Critical and distinct roles for key RET tyrosine docking sites in renal development

Genes and Development

Volumn 20, Issue 3, 2006, Pages 321-333

  Jain, Sanjay ^a   Encinas, Mario ^a,b   Johnson Jr , Eugene M ^a   Milbrandt, Jeffrey ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b De Ciencies Mediques Basiques   (Spain)

Author keywords

CAKUT; GDNF; Kidney; RET; RTK

Indexed keywords

DOCKING PROTEIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; ISOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN KINASE C GAMMA; PROTEIN RET; PROTEIN RET51; PROTEIN RET9; PROTEIN SH2; PROTEIN SHC; PROTEIN TYROSINE KINASE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAY REGION BINDING SITE; CONGENITAL ANOMALY OF KIDNEY AND THE LOWER URINARY TRACT; CONTROLLED STUDY; EMBRYO; EMBRYONIC STRUCTURES; ENZYME ACTIVATION; GENE MUTATION; GENETIC ASSOCIATION; KIDNEY AGENESIS; KIDNEY DEVELOPMENT; KIDNEY MALFORMATION; KNOCKOUT MOUSE; MEGAURETER; MOLECULAR DYNAMICS; MOUSE; MULTICYSTIC DYSPLASTIC KIDNEY; MUTAGENESIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; URETER MALFORMATION; URINARY TRACT MALFORMATION;

ANIMALS; APOPTOSIS; GONADS; HUMANS; KIDNEY; MICE; MICE, MUTANT STRAINS; MORPHOGENESIS; MUTATION; PHENYLALANINE; PHOSPHOLIPASE C GAMMA; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-RET; SIGNAL TRANSDUCTION; TYROSINE; URETER;

ANIMALIA; MURINAE; WOLFFIA;

EID: 32044436042     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1387206     Document Type: Article

References (61)

1. Abe, M. and Naski, M.C. 2004. Regulation of sprouty expression by PLCγ and calcium-dependent signals. Biochem. Biophys. Res. Commun. 323: 1040-1047.
2. Airaksinen, M.S. and Saarma, M. 2002. The GDNF family: Signalling, biological functions and therapeutic value. Nat. Rev. Neurosci. 3: 383-394.
3. Asai, N., Murakami, H., Iwashita, T., and Takahashi, M. 1996. A mutation at tyrosine 1062 in MEN2A-Ret and MEN2B-Ret impairs their transforming activity and association with shc adaptor proteins. J. Biol. Chem. 271: 17644-17649.
4. Baloh, R.H., Enomoto, H., Johnson Jr., E.M., and Milbrandt, J. 2000. The GDNF family ligands and receptors - Implications for neural development. Curr. Opin. Neurobiol. 10: 103-110.
5. Basson, M.A., Akbulut, S., Watson-Johnson, J., Simon, R., Carroll, T.J., Shakya, R., Gross, I., Martin, G.R., Lufkin, T., McMahon, A.P., et al. 2005. Sprouty1 is a critical regulator of GDNF/RET-mediated kidney induction. Dev. Cell 8: 229-239.
6. Batourina, E., Choi, C., Paragas, N., Bello, N., Hensle, T., Costantini, F.D., Schuchardt, A., Bacallao, R.L., and Mendelsohn, C.L. 2002. Distal ureter morphogenesis depends on epithelial cell remodeling mediated by vitamin A and Ret. Nat. Genet. 32: 109-115.
7. Besset, V., Scott, R.P., and Ibanez, C.F. 2000. Signaling complexes and protein-protein interactions involved in the activation of the Ras and phosphatidylinositol 3-kinase pathways by the c-Ret receptor tyrosine kinase. J. Biol. Chem. 275: 39159-39166.
8. Borrello, M.G., Mercalli, E., Perego, C., Degl'Innocenti, D., Ghizzoni, S., Arighi, E., Eroini, B., Rizzetti, M.G., and Pierotti, M.A. 2002. Differential interaction of Enigma protein with the two RET isoforms. Biochem. Biophys. Res. Commun. 296: 515-522.
9. Cabaner, C., Gajate, C., Macho, A., Munoz, E., Modolell, M., and Mollinedo, F. 1999. Induction of apoptosis in human mitogen-activated peripheral blood T-lymphocytes by the ether phospholipid ET-18-OCH3: Involvement of the Fas receptor/ ligand system. Br. J. Pharmacol. 127: 813-825.
10. 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.
11. Cheng, H.T., Miner, J.H., Lin, M., Tansey, M.G., Roth, K., and Kopan, R. 2003. γ-Secretase activity is dispensable for mesenchyme-to-epithelium transition but required for podocyte and proximal tubule formation in developing mouse kidney. Development 130: 5031-5042.
12. Chi, L., Zhang, S., Lin, Y., Prunskaite-Hyyrylainen, R., Vuolteenaho, R., Itaranta, P., and Vainio, S. 2004. Sprouty proteins regulate ureteric branching by coordinating reciprocal epithelial Wnt11, mesenchymal Gdnf and stromal Fgf7 signalling during kidney development. Development 131: 3345-3356.
13. Degl'Innocenti, D., Arighi, E., Popsueva, A., Sangregorio, R., Alberti, L., Rizzetti, M.G., Ferrario, C., Sariola, H., Pierotti, M.A., and Borrello, M.G. 2004. Differential requirement of Tyr1062 multidocking site by RET isoforms to promote neural cell scattering and epithelial cell branching. Oncogene 23: 7297-7309.
14. 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.
15. Encinas, M., Crowder, R.J., Milbrandt, J., and Johnson Jr., E.M. 2004. Tyrosine 981, a novel ret autophosphorylation site, binds c-Src to mediate neuronal survival. J. Biol. Chem. 279: 18262-18269.
16. Enomoto, H., Araki, T., Jackman, A., Heuckeroth, R.O., Snider, W.D., Johnson Jr., E.M., and Milbrandt, J. 1998. GFR α1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 21: 317-324.
17. 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.
18. Enomoto, H., Crawford, P.A., Gorodinsky, A., Heuckeroth, R.O., Johnson Jr., E.M., and Milbrandt, J. 2001. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 128: 3963-3974.
19. Fisher, C.E., Michael, L., Barnett, M.W., and Davies, J.A. 2001. Erk MAP kinase regulates branching morphogenesis in the developing mouse kidney. Development 128: 4329-4338.
20. Gajate, C. and Mollinedo, F. 2002. Biological activities, mechanisms of action and biomedical prospect of the antitumor ether phospholipid ET-18-OCH(3) (edelfosine), a proapoptotic agent in tumor cells. Curr. Drug Metab. 3: 491-525.
21. Grieshammer, U., Le, M., Plump, A.S., Wang, F., Tessier-Lavigne, M., and Martin, G.R. 2004. SLIT2-mediated ROBO2 signaling restricts kidney induction to a single site. Dev. Cell 6: 709-717.
22. Grisaru, S., Cano-Gauci, D., Tee, J., Filmus, J., and Rosenblum, N.D. 2001. Glypican-3 modulates BMP- and FGF-mediated effects during renal branching morphogenesis. Dev. Biol. 231: 31-46.
23. + exchanger: Induction mechanisms and treatment implications. Apoptosis 5: 87-89.
24. Hayashi, H., Ichihara, M., Iwashita, T., Murakami, H., Shimono, Y., Kawai, K., Kurokawa, K., Murakumo, Y., Imai, T., Funahashi, H., et al. 2000. Characterization of intracellular signals via tyrosine 1062 in RET activated by glial cell line-derived neurotrophic factor. Oncogene 19: 4469-4475.
25. 2+ requirement, and regulation of M current. J. Gen. Physiol. 126: 243-262.
26. Jain, S., Naughton, C.K., Yang, M., Strickland, A., Vij, K., Encinas, M., Golden, J., Heuckeroth, R., Johnson, E., and Milbrandt, J. 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.
27. Jijiwa, M., Fukuda, T., Kawai, K., Nakamura, A., Kurokawa, K., Murakumo, Y., Ichihara, M., and Takahashi, M. 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.
28. Kim, H.J. and Bar-Sagi, D. 2004. Modulation of signalling by Sprouty: A developing story. Nat. Rev. Mol. Cell Biol. 5: 441-450.
29. Lechner, M.S. and Dressler, G.R. 1997. The molecular basis of embryonic kidney development. Mech. Dev. 62: 105-120.
30. Lee, K.Y., Samy, E.T., Sham, M.H., Tam, P.K., and Lui, V.C. 2003. 3′ splicing variants of ret receptor tyrosine kinase are differentially expressed in mouse embryos and in adult mice. Biochim. Biophys. Acta 1627: 26-38.
31. Liu, X., Vega, Q.C., Decker, R.A., Pandey, A., Worby, C.A., and Dixon, J.E. 1996. Oncogenic RET receptors display different autophosphorylation sites and substrate binding specificities. J. Biol. Chem. 271: 5309-5312.
32. Lorenzo, M.J., Gish, G.D., Houghton, C., Stonehouse, T.J., Pawson, T., Ponder, B.A., and Smith, D.P. 1997. RET alternate splicing influences the interaction of activated RET with the SH2 and PTB domains of Shc, and the SH2 domain of Grb2. Oncogene 14: 763-771.
33. Madhani, H.D. 2001. Accounting for specificity in receptor tyrosine kinase signaling. Cell 106: 9-11.
34. 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.
35. McCallion, A.S., Stames, E., Conlon, R.A., and Chakravarti, A. 2003. Phenotype variation in two-locus mouse models of Hirschsprung disease: Tissue-specific interaction between Ret and Ednrb. Proc. Natl. Acad. Sci. 100: 1826-1831.
36. 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.
37. Noia, G., Masini, L., Caruso, A., Perrelli, L., Calisti, A., Salvaggio, E., and Mancuso, S. 1989. Prenatal diagnosis of congenital uropathies. Fetal Ther. 4 Suppl 1: 40-51.
38. Orian-Rousseau, V., Chen, L., Sleeman, J.P., Herrlich, P., and Ponta, H. 2002. CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes & Dev. 16: 3074-3086.
39. Pandini, G., Frasca, F., Mineo, R., Sciacca, L., Vigneri, R., and Belfiore, A. 2002. Insulin/insulin-like growth factor I hybrid receptors have different biological characteristics depending on the insulin receptor isoform involved. J. Biol. Chem. 277: 39684-39695.
40. 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.
41. Pope, J.C.T., Brock III, J.W., Adams, M.C., Stephens, F.D., and Ichikawa, I. 1999. How they begin and how they end: Classic and new theories for the development and deterioration of congenital anomalies of the kidney and urinary tract, CAKUT. J. Am. Soc. Nephrol. 10: 2018-2028.
42. Rogers, S.A., Ryan, G., and Hammerman, M.R. 1991. Insulin-like growth factors I and II are produced in the metanephros and are required for growth and development in vitro. J. Cell Biol. 113: 1447-1453.
43. Rossel, M., Pasini, A., Chappuis, S., Geneste, O., Fournier, L., Schuffenecker, I., Takahashi, M., van Grunsven, L.A., Urdiales, J.L., Rudkin, B.B., et al. 1997. Distinct biological properties of two RET isoforms activated by MEN 2A and MEN 2B mutations. Oncogene 14: 265-275.
44. Sainio, K., Suvanto, P., Saarma, M., Arumαe, U., Lindahl, M., Davies, J.A., and Sariola, H. 1997. Glial cell-line derived neurotrophic factor is a morphogen for the ureteric bud epithelium. Development 124: 4077-4087.
45. 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.
46. Sariola, H. and Saarma, M. 2003. Novel functions and signalling pathways for GDNF. J. Cell Sci. 116 (Pt 19): 3855-3862.
47. 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.
48. 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.
49. Schuetz, G., Rosario, M., Grimm, J., Boeckers, T.M., Gundelfinger, E.D., and Birchmeier, W. 2004. The neuronal scaffold protein Shank3 mediates signaling and biological function of the receptor tyrosine kinase Ret in epithelial cells. J. Cell Biol. 167: 945-952.
50. Segouffin-Cariou, C. and Billaud, M. 2000. Transforming ability of MEN2A-RET requires activation of the phosphatidylinositol 3-Kinase/AKT signaling pathway. J. Biol. Chem. 275: 3568-3576.
51. Shirane, M., Sawa, H., Kobayashi, Y., Nakano, T., Kitajima, K., Shinkai, Y., Nagashima, K., and Negishi, I. 2001. Deficiency of phospholipase C-γ1 impairs renal development and hematopoiesis. Development 128: 5173-5180.
52. Skinner, M.A., Kalyanaraman, S., Safford, S.D., Heuckeroth, R.O., Tourtellotte, W., Goyeau, D., Goodfellow, P., Milbrandt, J.D., and Freemerman, A. 2005. A human yeast artificial chromosome containing the multiple endocrine neoplasia type 2B Ret mutation does not induce medullary thyroid carcinoma but does support the growth of kidneys and partially rescues enteric nervous system development in Ret-deficient mice. Am. J. Pathol. 166: 265-274.
53. Srinivas, S., Wu, Z., Chen, C.M., D'Agati, V., and Costantini, F. 1999. Dominant effects of RET receptor misexpression and ligand-independent RET signaling on ureteric bud development. Development 126: 1375-1386.
54. 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.
55. Takahashi, M. 2001. The GDNF/RET signaling pathway and human diseases. Cytokine Growth Factor Rev. 12: 361-373.
56. Tang, M.J., Cai, Y., Tsai, S.J., Wang, Y.K., and Dressler, G.R. 2002. Ureteric bud outgrowth in response to RET activation is mediated by phosphatidylinositol 3-kinase. Dev. Biol. 243: 128-136.
57. Tsui-Pierchala, B.A., Ahrens, R.C., Crowder, R.J., Milbrandt, J., and Johnson Jr., E.M. 2002. The long and short isoforms of Ret function as independent signaling complexes. J. Biol. Chem. 277: 34618-34625.
58. Vize, P.D., Woolf, A.S., and Bard, J.B.L. 2003. The kidney from normal development to congenital disease. Academic Press, London.
59. Wong, A., Bogni, S., Kotka, P., de Graaff, E., D'Agati, V., Costantini, F., and Pachnis, V. 2005. Phosphotyrosine 1062 is critical for the in vivo activity of the Ret9 receptor tyrosine kinase isoform. Mol. Cell. Biol. 24: 9661-9673.
60. Woolf, A.S. and Thiruchelvam, N. 2001. Congenital obstructive uropathy: Its origin and contribution to end-stage renal disease in children. Adv. Ren. Replace Ther. 8: 157-163.
61. Yu, J., McMahon, A.P., and Valerius, M.T. 2004. Recent genetic studies of mouse kidney development. Curr. Opin. Genet. Dev. 14: 550-557.