Mice expressing a dominant-negative Ret mutation phenocopy human Hirschsprung disease and delineate a direct role of Ret in spermatogenesis

Development

Volumn 131, Issue 21, 2004, Pages 5503-5513

  Jain, Sanjay ^a   Naughton, Cathy K ^a   Yang, Mao ^a   Strickland, Amy ^a   Vij, Kiran ^a   Encinas, Mario ^a   Golden, Judy ^a   Gupta, Akshay ^a   Heuckeroth, Robert ^a   Johnson Jr , Eugene M ^a   Milbrandt, Jeffrey ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

GDNF; Hirschsprung disease; Ret; Spermatogenesis

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; PHOSPHOTRANSFERASE; PROTEIN KINASE B; PROTEIN RET;

ADRENERGIC SYSTEM; ANIMAL TISSUE; ARTICLE; CELL COUNT; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DISEASE SEVERITY; ENZYME ACTIVATION; ENZYME ACTIVITY; FLOW CYTOMETRY; GENE EXPRESSION; GENE MUTATION; HIRSCHSPRUNG DISEASE; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KIDNEY DEVELOPMENT; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULE; SPERMATOGENESIS; STOMACH MOTILITY; TESTIS;

ALLELES; ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, DOMINANT; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; HIRSCHSPRUNG DISEASE; HUMANS; KIDNEY; MALE; MICE; MICE, TRANSGENIC; MUTATION; NERVOUS SYSTEM; NEURONS; PHOSPHOTRANSFERASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-RET; RECEPTOR PROTEIN-TYROSINE KINASES; SPERMATOGENESIS; SURVIVAL RATE;

ANIMALIA;

EID: 9444225531     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01421     Document Type: Article

References (51)

1. Airaksinen, M. S. and Saarma, M. (2002). The GDNF family: signalling, biological functions and therapeutic value. Nat. Rev. Neurosci. 3, 383-394.
2. 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.
3. Barrow, J. R. and Capecchi, M. R. (1996). Targeted disruption of the Hoxb-2 locus in mice interferes with expression of Hoxb-1 and Hoxb-4. Development 122, 3817-3828.
4. Beck, K. D., Valverde, J., Alexi, T., Poulsen, K., Moffat, B., Vandlen, R. A., Rosenthal, A. and Hefti, F. (1995). Mesencephalic dopaminergic neurons protected by GDNF from axotomy-induced degeneration in the adult brain. Nature 373, 339-341.
5. Bennett, D. L., Michael, G. J., Ramachandran, N., Munson, J. B., Averill, S., Yan, Q., McMahon, S. B. and Priestley, J. V. (1998). A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J. Neurosci. 18, 3059-3072.
6. Bowenkamp, K. E., Hoffman, A. F., Gerhardt, G. A., Henry, M. A., Biddle, P. T., Hoffer, B. J. and Granholm, A.-C. E. (1995). Glial cell line-derived neurotrophic factor supports survival of injured midbrain dopaminergic neurons. J. Comp. Neurol. 355, 479-489.
7. Cacalano, G., Farinas, I., Wang, L.-C., Hagler, K., Forgie, A., Moore, M., Armanini, M., Phillips, H., Ryan, A. M., Reichardt, L. F. et al. (1998). GFRα1 is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron 21, 53-62.
8. Clarke, P. G. and Oppenheim, R. W. (1995). Neuron death in vertebrate development: in vitro methods. Methods Cell Biol. 46, 277-321.
9. Crowder, R. J., Enomoto, H., Yang, M., Johnson, E. M., Jr and Milbrandt, J. (2004). Dok-6, a novel p62 Dok family member, promotes Ret-mediated neurite outgrowth. J. Biol. Chem. 279, 42072-42081.
10. Davies, J. A. and Fisher, C. E. (2002). Genes and proteins in renal development. Exp. Nephrol. 10, 102-113.
11. de Graaff, E., Srinivas, S., Kilkenny, C., D'Agati, V., Mankoo, B. S., Costantini, F. and Pachnis, V. (2001). Differential activities of the RET tyrosine kinase receptor isoforms during mammalian embryogenesis. Genes Dev. 15, 2433-2444.
12. Encinas, M., Crowder, R. J., Milbrandt, J. and Johnson, E. M., Jr (2004). Tyrosine 981, a novel ret autophosphorylation site, binds c-Src to mediate neuronal survival. J. Biol. Chem. 279, 18262-18269.
13. Enders, G. C. and May, J. J., II (1994). Developmentally regulated expression of a mouse germ cell nuclear antigen examined from embryonic day 11 to adult in male and female mice. Dev. Biol. 163, 331-340.
14. Enomoto, H., Araki, T., Jackman, A., Heuckeroth, R. O., Snider, W. D., Johnson, E. M., Jr and Milbrandt, J. (1998). GFR α1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 21, 317-324.
15. Enomoto, H., Heuckeroth, R. O., Golden, J. P., Johnson, E. M. and Milbrandt, J. (2000). Development of cranial parasympathetic ganglia requires sequential actions of GDNF and neurturin. Development 127, 4877-4889.
16. Enomoto, H., Crawford, P. A., Gorodinsky, A., Heuckeroth, R. O., Johnson, E. M., Jr and Milbrandt, J. (2001). RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 128, 3963-3974.
17. Geneste, O., Bidaud, C., de Vita, G., Hofstra, R. M., Tartare-Deckert, S., Buys, C. H., Lenoir, G. M., Santoro, M. and Billaud, M. (1999). Two distinct mutations of the RET receptor causing Hirschsprung's disease impair the binding of signalling effectors to a multifunctional docking site. Hum. Mol. Genet. 8, 1989-1999.
18. Gianino, S., Grider, J. R., Cresswell, J., Enomoto, H. and Heuckeroth, R. O. (2003). GDNF availability determines enteric neuron number by controlling precursor proliferation. Development 130 2187-2198.
19. Henderson, C. E., Phillips, H. S., Pollock, R. A., Davies, A. M., Lemeulle, C., Armanini, M., Simpson, L. C., Moffet, B., Vandlen, R. A., Koliatsos, V. E. et al. (1994). GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266, 1062-1064.
20. Heuckeroth, R. O., Enomoto, H., Grider, J. R., Golden, J. P., Hanke, J. A, Jackman, A., Molliver, D. C., Bardgett, M. E., Snider, W. D., Johnson, E. M., Jr et al. (1999). Gene targeting reveals a critical role for neurturin in the development and maintenance of enteric, sensory, and parasympathetic neurons. Neuron 22, 253-263.
21. Homma, S., Yaginuma, H., Vinsant, S., Seino, M., Kawata, M., Gould, T., Shimada, T., Kobayashi, N. and Oppenheim, R. W. (2003 . Differential expression of the GDNF family receptors PET and GFRalpha1, 2, and 4 in subsets of motoneurons: a relationship between motoneuron birthdate and receptor expression. J. Comp. Neurol. 456, 245-259.
22. Iwashita, T., Kurokawa, K., Qiao, S., Murakami, H., Asai, N., Kawai, K., Hashimoto, M., Watanabe, T., Ichihara, M. and Takahashi, M. (2001). Functional analysis of PET with Hirschsprung mutations affecting its kinase domain. Gastroenterology 121, 24-33.
23. Lechner, M. S. and Dressier, G. R. (1997). The molecular basis of embryonic kidney development. Mech. Dev. 62 105-120.
24. Lee, D. C., Chan, K. W. and Chan, S. Y. (2002). PET receptor tyrosine kinase isoforms in kidney function and disease. Oncogene 21, 5582-5592.
25. Lin, L.-F. H., Doherty, D. H., Lile, J. D., Bektesh, S. and Collins, F. (1993). GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260, 1130-1132.
26. Lois, C., Hong, E. J., Pease, S., Brown, E. J. and Baltimore, D. (2002). Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295, 868-872.
27. Majumdar, A., Vainio, S., Kispert, A., McMahon, J. and McMahon, A. P. (2003). Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development. Development 130, 3175-3185.
28. Meng, X., Lindahl, M., Hyvonen, M. E., Parvinen, M., de Rooij, D. G., Hess, M. W., Raatikainen-Ahokas, A., Sainio, K., Rauvala, H., Lakso, M. et al. (2000). Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287, 1489-1493.
29. Meyers, E. N., Lewandoski, M. and Martin, G. R. (1998). An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 18, 136-141.
30. Molliver, D. C., Wright, D. E., Leitner, M. L., Parsadanian, A. S., Doster, K., Wen, D., Yan, Q. and Snider, W. D. (1997). IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19, 849-861.
31. Moore, M. W., Klein, R. D., Farinas, I., Sauer, H., Armanini, M., Phillips, H., Reichart, L. F., Ryan, A. M., Carver-Moore, K. and Rosenthal, A. (1996). Renal and neuronal abnormalities in mice lacking GDNF. Nature 382, 76-79.
32. Naldini, L., Blomer, U., Gage, F. H., Trono, D. and Verma, I. M. (1996). Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Acad. Sci. USA 93, 11382-11388.
33. Natarajan, D., Marcos-Guitierrez, C., Pachnis, V. and de Graaff, E. (2002). Requirement of signalling by receptor tyrosine kinase PET for the directed migration of enteric nervous system progenitor cells during mammalian embryogenesis. Development 129 5151-5160.
34. Oppenheim, R. W., Houenou, L. J., Johnson, J. E., Lin, L.-F. H., Li, L., Lo, A. C., Newsome, A. L., Prevette, D. M. and Wang, S. (1995). Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature 373, 344-346.
35. Oppenheim, R. W., Houenou, L. J., Parsadanian, A. S., Prevette, D., Snider, W. D. and Shen, L. (2000). Glial cell line-derived neurotrophic factor and developing mammalian motoneurons: regulation of programmed cell death among motoneuron subtypes. J. Neurosci. 20, 5001-5011.
36. Pichel, J. G., Shen, L., Hui, S. Z., Granholm, A.-C., Drago, J., Grinberg, A., Lee, E. J., Huang, S. P., Saarma, M., Hoffer, B. J. et al. (1996). Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 382, 73-76.
37. Ponder, B. A. and Smith, D. (1996). The MEN II syndromes and the role of the ret proto-oncogene. Adv. Cancer Res. 70, 179-222.
38. Rijli, F. M., Dolle, P., Fraulob, V., LeMeur, M. and Chambon, P. (1994). Insertion of a targeting construct in a Hoxd-10 allele can influence the control of Hoxd-9 expression. Dev. Dyn. 201, 366-377.
39. Rossi, J., Luukko, K., Poteryaev, D., Laurikainen, A., Sun, Y. F., Laakso, T., Eerikainen, S., Tuominen, R., Lakso, M., Rauvala, H. et al. (1999). Retarded growth and deficits in the enteric and parasympathetic nervous system in mice lacking GFR alpha2, a functional neurturin receptor. Neuron 22, 243-252.
40. Sanchez, M. P., Silos-Santiago, I., Frisen, J., He, B., Lira, S. A. and Barbacid, M. (1996). Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 382, 70-73.
41. Sariola, H. and Saarma, M. (2003). Novel functions and signalling pathways for GDNF. J. Cell Sci. 116, 3855-3862.
42. 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.
43. Schuchardt, A., D'Agati, V., Pachnis, V. and Costantini, F. (1996). Renal agenesis and hypodysplasia in ret-k-mutant mice result from defects in ureteric bud development. Development 122 1919-1929.
44. Shimotake, T., Go, S., Inoue, K., Tomiyama, H. and Iwai, N. (2001). A homozygous missense mutation in the tyrosine kinase domain of the PET proto-oncogene in an infant with total intestinal aganglionosis. Am. J. Gastroenterol. 96, 1286-1291.
45. Shimotake, T., Tomiyama, H., Aoi, S. and Iwai, N. (2003). Discrepancy between macroscopic and microscopic transitional zones in Hirschsprung[apos ]s disease with reference to the type of PET/GDNF/SOX10 gene mutation. J. Pediatr. Surg. 38, 698-701.
46. Solari, V., Ennis, S., Yoneda, A., Wong, L., Messineo, A., Hollwarth, M. E., Green, A. and Puri, P. (2003). Mutation analysis of the PET gene in total intestinal aganglionosis by wave DNA fragment analysis system. J. Pediatr. Surg. 38, 497-501.
47. Srinivas, S., Wu, Z., Chen, C. M., D'Agati, V. and Costantini, F. (1999). Dominant effects of PET receptor misexpression and ligand-independent RET signaling on ureteric bud development. Development 126, 1375-1386.
48. Svaren, J., Ehrig, T., Abdulkadir, S. A., Ehrengruber, M. U., Watson, M. A. and Milbrandt, J. (2000). EGR1 target genes in prostate carcinoma cells identified by microarray analysis. J. Biol. Chem. 275, 38524-38531.
49. Tang, M. J., Cai, Y., Tsai, S. J., Wang, Y. K. and Dressler, G. R. (2002). Ureteric bud outgrowth in response to PET activation is mediated by phosphatidylinositol 3-kinase. Dev. Biol. 243, 128-136.
50. Tsui-Pierchala, B. A., Ahrens, R. C., Crowder, R. J., Milbrandt, J. and Johnson, E. M., Jr (2002). The long and short isoforms of Ret function as independent signaling complexes. J. Biol. Chem. 277, 34618-34625.
51. Tsuji, H., Spitz, L., Kiely, E. M., Drake, D. P. and Pierro, A. (1999). Management and long-term follow-up of infants with total colonic aganglionosis. J. Pediatr. Surg. 34, 158-161.