Transgenic mice ectopically expressing HOXA5 in the dorsal spinal cord show structural defects of the cervical spinal cord along with sensory and motor defects of the forelimb

Developmental Brain Research

Volumn 150, Issue 2, 2004, Pages 125-139

  Krieger, Karin E ^a,c   Abbott, Matthew A ^a   Joksimovic, Milan ^a   Lueth, Paul A ^a   Sonea, Ioana M ^a   Jeannotte, Lucie ^b   Tuggle, Christopher K ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b LAVAL UNIVERSITY   (Canada)

^c UNIVERSITY OF WISCONSIN GREEN BAY   (United States)

Author keywords

Development and regeneration; Developmental genetics; Homeobox; Overexpression; Sensory disruption

Indexed keywords

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CERVICAL SPINAL CORD INJURY; CONTROLLED STUDY; EMBRYO; FEMALE; FORELIMB; GENE EXPRESSION REGULATION; HISTOPATHOLOGY; HOXA5 GENE; IMMUNOHISTOCHEMISTRY; MALE; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; MUSCLE STRENGTH; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SENSORY DYSFUNCTION; SENSORY EVALUATION; TISSUE DISTRIBUTION; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; BEHAVIOR, ANIMAL; BUTORPHANOL; CELL COUNT; CLONING, MOLECULAR; EMBRYO; FORELIMB; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; NARCOTICS; NEURAL PATHWAYS; NEUROKININ B; PAIN; PAIN THRESHOLD; PHOSPHOPROTEINS; PSYCHOMOTOR PERFORMANCE; REACTION TIME; RECEPTORS, NEUROKININ-1; RECEPTORS, NEUROKININ-3; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SENSATION DISORDERS; SPINAL CORD; SUBSTANCE P;

LAMIINAE; MURINAE; MUS MUSCULUS;

EID: 2442569868     PISSN: 01653806     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devbrainres.2004.03.005     Document Type: Article

References (94)

1. Anderson D.J. Lineages and transcription factors in the specification of vertebrate primary sensory neurons. Curr. Opin. Neurobiol. 9:1999;517-524
2. Andres C., Beeri R., Friedman A., Lev-Lehman E., Henis S., Timberg R., Shani M., Soreq H. Acetylcholinesterase-transgenic mice display embryonic modulations in spinal cord choline acetyltransferase and neurexin Iβ gene expression followed by late-onset neuromotor deterioration. Proc. Natl. Acad. Sci. U. S. A. 94:1997;8173-8178
3. Aubin J., Lemieux M., Tremblay M., Behringer R.R., Jeannotte L. Transcriptional interferences at the Hoxa4/Hoxa5 locus: importance of correct Hoxa5 expression for the proper specification of the axial skeleton. Dev. Dyn. 212:1998;141-156
4. Aubin J., Dery U., Lemieux M., Chailler P., Jeannotte L. Stomach regional specification requires Hoxa5-driven mesenchymal-epithelial signalling. Development. 129:2002;4075-4087
5. Aubin J., Lemieux M., Moreau J., Lapointe J., Jeannotte L. Cooperation of Hoxa5 and Pax1 genes during formation of the pectoral girdle. Dev. Biol. 244:2002;96-113
6. Awgulewitsch A., Jacobs D. Differential expression of Hox 3.1 protein in subregions of the embryonic and adult spinal cord. Development. 108:1990;411-420
7. Bang A.G., Goulding M.D. Regulation of vertebrate neural cell fate by transcription factors. Curr. Opin. Neurobiol. 6:1996;25-32
8. 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. 122:1996;3817-3828
9. Barrow J.R., Stadler H.S., Capecchi M.R. Roles of Hoxa1 and Hoxa2 in patterning the early hindbrain of the mouse. Development. 127:2000;933-944
10. Bell E., Wingate R.J.T., Lumsden A. Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. Science. 284:1999;2168-2171
11. Bermingham N.A., Hassan B.A., Wang V.Y., Fernandez M., Banfi S., Bellen H.J., Fritzsch B., Zoghbi H.Y. Proprioceptor pathway development is dependent on Math1. Neuron. 30:2001;411-422
12. Boulet A.M., Capecchi M.R. Targeted disruption of hoxc-4 causes esophageal defects and vertebral transformations. Dev. Biol. 177:1996;232-249
13. Briscoe J., Ericson J. Specification of neuronal fates in the ventral neural tube. Curr. Opin. Neurobiol. 11:2001;43-49
14. 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. 101:2000;435-445
15. Cabe P.A., Tilson H.A., Mitchell C.L., Dennis R. A simple recording grip strength device. Pharmacol. Biochem. Behav. 8:1978;101-102
16. Carpenter E.M. Hox genes and spinal cord development. Dev. Neurosci. 24:2002;24-34
17. 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. 118:1993;1063-1075
18. Carter R.B. Differentiating analgesic and non-analgesic drug activities on rat hot plate: effect of behavioral endpoint. Pain. 47:1991;211-220
19. Caspary T., Anderson K.V. Patterning cell types in the dorsal spinal cord: what the mouse mutants say. Nat. Rev. 4:2003;289-297
20. Charité J., deGraaff W., Deshamps J. Specification of multiple vertebral identities by ectopically expressed Hoxb-8. Dev. Dyn. 204:1995;13-21
21. Chen Z.F., Rebelo S., White F., Malmberg A.B., Baba H., Lima D., Woolf C.J., Basbaum A.I., Anderson D.J. The paired homeodomain protein DRG11 is required for the projection of cutaneous sensory afferent fibers to the dorsal spinal cord. Neuron. 31:2001;59-73
22. Chisaka O., Musci T.S., Capecchi M.R. Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox gene Hox-1.6. Nature. 355:1992;516-520
23. Choe A., Phun H., Lin A., Tieu D.D., Carpenter E.M. Three paralogous Hox genes pattern the lumbar spinal cord. Abstr.-Soc. Neurosci. 34:2001;135-137
24. Condie B.G., Capecchi M.R. Mice with targeted disruptions in the paralogous genes hoxa-3 and hoxd-3 reveal synergistic interactions. Nature. 370:1994;304-307
25. Davenne M., Maconochie M.K., Neun R., Pattyn A., Chambon P., Krumlauf R., Rijli F.M. Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain. Neuron. 22:1999;677-691
26. de la Cruz C.C., Der-Avakian A., Spyropoulos D.D., Tieu D.D., Carpenter E.M. Targeted disruption of Hoxd9 and Hoxd10 alters locomotor behavior, vertebral identity, and peripheral nervous system development. Dev. Biol. 216:1999;595-610
27. Diez del Corral R., Breitkreuz D.N., Storey K.G. Onset of neuronal differentiation is regulated by paraxial mesoderm and requires attenuation of FGF signalling. Development. 129:2002;1681-1691
28. Dony C., Gruss P. Specific expression of the Hox 1.3 homeo box gene in murine embryonic structures originating from or induced by the mesoderm. EMBO J. 6:1987;2965-2975
29. Eggenschwiler J.T., Espinosa E., Anderson K.V. Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway. Nature. 412:2001;194-198
30. Eisen J.S. Patterning motoneurons in the vertebrate nervous system. Trends Neurosci. 22:1999;321-326
31. Fanarraga M.L., Charité J., Hage W.J., Graaff W.D., Deschamps J. Hoxb-8 gain-of-function transgenic mice exhibit alterations in the peripheral nervous system. J. Neurosci. Methods. 71:1997;11-18
32. Foucher I., Volovitch M., Frain M., Kim J.J., Souderbielle J.C., Gan L., Unterman T.G., Prochiantz A., Trembleau A. Hoxa5 overexpression correlated with IGFBP1 upregulation and postnatal dwarfism: evidence for an interaction between Hoxa5 and Forkhead box transcription factors. Development. 129:2002;4065-4074
33. Francès H., Monier C., Bourre J.-M. Effects of dietary alpha-linolenic acid deficiency on neuromuscular and cognitive functions in mice. Life Sci. 57:1995;1935-1947
34. Gaunt S.J., Sharpe P.T., Duboule D. Spatially restricted domains of homeo-gene transcripts in mouse embryos: relation to a segmented body plan. Development. 104:1988;169-179. (Suppl.)
35. Gavalas A., Davenne M., Lumsden A. Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning. Development. 124:1997;3693-3702
36. Gavalas A., Studer M., Lumsden A., Rijli F.M., Krumlauf R. Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development. 125:1998;1123-1136
37. Gerlai R., Herrup K., Fabien K. Impaired motor learning performance in cerebellar En-2 mutant mice. Behav. Neurosci. 110:1996;126-133
38. Gilman S., Winans-Newman S. Essentials of Clinical Neuroanatomy and Neurophysiology. 9th ed. 1996;F.A. Davis, Philadelphia
39. Goddard J.M., Rossel M., Manley N.R., Capecchi M.R. Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve. Development. 122:1996;3217-3228
40. Gowan K., Helms A.W., Hunsaker T.L., Collisson T., Ebert P.J., Odom R., Johnson J.E. Crossinhibitory activities of Ngn1 and Math1 allow specification of distinct dorsal interneurons. Neuron. 31:1991;219-232
41. Gross M.K., Dottori M., Goulding M. Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron. 34:2002;535-549
42. Helms A.W., Johnson J.E. Specification of dorsal spinal cord interneurons. Curr. Opin. Neurobiol. 13:2003;29-42
43. Hogan B., Beddington R., Constatini F., Lacy E. Manipulating the Mouse Embryo: A Laboratory Manual. 1994;Cold Spring Harbor Laboratory Press, New York
44. Horan G.S.B., Kovàcs E.N., Behringer R.R., Featherstone M.S. Mutations in paralogous Hox genes result in overlapping homeotic transformations of the axial skeleton: evidence for unique and redundant function. Dev. Biol. 169:1995;359-372
45. Hostikka S.L., Capecchi M.R. The mouse Hoxc11 gene: genomic structure and expression pattern. Mech. Dev. 70:1998;133-145
46. Hunt P., Whiting J., Muchamore I., Marshall H., Krumlauf R. Homeobox genes and models for patterning the hindbrain and branchial arches. Development. (Suppl. 1):1991;187-196
47. Hunt P., Whiting J., Nonchev S., Sham M.-H., Marshall H., Graham A., Cook M., Allemann R., Ribgy P.W.J., Gulisano M., Faiella A., Boncinelli E., Krumlauf R. The branchial Hox code and its implications for gene regulation, patterning of the nervous system and head evolution. Development. (Suppl. 2):1991;63-77
48. Jaffe L., Jeannotte L., Bikoff E.K., Robertson E.J. Analysis of β2-microglobin in the developing mouse embryo and placenta. J. Immunol. 145:1990;3473-3483
49. Jeannotte L., Lemieux M., Charron J., Poirier F., Robertson E.J. Specification of axial identity in the mouse: role of the Hoxa-5 (Hox1.3) gene. Genes Dev. 7:1993;2085-2096
50. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev., Genet. 1:2000;20-29
51. Jungbluth S., Bell E., Lumsden A. Specification of distinct motor neuron identities by the singular activities of individual Hox genes. Development. 126:1999;2751-2758
52. Kania A., Johnson R.L., Jessell T.M. Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell. 102:2000;161-173
53. Krumlauf R., Marshall H., Studer M., Nonchev S., Sham M.H., Lumsden A. Hox homeobox genes and regionalisation of the nervous system. J. Neurobiol. 24:1993;1328-1340
54. Larochelle C., Tremblay M., Bernier D., Aubin J., Jeannotte L. Multiple cis-acting regulatory regions are required for restricted spatio-temporal Hoxa5 gene expression. Dev. Dyn. 214:1999;124-140
55. Lee S.K., Pfaff S.L. Transcriptional networks regulating neuronal identity in the developing spinal cord. Nat. Neurosci. 4:2001;1183-1191. (Suppl.)
56. Lee K.J., Dietrich P., Jessell T.M. Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification. Nature. 403:2000;734-740
57. LeMouellic H., Lallemand Y., Brûlet P. Homeosis in the mouse induced by a null mutation in the Hox-3.1 gene. Cell. 69:1992;251-264
58. Lowrie M.B., Lawson S.J. Cell death of spinal interneurones. Prog. Neurobiol. 61:2000;543-555
59. Lumsden A. Neural development: A 'LIM code' for motor neurons? Curr. Biol. 5:1995;491-495
60. Lumsden A., Krumlauf R. Patterning the vertebrate neuraxis. Science. 274:1996;1109-1115
61. Manzanares M., Krumlauf R. Raising the roof. Nature. 403:2000;720-721
62. Mark M., Lufkin T., Vonesch J.L., Ruberte E., Olivo J.C., Dolle P., Gorry P., Lumsden A., Chambon P. Two rhombomeres are altered in Hoxa-1 mutant mice. Development. 119:1993;319-338
63. Matise M. A dorsal elaboration in the spinal cord. Neuron. 34:2002;491-497
64. 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. 403:2000;764-772
65. Monk C.S., Webb S.J., Nelson C.A. Prenatal neurobiological development: molecular mechanisms and anatomical change. Dev. Neuropsychol. 19:1991;211-236
66. Muller T., Brohmann H., Pierani A., Heppenstall P.A., Lewin G.R., Jessell T.M., Birchmeier C. The homeodomain factor Lbx1 distinguishes two major programs of neuronal differentiation in the dorsal spinal cord. Neuron. 34:2002;551-562
67. Muller M., Jabs N., Lorke D.E., Fritzsch B., Sander M. Nkx6.1 controls migration and axon pathfinding of cranial branchiomotoneurons. Development. 130:2003;5815-5826
68. Odenwald W.F., Taylor C.F., Palmer-Hill F.J., Friedrich J.V., Tani M., Lazzarini R.A. Expression of a homeo domain protein in noncontact-inhibited cultured cells and postmitotic neurons. Genes Dev. 1:1987;482-496
69. Pattyn A., Vallstedt A., Dias J.M., Samad O.A., Krumlauf R., Rijii F.M., Brunet J.-F., Ericson J. Coordinated temporal and spatial control of motor neuron and serotonergic neuron generation from a common pool of CNS progenitors. Genes Dev. 17:2003;729-737
70. Pattyn A., Vallstedt A., Dias J.M., Sander M., Ericson J. Complementary roles for Nkx6 and Nkx2 class proteins in the establishment of motoneuron identity in the hindbrain. Development. 130:2003;4149-4159
71. Peterson R.L., Papenbrock T., Davda M.M., Awgulewitsch A. The murine Hoxc cluster contains five neighboring AbdB-related Hox genes that show unique spatially coordinated expression in posterior embryonic subregions. Mech. Dev. 47:1994;253-260
72. Pfaff S., Kintner C. Neuronal diversification: development of motor neuron subtypes. Curr. Opin. Neurobiol. 8:1998;27-36
73. Pierani A., Brenner-Morton S., Chiang C., Jessell T.M. A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell. 97:1999;903-915
74. Pitera J.E., Smith V.V., Thorogood P., Milla P.J. Coordinated expression of 3′ Hox genes during murine embryonal gut development: an enteric Hox code. Gastroenterology. 117:1999;1339-1351
75. Raman V., Martensen S.A., Reisman D., Evron E., Odenwald W.F., Jaffee E., Marks J., Sukumar S. Compromised HOXA5 function can limit p53 expression in human breast tumours. Nature. 405:2000;974-978
76. Rancourt D.E., Tsuzuki T., Capecchi M.R. Genetic interaction between hoxb-5 and hoxb-6 is revealed by nonallelic noncomplementation. Genes Dev. 9:1995;108-122
77. Richards L.J., Murphy M., Dutton R., Kilpatrick T.J., Puche A.C., Key B., Tan S.-S., Talman P.S., Bartlett P.F. Lineage specification of neuronal precursors in the mouse spinal cord. Proc. Natl. Acad. Sci. U. S. A. 92:1995;10079-10083
78. Rijli F.M., Matyas R., Pellegrini M., Dierich A., Gruss P., Dolle P., Chambon P. Cryptorchidism and homeotic transformations of spinal nerves and vertebrae in Hoxa-10 mutant mice. Proc. Natl. Acad. Sci. U. S. A. 92:1995;8185-8189
79. Rossel M., Capecchi M.R. Mice mutant for both Hoxa1 and Hoxb1 show extensive remodeling of the hindbrain and defects in craniofacial development. Development. 126:1999;5027-5040
80. Roth K.A., D'Sa C. Apoptosis and brain development. Ment. Retard. Dev. Disabil. Res. Rev. 7:2001;261-266
81. Sander M., Paydar S., Ericson J., Briscoe J., Berber E., German M., Jessell T.M., Rubenstein J.L. Ventral neural patterning by Nkx homeobox genes: Nkx6.1 controls somatic motor neuron and ventral interneuron fates. Genes Dev. 14:2000;2134-2139
82. Simon H., Hornbruch A., Lumsden A. Independent assignment of antero-posterior and dorso-ventral positional values in the developing chick hindbrain. Curr. Biol. 5:1995;205-214
83. Steward O. Functional Neuroscience. 2000;Springer-Verglag, New York, NY
84. 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. 384:1996;630-634
85. Tanabe Y., Jessell T.M. Diversity and pattern in the developing spinal cord. Science. 274:1996;1115-1123
86. Tiret L., LeMouellic H., Maury M., Brûlet P. Increased apoptosis of motoneurons and altered somatotopic maps in the brachial spinal cord of Hoxc-8-deficient mice. Development. 125:1998;279-291
87. Tuggle C.K., Zakany J., Cianetti L., Peschle C., Nguyen-Huu M.C. Region-specific enhancers near two mammalian homeo box genes define adjacent rostrocaudal domains in the central nervous system. Genes Dev. 4:1990;180-189
88. van den Akker E., Reijnen M., Korving J., Brouwer A., Meijlink F., Deschamps J. Targeted inactivation of Hoxb8 affects survival of spinal ganglion and causes aberrant limb reflexes. Mech. Dev. 89:1999;103-114
89. Wahba G.M., Hostikka S.L., Carpenter E.M. The paralogous Hox genes Hoxa10 and Hoxd10 interact to pattern the mouse hindlimb peripheral nervous system and skeleton. Dev. Biol. 231:2001;87-102
90. White F.A., Keller-Peck C.R., Knudson C.M., Korsmeyer S.J., Snider W.D. Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J. Neurosci. 18:1998;1428-1439
91. Yamamoto Y., Henderson C. Patterns of programmed cell death in populations of developing spinal motoneurons in chicken, mouse, and rat. Dev. Biol. 214:1999;60-71
92. Zakany J., Tuggle C.K., Patel M.D., Nguyen-Huu M.C. Spatial regulation of Homeobox gene fusions in the embryonic central nervous system of transgenic mice. Neuron. 1:1988;679-691
93. Zemen W., Innes J.R.M. Craigie's Neuroanatomy of the rat, Revised and Expanded by Wolfgang Zeman and James Robert Maitland Innes. 1963;Academic Press, New York
94. Zhao J.J., Lazzarini R.A., Pick L. Functional dissection of the mouse Hox-a5 gene. EMBO J. 15:1996;1313-1322