The ?1 subunit of laminin-1 promotes the development of neurons by interacting with LBP110 expressed by neural crest-derived cells immunoselected from the fetal mouse gut

Chalazonitis, Alcmène; Tennyson, Virginia M.; Kibbey, Maura C.; Rothman, Taube P.; Gershon, Michael D.

doi:10.1002/(sici)1097-4695(199708)33:2<118::aid-neu2>3.0.co;2-5

Cited by 68 publications

(42 citation statements)

References 59 publications

(1 reference statement)

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“…Immunoreactivity was used to detect markers that enabled cultured cells to be identified. Procedures used for the immunocytochemical detection of antigens in cultured cells were similar to those described in detail previously (Chalazonitis et al, 1994(Chalazonitis et al, , 1997(Chalazonitis et al, , 1998a(Chalazonitis et al, , 2001. Briefly, cultures were fixed for 1 hr with 4% formaldehyde (freshly prepared from paraformaldehyde) in 0.1 mM PBS.…”

Section: Methodsmentioning

confidence: 99%

“…The total number of cells in each culture and cells specifically identified with reagents (supplemental Tables 1, 2, available at www.jneurosci.org) were counted as described previously (Chalazonitis et al, 1994(Chalazonitis et al, , 1997(Chalazonitis et al, , 1998a(Chalazonitis et al, ,b, 2001. Counts of the total number of cells in cultures treated with experimental reagents were normalized as a percentage of cells found in replicate cultures that had only been treated with vehicle.…”

Section: Methodsmentioning

confidence: 99%

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Bone Morphogenetic Protein-2 and -4 Limit the Number of Enteric Neurons But Promote Development of a TrkC-Expressing Neurotrophin-3-Dependent Subset

Chalazonitis¹,

D’Autréaux²,

Guha³

et al. 2004

J. Neurosci.

121

212

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The hypothesis that BMPs (bone morphogenetic proteins), which act early in gut morphogenesis, also regulate specification and differentiation in the developing enteric nervous system (ENS) was tested. Expression of BMP-2 and BMP-4, BMPR-IA (BMP receptor subunit), BMPR-IB, and BMPR-II, and the BMP antagonists, noggin, gremlin, chordin, and follistatin was found when neurons first appear in the primordial bowel at embryonic day 12 (E12). Agonists, receptors, and antagonists were detected in separated populations of neural crestand noncrest-derived cells. When applied to immunopurified E12 ENS precursors, BMP-2 and BMP-4 induced nuclear translocation of phosphorylated Smad-1 (Sma and Mad-related protein). The number of neurons developing from these cells was increased by low concentrations and decreased by high concentrations of BMP-2 or BMP-4. BMPs induced the precocious appearance of TrkC-expressing neurons and their dependence on neurotrophin-3 for survival. BMP-4 interacted with glial cell line-derived neurotrophic factor (GDNF) to enhance neuronal development but limited GDNF-driven expansion of the precursor pool. BMPs also promoted development of smooth muscle from mesenchymal cells immunopurified at E12. To determine the physiological significance of these observations, the BMP antagonist noggin was overexpressed in the developing ENS of transgenic mice under the control of the neuron-specific enolase promoter. Neuronal numbers in both enteric plexuses and smooth muscle were increased throughout the postnatal small intestine. These increases were already apparent by E18. In contrast, TrkC-expressing neurons decreased in both plexuses of postnatal nogginoverexpressing animals, again an effect detectable at E18. BMP-2 and/or BMP-4 thus limit the size of the ENS but promote the development of specific subsets of enteric neurons, including those that express TrkC.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Bone Morphogenetic Protein-2 and -4 Limit the Number of Enteric Neurons But Promote Development of a TrkC-Expressing Neurotrophin-3-Dependent Subset

Chalazonitis¹,

D’Autréaux²,

Guha³

et al. 2004

J. Neurosci.

121

212

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“…ENS precursors express various receptors for ECM, such as ␣4 Kruger et al, 2002), ␣6 and ␤1 integrins (current study), and the 110 kDa laminin receptor (Chalazonitis et al, 1997). Integrins comprise a large family of 24 ␣␤ heterodimers that can activate signalling pathways that control cell proliferation, survival, migration or differentiation (Hynes, 2002).…”

Section: Introductionmentioning

confidence: 94%

“…ENCCs lacking ␤1 integrins do not lose all their migratory abilities, suggesting a role for other ECM receptors, such as the 110 kDa laminin receptor (Chalazonitis et al, 1997) and ␤3 and ␤5 integrins, or intercellular adhesion molecules in their migration through gut tissues. The importance of intercellular adhesion in ENCC progression is supported by the various repertoire of intercellular adhesion proteins we found to be expressed by ENCCs.…”

Section: ␤ ␤1 Integrins and Intercellular Adhesion In Enccsmentioning

confidence: 99%

Lack of β1 integrins in enteric neural crest cells leads to a Hirschsprung-like phenotype

et al. 2006

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The enteric nervous system arises mainly from vagal and sacral neural crest cells that colonise the gut between 9.5 and 14 days of development in mice. Using the Cre-LoxP system, we removed ␤1 integrins in the neural crest cells when they emerge from the neural tube. ␤1-null enteric neural crest cells fail to colonise the gut completely, leading to an aganglionosis of the descending colon, which resembles the human Hirschsprung's disease. Moreover, ␤1-null enteric neural crest cells form abnormal aggregates in the gut wall, leading to a severe alteration of the ganglia network organisation. Organotypic cultures of gut explants reveal that ␤1-null enteric neural crest cells show impaired adhesion on extracellular matrix and enhanced intercellular adhesion properties. They display migration defects in collagen gels and gut tissue environments. We also provide evidence that ␤1 integrins are required for the villi innervation in the small intestine. Our findings highlight the crucial roles played by ␤1 integrins at various steps of enteric nervous system development.

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“…The resulting cellular suspension was cultured or purified by immunoselection with rabbit polyclonal antibodies to the common neurotrophin receptor p75 NTR (gift from Moses Chao, New York University, NY) as described previously (Chalazonitis et al, 1994;Chalazonitis et al, 1997).…”

Section: Isolation Of Crest-derived Cellsmentioning

confidence: 99%

Hand2is necessary for terminal differentiation of enteric neurons from crest-derived precursors but not for their migration into the gut or for formation of glia

et al. 2007

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Hand genes encode basic helix-loop-helix transcription factors that are expressed in the developing gut, where their function is unknown. We now report that enteric Hand2 expression is limited to crest-derived cells, whereas Hand1 expression is restricted to muscle and interstitial cells of Cajal. Hand2 is developmentally regulated and is intranuclear in precursors but cytoplasmic in neurons. Neurons develop in explants from wild-type but not Hand2 -/-bowel, although, in both, crest-derived cells are present and glia arise. Similarly, small interfering RNA (siRNA) silencing of Hand2 in enteric crest-derived cells prevents neuronal development. Terminally differentiated enteric neurons do not develop after conditional inactivation of Hand2 in migrating crest-derived cells; nevertheless, conditional Hand2 inactivation does not prevent precursors from expressing early neural markers. We suggest that enteric neuronal development occurs in stages and that Hand2 expression is required for terminal differentiation but not for precursors to enter the neuronal lineage.

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The ?1 subunit of laminin-1 promotes the development of neurons by interacting with LBP110 expressed by neural crest-derived cells immunoselected from the fetal mouse gut

Cited by 68 publications

References 59 publications

Bone Morphogenetic Protein-2 and -4 Limit the Number of Enteric Neurons But Promote Development of a TrkC-Expressing Neurotrophin-3-Dependent Subset

Bone Morphogenetic Protein-2 and -4 Limit the Number of Enteric Neurons But Promote Development of a TrkC-Expressing Neurotrophin-3-Dependent Subset

Lack of β1 integrins in enteric neural crest cells leads to a Hirschsprung-like phenotype

Hand2is necessary for terminal differentiation of enteric neurons from crest-derived precursors but not for their migration into the gut or for formation of glia

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