Axonal commissures in the central nervous system: How to cross the midline?

Cellular and Molecular Life Sciences

Volumn 68, Issue 15, 2011, Pages 2539-2553

  Nawabi, Homaira ^a,b   Castellani, Valérie ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

Central nervous system; Commissural axon pathfinding; Midline crossing; Molecular strategies

Indexed keywords

EPHRIN B3; LIM PROTEIN; NERVE CELL ADHESION MOLECULE; NETRIN; OSTEOGENIC PROTEIN 1; ROUNDABOUT RECEPTOR; SEMAPHORIN; SEMAPHORIN 3B; SLIT PROTEIN; SONIC HEDGEHOG PROTEIN; STEM CELL FACTOR; TRANSCRIPTION FACTOR POU; UNCLASSIFIED DRUG; WNT4 PROTEIN;

ALTERNATIVE RNA SPLICING; BRAIN COMMISSURE; BRAIN CORTEX; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION REGULATION; INTERHEMISPHERIC TRANSFER; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; REVIEW; RNA TRANSLATION; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; SPINAL CORD; TRANSCRIPTION REGULATION; VISUAL SYSTEM;

ANIMALS; AXONAL TRANSPORT; AXONS; CELL MOVEMENT; CENTRAL NERVOUS SYSTEM; DROSOPHILA; DROSOPHILA PROTEINS; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; SYNAPSES;

EID: 79960968946     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0691-9     Document Type: Review

References (125)

1. Black DL, Zipursky SL (2008) To cross or not to cross: alternatively spliced forms of the Robo3 receptor regulate discrete steps in axonal midline crossing. Neuron 58(3):297-298 (Pubitemid 351615194)
2. Dickson BJ, Gilestro GF (2006) Regulation of commissural axon pathfinding by slit and its Robo receptors. Annu Rev Cell Dev Biol 22:651-675
3. Evans TA, Bashaw GJ (2010) Axon guidance at the midline: of mice and flies. Curr Opin Neurobiol 20(1):79-85
4. Shirasaki R, Katsumata R, Murakami F (1998) Change in chemoattractant responsiveness of developing axons at an intermediate target. Science 279(5347):105-107 (Pubitemid 28079166)
5. Brose K, Bland KS, Wang KH, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T (1999) Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96(6):795-806 (Pubitemid 29165083)
6. Butler SJ, Dodd J (2003) A role for BMP heterodimers in roof plate-mediated repulsion of commissural axons. Neuron 38(3):389-401 (Pubitemid 36579142)
7. Charron F, Stein E, Jeong J, McMahon AP, Tessier-Lavigne M (2003) The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 113(1):11-23 (Pubitemid 36411956)
8. Fazeli A, Dickinson SL, Hermiston ML, Tighe RV, Steen RG, Small CG, Stoeckli ET, Keino-Masu K, Masu M, Rayburn H, Simons J, Bronson RT, Gordon JI, Tessier-Lavigne M, Weinberg RA (1997) Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386(6627):796-804 (Pubitemid 27181247)
9. Gore BB, Wong KG, Tessier-Lavigne M (2008) Stem cell factor functions as an outgrowth-promoting factor to enable axon exit from the midline intermediate target. Neuron 57(4):501-510 (Pubitemid 351273993)
10. Jevince AR, Kadison SR, Pittman AJ, Chien CB, Kaprielian Z (2006) Distribution of EphB receptors and ephrin-B1 in the developing vertebrate spinal cord. J Comp Neurol 497(5):734-750 (Pubitemid 43993441)
11. Kadison SR, Makinen T, Klein R, Henkemeyer M, Kaprielian Z (2006) EphB receptors and ephrin-B3 regulate axon guidance at the ventral midline of the embryonic mouse spinal cord. J Neurosci 26(35):8909-8914 (Pubitemid 44319379)
12. Kullander K, Klein R (2002) Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 3(7):475-486 (Pubitemid 34733429)
13. Ly A, Nikolaev A, Suresh G, Zheng Y, Tessier-Lavigne M, Stein E (2008) DSCAM is a netrin receptor that collaborates with DCC in mediating turning responses to netrin-1. Cell 133(7):1241-1254 (Pubitemid 351852917)
14. Lyuksyutova AI, Lu CC, Milanesio N, King LA, Guo N, Wang Y, Nathans J, Tessier-Lavigne M, Zou Y (2003) Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science 302(5652):1984-1988 (Pubitemid 37523510)
15. Matsumoto Y, Irie F, Inatani M, Tessier-Lavigne M, Yamaguchi Y (2007) Netrin-1/DCC signaling in commissural axon guidance requires cell-autonomous expression of heparan sulfate. J Neurosci 27(16):4342-4350 (Pubitemid 46640711)
16. Nawabi H, Briancon-Marjollet A, Clark C, Sanyas I, Takamatsu H, Okuno T, Kumanogoh A, Bozon M, Takeshima K, Yoshida Y, Moret F, Abouzid K, Castellani V (2010) A midline switch of receptor processing regulates commissural axon guidance in vertebrates. Genes Dev 24(4):396-410
17. Okada A, Charron F, Morin S, Shin DS, Wong K, Fabre PJ, Tessier-Lavigne M, McConnell SK (2006) Boc is a receptor for sonic hedgehog in the guidance of commissural axons. Nature 444(7117):369-373 (Pubitemid 44764112)
18. Serafini T, Colamarino SA, Leonardo ED, Wang H, Beddington R, Skarnes WC, Tessier-Lavigne M (1996) Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87(6):1001-1014 (Pubitemid 26427984)
19. Stoeckli ET, Landmesser LT (1995) Axonin-1, Nr-CAM, and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. Neuron 14(6):1165-1179
20. Stoeckli ET, Sonderegger P, Pollerberg GE, Landmesser LT (1997) Interference with axonin-1 and NrCAM interactions unmasks a floor-plate activity inhibitory for commissural axons. Neuron 18(2):209-221 (Pubitemid 27111104)
21. Zou Y, Stoeckli E, Chen H, Tessier-Lavigne M (2000) Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102(3):363-375
22. Kidd T, Bland KS, Goodman CS (1999) Slit is the midline repellent for the robo receptor in Drosophila. Cell 96(6):785-794 (Pubitemid 29165082)
23. Bourikas D, Pekarik V, Baeriswyl T, Grunditz A, Sadhu R, Nardo M, Stoeckli ET (2005) Sonic hedgehog guides commissural axons along the longitudinal axis of the spinal cord. Nat Neurosci 8(3):297-304. doi:10.1038/nn1396 (Pubitemid 40300186)
24. Winckler B, Mellman I (2010) Trafficking guidance receptors. Cold Spring Harb Perspect Biol 2(7):a001826
25. Keleman K, Rajagopalan S, Cleppien D, Teis D, Paiha K, Huber LA, Technau GM, Dickson BJ (2002) Comm sorts robo to control axon guidance at the Drosophila midline. Cell 110(4):415-427 (Pubitemid 35232286)
26. Keleman K, Ribeiro C, Dickson BJ (2005) Comm function in commissural axon guidance: cell-autonomous sorting of Robo in vivo. Nat Neurosci 8(2):156-163 (Pubitemid 40194045)
27. Georgiou M, Tear G (2002) Commissureless is required both in commissural neurones and midline cells for axon guidance across the midline. Development (Cambridge) 129(12):2947-2956 (Pubitemid 34874272)
28. Georgiou M, Tear G (2003) The N-terminal and transmembrane domains of Commissureless are necessary for its function and trafficking within neurons. Mech Dev 120(9):1009-1019 (Pubitemid 37205044)
29. Stein E, Tessier-Lavigne M (2001) Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 291(5510):1928-1938 (Pubitemid 32216987)
30. Bashaw GJ, Klein R (2010) Signaling from axon guidance receptors. Cold Spring Harb Perspect Biol 2(5):a001941
31. Kania A, Jessell TM (2003) Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38(4):581-596 (Pubitemid 36645033)
32. Kania A, Johnson RL, Jessell TM (2000) Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102(2):161-173
33. Petros TJ, Rebsam A, Mason CA (2008) Retinal axon growth at the optic chiasm: to cross or not to cross. Annu Rev Neurosci 31:295-315
34. Drager UC (1985) Birth dates of retinal ganglion cells giving rise to the crossed and uncrossed optic projections in the mouse. Proc R Soc Lond B 224(1234):57-77
35. Guillery RW, Mason CA, Taylor JS (1995) Developmental determinants at the mammalian optic chiasm. J Neurosci 15(7 Pt 1):4727-4737
36. Marcus RC, Mason CA (1995) The first retinal axon growth in the mouse optic chiasm: axon patterning and the cellular environment. J Neurosci 15(10):6389-6402
37. Sretavan DW, Reichardt LF (1993) Time-lapse video analysis of retinal ganglion cell axon pathfinding at the mammalian optic chiasm: growth cone guidance using intrinsic chiasm cues. Neuron 10(4):761-777 (Pubitemid 23127978)
38. Wizenmann A, Thanos S, von Boxberg Y, Bonhoeffer F (1993) Differential reaction of crossing and non-crossing rat retinal axons on cell membrane preparations from the chiasm midline: an in vitro study. Development (Cambridge) 117(2):725-735 (Pubitemid 23103179)
39. Nakagawa S, Brennan C, Johnson KG, Shewan D, Harris WA, Holt CE (2000) Ephrin-B regulates the Ipsilateral routing of retinal axons at the optic chiasm. Neuron 25(3):599-610
40. Williams SE, Mann F, Erskine L, Sakurai T, Wei S, Rossi DJ, Gale NW, Holt CE, Mason CA, Henkemeyer M (2003) Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron 39(6):919-935 (Pubitemid 37130209)
41. Petros TJ, Shrestha BR, Mason C (2009) Specificity and sufficiency of EphB1 in driving the ipsilateral retinal projection. J Neurosci 29(11):3463-3474
42. Herrera E, Brown L, Aruga J, Rachel RA, Dolen G, Mikoshiba K, Brown S, Mason CA (2003) Zic2 patterns binocular vision by specifying the uncrossed retinal projection. Cell 114(5):545-557 (Pubitemid 37159252)
43. Merzdorf CS (2007) Emerging roles for zic genes in early development. Dev Dyn 236(4):922-940
44. Garcia-Frigola C, Carreres MI, Vegar C, Mason C, Herrera E (2008) Zic2 promotes axonal divergence at the optic chiasm midline by EphB1-dependent and -independent mechanisms. Development (Cambridge) 135(10):1833-1841
45. Lee R, Petros TJ, Mason CA (2008) Zic2 regulates retinal ganglion cell axon avoidance of ephrinB2 through inducing expression of the guidance receptor EphB1. J Neurosci 28(23):5910-5919
46. Wilson SI, Shafer B, Lee KJ, Dodd J (2008) A molecular program for contralateral trajectory: Rig-1 control by LIM homeodomain transcription factors. Neuron 59(3):413-424
47. Gowan K, Helms AW, Hunsaker TL, Collisson T, Ebert PJ, Odom R, Johnson JE (2001) Crossinhibitory activities of Ngn1 and Math1 allow specification of distinct dorsal interneurons. Neuron 31(2):219-232 (Pubitemid 32762976)
48. Gross MK, Dottori M, Goulding M (2002) Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34(4):535-549 (Pubitemid 34628751)
49. Lee KJ, Mendelsohn M, Jessell TM (1998) Neuronal patterning by BMPs: a requirement for GDF7 in the generation of a discrete class of commissural interneurons in the mouse spinal cord. Genes Dev 12(21):3394-3407 (Pubitemid 28520987)
50. Helms AW, Johnson JE (2003) Specification of dorsal spinal cord interneurons. Curr Opin Neurobiol 13(1):42-49 (Pubitemid 36197927)
51. Bermingham NA, Hassan BA, Wang VY, Fernandez M, Banfi S, Bellen HJ, Fritzsch B, Zoghbi HY (2001) Proprioceptor pathway development is dependent on Math1. Neuron 30(2):411-422 (Pubitemid 32530585)
52. Helms AW, Johnson JE (1998) Progenitors of dorsal commissural interneurons are defined by MATH1 expression. Development (Cambridge) 125(5):919-928 (Pubitemid 28143266)
53. Kidd T, Brose K, Mitchell KJ, Fetter RD, Tessier-Lavigne M, Goodman CS, Tear G (1998) Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92(2):205-215 (Pubitemid 28073044)
54. Kidd T, Russell C, Goodman CS, Tear G (1998) Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 20(1):25-33 (Pubitemid 28078346)
55. Bonkowsky JL, Yoshikawa S, O'Keefe DD, Scully AL, Thomas JB (1999) Axon routing across the midline controlled by the Drosophila Derailed receptor. Nature 402(6761):540-544
56. Yang L, Garbe DS, Bashaw GJ (2009) A frazzled/DCC-dependent transcriptional switch regulates midline axon guidance. Science 324(5929):944-947
57. Liu QX, Hiramoto M, Ueda H, Gojobori T, Hiromi Y, Hirose S (2009) Midline governs axon pathfinding by coordinating expression of two major guidance systems. Genes Dev 23(10):1165-1170
58. Buescher M, Svendsen PC, Tio M, Miskolczi-McCallum C, Tear G, Brook WJ, Chia W (2004) Drosophila T box proteins break the symmetry of hedgehog-dependent activation of wingless. Curr Biol 14(19):1694-1702 (Pubitemid 39306541)
59. Buescher M, Tio M, Tear G, Overton PM, Brook WJ, Chia W (2006) Functions of the segment polarity genes midline and H15 in Drosophila melanogaster neurogenesis. Dev Biol 292(2):418-429
60. Gaziova I, Bhat KM (2009) Ancestry-independent fate specification and plasticity in the developmental timing of a typical Drosophila neuronal lineage. Development (Cambridge) 136(2):263-274
61. Leal SM, Qian L, Lacin H, Bodmer R, Skeath JB (2009) Neuromancer1 and Neuromancer2 regulate cell fate specification in the developing embryonic CNS of Drosophila melanogaster. Dev Biol 325(1):138-150
62. Stennard FA, Harvey RP (2005) T-box transcription factors and their roles in regulatory hierarchies in the developing heart. Development (Cambridge) 132(22):4897-4910 (Pubitemid 41764003)
63. Rajagopalan S, Nicolas E, Vivancos V, Berger J, Dickson BJ (2000) Crossing the midline: roles and regulation of Robo receptors. Neuron 28(3):767-777 (Pubitemid 32038070)
64. Simpson JH, Kidd T, Bland KS, Goodman CS (2000) Short-range and long-range guidance by slit and its Robo receptors Robo and Robo2 play distinct roles in midline guidance. Neuron 28(3):753-766 (Pubitemid 32038069)
65. Spitzweck B, Brankatschk M, Dickson BJ (2010) Distinct protein domains and expression patterns confer divergent axon guidance functions for Drosophila Robo receptors. Cell 140(3):409-420
66. Black DL (2000) Protein diversity from alternative splicing: a challenge for bioinformatics and post-genome biology. Cell 103(3):367-370
67. Craig AM, Kang Y (2007) Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 17(1):43-52 (Pubitemid 46227985)
68. Chen Z, Gore BB, Long H, Ma L, Tessier-Lavigne M (2008) Alternative splicing of the Robo3 axon guidance receptor governs the midline switch from attraction to repulsion. Neuron 58(3):325-332 (Pubitemid 351615180)
69. Mambetisaeva ET, Andrews W, Camurri L, Annan A, Sundaresan V (2005) Robo family of proteins exhibit differential expression in mouse spinal cord and Robo-Slit interaction is required for midline crossing in vertebrate spinal cord. Dev Dyn 233(1):41-51 (Pubitemid 40548022)
70. Sabatier C, Plump AS, Le M, Brose K, Tamada A, Murakami F, Lee EY, Tessier-Lavigne M (2004) The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell 117(2):157-169 (Pubitemid 38496237)
71. Lin AC, Tan CL, Lin CL, Strochlic L, Huang YS, Richter JD, Holt CE (2009) Cytoplasmic polyadenylation and cytoplasmic polyadenylation element-dependent mRNA regulation are involved in Xenopus retinal axon development. Neural Dev 4:8
72. Richter JD (2007) CPEB: a life in translation. Trends Biochem Sci 32(6):279-285
73. Bassell GJ, Warren ST (2008) Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60(2):201-214. doi:10.1016/j.neuron.2008.10.004
74. Kuwako K, Kakumoto K, Imai T, Igarashi M, Hamakubo T, Sakakibara S, Tessier-Lavigne M, Okano HJ, Okano H (2010) Neural RNA-binding protein Musashi1 controls midline crossing of precerebellar neurons through posttranscriptional regulation of Robo3/Rig-1 expression. Neuron 67(3):407-421
75. Di Meglio T, Nguyen-Ba-Charvet KT, Tessier-Lavigne M, Sotelo C, Chedotal A (2008) Molecular mechanisms controlling midline crossing by precerebellar neurons. J Neurosci 28(25):6285-6294
76. Kuhl D, Skehel P (1998) Dendritic localization of mRNAs. Curr Opin Neurobiol 8(5):600-606 (Pubitemid 28488421)
77. Martin KC, Barad M, Kandel ER (2000) Local protein synthesis and its role in synapse-specific plasticity. Curr Opin Neurobiol 10(5):587-592
78. Steward O (1997) mRNA localization in neurons: a multipurpose mechanism? Neuron 18(1):9-12
79. Steward O, Levy WB (1982) Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci 2(3):284-291 (Pubitemid 12098607)
80. Davis L, Dou P, De Wit M, Kater SB (1992) Protein synthesis within neuronal growth cones. J Neurosci 12(12):4867-4877
81. Campbell DS, Holt CE (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32(6):1013-1026 (Pubitemid 34075393)
82. Merianda TT, Lin AC, Lam JS, Vuppalanchi D, Willis DE, Karin N, Holt CE, Twiss JL (2009) A functional equivalent of endoplasmic reticulum and Golgi in axons for secretion of locally synthesized proteins. Mol Cell Neurosci 40(2):128-142
83. Horton AC, Ehlers MD (2003) Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J Neurosci 23(15):6188-6199 (Pubitemid 36875619)
84. Zivraj KH, Tung YC, Piper M, Gumy L, Fawcett JW, Yeo GS, Holt CE (2010) Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J Neurosci 30(46):15464-15478
85. Lin AC, Holt CE (2007) Local translation and directional steering in axons. EMBO J 26(16):3729-3736 (Pubitemid 47295875)
86. Lin AC, Holt CE (2008) Function and regulation of local axonal translation. Curr Opin Neurobiol 18(1):60-68
87. Roche FK, Marsick BM, Letourneau PC (2009) Protein synthesis in distal axons is not required for growth cone responses to guidance cues. J Neurosci 29(3):638-652
88. Hengst U, Deglincerti A, Kim HJ, Jeon NL, Jaffrey SR (2009) Axonal elongation triggered by stimulus-induced local translation of a polarity complex protein. Nat Cell Biol 11(8):1024-1030
89. Dubacq C, Jamet S, Trembleau A (2009) Evidence for developmentally regulated local translation of odorant receptor mRNAs in the axons of olfactory sensory neurons. J Neurosci 29(33):10184-10190
90. Brittis PA, Lu Q, Flanagan JG (2002) Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110(2):223-235 (Pubitemid 34876550)
91. Tcherkezian J, Brittis PA, Thomas F, Roux PP, Flanagan JG (2010) Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell 141(4):632-644
92. Evans TA, Bashaw GJ (2010) Functional diversity of Robo receptor immunoglobulin domains promotes distinct axon guidance decisions. Curr Biol 20(6):567-572
93. Gilestro GF (2008) Redundant mechanisms for regulation of midline crossing in Drosophila. PloS one 3(11):e3798
94. Coleman HA, Labrador JP, Chance RK, Bashaw GJ (2010) The Adam family metalloprotease Kuzbanian regulates the cleavage of the roundabout receptor to control axon repulsion at the midline. Development (Cambridge) 137(14):2417-2426
95. Hattori M, Osterfield M, Flanagan JG (2000) Regulated cleavage of a contact-mediated axon repellent. Science 289(5483):1360-1365 (Pubitemid 30656055)
96. Chedotal A (2007) Slits and their receptors. Adv Exp Med Biol 621:65-80
97. Bagnard D, Lohrum M, Uziel D, Puschel AW, Bolz J (1998) Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. Development (Cambridge) 125(24):5043-5053 (Pubitemid 29026785)
98. Falk J, Bechara A, Fiore R, Nawabi H, Zhou H, Hoyo-Becerra C, Bozon M, Rougon G, Grumet M, Puschel AW, Sanes JR, Castellani V (2005) Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 48(1):63-75 (Pubitemid 41384166)
99. Kolodkin AL, Matthes DJ, Goodman CS (1993) The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75(7):1389-1399
100. Luo Y, Raible D, Raper JA (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75(2):217-227 (Pubitemid 23320286)
101. Huber AB, Kolodkin AL, Ginty DD, Cloutier JF (2003) Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 26:509-563 (Pubitemid 37064943)
102. Kruger RP, Aurandt J, Guan KL (2005) Semaphorins command cells to move. Nat Rev Mol Cell Biol 6(10):789-800 (Pubitemid 41726117)
103. Fujisawa H, Ohtsuki T, Takagi S, Tsuji T (1989) An aberrant retinal pathway and visual centers in Xenopus tadpoles share a common cell surface molecule, A5 antigen. Dev Biol 135(2):231-240 (Pubitemid 19248033)
104. He Z, Tessier-Lavigne M (1997) Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell 90(4):739-751 (Pubitemid 27357965)
105. Kolodkin AL, Levengood DV, Rowe EG, Tai YT, Giger RJ, Ginty DD (1997) Neuropilin is a semaphorin III receptor. Cell 90(4):753-762 (Pubitemid 27357966)
106. Satoda M, Takagi S, Ohta K, Hirata T, Fujisawa H (1995) Differential expression of two cell surface proteins, neuropilin and plexin, in Xenopus olfactory axon subclasses. J Neurosci 15(1 Pt 2):942-955
107. Takagi S, Kasuya Y, Shimizu M, Matsuura T, Tsuboi M, Kawakami A, Fujisawa H (1995) Expression of a cell adhesion molecule, neuropilin, in the developing chick nervous system. Dev Biol 170(1):207-222
108. Fujisawa H (2004) Discovery of semaphorin receptors, neuropilin and plexin, and their functions in neural development. J Neurobiol 59(1):24-33
109. Schwarz Q, Ruhrberg C (2010) Neuropilin, you gotta let me know: should I stay or should I go? Cell Adh Migr 4(1):61-66
110. Kameyama T, Murakami Y, Suto F, Kawakami A, Takagi S, Hirata T, Fujisawa H (1996) Identification of plexin family molecules in mice. Biochem Biophys Res Commun 226(2):396-402 (Pubitemid 26331913)
111. Ohta K, Takagi S, Asou H, Fujisawa H (1992) Involvement of neuronal cell surface molecule B2 in the formation of retinal plexiform layers. Neuron 9(1):151-161
112. Takahashi T, Fournier A, Nakamura F, Wang LH, Murakami Y, Kalb RG, Fujisawa H, Strittmatter SM (1999) Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 99(1):59-69 (Pubitemid 29468630)
113. Tamagnone L, Artigiani S, Chen H, He Z, Ming GI, Song H, Chedotal A, Winberg ML, Goodman CS, Poo M, Tessier-Lavigne M, Comoglio PM (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99(1):71-80 (Pubitemid 29468631)
114. Rohm B, Ottemeyer A, Lohrum M, Puschel AW (2000) Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A. Mech Dev 93(1-2):95-104 (Pubitemid 30216499)
115. Negishi M, Oinuma I, Katoh H (2005) Plexins: axon guidance and signal transduction. Cell Mol Life Sci 62(12):1363-1371 (Pubitemid 40853824)
116. Bechara A, Nawabi H, Moret F, Yaron A, Weaver E, Bozon M, Abouzid K, Guan JL, Tessier-Lavigne M, Lemmon V, Castellani V (2008) FAK-MAPK-dependent adhesion disassembly downstream of L1 contributes to semaphorin3A-induced collapse. EMBO J 27(11):1549-1562 (Pubitemid 351794032)
117. Parra LM, Zou Y (2010) Sonic hedgehog induces response of commissural axons to Semaphorin repulsion during midline crossing. Nat Neurosci 13(1):29-35
118. Carragher NO, Frame MC (2002) Calpain: a role in cell transformation and migration. Int J Biochem Cell Biol 34(12):1539-1543
119. Wu HY, Lynch DR (2006) Calpain and synaptic function. Mol Neurobiol 33(3):215-236
120. Bai G, Chivatakarn O, Bonanomi D, Lettieri K, Franco L, Xia C, Stein E, Ma L, Lewcock JW, Pfaff SL (2011) Presenilin-dependent receptor processing is required for axon guidance. Cell 144(1):106-118
121. Chow VW, Mattson MP, Wong PC, Gleichmann M (2010) An overview of APP processing enzymes and products. Neuromolecular Med 12(1):1-12
122. Guardia-Laguarta C, Pera M, Lleo A (2010) gamma-Secretase as a therapeutic target in Alzheimer's disease. Curr Drug Targets 11(4):506-517
123. Jorissen E, De Strooper B (2010) Gamma-secretase and the intramembrane proteolysis of Notch. Curr Top Dev Biol 92:201-230
124. Taniguchi Y, Kim SH, Sisodia SS (2003) Presenilin-dependent "gamma-secretase" processing of deleted in colorectal cancer (DCC). J Biol Chem 278(33):30425-30428
125. Sorimachi H, Hata S, Ono Y (2010) Expanding members and roles of the calpain superfamily and their genetically modified animals. Exp Anim 59(5):549-566