Loss of lysophosphatidic acid receptor LPA1 alters oligodendrocyte differentiation and myelination in the mouse cerebral cortex

Brain Structure and Function

Volumn 220, Issue 6, 2015, Pages 3701-3720

  García Díaz, Beatriz ^a,b   Riquelme, Raquel ^c   Varela Nieto, Isabel ^c   Jiménez, Antonio Jesús ^d   de Diego, Isabel ^e   Gómez Conde, Ana lsabel ^d   Matas Rico, Elisa ^a,f   Aguirre, José Ángel ^e   Chun, Jerold ^g   Pedraza, Carmen ^d   Santín, Luis Javier ^d   Fernández, Oscar ^d   Rodríguez de Fonseca, Fernando ^a   Estivill Torrús, Guillermo ^a,d  

^a HOSPITAL REGIONAL UNIVERSITARIO DE MÁLAGA   (Spain)

^b Department of Medicine   (United States)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d Institute of Biomedical Research in Malaga and BIONAND Nanomedicine Platform   (Spain)

^e UNIVERSITY OF MÁLAGA   (Spain)

^f NETHERLANDS CANCER INSTITUTE   (Netherlands)

^g SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Cerebral cortex; Lysophosphatidic acid receptor; Myelin; Oligodendrocyte

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; BRAIN PROTEIN; LYSOPHOSPHATIDIC ACID RECEPTOR; LYSOPHOSPHATIDIC ACID RECEPTOR A1; MYELIN BASIC PROTEIN; PROTEOLIPID PROTEIN; UNCLASSIFIED DRUG; MYELIN PROTEIN;

ADULT; ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CORTEX; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; CORPUS CALLOSUM; ELECTRON MICROSCOPY; ENZYME ACTIVITY; EXTERNAL CAPSULE; FIMBRIA; IMMUNOHISTOCHEMISTRY; INTRACELLULAR TRANSPORT; MOUSE; MYELINATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; STEADY STATE; STEREOMETRY; ANIMAL; AXON; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; MYELIN SHEATH; PHYSIOLOGY; PROTEIN TRANSPORT; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; AXONS; CELL DIFFERENTIATION; CEREBRAL CORTEX; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MICE; MICE, KNOCKOUT; MYELIN PROTEINS; MYELIN SHEATH; OLIGODENDROGLIA; PROTEIN TRANSPORT; RECEPTORS, LYSOPHOSPHATIDIC ACID;

EID: 84942342633     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0885-7     Document Type: Article

References (102)

1. Allard J, Barron S, Diaz J, Lubetzki C, Zalc B, Schwartz JC, Sokoloff P (1998) A rat G protein-coupled receptor selectively expressed in myelin-forming cells. Eur J Neurosci 10:1045–1053
2. Anliker B, Chun J (2004) Lysophospholipid G protein-coupled receptors. J Biol Chem 279:20555–20558
3. Anliker B, Choi JW, Lin ME, Gardell SE, Rivera RR, Kennedy G, Chun J (2013) Lysophosphatidic acid (LPA) and its receptor, LPA1, influence embryonic schwann cell migration, myelination, and cell-to-axon segregation. Glia 61:2009–2022
4. Baslow MH (2003) N-Acetylaspartate in the vertebrate brain: metabolism and function. Neurochem Res 28:941–953
5. Baumann N, Pham-Dinh D (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81:871–927
6. Bhakoo KK, Pearce D (2000) In vitro expression of N-acetyl aspartate by oligodendrocytes: implications for proton magnetic resonance spectroscopy signal in vivo. J Neurochem 74:254–262
7. Birgbauer E, Chun J (2006) New developments in the biological functions of lysophospholipids. Cell Mol Life Sci 63:2695–2701
8. Blanco E, Bilbao A, Luque MJ, Palomino A, Bermudez-Silva FJ, Suarez J, Santin L, Gutierrez A, Campos-Sandoval JA, Marquez J, Estivill-Torrus G, Rodriguez De Fonseca F (2012) Lack of cocaine-induced conditioned locomotion is associated with altered expression of hippocampal glutamate receptors in mice lacking lpa1 receptor. Psychopharmacology 220:27–42
9. Bonavita S, Di Salle F, Tedeschi G (1999) Proton MRS in neurological disorders. Eur J Radiol 30:125–131
10. Brinkmann V, Lynch KR (2002) FTY720: Targeting G-protein-coupled receptors for sphingosine 1-phosphate in transplantation and autoimmunity. Curr Opin Immunol 14:569–575
11. Castilla-Ortega E, Sánchez-López J, Hoyo-Becerra C, Matas Rico E, Zambrana-Infantes E, Chun J, Rodríguez de Fonseca F, Pedraza C, Estivill-Torrús G, Santín LJ (2010) Activity, anxiety and spatial memory impairments are dissociated in mice lacking the LPA1 receptor. Neurobiol Learn Mem 94:73–82
12. Castilla-Ortega E, Hoyo-Becerra C, Pedraza C, Chun J, Rodríguez de Fonseca F, Estivill-Torrús G, Santín LJ (2011) Aggravation of the pathological consequences of chronic stress on hippocampal neurogenesis and spatial memory in mice lacking the LPA1 receptor. PLoS ONE 6(9):e25522
13. Castilla-Ortega E, Pedraza C, Chun J, Rodríguez de Fonseca F, Estivill-Torrús G, Santin LJ (2012) Hippocampal c-Fos activation in normal and LPA1-null mice after two object recognition tasks with different memory demands. Behav Brain Res 232:400–405
14. Cervera P, Tirard M, Barron S, Allard J, Trottier S, Lacombe J, Daumas-Duport C, Sokoloff P (2002) Immunohistological localization of the myelinating cell-specific receptor LP(A1). Glia 38:126–136
15. Choi JW, Chun J (2013) Lysophospholipids and their receptors in the central nervous system. Biochim Biophys Acta 1831:20–32
16. Choi JW, Herr DR, Noguchi K, Yung YC, Lee CW, Mutoh T, Lin ME, Teo ST, Park KE, Mosley AN, Chun J (2010) LPA receptors: subtypes and biological actions. Annu Rev Pharmacol Toxicol 50:157–186
17. Chun J (2005) Lysophospholipids in the nervous system. Prostaglandins Other Lipid Mediat 77:46–51
18. Chun J, Rosen H (2006) Lysophospholipid receptors as potential drug targets in tissue transplantation and autoimmune diseases. Curr Pharm Des 12:161–171
19. Colman DR, Kreibich G, Frey AB, Sabatini DD (1982) Synthesis and incorporation of myelin polypeptides into CNS myelin. J Cell Biol 95:598–608
20. Contos JJ, Fukushima N, Weiner JA, Kaushal D, Chun J (2000) Requirement for the lpA1 lysophosphatidic acid receptor gene in normal suckling behavior. Proc Natl Acad Sci USA 97:13384–13389
21. Dawson J, Hotchin N, Lax S, Rumsby M (2003) Lysophosphatidic acid induces process retraction in CG-4 line oligodendrocytes and oligodendrocyte precursor cells but not in differentiated oligodendrocytes. J Neurochem 87:947–957
22. Dennis D, White MA, Forrest AD, Yuelling LM, Nogaroli L, Afshari FS, Fox MA, Fuss B (2008) Phosphodiesterase- I/Autotaxin’s MORFO domain regulates oligodendroglial process network formation and focal adhesion organization. Mol Cell Neurosci 37:412–424
23. Dimou L, Simon C, Kirchhoff F, Takebayashi H, Götz M (2008) Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci 28:10434–10442
24. Drøjdahl N, Nielsen HH, Gardi JE, Wree A, Peterson AC, Nyengaard JR, Eyer J, Finsen B (2010) Axonal plasticity elicits long-term changes in oligodendroglia and myelinated fibers. Glia 58:29–42
25. Edgar JM, Nave KA (2009) The role of CNS glia in preserving axon function. Curr Opin Neurobiol 19:498–504
26. Edgar JM, McLaughlin M, Werner HB, McCulloch MC, Barrie JA, Brown A, Faichney AB, Snaidero N, Nave KA, Griffiths IR (2009) Early ultrastructural defects of axons and axon-glia junctions in mice lacking expression of Cnp1. Glia 16:1815–1824
27. Emery B (2010) Regulation of oligodendrocyte differentiation and myelination. Science 330:779–782
28. Estivill-Torrús G, Llebrez-Zayas P, Matas-Rico E, Santín L, Pedraza C, De Diego I, Del Arco I, Fernández-Llebrez P, Chun J, Rodríguez de Fonseca F (2008) Absence of LPA1 signaling results in defective cortical development. Cereb Cortex 18:938–950
29. Estivill-Torrús G, Santín LJ, Pedraza C, Castilla-Ortega E, Rodriguez de Fonseca F (2013) Role of lysophosphatidic acid (LPA) in behavioral processes: implications for psychiatric disorders. In: Chun J (ed) Lysophospholipid receptors: signaling and biochemistry. Wiley, New Jersey, pp 451–474
30. Fannon AM, Moscarello MA (1990) Myelin basic protein is affected by reduced synthesis of myelin proteolipid protein in the jimpy mouse. Biochem J 268:105–110
31. Filippi CG, Uluğ AM, Deck MD, Zimmerman RD, Heier LA (2002) Developmental delay in children: assessment with proton MR spectroscopy. Am J Neuroradiol 23:882–888
32. Fox MA, Colello RJ, Macklin WB, Fuss B (2003) Phosphodiesterase-Ialpha/autotaxin: a counteradhesive protein expressed by oligodendrocytes during onset of myelination. Mol Cell Neurosci 23:507–519
33. García-Fernández M, Castilla-Ortega E, Pedraza C, Blanco E, Hurtado-Guerrero I, Barbancho MA, Chun J, Rodríguez-de-Fonseca F, Estivill-Torrús G, Santín Núñez LJ (2012) Chronic immobilization in the malpar1 knockout mice increases oxidative stress in the hippocampus. Int J Neurosci 122:583–589
34. Gow A, Southwood CM, Lazzarini RA (1998) Disrupted proteolipid protein trafficking results in oligodendrocyte apoptosis in an animal model of Pelizaeus–Merzbacher disease. J Cell Biol 140:925–934
35. Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C, Schwab MH, Schneider A, Zimmermann F, McCulloch M, Nadon N, Nave KA (1998) Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280:1610–1613
36. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ (1988) The new stereological tools: dissector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. Acta Pathol Microbiol Immunol Scand 96:857–881
37. Hamilton BA, Yu BD (2012) Modifier genes and the plasticity of genetic networks in mice. PLoS Genet 8(4):e1002644
38. Hammack BN, Fung KY, Hunsucker SW, Duncan MW, Burgoon MP, Owens GP, Gilden DH (2004) Proteomic analysis of multiple sclerosis cerebrospinal fluid. Mult Scler 10:245–260
39. Handford EJ, Smith D, Hewson L, McAllister G, Beer MS (2001) Edg2 receptor distribution in adult rat brain. Neuroreport 12:757–760
40. Ishibashi T, Dakin KA, Stevens B, Lee PR, Kozlov SV, Stewart CL, Fields RD (2006) Astrocytes promote myelination in response to electrical impulses. Neuron 49:823–832
41. Ishii A, Fyffe-Maricich SL, Furusho M, Miller RH, Bansal R (2012) ERK1/ERK2 MAPK signaling is required to increase myelin thickness independent of oligodendrocyte differentiation and initiation of myelination. J Neurosci 32:8855–8864
42. Kang SH, Fukaya M, Yang JK, Rothstein JD, Bergles DE (2010) NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 68: 668–681
43. Karim SA, Barrie JA, McCulloch MC, Montague P, Edgar JM, Kirkham D, Anderson TJ, Nave KA, Griffiths IR, McLaughlin M (2007) PLP overexpression perturbs myelin protein composition and myelination in a mouse model of Pelizaeus–Merzbacher disease. Glia 55:341–351
44. Kearney JA (2011) Genetic modifiers of neurological disease. Curr Opin Genet Dev 21:349–353
45. Keshavan MS, Diwadkar VA, Harenski K, Rosenberg DR, Sweeney JA, Pettegrew JW (2002) Abnormalities of the corpus callosum in first episode, treatment naive schizophrenia. J Neurol Neurosurg Psychiatry 72:757–760
46. Khiat A, Lesage J, Boulanger Y (2007) Quantitative MRS study of Baló’s concentric sclerosis lesions. Magn Reson Imaging 25:1112–1115
47. Klugmann M, Schwab MH, Pühlhofer A, Schneider A, Zimmermann F, Griffiths IR, Nave KA (1997) Assembly of CNS myelin in the absence of proteolipid protein. Neuron 18:59–70
48. Lin W, Popko B (2009) Endoplasmic reticulum stress in disorders of myelinating cells. Nat Neurosci 212:379–385
49. Lin ME, Herr DR, Chun J (2010) Lysophosphatidic acid (LPA) receptors: signaling properties and disease relevance. Prostaglandins Other Lipid Mediat 91:130–138
50. Linstedt AD, Mehta A, Suhan J, Reggio H, Hauri HP (1997) Sequence and overexpression of GPP130/GIMPc: evidence for saturable pH-sensitive targeting of a type II early Golgi membrane protein. Mol Biol Cell 8:1073–1087
51. Ma L, Hasan KM, Steinberg JL, Narayana PA, Lane SD, Zuniga EA, Kramer LA, Moeller FG (2009) Diffusion tensor imaging in cocaine dependence: regional effects of cocaine on corpus callosum and effect of cocaine administration route. Drug Alcohol Depend 104:262–267
52. Matas-Rico E, García-Díaz B, Llebrez-Zayas P, López-Barroso D, Santín L, Pedraza C, Fernández-Llebrez P, Téllez T, Redondo M, Chun J, Rodríguez de Fonseca F, Estivill-Torrús G (2008) Deletion of lysophosphatidic acid receptor LPA1 reduces neurogenesis in the mouse dentate gyrus. Mol Cell Neurosci 39:342–355
53. Matsushita T, Amagai Y, Soga T, Terai K, Obinata M, Hashimoto S (2005) A novel oligodendrocyte cell line OLP6 shows the successive stages of oligodendrocyte development: late progenitor, immature and mature stages. Neuroscience 136:115–121
54. McLaughlin M, Barrie JA, Karim SA, Montague P, Edgar JM, Kirkham D, Thomson CE, Griffiths IR (2006a) Processing of PLP in a model of Pelizaeus–Merzbacher disease/SPG2 due to the rumpshaker mutation. Glia 53:715–722
55. McLaughlin M, Karim SA, Montague P, Barrie JA, Kirkham D, Griffiths IR, Edgar JM (2006b) Genetic background influences UPR but not PLP processing in the rumpshaker model of PMD/SPG2. Neurochem Res 32:167–176
56. McLean IW, Nakane PK (1974) Periodate-lysine-paraformaldehyde fixative. A new fixative for immunoelectronmicroscopy. Histochem Cytochem 22:1077
57. Miller DH, Austin SJ, Connelly A, Youl BD, Gadian DG, McDonald WI (1991) Proton magnetic resonance spectroscopy of an acute and chronic lesion in multiple sclerosis. Lancet 337:58–59
58. Miyata S, Koyama Y, Takemoto K, Yoshikawa K, Ishikawa T, Taniguchi M, Inoue K, Aoki M, Hori O, Katayama T, Tohyama M (2011) Plasma corticosterone activates SGK1 and induces morphological changes in oligodendrocytes in corpus callosum. PLoS ONE 6:e19859
59. Möller T, Musante DB, Ransom BR (1999) Lysophosphatidic acid-induced calcium signals in cultured rat oligodendrocytes. NeuroReport 10:2929–2932
60. Monge M, Kadiiski D, Jacque CM, Zalc B (1986) Oligodendroglial expression and deposition of four major myelin constituents in the myelin sheath during development. An in vivo study. Dev Neurosci 8:222–235
61. Moolenar WH, van Meeteren LA, Giepmans BNG (2004) The ins and outs of lysophosphatidic acid signaling. BioEssays 26:870–881
62. Moore CS, Milner R, Nishiyama A, Frausto RF, Serwanski DR, Pagarigan RR, Whitton JL, Miller RH, Crocker SJ (2011) Astrocytic tissue inhibitor of metalloproteinase-1 (TIMP-1) promotes oligodendrocyte differentiation and enhances CNS myelination. J Neurosci 31:6247–6254
63. Nakahara J, Tan-Takeuchi K, Seiwa C, Yagi T, Aiso S, Kawamura K, Asou H (2001) Myelin basic protein is necessary for the regulation of myelin-associated glycoprotein expression in mouse oligodendroglia. Neurosci Lett 298:163–166
64. Narayana PA, Ahobila-Vajjula P, Ramu J, Herrera J, Steinberg JL, Moeller FG (2009) Diffusion tensor imaging of cocaine-treated rodents. Psychiatry Res 171:242–251
65. Nave KA (2010) Myelination and support of axonal integrity by glia. Nature 468:244–252
66. Nogaroli L, Yuelling LM, Dennis J, Gorse K, Payne SG, Fuss B (2009) Lysophosphatidic acid can support the formation of membranous structures and an increase in MBP mRNA levels in differentiating oligodendrocytes. Neurochem Res 34:182–193
67. Noguchi K, Herr D, Mutoh T, Chun J (2009) Lysophosphatidic acid (LPA) and its receptors. Curr Opin Pharmacol 9:15–23
68. Norton WT, Poduslo SE (1973) Myelination in rat brain: method of myelin isolation. J Neurochem 21:749–757
69. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. Academic Press, San Diego
70. Pedraza C, Sánchez-López J, Castilla-Ortega E, Rosell-Valle C, Zambrana-Infantes E, García-Fernández M, Rodriguez de Fonseca F, Chun J, Santín LJ, Estivill-Torrús G (2013) Fear extinction and acute stress reactivity reveal a role of LPA1 receptor in regulating emotional-like behaviors. Brain Struct Funct. doi:10.1007/s00429-013-0592-9
71. Penet MF, Laigle C, Fur YL, Confort-Gouny S, Heurteaux C, Cozzone PJ, Viola A (2006) In vivo characterization of brain morphometric and metabolic endophenotypes in three inbred strains of mice using magnetic resonance techniques. Behav Genet 36:732–744
72. Peters A, Palay SL, Webster HD (1991) The fine structure of the nervous system: neurons and their supporting cells. Oxford University Press, New York
73. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, Kessaris N, Richardson WD (2008) PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11:1392–1401
74. Roberts C, Winter P, Shilliam CS, Hughes ZA, Langmead C, Maycox PR, Dawson LA (2005) Neurochemical changes in LPA1 receptor deficient mice-a putative model of schizophrenia. Neurochem Res 30:371–377
75. Rohrer J, Schweizer A, Russell D, Kornfeld S (1996) The targeting of Lamp1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane. J Cell Biol 132:565–576
76. Rosenbluth J, Nave KA, Mierzwa A, Schiff R (2006) Subtle myelin defects in PLP-null mice. Glia 54:172–182
77. Santín L, Bilbao A, Pedraza C, Matas-Rico E, López-Barroso D, Castilla-Ortega E, Sánchez-López J, Riquelme R, Varela-Nieto I, De la Villa P, Suardiaz M, Chun J, Rodríguez de Fonseca F, Estivill-Torrús G (2009) Behavioral phenotype of maLPA1-null mice: increased anxiety-like behavior and spatial memory deficits. Genes Brain Behav 8:772–784
78. Sherman DL, Brophy PJ (2005) Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6:683–690
79. Simone IL, Federico F, Trojano M, Tortorella C, Liguori M, Giannini P, Picciola E, Natile G, Livrea P (1996) High resolution proton MR spectroscopy of cerebrospinal fluid in MS patients. Comparison with biochemical changes in demyelinating plaques. J Neurol Sci 144:182–190
80. Sohn J, Selvaraj V, Wakayama K, Orosco L, Lee E, Crawford SE, Guo F, Lang J, Horiuchi M, Zarbalis K, Itoh T, Deng W, Pleasure D (2012) PEDF is a novel oligodendrogenic morphogen acting on the adult SVZ and corpus callosum. J Neurosci 32:12152–12164
81. Somogyi P, Takagi H (1982) A note on the use of picric acid–paraformaldehyde–glutaraldehyde fixative for correlated light- and electron microscopic immunocytochemistry. Neuroscience 7:1779
82. Sorensen A, Moffat K, Thomson C, Barnett SC (2008) Astrocytes, but not olfactory ensheathing cells or Schwann cells, promote myelination of CNS axons in vitro. Glia 56:750–763
83. Southwood C, Gow A (2001) Molecular pathways of oligodendrocyte apoptosis revealed by mutations in the proteolipid protein gene. Microsc Res Tech 52:700–708
84. Southwood CM, Garbern J, Jiang W, Gow A (2002) The unfolded protein response modulates disease severity in Pelizaeus–Merzbacher disease. Neuron 36:585–596
85. Spohr TC, Choi JW, Gardell SE, Herr DR, Rehen SK, Gomes FC, Chun J (2008) Lysophosphatidic acid receptor-dependent secondary effects via astrocytes promote neuronal differentiation. J Biol Chem 283:7470–7479
86. Spohr TC, Dezonne RS, Rehen SK, Gomes FC (2011) Astrocytes treated by lysophosphatidic acid induce axonal outgrowth of cortical progenitors through extracellular matrix protein and epidermal growth factor signaling pathway. J Neurochem 119:113–123
87. Stankoff B, Barron S, Allard J, Barbin G, Noel F, Aigrot MS, Premont J, Sokoloff P, Zalc B, Lubetzki C (2002) Oligodendroglial expression of Edg-2 receptor: developmental analysis and pharmacological responses to lysophosphatidic acid. Mol Cell Neurosci 20:415–428
88. Steen RG, Ogg RJ (2005) Abnormally high levels of brain N-acetylaspartate in children with sickle cell disease. Am J Neuroradiol 26:463–468
89. Tigyi G (2010) Aiming drug discovery at lysophosphatidic acid targets. Br J Pharmacol 161:241–270
90. Tkachev D, Mimmack ML, Ryan MM, Wayland M, Freeman T, Jones PB, Starkey M, Webster MJ, Yolken RH, Bahn S (2003) Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet 362:798–804
91. Trapp BD, Moench M, Pulley E, Barbosa E, Tennekoon GI, Griffin J (1987) Spatial segregation of mRNA encoding myelinspecific proteins. Proc Natl Acad Sci USA 84:7773–7777
92. Urenjak J, Williams SR, Gadian DG, Noble M (1992) Specific expression of N-acetylaspartate in neurons, oligodendrocyte-type-2 astrocyte progenitors, and immature oligodendrocytes in vitro. J Neurochem 59:55–61
93. Van der Knaap LJ, van der Ham IJ (2011) How does the corpus callosum mediate interhemispheric transfer? A review. Behav Brain Res 223:211–221
94. Villarreal G, Hamilton DA, Graham DP, Driscoll I, Qualls C, Petropoulos H, Brooks WM (2004) Reduced area of the corpus callosum in posttraumatic stress disorder. Psychiatry Res 131:227–235
95. Wang CC (1998) Protein disulfide isomerase assists protein folding as both an isomerase and a chaperone. Ann N Y Acad Sci 864:9–13
96. Warringa RAJ, Hoeben RC, Koper JW, Sykes JEC, van Golde LMG, Lopes-Cardozo M (1987) Hydrocortisone stimulates the development of oligodendrocytes in primary glial cultures and affects glucose metabolism and lipid synthesis in these cultures. Dev Br Res 34:79–86
97. Watkins TA, Emery B, Mulinyawe S, Barres BA (2008) Distinct stages of myelination regulated by gamma-secretase and astrocytes in a rapidly myelinating CNS coculture system. Neuron 60:555–569
98. Weiner JA, Hecht JH, Chun J (1998) Lysophosphatidic acid receptor gene vzg-1/lpA1/edg-2 is expressed by mature oligodendrocytes during myelination in the postnatal murine brain. J Comp Neurol 398:587–598
99. Werner HB, Kuhlmann K, Shen S, Uecker M, Schardt A, Dimova K, Orfaniotou F, Dhaunchak A, Brinkmann BG, Möbius W, Guarente L, Casaccia-Bonnefil P, Jahn O, Nave KA (2007) Proteolipid protein is required for transport of sirtuin 2 into CNS myelin. J Neurosci 27:7717–7730
100. West MJ (1993) New stereological methods for counting neurons. Neurobiol Aging 14:275–285
101. Whitford TJ, Kubicki M, Schneiderman JS, O’Donnell LJ, King R, Alvarado JL, Khan U, Markant D, Nestor PG, Niznikiewicz M, McCarley RW, Westin CF, Shenton ME (2010) Corpus callosum abnormalities and their association with psychotic symptoms in patients with schizophrenia. Biol Psychiatry 68:70–77
102. Yu N, Lariosa-Willingham KD, Lin FF, Webb M, Rao TS (2004) Characterization of lysophosphatidic acid and sphingosine-1-phosphate-mediated signal transduction in rat cortical oligodendrocytes. Glia 45:17–27