Non-cell autonomous impairment of oligodendrocyte differentiation precedes CNS degeneration in the Zitter rat: Implications of macrophage/microglial activation in the pathogenesis

BMC Neuroscience

Volumn 9, Issue , 2008, Pages

  Sakakibara, Shin Ichi ^a   Nakadate, Kazuhiko ^a   Ookawara, Shigeo ^b   Ueda, Shuichi ^a  

^a DOKKYO MEDICAL UNIVERSITY   (Japan)

^b JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; ATTRACTIN; DIPEPTIDYL PEPTIDASE IV; INTERLEUKIN 1BETA; REACTIVE OXYGEN METABOLITE; ATRN PROTEIN, RAT; FERRITIN; IRON; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL INTERACTION; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEGENERATIVE DISEASE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IRON TRANSPORT; MACROPHAGE ACTIVATION; MICROGLIA; MONOCYTE; MYELINATION; NERVE CELL DEGENERATION; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PARENCHYMA; PATHOGENESIS; POSTNATAL DEVELOPMENT; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; UPREGULATION; ZITTER RAT; ANIMAL; BIOSYNTHESIS; BRAIN; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; MACROPHAGE; METABOLISM; MUTATION; NERVE DEGENERATION; PATHOLOGY; PHYSIOLOGY; RAT STRAIN;

ANIMALS; ANTIGENS, CD26; BRAIN; CELL DIFFERENTIATION; FERRITINS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-1BETA; IRON; MACROPHAGE ACTIVATION; MACROPHAGES; MEMBRANE PROTEINS; MICROGLIA; MUTATION; NERVE DEGENERATION; OLIGODENDROGLIA; RATS; RATS, MUTANT STRAINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 42449095557     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-9-35     Document Type: Article

References (64)

1. Gehrmann J Matsumoto Y Kreutzberg GW Microglia: Intrinsic immuneffector cell of the brain Brain Res Brain Res Rev 1995, 20:269-287. 10.1016/ 0165-0173(94)00015-H 7550361
2. Minagar A Shapshak P Fujimura R Ownby R Heyes M Eisdorfer C The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, alzheimer disease, and multiple sclerosis J Neurol Sci 2002, 202:13-23. 10.1016/ S0022-510X(02)00207-1 12220687
3. Sipe JC Lee P Beutler E Brain iron metabolism and neurodegenerative disorders Dev Neurosci 2002, 24:188-196. 10.1159/000065701 12401958
4. Rehm S Mehraein P Anzil AP Deerberg F A new rat mutant with defective overhairs and spongy degeneration of the central nervous system: Clinical and pathologic studies Lab Anim Sci 1982, 32:70-73. 7078076
5. Gomi H Ueno I Yamanouchi K Antioxidant enzymes in the brain of zitter rats: Abnormal metabolism of oxygen species and its relevance to pathogenic changes in the brain of zitter rats with genetic spongiform encephalopathy Brain Res 1994, 653:66-72. 10.1016/0006-8993(94)90373-5 7982077
6. Ueda S Sakakibara S Nakadate K Noda T Shinoda M Joyce JN Degeneration of dopaminergic neurons in the substantia nigra of zitter mutant rat and protection by chronic intake of vitamin E Neurosci Lett 2005, 380:252-256. 10.1016/j.neulet.2005.01.053 15862896
7. Ueda S Sakakibara S Watanabe E Yoshimoto K Koibuchi N Vulnerability of monoaminergic neurons in the brainstem of the zitter rat in oxidative stress Prog Brain Res 2002, 136:293-302. 12143389
8. Ueda S Aikawa M Ishizuya-Oka A Yamaoka S Koibuchi N Yoshimoto K Age-related dopamine deficiency in the mesostriatal dopamine system of zitter mutant rats: Regional fiber vulnerability in the striatum and the olfactory tubercle Neuroscience 2000, 95:389-398. 10.1016/ S0306-4522(99)00451-0 10658618
9. Nakadate K Noda T Sakakibara S Kumamoto K Matsuura T Joyce JN Ueda S Progressive dopaminergic neurodegeneration of substantia nigra in the zitter mutant rat Acta Neuropathol (Berl) 2006, 112:64-73. 10.1007/ s00401-006-0058-8
10. Kondo A Sendoh S Takamatsu J Nagara H The zitter rat: Membranous abnormality in the schwann cells of myelinated nerve fibers Brain Res 1993, 613:173-179. 10.1016/0006-8993(93)90471-X 8348302
11. Kondo A Sendoh S Akazawa K Sato Y Nagara H Early myelination in zitter rat: Morphological, immunocytochemical and morphometric studies Brain Res Dev Brain Res 1992, 67:217-228. 10.1016/0165-3806(92)90222-I 1380901
12. Kondo A Sato Y Nagara H An ultrastructural study of oligodendrocytes in zitter rat: A new animal model for hypomyelination in the CNS J Neurocytol 1991, 20:929-939. 10.1007/BF01190470 1761975
13. Kuramoto T Kitada K Inui T Sasaki Y Ito K Hase T Kawagachi S Ogawa Y Nakao K Barsh GS Nagao M Ushijima T Serikawa T Attractin/mahogany/zitter plays a critical role in myelination of the central nervous system Proc Natl Acad Sci USA 2001, 98:559-564. 14626 11209055 10.1073/pnas.98.2.559
14. Duke-Cohan JS Gu J McLaughlin DF Xu Y Freeman GJ Schlossman SF Attractin (DPPT-L), a member of the CUB family of cell adhesion and guidance proteins, is secreted by activated human T lymphocytes and modulates immune cell interactions Proc Natl Acad Sci USA 1998, 95:11336-11341. 21643 9736737 10.1073/pnas.95.19.11336
15. Blanc G Font B Eichenberger D Moreau C Ricard-Blum S Hulmes DJ Moali C Insights into how CUB domains can exert specific functions while sharing a common fold: Conserved and specific features of the CUB1 domain contribute to the molecular basis of procollagen C-proteinase enhancer-1 activity J Biol Chem 2007, 282:16924-16933. 10.1074/jbc.M701610200 17446170
16. Lu X Gunn TM Shieh K Barsh GS Akil H Watson SJ Distribution of Mahogany/ Attractin mRNA in the rat central nervous system FEBS Lett 1999, 462:101-107. 10.1016/S0014-5793(99)01494-5 10580100
17. Duke-Cohan JS Tang W Schlossman SF Attractin: A cub-family protease involved in T cell-monocyte/macrophage interactions Adv Exp Med Biol 2000, 477:173-185. 10849745
18. Gunn TM Miller KA He L Hyman RW Davis RW Azarani A Schlossman SF Duke-Cohan JS Barsh GS The mouse mahogany locus encodes a transmembrane form of human attractin Nature 1999, 398:152-156. 10.1038/18217 10086356
19. Nagle DL McGrail SH Vitale J Woolf EA Dussault BJ Jr DiRocco L Holmgren L Montagno J Bork P Huszar D Fairchild-Huntress V Ge P Keilty J Ebeling C Baldini L Gilchrist J Burn P Carlson GA Moore KJ The mahogany protein is a receptor involved in suppression of obesity Nature 1999, 398:148-152. 10.1038/18210 10086355
20. Wrenger S Faust J Friedrich D Hoffmann T Hartig R Lendeckel U Kahne T Thielitz A Neubert K Reinhold D Attractin, a dipeptidyl peptidase IV/ CD26-like enzyme, is expressed on human peripheral blood monocytes and potentially influences monocyte function J Leukoc Biol 2006, 80:621-629. 10.1189/jlb.1105678 16835316
21. Friedrich D Hoffmann T Bar J Wermann M Manhart S Heiser U Demuth HU Does human attractin have DP4 activity? Biol Chem 2007, 388:155-162. 10.1515/ BC.2007.017 17261078
22. Christopherson KW 2nd Hangoc G Broxmeyer HE Cell surface peptidase CD26/ dipeptidylpeptidase IV regulates CXCL12/stromal cell-derived factor-1 alpha-mediated chemotaxis of human cord blood CD34+ progenitor cells J Immunol 2002, 169:7000-7008. 12471135
23. Sedo A Duke-Cohan JS Balaziova E Sedova LR Dipeptidyl peptidase IV activity and/or structure homologs: Contributing factors in the pathogenesis of rheumatoid arthritis? Arthritis Res Ther 2005, 7:253-269. 1297595 16277701 10.1186/ar1852
24. Friedman B Hockfield S Black JA Woodruff KA Waxman SG In situ demonstration of mature oligodendrocytes and their processes: An immunocytochemical study with a new monoclonal antibody, rip Glia 1989, 2:380-390. 10.1002/glia.440020510 2530173
25. Goddard DR Berry M Butt AM In vivo actions of fibroblast growth factor-2 and insulin-like growth factor-I on oligodendrocyte development and myelination in the central nervous system J Neurosci Res 1999, 57:74-85. 10.1002/(SICI)1097-4547(19990701)57:1<74::AID-JNR8>3.0.CO;2-O 10397637
26. Hardy RJ Friedrich VL Jr Progressive remodeling of the oligodendrocyte process arbor during myelinogenesis Dev Neurosci 1996, 18:243-254. 10.1159/000111414 8911764
27. Connor JR Menzies SL Relationship of iron to oligodendrocytes and myelination Glia 1996, 17:83-93. 10.1002/ (SICI)1098-1136(199606)17:2<83::AID-GLIA1>3.0.CO;2-7 8776576
28. Zecca L Youdim MB Riederer P Connor JR Crichton RR Iron, brain ageing and neurodegenerative disorders Nat Rev Neurosci 2004, 5:863-873. 10.1038/nrn1537 15496864
29. Nakadate k Sakakibara S Ueda S Attractin/Mahogany protein expression in the rodent central nervous system J Comp Neurol
30. Nishiyama A Lin XH Giese N Heldin CH Stallcup WB Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain J Neurosci Res 1996, 43:299-314. 10.1002/ (SICI)1097-4547(19960201)43:3<299::AID-JNR5>3.0.CO;2-E 8714519
31. Marshall CA Novitch BG Goldman JE Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells J Neurosci 2005, 25:7289-7298. 10.1523/JNEUROSCI.1924-05.2005 16093378
32. Zhang SC Defining glial cells during CNS development Nat Rev Neurosci 2001, 2:840-843. 10.1038/35097593 11715061
33. Reinhold D Kahne T Steinbrecher A Wrenger S Neubert K Ansorge S Brocke S The role of dipeptidyl peptidase IV (DP IV) enzymatic activity in T cell activation and autoimmunity Biol Chem 2002, 383:1133-1138. 10.1515/ BC.2002.123 12437097
34. Karpus WJ Ransohoff RM Chemokine regulation of experimental autoimmune encephalomyelitis: Temporal and spatial expression patterns govern disease pathogenesis J Immunol 1998, 161:2667-2671. 9743321
35. Perrin FE Lacroix S Aviles-Trigueros M David S Involvement of monocyte chemoattractant protein-1, macrophage inflammatory protein-1alpha and interleukin-1beta in wallerian degeneration Brain 2005, 128:854-866. 10.1093/brain/awh407 15689362
36. Iwata S Yamaguchi N Munakata Y Ikushima H Lee JF Hosono O Schlossman SF Morimoto C CD26/dipeptidyl peptidase IV differentially regulates the chemotaxis of T cells and monocytes toward RANTES: Possible mechanism for the switch from innate to acquired immune response Int Immunol 1999, 11:417-426. 10.1093/intimm/11.3.417 10221653
37. Pedersen EB Fox LM Castro AJ McNulty JA Immunocytochemical and electron-microscopic characterization of macrophage/microglia cells and expression of class II major histocompatibility complex in the pineal gland of the rat Cell Tissue Res 1993, 272:257-265. 10.1007/BF00302731 8513480
38. Damoiseaux JG Dopp EA Calame W Chao D MacPherson GG Dijkstra CD Rat macrophage lysosomal membrane antigen recognized by monoclonal antibody ED1 Immunology 1994, 83:140-147. 1415006 7821959
39. Milligan CE Cunningham TJ Levitt P Differential immunochemical markers reveal the normal distribution of brain macrophages and microglia in the developing rat brain J Comp Neurol 1991, 314:125-135. 10.1002/ cne.903140112 1797868
40. Ruggeri ZM Ware J Von willebrand factor FASEB J 1993, 7:308-316. 8440408
41. Ito D Imai Y Ohsawa K Nakajima K Fukuuchi Y Kohsaka S Microglia-specific localisation of a novel calcium binding protein, Iba1 Brain Res Mol Brain Res 1998, 57:1-9. 10.1016/S0169-328X(98)00040-0 9630473
42. Kadowaki T Nakadate K Sakakibara S Hirata K Ueda S Expression of Iba1 protein in microglial cells of zitter mutant rat Neurosci Lett 2007, 411:26-31. 10.1016/j.neulet.2006.07.079 17110035
43. Vallières L Sawchenko PE Bone marrow-derived cells that populate the adult mouse brain preserve their hematopoietic identity J Neurosci 2003, 23:5197-5207. 12832544
44. Azouz A Gunn TM Duke-Cohan JS Juvenile-onset loss of lipid-raft domains in attractin-deficient mice Exp Cell Res 2007, 313:761-771. 10.1016/ j.yexcr.2006.11.018 17196964
45. Walker WP Aradhya S Hu CL Shen S Zhang W Azarani A Lu X Barsh GS Gunn TM Genetic analysis of attractin homologs Genesis 2007, 45:744-756. 10.1002/ dvg.20351 18064672
46. Kuwamura M Maeda M Kuramoto T Kitada K Kanehara T Moriyama M Nakane Y Yamate J Ushijima T Kotani T Serikawa T The myelin vacuolation (mv) rat with a null mutation in the attractin gene Lab Invest 2002, 82:1279-1286. 12379762
47. Tang W Duke-Cohan JS Human secreted attractin disrupts neurite formation in differentiating cortical neural cells in vitro J Neuropathol Exp Neurol 2002, 61:767-777. 12230323
48. Cuadros MA Navascues J Early origin and colonization of the developing central nervous system by microglial precursors Prog Brain Res 2001, 132:51-59. 11545016
49. Halliwell B Reactive oxygen species and the central nervous system J Neurochem 1992, 59:1609-1623. 10.1111/j.1471-4159.1992.tb10990.x 1402908
50. Husain J Juurlink BH Oligodendroglial precursor cell susceptibility to hypoxia is related to poor ability to cope with reactive oxygen species Brain Res 1995, 698:86-94. 10.1016/0006-8993(95)00832-B 8581507
51. Back SA Gan X Li Y Rosenberg PA Volpe JJ Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion J Neurosci 1998, 18:6241-6253. 9698317
52. Baerwald KD Popko B Developing and mature oligodendrocytes respond differently to the immune cytokine interferon-gamma J Neurosci Res 1998, 52:230-239. 10.1002/ (SICI)1097-4547(19980415)52:2<230::AID-JNR11>3.0.CO;2-B 9579413
53. Vartanian T Li Y Zhao M Stefansson K Interferon-gamma-induced oligodendrocyte cell death: Implications for the pathogenesis of multiple sclerosis Mol Med 1995, 1:732-743. 2230017 8612196
54. Buntinx M Moreels M Vandenabeele F Lambrichts I Raus J Steels P Stinissen P Ameloot M Cytokine-induced cell death in human oligodendroglial cell lines: I. synergistic effects of IFN-gamma and TNF-alpha on apoptosis J Neurosci Res 2004, 76:834-845. 10.1002/ jnr.20118 15160395
55. Andrews T Zhang P Bhat NR TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors J Neurosci Res 1998, 54:574-583. 10.1002/(SICI)1097-4547(19981201)54:5<574::AID-JNR2>3.0.CO;2-0 9843148
56. Vela JM Molina-Holgado E Arevalo-Martin A Almazan G Guaza C Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells Mol Cell Neurosci 2002, 20:489-502. 10.1006/mcne.2002.1127 12139924
57. Lambeir AM Proost P Durinx C Bal G Senten K Augustyns K Scharpe S Van Damme J De Meester I Kinetic investigation of chemokine truncation by CD26/dipeptidyl peptidase IV reveals a striking selectivity within the chemokine family J Biol Chem 2001, 276:29839-29845. 10.1074/ jbc.M103106200 11390394
58. Duke-Cohan JS Kim JH Azouz A Attractin: Cautionary tales for therapeutic intervention in molecules with pleiotropic functionality J Environ Pathol Toxicol Oncol 2004, 23:1-11. 10.1615/JEnvPathToxOncol.v23.i1.10 14994991
59. Pedchenko TV LeVine SM Desferrioxamine suppresses experimental allergic encephalomyelitis induced by MBP in SJL mice J Neuroimmunol 1998, 84:188-197. 10.1016/S0165-5728(97)00256-7 9628462
60. Heppner FL Greter M Marino D Falsig J Raivich G Hovelmeyer N Waisman A Rulicke T Prinz M Priller J Becher B Aguzzi A Experimental autoimmune encephalomyelitis repressed by microglial paralysis Nat Med 2005, 11:146-152. 10.1038/nm1177 15665833
61. Steinbrecher A Reinhold D Quigley L Gado A Tresser N Izikson L Born I Faust J Neubert K Martin R Ansorge S Brocke S Targeting dipeptidyl peptidase IV (CD26) suppresses autoimmune encephalomyelitis and up-regulates TGF-beta 1 secretion in vivo J Immunol 2001, 166:2041-2048. 11160254
62. Hill JM Switzer RC 3rd The regional distribution and cellular localization of iron in the rat brain Neuroscience 1984, 11:595-603. 10.1016/0306-4522(84)90046-0 6717804
63. Sakakibara S Nakamura Y Satoh H Okano H RNA-binding protein Musashi2: Developmentally regulated expression in neural precursor cells and subpopulations of neurons in mammalian CNS J Neurosci 2001, 21:8091-8107. 11588182
64. McCarthy KD de Vellis J Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue J Cell Biol 1980, 85:890-902. 10.1083/jcb.85.3.890 6248568