Molecular genetics of cranial nerve development in mouse

Nature Reviews Neuroscience

Volumn 2, Issue 9, 2001, Pages 611-623

  Cordes, Sabine P ^a  

^a MOUNT SINAI HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

VERTEBRATA;

ANIMAL; CRANIAL NERVE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HOMEOBOX; METABOLISM; MORPHOGENESIS; MOUSE; MOUSE MUTANT; PRENATAL DEVELOPMENT; REVIEW; RHOMBENCEPHALON;

ANIMALS; BODY PATTERNING; CRANIAL NERVES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; MICE; MICE, NEUROLOGIC MUTANTS; RHOMBENCEPHALON;

EID: 0035461440     PISSN: 14710048     EISSN: None     Source Type: Journal    
DOI: 10.1038/35090039     Document Type: Review

References (122)

1. Bergstrom, L. & Baker, B. B. Syndromes associated with congenital facial paralysis. Otolaryngol. Head Neck Surg. 89, 336-342 (1981).
2. Clarke, J. D. & Lumsden, A. Segmental repetition of neuronal phenotype sets in the chick embryo hindbrain. Development 118, 151-162 (1993).
3. Lumsden, A. & Keynes, R. Segmental patterns of neuronal development in the chick hindbrain. Nature 337, 424-428 (1989). This paper describes elegant cell-labelling experiments that demonstrate the compartmentaL nature of rhombomeres.
4. Orr, X. Contribution to the embryology of the lizard. J. Morphol. 1, 311-372 (1887).
5. Vaage, S. The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). Adv. Anat. Embryol. Cell Biol. 41, 1-88 (1969). This is a classic text on rhombomere development.
6. Fritzsch, B. Of mice and genes: evolution of vertebrate brain development. Brain Behav. Evol. 52, 207-217 (1998).
7. Gilland, E. & Baker, R. Conservation of neuroepithelial and mesodermal segments in the embryonic vertebrate head. Acta Anat. (Basel) 148, 110-123 (1993). References 6 and 7 describe some phylogenetic differences in hindbrain patterning.
8. Jacob, J., Hacker, A. & Guthrie, S. Mechanisms and molecules in motor neuron specification and axon pathfinding. Bioessays 23, 582-595 (2001).
9. Lumsden, A. & Krumlauf, R. Patterning the vertebrate neuraxis. Science 274, 1109-1115 (1996).
10. Guthrie, S. Patterning the hindbrain. Curr. Opin. Neurobiol. 6, 41-48 (1996).
11. Trainor, P. A. & Krumlauf, R. Patterning the cranial neural crest: hindbrain segmentation and Hox gene plasticity. Nature Rev. Neurosci. 1, 116-124 (2000).
12. Graham, A. & Lumsden, A. Interactions between rhombomeres modulate Krox20 and follistatin expression in the chick embryo hindbrain. Development 122, 473-480 (1996).
13. Guthrie, S. & Lumsden, A. Formation and regeneration of rhombomere boundaries in the developing chick hindbrain. Development 112, 221-229 (1991).
14. Deol, M. S. The abnormalities of the inner ear in kreisler mice. J. Embryol. Exp. Morphol. 12, 475-490 (1964).
15. Hertwig, P. Neue Mutationen und Koppelungsgruppen bei der Hausmaus. Z. indukt. Abstamm. Vererbungsl. 80, 220-246 (1942).
16. Murphy, P., Davidson, D. R. & Hill, R. E. Segment-specific expression of a homeobox-containing gene in the mouse hindbrain. Nature 341, 156-159 (1989).
17. Wilkinson, D. G., Bhatt, S., Cook, M., Boncinelli, E. & Krumlauf, R. Segmental expression of Hox-2 homoeobox-containing genes in the developing mouse hindbrain. Nature 341, 405-409 (1989).
18. Cappecchi, M. in Molecular Approaches to Neural Development (eds Cowan, W. M., Jessell, T. M. & Zipursky, S. L.) (Oxford Univ. Press, New York, 1997).
19. Krumlauf, R. Hox genes and pattern formation in the branchial region of the vertebrate head. Trends Genet. 9, 106-112 (1993).
20. McGinnis, W. & Krumlauf, R. Homeobox genes and axial patterning. Cell 68, 283-302 (1992).
21. Studer, M., Lumsden, A., Ariza-McNaughton, L., Bradley, A. & Krumlauf, R. Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384, 630-634 (1996).
22. Rossel, M. & Capecchi, M. R. Mice mutant for both Hoxa1 and Hoxb1 show extensive remodeling of the hindbrain and defects in craniofacial development. Development 126, 5027-5040 (1999).
23. Barrow, J. R., Stadler, H. S. & Capecchi, M. R. Roles of Hoxa1 and Hoxa2 in patterning the early hindbrain of the mouse. Development 127, 933-944 (2000).
24. Carpenter, E. M., Goddard, J. M., Chisaka, O., Manley, N. R. & Capecchi, M. R. Loss of Hox-A1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Development 118, 1063-1075 (1993).
25. Frohman, M. A., Martin, G. R., Cordes, S. P., Halamek, L. P. & Barsh, G. S. Altered rhombomere-specific gene expression and hyoid bone differentiation in the mouse segmentation mutant, kreisler (kr). Development 117, 925-936 (1993).
26. McKay, I. J. et al. The kreisler mouse: a hindbrain segmentation mutant that lacks two rhombomeres. Development 120, 2199-2211 (1994).
27. Manzanares, M. et al. The role of kreisler in segmentation during hindbrain development. Dev. Biol. 211, 220-237 (1999).
28. Cordes, S. P. & Barsh, G. S. The mouse segmentation gene kr encondes a novel basic domain-leucine zipper transcription factor. Cell 79, 1025-1034 (1994).
29. Wassarman, K. M. et al. Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function. Development 124, 2923-2934 (1997).
30. Ericson, J., Briscoe, J., Rashbass, P., Van Heyningen, V. & Jessell, T. M. Graded sonic hedgehog signaling and the specification of cell fate in the ventral neural tube. Cold Spring Harb. Symp. Quant. Biol. 62, 451-466 (1997).
31. Liem, K. F. Jr, Tremml, G. & Jessell, T. M. A role for the roof plate and its resident TGFβ-related proteins in neuronal patterning in the dorsal spinal cord. Cell 91, 127-138 (1997).
32. Yamada, T., Pfaff, S. L., Edlund, T. & Jessell, T. M. Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from notochord and floor plate. Cell 73, 673-686 (1993).
33. Briscoe, J., Pierani, A., Jessell, T. M. & Ericson, J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101, 435-445 (2000).
34. Sander, M. et al. Ventral neural patterning by Nkx homeobox genes: Nkx6.1 controls somatic motor neuron and ventral interneuron fates. Genes Dev. 14, 2134-2139 (2000).
35. Briscoe, J. et al. Homeobox gene Nkx2. 2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 398, 622-627 (1999). References 34 and 35 describe the interpretation of the Shh signal by neuronal determinants.
36. Deol, M. S. The origin of the abnormalities of the inner ear in dreher mice. J. Embryol. Exp. Morphol. 12, 727-733 (1964).
37. Millonig, J. H., Millen, K. J. & Hatten, M. E. The mouse Dreher gene Lmx1a controls formation of the roof plate in the vertebrate CNS. Nature 403, 764-769 (2000).
38. J) mouse mutant. Mech. Dev. 94, 147-156 (2000).
39. Davenne, M. et al. Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain. Neuron 22, 677-691 (1999). This study examines the integration of anteroposterior and dorsoventral positional information in Hox gene expression and neuronal specification. It examines the possible roles of Hox genes in the specification of motor neurons.
40. Ericson, J. et al. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169-180 (1997).
41. Sharma, K. et al. LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons. Cell 95, 817-628 (1998). An elegant series of transgenic and knockout experiments demonstrates that Lhx3 and Lhx4 Lim homeodomain proteins act as neuronal determinants and that a Lim homeodomain code might be of functional significance.
42. Tsuchida, T. et al. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 935-943 (1994).
43. Varela-Echavarria, A., Pfaff, S. L. & Guthrie, S. Differential expression of LIM homeobox genes among motor neuron subpopulations in the developing chick brainstem. Mol. Cell. Neurosci. 8, 242-257 (1996).
44. Pattyn, A., Hirsch, M., Goridis, C. & Brunet, J. F. Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. Development 127, 1349-1358 (2000).
45. Pata, I. et al. The transcription factor GATA3 is a downstream effector of Hoxb1 specification in rhombomere 4. Development 126, 5523-5531 (1999).
46. Nardelli, J., Thiesson, D., Fujiwara, Y., Tsai, F. Y. & Orkin, S. H. Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Dev. Biol. 210, 305-321 (1999). Here, the GATA2 and GATA3 genes are found to act downstream of Hox genes in neuronal specification.
47. Studer, M. et al. Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 125, 1025-1036 (1998).
48. Garel, S., Garcia-Dominguez, M. & Chamay, P. Control of the migratory pathway of facial branchiomotor neurones. Development 127, 5297-5307 (2000). Here, the role of the basic helix-loop-helix transcription factor in the regulation of transient gene expression patterns and FBM neuron migration is examined, and a functional link between such expression and migratory patterns is suggested.
49. Ma, Q., Chen, Z. F., Del Barco Barrantes, I., De la Pompa, J. L. & Anderson, D. J. neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 20, 469-482 (1998). Identification of neurogenin 1 as one of the few known sensory neuron determinants.
50. Erickson, S. L. et al. ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice. Development 124, 4999-5011 (1997).
51. Lee, K. F. et al. Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378, 394-398 (1995).
52. Meyer, D. & Birchmeier, C. Multiple essential functions of neuregulin in development. Nature 378, 386-390 (1995).
53. Britsch, S. et al. The ErbB2 and ErbB3 receptors and their ligand, neuregulin, are essential for development of the sympathetic nervous system. Genes Dev. 12, 1825-36 (1998).
54. Fode, C. et al. The bHLH protein NEUROGENIN2 is determination factor for epibranchial placode-derived sensory neurons. Neuron 20, 483-494 (1998). Identification of neurogenin 2 as one of the few known sensory neuron determinants.
55. Morin, X. et al. Defects in sensory and autonomic ganglia and absence of locus coeruleus in mice deficient for the homeobox gene Phox2a. Neuron 18, 411-423 (1997). With reference 65, one of a series of papers examining the intriguing role of Phox2a in mouse mutants.
56. Pattyn, A., Morin, X., Cremer, H., Goridis, C. & Brunet, J.-F. The homeobox gene Phox2b is essential for development of autonomic neural crest derivatives. Nature 399, 366-370 (1998).
57. Pattyn, A., Goridis, C. & Brunet, J. F. Specification of the central noradrenergic phenotype by the homeobox gene Phox2b. Mol. Cell. Neurosci. 15, 235-243 (2000).
58. Anderson, D. J. Lineages and transcription factors in the specification of vertebrate primary sensory neurons. Curr. Opin. Neurobiol. 9, 517-524 (1999).
59. Howad, M. J., Stanke, M., Schneider, C., Wu, X. & Rohrer, H. The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification. Development 127, 4073-4081 (2000).
60. Lo, L, Morin, X., Brunet, J. F. & Anderson, D. J. Specification of neurotransmitter identity by Phox2 proteins in neural crest stem cells. Neuron 22, 693-705 (1999).
61. Guo, S. et al. Development of noradrenergic neurons in the zebrafish hindbrain requires BMP, FGF8, and the homeodomain protein soulless/Phox2a. Neuron 24, 555-566 (1999).
62. Stanke, M. et al. The Phox2 homeodomain proteins are sufficient to promote the development of sympathetic neurons. Development 126, 4087-4094 (1999).
63. Lim, K. C. et al. Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nature Genet. 25, 209-212 (2000).
64. Guillemot, F. et al. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75, 463-476 (1993).
65. Morin, X. et al. Defects in sensory and autonomic ganglia and absence of locus coeruleus in mice deficient for the homeobox gene Phox2a. Neuron 18, 411-423 (1997).
66. Enomoto, H., Heuckeroth, R. O., Golden, J. P., Johnson, E. M. & Milbrandt, J. Development of cranial parasympathetic ganglia requires sequential actions of GDNF and neurturin. Development 127, 4877-4889 (2000).
67. Hiltunen, J. O., Laurikainen, A., Airaksinen, M. S. & Saarma, M. GDNF family receptors in the embryonic and postnatal rat heart and reduced cholinergic innervation in mice hearts lacking ret or GFRα2. Dev. Dyn. 219, 28-39 (2000).
68. Rossi, J. et al. Retarded growth and deficits in the enteric and parasympathetic nervous system in mice lacking GFRα2, a functional neurturin receptor. Neuron 22, 243-252 (1999).
69. Cacalano, G. et al. GFRα1 is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron 21, 53-62 (1998).
70. Garces, A. et al. GFRα1 is required for development of distinct subpopulations of motoneuron. J. Neurosci. 20, 4992-5000 (2000).
71. Moore, M. W. et al. Renal and neuronal abnormalities in mice lacking GDNF. Nature 382, 76-79 (1996). The first genetic evidence that GDNF acts as a survival factor for neurons.
72. Baloh, R. H. et al. Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRα3-RET receptor complex. Neuron 21, 1291-1302 (1998).
73. Milbrandt, J. et al. Persephin, a novel neurotrophic factor related to GDNF and neurturin. Neuron 20, 245-253 (1998).
74. Champagnat, J. & Fortin, G. Primordial respiratory-like rhythm generation in the vertebrate embryo. Trends Neurosci 20, 119-124 (1997). This is a review that describes well the intricacies of the respiratory centre.
75. Arniel, J. et al. Mutations of the RET-GDNF signaling pathway in Ondine's curse. Am. J. Hum. Genet. 62, 715-717 (1998).
76. Bolk, S. et al. Endothelin-3 frameshift mutation in congenital central hypoventilation syndrome. Nature Genet. 13, 395-396 (1996).
77. Ramirez, J. M., Quellmalz, U. J. & Wilken, B. Developmental changes in the hypoxic response of the hypoglossus respiratory motor output in vitro. J. Neurophysiol. 78, 383-392 (1997).
78. Jacquin, T. D. et al. Reorganization of pontine rhythmogenic neuronal networks in Krox-20 knockout mice. Neuron 17, 747-758 (1996).
79. Borday, V. Kato, F. & Champagnat, J. A ventral pontine pathway promotes rhythmic activity in the medulla of neonate mice. Neuroreport 8, 3679-3683 (1997).
80. Jacquin, T. D., Sadoc, G., Borday, V. & Champagnat, J. Pontine and medullary control of the respiratory activity in the trigeminal and facial nerves of the newborn mouse: an in vitro study. Eur. J. Neurosci. 11, 213-222 (1999).
81. Shirasawa, S. et al. Rnx deficiency results in congenital central hypoventilation. Nature Genet. 24, 287-290 (2000).
82. Rocha, B. A. et al. Increased vulnerability to cocaine in mice lacking the serotonin-1B receptor. Nature 393, 175-178 (1998).
83. 2c receptor mutant mice. Nature Genet. 16, 387-390 (1997).
84. Van Doorninck, J. H. et al. GATA-3 is involved in the development of serotonergic neurons in the caudal raphe nuclei. J. Neurosci. 19, RC12, 1-8 (1999). This is one of the few papers to examine 5-HT neuron differentiation by chimeric analyses.
85. Matise, M. P., Epstein, D. J., Park, H. L. Platt, K. A. & Joyner, A. L. Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development 125, 2759-2770 (1998).
86. Hynes, M. et al. Control of cell pattern in the neural tube by the zinc finger transcription factor and oncogene Gli-1. Neuron 19, 15-26 (1997).
87. Hynes, M. et al. The seven-transmembrane receptor smoothened cell-autonomously induces multiple ventral cell types. Nature Neurosci. 3, 41-46 (2000).
88. Mo, R. et al. Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124, 113-123 (1997).
89. Galas, J. Sequence interpretation. Making sense of the sequence. Science 291, 1232-1249 (2001).
90. Kitsukawa, T. et al. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19, 995-1005 (1997).
91. Chen, H. et al. Neuropilin-2 regulates the development of selective cranial and sensorynerves and hippocampal mossy fiber projections. Neuron 25, 43-56 (2000).
92. White, F. A. & Behar, O. The development and subsequent elimination of aberrant peripheral axon projections in Semaphorin3A null mutant mice. Dev. Boil. 225, 79-86 (2000). This work describes the ability of the defasciculation phenotype observed in E10.5 mutants to be self-corrected by E15 through unknown mechanisms.
93. Serafini, T. et al. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424 (1994).
94. Hamelin, M., Zhou, Y., Su, M. W., Scott, I. M. & Culotti, J. G. Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 364, 327-330 (1993).
95. Leung-Hagesteijn, C. et al. UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell 71, 289-299 (1992).
96. Kennedy, T. E., Serafini, T., De la Torre, J. R. & Tessier-Lavigne, M. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78, 425-435 (1994).
97. Tessier-Lavigne, M. & Goodman, C. S. The molecular biology of axon guidance. Science 274, 1123-1133 (1996).
98. Colamarino, S. A. & Tessier-Lavigne, M. The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81, 621-629 (1995).
99. Serafini, T. et al. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87, 1001-1014 (1996).
100. Brose, K. et al. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96, 795-806 (1999).
101. Wilkinson, D. G. Multiple roles of EPH receptors and ephrins in neural development. Nature Rev. Neurosci. 2, 155-164 (2001).
102. Klein, R. Excitatory Eph receptors and adhesive ephrin ligands. Curr. Opin. Cell Biol. 13, 196-203 (2001).
103. Holland, S. J., Peles, E., Pawson, T. & Schlessinger, J. Cell-contact-dependent signalling in axon growth and guidance: Eph receptor tyrosine kinases and receptor protein tyrosine phosphatase β. Curr. Opin. Neurobiol. 8, 117-127 (1998).
104. Gassmann, M. et al. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378, 390-394 (1995). Here, the aberrant routing of cranial ganglia is described, and the possibility that ErbB4 can act as a barrier molecule to axon migration presented.
105. Jacob, J., Tiveron, M. C., Brunet, J. F. & Guthrie, S. Role of the target in the pathfinding of facial visceral motor axons. Mol. Cell. Neurosci. 16, 14-26 (2000).
106. Caton, A. et al. The branchial arches and HGF are growth-promoting and chemoattractant for cranial motor axons. Development 127, 1751-1766 (2000).
107. Dietrich, S. et al. The role of SF/HGF and c-Met in the development of skeletal muscle. Development 126, 1621-1629 (1999). So far, this signalling system is the only one known to guide one specific cranial nerve towards its target.
108. Wang, H. & Tessier-Lavigne, M. En passant neurotrophic action of an intermediate axonal target in the developing mammalian CNS. Nature 401, 765-769 (1999).
109. O'Connor, R. & Tessier-Lavigne, M. Identification of maxillary factor, a maxillary process-derived chemoattractant for developing trigeminal sensory axons. Neuron 24, 165-78 (1999).
110. Mendelsohn, C. et al. Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120, 2749-2771 (1994).
111. McMahon, A. P., Joyner, A. L. Bradley, A. & McMahon, J. A. The midbrain-hindbrain phenotype of Wnt-1-/Wnt-mice results from stepwise deletion of engrailed-expressing cells by 9.5 days postcoitum. Cell 69, 581-595 (1992).
112. Swiatek, P. J. & Gridley, T. Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger gene Krox20. Genes Dev. 7, 2071-2084 (1993).
113. Schneider-Maunoury, S. et al. Disruption of Krox-20 results in ateration of rhombomeres 3 and 5 in the developing hindbrain. Cell 75, 1199-1214 (1993).
114. Manley, N. R. & Capecchi, M. R. Hox group 3 paralogous genes act synergistically in the formation of somitic and neural crest-derived structures. Dev. Biol. 192, 274-288 (1997).
115. Gavalas, A. et al. Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development 125, 1123-1136 (1998).
116. Barrow, J. R. & Capecchi, M. R. Targeted disruption of the Hoxb-2 locus in mice interferes with expression of Hoxb-1 and Hoxb-4. Development 122, 3817-3828 (1996).
117. Qiu, Y. et al. Null mutation of mCOUP-TFI results in defects in morphogenesis of the glossopharyngeal ganglion, axonal projection, and arborization. Genes Dev. 11, 1925-1937 (1997).
118. Osumi, N. et al. Pax-6 is involved in the specification of hindbrain motor neuron subtype. Development 124, 2961-2972 (1997).
119. Matzuk, M. M. et al. Multiple defects and perinatal death in mice deficient in follistatin. Nature 374, 360-363 (1995).
120. Szucsik, J. C. et al. Altered forebrain and hindbrain development in mice mutant for the Gsh-2 homeobox gene. Dev. Biol. 191, 230-242 (1997).
121. Durbec, P. L., Larsson-Blomberg, L. B., Schuchardt, A., Costantini, F. & Pachnis, V. Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts. Development 122, 349-358 (1996).
122. Huang, E. J. et al. POU domain factor Bm-3a controls the differentiation and survival of trigeminal neurons by regulating Trk receptor expression. Development 126, 2869-2882 (1999).