A subtractive approach to characterize genes with regionalized expression in the gliogenic ventral neuroepithelium: Identification of chick Sulfatase 1 as a new oligodendrocyte lineage gene

Molecular and Cellular Neuroscience

Volumn 25, Issue 4, 2004, Pages 612-628

  Braquart Varnier, Christine ^a   Danesin, Cathy ^a   Clouscard Martinato, Catherine ^a   Agius, Eric ^a   Escalas, Nathalie ^a   Benazeraf, Bertrand ^a   Ai, Xingbin ^b   Emerson, Charles ^b   Cochard, Philippe ^a   Soula, Cathy ^a  

^a Centre de Biologie du Developpement Toulouse   (France)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL MARKER; CELL SURFACE PROTEIN; SULFATASE 1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL SPECIFICITY; CHICKEN; DNA LIBRARY; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC CODE; GENETIC LINKAGE; GLIA CELL; INCUBATION TIME; MOLECULAR CLONING; NERVOUS SYSTEM DEVELOPMENT; NEUROEPITHELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PRIORITY JOURNAL; SPINAL CORD; STEM CELL; SUPPRESSION SUBTRACTIVE HYBRIDIZATION;

ANIMALS; BIOLOGICAL MARKERS; BODY PATTERNING; CELL DIFFERENTIATION; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; CHICK EMBRYO; DNA, COMPLEMENTARY; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENOMIC LIBRARY; NERVE TISSUE PROTEINS; NUCLEIC ACID HYBRIDIZATION; OLIGODENDROGLIA; STEM CELLS; SULFOTRANSFERASES;

EID: 11144354263     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2003.11.013     Document Type: Article

References (98)

1. Ai X., Do A.T., Lozynska O., Kusche-Gullberg M., Lindahl U., Emerson C.P. Jr. QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J. Cell Biol. 162:2003;341-351.
2. Angelotti T., Hofmann F. Tissue-specific expression of splice variants of the mouse voltage-gated calcium channel alpha2/delta subunit. FEBS Lett. 397:1996;331-337.
3. Bächner D., Ahrens M., Betat N., Schroder D., Gross G. Developmental expression analysis of murine autotaxin (ATX). Mech. Dev. 84:1999;121-125.
4. Bennett V., Chen L. Ankyrins and cellular targeting of diverse membrane proteins to physiological sites. Curr. Opin. Cell Biol. 13:2001;61-67.
5. Berezowsky C., Bag J. Slow troponin C is present in both muscle and nonmuscle cells. Biochem. Cell. Biol. 70:1992;691-697.
6. Bergsma D.J., Chang K.S., Schwartz R.J. Novel chicken actin gene: third cytoplasmic isoform. Mol. Cell. Biol. 5:1985;1151-1162.
7. Binart N., Chambraud B., Dumas B., Rowlands D.A., Bigogne C., Levin J.M., Garnier J., Baulieu E.E., Catelli M.G. The cDNA-derived amino acid sequence of chick heat shock protein Mr 90,000 (HSP 90) reveals a "DNA like" structure: potential site of interaction with steroid receptors. Biochem. Biophys. Res. Commun. 159:1989;140-147.
8. Blass-Kampmann S., Kindler-Rohrborn A., Deissler H., D'Urso D., Rajewsky M.F. In vitro differentiation of neural progenitor cells from prenatal rat brain: common cell surface glycoprotein on three glial cell subsets. J. Neurosci. Res. 48:1997;95-111.
9. Bollen M., Gijsbers R., Ceulemans H., Stalmans W., Stefan C. Nucleotide pyrophosphatases/phosphodiesterases on the move. Crit. Rev. Biochem. Mol. Biol. 35:2000;393-432.
10. Bowser R., Novick P. Sec15 protein, an essential component of the exocytotic apparatus, is associated with the plasma membrane and with a soluble 19.5S particle. J. Cell Biol. 112:1991;1117-1131.
11. Briscoe J., Pierani A., Jessell T.M., Ericson J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell. 101:2000;435-445.
12. Bucher K., Sofroniew M.V., Pannell R., Impey H., Smith A.J., Torres E.M., Dunnett S.B., Jin Y., Baer R., Rabbitts T.H. The T cell oncogene Tal2 is necessary for normal development of the mouse brain. Dev. Biol. 227:2000;533-544.
13. Carninci P., Hayashizaki Y. High-efficiency full-length cDNA cloning. Methods Enzymol. 303:1999;19-44.
14. Casado F.J., Pouponnot C., Jeanny J.C., Lecoq O., Calothy G., Pierani A. QRI, a retina-specific gene, encodes an extracellular matrix protein exclusively expressed during neural retina differentiation. Mech. Dev. 54:1996;237-250.
15. Cenciarelli C., Chiaur D.S., Guardavaccaro D., Parks W., Vidal M., Pagano M. Identification of a family of human F-box proteins. Curr. Biol. 9:1999;1177-1179.
16. Chan W., Kordeli E., Bennett V. 440-kD ankyrinB: structure of the major developmentally regulated domain and selective localization in unmyelinated axons. J. Cell Biol. 123:1993;1463-1473.
17. Christiansen J.H., Coles E.G., Robinson V., Pasini A., Wilkinson D.G. Screening from a subtracted embryonic chick hindbrain cDNA library: identification of genes expressed during hindbrain, midbrain and cranial neural crest development. Mech. Dev. 102:2001;119-133.
18. Deissler H., Blass-Kampmann S., Bruyneel E., Mareel M., Rajewsky M.F. Neural cell surface differentiation antigen gp130(RB13-6) induces fibroblasts and glioma cells to express astroglial proteins and invasive properties. FASEB J. 13:1999;657-666.
19. Dhoot G.K., Gustafsson M.K., Ai X., Sun W., Standiford D.M., Emerson C.P. Jr. Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science. 293:2001;1663-1666.
20. Diatchenko L., Lau Y.F., Campbell A.P., Chenchik A., Moqadam F., Huang B., Lukyanov S., Lukyanov K., Gurskaya N., Sverdlov E.D., Siebert P.D. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl. Acad. Sci. U. S. A. 93:1996;6025-6030.
21. Duan H., Wang Y., Aviram M., Swaroop M., Loo J.A., Bian J., Tian Y., Mueller T., Bisgaier C.L., Sun Y. SAG, a novel zinc RING finger protein that protects cells from apoptosis induced by redox agents. Mol. Cell. Biol. 19:1999;3145-3155.
22. Ericson J., Rashbass P., Schedl A., Brenner-Morton S., Kawakami A., van Heyningen V., Jessell T.M., Briscoe J. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell. 90:1997;169-180.
23. Farah C.S., Reinach F.C. The troponin complex and regulation of muscle contraction. FASEB J. 9:1995;755-767.
24. Feliciello A., Gottesman M.E., Avvedimento E.V. The biological functions of A-kinase anchor proteins. J. Mol. Biol. 308:2001;99-114.
25. Fu H., Qi Y., Tan M., Cai J., Takebayashi H., Nakafuku M., Richardson W., Qiu M. Dual origin of spinal oligodendrocyte progenitors and evidence for the cooperative role of Olig2 and Nkx2.2 in the control of oligodendrocyte differentiation. Development. 129:2002;681-693.
26. Garel S., Marin F., Mattei M.G., Vesque C., Vincent A., Charnay P. Family of Ebf/Olf-1-related genes potentially involved in neuronal differentiation and regional specification in the central nervous system. Dev. Dyn. 210:1997;191-205.
27. Gijsbers R., Ceulemans H., Stalmans W., Bollen M. Structural and catalytic similarities between nucleotide pyrophosphatases/phosphodiesterases and alkaline phosphatases. J. Biol. Chem. 276:2001;1361-1368.
28. Girard J.P., Baekkevold E.S., Amalric F. Sulfation in high endothelial venules: cloning and expression of the human PAPS synthetase. FASEB J. 12:1998;603-612.
29. Guermah M., Crisanti P., Laugier D., Dezelee P., Bidou L., Pessac B., Calothy G. Transcription of a quail gene expressed in embryonic retinal cells is shut off sharply at hatching. Proc. Natl. Acad. Sci. U. S. A. 88:1991;4503-4507.
30. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. 1951 (classical article). (see comments) Dev. Dyn. 195:1992;231-272.
31. Hausman R.E., Rao A.S., Ren Y., Sagar G.D., Shah B.H. Retina cognin, cell signaling, and neuronal differentiation in the developing retina. Dev. Dyn. 196:1993;263-266.
32. Hemler M.E. Specific tetraspanin functions. J. Cell Biol. 155:2001;1103-1107.
33. Hermann S., Saarikettu J., Onions J., Hughes K., Grundstrom T. Calcium regulation of basic helix-loop-helix transcription factors. Cell Calcium. 23:1998;135-142.
34. Holmes G., Niswander L. Expression of slit-2 and slit-3 during chick development. Dev. Dyn. 222:2001;301-307.
35. Ilyin G.P., Rialland M., Pigeon C., Guguen-Guillouzo C. cDNA cloning and expression analysis of new members of the mammalian F-box protein family. Genomics. 67:2000;40-47.
36. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev., Genet. 1:2000;20-29.
37. Kasof G.M., Goyal L., White E. Btf, a novel death-promoting transcriptional repressor that interacts with Bcl-2-related proteins. Mol. Cell. Biol. 19:1999;4390-4404.
38. Kattar-Cooley P.A., Wang H.H., Mende-Mueller L.M., Miziorko H.M. Avian liver 3-hydroxy-3-methylglutaryl-CoA synthase: distinct genes encode the cholesterogenic and ketogenic isozymes. Arch. Biochem. Biophys. 283:1990;523-529.
39. Kruse C., Willkomm D.K., Grunweller A., Vollbrandt T., Sommer S., Busch S., Pfeiffer T., Brinkmann J., Hartmann R.K., Muller P.K. Export and transport of tRNA are coupled to a multi-protein complex. Biochem. J. 346(Pt 1):2000;107-115.
40. Kunimoto M., Otto E., Bennett V. A new 440-kD isoform is the major ankyrin in neonatal rat brain. J. Cell Biol. 115:1991;1319-1331.
41. Kurosawa N., Hamamoto T., Lee Y.C., Nakaoka T., Kojima N., Tsuji S. Molecular cloning and expression of GalNAc alpha 2,6-sialyltransferase. J. Biol. Chem. 269:1994;1402-1409.
42. Lee J., Wu Y., Qi Y., Xue H., Liu Y., Scheel D., German M., Qiu M., Guillemot F., Rao M., Gradwohl G. Neurogenin3 participates in gliogenesis in the developing vertebrate spinal cord. Dev. Biol. 253:2003;84-98.
43. Li H., Deyrup A., Mensch J.R.Jr., Domowicz M., Konstantinidis A.K., Schwartz N.B. The isolation and characterization of cDNA encoding the mouse bifunctional ATP sulfurylase-adenosine 5′-phosphosulfate kinase. J. Biol. Chem. 270:1995;29453-29459.
44. Lu Q.R., Yuk D., Alberta J.A., Zhu Z., Pawlitzky I., Chan J., McMahon A.P., Stiles C.D., Rowitch D.H. Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron. 25:2000;317-329.
45. Miller R.H. Oligodendrocyte origins. Trends Neurosci. 19:1996;92-96.
46. Miyake A., Hattori Y., Ohta M., Itoh N. Rat oligodendrocytes and astrocytes preferentially express fibroblast growth factor receptor-2 and -3 mRNAs. J. Neurosci. Res. 45:1996;534-541.
47. Mizuguchi R., Sugimori M., Takebayashi H., Kosako H., Nagao M., Yoshida S., Nabeshima Y., Shimamura K., Nakafuku M. Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron. 31:2001;757-771.
48. Mori S., Sugawara S., Kikuchi T., Tanji M., Narumi O., Stoykova A., Nishikawa S.I., Yokota Y. The leukemic oncogene tal-2 is expressed in the developing mouse brain. Brain Res. Mol. Brain Res. 64:1999;199-210.
49. Morimoto-Tomita M., Uchimura K., Werb Z., Hemmerich S., Rosen S.D. Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J. Biol. Chem. 277:2002;49175-49185.
50. Muhr J., Andersson E., Persson M., Jessell T.M., Ericson J. Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube. Cell. 104:2001;861-873.
51. Nagase T., Kikuno R., Ishikawa K., Hirosawa M., Ohara O. Prediction of the coding sequences of unidentified human genes. XVII. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Res. 7:2000;143-150.
52. Nieto M.A., Patel K., Wilkinson D.G. In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol. 51:1996;219-235.
53. Nishiyama H., Gill J.H., Pitt E., Kennedy W., Knowles M.A. Negative regulation of G(1)/S transition by the candidate bladder tumour suppressor gene DBCCR1. Oncogene. 20:2001;2956-2964.
54. Novitch B.G., Chen A.I., Jessell T.M. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron. 31:2001;773-789.
55. Nybakken K., Perrimon N. Hedgehog signal transduction: recent findings. Curr. Opin. Genet. Dev. 12:2002;503-511.
56. Ohto T., Uchida H., Yamazaki H., Keino-Masu K., Matsui A., Masu M. Identification of a novel nonlysosomal sulphatase expressed in the floor plate, choroid plexus and cartilage. Genes Cells. 7:2002;173-185.
57. Ono K., Bansal R., Payne J., Rutishauser U., Miller R.H. Early development and dispersal of oligodendrocyte precursors in the embryonic chick spinal cord. Development. 121:1995;1743-1754.
58. Orentas D.M., Hayes J.E., Dyer K.L., Miller R.H. Sonic hedgehog signaling is required during the appearance of spinal cord oligodendrocyte precursors. Development. 126:1999;2419-2429.
59. Otto E., Kunimoto M., McLaughlin T., Bennett V. Isolation and characterization of cDNAs encoding human brain ankyrins reveal a family of alternatively spliced genes. J. Cell Biol. 114:1991;241-253.
60. Parkkonen T., Kivirikko K.I., Pihlajaniemi T. Molecular cloning of a multifunctional chicken protein acting as the prolyl 4-hydroxylase beta-subunit, protein disulphide-isomerase and a cellular thyroid-hormone-binding protein. Comparison of cDNA-deduced amino acid sequences with those in other species. Biochem. J. 256:1988;1005-1011.
61. Pestonjamasp K.N., Pope R.K., Wulfkuhle J.D., Luna E.J. Supervillin (p205): a novel membrane-associated, F-actin-binding protein in the villin/gelsolin superfamily. J. Cell Biol. 139:1997;1255-1269.
62. Peters K., Ornitz D., Werner S., Williams L. Unique expression pattern of the FGF receptor 3 gene during mouse organogenesis. Dev. Biol. 155:1993;423-430.
63. Poncet C., Soula C., Trousse F., Kan P., Hirsinger E., Pourquie O., Duprat A.M., Cochard P. Induction of oligodendrocyte progenitors in the trunk neural tube by ventralizing signals: effects of notochord and floor plate grafts, and of sonic hedgehog. Mech. Dev. 60:1996;13-32.
64. Pope R.K., Pestonjamasp K.N., Smith K.P., Wulfkuhle J.D., Strassel C.P., Lawrence J.B., Luna E.J. Cloning, characterization, and chromosomal localization of human superillin (SVIL). Genomics. 52:1998;342-351.
65. Pringle N.P., Richardson W.D. A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development. 117:1993;525-533.
66. Pringle N.P., Yu W.P., Guthrie S., Roelink H., Lumsden A., Peterson A.C., Richardson W.D. Determination of neuroepithelial cell fate: induction of the oligodendrocyte lineage by ventral midline cells and sonic hedgehog. Dev. Biol. 177:1996;30-42.
67. Pringle N.P., Guthrie S., Lumsden A., Richardson W.D. Dorsal spinal cord neuroepithelium generates astrocytes but not oligodendrocytes. Neuron. 20:1998;883-893.
68. Pringle N.P., Yu W.P., Howell M., Colvin J.S., Ornitz D.M., Richardson W.D. Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development. 130:2003;93-102.
69. Puls K.L., Wright M.D. The molecular characterisation of mouse tspan-3. DNA Seq. 11:2000;271-275.
70. Rao M.S., Mayer-Proschel M. Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev. Biol. 188:1997;48-63.
71. Rao M.S., Noble M., Mayer-Proschel M. A tripotential glial precursor cell is present in the developing spinal cord. Proc. Natl. Acad. Sci. U. S. A. 95:1998;3996-4001.
72. Rapraeger A.C. Heparan sulfate-growth factor interactions. Methods Cell Biol. 69:2002;83-109.
73. Rubtsov A.M., Lopina O.D. Ankyrins. FEBS Lett. 482:2000;1-5.
74. Sato R., Takano T. Regulation of intracellular cholesterol metabolism. Cell Struct. Funct. 20:1995;421-427.
75. Schauer R., Sommer U., Kruger D., van Unen H., Traving C. The terminal enzymes of sialic acid metabolism: acylneuraminate pyruvate-lyases. Biosci. Rep. 19:1999;373-383.
76. Schmidt C., Henkel B., Poschl E., Zorbas H., Purschke W.G., Gloe T.R., Muller P.K. Complete cDNA sequence of chicken vigilin, a novel protein with amplified and evolutionary conserved domains. Eur. J. Biochem. 206:1992;625-634.
77. Scott H.S., Antonarakis S.E., Lalioti M.D., Rossier C., Silver P.A., Henry M.F. Identification and characterization of two putative human arginine methyltransferases (HRMT1L1 and HRMT1L2). Genomics. 48:1998;330-340.
78. Shimizu K., Kawabe H., Minami S., Honda T., Takaishi K., Shirataki H., Takai Y. SMAP, an Smg GDS-associating protein having arm repeats and phosphorylated by Src tyrosine kinase. J. Biol. Chem. 271:1996;27013-27017.
79. Son M.Y., Park J.W., Kim Y.S., Kang S.W., Marshak D.R., Park W., Bae Y.S. Protein kinase CKII interacts with and phosphorylates the SAG protein containing ring-H2 finger motif. Biochem. Biophys. Res. Commun. 263:1999;743-748.
80. Soula C., Danesin C., Kan P., Grob M., Poncet C., Cochard P. Distinct sites of origin of oligodendrocytes and somatic motoneurons in the chick spinal cord: oligodendrocytes arise from Nkx2.2-expressing progenitors by a Shh-dependent mechanism. Development. 128:2001;1369-1379.
81. Spassky N., Goujet-Zalc C., Parmantier E., Olivier C., Martinez S., Ivanova A., Ikenaka K., Macklin W., Cerruti I., Zalc B., Thomas J.L. Multiple restricted origin of oligodendrocytes. J. Neurosci. 18:1998;8331-8343.
82. Strausberg R.L., Feingold E.A., Grouse L.H., Derge J.G., Klausner R.D., Collins F.S., Wagner L., Shenmen C.M., Schuler G.D., Altschul S.F., Zeeberg B., Buetow K.H., Schaefer C.F., Bhat N.K., Hopkins R.F., Jordan H., Moore T., Max S.I., Wang J., Hsieh F., Diatchenko L., Marusina K., Farmer A.A., Rubin G.M., Hong L., Stapleton M., Soares M.B., Bonaldo M.F., Casavant T.L., Scheetz T.E., Brownstein M.J., Usdin T.B., Toshiyuki S., Carninci P., Prange C., Raha S.S., Loquellano N.A., Peters G.J., Abramson R.D., Mullahy S.J., Bosak S.A., McEwan P.J., McKernan K.J., Malek J.A., Gunaratne P.H., Richards S., Worley K.C., Hale S., Garcia A.M., Gay L.J., Hulyk S.W., Villalon D.K., Muzny D.M., Sodergren E.J., Lu X., Gibbs R.A., Fahey J., Helton E., Ketteman M., Madan A., Rodrigues S., Sanchez A., Whiting M., Young A.C., Shevchenko Y., Bouffard G.G., Blakesley R.W., Touchman J.W., Green E.D., Dickson M.C., Rodriguez A.C., Grimwood J., Schmutz J., Myers R.M., Butterfield Y.S., Krzywinski M.I., Skalska U., Smailus D.E., Schnerch A., Schein J.E., Jones S.J., Marra M.A. Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc. Natl. Acad. Sci. U. S. A. 99:2002;16899-16903.
83. Timsit S., Martinez S., Allinquant B., Peyron F., Puelles L., Zalc B. Oligodendrocytes originate in a restricted zone of the embryonic ventral neural tube defined by DM-20 mRNA expression. J. Neurosci. 15:1995;1012-1024.
84. Todd S.C., Doctor V.S., Levy S. Sequences and expression of six new members of the tetraspanin/TM4SF family. Biochim. Biophys. Acta. 1399:1998;101-104.
85. Traving C., Schauer R. Structure, function and metabolism of sialic acids. Cell. Mol. Life Sci. 54:1998;1330-1349.
86. Trousse F., Giess M.C., Soula C., Ghandour S., Duprat A.M., Cochard P. Notochord and floor plate stimulate oligodendrocyte differentiation in cultures of the chick dorsal neural tube. J. Neurosci. Res. 41:1995;552-560.
87. Tse W.T., Menninger J.C., Yang-Feng T.L., Francke U., Sahr K.E., Lux S.E., Ward D.C., Forget B.G. Isolation and chromosomal localization of a novel nonerythroid ankyrin gene. Genomics. 10:1991;858-866.
88. Vargesson N., Luria V., Messina I., Erskine L., Laufer E. Expression patterns of Slit and Robo family members during vertebrate limb development. Mech. Dev. 106:2001;175-180.
89. Wada K., Inoue K., Hagiwara M. Identification of methylated proteins by protein arginine N-methyltransferase 1, PRMT1, with a new expression cloning strategy. Biochim. Biophys. Acta. 1591:2002;1-10.
90. Wang S.S., Tsai R.Y., Reed R.R. The characterization of the Olf-1/EBF-like HLH transcription factor family: implications in olfactory gene regulation and neuronal development. J. Neurosci. 17:1997;4149-4158.
91. Wang W., Chi T., Xue Y., Zhou S., Kuo A., Crabtree G.R. Architectural DNA binding by a high-mobility-group/kinesin-like subunit in mammalian SWI/SNF-related complexes. Proc. Natl. Acad. Sci. U. S. A. 95:1998;492-498.
92. Warf B.C., Fok-Seang J., Miller R.H. Evidence for the ventral origin of oligodendrocyte precursors in the rat spinal cord. J. Neurosci. 11:1991;2477-2488.
93. Wulfkuhle J.D., Donina I.E., Stark N.H., Pope R.K., Pestonjamasp K.N., Niswonger M.L., Luna E.J. Domain analysis of supervillin, an F-actin bundling plasma membrane protein with functional nuclear localization signals. J. Cell. Sci. 112(Pt 13):1999;2125-2136.
94. Xu X., Cai J., Fu H., Wu R., Qi Y., Modderman G., Liu R., Qiu M. Selective expression of Nkx-2.2 transcription factor in chicken oligodendrocyte progenitors and implications for the embryonic origin of oligodendrocytes. Mol. Cell. Neurosci. 16:2000;740-753.
95. Xu X.M., Fisher D.A., Zhou L., White F.A., Ng S., Snider W.D., Luo Y. The transmembrane protein semaphorin 6A repels embryonic sympathetic axons. J. Neurosci. 20:2000;2638-2648.
96. Yu W.P., Collarini E.J., Pringle N.P., Richardson W.D. Embryonic expression of myelin genes: evidence for a focal source of oligodendrocyte precursors in the ventricular zone of the neural tube. Neuron. 12:1994;1353-1362.
97. Zhou L., White F.A., Lentz S.I., Wright D.E., Fisher D.A., Snider W.D. Cloning and expression of a novel murine semaphorin with structural similarity to insect semaphorin I. Mol. Cell. Neurosci. 9:1997;26-41.
98. Zhou Q., Wang S., Anderson D.J. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron. 25:2000;331-343.