1932

Abstract

Abnormalities in cranial motor nerve development cause paralytic strabismus syndromes, collectively referred to as congenital cranial dysinnervation disorders, in which patients cannot fully move their eyes. These disorders can arise through one of two mechanisms: () defective motor neuron specification, usually by loss of a transcription factor necessary for brainstem patterning, or () axon growth and guidance abnormalities of the oculomotor, trochlear, and abducens nerves. This review focuses on our current understanding of axon guidance mechanisms in the cranial motor nerves and how disease-causing mutations disrupt axon targeting. Abnormalities of axon growth and guidance are often limited to a single nerve or subdivision, even when the causative gene is ubiquitously expressed. Additionally, when one nerve is absent, its normal target muscles attract other motor neurons. Study of these disorders highlights the complexities of axon guidance and how each population of neurons uses a unique but overlapping set of axon guidance pathways.

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2021-09-15
2024-04-23
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Literature Cited

  1. Abe P, Molnar Z, Tzeng YS, Lai DM, Arnold SJ, Stumm R 2015. Intermediate progenitors facilitate intracortical progression of thalamocortical axons and interneurons through CXCL12 chemokine signaling. J. Neurosci 35:13053–63
    [Google Scholar]
  2. Abe P, Mueller W, Schutz D, MacKay F, Thelen M et al. 2014. CXCR7 prevents excessive CXCL12-mediated downregulation of CXCR4 in migrating cortical interneurons. Development 141:1857–63
    [Google Scholar]
  3. Accogli A, Calabretta S, St-Onge J, Boudrahem-Addour N, Dionne-Laporte A et al. 2019.. A De novo pathogenic variants in N-cadherin cause a syndromic neurodevelopmental disorder with corpus collosum, axon, cardiac, ocular, and genital defects. Am. J. Hum. Genet 105:854–68
    [Google Scholar]
  4. Al-Baradie R, Yamada K, St. Hilaire C, Chan WM, Andrews C et al. 2002. Duane radial ray syndrome (Okihiro syndrome) maps to 20q13 and results from mutations in SALL4, a new member of the SAL family. Am. J. Hum. Genet 71:1195–99
    [Google Scholar]
  5. Asakawa K, Kawakami K 2018. Protocadherin-mediated cell repulsion controls the central topography and efferent projections of the abducens nucleus. Cell Rep 24:1562–72
    [Google Scholar]
  6. Astick M, Tubby K, Mubarak WM, Guthrie S, Price SR 2014. Central topography of cranial motor nuclei controlled by differential cadherin expression. Curr. Biol 24:2541–47
    [Google Scholar]
  7. Bai G, Pfaff SL 2011. Protease regulation: the yin and yang of neural development and disease. Neuron 72:9–21
    [Google Scholar]
  8. Barry BJ, Whitman MC, Hunter DG, Engle EC 1993. Duane syndrome. GeneReviews MP Adam, HH Ardinger, RA Pagon, SE Wallace, LJH Bean et al. Seattle: Univ. Wash https://www.ncbi.nlm.nih.gov/books/NBK1190/
    [Google Scholar]
  9. Beg AA, Sommer JE, Martin JH, Scheiffele P 2007. α2-Chimaerin is an essential EphA4 effector in the assembly of neuronal locomotor circuits. Neuron 55:768–78
    [Google Scholar]
  10. Bianchi S, van Riel WE, Kraatz SH, Olieric N, Frey D et al. 2016. Structural basis for misregulation of kinesin KIF21A autoinhibition by CFEOM1 disease mutations. Sci. Rep 6:30668
    [Google Scholar]
  11. Bjorke B, Shoja-Taheri F, Kim M, Robinson GE, Fontelonga T et al. 2016. Contralateral migration of oculomotor neurons is regulated by Slit/Robo signaling. Neural Dev 11:18
    [Google Scholar]
  12. Boldajipour B, Mahabaleshwar H, Kardash E, Reichman-Fried M, Blaser H et al. 2008. Control of chemokine-guided cell migration by ligand sequestration. Cell 132:463–73
    [Google Scholar]
  13. Bosley TM, Oystreck DT, Robertson RL, al Awad A, Abu-Amero K, Engle EC. 2006. Neurological features of congenital fibrosis of the extraocular muscles type 2 with mutations in PHOX2A. Brain 129:2363–74
    [Google Scholar]
  14. Bosley TM, Salih MA, Jen JC, Lin DD, Oystreck D et al. 2005. Neurologic features of horizontal gaze palsy and progressive scoliosis with mutations in ROBO3. Neurology 64:1196–203
    [Google Scholar]
  15. Burgess RW, Jucius TJ, Ackerman SL. 2006. Motor axon guidance of the mammalian trochlear and phrenic nerves: dependence on the netrin receptor Unc5c and modifier loci. J. Neurosci. 26:5756–66
    [Google Scholar]
  16. Cederquist GY, Luchniak A, Tischfield MA, Peeva M, Song Y et al. 2012. An inherited TUBB2B mutation alters a kinesin-binding site and causes polymicrogyria, CFEOM and axon dysinnervation. Hum. Mol. Genet. 21:5484–99
    [Google Scholar]
  17. Chan WM, Andrews C, Dragan L, Fredrick D, Armstrong L et al. 2007. Three novel mutations in KIF21A highlight the importance of the third coiled-coil stalk domain in the etiology of CFEOM1. BMC Genet 8:26
    [Google Scholar]
  18. Chen H, Bagri A, Zupicich JA, Zou Y, Stoeckli E et al. 2000. Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 25:43–56
    [Google Scholar]
  19. Chen H, Chedotal A, He Z, Goodman CS, Tessier-Lavigne M. 1997. 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 19:547–59
    [Google Scholar]
  20. Cheng L, Desai J, Miranda CJ, Duncan JS, Qiu W et al. 2014. Human CFEOM1 mutations attenuate KIF21A autoinhibition and cause oculomotor axon stalling. Neuron 82:334–49
    [Google Scholar]
  21. Chew S, Balasubramanian R, Chan WM, Kang PB, Andrews C et al. 2013. A novel syndrome caused by the E410K amino acid substitution in the neuronal β-tubulin isotype 3. Brain 136:522–35
    [Google Scholar]
  22. Chilton JK, Guthrie S 2003. Cranial expression of class 3 secreted semaphorins and their neuropilin receptors. Dev. Dyn. 228:726–33
    [Google Scholar]
  23. Clark C, Austen O, Poparic I, Guthrie S 2013. α2-Chimaerin regulates a key axon guidance transition during development of the oculomotor projection. J. Neurosci. 33:16540–51
    [Google Scholar]
  24. Colamarino SA, Tessier-Lavigne M. 1995. The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81:621–29
    [Google Scholar]
  25. Cordes SP, Barsh GS. 1994. The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell 79:1025–34
    [Google Scholar]
  26. Demer JL, Clark RA, Engle EC. 2005. Magnetic resonance imaging evidence for widespread orbital dysinnervation in congenital fibrosis of extraocular muscles due to mutations in KIF21A. Investig. Ophthalmol. Vis. Sci. 46:530–39
    [Google Scholar]
  27. Demer JL, Clark RA, Lim KH, Engle EC. 2007. Magnetic resonance imaging evidence for widespread orbital dysinnervation in dominant Duane's retraction syndrome linked to the DURS2 locus. Investig. Ophthalmol. Vis. Sci. 48:194–202
    [Google Scholar]
  28. Demer JL, Clark RA, Tischfield MA, Engle EC. 2010. Evidence of an asymmetrical endophenotype in congenital fibrosis of extraocular muscles type 3 resulting from TUBB3 mutations. Investig. Ophthalmol. Vis. Sci. 51:4600–11
    [Google Scholar]
  29. Desai J, Velo MP, Yamada K, Overman LM, Engle EC. 2012. Spatiotemporal expression pattern of KIF21A during normal embryonic development and in congenital fibrosis of the extraocular muscles type 1 (CFEOM1). Gene Expr. Patterns 12:180–88
    [Google Scholar]
  30. Di Gioia SA, Shaaban S, Tuysuz B, Elcioglu NH, Chan WM et al. 2018. Recessive MYF5 mutations cause external ophthalmoplegia, rib, and vertebral anomalies. Am. J. Hum. Genet. 103:115–24
    [Google Scholar]
  31. Dieterich K, Quijano-Roy S, Monnier N, Zhou J, Faure J et al. 2013. The neuronal endopeptidase ECEL1 is associated with a distinct form of recessive distal arthrogryposis. Hum. Mol. Genet. 22:1483–92
    [Google Scholar]
  32. Dun XP, Bandeira de Lima T, Allen J, Geraldo S, Gordon-Weeks P, Chilton JK 2012. Drebrin controls neuronal migration through the formation and alignment of the leading process. Mol. Cell Neurosci. 49:341–50
    [Google Scholar]
  33. Easter SS Jr., Ross LS, Frankfurter A. 1993. Initial tract formation in the mouse brain. J. Neurosci. 13:285–99
    [Google Scholar]
  34. Eichmann A, Grapin-Botton A, Kelly L, Graf T, Le Douarin NM, Sieweke M 1997. The expression pattern of the mafB/kr gene in birds and mice reveals that the kreisler phenotype does not represent a null mutant. Mech. Dev. 65:111–22
    [Google Scholar]
  35. Engle EC. 2006. The genetic basis of complex strabismus. Pediatr. Res. 59:343–48
    [Google Scholar]
  36. Engle EC, Goumnerov BC, McKeown CA, Schatz M, Johns DR et al. 1997. Oculomotor nerve and muscle abnormalities in congenital fibrosis of the extraocular muscles. Ann. Neurol. 41:314–25
    [Google Scholar]
  37. Fazeli W, Herkenrath P, Stiller B, Neugebauer A, Fricke J et al. 2017. A TUBB6 mutation is associated with autosomal dominant non-progressive congenital facial palsy, bilateral ptosis and velopharyngeal dysfunction. Hum. Mol. Genet. 26:4055–66
    [Google Scholar]
  38. Feiner L, Webber AL, Brown CB, Lu MM, Jia L et al. 2001. Targeted disruption of semaphorin 3C leads to persistent truncus arteriosus and aortic arch interruption. Development 128:3061–70
    [Google Scholar]
  39. Ferrario JE, Baskaran P, Clark C, Hendry A, Lerner O et al. 2012. Axon guidance in the developing ocular motor system and Duane retraction syndrome depends on Semaphorin signaling via alpha2-chimaerin. PNAS 109:14669–74
    [Google Scholar]
  40. Friocourt F, Chedotal A. 2017. The Robo3 receptor, a key player in the development, evolution, and function of commissural systems. Dev. Neurobiol. 77:876–90
    [Google Scholar]
  41. Giger RJ, Cloutier JF, Sahay A, Prinjha RK, Levengood DV et al. 2000. Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 25:29–41
    [Google Scholar]
  42. Graeber CP, Hunter DG, Engle EC. 2013. The genetic basis of incomitant strabismus: consolidation of the current knowledge of the genetic foundations of disease. Semin. Ophthalmol. 28:427–37
    [Google Scholar]
  43. Greaney MR, Privorotskiy AE, D'Elia KP, Schoppik D 2017. Extraocular motoneuron pools develop along a dorsoventral axis in zebrafish, Daniorerio. J. Comp. Neurol. 525:65–78
    [Google Scholar]
  44. Guerrini R, Mei D, Cordelli DM, Pucatti D, Franzoni E, Parrini E. 2012. Symmetric polymicrogyria and pachygyria associated with TUBB2B gene mutations. Eur. J. Hum. Genet. 20:995–98
    [Google Scholar]
  45. Hammond R, Vivancos V, Naeem A, Chilton J, Mambetisaeva E et al. 2005. Slit-mediated repulsion is a key regulator of motor axon pathfinding in the hindbrain. Development 132:4483–95
    [Google Scholar]
  46. Hotchkiss MG, Miller NR, Clark AW, Green WR. 1980. Bilateral Duane's retraction syndrome. A clinical-pathologic case report. Arch. Ophthalmol. 98:870–74
    [Google Scholar]
  47. Huang H, Shao Q, Qu C, Yang T, Dwyer T, Liu G. 2015. Coordinated interaction of Down syndrome cell adhesion molecule and deleted in colorectal cancer with dynamic TUBB3 mediates Netrin-1-induced axon branching. Neuroscience 293:109–22
    [Google Scholar]
  48. Huang H, Yang T, Shao Q, Majumder T, Mell K, Liu G. 2018. Human TUBB3 mutations disrupt netrin attractive signaling. Neuroscience 374:155–71
    [Google Scholar]
  49. Huber A. 1974. Electrophysiology of the retraction syndromes. Br. J. Ophthalmol. 58:293–300
    [Google Scholar]
  50. 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. 26:509–63
    [Google Scholar]
  51. Huettl RE, Huber AB. 2011. Cranial nerve fasciculation and Schwann cell migration are impaired after loss of Npn-1. Dev. Biol. 359:230–41
    [Google Scholar]
  52. Iwasato T, Katoh H, Nishimaru H, Ishikawa Y, Inoue H et al. 2007. Rac-GAP α-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell 130:742–53
    [Google Scholar]
  53. Jaglin XH, Poirier K, Saillour Y, Buhler E, Tian G et al. 2009. Mutations in the β-tubulin gene TUBB2B result in asymmetrical polymicrogyria. Nat. Genet. 41:746–52
    [Google Scholar]
  54. Jen JC, Chan WM, Bosley TM, Wan J, Carr JR et al. 2004. Mutations in a human ROBO gene disrupt hindbrain axon pathway crossing and morphogenesis. Science 304:1509–13
    [Google Scholar]
  55. Kakinuma N, Kiyama R. 2009. A major mutation of KIF21A associated with congenital fibrosis of the extraocular muscles type 1 (CFEOM1) enhances translocation of Kank1 to the membrane. Biochem. Biophys. Res. Commun. 386:639–44
    [Google Scholar]
  56. Kalil K, Szebenyi G, Dent EW. 2000. Common mechanisms underlying growth cone guidance and axon branching. J. Neurobiol. 44:145–58
    [Google Scholar]
  57. Khan AO, Al-Mesfer S. 2015. Recessive COL25A1 mutations cause isolated congenital ptosis or exotropic Duane syndrome with synergistic divergence. J. AAPOS 19:463–65
    [Google Scholar]
  58. Khan AO, Almutlaq M, Oystreck DT, Engle EC, Abu-Amero K, Bosley T. 2014a. Retinal dysfunction in patients with congenital fibrosis of the extraocular muscles type 2. Ophthalmic Genet 37:130–36
    [Google Scholar]
  59. Khan AO, Shaheen R, Alkuraya FS. 2014b. The ECEL1-related strabismus phenotype is consistent with congenital cranial dysinnervation disorder. J. AAPOS 18:362–67
    [Google Scholar]
  60. Kim FA, Sing A, Kaneko T, Bieman M, Stallwood N et al. 2005. The vHNF1 homeodomain protein establishes early rhombomere identity by direct regulation of Kreisler expression. Mech. Dev. 122:1300–9
    [Google Scholar]
  61. Kim JH, Hwang JM. 2010. Absence of the trochlear nerve in patients with superior oblique hypoplasia. Ophthalmology 117:2208–13.e2
    [Google Scholar]
  62. Kohlhase J, Heinrich M, Schubert L, Liebers M, Kispert A et al. 2002. Okihiro syndrome is caused by SALL4 mutations. Hum. Mol. Genet. 11:2979–87
    [Google Scholar]
  63. Latremoliere A, Cheng L, DeLisle M, Wu C, Chew S et al. 2018. Neuronal-specific TUBB3 is not required for normal neuronal function but is essential for timely axon regeneration. Cell Rep 24:1865–79.e9
    [Google Scholar]
  64. Lee DS, Yang HK, Kim JH, Hwang JM. 2014. Morphometry of the trochlear nerve and superior oblique muscle volume in congenital superior oblique palsy. Investig. Ophthalmol. Vis. Sci. 55:8571–75
    [Google Scholar]
  65. Lee KH, Lee JS, Lee D, Seog DH, Lytton J et al. 2012. KIF21A-mediated axonal transport and selective endocytosis underlie the polarized targeting of NCKX2. J. Neurosci. 32:4102–17
    [Google Scholar]
  66. Lerner O, Davenport D, Patel P, Psatha M, Lieberam I, Guthrie S 2010. Stromal cell-derived factor-1 and hepatocyte growth factor guide axon projections to the extraocular muscles. Dev. Neurobiol. 70:549–64
    [Google Scholar]
  67. Lewellis SW, Nagelberg D, Subedi A, Staton A, LeBlanc M et al. 2013. Precise SDF1-mediated cell guidance is achieved through ligand clearance and microRNA-mediated decay. J. Cell Biol. 200:337–55
    [Google Scholar]
  68. Li M, Ransohoff RM. 2008. Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog. Neurobiol. 84:116–31
    [Google Scholar]
  69. Li XF, Kiedrowski L, Tremblay F, Fernandez FR, Perizzolo M et al. 2006. Importance of K+-dependent Na+/Ca2+-exchanger 2, NCKX2, in motor learning and memory. J. Biol. Chem. 281:6273–82
    [Google Scholar]
  70. Lieberam I, Agalliu D, Nagasawa T, Ericson J, Jessell TM. 2005. A Cxcl12-Cxcr4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron 47:667–79
    [Google Scholar]
  71. Liu Q, Bhattarai S, Wang N, Sochacka-Marlowe A. 2015. Differential expression of protocadherin-19, protocadherin-17, and cadherin-6 in adult zebrafish brain. J. Comp. Neurol. 523:1419–42
    [Google Scholar]
  72. Liu Q, Chen Y, Pan JJ, Murakami T. 2009. Expression of protocadherin-9 and protocadherin-17 in the nervous system of the embryonic zebrafish. Gene Expr. Patterns 9:490–96
    [Google Scholar]
  73. Lopata MA, Cleveland DW. 1987. In vivo microtubules are copolymers of available β-tubulin isotypes: localization of each of six vertebrate β-tubulin isotypes using polyclonal antibodies elicited by synthetic peptide antigens. J. Cell Biol. 105:1707–20
    [Google Scholar]
  74. MacKinnon S, Oystreck DT, Andrews C, Chan WM, Hunter DG, Engle EC. 2014. Diagnostic distinctions and genetic analysis of patients diagnosed with Moebius syndrome. Ophthalmology 121:1461–68
    [Google Scholar]
  75. Marillat V, Sabatier C, Failli V, Matsunaga E, Sotelo C et al. 2004. The slit receptor Rig-1/Robo3 controls midline crossing by hindbrain precerebellar neurons and axons. Neuron 43:69–79
    [Google Scholar]
  76. Marszalek JR, Weiner JA, Farlow SJ, Chun J, Goldstein LS 1999. Novel dendritic kinesin sorting identified by different process targeting of two related kinesins: KIF21A and KIF21B. J. Cell Biol. 145:469–79
    [Google Scholar]
  77. Mason C, Erskine L. 2000. Growth cone form, behavior, and interactions in vivo: retinal axon pathfinding as a model. J. Neurobiol. 44:260–70
    [Google Scholar]
  78. Masuda T, Taniguchi M. 2016. Contribution of semaphorins to the formation of the peripheral nervous system in higher vertebrates. Cell Adhes. Migr. 10:593–603
    [Google Scholar]
  79. McMillin MJ, Below JE, Shively KM, Beck AE, Gildersleeve HI et al. 2013. Mutations in ECEL1 cause distal arthrogryposis type 5D. Am. J. Hum. Genet. 92:150–56
    [Google Scholar]
  80. Michalak SM, Whitman MC, Park JG, Tischfield MA, Nguyen EH, Engle EC. 2017. Ocular motor nerve development in the presence and absence of extraocular muscle. Investig. Ophthalmol. Vis. Sci. 58:2388–96
    [Google Scholar]
  81. Miller NR, Kiel SM, Green WR, Clark AW. 1982. Unilateral Duane's retraction syndrome (Type 1). Arch. Ophthalmol. 100:1468–72
    [Google Scholar]
  82. Minoura I, Takazaki H, Ayukawa R, Saruta C, Hachikubo Y et al. 2016. Reversal of axonal growth defects in an extraocular fibrosis model by engineering the kinesin-microtubule interface. Nat. Commun. 7:10058
    [Google Scholar]
  83. Miyake N, Chilton J, Psatha M, Cheng L, Andrews C et al. 2008. Human CHN1 mutations hyperactivate α2-chimaerin and cause Duane's retraction syndrome. Science 321:839–43
    [Google Scholar]
  84. Miyake N, Demer JL, Shaaban S, Andrews C, Chan WM et al. 2011. Expansion of the CHN1 strabismus phenotype. Investig. Ophthalmol. Vis. Sci. 52:6321–28
    [Google Scholar]
  85. Munezane H, Oizumi H, Wakabayashi T, Nishio S, Hirasawa T et al. 2019. Roles of collagen XXV and its putative receptors PTPσ/δ in intramuscular motor innervation and congenital cranial dysinnervation disorder. Cell Rep 29:4362–76.e6
    [Google Scholar]
  86. Nagata K, Kiryu-Seo S, Kiyama H. 2006. Localization and ontogeny of damage-induced neuronal endopeptidase mRNA-expressing neurons in the rat nervous system. Neuroscience 141:299–310
    [Google Scholar]
  87. Nagata K, Kiryu-Seo S, Maeda M, Yoshida K, Morita T, Kiyama H. 2010. Damage-induced neuronal endopeptidase is critical for presynaptic formation of neuromuscular junctions. J. Neurosci. 30:6954–62
    [Google Scholar]
  88. Nagata K, Kiryu-Seo S, Tamada H, Okuyama-Uchimura F, Kiyama H, Saido TC. 2016. ECEL1 mutation implicates impaired axonal arborization of motor nerves in the pathogenesis of distal arthrogryposis. Acta Neuropathol 132:111–26
    [Google Scholar]
  89. Nagata K, Takahashi M, Kiryu-Seo S, Kiyama H, Saido TC. 2017. Distinct functional consequences of ECEL1/DINE missense mutations in the pathogenesis of congenital contracture disorders. Acta Neuropathol. Commun. 5:83
    [Google Scholar]
  90. Nakano M, Yamada K, Fain J, Sener EC, Selleck CJ et al. 2001. Homozygous mutations in ARIX(PHOX2A) result in congenital fibrosis of the extraocular muscles type 2. Nat. Genet. 29:315–20
    [Google Scholar]
  91. Naumann U, Cameroni E, Pruenster M, Mahabaleshwar H, Raz E et al. 2010. CXCR7 functions as a scavenger for CXCL12 and CXCL11. PLOS ONE 5:e9175
    [Google Scholar]
  92. Niwa S, Takahashi H, Hirokawa N. 2013. β-Tubulin mutations that cause severe neuropathies disrupt axonal transport. EMBO J 32:1352–64
    [Google Scholar]
  93. Nugent AA, Park JG, Wei Y, Tenney AP, Gilette NM et al. 2017. Mutant α2-chimaerin signals via bidirectional ephrin pathways in Duane retraction syndrome. J. Clin. Investig. 127:1664–82
    [Google Scholar]
  94. Park JG, Tischfield MA, Nugent AA, Cheng L, Di Gioia SA et al. 2016. Loss of MAFB function in humans and mice causes Duane syndrome, aberrant extraocular muscle innervation, and inner-ear defects. Am. J. Hum. Genet. 98:1220–27
    [Google Scholar]
  95. Poirier K, Saillour Y, Bahi-Buisson N, Jaglin XH, Fallet-Bianco C et al. 2010. Mutations in the neuronal β-tubulin subunit TUBB3 result in malformation of cortical development and neuronal migration defects. Hum. Mol. Genet. 19:4462–73
    [Google Scholar]
  96. Prakash N, Puelles E, Freude K, Trumbach D, Omodei D et al. 2009. Nkx6-1 controls the identity and fate of red nucleus and oculomotor neurons in the mouse midbrain. Development 136:2545–55
    [Google Scholar]
  97. Qu C, Dwyer T, Shao Q, Yang T, Huang H, Liu G. 2013. Direct binding of TUBB3 with DCC couples netrin-1 signaling to intracellular microtubule dynamics in axon outgrowth and guidance. J. Cell Sci. 126:3070–81
    [Google Scholar]
  98. Quinn KE, Mackie DI, Caron KM. 2018. Emerging roles of atypical chemokine receptor 3 (ACKR3) in normal development and physiology. Cytokine 109:17–23
    [Google Scholar]
  99. Renier N, Schonewille M, Giraudet F, Badura A, Tessier-Lavigne M et al. 2010. Genetic dissection of the function of hindbrain axonal commissures. PLOS Biol 8:e1000325
    [Google Scholar]
  100. Romaniello R, Tonelli A, Arrigoni F, Baschirotto C, Triulzi F et al. 2012. A novel mutation in the β-tubulin gene TUBB2B associated with complex malformation of cortical development and deficits in axonal guidance. Dev. Med. Child Neurol. 54:765–69
    [Google Scholar]
  101. Sabatier C, Plump AS, Le M, Brose K, Tamada A et al. 2004. The divergent Robo family protein Rig-1/Robo3 is a negative regulator of Slit responsiveness required for midline crossing by commissural axons. Cell 117:157–69
    [Google Scholar]
  102. Sadl VS, Sing A, Mar L, Jin F, Cordes SP 2003. Analysis of hindbrain patterning defects caused by the kreislerenu mutation reveals multiple roles of Kreisler in hindbrain segmentation. Dev. Dyn. 227:134–42
    [Google Scholar]
  103. Sahay A, Molliver ME, Ginty DD, Kolodkin AL. 2003. Semaphorin 3F is critical for development of limbic system circuitry and is required in neurons for selective CNS axon guidance events. J. Neurosci. 23:6671–80
    [Google Scholar]
  104. Sakaki-Yumoto M, Kobayashi C, Sato A, Fujimura S, Matsumoto Y et al. 2006. The murine homolog of SALL4, a causative gene in Okihiro syndrome, is essential for embryonic stem cell proliferation, and cooperates with Sall1 in anorectal, heart, brain and kidney development. Development 133:3005–13
    [Google Scholar]
  105. Sambasivan R, Gayraud-Morel B, Dumas G, Cimper C, Paisant S et al. 2009. Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev. Cell 16:810–21
    [Google Scholar]
  106. Sanes JR, Zipursky SL. 2020. Synaptic specificity, recognition molecules, and assembly of neural circuits. Cell 181:536–56
    [Google Scholar]
  107. Sato Y, Tsukaguchi H, Morita H, Higasa K, Tran MTN et al. 2018. A mutation in transcription factor MAFB causes Focal Segmental Glomerulosclerosis with Duane Retraction Syndrome. Kidney Int 94:396–407
    [Google Scholar]
  108. Serafini T, Colamarino SA, Leonardo ED, Wang H, Beddington R et al. 1996. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87:1001–14
    [Google Scholar]
  109. Shaaban S, Duzcan F, Yildirim C, Chan WM, Andrews C et al. 2014. Expanding the phenotypic spectrum of ECEL1-related congenital contracture syndromes. Clin. Genet. 85:562–67
    [Google Scholar]
  110. Shao Q, Yang T, Huang H, Alarmanazi F, Liu G. 2017. Uncoupling of UNC5C with polymerized TUBB3 in microtubules mediates netrin-1 repulsion. J. Neurosci. 37:5620–33
    [Google Scholar]
  111. Shao Q, Yang T, Huang H, Majumder T, Khot BA et al. 2019. Disease-associated mutations in human TUBB3 disturb netrin repulsive signaling. PLOS ONE 14:e0218811
    [Google Scholar]
  112. Shi L, Fu W-Y, Hung K-W, Porchetta C, Hall C et al. 2007. α2-Chimaerin interacts with EphA4 and regulates EphA4-dependent growth cone collapse. PNAS 104:16347–52
    [Google Scholar]
  113. Shinwari JM, Khan A, Awad S, Shinwari Z, Alaiya A et al. 2015. Recessive mutations in COL25A1 are a cause of congenital cranial dysinnervation disorder. Am. J. Hum. Genet. 96:147–52
    [Google Scholar]
  114. Tanaka T, Wakabayashi T, Oizumi H, Nishio S, Sato T et al. 2014. CLAC-P/collagen type XXV is required for the intramuscular innervation of motoneurons during neuromuscular development. J. Neurosci. 34:1370–79
    [Google Scholar]
  115. Taniguchi M, Yuasa S, Fujisawa H, Naruse I, Saga S et al. 1997. Disruption of semaphorinIII/D gene causes severe abnormality in peripheral nerve projection. Neuron 19:519–30
    [Google Scholar]
  116. Tischfield MA, Baris HN, Wu C, Rudolph G, Van Maldergem L et al. 2010. Human TUBB3 mutations perturb microtubule dynamics, kinesin interactions, and axon guidance. Cell 140:74–87
    [Google Scholar]
  117. Tischfield MA, Bosley TM, Salih MA, Alorainy IA, Sener EC et al. 2005. Homozygous HOXA1 mutations disrupt human brainstem, inner ear, cardiovascular and cognitive development. Nat. Genet. 37:1035–37
    [Google Scholar]
  118. Tischfield MA, Cederquist GY, Gupta ML Jr., Engle EC. 2011. Phenotypic spectrum of the tubulin-related disorders and functional implications of disease-causing mutations. Curr. Opin. Genet. Dev. 21:286–94
    [Google Scholar]
  119. Tosney KW, Landmesser LT. 1985. Growth cone morphology and trajectory in the lumbosacral region of the chick embryo. J. Neurosci. 5:2345–58
    [Google Scholar]
  120. Uchimura S, Oguchi Y, Hachikubo Y, Ishiwata S, Muto E. 2010. Key residues on microtubule responsible for activation of kinesin ATPase. EMBO J 29:1167–75
    [Google Scholar]
  121. Uchimura S, Oguchi Y, Katsuki M, Usui T, Osada H et al. 2006. Identification of a strong binding site for kinesin on the microtubule using mutant analysis of tubulin. EMBO J 25:5932–41
    [Google Scholar]
  122. Valdenaire O, Richards JG, Faull RL, Schweizer A. 1999. XCE, a new member of the endothelin-converting enzyme and neutral endopeptidase family, is preferentially expressed in the CNS. Brain Res. Mol. Brain Res. 64:211–21
    [Google Scholar]
  123. van der Vaart B, van Riel WE, Doodhi H, Kevenaar JT, Katrukha EA et al. 2013. CFEOM1-associated kinesin KIF21A is a cortical microtubule growth inhibitor. Dev. Cell 27:145–60
    [Google Scholar]
  124. Wang P, Li S, Xiao X, Guo X, Zhang Q. 2011. KIF21A novel deletion and recurrent mutation in patients with congenital fibrosis of the extraocular muscles-1. Int. J. Mol. Med. 28:973–75
    [Google Scholar]
  125. Wegmeyer H, Egea J, Rabe N, Gezelius H, Filosa A et al. 2007. EphA4-dependent axon guidance is mediated by the RacGAP α2-chimaerin. Neuron 55:756–67
    [Google Scholar]
  126. Whitman MC, Andrews C, Chan WM, Tischfield MA, Stasheff SF et al. 2016. Two unique TUBB3 mutations cause both CFEOM3 and malformations of cortical development. Am. J. Med. Genet. A 170:297–305
    [Google Scholar]
  127. Whitman MC, Engle EC. 2017. Ocular congenital cranial dysinnervation disorders (CCDDs): insights into axon growth and guidance. Hum. Mol. Genet. 26:R37–44
    [Google Scholar]
  128. Whitman MC, Miyake N, Nguyen EH, Bell JL, Matos Ruiz PM et al. 2019. Decreased ACKR3 (CXCR7) function causes oculomotor synkinesis in mice and humans. Hum. Mol. Genet. 28:3113–25
    [Google Scholar]
  129. Whitman MC, Nguyen EH, Bell JL, Tenney AP, Gelber A, Engle EC. 2018. Loss of CXCR4/CXCL12 signaling causes oculomotor nerve misrouting and development of motor trigeminal to oculomotor synkinesis. Investig. Ophthalmol. Vis. Sci. 59:5201–9
    [Google Scholar]
  130. Yamada K, Andrews C, Chan WM, McKeown CA, Magli A et al. 2003. Heterozygous mutations of the kinesin KIF21A in congenital fibrosis of the extraocular muscles type 1 (CFEOM1). Nat. Genet. 35:318–21
    [Google Scholar]
  131. Yamada K, Hunter DG, Andrews C, Engle EC. 2005. A novel KIF21A mutation in a patient with congenital fibrosis of the extraocular muscles and Marcus Gunn jaw-winking phenomenon. Arch. Ophthalmol. 123:1254–59
    [Google Scholar]
  132. Yang HK, Kim JH, Hwang JM. 2012. Congenital superior oblique palsy and trochlear nerve absence: a clinical and radiological study. Ophthalmology 119:170–77
    [Google Scholar]
  133. Zelina P, Blockus H, Zagar Y, Péres A, Friocourt F et al. 2014. Signaling switch of the axon guidance receptor Robo3 during vertebrate evolution. Neuron 84:1258–72
    [Google Scholar]
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