Traditional and targeted exome sequencing reveals common, rare and novel functional deleterious variants in RET-signaling complex in a cohort of living US patients with urinary tract malformations

Human Genetics

Volumn 131, Issue 11, 2012, Pages 1725-1738

  Chatterjee, Rajshekhar ^a   Ramos, Enrique ^a   Hoffman, Mary ^a   Vanwinkle, Jessica ^a   Martin, Daniel R ^a   Davis, Thomas K ^a   Hoshi, Masato ^a   Hmiel, Stanley P ^a   Beck, Anne ^a   Hruska, Keith ^a   Coplen, Doug ^a   Liapis, Helen ^a   Mitra, Robi ^a   Druley, Todd ^a   Austin, Paul ^a   Jain, Sanjay ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN RET; SPROUTY PROTEIN;

ADULT; AGED; ARTICLE; COHORT ANALYSIS; CONGENITAL ANOMALY OF THE KIDNEY OR URINARY TRACT; CONTROLLED STUDY; CRYPTORCHISM; ENZYME ACTIVITY; EXOME; FEMALE; GENE MUTATION; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HUMAN; HUMAN CELL; IN VITRO STUDY; KIDNEY AGENESIS; KIDNEY DYSPLASIA; KIDNEY MALFORMATION; MAJOR CLINICAL STUDY; MALE; MEGAURETER; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; UNITED STATES; URINARY TRACT MALFORMATION;

ADOLESCENT; ADULT; AMINO ACID SEQUENCE; BLOTTING, WESTERN; CELLS, CULTURED; COHORT STUDIES; EXOME; FEMALE; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; HUMANS; MALE; MEMBRANE PROTEINS; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PEDIGREE; PHENOTYPE; PHOSPHOPROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTO-ONCOGENE PROTEINS C-RET; SEQUENCE HOMOLOGY, AMINO ACID; UNITED STATES; URINARY TRACT; VESICO-URETERAL REFLUX; YOUNG ADULT;

MUS;

EID: 84867575832     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-012-1181-3     Document Type: Article

References (40)

1. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR (2010) A method and server for predicting damaging missense mutations. Nat Methods 7:248-249
2. Akbulut S, Reddi AL, Aggarwal P, Ambardekar C, Canciani B, Kim MKH, Hix L, Vilimas T, Mason J, Basson MA, Lovatt M, Powell J, Collins S, Quatela S, Phillips M, Licht JD (2010) Sprouty proteins inhibit receptor-mediated activation of phosphatidylinositol-specific phospholipase C. Mol Biol Cell 21:3487-3496
3. Amiel J, Salomon R, Attie T, Pelet A, Trang H, Mokhtari M, Gaultier C, Munnich A, Lyonnet S (1998) Mutations of the RET-GDNF signaling pathway in Ondine's curse. Am J Hum Genet 62:715-717 (Pubitemid 28164631)
4. Baloh RH, Enomoto H, Johnson EM Jr, Milbrandt J (2000) The GDNF family ligands and receptorsimplications for neural development. Curr Opin Neurobiol 10:103-110 (Pubitemid 30102862)
5. Basson MA, Akbulut S, Watson-Johnson J, Simon R, Carroll TJ, Shakya R, Gross I, Martin GR, Lufkin T, McMahon AP, Wilson PD, Costantini FD, Mason IJ, Licht JD (2005) Sprouty1 is a critical regulator of GDNF/RET-mediated kidney induction. Dev Cell 8:229-239 (Pubitemid 40197739)
6. Batourina E, Choi C, Paragas N, Bello N, Hensle T, Costantini FD, Schuchardt A, Bacallao RL, Mendelsohn CL (2002) Distal ureter morphogenesis depends on epithelial cell remodeling mediated by vitamin A and Ret. Nat Genet 32:109-115 (Pubitemid 34977205)
7. Borrello MG, Aiello A, Peissel B, Rizzetti MG, Mondellini P, Degl'Innocenti D, Catalano V, Gobbo M, Collini P, Bongarzone I, Pierotti MA, Greco A, Seregni E (2011) Functional characterization of the MTC-associated germline RET-K666E mutation: evidence of oncogenic potential enhanced by the G691S polymorphism. Endocr Relat Cancer 18:519-527
8. Darlow JM, Molloy NHN, Green AJ, Puri P, Barton DE (2009) The increased incidence of the RET p.Gly691Ser variant in French-Canadian vesicoureteric reflux patients is not replicated by a larger study in Ireland. Hum Mutat 30:E612-E617
9. Dressler GR (2006) The cellular basis of kidney development. Annu Rev Cell Dev Biol 22:509-529
10. Encinas M, Rozen EJ, Dolcet X, Jain S, Comella JX, Milbrandt J, Johnson EM (2008) Analysis of Ret knockin mice reveals a critical role for IKKs, but not PI 3-K, in neurotrophic factor-induced survival of sympathetic neurons. Cell Death Differ 15:1510-1521
11. Enomoto H, Araki T, Jackman A, Heuckeroth RO, Snider WD, Johnson EM Jr, Milbrandt J (1998) GFR α1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 21:317-324 (Pubitemid 28399692)
12. Ghosh S, Krux F, Binder V, Gombert M, Niehues T, Feyen O, Laws H-J, Borkhardt A, on behalf of PIDNETGNoPID (2012) Array based sequence capture and next generation sequencing for identification of primary immunodeficiencies. Scand J Immunol 75:350-354
13. Gustin JA, Yang M, Johnson EM, Milbrandt J (2007) Deciphering adaptor specificity in GFL-dependent RET-mediated proliferation and neurite outgrowth. J Neurochem 102:1184-1194 (Pubitemid 47174234)
14. Heanue TA, Pachnis V (2007) Enteric nervous system development and Hirschsprung's disease: advances in genetic and stem cell studies. Nat Rev Neurosci 8:466-479 (Pubitemid 46789228)
15. Jain S (2009) The many faces of RET dysfunction in kidney. Organogenesis 5:1-14
16. Jain S, Naughton CK, Yang M, Strickland A, Vij K, Encinas M, Golden J, Gupta A, Heuckeroth R, Johnson EM Jr, Milbrandt J (2004a) Mice expressing a dominant-negative Ret mutation phenocopy human Hirschsprung disease and delineate a direct role of Ret in spermatogenesis. Development 131:5503-5513 (Pubitemid 39562192)
17. Jain S, Watson MA, DeBenedetti MK, Hiraki Y, Moley JF, Milbrandt J (2004b) Expression profiles provide insights into early malignant potential and skeletal abnormalities in multiple endocrine neoplasia type 2B syndrome tumors. Cancer Res 64:3907-3913 (Pubitemid 38697303)
18. Jain S, Encinas M, Johnson EM Jr, Milbrandt J (2006) Critical and distinct roles for key RET tyrosine docking sites in renal development. Genes Dev 20:321-333 (Pubitemid 43200286)
19. Jain S, Knoten A, Hoshi M, Wang H, Vohra BP, Heuckeroth RO, Milbrandt J (2010) Organotypic specificity of RET-docking tyrosine residues in pathogenesis of neurocristopathies and renal malformations. JCI 120:778-790
20. Jeanpierre C, Mace G, Parisot M, Moriniere V, Pawtowsky A, Benabou M, Martinovic J, Amiel J, Attie-Bitach T, Delezoide AL, Loget P, Blanchet P, Gaillard D, Gonzales M, Carpentier W, Nitschke P, Tores F, Heidet L, Antignac C, Salomon R (2011) RET and GDNF mutations are rare in fetuses with renal agenesis or other severe kidney development defects. J Med Genet 48:497-504
21. Li B, Leal SM (2009) Discovery of rare variants via sequencing: implications for the design of complex trait association studies. PLoS Genet 5:e1000481
22. Liu L, Okada S, Kong XF, Kreins AY, Cypowyj S, Abhyankar A, Toubiana J, Itan Y, Audry M, Nitschke P, Masson C, Toth B, Flatot J, Migaud M, Chrabieh M, Kochetkov T, Bolze A, Borghesi A, Toulon A, Hiller J, Eyerich S, Eyerich K, Gulácsy V, Chernyshova L, Chernyshov V, Bondarenko A, Grimaldo RM, Blancas-Galicia L, Beas IM, Roesler J, Magdorf K, Engelhard D, Thumerelle C, Burgel PR, Hoernes M, Drexel B, Seger R, Kusuma T, Jansson AF, Sawalle-Belohradsky J, Belohradsky B, Jouanguy E, Bustamante J, Bué M, Karin N, Wildbaum G, Bodemer C, Lortholary O, Fischer A, Blanche S, Al-Muhsen S, Reichenbach J, Kobayashi M, Rosales FE, Lozano CT, Kilic SS, Oleastro M, Etzioni A, Traidl-Hoffmann C, Renner ED, Abel L, Picard C, Maródi L, Boisson-Dupuis S, Puel A, Casanova JL (2011) Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronic mucocutaneous candidiasis. J Exp Med 208:1635-1648
23. Michos O, Cebrian C, Hyink D, Grieshammer U, Williams L, D'Agati V, Licht JD, Martin GR, Costantini F (2010) Kidney development in the absence of Gdnf and Spry1 requires Fgf10. PLoS Genet 6:e1000809
24. Moore MW, Klein RD, Farinas I, Sauer H, Armanini M, Phillips H, Reichart LF, Ryan AM, Carver-Moore K, Rosenthal A (1996) Renal and neuronal abnormalities in mice lacking GDNF. Nature 382:76-79 (Pubitemid 26243361)
25. Ng SB, Turner EH, Robertson PD, Flygare SD, Bigham AW, Lee C, Shaffer T, Wong M, Bhattacharjee A, Eichler EE, Bamshad M, Nickerson DA, Shendure J (2009) Targeted capture and massively parallel sequencing of 12 human exomes. Nature 461:272-276
26. Ng SB, Buckingham KJ, Lee C, Bigham AW, Tabor HK, Dent KM, Huff CD, Shannon PT, Jabs EW, Nickerson DA, Shendure J, Bamshad MJ (2010) Exome sequencing identifies the cause of a Mendelian disorder. Nat Genet 42:30-35
27. Pichel JG, Shen L, Hui SZ, Granholm A-C, Drago J, Grinberg A, Lee EJ, Huang SP, Saarma M, Hoffer BJ, Sariola H, Westphal H (1996) Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 382:73-76 (Pubitemid 26243360)
28. Pope JCt, Brock JW 3rd, Adams MC, Stephens FD, 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 (Pubitemid 29402525)
29. Rozen EJ, Schmidt H, Dolcet X, Basson MA, Jain S, Encinas M (2009) Loss of Sprouty1 rescues renal agenesis caused by Ret mutation. J Am Soc Nephrol 20:255-259
30. Salomon R, Attie T, Pelet A, Bidaud C, Eng C, Amiel J, Sarnacki S, Goulet O, Ricour C, Nihoul-Fekete C, Munnich A, Lyonnet S (1996) Germline mutations of the RET ligand GDNF are not sufficient to cause Hirschsprung disease. Nat Genet 14:345-347
31. Sanchez MP, Silos-Santiago I, Frisen J, He B, Lira SA, Barbacid M (1996) Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 382:70-73 (Pubitemid 26243359)
32. Sasieni PD (1997) From genotypes to genes: doubling the sample size. Biometrics 53:1253-1261 (Pubitemid 28013569)
33. Schuchardt A, D'Agati V, Larsson-Blomberg L, Costantini F, Pachnis V (1994) Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 367:380-383
34. Skinner MA, Kalyanaraman S, Safford SD, Heuckeroth RO, Tourtellotte W, Goyeau D, Goodfellow P, Milbrandt JD, 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 (Pubitemid 40051678)
35. Skinner MA, Safford SD, Reeves JG, Jackson ME, Freemerman AJ (2008) Renal aplasia in humans is associated with RET mutations. Am J Hum Genet 82:344-351
36. Song R, Yosypiv I (2011) Genetics of congenital anomalies of the kidney and urinary tract. Pediatr Nephrol 26:353-364
37. Tsui-Pierchala BA, Ahrens RC, Crowder RJ, Milbrandt J, Johnson EM Jr (2002) The long and short isoforms of Ret function as independent signaling complexes. J Biol Chem 277:34618-34625
38. Yang Y, Houle AM, Letendre J, Richter A (2008) RET Gly691Ser mutation is associated with primary vesicoureteral reflux in the French-Canadian population from Quebec. Hum Mutat 29:695-702 (Pubitemid 351614594)
39. Yu OH, Murawski IJ, Myburgh DB, Gupta IR (2004) Overexpression of RET leads to vesicoureteric reflux in mice. Am J Physiol Renal Physiol 287:F1123-F1130 (Pubitemid 39517012)
40. Zhang Z, Quinlan J, Grote D, Lemire M, Hudson T, Benjamin A, Roy A, Pascuet E, Goodyer M, Raju C, Houghton F, Bouchard M, Goodyer P (2009) Common variants of the glial cell-derived neurotrophic factor gene do not influence kidney size of the healthy newborn. Pediatr Nephrol 24:1151-1157