CCBE1 Mutation in Two Siblings, One Manifesting Lymphedema-Cholestasis Syndrome, and the Other, Fetal Hydrops

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Shah, Sohela ^a   Conlin, Laura K ^b   Gomez, Luis ^b   Aagenaes, Øystein ^c   Eiklid, Kristin ^d   Knisely, A S ^e   Mennuti, Michael T ^b   Matthews, Randolph P ^f   Spinner, Nancy B ^b   Bull, Laura N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

^e KING S COLLEGE HOSPITAL   (United Kingdom)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AUTOSOMAL RECESSIVE DISORDER; CASE REPORT; CCBE1 GENE; CHILD; CHROMOSOME 18; CONSANGUINEOUS MARRIAGE; CONTROLLED STUDY; FEMALE; FETUS HYDROPS; GENE; GENE IDENTIFICATION; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENOTYPE; HOMOZYGOSITY; HUMAN; HUMAN TISSUE; INFANT; INTRAHEPATIC CHOLESTASIS; LCS1 GENE; LYMPHEDEMA; LYMPHEDEMA CHOLESTASIS SYNDROME; MALE; MEXICO; MISSENSE MUTATION; PHENOTYPE; PREGNANCY TERMINATION; SIBLING; SINGLE NUCLEOTIDE POLYMORPHISM;

CALCIUM-BINDING PROTEINS; CHOLESTASIS; CRANIOFACIAL ABNORMALITIES; FEMALE; GENITAL DISEASES, MALE; GENOTYPE; HOMOZYGOTE; HUMANS; HYDROPS FETALIS; INFANT; LYMPHANGIECTASIS, INTESTINAL; LYMPHEDEMA; MALE; MUTATION; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; SIBLINGS; TUMOR SUPPRESSOR PROTEINS;

EID: 84884664383     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075770     Document Type: Article

References (35)

1. Aagenaes O, Sigstad H, Bjorn-Hansen R, (1970) Lymphoedema in hereditary recurrent cholestasis from birth. Arch Dis Child 45: 690-695. doi:10.1136/adc.45.243.690. PubMed: 5477684.
2. Bull LN, Roche E, Song EJ, Pedersen J, Knisely AS, et al. (2000) Mapping of the locus for cholestasis-lymphedema syndrome (Aagenaes syndrome) to a 6.6-cM interval on chromosome 15q. Am J Hum Genet 67: 994-999. doi:10.1086/303080. PubMed: 10968776.
3. Frühwirth M, Janecke AR, Müller T, Carlton VE, Kronenberg F, et al. (2003) Evidence for genetic heterogeneity in lymphedema-cholestasis syndrome. J Pediatr 142: 441-447. doi:10.1067/mpd.2003.148. PubMed: 12712065.
4. Zollner G, Trauner M, (2006) Molecular mechanisms of cholestasis. Wien Med Wochenschr 156: 380-385. doi:10.1007/s10354-006-0312-7. PubMed: 16937039.
5. Carlton VE, Pawlikowska L, Bull LN, (2004) Molecular basis of intrahepatic cholestasis. Ann Med 36: 606-617. doi:10.1080/07853890410018916. PubMed: 15768832.
6. Schulte-Merker S, Sabine A, Petrova TV, (2011) Lymphatic vascular morphogenesis in development, physiology, and disease. J Cell Biol 193: 607-618. doi:10.1083/jcb.201012094. PubMed: 21576390.
7. Alders M, Hogan BM, Gjini E, Salehi F, Al-Gazali L, et al. (2009) Mutations in CCBE1 cause generalized lymph vessel dysplasia in humans. Nat Genet 41: 1272-1274. doi:10.1038/ng.484. PubMed: 19935664.
8. Connell FC, Kalidas K, Ostergaard P, Brice G, Murday V, et al. (2012) CCBE1 mutations can cause a mild, atypical form of generalized lymphatic dysplasia but are not a common cause of non-immune hydrops fetalis. Clin Genet 81: 191-197. doi:10.1111/j.1399-0004.2011.01731.x. PubMed: 22239599.
9. Connell F, Kalidas K, Ostergaard P, Brice G, Homfray T, et al. (2010) Linkage and sequence analysis indicate that CCBE1 is mutated in recessively inherited generalised lymphatic dysplasia. Hum Genet 127: 231-241. doi:10.1007/s00439-009-0766-y. PubMed: 19911200.
10. Alders M, Mendola A, Adès L, Al Gazali L, Bellini C, et al. (2013) Evaluation of Clinical Manifestations in Patients with Severe Lymphedema with and without CCBE1 Mutations. Mol Syndromol 4: 107-113. PubMed: 23653581.
11. Bellini C, Fulcheri E, Rutigliani M, Calevo MG, Boccardo F, et al. (2010) Immunohistochemistry in non-immune hydrops fetalis: a single center experience in 79 fetuses. Am J Med Genet A 152A: 1189-1196. doi:10.1002/ajmg.a.33191. PubMed: 20425823.
12. Jin ZW, Nakamura T, Yu HC, Kimura W, Murakami G, et al. (2010) Fetal anatomy of peripheral lymphatic vessels: a D2-40 immunohistochemical study using an 18-week human fetus (CRL 155 mm). J Anat 216: 671-682. doi:10.1111/j.1469-7580.2010.01229.x. PubMed: 20408907.
13. Gunderson KL, Steemers FJ, Lee G, Mendoza LG, Chee MS, (2005) A genome-wide scalable SNP genotyping assay using microarray technology. Nat Genet 37: 549-554. doi:10.1038/ng1547. PubMed: 15838508.
14. Klomp LW, Vargas JC, van Mil SW, Pawlikowska L, Strautnieks SS, et al. (2004) Characterization of mutations in ATP8B1 associated with hereditary cholestasis. Hepatology 40: 27-38. doi:10.1002/hep.20285. PubMed: 15239083.
15. Frazer KA, Ballinger DG, Cox DR, Hinds DA, Stuve LL, et al. (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851-861. doi:10.1038/nature06258. PubMed: 17943122.
16. Bull LN, van Eijk MJ, Pawlikowska L, DeYoung JA, Juijn JA, et al. (1998) A gene encoding a P-type ATPase mutated in two forms of hereditary cholestasis. Nat Genet 18: 219-224. doi:10.1038/ng0398-219. PubMed: 9500542.
17. Hogan BM, Bos FL, Bussmann J, Witte M, Chi NC, et al. (2009) Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat Genet 41: 396-398. doi:10.1038/ng.321. PubMed: 19287381.
18. Bos FL, Caunt M, Peterson-Maduro J, Planas-Paz L, Kowalski J, et al. (2011) CCBE1 is essential for mammalian lymphatic vascular development and enhances the lymphangiogenic effect of vascular endothelial growth factor-C in vivo. Circ Res 109: 486-491. doi:10.1161/CIRCRESAHA.111.250738. PubMed: 21778431.
19. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, et al. (2010) A method and server for predicting damaging missense mutations. Nat Methods 7: 248-249. doi:10.1038/nmeth0410-248. PubMed: 20354512.
20. Strautnieks SS, Bull LN, Knisely AS, Kocoshis SA, Dahl N, et al. (1998) A gene encoding a liver-specific ABC transporter is mutated in progressive familial intrahepatic cholestasis. Nat Genet 20: 233-238. doi:10.1038/3034. PubMed: 9806540.
21. de Vree JM, Jacquemin E, Sturm E, Cresteil D, Bosma PJ, et al. (1998) Mutations in the MDR3 gene cause progressive familial intrahepatic cholestasis. Proc Natl Acad Sci U S A 95: 282-287. doi:10.1073/pnas.95.1.282. PubMed: 9419367.
22. Zhu QS, Xing W, Qian B, von Dippe P, Shneider BL, et al. (2003) Inhibition of human m-epoxide hydrolase gene expression in a case of hypercholanemia. Biochim Biophys Acta 1638: 208-216. doi:10.1016/S0925-4439(03)00085-1. PubMed: 12878321.
23. Carlton VE, Harris BZ, Puffenberger EG, Batta AK, Knisely AS, et al. (2003) Complex inheritance of familial hypercholanemia with associated mutations in TJP2 and BAAT. Nat Genet 34: 91-96. doi:10.1038/ng1147. PubMed: 12704386.
24. Hadj-Rabia S, Baala L, Vabres P, Hamel-Teillac D, Jacquemin E, et al. (2004) Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: a tight junction disease. Gastroenterology 127: 1386-1390. doi:10.1053/j.gastro.2004.07.022. PubMed: 15521008.
25. Van Mil SW, Milona A, Dixon PH, Mullenbach R, Geenes VL, et al. (2007) Functional variants of the central bile acid sensor FXR identified in intrahepatic cholestasis of pregnancy. Gastroenterology 133: 507-516. doi:10.1053/j.gastro.2007.05.015. PubMed: 17681172.
26. Chong CP, Mills PB, McClean P, Gissen P, Bruce C, et al. (2012) Bile acid-CoA ligase deficiency--a new inborn error of bile acid metabolism. J Inherit Metab Dis 35: 521-530. doi:10.1007/s10545-011-9416-3. PubMed: 22089923.
27. Chagnon P, Michaud J, Mitchell G, Mercier J, Marion JF, et al. (2002) A missense mutation (R565W) in cirrhin (FLJ14728) in North American Indian childhood cirrhosis. Am J Hum Genet 71: 1443-1449. doi:10.1086/344580. PubMed: 12417987.
28. Gissen P, Johnson CA, Morgan NV, Stapelbroek JM, Forshew T, et al. (2004) Mutations in VPS33B, encoding a regulator of SNARE-dependent membrane fusion, cause arthrogryposis-renal dysfunction-cholestasis (ARC) syndrome. Nat Genet 36: 400-404. doi:10.1038/ng1325. PubMed: 15052268.
29. Cullinane AR, Straatman-Iwanowska A, Zaucker A, Wakabayashi Y, Bruce CK, et al. (2010) Mutations in VIPAR cause an arthrogryposis, renal dysfunction and cholestasis syndrome phenotype with defects in epithelial polarization. Nat Genet 42: 303-312. doi:10.1038/ng.538. PubMed: 20190753.
30. Wada M, Toh S, Taniguchi K, Nakamura T, Uchiumi T, et al. (1998) Mutations in the canalicular multispecific organic anion transporter (cMOAT) gene, a novel ABC transporter, in patients with hyperbilirubinemia II/Dubin-Johnson syndrome. Hum Mol Genet 7: 203-207. doi:10.1093/hmg/7.2.203. PubMed: 9425227.
31. Schwarz M, Wright AC, Davis DL, Nazer H, Björkhem I, et al. (2000) The bile acid synthetic gene 3beta-hydroxy-Delta(5)-C(27)-steroid oxidoreductase is mutated in progressive intrahepatic cholestasis. J Clin Invest 106: 1175-1184. doi:10.1172/JCI10902. PubMed: 11067870.
32. Lemonde HA, Custard EJ, Bouquet J, Duran M, Overmars H, et al. (2003) Mutations in SRD5B1 (AKR1D1), the gene encoding delta(4)-3-oxosteroid 5beta-reductase, in hepatitis and liver failure in infancy. Gut 52: 1494-1499. doi:10.1136/gut.52.10.1494. PubMed: 12970144.
33. Zou Z, Enis DR, Bui H, Khandros E, Kumar V, et al. (2013) The secreted lymphangiogenic factor CCBE1 is essential for fetal liver erythropoiesis. Blood 121: 3228-3236. doi:10.1182/blood-2012-10-462689. PubMed: 23426945.
34. Facucho-Oliveira J, Bento M, Belo JA, (2011) Ccbe1 expression marks the cardiac and lymphatic progenitor lineages during early stages of mouse development. Int J Dev Biol 55: 1007-1014. doi:10.1387/ijdb.113394jf. PubMed: 22252499.
35. Fabris L, Cadamuro M, Fiorotto R, Roskams T, Spirlì C, et al. (2006) Effects of angiogenic factor overexpression by human and rodent cholangiocytes in polycystic liver diseases. Hepatology 43: 1001-1012. doi:10.1002/hep.21143. PubMed: 16628643.