Transgenic expression of the endothelin-B receptor prevents congenital intestinal aganglionosis in a rat model of Hirschsprung disease

Journal of Clinical Investigation

Volumn 102, Issue 6, 1998, Pages 1092-1101

  Gariepy, Cheryl E ^a   Williams, S Clay ^a   Richardson, James A ^b   Hammer, Robert E ^a,b   Yanagisawa, Masashi ^a,b  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Enteric nervous system; Neural crest; Shah Waardenburg syndrome; Spotting lethal rat

Indexed keywords

DOPAMINE BETA MONOOXYGENASE; ENDOTHELIN B RECEPTOR; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; GENE DELETION; GENE DOSAGE; GENE EXPRESSION; HIRSCHSPRUNG DISEASE; IN SITU HYBRIDIZATION; INTESTINE INNERVATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; RAT; TRANSGENIC ANIMAL; WAARDENBURG SYNDROME;

EID: 0032530761     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI3702     Document Type: Article

References (59)

1. Rawles, M. 1940. The development of meanophores from embryonic mouse tissues grown in the coelom of chick embryos. Proc. Natl. Acad. Sci. USA. 26:673-680.
2. Rawles, M. 1947. Origin of pigment cells from the neural crest in the mouse embryo. Physiol. Zool. 20:248-270.
3. Le Douarin, N.M., and M. Teiltet. 1973. The migration of neural crest cells to the wall of the digestive tract in avian embryo. J. Embryol. Exp. Morphol. 30:31-48.
4. Mayer, T. 1973. The migratory pathway of neural crest cells into the skin of mouse embryos. Dev. Biol. 34:39-46.
5. Serbedzija, G., S. Fraser, and M. Bronner-Fraser. 1990. Pathways of trunk neural crest cell migration in the mouse embryo as revealed by vital dye labeling. Development. 108:605-612.
6. Webster, W. 1973. Embryogenesis of the enteric ganglia in normal mice and mice that develop congenital aganglionic megacolon. J. Embryol. Exp. Morph. 30:573-585.
7. Yntema, C.L., and W.S. Hammond. 1954. The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. Neurology. 101: 515-542.
8. Kapur, R.P., C. Yost, and R.D. Palmiter. 1992. A transgenic model for studying development of the enteric nervous system in normal and aganglionic mice. Development. 116:167-175.
9. Peters-van der Sanden, M.J., M.L. Kirby, A. Guttenberger-de Groot, D. Tibboel, M.P. Mulder, and C. Meijers. 1993. Colonization of the bowel by neural crest-derived cells re-migrating from foregut backtransplanted to vagal or sacral regions of host embryos. Dev. Dyn. 196:217-233.
10. Lane, P.W. 1966. Association of megacolon with two recessive spotting genes in the mouse. J. Hered. 57:28-31.
11. Lyon, M., and A. Searle. 1989. Genetic Variants and Strains of the Laboratory Mouse. Oxford University Press. Oxford, UK.
12. Ikadai, H., H. Fujita, Y. Agematsu, and T. Imanichi. 1979. Observation of congenital aganglionosis rat (Hirschsprung's disease) and its genetical analysis, (in Japanese). Congenital. Anom. 19:31-36.
13. McCabe, L., L. Griffin, A. Kinzer, M. Chandler, J. Beckwith, and E. McCabe. 1990. Overo lethal white foal syndrome: equine model of aganglionic megacolon (Hirschsprung disease). Am. J. Med. Genet. 36:336-340.
14. Shah, K., S. Dalal, M. Desai, P. Sheth, N. Joshi, and L. Ambani. 1981. White forelock, pigmentary disorder of irides, and long segment Hirschsprung disease: possible variant of Waardenburg syndrome. J. Pediatr. 99:432-435.
15. Edery, P., T. Attie, J. Amiel, A. Pelet, C. Eng, R. Hofstra, Martelli, C. Bidaud, A. Munnich, and S. Lyonnet. 1996. Mutation of the endothelin-3 gene in Waardenburg-Hirschsprung disease (Shah-Waardenburg Syndrome). Nat. Genet. 12:442-444.
16. Attie, T., M. Till, A. Pelet, J. Amiel, P. Edery, L. Bautrand, A. Munnich, and S. Lyonnet. 1995. Mutation of the endothelin-receptor B gene in Waardenburg-Hirschsprung disease. Hum. Mol. Genet. 4:2407-2409.
17. Auricchio, A., G. Casari, A. Staiano, and A. Ballabio. 1996. Endothelin-B receptor mutations in patients with isolated Hirschsprung disease from a non-inbred population. Hum. Mol. Genet. 5:351-354.
18. Amiel, J., T. Attie, D. Jan, A. Pelet, P. Edery, C. Bidaud, D. Lacombe, P. Tam, J. Simeoni, E. Flori, et al. 1996. Heterozygous endothelin receptor B (EDNRB) mutations in isolated Hirschsprung disease. Hum. Mol. Genet. 5: 355-357.
19. Hofstra, R.M.W., J. Osinga, G. Tan-Sindhunata, Y. Wu. E.-J. Kamsteeg, R.P. Stulp, C.V. Ravenswaaij-Arts, D. Majoor-Krakauer, M. Angrist, A. Chakravarti, C. Meijers, and C.H.C.M. Buys. 1996. A homozygous mutation in the endothelin-3 gene associated with a combined Waardenburg type 2 and Hirschsprung phenotype (Shah-Waardenburg syndrome). Nat. Genet. 12:445-447.
20. Puffenberger, E.G., K. Hosoda, S.S. Washington, K. Nakao, D. deWit, M. Yanagisawa, and A. Chakravarti. 1994. A missense mutation of the endothelin-B receptor gene in multigenic Hirschsprung disease. Cell. 79:1257-1266.
21. Kusafuka, T., Y. Wang, and P. Puri. 1996. Novel mutations of the endothelin-B receptor gene in isolated patients with Hirschsprung's disease. Hum. Mol. Genet. 5:347-349.
22. Baynash, A.G., K. Hosoda, A. Giaid, J.A. Richardson, N. Emoto, R.E. Hammer, and M. Yanagisawa. 1994. Interaction of endothelin-3 with endothelin-B receptor is essential for development of neural crest-derived melanocytes and enteric neurons: missense mutation of endothelin-3 gene in lethal spotting mice. Cell. 79:1277-1285.
23. Hosoda, K., R.E. Hammer, J.A. Richardson, A. Greenstein Baynash, J.C. Cheung, A. Giaid, and M. Yanagisawa. 1994. Targeted and natural (piebald-lethal) mutations of endothelin-B receptor gene produce aganglionic megacolon associated with white-spotted coat color in mice. Cell. 79:1267-3276.
24. Yanagisawa, H., M. Yanagisawa, R. Kapur, J. Richardson, S. Williams, D. Clouthier, D. de Wit, N. Emoto, and R. Hammer. 1998. Dual genetic pathways of endothelin-mediated intercelluar signaling revealed by targeted disruption of endothelin convertin enzyme-1 gene. Development. 125:825-836.
25. Santschi, E., A. Purdy, S. Valberg, P. Vrotsos, H. Kaese, and J. Mickelson. 1998. Endothelin receptor B polymorphism associated with lethal white foal syndrome in horses. Mamm. Genome. 9:306-309.
26. Gariepy, C.E., D.T. Cass, and M. Yanagisawa. 1996. Null mutation of endothelin-B receptor gene in spotting lethal rats causes aganglionic megacolon and white coat color. Proc. Natl. Acacl. Sci. USA. 93:867-872.
27. Nagahama, M., T. Ozaki, and K. Hama. 1985. A study of the myenteric plexus of the congenital aganglionosis rat (spotting lethal). Anat. Embryol. 171: 285-296.
28. Yanagisawa, M., H. Kurihara, S. Kimura, Y. Tomobe, M. Kobayashi, Y. Mitsui, Y. Yazaki, K. Goto, and T. Masaki. 1988. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature. 332:411-415.
29. Yanagisawa, M. 1994. The endothelin system: a new target for therapeutic intervention. Circulation. 89:1320-1322.
30. Sokolovsky, M. 1994. Endothelins and sarafotoxins: receptor heterogeneity. Int. J. Biochem. 26:335-340.
31. Sakamoto, A.; M. Yanagisawa, T. Sawamura, T. Enoki, T. Ohtani, T. Sakurai, K. Nakao, T. Toyo-oka, and T. Masaki. 1993. Distinct subdomains of human endothelin receptors determine their selectivity to ETA-selective antagonist and ETB-selective agonists. J. Biol. Chem. 268:8547-8553.
32. Arai, H., S. Hori, I. Aramori, H. Ohkubo, and S. Nakanishi. 1990. Cloning and expression of a cDNA encoding an endothelin receptor. Nature. 348: 730-732.
33. Sakurai, T., M. Yanagisawa, Y. Takuwa, H. Miyazaki, S. Kimura, K. Goto, and T. Masaki. 1990. Cloning of a cDNA encoding a non-isopeptide-selective subtype of the endothelin receptor. Nature. 348:732-735.
34. Brand, M., J.-M. Le Moullec, P. Corval, and J.-M. Gasc. 1998. Ontogeny of endothelins-1 and -3. their receptors, and endothelin converting enzyme-1 in the early human embryo. J. Clin. Invest. 101:549-559.
35. Baetge, G., and M.D. Gershon. 1988. Transient catecholaminergic (TC) cells in the vagus nerves and bowel of fetal mice: relationship to the development of enteric neurons. Dev. Biol. 132:189-211.
36. Baetge, G., J.E. Pintar, and M.D. Gershon. 1990. Transiently catecholaminergic (TC) cells in the bowel of fetal rats and mice: precursors of non-catecholaminergic enteric neurons. Dev. Biol. 141:353-380.
37. Baetge, G., K. A. Schneider, and M.D. Gershon. 1990. Development and persistence of catecholaminergic neurons in cultured expiants of fetal murine vagus nerves and bowel. Development. 110:689-701.
38. Blaugrund, E., T.D. Pham, V.M. Tennyson, L. Lo, L. Sommer, D.J. Anderson, and M.D. Gershon. 1996. Distinct subpopulations of enteric neuronal progenitors defined by time and place of development, sympathoadrenal lineage markers and Mash-1-dependence. Development. 122:309-320.
39. Kapur, R.P., G.W. Hoyle, E.H. Mercer, R.L. Brinster, and R.D. Palmiter. 1991. Some neuronal cell populations express human dopaminc β-hydroxylase-lacZ transgenes transiently during embryonic development. Neuron. 7: 717-727.
40. Clouthier, D., K. Hosoda, J. Richardson, S. Williams, H. Yanagisawa, T. Kuwaki, M. Kumada, R. Hammer, and M. Yanagisawa. 1998. Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice. Development. 125:813-824.
41. Hoyle, G.W., E.H. Mercer, R.D. Palmiter, and R.L. Brinster. 1993. Expression of NGF in sympathetic neurons leads to excessive axon outgrowth from ganglia but decreased terminal innervation within tissues. Neuron. 10: 1019-1034.
42. Hammer, R., S. Maika, J. Richardson, J.-P. Tang, and J. Taurog. 1990. Spontaneous inflammatory disease in transgenic rats expression HLA-B27 and human β2m: an animal model of HLA-B27-associated human disorders. Cell. 63:1099-1112.
43. Xu, D., N. Emoto, A. Giaid, C. Slaughter, S. Kaw, D. de Wit, and M. Yanagisawa. 1994. ECE-1: a membrane-bound metalloprotease that catalyzes the proteolytic activation of big endothelin-1. Cell. 78:473-485.
44. Newgreen, D., and L. Hartley. 1995. Extracellular matrix and adhesive molecules in the early development of the gut and its innervation in normal and spotting lethal rat embryos. Acta Anat. 154:243-260.
45. Watanabe, Y., T. Harada, T. Ito, Y. Ishiguro, H. Ando, T. Seo, S. Kobayashi, M. Takahashi, and Y. Nimura. 1997. ret proto-oncogene product is a useful marker of lineage determination in the development of the enteric nervous system in rats. J Pediatr Surg. 32:28-33.
46. Nataf, V., L. Lecoin, A. Eichmann, and N.M. Le Douarin. 1996. Endothelin-B receptor is expressed by neural crest cells in the avian embryo. Proc. Natl. Acad. Sci. USA. 93:9645-9650.
47. Payette, R., V. Tennyson, H. Pomeranz, T. Pham, T. Rothman, and M. Gershon. 1988. 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. 125:341-360.
48. Watanabe, Y., T. Ito, S. lino, T. Harada, H. Ando, T. Seo, S. Kobayashi, and T. Ozaki. 1997. Unique spindle cells in the involved ileal segment of rats with congenital aganglionosis. J. Pediatr. Surg. 32:1229-1233.
49. Shimotake, T., N. Iwai, J. Yanagihara, E. Deguchi, and S. Fushiki, 1995. Impared proliferative activity of mesenchymal cells affects the migratory pathway for neural crest cells in the developing gut of mutant murine embryos. J. Pediatr. Surg. 30:445-447.
50. Langer, J., P. Betti, and M. Blennerhassett. 1994. Smooth muscle from aganglionic bowel in Hirschsprung's disease impairs neuronal development in vitro. Cell Tissue Res. 276:181-186.
51. Parikh, D., P. Tam, D. Van Velzen, and D. Edgar. 1992. Abnormalities in the distribution of laminin and collagen type IV in Hirschsprung's disease. Gastroenterology. 102:1236-1241.
52. Parikh, D., P. Tam, D. Lloyd, D. Van Velzen, and D. Edgar. 1992. Quantitative and qualitative analysis of the extracellular matrix protein, laminin, in Hirschsprung's disease. J. Pediatr. Surg. 27:991-995.
53. Jacobs-Cohen, R., R. Payette, M. Gershon, and T. Rothman. 1987. Inability of neural crest cells to colonize the presumptive aganglionic bowel of ls/ ls mutant mice: requirement for a permissive microenvironment. J. Comp. Neural. 255:425-438.
54. Rothman, T., D. Goldowitz, and M. Gershon. 1993. Inhibition of migration of neural crest-derived cells by the abnormal mesenchyme of the presumptive aganglionic bowel of ls/ls mice: analysis with aggregation and inlerspecies chimeras. Dev. Biol. 159:559-573.
55. Pomeranz, H., T. Rothman, A. Chalazonitis, V. Tennyson, and M. Gershon. 1993. Neural crest-derived cells isolated from the gut by immunoselection develop neuronal and glial phenotypes when cultured on laminin. Dev Biol. 156:341-361.
56. Chalazonitis, A., V. Tennyson, M. Kibbey, T. Rothman, and M. Gershon. 1997. The α1 subunit of laminin-1 promotes the development of neurons by interacting with LBP 110 expressed by neural crest-derived cells immunoselected from the fetal mouse gut. J. Neurobiol. 33:118-138.
57. Kapur, R.P., D.A. Sweetser, B. Doggett, J.R. Siebert, and R.D. Palmiter. 1995. Intercellular signals downstream of endothelin receptor-B mediate colonization of the large intestine by enteric neuroblasts. Development. 121: 3787-3795.
58. Rothman, T.P., and M.D. Gershon. 1982. Phenotypic expression in the developing murine enteric nervous system. J. Neurosci. 2:381-393.
59. Silvers, W. 1979. The Coat Colors of Mice: A Model for Mammalian Gene Action and Interaction. Springer-Verlag, Inc., New York.