A heterozygous female with Fabry disease due to a novel α-galactosidase A mutation exhibits a unique synaptopodin distribution in vacuolated podocytes

Clinical Nephrology

Volumn 83, Issue 5, 2015, Pages 301-308

  Takahashi, Naoki ^a   Yokoi, Seiji ^a   Kasuno, Kenji ^a   Kogami, Akiya ^a   Tsukimura, Takahiro ^c   Togawa, Tadayasu ^c   Saito, Seiji ^d   Ohno, Kazuki ^e   Hara, Masanori ^f   Kurosawa, Hiroyuki ^g   Hirayama, Yoshiaki ^g   Kurose, Tomomi ^b   Yokoyama, Yoshinari ^a   Mikami, Daisuke ^a   Kimura, Hideki ^b   Naiki, Hironobu ^a   Sakuraba, Hitoshi ^c   Iwano, Masayuki ^a  

^a UNIVERSITY OF FUKUI   (Japan)

^b UNIVERSITY OF FUKUI HOSPITAL   (Japan)

^c MEIJI PHARMACEUTICAL UNIVERSITY   (Japan)

^d HOKKAIDO INFORMATION UNIVERSITY   (Japan)

^e NPO for the Promotion of Research on Intellectual Property Tokyo   (Japan)

^f Yoshida Hospital   (Japan)

^g DENKA COMPANY LIMITED   (Japan)

Author keywords

Fabry disease; Globotriaosylceramide; P210S; Podocalyxin; Podocyte; Synaptopodin

Indexed keywords

GLOBOTRIAOSYLCERAMIDE; SYNAPTOPODIN; ACTIN BINDING PROTEIN; ALPHA GALACTOSIDASE; ALPHA-GALACTOSIDASE A, HUMAN; CERAMIDE TRIHEXOSIDE; SYNPO PROTEIN, HUMAN;

ADULT; ALPHA GALACTOSIDASE A GENE; ARTICLE; CASE REPORT; CELL VACUOLE; ELECTRON MICROSCOPY; FABRY DISEASE; FEMALE; GENE; GENETIC ANALYSIS; HETEROZYGOTE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KIDNEY BIOPSY; MICROSCOPY; MISSENSE MUTATION; PODOCYTE; PROTEINURIA; URINALYSIS; BIOPSY; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME REPLACEMENT; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; GENETIC PREDISPOSITION; GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; ULTRASTRUCTURE;

ADULT; ALPHA-GALACTOSIDASE; BIOPSY; DNA MUTATIONAL ANALYSIS; ENZYME REPLACEMENT THERAPY; FABRY DISEASE; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HETEROZYGOTE; HUMANS; IMMUNOHISTOCHEMISTRY; MICROFILAMENT PROTEINS; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MUTATION, MISSENSE; PHENOTYPE; PODOCYTES; TRIHEXOSYLCERAMIDES; VACUOLES;

EID: 84940041478     PISSN: 03010430     EISSN: None     Source Type: Journal    
DOI: 10.5414/CN108317     Document Type: Article

References (32)

1. Brady RO, Gal AE, Bradley RM, Martensson E, Warshaw AL, Laster L. Enzymatic defect in Fabry's disease. Ceramidetrihexosidase deficiency. N Engl J Med. 1967; 276: 1163-1167.
2. Zarate YA, Hopkin RJ. Fabry's disease. Lancet. 2008; 372: 1427-1435.
3. Cybulla M, Schaefer E, Wendt S, Ling H, Krober SM, Hovelborn U, Schandelmaier S, Rohrbach R, Neumann HP. Chronic renal failure and proteinuria in adulthood: Fabry disease predominantly affecting the kidneys. Am J Kidney Dis. 2005; 45: e82-89.
4. Deegan PB, Baehner AF, Barba Romero MA, Hughes DA, Kampmann C, Beck M; European FOS Investigators. Natural history of Fabry disease in females in the Fabry Outcome Survey. J Med Genet. 2006; 43: 347-352.
5. Lyon MF. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature. 1961; 190: 372-373.
6. Thurberg BL, Rennke H, Colvin RB, Dikman S, Gordon RE, Collins AB, Desnick RJ, O'Callaghan M. Globotriaosylceramide accumulation in the Fabry kidney is cleared from multiple cell types after enzyme replacement therapy. Kidney Int. 2002; 62: 1933-1946.
7. Fukushima M, Tsuchiyama Y, Nakato T, Yokoi T, Ikeda H, Yoshida S, Kusumoto T, Itoh K, Sakuraba H. A female heterozygous patient with Fabry's disease with renal accumulation of trihexosylceramide detected with a monoclonal antibody. Am J Kidney Dis. 1995; 26: 952-955.
8. Askari H, Kaneski CR, Semino-Mora C, Desai P, Ang A, Kleiner DE, Perlee LT, Quezado M, Spollen LE, Wustman BA, Schiffmann R. Cellular and tissue localization of globotriaosylceramide in Fabry disease. Virchows Arch. 2007; 451: 823-834.
9. Keslova-Veselikova J, Hulkova H, Dobrovolny R, Asfaw B, Poupetova H, Berna L, Sikora J, Golan L, Ledvinova J, Elleder M. Replacement of alpha-galactosidase A in Fabry disease: effect on fibroblast cultures compared with biopsied tissues of treated patients. Virchows Arch. 2008; 452: 651-665.
10. Valbuena C, Leitao D, Carneiro F, Oliveira JP. Immunohistochemical diagnosis of Fabry nephropathy and localisation of globotriaosylceramide deposits in paraffin-embedded kidney tissue sections. Virchows Arch. 2012; 460: 211-221.
11. Hara M, Yamagata K, Tomino Y, Saito A, Hirayama Y, Ogasawara S, Kurosawa H, Sekine S, Yan K. Urinary podocalyxin is an early marker for podocyte injury in patients with diabetes: establishment of a highly sensitive ELISA to detect urinary podocalyxin. Diabetologia. 2012; 55: 2913-2919.
12. Kotani M, Kawashima I, Ozawa H, Ogura K, Ariga T, Tai T. Generation of one set of murine monoclonal antibodies specific for globo-series glycolipids: evidence for differential distribution of the glycolipids in rat small intestine. Arch Biochem Biophys. 1994; 310: 89-96.
13. Tajima Y, Kawashima I, Tsukimura T, Sugawara K, Kuroda M, Suzuki T, Togawa T, Chiba Y, Jigami Y, Ohno K, Fukushige T, Kanekura T, Itoh K, Ohashi T, Sakuraba H. Use of a modified alpha-N-acetylgalactosaminidase in the development of enzyme replacement therapy for Fabry disease. Am J Hum Genet. 2009; 85: 569-580.
14. Garman SC, Garboczi DN. The molecular defect leading to Fabry disease: structure of human alphagalactosidase. J Mol Biol. 2004; 337: 319-335.
15. Matsuzawa F, Aikawa S, Doi H, Okumiya T, Sakuraba H. Fabry disease: correlation between structural changes in alpha-galactosidase, and clinical and biochemical phenotypes. Hum Genet. 2005; 117: 317-328.
16. McDonald IK, Thornton JM. Satisfying hydrogen bonding potential in proteins. J Mol Biol. 1994; 238: 777-793.
17. Ohno K, Saito S, Sugawara K, Sakuraba H. Structural consequences of amino acid substitutions causing Tay-Sachs disease. Mol Genet Metab. 2008; 94: 462-468.
18. Sakuraba H, Oshima A, Fukuhara Y, Shimmoto M, Nagao Y, Bishop DF, Desnick RJ, Suzuki Y. Identification of point mutations in the alpha-galactosidase A gene in classical and atypical hemizygotes with Fabry disease. Am J Hum Genet. 1990; 47: 784-789.
19. Sakuraba H, Eng CM, Desnick RJ, Bishop DF. Invariant exon skipping in the human alpha-galactosidase A pre-mRNA: Ag+1 to t substitution in a 5'-splice site causing Fabry disease. Genomics. 1992; 12: 643-650.
20. Poeppl AG, Murray GJ, Medin JA. Enhanced filter paper enzyme assay for high-throughput population screening for Fabry disease. Anal Biochem. 2005; 337: 161-163.
21. Ebrahim HY, Baker RJ, Mehta AB, Hughes DA. Functional analysis of variant lysosomal acid glycosidases of Anderson-Fabry and Pompe disease in a human embryonic kidney epithelial cell line (HEK 293 T). J Inherit Metab Dis. 2012; 35: 325-334.
22. Filoni C, Caciotti A, Carraresi L, Cavicchi C, Parini R, Antuzzi D, Zampetti A, Feriozzi S, Poisetti P, Garman SC, Guerrini R, Zammarchi E, Donati MA, Morrone A. Functional studies of new GLA gene mutations leading to conformational Fabry disease. Biochim Biophys Acta. 2010; 1802: 247-252.
23. Asanuma K, Kim K, Oh J, Giardino L, Chabanis S, Faul C, Reiser J, Mundel P. Synaptopodin regulates the actin-bundling activity of alpha-actinin in an isoform-specific manner. J Clin Invest. 2005; 115: 1188-1198.
24. Ichimura K, Kurihara H, Sakai T. Actin filament organization of foot processes in rat podocytes. J Histochem Cytochem. 2003; 51: 1589-1600.
25. Endlich N, Kress KR, Reiser J, Uttenweiler D, Kriz W, Mundel P, Endlich K. Podocytes respond to mechanical stress in vitro. J Am Soc Nephrol. 2001; 12: 413-422.
26. Asanuma K, Yanagida-Asanuma E, Faul C, Tomino Y, Kim K, Mundel P. Synaptopodin orchestrates actin organization and cell motility via regulation of RhoA signalling. Nat Cell Biol. 2006; 8: 485-491.
27. Park SS, Kim MO, Yun SP, Ryu JM, Park JH, Seo BN, Jeon JH, Han HJ. C(16)-Ceramide-induced F-actin regulation stimulates mouse embryonic stem cell migration: involvement of N-WASP/ Cdc42/Arp2/3 complex and cofilin-1/a-actinin. Biochim Biophys Acta. 2013; 1831: 350-360.
28. Nishibori Y, Liu L, Hosoyamada M, Endou H, Kudo A, Takenaka H, Higashihara E, Bessho F, Takahashi S, Kershaw D, Ruotsalainen V, Tryggvason K, Khoshnoodi J, Yan K. Disease-causing missense mutations in NPHS2 gene alter normal nephrin trafficking to the plasma membrane. Kidney Int. 2004; 66: 1755-1765.
29. Chévrier M, Brakch N, Céline L, Genty D, Ramdani Y, Moll S, Djavaheri-Mergny M, Brasse-Lagnel C, Annie Laquerriàre AL, Barbey F, Bekri S. Autophagosome maturation is impaired in Fabry disease. Autophagy. 2010; 6: 589-599.
30. Ballabio A, Gieselmann V. Lysosomal disorders: from storage to cellular damage. Biochim Biophys Acta. 2009; 1793: 684-696.
31. Selvarajah M, Nicholls K, Hewitson TD, Becker GJ. Targeted urine microscopy in Anderson-Fabry disease: a cheap, sensitive and specific diagnostic technique. Nephrol Dial Transplant. 2011; 26: 3195-3202.
32. Hara M, Yamamoto T, Yanagihara T, Takada T, Itoh M, Adachi Y, Yoshizumi A, Kawasaki K, Kihara I. Urinary excretion of podocalyxin indicates glomerular epithelial cell injuries in glomerulonephritis. Nephron. 1995; 69: 397-403.