Coinheritance of COL4A5 and MYO1E mutations accentuate the severity of kidney disease

Pediatric Nephrology

Volumn 30, Issue 9, 2015, Pages 1459-1465

  Lennon, Rachel ^a,b,c   Stuart, Helen M ^d   Bierzynska, Agnieszka ^e   Randles, Michael J ^a,b   Kerr, Bronwyn ^d   Hillman, Katherine A ^f   Batra, Gauri ^f   Campbell, Joanna ^g   Storey, Helen ^g   Flinter, Frances A ^h   Koziell, Ania ^h   Welsh, Gavin I ^e   Saleem, Moin A ^e   Webb, Nicholas J A ^c   Woolf, Adrian S ^b,c  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c MANCHESTER UNIVERSITY NHS FOUNDATION TRUST   (United Kingdom)

^d Manchester Centre for Genomic Medicine   (United Kingdom)

^e UNIVERSITY OF BRISTOL   (United Kingdom)

^f Department of Paediatric Histopathology CMFT   (United Kingdom)

^g GUY S HOSPITAL   (United Kingdom)

^h GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Alport syndrome; COL4A5; Genetics; MYO1E; Nephrotic syndrome; Whole exome sequencing

Indexed keywords

DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DIURETIC AGENT; FUROSEMIDE; HUMAN ALBUMIN; COL4A5 PROTEIN, HUMAN; COLLAGEN TYPE 4; MYO1E PROTEIN, HUMAN; MYOSIN I;

ADULT; ALLELE; ALPORT SYNDROME; ARTICLE; CHILD; COLLAGEN IV ALPHA 5 GENE; END STAGE RENAL DISEASE; EXOME; FEMALE; FOCAL GLOMERULOSCLEROSIS; GENE; GENE MUTATION; GLOMERULOPATHY; HEMATURIA; HUMAN; HUMAN TISSUE; KIDNEY BIOPSY; KIDNEY DISEASE; MALE; MYOSIN 1E GENE; NEPHROTIC SYNDROME; PHENOTYPE; PHENOTYPIC VARIATION; PODOCYTE; PRIORITY JOURNAL; PROTEIN INTERACTION; SCHOOL CHILD; SIBLING; X CHROMOSOME INACTIVATION; GENETICS; GLOMERULUS; INFANT; INHERITANCE; MUTATION; NEPHRITIS, HEREDITARY; PATHOLOGY; PATHOPHYSIOLOGY; PEDIGREE; PRESCHOOL CHILD; SEVERITY OF ILLNESS INDEX;

ADULT; CHILD; CHILD, PRESCHOOL; COLLAGEN TYPE IV; FEMALE; HUMANS; INFANT; INHERITANCE PATTERNS; KIDNEY GLOMERULUS; MALE; MUTATION; MYOSIN TYPE I; NEPHRITIS, HEREDITARY; PEDIGREE; SEVERITY OF ILLNESS INDEX; SIBLINGS;

EID: 84939267800     PISSN: 0931041X     EISSN: 1432198X     Source Type: Journal    
DOI: 10.1007/s00467-015-3067-9     Document Type: Article

References (36)

1. Alport AC (1927) Hereditary familial congenital haemorrhagic nephritis. Br Med J 1:504–506
2. Heidet L, Gubler MC (2009) The renal lesions of Alport syndrome. J Am Soc Nephrol 20:1210–1215
3. Barker DF, Hostikka SL, Zhou J, Chow LT, Oliphant AR, Gerken SC, Gregory MC, Skolnick MH, Atkin CL, Tryggvason K (1990) Identification of mutations in the COL4A5 collagen gene in Alport syndrome. Science 248:1224–1227
4. Mochizuki T, Lemmink HH, Mariyama M, Antignac C, Gubler MC, Pirson Y, Verellen-Dumoulin C, Chan B, Schröder CH, Smeets HJ, Reeders ST (1994) Identification of mutations in the alpha 3(IV) and alpha 4(IV) collagen genes in autosomal recessive Alport syndrome. Nat Genet 8:77–81
5. Jais JP, Knebelmann B, Giatras I, De Marchi M, Rizzoni G, Renieri A, Weber M, Gross O, Netzer KO, Flinter F, Pirson Y, Dahan K, Wieslander J, Persson U, Tryggvason K, Martin P, Hertz JM, Schröder C, Sanak M, Carvalho MF, Saus J, Antignac C, Smeets H, Gubler MC (2003) X-linked Alport syndrome: natural history and genotype-phenotype correlations in girls and women belonging to 195 families: a “European community Alport syndrome concerted action” study. J Am Soc Nephrol 14:2603–2610
6. Hanson H, Storey H, Pagan J, Flinter F (2011) The value of clinical criteria in identifying patients with X-linked Alport syndrome. Clin J Am Soc Nephrol 6:198–203
7. Pierides A, Voskarides K, Kkolou M, Hadjigavriel M, Deltas C (2013) X-linked, COL4A5 hypomorphic Alport mutations such as G624D and P628L may only exhibit thin basement membrane nephropathy with microhematuria and late onset kidney failure. Hippokratia 17:207–213
8. Storey H, Savige J, Sivakumar V, Abbs S, Flinter FA (2013) COL4A3/COL4A4 mutations and features in individuals with autosomal recessive Alport syndrome. J Am Soc Nephrol 24:1945–1954
9. McCauley J, Masand N, McGowan R, Rajagopalan S, Hunter A, Michaud JL, Gibson K, Robertson J, Vaz F, Abbs S, Holden ST (2011) X-linked VACTERL with hydrocephalus syndrome: further delineation of the phenotype caused by FANCB mutations. Am J Med Genet A 155A:2370–2380
10. Mele C, Iatropoulos P, Donadelli R, Calabria A, Maranta R, Cassis P, Buelli S, Tomasoni S, Piras R, Krendel M, Bettoni S, Morigi M, Delledonne M, Pecoraro C, Abbate I, Capobianchi MR, Hildebrandt F, Otto E, Schaefer F, Macciardi F, Ozaltin F, Emre S, Ibsirlioglu T, Benigni A, Remuzzi G, Noris M, PodoNet Consortium (2011) MYO1E mutations and childhood familial focal segmental glomerulosclerosis. N Engl J Med 365:295–306
11. Martin P, Heiskari N, Zhou J, Leinonen A, Tumelius T, Hertz JM, Barker D, Gregory M, Atkin C, Styrkarsdottir U, Neumann H, Springate J, Shows T, Pettersson E, Tryggvason K (1998) High mutation detection rate in the COL4A5 collagen gene in suspected Alport syndrome using PCR and direct DNA sequencing. J Am Soc Nephrol 9:2291–2301
12. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504
13. Wu J, Vallenius T, Ovaska K, Westermarck J, Mäkelä TP, Hautaniemi S (2009) Integrated network analysis platform for protein–protein interactions. Nat Methods 6:75–77
14. Chautard E, Ballut L, Thierry-Mieg N, Ricard-Blum S (2009) MatrixDB, a database focused on extracellular protein–protein and protein–carbohydrate interactions. Bioinformatics 25:690–691
15. Zaidel-Bar R, Geiger B (2010) The switchable integrin adhesome. J Cell Sci 123:1385–1388
16. Assenov Y, Ramirez F, Schelhorn SE, Lengauer T, Albrecht M (2008) Computing topological parameters of biological networks. Bioinformatics 24:282–284
17. Tan R, Colville D, Wang YY, Rigby L, Savige J (2010) Alport retinopathy results from “severe” COL4A5 mutations and predicts early renal failure. Clin J Am Soc Nephrol 5:34–38
18. Knebelmann B, Breillat C, Forestier L, Arrondel C, Jacassier D, Giatras I, Drouot L, Deschenes G, Grunfeld JP, Broyer M, Gubler MC, Antignac C (1996) Spectrum of mutations in the COL4A5 collagen gene in X-linked Alport syndrome. Am J Hum Genet 59:1221–1232
19. Amos-Landgraf JM, Cottle A, Plenge RM, Friez M, Schwartz CE, Longshore J, Willard HF (2006) X chromosome-inactivation patterns of 1,005 phenotypically unaffected females. Am J Hum Genet 79:493–499
20. Savige J, Gregory M, Gross O, Kashtan C, Ding J, Flinter F (2013) Expert guidelines for the management of Alport syndrome and thin basement membrane nephropathy. J Am Soc Nephrol 24:364–375
21. Gross O, Licht C, Anders HJ, Hoppe B, Beck B, Tönshoff B, Höcker B, Wygoda S, Ehrich JH, Pape L, Konrad M, Rascher W, Dötsch J, Müller-Wiefel DE, Hoyer P, Study Group Members of the Gesellschaft für Pädiatrische Nephrologie, Knebelmann B, Pirson Y, Grunfeld JP, Niaudet P, Cochat P, Heidet L, Lebbah S, Torra R, Friede T, Lange K, Müller GA, Weber M (2012) Early angiotensin-converting enzyme inhibition in Alport syndrome delays renal failure and improves life expectancy. Kidney Int 81:494–501
22. Temme J, Peters F, Lange K, Pirson Y, Heidet L, Torra R, Grunfeld JP, Weber M, Licht C, Müller GA, Gross O (2012) Incidence of renal failure and nephroprotection by RAAS inhibition in heterozygous carriers of X-chromosomal and autosomal recessive Alport mutations. Kidney Int 81:779–783
23. Webb NJ, Lam C, Shahinfar S, Strehlau J, Wells TG, Gleim GW, Le Bailly De Tilleghem C (2011) Efficacy and safety of losartan in children with Alport syndrome–results from a subgroup analysis of a prospective, randomized, placebo- or amlodipine-controlled trial. Nephrol Dial Transplant 26:2521–2526
24. Kestilä M, Lenkkeri U, Männikkö M, Lamerdin J, McCready P, Putaala H, Ruotsalainen V, Morita T, Nissinen M, Herva R, Kashtan CE, Peltonen L, Holmberg C, Olsen A, Tryggvason K (1998) Positionally cloned gene for a novel glomerular protein–nephrin–is mutated in congenital nephrotic syndrome. Mol Cell 1:575–582
25. Kaplan JM, Kim SH, North KN, Rennke H, Correia LA, Tong HQ, Mathis BJ, Rodríguez-Pérez JC, Allen PG, Beggs AH, Pollak MR (2000) Mutations in ACTN4, encoding alpha-actinin-4, cause familial focal segmental glomerulosclerosis. Nat Genet 24:251–256
26. Boute N, Gribouval O, Roselli S, Benessy F, Lee H, Fuchshuber A, Dahan K, Gubler MC, Niaudet P, Antignac C (2000) NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat Genet 24:349–354
27. Zenker M, Aigner T, Wendler O, Tralau T, Müntefering H, Fenski R, Pitz S, Schumacher V, Royer-Pokora B, Wühl E, Cochat P, Bouvier R, Kraus C, Mark K, Madlon H, Dötsch J, Rascher W, Maruniak-Chudek I, Lennert T, Neumann LM, Reis A (2004) Human laminin beta2 deficiency causes congenital nephrosis with mesangial sclerosis and distinct eye abnormalities. Hum Mol Genet 13:2625–2632
28. Winn MP, Conlon PJ, Lynn KL, Farrington MK, Creazzo T, Hawkins AF, Daskalakis N, Kwan SY, Ebersviller S, Burchette JL, Pericak-Vance MA, Howell DN, Vance JM, Rosenberg PB (2005) A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 308:1801–1804
29. McCarthy HJ, Bierzynska A, Wherlock M, Ognjanovic M, Kerecuk L, Hegde S, Feather S, Gilbert RD, Krischock L, Jones C, Sinha MD, Webb NJ, Christian M, Williams MM, Marks S, Koziell A, Welsh GI, Saleem MA, RADAR the UK SRNS Study Group (2013) Simultaneous sequencing of 24 genes associated with steroid-resistant nephrotic syndrome. Clin J Am Soc Nephrol 8:637–648
30. Voskarides K, Arsali M, Athanasiou Y, Elia A, Pierides A, Deltas C (2012) Evidence that NPHS2-R229Q predisposes to proteinuria and renal failure in familial hematuria. Pediatr Nephrol 27:675–679
31. Lennon R, Byron A, Humphries JD, Randles MJ, Carisey A, Murphy S, Knight D, Brenchley PE, Zent R, Humphries MJ (2014) Global analysis reveals the complexity of the human glomerular extracellular matrix. J Am Soc Nephrol 25:939–951
32. Jin X, Wang W, Mao J, Shen H, Fu H, Wang X, Gu W, Liu A, Yu H, Shu Q, Du L (2014) Overexpression of Myo1e in mouse podocytes enhances cellular endocytosis, migration, and adhesion. J Cell Biochem 115:410–419
33. Ouderkirk JL, Krendel M (2014) Myosin 1e is a component of the invadosome core that contributes to regulation of invadosome dynamics. Exp Cell Res 322:265–276
34. Chase SE, Encina CV, Stolzenburg LR, Tatum AH, Holzman LB, Krendel M (2012) Podocyte-specific knockout of myosin 1e disrupts glomerular filtration. Am J Physiol Renal Physiol 303:F1099–F1106
35. Sanna-Cherchi S, Burgess KE, Nees SN, Caridi G, Weng PL, Dagnino M, Bodria M, Carrea A, Allegretta MA, Kim HR, Perry BJ, Gigante M, Clark LN, Kisselev S, Cusi D, Gesualdo L, Allegri L, Scolari F, D'Agati V, Shapiro LS, Pecoraro C, Palomero T, Ghiggeri GM, Gharavi AG (2011) Exome sequencing identified MYO1E and NEIL1 as candidate genes for human autosomal recessive steroid-resistant nephrotic syndrome. Kidney Int 80:389–396
36. Al-Hamed MH, Al-Sabban E, Al-Mojalli H, Al-Harbi N, Faqeih E, Al Shaya H, Alhasan K, Al-Hissi S, Rajab M, Edwards N, Al-Abbad A, Al-Hassoun I, Sayer JA, Meyer BF (2013) A molecular genetic analysis of childhood nephrotic syndrome in a cohort of Saudi Arabian families. J Hum Genet 58:480–489