Neuronal guidance genes in health and diseases

Junichi Yuasa-Kawada, Mariko Kinoshita-Kawada, Yoshio Tsuboi, Jane Y. Wu

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Protein Cell ›› 2023, Vol. 14 ›› Issue (4) : 238-261. DOI: 10.1093/procel/pwac030
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Neuronal guidance genes in health and diseases

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Abstract

Neurons migrate from their birthplaces to the destinations, and extending axons navigate to their synaptic targets by sensing various extracellular cues in spatiotemporally controlled manners. These evolutionally conserved guidance cues and their receptors regulate multiple aspects of neural development to establish the highly complex nervous system by mediating both short- and long-range cell–cell communications. Neuronal guidance genes (encoding cues, receptors, or downstream signal transducers) are critical not only for development of the nervous system but also for synaptic maintenance, remodeling, and function in the adult brain. One emerging theme is the combinatorial and complementary functions of relatively limited classes of neuronal guidance genes in multiple processes, including neuronal migration, axonal guidance, synaptogenesis, and circuit formation. Importantly, neuronal guidance genes also regulate cell migration and cell–cell communications outside the nervous system. We are just beginning to understand how cells integrate multiple guidance and adhesion signaling inputs to determine overall cellular/subcellular behavior and how aberrant guidance signaling in various cell types contributes to diverse human diseases, ranging from developmental, neuropsychiatric, and neurodegenerative disorders to cancer metastasis. We review classic studies and recent advances in understanding signaling mechanisms of the guidance genes as well as their roles in human diseases. Furthermore, we discuss the remaining challenges and therapeutic potentials of modulating neuronal guidance pathways in neural repair.

Keywords

axon guidance / neuronal migration / synaptogenesis / neural circuit formation / neural mapping / cell-cell communications / angiogenesis / organogenesis / cancer metastasis

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Junichi Yuasa-Kawada, Mariko Kinoshita-Kawada, Yoshio Tsuboi, Jane Y. Wu. Neuronal guidance genes in health and diseases. Protein Cell, 2023, 14(4): 238‒261 https://doi.org/10.1093/procel/pwac030

References

[1]
Abe H, Jitsuki S, Nakajima W et al. CRMP2-binding compound, edonerpic maleate, accelerates motor function recovery from brain damage. Science 2018;360:50–57.
CrossRef Google scholar
[2]
Adams RH, Eichmann A. Axon guidance molecules in vascular patterning. Cold Spring Harb Perspect Biol 2010;2:a001875.
CrossRef Google scholar
[3]
Alavi M, Song MM, King GLA et al. Dscam1 forms a complex with Robo1 and the N-terminal fragment of Slit to promote the growth of longitudinal axons. PLoS Biol 2016;14:e1002560.
CrossRef Google scholar
[4]
Bai G, Chivatakarn O, Bonanomi D et al. Presenilin-dependent receptor processing is required for axon guidance. Cell 2011;144:106–118.
CrossRef Google scholar
[5]
Barker RA, Götz M, Parmar M. New approaches for brain repair-from rescue to reprogramming. Nature 2018;557:329–334.
CrossRef Google scholar
[6]
Bashaw GJ, Kidd T, Murray D, Pawson T, Goodman CS. Repulsive axon guidance: Abelson and Enabled play opposing roles down-stream of the roundabout receptor. Cell 2000;101:703–715.
CrossRef Google scholar
[7]
Beamish IV, Hinck L, Kennedy TE. Making connections: guidance cues and receptors at nonneural cell-cell junctions. Cold Spring Harb Perspect Biol 2018;10:a029165.
CrossRef Google scholar
[8]
Berns DS, DeNardo LA, Pederick DT et al. Teneurin-3 controls topographic circuit assembly in the hippocampus. Nature 2018;554:328–333.
CrossRef Google scholar
[9]
Bhosle VK, Mukherjee T, Huang YW et al. Slit2/ROBO1-signaling inhibits macropinocytosis via RhoA-mediated cytoskeletal changes in macrophages. Nat Commun 2020;11:4112.
CrossRef Google scholar
[10]
Biankin AV, Waddell N, Kassahn KS et al. Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes. Nature 2012;491:399–1405.
CrossRef Google scholar
[11]
Blockus H, Chédotal A. Slit-Robo signaling. Development 2016;143:3037–3044.
CrossRef Google scholar
[12]
Borrell V, Cardenas A, Ciceri G et al. Slit/Robo signaling modulates the proliferation of central nervous system progenitors. Neuron 2012;76:1284–1293.
CrossRef Google scholar
[13]
Bourikas D, Pekarik V, Baeriswyl T et al. Sonic hedgehog guides commissural axons along the longitudinal axis of the spinal cord. Nat Neurosci 2005;8:297–304.
CrossRef Google scholar
[14]
BRAIN Initiative Cell Census Network (BICCN). A multimodal cell census and atlas of the mammalian primary motor cortex. Nature 2021;598:86–102.
[15]
Branchfield K, Nantie L, Verheyden JM et al. Pulmonary neuroendocrine cells function as airway sensors to control lung immune response. Science 2016;351:707–710.
CrossRef Google scholar
[16]
Brignani S, Raj DDA, Schmidt ERE et al. Remotely produced and axon-derived netrin-1 instructs GABAergic neuron migration and dopaminergic substantia nigra development. Neuron 2020;107:684–702
CrossRef Google scholar
[17]
Brose K, Bland KS, Wang KH et al. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 1999;96:795–806.
CrossRef Google scholar
[18]
Buck L, Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 1991;65:175–187.
CrossRef Google scholar
[19]
Cajal SRY (1995) Histology of the nervous system of man and vertebrates (ed. Swanson, N. & Swanson, L. W.) (Oxford University Press, Oxford).
[20]
Campbell DS, Holt CE. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 2003;37:939–952.
CrossRef Google scholar
[21]
Cang J, Niell CM, Liu XR et al. Selective disruption of one Cartesian axis of cortical maps and receptive fields by deficiency in ephrin-As and structured activity. Neuron 2008;57:511–523.
CrossRef Google scholar
[22]
Cárdenas A, Villalba A, Romero CD et al. Evolution of cortical neurogenesis in amniotes controlled by Robo signaling levels. Cell 2018;174:590–606.
CrossRef Google scholar
[23]
Carmeliet P, Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature 2005;436:193–200.
CrossRef Google scholar
[24]
Carrillo RA, Olsen DP, Yoon KS et al. Presynaptic activity and CaMKII modulate retrograde semaphorin signaling and synaptic refinement. Neuron 2010;68:32–44.
CrossRef Google scholar
[25]
Chaudhari K, Gorla M, Chang C et al. Robo recruitment of the Wave regulatory complex plays an essential and conserved role in midline repulsion. Elife 2021;10:e64474.
CrossRef Google scholar
[26]
Chédotal A. Roles of axon guidance molecules in neuronal wiring in the developing spinal cord. Nat Rev Neurosci 2019;20:380–396.
CrossRef Google scholar
[27]
Chen G, Kang SS, Wang Z et al. Netrin-1 receptor UNC5C cleavage by active δ-secretase enhances neurodegeneration, promoting Alzheimer’s disease pathologies. Sci Adv 2021;7:eabe4499.
CrossRef Google scholar
[28]
Chen Z, Gore BB, Long H et al. Alternative splicing of the Robo3 axon guidance receptor governs the midline switch from attraction to repulsion. Neuron 2008;58:325–332.
CrossRef Google scholar
[29]
Cheng HJ, Nakamoto M, Bergemann AD, Flanagan JG. Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 1995;82:371–381.
CrossRef Google scholar
[30]
Croarkin PE, Luby JL, Cercy K et al. Genetic risk score analysis in early-onset bipolar disorder. J Clin Psychiatry 2017;78:1337–1343.
CrossRef Google scholar
[31]
Dallol A, Da Silva NF, Viacava P et al. SLIT2, a human homologue of the Drosophila Slit2 gene, has tumor suppressor activity and is frequently inactivated in lung and breast cancers. Cancer Res 2002;62:5874–5880.
[32]
Dascenco D, Erfurth ML, Izadifar A et al. Slit and receptor tyrosine phosphatase 69D confer spatial specificity to axon branching via Dscam1. Cell 2015;162:1140–1154.
CrossRef Google scholar
[33]
del Toro D, Carrasquero-Ordaz MA, Chu A et al. Structural basis of Teneurin-Latrophilin interaction in repulsive guidance of migrating neurons. Cell 2020;180:323–339
CrossRef Google scholar
[34]
Delloye-Bourgeois C, Jacquier A, Charoy C et al. PlexinA1 is a new Slit receptor and mediates axon guidance function of Slit C-terminal fragments. Nat Neurosci 2015;18:36–45.
CrossRef Google scholar
[35]
Delloye-Bourgeois C, Bertin L, Thoinet K et al. Microenvironment-driven shift of cohesion/detachment balance within tumors induces a switch toward metastasis in neuroblastoma. Cancer Cell 2017;32:427–443.
CrossRef Google scholar
[36]
Denoth-Lippuner A, Jessberger S. Formation and integration of new neurons in the adult hippocampus. Nat Rev Neurosci 2021;22:223–236.
CrossRef Google scholar
[37]
Depaepe V, Suarez-Gonzalez N, Dufour A et al. Ephrin signaling controls brain size by regulating apoptosis of neural progenitors. Nature 2005;435:1244–1250.
CrossRef Google scholar
[38]
Depienne C, Bouteiller D, Meneret A et al. RAD51 haploinsufficiency causes congenital mirror movements in humans. Am J Hum Genet 2012;90:301–307.
CrossRef Google scholar
[39]
Dickson BJ, Zou Y. Navigating intermediate targets: the nervous system midline. Cold Spring Harb Perspect Biol 2010;2:a002055.
CrossRef Google scholar
[40]
Dominici C, Moreno-Bravo JA, Puiggros SR et al. Floor-plate-derived netrin-1 is dispensable for commissural axon guidance. Nature 2017;545:350–354.
CrossRef Google scholar
[41]
Domyan ET, Branchfield K, Gibson DA et al. Roundabout receptors are critical for foregut separation from the body wall. Dev Cell 2013;24:52–63.
CrossRef Google scholar
[42]
Dong X, Shen K, Bülow HE. Intrinsic and extrinsic mechanisms of dendritic morphogenesis. Annu Rev Physiol 2015;7:271–300.
CrossRef Google scholar
[43]
Dorskind JM, Kolodkin AL. Revisiting and refining roles of neural guidance cues in circuit assembly. Curr Opin Neurobiol 2021;66:10–21.
CrossRef Google scholar
[44]
Drescher U, Kremoser C, Handwerker C et al. In vitro guidance of tetinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 1995;82:359–370.
CrossRef Google scholar
[45]
Ducuing H, Gardette T, Pignata A et al. SlitC-PlexinA1 mediates iterative inhibition for orderly passage of spinal commissural axons through the floor plate. Elife 2020;9:e63205.
CrossRef Google scholar
[46]
Fan X, Labrador JP, Hing H et al. Slit stimulation recruits Dock and Pak to the roundabout receptor and increases Rac activity to regulate axon repulsion at the CNS midline. Neuron 2003;40:113–127.
CrossRef Google scholar
[47]
Feldheim DA, Kim YI, Bergemann AD et al. Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 2000;25:563–574.
CrossRef Google scholar
[48]
Fernandopulle MS, Lippincott-Schwartz J, Ward ME. RNA transport and local translation in neurodevelopmental and neurodegenerative disease. Nat Neurosci 2021;24:622–632.
CrossRef Google scholar
[49]
Franke B, Faraone SV, Asherson P et al. The genetics of attention deficit/hyperactivity disorder in adults, a review. Mol Psychiatry 2012;17:960–987.
CrossRef Google scholar
[50]
Fukushima Y, Nishiyama K, Kataoka H et al. RhoJ integrates attractive and repulsive cues in directional migration of endothelial cells. EMBO J 2020;39:e102930.
CrossRef Google scholar
[51]
Ge X, Zhang K, Gribizis A et al. Retinal waves prime visual motion detection by simulating future optic flow. Science 2021;373:eabd0830.
CrossRef Google scholar
[52]
Gitler AD, Lu MM, Epstein JA. PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development. Dev Cell 2004;7:107–116.
CrossRef Google scholar
[53]
Glasgow SD, Ruthazer ES, Kennedy TE. Guiding synaptic plasticity: novel roles for netrin-1 in synaptic plasticity and memory formation in the adult brain. J Physiol 2021;599:493–505.
CrossRef Google scholar
[54]
Gomez TM, Zheng JQ. The molecular basis for calcium-dependent axon pathfinding. Nat Rev Neurosci 2006;7:115–125.
CrossRef Google scholar
[55]
Gorla M, Santiago C, Chaudhari K et al. Ndfip proteins target Robo receptors for degradation and allow commissural axons to cross the midline in the developing spinal cord. Cell Rep 2019;26:3298–3312.
CrossRef Google scholar
[56]
Goshima Y, Nakamura F, Strittmatter P et al. Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 1995;376:509–514.
CrossRef Google scholar
[57]
Gould RA, Aziz H, Woods CE et al. ROBO4 variants predispose individual s to bicuspid aortic valve and thoracic aortic aneurysm. Nat Genet 2019;51:42–50.
CrossRef Google scholar
[58]
Gu C, Rodriguez ER, Reimert DV et al. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell 2003;5:45–57.
CrossRef Google scholar
[59]
Gu C, Yoshida Y, Livet J et al. Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science 2005;307:265–268.
CrossRef Google scholar
[60]
Guan KL, Rao Y. Signalling mechanisms mediating neuronal responses to guidance cues. Nat Rev Neurosci 2003;4:941–956.
CrossRef Google scholar
[61]
Guerrier S, Coutinho-Budd J, Sassa T et al. The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 2009;138:990–1004.
CrossRef Google scholar
[62]
Gulsuner S, Walsh T, Watts AC et al. Spatial and temporal mapping of de novo mutations in schizophrenia to a fetal prefrontal cortical network. Cell 2013;154:518–529.
CrossRef Google scholar
[63]
Hayashi M, Nakashima T, Taniguchi M et al. Osteoprotection by semaphorin 3A. Nature 2012;485:69–74.
CrossRef Google scholar
[64]
Hayashi M, Nakashima T, Yoshimura N et al. Autoregulation of osteocyte Sema3A orchestrates estrogen action and counteracts bone aging. Cell Metab 2019;29:627–637.
CrossRef Google scholar
[65]
Hayashi S, Inoue Y, Kiyonari H et al. Protocadherin-17 mediates collective axon extension by recruiting actin regulator complexes to interaxonal contacts. Dev Cell 2014;30:673–687.
CrossRef Google scholar
[66]
He XF, Li G, Li LL et al. Overexpression of Slit2 decreases neuronal excitotoxicity, accelerates glymphatic clearance, and improves cognition in a multiple microinfarcts model. Mol Brain 2020;13:135.
CrossRef Google scholar
[67]
Hempel CM, Vincent P, Adams SR et al. Spatio-temporal dynamics of cyclic AMP signals in an intact neural circuitm. Nature 1996;384:166–169.
CrossRef Google scholar
[68]
Hiramoto M, Hiromi Y, Giniger E et al. The Drosophila Netrin receptor Frazzled guides axons by controlling Netrin distribution. Nature 2000;406:886–889.
CrossRef Google scholar
[69]
Hollis ER, Ishiko N, Yu T et al. Ryk controls remapping of motor cortex during functional recovery after spinal cord injury. Nat Neurosci 2016;19:697–705.
CrossRef Google scholar
[70]
Höpker VH, Shewan D, Tessier-Lavigne M et al. Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 1999;401:69–73.
CrossRef Google scholar
[71]
Hornberger MR, Dutting D, Ciossek T et al. Modulation of EphA receptor function by coexpressed ephrinA ligands on retinal ganglion cell axons. Neuron 1999;22:731–742.
CrossRef Google scholar
[72]
Hung RJ, Pak CW, Terman JR. Direct redox regulation of F-actin assembly and disassembly by Mical. Science 2011;334:1710–1713.
CrossRef Google scholar
[73]
Imai T, Yamazaki T, Kobayakawa R et al. Pre-target axon sorting establishes the neural map topography. Science 2009;325:585–590.
CrossRef Google scholar
[74]
Imai T, Suzuki M, Sakano H. Odorant receptor-derived cAMP signals direct axonal targeting. Science 2006;314:657–661.
CrossRef Google scholar
[75]
Inoue N, Nishizumi H, Ooyama R et al. The olfactory critical period is determined by activity-dependent Sema7A/PlxnC1 signaling within glomeruli. Elife 2021;10:e65078.
CrossRef Google scholar
[76]
Iwasato T, Katoh H, Nishimaru H et al. Rac-GAP alpha-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell 2007;130:742–753.
CrossRef Google scholar
[77]
Jamuar SS, Schmitz-Abe K, D’Gama AM et al. Biallelic mutations in human DCC cause developmental split-brain syndrome. Nat Genet 2017;49:606–612.
CrossRef Google scholar
[78]
Janes PW, Vail ME, Ernst M et al. Eph receptors in the immunosuppressive tumor microenvironment. Cancer Res 2021;81:801–805.
CrossRef Google scholar
[79]
Jasmin M, Ahn EH, Voutilainen MH et al. Netrin-1 and its receptor DCC modulate survival and death of dopamine neurons and Parkinson’s disease features. EMBO J 2021;40:e105537.
CrossRef Google scholar
[80]
Jaworski A, Tom I, Tong RK et al. Operational redundancy in axon guidance through the multifunctional receptor Robo3 and its ligand NELL2. Science 2015;350:961–965.
CrossRef Google scholar
[81]
Jaworski A, Long H, Tessier-Lavigne M. Collaborative and specialized functions of Robo1 and Robo2 in spinal commissural axon guidance. J Neurosci 2010;30:9445–9453.
CrossRef Google scholar
[82]
Jaworski A, Tessier-Lavigne M. Autocrine/juxtaparacrine regulation of axon fasciculation by Slit-Robo signaling. Nat Neurosci 2012;15:367–369.
CrossRef Google scholar
[83]
Jen JC, Chan WM, Bosley TM et al. Mutations in a human ROBO gene disrupt hindbrain axon pathway crossing and morphogenesis. Science 2004;304:1509–1513.
CrossRef Google scholar
[84]
Jessell TM. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 2000;1:20–29.
CrossRef Google scholar
[85]
Jones CA, Nishiya N, London NR et al. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat Cell Biol 2009;11:1325–1331.
CrossRef Google scholar
[86]
Jongbloets BC, Lemstra S, Schellino R et al. Stage-specific functions of Semaphorin7A during adult hippocampal neurogenesis rely on distinct receptors. Nat Commun 2017;8:14666.
CrossRef Google scholar
[87]
Jørgensen C, Sherman A, Chen GI et al. Cell-specific information processing in segregating populations of Eph receptor ephrin-expressing cells. Science 2009;326:1502–1509.
CrossRef Google scholar
[88]
Justice ED, Barnum SJ, Kidd T. The WAGR syndrome gene PRRG4 is a functional homologue of the commissureless axon guidance gene. PLoS Genet 2017;13:e1006865.
CrossRef Google scholar
[89]
Kaneko N, Herranz-Perez V, Otsuka T et al. New neurons use Slit-Robo signaling to migrate through the glial meshwork and approach a lesion for functional regeneration. Sci Adv 2018;4:eaav0618.
CrossRef Google scholar
[90]
Kania A, Klein R. Mechanisms of ephrin-Eph signalling in development, physiology and disease. Nat Rev Mol Cell Biol 2016;17:240–256.
CrossRef Google scholar
[91]
Kanth SM, Gairhe S, Torabi-Parizi P. The role of semaphorins and their receptors in innate immune responses and clinical diseases of acute inflammation. Front Immunol 2021;12:672441.
CrossRef Google scholar
[92]
Karch CM, Goate AM. Alzheimer’s disease risk genes and mechanisms of disease pathogenesis. Biol Psychiatry 2015;77:43–51.
CrossRef Google scholar
[93]
Keleman K, Ribeiro C, Dickson BJ. Comm function in commissural axon guidance: cell-autonomous sorting of Robo in vivo. Nat Neurosci 2005;8:156–163.
CrossRef Google scholar
[94]
Kellermeyer R, Heydman LM, Gillis T et al. Proteolytic cleavage of Slit by the Tolkin protease converts an axon repulsion cue to an axon growth cue in vivo. Development 2020;147:dev196055.
CrossRef Google scholar
[95]
Kellermeyer R, Heydman LM, Mastick GS et al. The role of apoptotic signaling in axon guidance. J Dev Biol 2018;6:E24.
CrossRef Google scholar
[96]
Kennedy TE, Serafini T, de la Torre JR et al. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 1994;78:425–435.
CrossRef Google scholar
[97]
Kidd T, Brose K, Mitchell KJ et al. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 1998;92:205–215.
CrossRef Google scholar
[98]
Kidd T, Bland KS, Goodman CS. Slit is the midline repellent for the Robo receptor in Drosophila. Cell 1999;96:785–794.
CrossRef Google scholar
[99]
Kindberg AA, Srivastava V, Muncie JM et al. EPH/EPHRIN regulates cellular organization by actomyosin contractility effects on cell contacts. J Cell Biol 2021;220:e202005216.
CrossRef Google scholar
[100]
Kinoshita-Kawada M, Hasegawa H, Hongu T et al. A crucial role of Arf6 in the response of commissural axons to Slit. Development 2019;146:dev172106.
CrossRef Google scholar
[101]
Koch AW, Mathivet T, Larrivee B et al. Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Dev Cell 2011;20:33–46.
CrossRef Google scholar
[102]
Köhler D, Granja T, Volz J et al. Red blood cell-derived semaphorin 7A promotes thrombo-inflammation in myocardial ischemia-reperfusion injury through platelet GPIb. Nat Commun 2020;11:1315.
CrossRef Google scholar
[103]
Kolodkin AL, Matthes DJ, Goodman CS. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 1993;75:1389–1399.
CrossRef Google scholar
[104]
Kong R, Yi FS, Wen PS et al. Myo9b is a key player in SLIT/ROBO-mediated lung tumor suppression. J Clin Invest 2015;125:4407–4420.
CrossRef Google scholar
[105]
Körner A, Bernard A, Fitzgerald JC et al. Sema7A is crucial for resolution of severe inflammation. Proc Natl Acad Sci USA 2021;118:e2017527118.
CrossRef Google scholar
[106]
Kruszka P, Tanpaiboon P, Neas K et al. Loss of function in ROBO1 is associated with tetralogy of Fallot and septal defects. J Med Genet 2017;54:825–829.
CrossRef Google scholar
[107]
Lai Wing Sun K, Correia JP, Kennedy TE. Netrins: versatile extracellular cues with diverse functions. Development 2011;138:2153–2169.
CrossRef Google scholar
[108]
Li HS, Chen JH, Wu W et al. Vertebrate Slit, a secreted ligand for the transmembrane protein Roundabout, is a repellent for olfactory bulb axons. Cell 1999;96:807–818.
CrossRef Google scholar
[109]
Li X, Gao X, Liu GF et al. Netrin signal transduction and the guanine nucleotide exchange factor DOCK180 in attractive signaling. Nat Neurosci 2008;11:28–35.
CrossRef Google scholar
[110]
Lieberam I, Agalliu D, Nagasawa T et al. A Cxcl12-CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron 2005;47:667–679.
CrossRef Google scholar
[111]
Liu G, Beggs H, Jurgensen C et al. Netrin requires focal adhesion kinase and Src family kinases for axon outgrowth and attraction. Nat Neurosci 2004;7:1222–1232.
CrossRef Google scholar
[112]
Liu G, Li W, Gao X et al. p130CAS is required for netrin signaling and commissural axon guidance. J Neurosci 2007;27:957–968.
CrossRef Google scholar
[113]
Llinares-Benadero C, Borrell V. Deconstructing cortical folding: genetic, cellular and mechanical determinants. Nat Rev Neurosci 2019;20:161–176.
CrossRef Google scholar
[114]
Lodovichi C. Topographic organization in the olfactory bulb. Cell Tissue Res 2021;383:457–472.
CrossRef Google scholar
[115]
Lowery LA, Van Vactor D. The trip of the tip: understanding the growth cone machinery. Nat Rev Mol Cell Biol 2009;10:332–343.
CrossRef Google scholar
[116]
Lu X, le Noble F, Yuan L et al. The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 2004;432:179–186.
CrossRef Google scholar
[117]
Luo L. Architectures of neuronal circuits. Science 2021;373:eabg7285.
CrossRef Google scholar
[118]
Luo Y, Raible D, Raper JA. Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 1993;75:217–227.
CrossRef Google scholar
[119]
Ly A, Nikolaev A, Suresh G et al. DSCAM is a netrin receptor that collaborates with DCC in mediating turning responses to netrin-1. Cell 2008;133:1241–1254.
CrossRef Google scholar
[120]
Lyuksyutova AI, Lu CC, Milanesio N et al. Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science 2003;302:1984–1988.
CrossRef Google scholar
[121]
Mann F, Ray S, Harris W et al. Topographic mapping in dorsoventral axis of the Xenopus retinotectal system depends on signaling through ephrin-B ligands. Neuron 2002;35:461–473.
CrossRef Google scholar
[122]
Marlow R, Strickland P, Lee JS et al. SLITs suppress tumor growth in vivo by silencing Sdf1/Cxcr4 within breast epithelium. Cancer Res 2008;68:7819–7827.
CrossRef Google scholar
[123]
Matsuoka RL, Nguyen-Ba-Charvet KT, Parray A et al. Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 2011;470:259–263.
CrossRef Google scholar
[124]
McConnell RE, van Veen JE, Vidaki M et al. A requirement for filopodia extension toward Slit during Robo-mediated axon repulsion. J Cell Biol 2016;213:261–274.
CrossRef Google scholar
[125]
McLaughlin T, Torborg CL, Feller MB et al. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 2003;40:1147–1160.
CrossRef Google scholar
[126]
Mehlen P, Rabizadeh S, Snipas SJ et al. The DCC gene product induces apoptosis by a mechanisms requiring receptor proteolysis. Nature 1998;395:801–804.
CrossRef Google scholar
[127]
Mehlen P, Delloye-Bourgeois C, Chédotal A. Novel roles for Slits and netrins: axon guidance cues as anticancer targets? Nat Rev Cancer 2011;11:188–197.
CrossRef Google scholar
[128]
Mehta V, Pang KL, Rozbesky D et al. The guidance receptor plexin D1 is a mechanosensor in endothelial cells. Nature 2020;578:90–295.
CrossRef Google scholar
[129]
Meijers R, Smock RG, Zhang Y et al. Netrin synergizes signaling and adhesion through DCC. Trends Biochem Sci 2020;45:6–12.
CrossRef Google scholar
[130]
Menon S, Boyer NP, Winkle CC et al. The E3 ubiquitin ligase TRIM9 is a filopodia off switch required for netrin-dependent axon guidance. Dev Cell 2015;35:698–712.
CrossRef Google scholar
[131]
Ming GL, Song HJ, Berninger B et al. cAMP-dependent growth cone guidance by netrin-1. Neuron 1997;19:1225–1235.
CrossRef Google scholar
[132]
Ming GL, Henley J, Tessier-Lavigne M et al. Electrical activity modulates growth cone guidance by diffusible factors. Neuron 2001;29:441–452.
CrossRef Google scholar
[133]
Miyake N, Chilton J, Psatha M et al. Human CHN1 mutations hyper-activate alpha2-chimaerin and cause Duane’s retraction syndrome. Science 2008;321:839–843.
CrossRef Google scholar
[134]
Monnier PP, Sierra A, Macchi P et al. RGM is a repulsive guidance molecule for retinal axons. Nature 2002;419:392–395.
CrossRef Google scholar
[135]
Moore SW, Zhang X, Lynch CD et al. Netrin-1 attracts axons through FAK-dependent mechanotransduction. J Neurosci 2012;32:11574–11585.
CrossRef Google scholar
[136]
Moreno-Bravo JA, Roig Puiggros S, Mehlen P et al. Synergistic activity of floor-plate- and ventricular-zone-derived netrin-1 in spinal cord commissural axon guidance. Neuron 2019;101:625–634.
CrossRef Google scholar
[137]
Mori K, Sakano H. How is the olfactory map formed and interpreted in the mammalian brain? Annu Rev Neurosci 2011;34:467–499.
CrossRef Google scholar
[138]
Müller A, Homey B, Soto H et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001;410:50–56.
CrossRef Google scholar
[139]
Müller PM, Rademacher J, Bagshaw RD et al. Systems analysis of RhoGEF and RhoGAP regulatory proteins reveals spatially organized RAC1 signalling from integrin adhesions. Nat Cell Biol 2020;22:498–511.
CrossRef Google scholar
[140]
Nakashima A, Takeuchi H, Imai T et al. Agonist-independent GPCR activity regulates anterior-posterior targeting of olfactory sensory neurons. Cell 2013;154:1314–1325.
CrossRef Google scholar
[141]
Nakashima A, Ihara N, Shigeta M et al. Structured spike series specify gene expression patterns for olfactory circuit formation. Science 2019;365:eaaw5030.
CrossRef Google scholar
[142]
Napolitano V, Tamagnone L. Neuropilins controlling cancer therapy responsiveness. Int J Mol Sci 2019;20:2049.
CrossRef Google scholar
[143]
Negishi-Koga T, Shinohara M, Komatsu N et al. Suppression of bone formation by osteoclastic expression of semaphorin 4D. Nat Med 2011;17:1473–1480.
CrossRef Google scholar
[144]
Neuhaus-Follini A, Bashaw GJ. The intracellular domain of the Frazzled/DCC receptor is a transcription factor required for commissural axon guidance. Neuron 2015;87:751–763.
CrossRef Google scholar
[145]
Niftullayev S, Lamarche-Vane N. Regulators of Rho GTPases in the nervous system: molecular implication in axon guidance and neurological disorders. Int J Mol Sci 2019;20:1497.
CrossRef Google scholar
[146]
Oinuma I, Ishikawa Y, Katoh H et al. The Semaphorin 4D receptor Plexin-B1 is a GTPase activating protein for R-Ras. Science 2004;305:862–865.
CrossRef Google scholar
[147]
Onishi K, Tian RY, Feng B et al. LRRK2 mediates axon development by regulating Frizzled3 phosphorylation and growth cone-growth cone communication. Proc Natl Acad Sci USA 2020;117:18037–18048.
CrossRef Google scholar
[148]
Ordan E, Brankatschk M, Dickson B et al. Slit cleavage is essential for producing an active, stable, non-diffusible short-range signal that guides muscle migration. Development 2015;142:1431–1436.
CrossRef Google scholar
[149]
Orr BO, Fetter RD, Davis GW. Retrograde semaphorin-plexin signalling drives homeostatic synaptic plasticity. Nature 2017;550:109–113.
CrossRef Google scholar
[150]
Pasterkamp RJ. Getting neural circuits into shape with semaphorins. Nat Rev Neurosci 2012;13:605–618.
CrossRef Google scholar
[151]
Pederick DT, Lui JH, Gingrich EC et al. Reciprocal repulsions instruct the precise assembly of parallel hippocampal networks. Science 2021;372:1068–1073.
CrossRef Google scholar
[152]
Pignata A, Ducuing H, Boubakar L et al. A spatiotemporal sequence of sensitization to Slits and Semaphorins orchestrates commissural axon navigation. Cell Rep 2019;29:347–362.
CrossRef Google scholar
[153]
Pinho AV, Van Bulck M, Chantrill L et al. ROBO2 is a stroma suppressor gene in the pancreas and acts via TGF-β signalling. Nat Commun 2018;9:5083.
CrossRef Google scholar
[154]
Polleux F, Morrow T, Ghosh A. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 2000;404:567–573.
CrossRef Google scholar
[155]
Poon VY, Klassen MP, Shen K. UNC-6/netrin and its receptor UNC-5 locally exclude presynaptic components from dendrites. Nature 2008;455:669–673.
CrossRef Google scholar
[156]
Rama N, Dubrac A, Mathivet T et al. Slit2 signaling through Robo1 and Robo2 is required for retinal neovascularization. Nat Med 2015;21:483–491.
CrossRef Google scholar
[157]
Ramirez-Suarez NJ, Belalcazar HM, Salazar CJ et al. Axon-dependent patterning and maintenance of somatosensory dendritic arbors. Dev Cell 2019;48:229–244
CrossRef Google scholar
[158]
Rashid T, Upton AL, Blentic A et al. Opposing gradients of ephrin-As and EphA7 in the superior colliculus are essential for topographic mapping in the mammalian visual system. Neuron 2005;47:57–69.
CrossRef Google scholar
[159]
Renders S, Svendsen AF, Panten J et al. Niche derived netrin-1 regulates hematopoietic stem cell dormancy via its receptor neogenin-1. Nat Commun 2021;12:608.
CrossRef Google scholar
[160]
Rhee J, Buchan T, Zukerberg L et al. Cables links Robo-bound Abl kinase to N-cadherin-bound beta-catenin to mediate Slit-induced modulation of adhesion and transcription. Nat Cell Biol 2007;9:883–892.
CrossRef Google scholar
[161]
Riccomagno MM, Hurtado A, Wang HB et al. The RacGAP β2-chimaerin selectively mediates axonal pruning in the hippocampus. Cell 2012;149:1594–1606.
CrossRef Google scholar
[162]
Robinson RA, Griffiths SC, van de Haar LL et al. Simultaneous binding of guidance cues NET1 and RGM blocks extracellular NEO1 signaling. Cell 2021;184:2103–2120
CrossRef Google scholar
[163]
Sabatier C, Plump AS, Ma L et al. The divergent Robo family protein Rig-1/Robo3 is a negative regulator of Slit responsiveness required for midline crossing by commissural axons. Cell 2004;117:157–169.
CrossRef Google scholar
[164]
Sando R, Jiang X, Südhof TC. Latrophilin GPCRs direct synapse specificity by coincident binding of FLRTs and teneurins. Science 2019;363:eaav7969.
CrossRef Google scholar
[165]
Sanes JR, Zipursky SL. Synaptic specificity, recognition molecules, and assembly of neural circuits. Cell 2020;181:536–556.
CrossRef Google scholar
[166]
Schmitt AM, Shi J, Wolf AM et al. Wnt-Ryk signalling mediates medial-lateral retinotectal topographic mapping. Nature 2006;439:31–37.
CrossRef Google scholar
[167]
Seeger M, Tear G, Ferres-Marco D et al. Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 1993;10:409–426.
CrossRef Google scholar
[168]
Seiradake E, del Toro D, Nagel D et al. FLRT structure: balancing repulsion and cell adhesion in cortical and vascular development. Neuron 2014;84:370–385.
CrossRef Google scholar
[169]
Serafini T, Kennedy TE, Galko MJ et al. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 1994;78:409–424.
CrossRef Google scholar
[170]
Serini G, Valdembri D, Zanivan S et al. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 2003;424:391–397.
CrossRef Google scholar
[171]
Shelly M, Cancedda L, Lim BK et al. Semaphorin3A regulates neuronal polarization by suppressing axon formation and promoting dendrite growth. Neuron 2011;71:433–446.
CrossRef Google scholar
[172]
Shirasaki R, Katsumata R, Murakami F. Change in chemoattractant responsiveness of developing axons at an intermediate target. Science 1998;279:105–107.
CrossRef Google scholar
[173]
Sigismund S, Lanzetti L, Scita G et al. Endocytosis in the context-dependent regulation of individual and collective cell properties. Nat Rev Mol Cell Biol 2021;22:625–643.
CrossRef Google scholar
[174]
Soker S, Takashima S, Miao HQ et al. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998;92:735–745.
CrossRef Google scholar
[175]
Song HJ, Ming GL, He ZG et al. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 1998;281:1515–1518.
CrossRef Google scholar
[176]
Sperry RW. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci USA 1963;50:703–710.
CrossRef Google scholar
[177]
Srour M, Riviere JB, Pham JMT et al. Mutations in DCC cause congenital mirror movements. Science 2010;328:592.
CrossRef Google scholar
[178]
Stein E, Tessier-Lavigne M. Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 2001;291:1928–1938.
CrossRef Google scholar
[179]
Südhof TC. Synaptic neurexin complexes: A molecular code for the logic of neural circuits. Cell 2017;171:745–769.
CrossRef Google scholar
[180]
Südhof TC. The cell biology of synapse formation. J Cell Biol 2021;22:e202103052.
CrossRef Google scholar
[181]
Sun D, Tan ZB, Sun XD et al. Hippocampal astrocytic neogenin regulating glutamate uptake, a critical pathway for preventing epileptic response. Proc Natl Acad Sci USA 2021;118:e2022921118.
CrossRef Google scholar
[182]
Sun LO, Jiang Z, Rivlin-Etzion M et al. On and off retinal circuit assembly by divergent molecular mechanisms. Science 2013;342:1241974.
CrossRef Google scholar
[183]
Suzuki K, Kumanogoh A, Kikutani H. Semaphorins and their receptors in immune cell interactions. Nat Immunol 2008;9:17–23.
CrossRef Google scholar
[184]
Takeuchi H, Inokuchi K, Aoki M et al. Sequential arrival and graded secretion of Sema3F by olfactory neuron axons specify map topography at the bulb. Cell 2010;141:1056–1067.
CrossRef Google scholar
[185]
Tamagnone L, Artigiani S, Chen H et al. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 1999;99:71–80.
CrossRef Google scholar
[186]
Tavora B, Mederer T, Wessel KJ et al. Tumoural activation of TLR3-SLIT2 axis in endothelium drives metastasis. Nature 2020;586:299–304.
CrossRef Google scholar
[187]
Terman JR, Mao T, Pasterkamp RJ et al. MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell 2002;109:887–900.
CrossRef Google scholar
[188]
Tessier-Lavigne M, Placzek M, Lumsden AG et al. Chemotropic guidance of developing axons in the mammalian central nervous system. Nature 1988;336:775–778.
CrossRef Google scholar
[189]
Tessier-Lavigne M, Goodman CS. The molecular biology of axon guidance. Science 1996;274:1123–1133.
CrossRef Google scholar
[190]
Toledano S, Nir-Zvi I, Engelman R et al. Class-3 semaphorins and their receptors: potent multifunctional modulators of tumor progression. Int J Mol Sci 2019;20:556.
CrossRef Google scholar
[191]
Tseng RC, Lee SH, Hsu HS et al. SLIT2 attenuation during lung cancer progression deregulates beta-catenin and E-cadherin and associates with poor prognosis. Cancer Res 2010;70:543–551.
CrossRef Google scholar
[192]
Turrigiano GG. The dialectic of Hebb and homeostasis. Phil. Trans. R. Soc. B 2017;372:20160258.
CrossRef Google scholar
[193]
Twigg SR, Kan R, Babbs C et al. Mutations of ephrin-B1 (EFNB1), a marker of tissue boundary formation, cause craniofrontonasal syndrome. Proc Natl Acad Sci USA 2004;101:8652–8657.
CrossRef Google scholar
[194]
Uesaka N, Uchigashima M, Mikuni T et al. Retrograde semaphorin signaling regulates synapse elimination in the developing mouse brain. Science 2014;344:1020–1023.
CrossRef Google scholar
[195]
Van Battum EY, Brignani S, Pasterkamp RJ. Axon guidance proteins in neurological disorders. Lancet Neurol 2015;14:532–546.
CrossRef Google scholar
[196]
van der Zee YY, Lardner CK, Parise EM et al. Sex-specific role for SLIT1 in regulating stress susceptibility. Biol Psychiatry 2022;91:81–91.
CrossRef Google scholar
[197]
Van Hoecke A, Schoonaert L, Lemmens R et al. EPHA4 is a disease modifier of amyotrophic lateral sclerosis in animal models and in humans. Nat Med 2012;18:1418–1422.
CrossRef Google scholar
[198]
Vitriol EA, Zheng JQ. Growth cone travel in space and time: the cellular ensemble of cytoskeleton, adhesion, and membrane. Neuron 2012;73:1068–1081.
CrossRef Google scholar
[199]
Walter J, Henke-Fahle S, Bonhoeffer F. Avoidance of posterior tectal membranes by temporal retinal axons. Development 1987;101:909–913.
CrossRef Google scholar
[200]
Wang B, Xiao Y, Ding BB et al. Induction of tumor angiogenesis by Slit-Robo signaling and inhibition of cancer growth by blocking Robo activity. Cancer Cell 2003;4:19–29.
CrossRef Google scholar
[201]
Wang F, Chen X, Cheng H et al. MICAL2PV suppresses the formation of tunneling nanotubes and modulates mitochondrial trafficking. EMBO Rep 2021;22:e52006.
CrossRef Google scholar
[202]
Wang HU, Chen ZF, Anderson DJ. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 1998;93:741–753.
CrossRef Google scholar
[203]
Wang J, Miao Y, Wicklein R et al. RTN4/NoGo-receptor binding to BAI adhesion-GPCRs regulates neuronal development. Cell 2021;184:5869–5885
CrossRef Google scholar
[204]
Wang KH, Brose K, Arnott D et al. Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 1999;96:771–784.
CrossRef Google scholar
[205]
Wang Q, Chiu SL, Koropouli E et al. Neuropilin-2/PlexinA3 receptors associate with GluA1 and mediate Sema3F-dependent homeostatic scaling in cortical neurons. Neuron 2017;96:1084–1098
CrossRef Google scholar
[206]
Wang X, Zhou TN, Maynard GD et al. Nogo receptor decoy promotes recovery and corticospinal growth in non-human primate spinal cord injury. Brain 2020;143:1697–1713.
CrossRef Google scholar
[207]
Wang Y, Nakayama M, Pitulescu ME et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 2010;465:483–486.
CrossRef Google scholar
[208]
Wetzel-Smith MK, Hunkapiller J, Bhangale TR et al. A rare mutation in UNC5C predisposes to late-onset Alzheimer’s disease and increases neuronal cell death. Nat Med 2014;20:1452–1457.
CrossRef Google scholar
[209]
Whitford KL, Marillat V, Stein E et al. Regulation of cortical dendrite development by Slit-Robo interactions. Neuron 2002;33:47–61.
CrossRef Google scholar
[210]
Williams ME, Lu XW, McKenna WL et al. UNC5A promotes neuronal apoptosis during spinal cord development independent of netrin-1. Nat Neurosci 2006;9:996–998.
CrossRef Google scholar
[211]
Wilson BD, Ii M, Park KW et al. Netrins promote developmental and therapeutic angiogenesis. Science 2006;313:640–644.
CrossRef Google scholar
[212]
Winter CC, He Z, Jacobi A. Axon regeneration: a subcellular extension in multiple dimensions. Cold Spring Harb Perspect Biol 2021:a040923.
CrossRef Google scholar
[213]
Wong K, Ren XR, Huang YZ et al. Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 2001;107:209–221.
CrossRef Google scholar
[214]
Woo J, Kwon SK, Kim E. The NGL family of leucine-rich repeat-containing synaptic adhesion molecules. Mol Cell Neurosci 2009;42:1–10.
CrossRef Google scholar
[215]
Worzfeld T, Offermanns S. Semaphorins and plexins as therapeutic targets. Nat Rev Drug Discov 2014;13:603–621.
CrossRef Google scholar
[216]
Wu H, Barik A, Lu YS et al. Slit2 as a β-catenin/Ctnnb1-dependent retrograde signal for presynaptic differentiation. Elife 2015;4:e07266.
CrossRef Google scholar
[217]
Wu JY, Feng LL, Park HT et al. The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature 2001;410:948–952.
CrossRef Google scholar
[218]
Wu W, Wong K, Chen JH et al. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 1999;400:331–336.
CrossRef Google scholar
[219]
Wu Z, Makihara S, Yam PT et al. Long-range guidance of spinal commissural axons by netrin1 and Sonic Hedgehog from midline floor plate cells. Neuron 2019;101:635–647.
CrossRef Google scholar
[220]
Xu K, Wu ZH, Renier N et al. Structures of netrin-1 bound to two receptors provide insight into its axon guidance mechanism. Science 2014;344:1275–1279.
CrossRef Google scholar
[221]
Xu S, Liu YQ, Li XL et al. The binding of DCC-P3 motif and FAK-FAT domain mediates the initial step of netrin-1/DCC signaling for axon attraction. Cell Discov 2018;4:8.
CrossRef Google scholar
[222]
Yamagishi S, Hampel F, Hata K et al. FLRT2 and FLRT3 act as repulsive guidance cues for Unc5-positive neurons. EMBO J 2011;30:2920–2933.
CrossRef Google scholar
[223]
Yang L, Bashaw GJ. Son of sevenless directly links the Robo receptor to rac activation to control axon repulsion at the midline. Neuron 2006;52:595–607.
CrossRef Google scholar
[224]
Yebra M, Montgomery AMP, Diaferia GR et al. Recognition of the neural chemoattractant Netrin-1 by integrins alpha6beta4 and alpha3beta1 regulates epithelial cell adhesion and migration. Dev Cell 2003;5:695–707.
CrossRef Google scholar
[225]
Yi X, Li MZ, He G et al. Genetic and functional analysis reveals TENM4 contributes to schizophrenia. iScience 2021;24:103063.
CrossRef Google scholar
[226]
Yuan W, Rao Y, Babiuk RP et al. A genetic model for a central (septum transversum) congenital diaphragmatic hernia in mice lacking Slit3. Proc Natl Acad Sci USA 2003;100:5217–5222.
CrossRef Google scholar
[227]
Yuasa-Kawada J, Kinoshita-Kawada M, Wu G et al. Midline crossing and Slit responsiveness of commissural axons require USP33. Nat Neurosci 2009;12:1087–1089.
CrossRef Google scholar
[228]
Zallen JA, Yi BA, Bargmann CI. The conserved immunoglobulin superfamily member SAX-3/Robo directs multiple aspects of axon guidance in C. elegans. Cell 1998;92:217–227.
CrossRef Google scholar
[229]
Zang Y, Chaudhari K, Bashaw GJ. New insights into the molecular mechanisms of axon guidance receptor regulation and signaling. Curr Top Dev Biol 2021;142:147–196.
CrossRef Google scholar
[230]
Zelina P, Blockus H, Zagar Y et al. Signaling switch of the axon guidance receptor Robo3 during vertebrate evolution. Neuron 2014;84:1258–1272.
CrossRef Google scholar
[231]
Zhao H, Ahirwar DK, Oghumu S et al. Endothelial Robo4 suppresses breast cancer growth and metastasis through regulation of tumor angiogenesis. Mol Oncol 2016;10:272–281.
CrossRef Google scholar
[232]
Zou Y. Breaking symmetry - cell polarity signaling pathways in growth cone guidance and synapse formation. Curr Opin Neurobiol 2020a;63:77–86.
CrossRef Google scholar
[233]
Zou Y. Targeting axon guidance cues for neural circuity repair after spinal cord injury. J Cereb Blood Flow Metab 2020b;41:197–205.
CrossRef Google scholar
[234]
Zou YR, Kottmann AH, Kuroda M et al. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998;393:595–599.
CrossRef Google scholar
[235]
Zou Y, Stoeckli E, Chen H et al. Squeezing axons out of the gray matter: a role for Slit and Semaphorin proteins from midline and ventral spinal cord. Cell 2000;102:363–375.
CrossRef Google scholar

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