Expression by midbrain dopamine neurons of Sema3A and 3F receptors is associated with chemorepulsion in vitro but a mild in vivo phenotype

Molecular and Cellular Neuroscience

Volumn 44, Issue 2, 2010, Pages 135-153

  Torre, Enrique R ^a   Gutekunst, Claire Anne ^a   Gross, Robert E ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE L1; NEUROPILIN 1; NEUROPILIN 2; PLEXIN; PLEXIN A1; PLEXIN A3; PLEXIN A4; SEMAPHORIN 3A; SEMAPHORIN 3F; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CATECHOLAMINE NERVE CELL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYO; GROWTH CONE; HABENULA; IN VITRO STUDY; IN VIVO STUDY; LOCOMOTION; MESENCEPHALON; NERVE GROWTH; NEWBORN; NONHUMAN; PHENOTYPE; PLACE PREFERENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT; SYNAPSE; TELENCEPHALON; THALAMUS MIDLINE NUCLEUS;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CHEMOTAXIS; DIENCEPHALON; DOPAMINE; FEMALE; GROWTH CONES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MESENCEPHALON; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; NEURONS; RATS; RATS, WISTAR; SEMAPHORIN-3A; TELENCEPHALON;

MUS; RATTUS;

EID: 77952541715     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.03.003     Document Type: Article

References (126)

1. Anon Troublesome variability in mouse studies. Nat. Neurosci. 2009, 12:1075.
2. Adams R.H., Lohrum M., Klostermann A., Betz H., Puschel A.W. The chemorepulsive activity of secreted semaphorins is regulated by furin-dependent proteolytic processing. EMBO J. 1997, 16:6077-6086.
3. Altman J., Bayer S.A. Development of the brain stem in the rat: V. Thymidine-radiographic study of the time of origin of neurons in the midbrain tegmentum. J. Comp. Neurol. 1981, 198:677-716.
4. Bachelder R.E., Lipscomb E.A., Lin X., Wendt M.A., Chadborn N.H., Eickholt B.J., Mercurio A.M. Competing autocrine pathways involving alternative neuropilin-1 ligands regulate chemotaxis of carcinoma cells. Cancer Res. 2003, 63:5230-5233.
5. Bagri A., Tessier-Lavigne M. Neuropilins as Semaphorin receptors: in vivo functions in neuronal cell migration and axon guidance. Adv. Exp. Med. Biol. 2002, 515:13-31.
6. Bagri A., Marin O., Plump A.S., Mak J., Pleasure S.J., Rubenstein J.L.R., Tessier-Lavigne M. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 2002, 33:233-248.
7. Bals-Kubik R., Ableitner A., Herz A., Shippenberg T.S. Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats. J. Pharmacol. Exp. Ther. 1993, 264:489-495.
8. Barnes G., Puranam R.S., Luo Y., McNamara J.O. Temporal specific patterns of semaphorin gene expression in rat brain after kainic acid-induced status epilepticus. Hippocampus 2003, 13:1-20.
9. Barzilai A., Zilkha-Falb R., Daily D., Stern N., Offen D., Ziv I., Melamed E., Shirvan A. The molecular mechanism of dopamine-induced apoptosis: identification and characterization of genes that mediate dopamine toxicity. J. Neural. Transm. Suppl. 2000, 59-76.
10. Bayer S.A., Triarhou L.C., Thomas J.D., Ghetti B. Correlated quantitative studies of the neostriatum, nucleus accumbens, substantia nigra, and ventral tegmental area in normal and weaver mutant mice. J. Neurosci. 1994, 14:6901-6910.
11. Bayer S.A., Wills K.V., Triarhou L.C., Ghetti B. Time of neuron origin and gradients of neurogenesis in midbrain dopaminergic neurons in the mouse. Exp. Brain Res. 1995, 105:191-199.
12. Belanger M., Auclair F., Bertrand L., Marchand R. The early neuronal organization predicts the path followed by some major axonal bundles in the embryonic brainstem. Neuroscience 1997, 78:259-270.
13. Benson D.L., Colman D.R., Huntley G.W. Molecules, maps and synapse specificity. Nat. Rev. Neurosci. 2001, 2.
14. Betarbet R., Sherer T.B., Greenamyre J.T. Ubiquitin-proteasome system and Parkinson's diseases. Exp. Neurol. 2005, 191:S17-S27.
15. Brose K., Bland K.S., Wang K.H., Arnott D., Henzel W., Goodman C.S., Tessier-Lavigne M., Kidd T. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 1999, 96:795-806.
16. Castellani V. The function of neuropilin/L1 complex. Adv. Exp. Med. Biol. 2002, 515:91-102.
17. Castellani V., Chedotal A., Schachner M., Faivre-Sarrailh C., Rougon G. Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron 2000, 27:237-249.
18. Castellani V., De Angelis E., Kenwrick S., Rougon G. Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO J. 2002, 21:6348-6357.
19. Catalano S.M., Messersmith E.K., Goodman C.S., Shatz C.J., Chedotal A. Many major CNS axon projections develop normally in the absence of semaphorin III. Mol. Cell. Neurosci. 1998, 11:173-182.
20. Catalano A., Caprari P., Rodilossi S., Betta P., Castellucci M., Casazza A., Tamagnone L., Procopio A. Cross-talk between vascular endothelial growth factor and semaphorin-3A pathway in the regulation of normal and malignant mesothelial cell proliferation. FASEB J. 2004, 18:358-360.
21. Chen H., Chedotal A., He Z., Goodman C.S., Tessier-Lavigne M. Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 1997, 19:547-559.
22. Chen H., He Z., Bagri A., Tessier-Lavigne M. Semaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins. Neuron 1998, 21:1283-1290.
23. Chen H., He Z., Tessier-Lavigne M. Axon guidance mechanisms: semaphorins as simultaneous repellents and anti-repellents. Nat. Neurosci. 1998, 1:436-439.
24. Chen H., Bagri A., Zupicich J.A., Zou Y., Stoeckli E., Pleasure S.J., Lowenstein D.H., Skarnes W.C., Chedotal A., Tessier-Lavigne M. Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 2000, 25:43-56.
25. Chen G., Sima J., Jin M., Wang K.Y., Xue X.J., Zheng W., Ding Y.Q., Yuan X.B. Semaphorin-3A guides radial migration of cortical neurons during development. Nat. Neurosci. 2008, 11:36-44.
26. Cheng H.J., Bagri A., Yaron A., Stein E., Pleasure S.J., Tessier-Lavigne M. Plexin-A3 mediates semaphorin signaling and regulates the development of hippocampal axonal projections. Neuron 2001, 32:249-263.
27. Cloutier J.F., Giger R.J., Koentges G., Dulac C., Kolodkin A.L., Ginty D.D. Neuropilin-2 mediates axonal fasciculation, zonal segregation, but not axonal convergence, of primary accessory olfactory neurons. Neuron 2002, 33:877-892.
28. Dahlstrand J., Lardelli M., Lendahl U. Nestin mRNA expression correlates with the central nervous system progenitor cell state in many, but not all, regions of developing central nervous system. Brain Res. Dev. Brain Res. 1995, 84:109-129.
29. Demyanenko G., Shibata Y., Maness P. Altered distribution of dopaminergic neurons in the brain of L1 null mice. Brain Res. Dev. Brain Res. 2001, 126:21.
30. Deo R.C., Schmidt E.F., Elhabazi A., Togashi H., Burley S.K., Strittmatter S.M. Structural bases for CRMP function in plexin-dependent semaphorin3A signaling. EMBO J. 2004, 23:9-22.
31. Di Monte D.A. The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins?. Lancet Neurol. 2003, 2:531-538.
32. Dontchev V.D., Letourneau P.C. Nerve growth factor and semaphorin 3A signaling pathways interact in regulating sensory neuronal growth cone motility. J. Neurosci. 2002, 22:6659-6669.
33. Eickholt B.J., Mackenzie S.L., Graham A., Walsh F.S., Doherty P. Evidence for collapsin-1 functioning in the control of neural crest migration in both trunk and hindbrain regions. Development (Cambridge, England) 1999, 126:2181-2189.
34. Falk J., Bechara A., Fiore R., Nawabi H., Zhou H., Hoyo-Becerra C., Bozon M., Rougon G., Grumet M., Puschel A.W., Sanes J.R., Castellani V. Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 2005, 48:63-75.
35. Flores C., Manitt C., Rodaros D., Thompson K.M., Rajabi H., Luk K.C., Tritsch N.X., Sadikot A.F., Stewart J., Kennedy T.E. Netrin receptor deficient mice exhibit functional reorganization of dopaminergic systems and do not sensitize to amphetamine. Mol. Psychiatry 2005, 10:606-612.
36. Fu S.Y., Sharma K., Luo Y., Raper J.A., Frank E. SEMA3A regulates developing sensory projections in the chicken spinal cord. J. Neurobiol. 2000, 45:227-236.
37. Funato H., Saito-Nakazato Y., Takahashi H. Axonal growth from the habenular nucleus along the neuromere boundary region of the diencephalon is regulated by semaphorin 3F and netrin-1. Mol. Cell. Neurosci. 2000, 16:206-220.
38. Garcez P.P., Henrique N.P., Furtado D.A., Bolz J., Lent R., Uziel D. Axons of callosal neurons bifurcate transiently at the white matter before consolidating an interhemispheric projection. Eur. J. NeuroSci. 2007, 25:1384-1394.
39. Gates M.A., Coupe V.M., Torres E.M., Fricker-Gates R.A., Dunnet S.B. Spatially and tewmporally restricted chemoattractive and chemorepulsice cues direct the formation of the nigro-straiatal system circuit. Eur. J. NeuroSci. 2004, 19:831-844.
40. Gelman D.M., Noain D., Avale M.E., Otero V., Low M.J., Rubinstein M. Transgenic mice engineered to target Cre/loxP-mediated DNA recombination into catecholaminergic neurons. Genesis 2003, 36:196-202.
41. Gerlai R. Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype?. Trends Neurosci. 1996, 19:177-181.
42. Giger R.J., Cloutier J.F., Sahay A., Prinjha R.K., Levengood D.V., Moore S.E., Pickering S., Simmons D., Rastan S., Walsh F.S., Kolodkin A.L., Ginty D.D., Geppert M. Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 2000, 25:29-41.
43. Gong S., Doughty M., Harbaugh C.R., Cummins A., Hatten M.E., Heintz N., Gerfen C.R. Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J. Neurosci. 2007, 27:9817-9823.
44. Goshima Y., Sasaki Y., Nakayama T., Ito T., Kimura T. Functions of semaphorins in axon guidance and neuronal regeneration. Jpn. J. Pharmacol. 2000, 82:273-279.
45. Goshima Y., Ito T., Sasaki Y., Nakamura F. Semaphorins as signals for cell repulsion and invasion. J. Clin. Invest 2002, 109:993-998.
46. Gruber C., Kahl A., Lebenheim L., Kowski A., Dittgen A., Veh R.W. Dopaminergic projections from the VTA substantially contribute to the mesohabenular pathway in the rat. Neurosci. Lett. 2007, 427:165-170.
47. Gu C., Rodriguez E.R., Reimert D.V., Shu T., Fritzsch B., Richards L.J., Kolodkin A.L., Ginty D.D. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev. Cell. 2003, 5:45-57.
48. Haber S.N. The primate basal ganglia: parallel and integrative networks. J. Chem. Neuroanat. 2003, 26:317-330.
49. Hague S.M., Klaffke S., Bandmann O. Neurodegenerative disorders: Parkinson's disease and Huntington's disease. J. Neurol. Neurosurg. Psychiatry 2005, 76:1058-1063.
50. Henion T.R., Schwarting G.A. Patterning the developing and regenerating olfactory system. J. Cell Physiol. 2007, 210:290-297.
51. Hernandez-Montiel H.L., Tamariz E., Sandoval-Minero M.T., Varela-Echavarria A. Semaphorins 3A, 3C, and 3F in mesencephalic dopaminergic axon pathfinding. J. Comp. Neurol. 2008, 506:387-397.
52. Horinouchi K., Nakamura Y., Yamanaka H., Watabe T., Shiosaka S. Distribution of L1cam mRNA in the adult mouse brain: in situ hybridization and Northern blot analyses. J. Comp. Neurol. 2005, 482:386-404.
53. Huber A.B., Kolodkin A.L., Ginty D.D., Cloutier J.F. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Ann. Rev. Neurosci. 2003, 26:509-563.
54. Hulley P., Schachner M., Lubbert H. L1 neural cell adhesion molecule is a survival factor for fetal dopaminergic neurons. J. Neurosci. Res. 1998, 53:129-134.
55. Imai T., Yamazaki T., Kobayakawa R., Kobayakawa K., Abe T., Suzuki M., Sakano H. Pre-target axon sorting establishes the neural map topography. Science 2009, 325:585-590.
56. Joel D., Weiner I. The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum. Neuroscience 2000, 96:451-474.
57. Kawano H., Ohyama K., Kawamura K., Nagatsu I. Migration of dopaminergic neurons in the embryonic mesencephalon of mice. Brain Res. Dev. Brain Res. 1995, 86:101-113.
58. Kawano H., Horie M., Honma S., Kawamura K., Takeuchi K., Kimura S. Aberrant trajectory of ascending dopaminergic pathway in mice lacking Nkx2.1. Exp. Neurol. 2003, 182:103-112.
59. Kawasaki T., Kitsukawa T., Bekku Y., Matsuda Y., Sanbo M., Yagi T., Fujisawa H. A requirement for neuropilin-1 in embryonic vessel formation. Development (Cambridge, England) 1999, 126:4895-4902.
60. Winberg M.L., Mitchell K.J., Goodman C.S. Genetic analysis of the mechanisms controlling target selection: complementary and combinatorial functions of netrins, semaphorins, and IgCAMs. Cell 1998, 93:581-591.
61. Kawasaki T., Bekku Y., Suto F., Kitsukawa T., Taniguchi M., Nagatsu I., Nagatsu T., Itoh K., Yagi T., Fujisawa H. Requirement of neuropilin 1-mediated Sema3A signals in patterning of the sympathetic nervous system. Development (Cambridge, England) 2002, 129:671-680.
62. Kitsukawa T., Shimizu M., Sanbo M., Hirata T., Taniguchi M., Bekku Y., Yagi T., Fujisawa H. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 1997, 19:995-1005.
63. Knoll B., Drescher U. Ephrin-As as receptors in topographic projections. Trends Neurosci. 2002, 25:145-149.
64. Kolk S.M., Gunput R.A., Tran T.S., van den Heuvel D.M., Prasad A.A., Hellemons A.J., Adolfs Y., Ginty D.D., Kolodkin A.L., Burbach J.P., Smidt M.P., Pasterkamp R.J. Semaphorin 3F is a bifunctional guidance cue for dopaminergic axons and controls their fasciculation, channeling, rostral growth, and intracortical targeting. J. Neurosci. 2009, 29:12542-12557.
65. Kurschat P., Bielenberg D., Rossignol-Tallandier M., Stahl A., Klagsbrun M. Neuron restrictive silencer factor NRSF/REST is a transcriptional repressor of neuropilin-1 and diminishes the ability of semaphorin 3A to inhibit keratinocyte migration. J. Biol. Chem. 2006, 281(5):2721-2729.
66. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., Chen L., Chen T.M., Chin M.C., Chong J., Crook B.E., Czaplinska A., Dang C.N., Datta S., Dee N.R., Desaki A.L., Desta T., Diep E., Dolbeare T.A., Donelan M.J., Dong H.W., Dougherty J.G., Duncan B.J., Ebbert A.J., Eichele G., Estin L.K., Faber C., Facer B.A., Fields R., Fischer S.R., Fliss T.P., Frensley C., Gates S.N., Glattfelder K.J., Halverson K.R., Hart M.R., Hohmann J.G., Howell M.P., Jeung D.P., Johnson R.A., Karr P.T., Kawal R., Kidney J.M., Knapik R.H., Kuan C.L., Lake J.H., Laramee A.R., Larsen K.D., Lau C., Lemon T.A., Liang A.J., Liu Y., Luong L.T., Michaels J., Morgan J.J., Morgan R.J., Mortrud M.T., Mosqueda N.F., Ng L.L., Ng R., Orta G.J., Overly C.C., Pak T.H., Parry S.E., Pathak S.D., Pearson O.C., Puchalski R.B., Riley Z.L., Rockett H.R., Rowland S.A., Royall J.J., Ruiz M.J., Sarno N.R., Schaffnit K., Shapovalova N.V., Sivisay T., Slaughterbeck C.R., Smith S.C., Smith K.A., Smith B.I., Sodt A.J., Stewart N.N., Stumpf K.R., Sunkin S.M., Sutram M., Tam A., Teemer C.D., Thaller C., Thompson C.L., Varnam L.R., Visel A., Whitlock R.M., Wohnoutka P.E., Wolkey C.K., Wong V.Y., Wood M., Yaylaoglu M.B., Young R.C., Youngstrom B.L., Yuan X.F., Zhang B., Zwingman T.A., Jones A.R. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
67. Leonardo E.D., Hinck L., Masu M., Keino-Masu K., Fazeli A., Stoeckli E.T., Ackerman S.L., Weinberg R.A., Tessier-Lavigne M. Guidance of developing axons by netrin-1 and its receptors. Cold Spring Harb. Symp. Quant. Biol. 1997, 62:467-478.
68. Lim K.L., Lim T.M. Molecular mechanisms of neurodegeneration in Parkinson's disease: clues from Mendelian syndromes. IUBMB Life 2003, 55:315-322.
69. Lin L., Isacson O. Axonal growth regulation of fetal and embryonic stem cell-derived dopaminergic neurons by Netrin-1 and Slits. Stem. Cells 2006, 24:2504-2513.
70. Lin L., Rao Y., Isacson O. Netrin-1 and slit-2 regulate and direct neurite growth of ventral midbrain dopaminergic neurons. Mol. Cell. Neurosci. 2005, 28:547-555.
71. Lindwall C., Fothergill T., Richards L.J. Commissure formation in the mammalian forebrain. Curr. Opin. Neurobiol. 2007, 17:3-14.
72. MacLennan A.J., McLaurin D.L., Marks L., Vinson E.N., Pfeifer M., Szulc S.V., Heaton M.B., Lee N. Immunohistochemical localization of netrin-1 in the embryonic chick nervous system. J. Neurosci. 1997, 17:5466-5479.
73. Marillat V., Cases O., Nguyen-Ba-Charvet K.T., Tessier-Lavigne M., Sotelo C., Chedotal A. Spatiotemporal expression patterns of slit and robo genes in the rat brain. J. Comp. Neurol. 2002, 442:130-155.
74. Mastick G.S., Easter S.S. Initial organization of neurons and tracts in the embryonic mouse fore- and midbrain. Dev. Biol. 1996, 173:79-94.
75. Masuda T., Tsuji H., Taniguchi M., Yagi T., Tessier-Lavigne M., Fujisawa H., Okado N., Shiga T. Differential non-target-derived repulsive signals play a critical role in shaping initial axonal growth of dorsal root ganglion neurons. Dev. Biol. 2003, 254:289-302.
76. Melendez-Herrera E., Varela-Echavarria A. Expression of secreted semaphorins and their receptors in specific neuromeres, boundaries, and neuronal groups in the developing mouse and chick brain. Brain Res. 2006, 1067:126-137.
77. Metin C., Deleglise D., Serafini T., Kennedy T.E., Tessier-Lavigne M. A role for netrin-1 in the guidance of cortical efferents. Development 1997, 124:5063-5074.
78. Mitsui N., Inatome R., Takahashi S., Goshima Y., Yamamura H., Yanagi S. Involvement of Fes/Fps tyrosine kinase in semaphorin3A signaling. EMBO J. 2002, 21:3274-3285.
79. Moore D.J., West A.B., Dawson V.L., Dawson T.M. Molecular pathophysiology of Parkinson's disease. Annu. Rev. Neurosci. 2005, 28:57-87.
80. Munakata H., Nakamura Y., Matsumoto-Miyai K., Itoh K., Yamasaki H., Shiosaka S. Distribution and densitometry mapping of L1-CAM immunoreactivity in the adult mouse brain-light microscopic observation. BMC Neurosci. 2003, 4:7.
81. Nakamura F., Kalb R.G., Strittmatter S.M. Molecular basis of semaphorin-mediated axon guidance. J. Neurobiol. 2000, 44:219-229.
82. Nakamura S., Ito Y., Shirasaki R., Murakami F. Local directional cues control growth polarity of dopaminergic axons along the rostrocaudal axis. J. Neurosci. 2000, 20:4112-4119.
83. Nasarre P., Constantin B., Rouhaud L., Harnois T., Raymond G., Drabkin H.A., Bourmeyster N., Roche J. Semaphorin SEMA3F and VEGF have opposing effects on cell attachment and spreading. Neoplasia 2003, 5:83-92.
84. Niclou S.P., Jia L., Raper J.A. Slit2 is a repellent for retinal ganglion cell axons. J. Neurosci. 2000, 20:4962-4974.
85. Ohyama K., Kawano H., Asou H., Fukuda T., Oohira A., Uyemura K.K.K. Coordinate expression of L1 and 6B4 proteoglycan/phosphacan is correlated with the migration of mesencephalic dopaminergic neurons in mice. Brain Res. Dev. Brain Res. 1998, 107:219.
86. Osborne N.J., Begbie J., Chilton J.K., Schmidt H., Eickholt B.J. Semaphorin/neuropilin signaling influences the positioning of migratory neural crest cells within the hindbrain region of the chick. Dev. Dyn. 2005, 232:939-949.
87. Osborne P.B., Halliday G.M., Cooper H.M., Keast J.R. Localization of immunoreactivity for deleted in colorectal cancer (DCC), the receptor for the guidance factor netrin-1, in ventral tier dopamine projection pathways in adult rodents. Neuroscience 2005, 131:671-681.
88. Park D., Xiang A.P., Zhang L., Mao F.F., Walton N.M., Choi S.S., Lahn B.T. The radial glia antibody RC2 recognizes a protein encoded by Nestin. Biochem. Biophys. Res. Commun. 2009, 382:588-592.
89. Perrone-Capano C., Di Porzio U. Genetic and epigenetic control of midbrain dopaminergic neuron development. Int. J. Dev. Biol. 2000, 44:679-687.
90. Phillips T.J., Hen R., Crabbe J.C. Complications associated with genetic background effects in research using knockout mice. Psychopharmacology (Berl) 1999, 147:5-7.
91. Phillipson O., Griffith A. The neurones of origin for the mesohabenular dopamine pathway. Brain Res. 1980, 197:213-218.
92. Potiron V.A., Sharma G., Nasarre P., Clarhaut J.A., Augustin H.G., Gemmill R.M., Roche J., Drabkin H.A. Semaphorin SEMA3F affects multiple signaling pathways in lung cancer cells. Cancer Res. 2007, 67:8708-8715.
93. Price D.J., Kennedy H., Dehay C., Zhou L., Mercier M., Jossin Y., Goffinet A.M., Tissir F., Blakey D., Molnar Z. The development of cortical connections. Eur. J. NeuroSci. 2006, 23:910-920.
94. Puschel A.W., Adams R.H., Betz H. Murine semaphorin D/collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension. Neuron 1995, 14:941-948.
95. Recio-Pinto E., Rechler M.M., Ishii D.N. Effects of insulin, insulin-like growth factor-II, and nerve growth factor on neurite formation and survival in cultured sympathetic and sensory neurons. J. Neurosci. 1986, 6:1211-1219.
96. Rohm B., Ottemeyer A., Lohrum M., Puschel A.W. Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A. Mech. Dev. 2000, 93:95-104.
97. Rohm B., Rahim B., Kleiber B., Hovatta I., Puschel A.W. The semaphorin 3A receptor may directly regulate the activity of small GTPases. FEBS Lett. 2000, 486:68-72.
98. Sahay A., Molliver M.E., Ginty D.D., Kolodkin A.L. Semaphorin 3F is critical for development of limbic system circuitry and is required in neurons for selective CNS axon guidance events. J. Neurosci. 2003, 23:6671-6680.
99. Scarlato M., Ara J., Bannerman P., Scherer S., Pleasure D. Induction of neuropilins-1 and -2 and their ligands, Sema3A, Sema3F, and VEGF, during Wallerian degeneration in the peripheral nervous system. Exp. Neurol. 2003, 183:489-498.
100. Schambra U.B., Silver J., Lauder J.M. An atlas of the prenatal mouse brain: gestational day 14. Exp. Neurol. 1991, 114:145-183.
101. Schlumpf M., Shoemaker W.J., Bloom F.E. Explant cultures of catecholamine-containing neurons from rat brain: biochemical, histofluorescence, and electron microscopic studies. Proc. Natl. Acad. Sci. U. S. A. 1977, 74:4471-4475.
102. Shimizu A., Mammoto A., Italiano J.E., Pravda E., Dudley A.C., Ingber D.E., Klagsbrun M. ABL2/ARG tyrosine kinase mediates SEMA3F-induced RhoA inactivation and cytoskeleton collapse in human glioma cells. J. Biol. Chem. 2008, 283:27230-27238.
103. Shirasaki R., Mirzayan C., Tessier-Lavigne M., Murakami F. Guidance of circumferentially growing axons by netrin-dependent and -independent floor plate chemotropism in the vertebrate brain. Neuron 1996, 17:1079-1088.
104. Shults C., Hashimoto R., Brady R., Gage F. Dopaminergic cells align along radial glia in the developing mesencephalon of the rat. Neuroscience 1990, 38:427-436.
105. Skagerberg G., Lindvall O., Bjorklund A. Origin, course and termination of the mesohabenular dopamine pathway in the rat. Brain Res. 1984, 307:99-108.
106. Slotnik B.M., Leonard C.M. A Stereotaxic Atlas of the Albino Mouse Forebrain. U.S. Dept. of Health, Education, and Welfare, Public Health Service, Alcohol, Drug Abuse, and Mental Health Administration 1975, Rockville, MD, Washington.
107. Spassky N., de Castro F., Le Bras B., Heydon K., Queraud-LeSaux F., Bloch-Gallego E., Chedotal A., Zalc B., Thomas J.L. Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J. Neurosci. 2002, 22:5992-6004.
108. Steward O., Trimmer P.A. Genetic influences on cellular reactions to CNS injury: the reactive response of astrocytes in denervated neuropil regions in mice carrying a mutation (Wld(S)) that causes delayed Wallerian degeneration. J. Comp. Neurol. 1997, 380:70-81.
109. Suto F., Murakami Y., Nakamura F., Goshima Y., Fujisawa H. Identification and characterization of a novel mouse plexin, plexin-A4. Mech. Dev. 2003, 120:385-396.
110. Suto F., Ito K., Uemura M., Shimizu M., Shinkawa Y., Sanbo M., Shinoda T., Tsuboi M., Takashima S., Yagi T., Fujisawa H. Plexin-a4 mediates axon-repulsive activities of both secreted and transmembrane semaphorins and plays roles in nerve fiber guidance. J. Neurosci. 2005, 25:3628-3637.
111. Takahashi T., Strittmatter S.M. Plexina1 autoinhibition by the plexin sema domain. Neuron 2001, 29:429-439.
112. Takahashi T., Fournier A., Nakamura F., Wang L.H., Murakami Y., Kalb R.G., Fujisawa H., Strittmatter S.M. Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 1999, 99:59-69.
113. Tamamaki N., Fujimori K., Nojyo Y., Kaneko T., Takauji R. Evidence that Sema3A and Sema3F regulate the migration of GABAergic neurons in the developing neocortex. J. Comp. Neurol. 2003, 455:238-248.
114. Taniguchi M., Yuasa S., Fujisawa H., Naruse I., Saga S., Mishina M., Yagi T. Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 1997, 19:519-530.
115. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science 1996, 274:1123-1133.
116. Tsai H.H., Miller R.H. Glial cell migration directed by axon guidance cues. Trends Neurosci. 2002, 25:173-175. discussion 175-176.
117. Tzschentke T.M. Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog. Neurobiol. 1998, 56:613-672.
118. Vitalis T., Cases O., Engelkamp D., Verney C., Price D.J. Defect of tyrosine hydroxylase-immunoreactive neurons in the brains of mice lacking the transcription factor Pax6. J. Neurosci. 2000, 20:6501-6516.
119. Voorn P., Kalsbeek A., Jorritsma-Byham B., Groenewegen H.J. The pre- and postnatal deveelopment of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum. Neuroscience 1988, 25:857-887.
120. Watanabe K., Ueno M., Kamiya D., Nishiyama A., Matsumura M., Wataya T., Takahashi J.B., Nishikawa S., Nishikawa S., Muguruma K., Sasai Y. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol. 2007, 25:681-686.
121. Webber A., Raz Y. Axon guidance cues in auditory development. Anat. Rec. A. Discov. Mol. Cell Evol. Biol. 2006, 288:390-396.
122. Wei L.C., Shi M., Chen L.W., Cao R., Zhang P., Chan Y.S. Nestin-containing cells express glial fibrillary acidic protein in the proliferative regions of central nervous system of postnatal developing and adult mice. Brain Res. Dev. Brain Res. 2002, 139:9-17.
123. Wright A.G., Demyanenko G.P., Powell A., Schachner M., Enriquez-Barreto L., Tran T.S., Polleux F., Maness P.F. Close homolog of L1 and neuropilin 1 mediate guidance of thalamocortical axons at the ventral telencephalon. J. Neurosci. 2007, 27:13667-13679.
124. Yamauchi K., Mizushima S., Tamada A., Yamamoto N., Takashima S., Murakami F. FGF8 signaling regulates growth of midbrain dopaminergic axons by inducing semaphorin 3F. J. Neurosci. 2009, 29:4044-4055.
125. Yaron A., Huang P.H., Cheng H.J., Tessier-Lavigne M. Differential requirement for Plexin-A3 and -A4 in mediating responses of sensory and sympathetic neurons to distinct class 3 Semaphorins. Neuron 2005, 45:513-523.
126. Yue Y., Widmer D.A., Halladay A.K., Cerretti D.P., Wagner G.C., Dreyer J.L., Zhou R. Specification of distinct dopaminergic neural pathways: roles of the Eph family receptor EphB1 and ligand ephrin-B2. J. Neurosci. 1999, 19:2090-2101.