 30:791-803.
43. Kaldor I. Studies on intermediary iron metabolism: V. The measurement of non-haemoglobin tissue iron. Aust J Exp Biol Med Sci 1954, 32:795-799.
44. Kawabata H., Yang R., Hirama T., Vuong P.T., Kawano S., Gombart A.F., Koeffler H.P. Molecular cloning of transferrin receptor: 2. A new member of the transferrin receptor-like family. J Biol Chem 1999, 274:20826-20832.
45. Lee Y.S., Silva A.J. The molecular and cellular biology of enhanced cognition. Nat Rev Neurosci 2009, 10:126-140.
46. Massey P.V., Bashir Z.I. Long-term depression: multiple forms and implications for brain function. Trends Neurosci 2007, 30:176-184.
47. McLachlan S., Lee S.M., Steele T.M., Hawthorne P.L., Zapala M.A., Eskin E., Schork N.J., Anderson G.J., Vulpe C.D. In silico QTL mapping of basal liver iron levels in inbred mouse strains. Physiol Genomics 2011, 43:136-147.
48. McLaren G.D., McLaren C.E., Adams P.C., Barton J.C., Reboussin D.M., Gordeuk V.R., Acton R.T., Harris E.L., Speechley M.R., Sholinsky P., Dawkins F.W., Snively B.M., Vogt T.M., Eckfeldt J.H. Clinical manifestations of hemochromatosis in HFE C282Y homozygotes identified by screening. Can J Gastroenterol 2008, 22:923-930.
49. Migues P.V., Hardt O., Wu D.C., Gamache K., Sacktor T.C., Wang Y.T., Nader K. PKMzeta maintains memories by regulating GluR2-dependent AMPA receptor trafficking. Nat Neurosci 2010, 13:630-634.
50. Mikula M., Schreiber M., Husak Z., Kucerova L., Ruth J., Wieser R., Zatloukal K., Beug H., Wagner E.F., Baccarini M. Embryonic lethality and fetal liver apoptosis in mice lacking the c-raf-1 gene. EMBO J 2001, 20:1952-1962.
51. Muckenthaler M.U., Galy B., Hentze M.W. Systemic iron homeostasis and the iron-responsive element/iron-regulatory protein (IRE/IRP) regulatory network. Annu Rev Nutr 2008, 28:197-213.
52. Nemeth E., Roetto A., Garozzo G., Ganz T., Camaschella C. Hepcidin is decreased in TFR2 hemochromatosis. Blood 2005, 105:1803-1806.
53. Nemeth E., Tuttle M.S., Powelson J., Vaughn M.B., Donovan A., Ward D.M., Ganz T., Kaplan J. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 2004, 306:2090-2093.
54. Nielsen J.E., Jensen L.N., Krabbe K. Hereditary haemochromatosis: a case of iron accumulation in the basal ganglia associated with a parkinsonian syndrome. J Neurol Neurosurg Psychiatry 1995, 59:318-321.
55. Olynyk J.K., Cullen D.J., Aquilia S., Rossi E., Summerville L., Powell L.W. A population-based study of the clinical expression of the hemochromatosis gene. N Engl J Med 1999, 341:718-724.
56. Pietrangelo A. Hereditary hemochromatosis. Annu Rev Nutr 2006, 26:251-270.
57. Pietrobon D. Calcium channels and channelopathies of the central nervous system. Mol Neurobiol 2002, 25:31-50.
58. Roetto A., Di Cunto F., Pellegrino R.M., Hirsch E., Azzolino O., Bondi A., Defilippi I., Carturan S., Miniscalco B., Riondato F., Cilloni D., Silengo L., Altruda F., Camaschella C., Saglio G. Comparison of 3 Tfr2-deficient murine models suggests distinct functions for Tfr2-alpha and Tfr2-beta isoforms in different tissues. Blood 2010, 115:3382-3389.
59. Roetto A., Totaro A., Piperno A., Piga A., Longo F., Garozzo G., Cali A., De Gobbi M., Gasparini P., Camaschella C. New mutations inactivating transferrin receptor 2 in hemochromatosis type 3. Blood 2001, 97:2555-2560.
60. Russo N., Edwards M., Andrews T., O'Brien M., Bhatia K.P. Hereditary haemochromatosis is unlikely to cause movement disorders - a critical review. J Neurol 2004, 251:849-852.
61. Rutgers M.P., Pielen A., Gille M. Chronic cerebellar ataxia and hereditary hemochromatosis: causal or coincidental association?. J Neurol 2007, 254:1296-1297.
62. Stovner L.J., Hagen K., Waage A., Bjerve K.S. Hereditary haemochromatosis in two cousins with cluster headache. Cephalgia 2002, 22:317-319.
63. Wallace D.F., Summerville L., Crampton E.M., Frazer D.M., Anderson G.J., Subramaniam V.N. Combined deletion of Hfe and transferrin receptor 2 in mice leads to marked dysregulation of hepcidin and iron overload. Hepatology 2009, 50:1992-2000.
64. Wallace D.F., Trinder D., Subramaniam V.N. Hepcidin regulation by HFE and TFR2: is it enough to give a hepatocyte a complex?. Gastroenterology 2009, 137:1173-1175. discussion 1175.
65. Whitlock E.P., Garlitz B.A., Harris E.L., Beil T.L., Smith P.R. Screening for hereditary hemochromatosis: a systematic review for the U.S. Preventive Services Task Force. Ann Intern Med 2006, 145:209-223.
66. 2+/calmodulin-dependent protein kinase II - discovery, progress in a quarter of a century, and perspective: implication for learning and memory. Biol Pharm Bull 2005, 28:1342-1354.