Diminished Ret expression compromises neuronal survival in the colon and causes intestinal aganglionosis in mice

Journal of Clinical Investigation

Volumn 118, Issue 5, 2008, Pages 1890-1898

  Uesaka, Toshihiro ^a   Nagashimada, Mayumi ^a   Yonemura, Shigenobu ^a   Enomoto, Hideki ^a  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN RET;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; GENE CONTROL; HIRSCHSPRUNG DISEASE; INTESTINE CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; APOPTOSIS; CELL MOVEMENT; CELL SURVIVAL; COLON; DISEASE MODELS, ANIMAL; ENTERIC NERVOUS SYSTEM; FEMALE; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; HIRSCHSPRUNG DISEASE; HUMANS; MALE; MICE; MICE, KNOCKOUT; NEURONS; PROTO-ONCOGENE PROTEINS C-RET;

EID: 43049141138     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI34425     Document Type: Article

References (39)

1. Badner, J.A., Sieber, W.K., Garver, K.L., and Chakravarti, A. 1990. A genetic study of Hirschsprung disease. Am. J. Hum. Genet. 46:568-580.
2. Skinner, M.A. 1996. Hirschsprung's disease. Curr. Probl. Surg. 33:389-460.
3. Parisi, M.A., and Kapur, R.P. 2000. Genetics of Hirschsprung disease. Curr. Opin. Pediatr. 12:610-617.
4. Amiel, J., and Lyonnet, S. 2001. Hirschsprung disease, associated syndromes, and genetics: a review. J. Med. Genet. 38:729-739.
5. Passarge, E. 2002. Dissecting Hirschsprung disease. Nat. Genet. 31:11-12.
6. Edery, P., et al. 1994. Mutations of the RET proto-oncogene in Hirschsprung's disease. Nature. 367:378-380.
7. Romeo, G., et al. 1994. Point mutations affecting the tyrosine kinase domain of the RET proto-oncogene in Hirschsprung's disease. Nature. 367:377-378.
8. Airaksinen, M.S., and Saarma, M. 2002. The GDNF family: signalling, biological functions and therapeutic value. Nat. Rev. Neurosci. 3:383-394.
9. Baloh, R.H., Enomoto, H., Johnson, E.M., Jr., and Milbrandt, J. 2000. The GDNF family ligands and receptors - implications for neural development. Curr. Opin. Neurobiol. 10:103-110.
10. Natarajan, D., Marcos-Gutierrez, C., Pachnis, V., and de Graaff, E. 2002. Requirement of signalling by receptor tyrosine kinase RET for the directed migration of enteric nervous system progenitor cells during mammalian embryogenesis. Development. 129:5151-5160.
11. Schuchardt, A., D'Agati, V., Larsson-Blomberg, L., Costantini, F., and Pachnis, V. 1994. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature. 367:380-383.
12. Young, H.M., et al. 2001. GDNF is a chemoattractant for enteric neural cells. Dev. Biol. 229:503-516.
13. Chalazonitis, A., Rothman, T.P., Chen, J., and Gershon, M.D. 1998. Age-dependent differences in the effects of GDNF and NT-3 on the development of neurons and glia from neural crest-derived precursors immunoselected from the fetal rat gut: expression of GFRalpha-1 in vitro and in vivo. Dev. Biol. 204:385-406.
14. Heuckeroth, R.O., Lampe, P.A., Johnson, E.M., and Milbrandt, J. 1998. Neurturin and GDNF promote proliferation and survival of enteric neuron and glial progenitors in vitro. Dev. Biol. 200:116-129.
15. Taraviras, S., et al. 1999. Signalling by the RET receptor tyrosine kinase and its role in the development of the mammalian enteric nervous system. Development. 126:2785-2797.
16. Uesaka, T., et al. 2007. Conditional ablation of GFRα1 in postmigratory enteric neurons triggers unconventional neuronal death in the colon and causes a Hirschsprung's disease phenotype. Development. 134:2171-2181.
17. Emison, E.S., et al. 2005. A common sex-dependent mutation in a RET enhancer underlies Hirschsprung disease risk. Nature. 434:857-863.
18. Asai, N., et al. 2006. Targeted mutation of serine 697 in the Ret tyrosine kinase causes migration defect of enteric neural crest cells. Development 133:4507-4516.
19. Carniti, C., et al. 2006. The Ret(C620R) mutation affects renal and enteric development in a mouse model of Hirschsprung's disease. Am. J. Pathol. 168:1262-1275.
20. de Graaff, E., et al. 2001. Differential activities of the RET tyrosine kinase receptor isoforms during mammalian embryogenesis. Genes Dev. 15:2433-2444.
21. Jain, S., et al. 2004. Mice expressing a dominant-negative Ret mutation phenocopy human Hirschsprung disease and delineate a direct role of Ret in spermatogenesis. Development. 131:5503-5513.
22. Jijiwa, M., et al. 2004. A targeting mutation of tyrosine 1062 in Ret causes a marked decrease of enteric neurons and renal hypoplasia. Mol. Cell. Biol. 24:8026-8036.
23. Wong, A., et al. 2005. Phosphotyrosine 1062 is critical for the in vivo activity of the Ret9 receptor tyrosine kinase isoform. Mol. Cell. Biol. 25:9661-9673.
24. Santos, H., Mateus, J., and Leal, M.J. 1988. Hirschsprung disease associated with polydactyly, unilateral renal agenesis, hypertelorism, and congenital deafness: a new autosomal recessive syndrome. J. Med. Genet. 25:204-205.
25. Jain, S., Encinas, M., Johnson, E.M., Jr., and Milbrandt, J. 2006. Critical and distinct roles for key RET tyrosine docking sites in renal development. Genes Dev. 20:321-333.
26. Haase, G., et al. 2002. GDNF acts through PEA3 to regulate cell body positioning and muscle innervation of specific motor neuron pools. Neuron. 35:893-905.
27. Young, H.M., et al. 1998. A single rostrocaudal colonization of the rodent intestine by enteric neuron precursors is revealed by the expression of Phox2b, Ret, and p75 and by explants grown under the kidney capsule or in organ culture. Dev. Biol. 202:67-84.
28. Jain, S., et al. 2006. RET is dispensable for maintenance of midbrain dopaminergic neurons in adult mice. J. Neurosci. 26:11230-11238.
29. Kramer, E.R., et al. 2007. Absence of Ret signaling in mice causes progressive and late degeneration of the nigrostriatal system. PLoS Biol. 5:e39.
30. Luo, W., et al. 2007. A hierarchical NGF signaling cascade controls Ret-dependent and Ret-independent events during development of nonpeptidergic DRG neurons. Neuron. 54:739-754.
31. Bordeaux, M.C., et al. 2000. The RET proto-oncogene induces apoptosis: a novel mechanism for Hirschsprung disease. EMBO J. 19:4056-4063.
32. Canibano, C., et al. 2007. The dependence receptor Ret induces apoptosis in somatotrophs through a Pit-1/p53 pathway, preventing tumor growth. EMBO J. 26:2015-2028.
33. Hofstra, R.M., et al. 2000. RET and GDNF gene scanning in Hirschsprung patients using two dual denaturing gel systems. Hum. Mutat. 15:418-429.
34. Griseri, P., et al. 2007. A common variant located in the 3′UTR of the RET gene is associated with protection from Hirschsprung disease. Hum. Mutat. 28:168-176.
35. Enomoto, H., et al. 2001. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development. 128:3963-3974.
36. Hayashi, S., and McMahon, A.P. 2002. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 244:305-318.
37. Kunath, T., et al. 2005. Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts. Development. 132:1649-1661.
38. Enomoto, H., et al. 1998. GFR α1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron. 21:317-324.
39. Young, H.M., et al. 2004. Dynamics of neural crestderived cell migration in the embryonic mouse gut. Dev. Biol. 270:455-473.