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PMID: 15198977 Published · ppublish English Journal Article

Hoxb1 functions in both motoneurons and in tissues of the periphery to establish and maintain the proper neuronal circuitry.

Genes & development ·Vol. 18 ·No. 13 ·2004-07-01 ·Pages 1539-52

Arenkiel BR, Tvrdik P, Gaufo GO, Capecchi MR

Abstract

Formation of neuronal circuits in the head requires the coordinated development of neurons within the central nervous system (CNS) and neural crest-derived peripheral target tissues. Hoxb1, which is expressed throughout rhombomere 4 (r4), has been shown to be required for the specification of facial branchiomotor neuron progenitors that are programmed to innervate the muscles of facial expression. In this study, we have uncovered additional roles for Hoxb1-expressing cells in the formation and maintenance of the VIIth cranial nerve circuitry. By conditionally deleting the Hoxb1 locus in neural crest, we demonstrate that Hoxb1 is also required in r4-derived neural crest to facilitate and maintain formation of the VIIth nerve circuitry. Genetic lineage analysis revealed that a significant population of r4-derived neural crest is fated to generate glia that myelinate the VIIth cranial nerve. Neural crest cultures show that the absence of Hoxb1 function does not appear to affect overall glial progenitor specification, suggesting that a later glial function is critical for maintenance of the VIIth nerve. Taken together, these results suggest that the molecular program governing the development and maintenance of the VIIth cranial nerve is dependent upon Hoxb1, both in the neural crest-derived glia and in the facial branchiomotor neurons.

MeSH Terms
Animals Axons/pathology Base Sequence Cell Movement/genetics Facial Nerve/embryology Female Gene Expression Regulation, Developmental Homeodomain Proteins/physiology Mice Mice, Mutant Strains Molecular Sequence Data Mosaicism Motor Neurons/physiology Neural Crest/embryology Neuroglia/physiology Peripheral Nervous System/embryology
Chemicals
HOXB1 homeodomain protein Homeodomain Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Arenkiel Benjamin R
Howard Hughes Medical Institute, University of Utah, Salt Lake City, Utah 84112, USA.
Tvrdik Petr
Gaufo Gary O
Capecchi Mario R
References (45)
45 references, click to expand
  1. Autonomous and nonautonomous functions for Hox/Pbx in branchiomotor neuron development.
    Dev Biol. 2003 Jan 15;253(2):200-13 PMID: 12645925
  2. ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools.
    Neuron. 2002 Aug 29;35(5):877-92 PMID: 12372283
  3. Hoxb1 neural crest preferentially form glia of the PNS.
    Dev Dyn. 2003 Jul;227(3):379-86 PMID: 12815623
  4. Neural crest motility and integrin regulation are distinct in cranial and trunk populations.
    Dev Biol. 2003 Jul 15;259(2):288-302 PMID: 12871702
  5. Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development.
    Development. 2003 Dec;130(25):6361-74 PMID: 14623825
  6. Contributions of placodal and neural crest cells to avian cranial peripheral ganglia.
    Am J Anat. 1983 Apr;166(4):445-68 PMID: 6858941
  7. Segmental expression of Hox-2 homoeobox-containing genes in the developing mouse hindbrain.
    Nature. 1989 Oct 5;341(6241):405-9 PMID: 2571936
  8. Transcription factor AP2 and its role in epidermal-specific gene expression.
    Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):7948-52 PMID: 1716766
  9. A distinct Hox code for the branchial region of the vertebrate head.
    Nature. 1991 Oct 31;353(6347):861-4 PMID: 1682814
  10. Molecular mechanisms of segmental patterning in the vertebrate hindbrain.
    Perspect Dev Neurobiol. 1993;1(3):117-25 PMID: 7916256
  11. Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx.
    Cell. 1995 Jun 30;81(7):1031-42 PMID: 7600572
  12. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells.
    Nucleic Acids Res. 1995 Dec 25;23(24):5080-1 PMID: 8559668
  13. Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation.
    Cell. 1996 Jan 26;84(2):309-20 PMID: 8565076
  14. Transcription factor AP-2 essential for cranial closure and craniofacial development.
    Nature. 1996 May 16;381(6579):235-8 PMID: 8622765
  15. Late emigrating neural crest cells migrate specifically to the exit points of cranial branchiomotor nerves.
    Development. 1996 Aug;122(8):2367-74 PMID: 8756282
  16. Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve.
    Development. 1996 Oct;122(10):3217-28 PMID: 8898234
  17. Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1.
    Nature. 1996 Dec 19-26;384(6610):630-4 PMID: 8967950
  18. Eph family transmembrane ligands can mediate repulsive guidance of trunk neural crest migration and motor axon outgrowth.
    Neuron. 1997 Mar;18(3):383-96 PMID: 9115733
  19. Severe neuropathies in mice with targeted mutations in the ErbB3 receptor.
    Nature. 1997 Oct 16;389(6652):725-30 PMID: 9338783
  20. Functionally related motor neuron pool and muscle sensory afferent subtypes defined by coordinate ETS gene expression.
    Cell. 1998 Oct 30;95(3):393-407 PMID: 9814709
  21. Neural crest cell dynamics revealed by time-lapse video microscopy of whole embryo chick explant cultures.
    Dev Biol. 1998 Dec 15;204(2):327-44 PMID: 9882474
  22. Generalized lacZ expression with the ROSA26 Cre reporter strain.
    Nat Genet. 1999 Jan;21(1):70-1 PMID: 9916792
  23. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells.
    Cell. 1999 Mar 5;96(5):737-49 PMID: 10089888
  24. Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain.
    Neuron. 1999 Apr;22(4):677-91 PMID: 10230789
  25. Neural tube-ectoderm interactions are required for trigeminal placode formation.
    Development. 1997 Nov;124(21):4287-95 PMID: 9334277
  26. Hox group 3 paralogous genes act synergistically in the formation of somitic and neural crest-derived structures.
    Dev Biol. 1997 Dec 15;192(2):274-88 PMID: 9441667
  27. Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch.
    Development. 1998 Mar;125(6):1123-36 PMID: 9463359
  28. Increased apoptosis of motoneurons and altered somatotopic maps in the brachial spinal cord of Hoxc-8-deficient mice.
    Development. 1998 Jan;125(2):279-91 PMID: 9486801
  29. The trophic requirements of mature motoneurons.
    Brain Res. 1998 Apr 13;789(2):315-21 PMID: 9573391
  30. Mice mutant for both Hoxa1 and Hoxb1 show extensive remodeling of the hindbrain and defects in craniofacial development.
    Development. 1999 Nov;126(22):5027-40 PMID: 10529420
  31. Plasticity in mouse neural crest cells reveals a new patterning role for cranial mesoderm.
    Nat Cell Biol. 2000 Feb;2(2):96-102 PMID: 10655589
  32. Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b.
    Development. 2000 Apr;127(7):1349-58 PMID: 10704382
  33. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis.
    Development. 2000 Apr;127(8):1671-9 PMID: 10725243
  34. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP.
    Nat Genet. 2000 Jun;25(2):139-40 PMID: 10835623
  35. ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons.
    Cell. 2000 May 26;101(5):485-98 PMID: 10850491
  36. Glial cell line-derived neurotrophic factor and developing mammalian motoneurons: regulation of programmed cell death among motoneuron subtypes.
    J Neurosci. 2000 Jul 1;20(13):5001-11 PMID: 10864958
  37. Hoxb1 controls effectors of sonic hedgehog and Mash1 signaling pathways.
    Development. 2000 Dec;127(24):5343-54 PMID: 11076756
  38. Activation of EGFP expression by Cre-mediated excision in a new ROSA26 reporter mouse strain.
    Blood. 2001 Jan 1;97(1):324-6 PMID: 11133778
  39. The transcription factor Sox10 is a key regulator of peripheral glial development.
    Genes Dev. 2001 Jan 1;15(1):66-78 PMID: 11156606
  40. Patterning the cranial neural crest: hindbrain segmentation and Hox gene plasticity.
    Nat Rev Neurosci. 2000 Nov;1(2):116-24 PMID: 11252774
  41. Generation of a novel functional neuronal circuit in Hoxa1 mutant mice.
    J Neurosci. 2001 Aug 1;21(15):5637-42 PMID: 11466434
  42. Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling.
    Development. 2001 Oct;128(20):3949-61 PMID: 11641219
  43. Hox genes, neural crest cells and branchial arch patterning.
    Curr Opin Cell Biol. 2001 Dec;13(6):698-705 PMID: 11698185
  44. Hoxa3 regulates integration of glossopharyngeal nerve precursor cells.
    Dev Biol. 2001 Dec 1;240(1):15-31 PMID: 11784044
  45. Coordinated temporal and spatial control of motor neuron and serotonergic neuron generation from a common pool of CNS progenitors.
    Genes Dev. 2003 Mar 15;17(6):729-37 PMID: 12651891
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
2004-07-01
Epub
2004-00-15
Pages
1539-52
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC443517
Subset
IM
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