The mechanism of vanadium-mediated developmental hypomyelination is related to destruction of oligodendrocyte progenitors through a relationship with ferritin and iron

Neurotoxicity Research

Volumn 19, Issue 3, 2011, Pages 361-373

  Todorich, Bozho ^a   Olopade, James O ^a,b   Surguladze, Nodar ^a,c   Zhang, Xuesheng ^a   Neely, Elizabeth ^a   Connor, James R ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF IBADAN   (Nigeria)

^c Institute of Molecular Biology and Biological Physics   (Georgia)

Author keywords

Development; Ferritin; Iron; Myelination; Oligodendrocytes; Vanadium

Indexed keywords

APOFERRITIN; DEFEROXAMINE; FERRITIN; IRON; LIPOCORTIN 5; REACTIVE OXYGEN METABOLITE; VANADIUM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; CENTRAL NERVOUS SYSTEM DISEASE; CHEMOSENSITIVITY; CONTROLLED STUDY; CYTOTOXICITY; DOUBLE STRANDED DNA BREAK; HYPOMYELINATION; IN VITRO STUDY; IN VIVO STUDY; NEURAL STEM CELL; NEUROTOXICITY; NEWBORN; NONHUMAN; OLIGODENDROCYTE PROGENITOR CELL; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; DEMYELINATING DISEASES; FEMALE; FERRITINS; IRON; NERVE FIBERS, MYELINATED; OLIGODENDROGLIA; OXIDATIVE STRESS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; STEM CELLS; VANADIUM;

RATTUS;

EID: 79951953171     PISSN: 10298428     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12640-010-9167-1     Document Type: Article

References (39)

1. JE Bottenstein 1986 Growth requirements in vitro of oligodendrocyte cell lines and neonatal rat brain oligodendrocytes Proc Natl Acad Sci USA 83 6 1955 1959 1:CAS (Pubitemid 16018682)
2. P Cheepsunthorn C Palmer JR Connor 1998 Cellular distribution of ferritin subunits in postnatal rat brain J Comp Neurol 400 1 73 86 1:CAS:528: DyaK1cXmt1Gjs70%3D 10.1002/(SICI)1096-9861(19981012)400:1<73::AID-CNE5>3. 0.CO;2-Q 9762867 (Pubitemid 28440754)
3. JR Connor SL Menzies 1996 Relationship of iron to oligodendrocytes and myelination Glia 17 2 83 93 1:STN:280:DyaK28znt1OrsQ%3D%3D 10.1002/(SICI)1098- 1136(199606)17:2<83::AID-GLIA1>3.0.CO;2-7 8776576 (Pubitemid 26309437)
4. JR Connor SL Menzies SM St Martin EJ Mufson 1990 Cellular distribution of transferrin, ferritin, and iron in normal and aged human brains J Neurosci Res 27 4 595 611 1:CAS:528:DyaK3MXnvFWktQ%3D%3D 10.1002/jnr.490270421 2079720
5. JR Connor KL Boeshore SA Benkovic SL Menzies 1994 Isoforms of ferritin have a specific cellular distribution in the brain J Neurosci Res 37 4 461 465 1:CAS:528:DyaK2cXitFegsbY%3D 10.1002/jnr.490370405 8021970 (Pubitemid 24105152)
6. H Degani M Gochin SJ Karlish Y Shechter 1981 Electron paramagnetic resonance studies and insulin-like effects of vanadium in rat adipocytes Biochemistry 20 20 5795 5799 1:CAS:528:DyaL3MXlt1KltL8%3D 10.1021/bi00523a023 6271193 (Pubitemid 12217508)
7. AM Evangelou 2002 Vanadium in cancer treatment Crit Rev Oncol Hematol 42 3 249 265 10.1016/S1040-8428(01)00221-9 12050018 (Pubitemid 34615688)
8. EVM (2002) Expert group on vitamins and minerals. Review of vanadium. EVM/00/04:1-16
9. GB Garcia AD Quiroga N Sturtz AI Martinez ME Biancardi 2004 Morphological alterations of central nervous system (CNS) myelin in vanadium (V)-exposed adult rats Drug Chem Toxicol 27 3 281 293 1:CAS:528:DC%2BD2cXmsFClsr4%3D 10.1081/DCT-120037747 15478949 (Pubitemid 39238079)
10. SJ Garcia K Gellein T Syversen M Aschner 2007 Iron deficient and manganese supplemented diets alter metals and transporters in the developing rat brain Toxicol Sci 95 1 205 214 1:CAS:528:DC%2BD28XhtlChtLbK 10.1093/toxsci/kfl139 17060373 (Pubitemid 44942791)
11. SS Haider AA Abdel-Gayoum M el-Fakhri KM Ghwarsha 1998 Effect of selenium on vanadium toxicity in different regions of rat brain Hum Exp Toxicol 17 1 23 28 1:CAS:528:DyaK1cXhtVaiu7Y%3D 10.1191/096032798678907784 9491334 (Pubitemid 28043835)
12. PM Harrison P Arosio 1996 The ferritins: molecular properties, iron storage function and cellular regulation Biochim Biophys Acta 1275 161 203 10.1016/0005-2728(96)00022-9 8695634 (Pubitemid 26248989)
13. A Heinz KA Rubinson JJ Grantham 1982 The transport and accumulation of oxyvanadium compounds in human erythrocytes in vitro J Lab Clin Med 100 4 593 612 1:CAS:528:DyaL38Xlsl2ntb4%3D 6288820 (Pubitemid 12003129)
14. S Hemdan G Almazan 2007 Deficient peroxide detoxification underlies the susceptibility of oligodendrocyte progenitors to dopamine toxicity Neuropharmacology 52 6 1385 1395 1:CAS:528:DC%2BD2sXksFahu7Y%3D 10.1016/j.neuropharm.2007.01.019 17400258 (Pubitemid 46628696)
15. BK Hope 1994 A global biogeochemical budget for vanadium Sci Total Environ 141 1-3 1 10 1:CAS:528:DyaK2cXisFajsLc%3D 8178118
16. SW Hulet SO Heyliger S Powers JR Connor 2000 Oligodendrocyte progenitor cells internalize ferritin via clathrin-dependent receptor mediated endocytosis J Neurosci Res 61 1 52 60 1:CAS:528:DC%2BD3cXksF2iu7o%3D 10.1002/1097- 4547(20000701)61:1<52::AID-JNR6>3.0.CO;2-T 10861799 (Pubitemid 30436474)
17. J Husain BH Juurlink 1995 Oligodendroglial precursor cell susceptibility to hypoxia is related to poor ability to cope with reactive oxygen species Brain Res 698 1-2 86 94 1:CAS:528:DyaK2MXptVehtrk%3D 10.1016/0006-8993(95)00832-B 8581507
18. OO Igado JO Olopade SK Onwuka AC Chukwudi OA Daramola UE Ajufo 2008 Evidence of environmental pollution in caprine brains obtained from a relatively unindustrialized area in Nigeria AJBR 11 305 309
19. BH Juurlink SK Thorburne L Hertz 1998 Peroxide-scavenging deficit underlies oligodendrocyte susceptibility to oxidative stress Glia 22 4 371 378 1:STN:280:DyaK1c7ns1OntA%3D%3D 10.1002/(SICI)1098-1136(199804)22:4<371::AID- GLIA6>3.0.CO;2-6 9517569 (Pubitemid 28129714)
20. M Mates 2000 Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology Toxicology 153 83 104 1:CAS:528: DC%2BD3cXot12ksrc%3D 10.1016/S0300-483X(00)00306-1 11090949
21. K Mawatari Y Yasui K Sugitani T Takadera S Kato 1996 Reactive oxygen species involved in the glutamate toxicity of C6 glioma cells via xc antiporter system Neuroscience 73 1 201 208 1:CAS:528:DyaK28Xjs1akt7w%3D 10.1016/0306-4522(96)00025-5 8783242
22. KD McCarthy J de Vellis 1980 Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue J Cell Biol 85 3 890 902 1:CAS:528:DyaL3cXkvFaltL0%3D 10.1083/jcb.85.3.890 6248568 (Pubitemid 10007455)
23. Monteiro HP, Winterbourn CC, Stern A (1991) Tetravalent vanadium releases ferritin iron which stimulates vanadium-dependent lipid peroxidation. Free Radic Res Commun 12-13(Pt 1):125-129
24. MH Nagaoka H Akiyama T Maitani 2004 Binding patterns of vanadium to transferrin in healthy human serum studied with HPLC/high resolution ICP-MS Analyst 129 1 51 54 1:CAS:528:DC%2BD2cXksFWg 10.1039/b311013n 14737583 (Pubitemid 38130301)
25. JO Nriagu JM Pacyna 1988 Quantitative assessment of worldwide contamination of air, water and soils by trace metals Nature 333 6169 134 139 1:CAS:528:DyaL1cXktFSqsrw%3D 10.1038/333134a0 3285219 (Pubitemid 18624142)
26. RS Ray B Rana B Swami V Venu M Chatterjee 2006 Vanadium mediated apoptosis and cell cycle arrest in MCF7 cell line Chem Biol Interact 163 3 239 247 1:CAS:528:DC%2BD28XhtFSksbjF 10.1016/j.cbi.2006.08.006 16970931 (Pubitemid 44572229)
27. AJ Roskams JR Connor 1990 Aluminum access to the brain: a role for transferrin and its receptor Proc Natl Acad Sci USA 87 22 9024 9027 1:CAS:528:DyaK3MXjsleltA%3D%3D 10.1073/pnas.87.22.9024 2247478 (Pubitemid 120007642)
28. E Sabbioni E Marafante 1981 Relations between iron and vanadium metabolism: in vivo incorporation of vanadium into iron proteins of the rat J Toxicol Environ Health 8 3 419 429 1:CAS:528:DyaL38XjtVSi 10.1080/ 15287398109530080 7345166 (Pubitemid 12233798)
29. E Sabbioni J Rade F Bertolero 1980 Relationships between iron and vanadium metabolism: the exchange of vanadium between transferrin and ferritin J Inorg Biochem 12 4 307 315 1:CAS:528:DyaL3cXltV2htLc%3D 10.1016/S0162-0134(00) 80271-8 7411140 (Pubitemid 11231697)
30. E Sabbioni G Pozzi S Devos A Pintar L Casella M Fischbach 1993 The intensity of vanadium(V)-induced cytotoxicity and morphological transformation in BALB/3T3 cells is dependent on glutathione-mediated bioreduction to vanadium(IV) Carcinogenesis 14 12 2565 2568 1:CAS:528:DyaK2cXpvFSqsQ%3D%3D 10.1093/carcin/14.12.2565 8269628 (Pubitemid 24016597)
31. MM Sasi SS Haider M el-Fakhri KM Ghwarsha 1994 Microchromatographic analysis of lipids, protein, and occurrence of lipid peroxidation in various brain areas of vanadium exposed rats: a possible mechanism of vanadium neurotoxicity Neurotoxicology 15 2 413 420 1:CAS:528:DyaK2cXmslCjsLw%3D 7991230 (Pubitemid 24249429)
32. S Shrivastava 2007 Effect of tiron and its combination with nutritional supplements against vanadium intoxication in female albino rats J Toxicol Sci 32 2 185 192 1:CAS:528:DC%2BD2sXovFSnurw%3D 10.2131/jts.32.185 17538242 (Pubitemid 46849775)
33. M Soazo GB Garcia 2007 Vanadium exposure through lactation produces behavioral alterations and CNS myelin deficit in neonatal rats Neurotoxicol Teratol 29 4 503 510 1:CAS:528:DC%2BD2sXmtVOmu7k%3D 10.1016/j.ntt.2007.03.001 17493788 (Pubitemid 46818890)
34. N Surguladze KM Thompson JL Beard JR Connor MG Fried 2004 Interactions and reactions of ferritin with DNA J Biol Chem 279 15 14694 14702 1:CAS:528:DC%2BD2cXivVKht7c%3D 10.1074/jbc.M313348200 14734543 (Pubitemid 38618859)
35. SK Thorburne BH Juurlink 1996 Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress J Neurochem 67 3 1014 1022 1:CAS:528:DyaK28XltlKkt7k%3D 10.1046/j.1471-4159.1996.67031014.x 8752107 (Pubitemid 26277913)
36. Todorich B, Zhang X, Connor JR (submitted) H-ferritin is an alternative iron delivery system to transferrin in oligodendrocytes. Glia
37. B Todorich X Zhang B Slagle-Webb WE Seaman JR Connor 2008 Tim-2 is the receptor for H-ferritin on oligodendrocytes J Neurochem 107 6 1495 1505 1:CAS:528:DC%2BD1MXis1Sksw%3D%3D 10.1111/j.1471-4159.2008.05678.x 19014383
38. B Todorich JM Pasquini CI Garcia PM Paez JR Connor 2009 Oligodendrocytes and myelination: the role of iron Glia 57 5 467 478 10.1002/glia.20784 18837051
39. X Zhang M Haaf B Todorich E Grosstephan H Schieremberg N Surguladze JR Connor 2005 Cytokine toxicity to oligodendrocyte precursors is mediated by iron Glia 52 3 199 208 10.1002/glia.20235 15968631 (Pubitemid 43078509)