Whole-exome sequencing identifies mutations of TBC1D1 encoding a Rab-GTPase-activating protein in patients with congenital anomalies of the kidneys and urinary tract (CAKUT)

Human Genetics

Volumn 135, Issue 1, 2016, Pages 69-87

  Kosfeld, Anne ^a   Kreuzer, Martin ^a   Daniel, Christoph ^b   Brand, Frank ^a   Schäfer, Anne Kathrin ^a   Chadt, Alexandra ^c   Weiss, Anna Carina ^a   Riehmer, Vera ^a   Jeanpierre, Cécile ^d,e   Klintschar, Michael ^a   Bräsen, Jan Hinrich ^a   Amann, Kerstin ^b   Pape, Lars ^a   Kispert, Andreas ^a   Al Hasani, Hadi ^c   Haffner, Dieter ^a   Weber, Ruthild G ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

^d HÔPITAL NECKER ENFANTS MALADES   (France)

^e IMAGINE INSTITUTE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER 4; PROTEIN; RAB PROTEIN; TBC1D1 PROTEIN; UNCLASSIFIED DRUG; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; TBC1D1 PROTEIN, HUMAN;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHILD; CHRONIC KIDNEY DISEASE; CONGENITAL ANOMALIES OF THE KIDNEY AND URINARY TRACT; CONTROLLED STUDY; DEHYDRATION; EXOME; FEMALE; FETUS; FOLLOW UP; GENE FREQUENCY; GENE MUTATION; GENE SEQUENCE; GENETIC VARIABILITY; GLOMERULOSCLEROSIS; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDRONEPHROSIS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INSULIN RESISTANCE; KIDNEY DYSPLASIA; KIDNEY FAILURE; KIDNEY MALFORMATION; MAJOR CLINICAL STUDY; MALE; MEGAURETER; MISSENSE MUTATION; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REAL TIME POLYMERASE CHAIN REACTION; SCHOOL CHILD; SITE DIRECTED MUTAGENESIS; SMOOTH MUSCLE FIBER; URINARY TRACT MALFORMATION; AMINO ACID SEQUENCE; ANIMAL; C57BL MOUSE; CHEMISTRY; GENETICS; HIGH THROUGHPUT SEQUENCING; INFANT; MOLECULAR GENETICS; MUTATION; PEDIGREE; PROCEDURES; SEQUENCE HOMOLOGY; TRANSGENIC MOUSE; UROGENITAL TRACT MALFORMATION; VESICOURETERAL REFLUX; YOUNG ADULT;

ADOLESCENT; ADULT; AMINO ACID SEQUENCE; ANIMALS; CHILD; CHILD, PRESCHOOL; EXOME; FEMALE; GTPASE-ACTIVATING PROTEINS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INFANT; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MUTATION; PEDIGREE; SEQUENCE HOMOLOGY, AMINO ACID; UROGENITAL ABNORMALITIES; VESICO-URETERAL REFLUX; YOUNG ADULT;

EID: 84952719288     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-015-1610-1     Document Type: Article

References (41)

1. An D, Toyoda T, Taylor EB, Yu H, Fujii N, Hirshman MF, Goodyear LJ (2010) TBC1D1 regulates insulin- and contraction-induced glucose transport in mouse skeletal muscle. Diabetes 59:1358–1365. doi:10.2337/db09-1266
2. Boycott KM, Vanstone MR, Bulman DE, MacKenzie AE (2013) Rare-disease genetics in the era of next-generation sequencing: discovery to translation. Nat Rev Genet 14:681–691. doi:10.1038/nrg3555
3. Chadt A, Leicht K, Deshmukh A, Jiang LQ, Scherneck S, Bernhardt U, Dreja T, Vogel H, Schmolz K, Kluge R, Zierath JR, Hultschig C, Hoeben RC, Schürmann A, Joost HG, Al-Hasani H (2008) Tbc1d1 mutation in lean mouse strain confers leanness and protects from diet-induced obesity. Nat Genet 40:1354–1359. doi:10.1038/ng.244
4. Chadt A, Immisch A, de Wendt C, Springer C, Zhou Z, Stermann T, Holman GD, Loffing-Cueni D, Loffing J, Joost HG, Al-Hasani H (2015) Deletion of both Rab-GTPase-activating proteins TBC1D1 and TBC1D4 in mice eliminates insulin- and AICAR-stimulated glucose transport. Diabetes 64:746–759. doi:10.2337/db15-er04
5. Chen S, Murphy J, Toth R, Campbell DG, Morrice NA, Mackintosh C (2008) Complementary regulation of TBC1D1 and AS160 by growth factors, insulin and AMPK activators. Biochem J 409:449–459
6. Classen CF, Riehmer V, Landwehr C, Kosfeld A, Heilmann S, Scholz C, Kabisch S, Engels H, Tierling S, Zivicnjak M, Schacherer F, Haffner D, Weber RG (2013) Dissecting the genotype in syndromic intellectual disability using whole exome sequencing in addition to genome-wide copy number analysis. Hum Genet 132:825–841. doi:10.1007/s00439-013-1296-1
7. Cooper DN, Krawczak M, Polychronakos C, Tyler-Smith C, Kehrer-Sawatzki H (2013) Where genotype is not predictive of phenotype: towards an understanding of the molecular basis of reduced penetrance in human inherited disease. Hum Genet 132:1077–1130. doi:10.1007/s00439-013-1331-2
8. Dash S, Sano H, Rochford JJ, Semple RK, Yeo G, Hyden CS, Soos MA, Clark J, Rodin A, Langenberg C, Druet C, Fawcett KA, Tung YC, Wareham NJ, Barroso I, Lienhard GE, O’Rahilly S, Savage DB (2009) A truncation mutation in TBC1D4 in a family with acanthosis nigricans and postprandial hyperinsulinemia. Proc Natl Acad Sci 106:9350–9355. doi:10.1073/pnas.0900909106
9. Davis TK, Hoshi M, Jain S (2014) To bud or not to bud: the RET perspective in CAKUT. Pediatr Nephrol 29:597–608
10. de Ligt J, Willemsen MH, van Bon BW, Kleefstra T, Yntema HG, Kroes T, Vulto-van Silfhout AT, Koolen DA, de Vries P, Gilissen C, del Rosario M, Hoischen A, Scheffer H, de Vries BB, Brunner HG, Veltman JA, Vissers LE (2012) Diagnostic exome sequencing in persons with severe intellectual disability. N Engl J Med 367:1921–1929. doi:10.1056/NEJMoa1206524
11. Dokas J, Chadt A, Nolden T, Himmelbauer H, Zierath JR, Joost HG, Al-Hasani H (2013) Conventional knockout of Tbc1d1 in mice impairs insulin- and AICAR-stimulated glucose uptake in skeletal muscle. Endocrinology 154:3502–3514. doi:10.1210/en.2012-2147
12. Dorschner MO, Amendola LM, Turner EH, Robertson PD, Shirts BH, Gallego CJ, Bennett RL, Jones KL, Tokita MJ, Bennett JT, Kim JH, Rosenthal EA, Kim DS, National Heart, Lung, and Blood Institute Grand Opportunity Exome Sequencing Project, Tabor HK, Bamshad MJ, Motulsky AG, Scott CR, Pritchard CC, Walsh T, Burke W, Raskind WH, Byers P, Hisama FM, Nickerson DA, Jarvik GP (2013) Actionable, pathogenic incidental findings in 1,000 participants’ exomes. Am J Hum Genet 93:631–640. doi:10.1016/j.ajhg.2013.08.006
13. El Nahas AM, Bassett AH, Cope GH, Le Carpentier JE (1991) Role of growth hormone in the development of experimental renal scarring. Kidney Int 40:29–34
14. Fontanesi L, Bertolini F (2013) The TBC1D1 gene: structure, function, and association with obesity and related traits. Vitam Horm 91:77–95. doi:10.1016/B978-0-12-407766-9.00004-3
15. Frøsig C, Pehmøller C, Birk JB, Richter EA, Wojtaszewski JF (2010) Exercise-induced TBC1D1 Ser237 phosphorylation and 14-3-3 protein binding capacity in human skeletal muscle. J Physiol 588:4539–4548. doi:10.1113/jphysiol.2010.194811
16. Goumenos DS, Brown CB, Shortland J, el Nahas AM (1994) Myofibroblasts, predictors of progression of mesangial IgA nephropathy? Nephrol Dial Transplant 9:1418–1425
17. Guzman J, Jauregui AN, Merscher-Gomez S, Maiguel D, Muresan C, Mitrofanova A, Diez-Sampedro A, Szust J, Yoo TH, Villarreal R, Pedigo C, Molano RD, Johnson K, Kahn B, Hartleben B, Huber TB, Saha J, Burke GW 3rd, Abel ED, Brosius FC, Fornoni A (2014) Podocyte-specific GLUT4-deficient mice have fewer and larger podocytes and are protected from diabetic nephropathy. Diabetes 63:701–714. doi:10.2337/db13-0752
18. Haas CS, Amann K, Schittny J, Blaser B, Müller U, Hartner A (2003) Glomerular and renal vascular structural changes in alpha8 integrin-deficient mice. J Am Soc Nephrol 14:2288–2296
19. Harambat J, van Stralen KJ, Kim JJ, Tizard EJ (2012) Epidemiology of chronic kidney disease in children. Pediatr Nephrol 27:363–373. doi:10.1007/s00467-011-1939-1
20. Humbert C, Silbermann F, Morar B, Parisot M, Zarhrate M, Masson C, Tores F, Blanchet P, Perez MJ, Petrov Y, Khau Van Kien P, Roume J, Leroy B, Gribouval O, Kalaydjieva L, Heidet L, Salomon R, Antignac C, Benmerah A, Saunier S, Jeanpierre C (2014) Integrin alpha 8 recessive mutations are responsible for bilateral renal agenesis in humans. Am J Hum Genet 94:288–294. doi:10.1016/j.ajhg.2013.12.017
21. Hwang DY, Dworschak GC, Kohl S, Saisawat P, Vivante A, Hilger AC, Reutter HM, Soliman NA, Bogdanovic R, Kehinde EO, Tasic V, Hildebrandt F (2014) Mutations in 12 known dominant disease-causing genes clarify many congenital anomalies of the kidney and urinary tract. Kidney Int 85:1429–1433. doi:10.1038/ki.2013.508
22. Hwang DY, Kohl S, Fan X, Vivante A, Chan S, Dworschak GC, Schulz J, van Eerde AM, Hilger AC, Gee HY, Pennimpede T, Herrmann BG, van de Hoek G, Renkema KY, Schell C, Huber TB, Reutter HM, Soliman NA, Stajic N, Bogdanovic R, Kehinde EO, Lifton RP, Tasic V, Lu W, Hildebrandt F (2015) Mutations of the SLIT2-ROBO2 pathway genes SLIT2 and SRGAP1 confer risk for congenital anomalies of the kidney and urinary tract. Hum Genet 134:905–916. doi:10.1007/s00439-015-1570-5
23. Ichikawa I, Kuwayama F, Pope JC 4th, Stephens FD, Miyazaki Y (2002) Paradigm shift from classic anatomic theories to contemporary cell biological views of CAKUT. Kidney Int 61:889–898
24. Jeanpierre C, Macé G, Parisot M, Morinière V, Pawtowsky A, Benabou M, Martinovic J, Amiel J, Attié-Bitach T, Delezoide AL, Loget P, Blanchet P, Gaillard D, Gonzales M, Carpentier W, Nitschke P, Tores F, Heidet L, Antignac C, Salomon R, Société Française de Foetopathologie (2011) RET and GDNF mutations are rare in fetuses with renal agenesis or other severe kidney development defects. J Med Genet 48:497–504. doi:10.1136/jmg.2010.088526
25. Johnston JJ, Rubinstein WS, Facio FM, Ng D, Singh LN, Teer JK, Mullikin JC, Biesecker LG (2012) Secondary variants in individuals undergoing exome sequencing: screening of 572 individuals identifies high-penetrance mutations in cancer-susceptibility genes. Am J Hum Genet 91:97–108. doi:10.1016/j.ajhg.2012.05.021
26. Kane S, Sano H, Liu SC, Asara JM, Lane WS, Garner CC, Lienhard GE (2002) A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain. J Biol Chem 277:22115–22118
27. Katz EB, Stenbit AE, Hatton K, DePinho R, Charron MJ (1995) Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4. Nature 377:151–155
28. Kjær S, Hanrahan S, Totty N, McDonald NQ (2010) Mammal-restricted elements predispose human RET to folding impairment by HSCR mutations. Nat Struct Mol Biol 17:726–731. doi:10.1038/nsmb.1808
29. Limwongse C (2009) Syndromes and malformations of the urinary tract. In: Avner ED, Harman WE, Niaudet P, Yoshikawa N (eds) Pediatric Nephrology, 6th edn. Springer, Berlin, pp 121–156
30. Moorman AF, Houweling AC, de Boer PA, Christoffels VM (2001) Sensitive nonradioactive detection of mRNA in tissue sections: novel application of the whole-mount in situ hybridization protocol. J Histochem Cytochem 49:1–8
31. Pan X, Eathiraj S, Munson M, Lambright DG (2006) TBC-domain GAPs for Rab GTPases accelerate GTP hydrolysis by a dual-finger mechanism. Nature 442:303–306
32. Roach WG, Chavez JA, Mîinea CP, Lienhard GE (2007) Substrate specificity and effect on GLUT4 translocation of the Rab GTPase-activating protein Tbc1d1. Biochem J 403:353–358
33. Saisawat P, Kohl S, Hilger AC, Hwang DY, Yung Gee H, Dworschak GC, Tasic V, Pennimpede T, Natarajan S, Sperry E, Matassa DS, Stajić N, Bogdanovic R, de Blaauw I, Marcelis CL, Wijers CH, Bartels E, Schmiedeke E, Schmidt D, Märzheuser S, Grasshoff-Derr S, Holland-Cunz S, Ludwig M, Nöthen MM, Draaken M, Brosens E, Heij H, Tibboel D, Herrmann BG, Solomon BD, de Klein A, van Rooij IA, Esposito F, Reutter HM, Hildebrandt F (2014) Whole-exome resequencing reveals recessive mutations in TRAP1 in individuals with CAKUT and VACTERL association. Kidney Int 85:1310–1317. doi:10.1038/ki.2013.417
34. Sano H, Kane S, Sano E, Miinea CP, Asara JM, Lane WS, Garner CW, Lienhard GE (2003) Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J Biol Chem 278:14599–14602
35. 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
36. Steinberg KM, Yu B, Koboldt DC, Mardis ER, Pamphlett R (2015) Exome sequencing of case-unaffected-parents trios reveals recessive and de novo genetic variants in sporadic ALS. Sci Rep 5:9124. doi:10.1038/srep09124
37. Stenbit AE, Tsao TS, Li J, Burcelin R, Geenen DL, Factor SM, Houseknecht K, Katz EB, Charron MJ (1997) GLUT4 heterozygous knockout mice develop muscle insulin resistance and diabetes. Nat Med 3:1096–1101
38. Vivante A, Kohl S, Hwang DY, Dworschak GC, Hildebrandt F (2014) Single-gene causes of congenital anomalies of the kidney and urinary tract (CAKUT) in humans. Pediatr Nephrol 29:695–704. doi:10.1007/s00467-013-2684-4
39. Weibel ER (1979) Morphometry of the human lung: the state of the art after two decades. Bull Eur Physiopathol Respir 15:999–1013
40. Wilkinson DG, Nieto MA (1993) Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol 225:361–373
41. Yosypiv IV (2012) Congenital anomalies of the kidney and urinary tract: a genetic disorder? Int J Nephrol 2012:909083. doi:10.1155/2012/909083