Home LiteratureArticle Details
PMID: 9391239 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Hirschsprung's disease: genetic mutations in mice and men.

Gut ·Vol. 41 ·No. 4 ·1997-10-00 ·Pages 436-41

Robertson K, Mason I, Hall S

Abstract

Hirschsprung's disease is a neuronal dysplasia of the hindgut, characterised by a loss of neurones, which affects about 1 in 5000 live births. Genetic factors have been implicated in the aetiology of this disease in about 20% of cases and a dominant pattern of inheritance has been revealed in several families. The pathogenesis of the aganglionosis is often attributed to a failure of migration of neural crest cells, although this has not been proven. Recently, mutations in a developmentally regulated receptor tyrosine kinase gene, ret, and mutations in the endothelin receptor-B gene (ENDR-B) have both been linked to familial Hirschsprung's disease in humans. Moreover, certain mutant mouse strains--namely piebald lethal and lethal spotted--exhibit striking similarities to the human condition. The mutation which gives rise to piebald lethal has now been found to be in the ENDR-B gene, and the mutation associated with lethal spotted occurs in the gene for endothelin-3 (ET-3), a ligand for ENDR-B. Two transgenic mouse lines have been developed which also reflect the human disease: ret-k-, which has a loss of function mutation of the ret gene, and ENDR-B null. In addition, the introduction of a Lac-Z reporter gene into neural crest cells of aganglionic mice has made it possible to study directly the fate of enteric neuroblasts which are affected by "Hirschsprung's-like" mutations. Here, we review the possible roles of RET and endothelin in the normal development of the enteric nervous system, and the significance of their mutated forms in the pathogenesis of familial aganglionosis. This review focuses on recent advances in our understanding of the genetic basis of the lesions which have been implicated in congenital forms of Hirschsprung's disease. Disruption of these genes in the mouse, either by transgenic "knockout" approaches or in mutant mouse lines, offers the prospect of greater understanding of both the cellular and developmental bases of the human disease.

MeSH Terms
Animals Chromosomes, Human, Pair 10 Disease Models, Animal Hirschsprung Disease/genetics,physiopathology Humans Mice Mice, Transgenic Mutation Superior Cervical Ganglion/abnormalities
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Robertson K
Department of Developmental Neurobiology, UMDS Guy's Hospital, London, UK.
Mason I
Hall S
References (44)
44 references, click to expand
  1. Targeted and natural (piebald-lethal) mutations of endothelin-B receptor gene produce megacolon associated with spotted coat color in mice.
    Cell. 1994 Dec 30;79(7):1267-76 PMID: 8001159
  2. Innervation of bladder and bowel.
    Ciba Found Symp. 1990;151:2-18; discussion 18-26 PMID: 1977565
  3. Phylogenetic analysis of the cadherin superfamily.
    Bioessays. 1992 Nov;14(11):743-8 PMID: 1365887
  4. GDNF is an age-specific survival factor for sensory and autonomic neurons.
    Neuron. 1995 Oct;15(4):821-8 PMID: 7576631
  5. Intercellular signals downstream of endothelin receptor-B mediate colonization of the large intestine by enteric neuroblasts.
    Development. 1995 Nov;121(11):3787-95 PMID: 8582288
  6. Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts.
    Development. 1996 Jan;122(1):349-58 PMID: 8565847
  7. Expression of ret in the chicken embryo suggests roles in regionalisation of the vagal neural tube and somites and in development of multiple neural crest and placodal lineages.
    Mech Dev. 1995 Nov;53(3):329-44 PMID: 8645600
  8. Functional receptor for GDNF encoded by the c-ret proto-oncogene.
    Nature. 1996 Jun 27;381(6585):785-9 PMID: 8657281
  9. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF.
    Cell. 1996 Jun 28;85(7):1113-24 PMID: 8674117
  10. Renal agenesis and the absence of enteric neurons in mice lacking GDNF.
    Nature. 1996 Jul 4;382(6586):70-3 PMID: 8657306
  11. Defects in enteric innervation and kidney development in mice lacking GDNF.
    Nature. 1996 Jul 4;382(6586):73-6 PMID: 8657307
  12. Renal and neuronal abnormalities in mice lacking GDNF.
    Nature. 1996 Jul 4;382(6586):76-9 PMID: 8657308
  13. Characterization of a multicomponent receptor for GDNF.
    Nature. 1996 Jul 4;382(6586):80-3 PMID: 8657309
  14. The GDNF receptor: recent progress and unanswered questions.
    Mol Cell Neurosci. 1996;8(2-3):112-9 PMID: 8918828
  15. The GDNF-RET signalling partnership.
    Trends Genet. 1997 Jan;13(1):1-3 PMID: 9009838
  16. The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo.
    J Comp Neurol. 1954 Oct;101(2):515-41 PMID: 13221667
  17. The genetics of Hirschsprung's disease. Evidence for heterogeneous etiology and a study of sixty-three families.
    N Engl J Med. 1967 Jan 19;276(3):138-43 PMID: 4224912
  18. Histochemical diagnosis of Hirschsprung's disease.
    Lancet. 1969 Apr 26;1(7600):894-5 PMID: 4180562
  19. The migration of neural crest cells to the wall of the digestive tract in avian embryo.
    J Embryol Exp Morphol. 1973 Aug;30(1):31-48 PMID: 4729950
  20. Pathways and mechanisms of avian trunk neural crest cell migration and localization.
    Dev Biol. 1982 Oct;93(2):324-43 PMID: 7141101
  21. Hirschsprung disease: a genetic study.
    Clin Genet. 1985 Dec;28(6):503-8 PMID: 2934185
  22. Abnormalities of smooth muscle, basal laminae, and nerves in the aganglionic segments of the bowel of lethal spotted mutant mice.
    Anat Rec. 1986 Jul;215(3):267-81 PMID: 3740466
  23. Accumulation of components of basal laminae: association with the failure of neural crest cells to colonize the presumptive aganglionic bowel of ls/ls mutant mice.
    Dev Biol. 1988 Feb;125(2):341-60 PMID: 3338619
  24. Concurrent de novo interstitial deletion of band 2p22 and reciprocal translocation (3;7)(p21;q22).
    J Med Genet. 1988 Feb;25(2):125-7 PMID: 3346886
  25. Hirschsprung disease associated with polydactyly, unilateral renal agenesis, hypertelorism, and congenital deafness: a new autosomal recessive syndrome.
    J Med Genet. 1988 Mar;25(3):204-5 PMID: 3351909
  26. A study of the extracellular matrix protein as the migration pathway of neural crest cells in the gut: analysis in human embryos with special reference to the pathogenesis of Hirschsprung's disease.
    J Pediatr Surg. 1989 Jun;24(6):550-6 PMID: 2738822
  27. A model for aganglionosis in the chicken embryo.
    J Pediatr Surg. 1989 Jun;24(6):557-61 PMID: 2738823
  28. The syndrome of Hirschsprung disease, microcephaly, unusual face, and mental retardation.
    Am J Med Genet. 1990 Sep;37(1):106-8 PMID: 2240026
  29. A case of Hirschsprung disease with a chromosome 13 microdeletion, del(13)(q32.3q33.2): potential mapping of one disease locus.
    Hum Genet. 1991 Oct;87(6):748-50 PMID: 1937482
  30. A transgenic model for studying development of the enteric nervous system in normal and aganglionic mice.
    Development. 1992 Sep;116(1):167-75 PMID: 1483385
  31. From neural crest to bowel: development of the enteric nervous system.
    J Neurobiol. 1993 Feb;24(2):199-214 PMID: 8445388
  32. cDNA cloning of mouse ret proto-oncogene and its sequence similarity to the cadherin superfamily.
    Oncogene. 1993 Apr;8(4):1087-91 PMID: 8455936
  33. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons.
    Science. 1993 May 21;260(5111):1130-2 PMID: 8493557
  34. A gene for Hirschsprung disease maps to the proximal long arm of chromosome 10.
    Nat Genet. 1993 Aug;4(4):346-50 PMID: 8401580
  35. A gene for Hirschsprung disease (megacolon) in the pericentromeric region of human chromosome 10.
    Nat Genet. 1993 Aug;4(4):351-6 PMID: 8401581
  36. Expression of the c-ret proto-oncogene during mouse embryogenesis.
    Development. 1993 Dec;119(4):1005-17 PMID: 8306871
  37. Point mutations affecting the tyrosine kinase domain of the RET proto-oncogene in Hirschsprung's disease.
    Nature. 1994 Jan 27;367(6461):377-8 PMID: 8114938
  38. Mutations of the RET proto-oncogene in Hirschsprung's disease.
    Nature. 1994 Jan 27;367(6461):378-80 PMID: 8114939
  39. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret.
    Nature. 1994 Jan 27;367(6461):380-3 PMID: 8114940
  40. A missense mutation of the endothelin-B receptor gene in multigenic Hirschsprung's disease.
    Cell. 1994 Dec 30;79(7):1257-66 PMID: 8001158
  41. Colonization of the avian hindgut by cells derived from the sacral neural crest.
    Dev Biol. 1990 Feb;137(2):378-94 PMID: 2406176
  42. A genetic study of Hirschsprung disease.
    Am J Hum Genet. 1990 Mar;46(3):568-80 PMID: 2309705
  43. Developmental potential of neural crest-derived cells migrating from segments of developing quail bowel back-grafted into younger chick host embryos.
    Development. 1990 Jun;109(2):411-23 PMID: 2401204
  44. Interaction of endothelin-3 with endothelin-B receptor is essential for development of epidermal melanocytes and enteric neurons.
    Cell. 1994 Dec 30;79(7):1277-85 PMID: 8001160
Article Info
Journal
Gut
Abbr.
Gut
ISSN
0017-5749
Published
1997-10-00
Pages
436-41
Language
English
Region
England
NLM ID
2985108R
PMCID
PMC1891517
Subset
IM
Grants
Wellcome Trust · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com