Gene expression profiling of ABC transporters in dermal fibroblasts of pseudoxanthoma elasticum patients identifies new candidates involved in PXE pathogenesis

Laboratory Investigation

Volumn 88, Issue 12, 2008, Pages 1303-1315

  Hendig, Doris ^a   Langmann, Thomas ^b   Kocken, Sarah ^a   Zarbock, Ralf ^a   Szliska, Christiane ^c   Schmitz, Gerd ^b   Kleesiek, Knut ^a   Götting, Christian ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c Krankenhaus Bethesda   (Germany)

Author keywords

ABCC6; Dermal fibroblast; Gene expression profiling; MRP6; Pseudoxanthoma elasticum; PXE

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A10; ABC TRANSPORTER A3; ABC TRANSPORTER A6; ABC TRANSPORTER A9; ABC TRANSPORTER B5; ABC TRANSPORTER C2; ABC TRANSPORTER C9; ABC TRANSPORTER D2; MULTIDRUG RESISTANCE PROTEIN 6; SMALL INTERFERING RNA; STEROL; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CELL LINEAGE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FIBROBLAST CULTURE; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; GENETIC VARIABILITY; HERITABILITY; HUMAN; IMMUNOPATHOGENESIS; MALE; MARKER GENE; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDOXANTHOMA ELASTICUM;

EID: 56649123417     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2008.96     Document Type: Article

References (54)

1. Kool M, van der Linden M, de Haas M, et al. Expression of human MRP6, a homologue of the multidrug resistance protein gene MRP1, in tissues and cancer cells. Cancer Res 1999;59:175-182.
2. Bergen AA, Plomp AS, Schuurman EJ, et al. Mutations in ABCC6 cause pseudoxanthoma elasticum. Nat Genet 2000;25:228-231.
3. Le Saux O, Urban Z, Tschuch C, et al. Mutations in a gene encoding an ABC transporter cause pseudoxanthoma elasticum. Nat Genet 2000;25:223-227.
4. Ringpfeil F, Lebwohl MG, Christiano AM, et al. Pseudoxanthoma elasticum: mutations in the MRP6 gene encoding a transmembrane ATP-binding cassette (ABC) transporter. Proc Natl Acad Sci USA 2000;97:6001-6006.
5. Neldner K, Struk B. Pseudoxanthoma elasticum. In: Royce PM, Steinmann B (eds). Connective Tissue and its Heritable Disorders. Wiley-Liss Inc.: New York, 2002, pp 561-583.
6. Schulz V, Hendig D, Henjakovic M, et al. Mutational analysis of the ABCC6 gene and the proximal ABCC6 gene promoter in German patients with pseudoxanthoma elasticum (PXE). Hum Mutat 2006;27:831.
7. Klement JF, Matsuzaki Y, Jiang QJ, et al. Targeted ablation of the abcc6 gene results in ectopic mineralization of connective tissues. Mol Cell Biol 2005;25:8299-8310.
8. Gorgels TG, Hu X, Scheffer GL, et al. Disruption of Abcc6 in the mouse: novel insight in the pathogenesis of pseudoxanthoma elasticum. Hum Mol Genet 2005;14:1763-1773.
9. Haimeur A, Conseil G, Deeley RG, et al. The MRP-related and BCRP/ABCG2 multidrug resistance proteins: biology, substrate specificity and regulation. Curr Drug Metab 2004;5:21-53.
10. Deeley RG, Westlake C, Cole SP. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 2006;86:849-899.
11. Scheffer GL, Hu X, Pijnenborg AC, et al. MRP6 (ABCC6) detection in normal human tissues and tumors. Lab Invest 2002;82:515-518.
12. Jiang Q, Uitto J. Pseudoxanthoma elasticum: a metabolic disease? J Invest Dermatol 2006;126:1440-1441.
13. Madon J, Hagenbuch B, Landmann L, et al. Transport function and hepatocellular localization of mrp6 in rat liver. Mol Pharmacol 2000;57:634-641.
14. Götting C, Hendig D, Adam A, et al. Elevated xylosyltransferase I activities in pseudoxanthoma elasticum (PXE) patients as a marker of stimulated proteoglycan biosynthesis. J Mol Med 2005;83:984-992.
15. Hendig D, Schulz V, Arndt M, et al. Role of serum fetuin-A, a major inhibitor of systemic calcification, in pseudoxanthoma elasticum. Clin Chem 2006;52:227-234.
16. Le Saux O, Bunda S, VanWart CM, et al. Serum factors from pseudoxanthoma elasticum patients alter elastic fiber formation in vitro. J Invest Dermatol 2006;126:1497-1505.
17. Gheduzzi D, Boraldi F, Annovi G, et al. Matrix Gla protein is involved in elastic fiber calcification in the dermis of pseudoxanthoma elasticum patients. Lab Invest 2007;87:998-1008.
18. Jiang Q, Li Q, Uitto J. Aberrant mineralization of connective tissues in a mouse model of pseudoxanthoma elasticum: systemic and local regulatory factors. J Invest Dermatol 2007;127:1392-1402.
19. Li Q, Jiang Q, Schurgers LJ, et al. Pseudoxanthoma elasticum: reduced gamma-glutamyl carboxylation of matrix gla protein in a mouse model (Abcc6-/-). Biochem Biophys Res Commun 2007;364:208-213.
20. Meng H, Vera I, Che N, et al. Identification of Abcc6 as the major causal gene for dystrophic cardiac calcification in mice through integrative genomics. Proc Natl Acad Sci USA 2007;104:4530-4535.
21. -/-) by transplantation of wild-type hepatocytes. J Invest Dermatol 2008, (Abstract).
22. Jiang Q, Endo M, Dibra F, et al. Pseudoxanthoma elasticum is a metabolic disease. J Invest Dermatol 2008.
23. Uitto J, Pulkkinen L, Ringpfeil F. Molecular genetics of pseudoxanthoma elasticum: a metabolic disorder at the environment-genome interface? Trends Mol Med 2001;7:13-17.
24. Hu X, Peek R, Plomp A, et al. Analysis of the frequent R1141X mutation in the ABCC6 gene in pseudoxanthoma elasticum. Invest Ophthalmol Vis Sci 2003;44:1824-1829.
25. Quaglino D, Boraldi F, Barbieri D, et al. Abnormal phenotype of in vitro dermal fibroblasts from patients with Pseudoxanthoma elasticum (PXE). Biochim Biophys Acta 2000;1501:51-62.
26. Passi A, Albertini R, Baccarani Contri M, et al. Proteoglycan alterations in skin fibroblast cultures from patients affected with pseudoxanthoma elasticum. Cell Biochem Funct 1996;14:111-120.
27. Quaglino D, Sartor L, Garbisa S, et al. Dermal fibroblasts from pseudoxanthoma elasticum patients have raised MMP-2 degradative potential. Biochim Biophys Acta 2005;1741:42-47.
28. Pasquali-Ronchetti I, Garcia-Fernandez MI, Boraldi F, et al. Oxidative stress in fibroblasts from patients with pseudoxanthoma elasticum: possible role in the pathogenesis of clinical manifestations. J Pathol 2006;208:54-61.
29. Belinsky MG, Chen ZS, Shchaveleva I, et al. Characterization of the drug resistance and transport properties of multidrug resistance protein 6 (MRP6, ABCC6). Cancer Res 2002;62:6172-6177.
30. Ilias A, Urban Z, Seidl TL, et al. Loss of ATP-dependent transport activity in pseudoxanthoma elasticum-associated mutants of human ABCC6 (MRP6). J Biol Chem 2002;277:16860-16867.
31. Boraldi F, Quaglino D, Croce MA, et al. Multidrug resistance protein-6 (MRP6) in human dermal fibroblasts. Comparison between cells from normal subjects and from pseudoxanthoma elasticum patients. Matrix Biol 2003;22:491-500.
32. Hirohashi T, Suzuki H, Ito K, et al. Hepatic expression of multidrug resistance-associated protein-like proteins maintained in eisai hyperbilirubinemic rats. Mol Pharmacol 1998;53:1068-1075.
33. Kuroda M, Kobayashi Y, Tanaka Y, et al. Increased hepatic and renal expressions of multidrug resistance-associated protein 3 in Eisai hyperbilirubinuria rats. J Gastroenterol Hepatol 2004;19:146-153.
34. Li Q, Jiang Q, Larusso J, et al. Targeted ablation of Abcc1 or Abcc3 in Abcc6(-/-) mice does not modify the ectopic mineralization process. Exp Dermatol 2007;16:853-859.
35. Christiano AM, Lebwohl MG, Boyd CD, et al. Workshop on pseudoxanthoma elasticum: molecular biology and pathology of the elastic fibers. Jefferson Medical College, Philadelphia, Pennsylvania, June 10, 1992. J Invest Dermatol 1992;99:660-663.
36. Lebwohl M, Neldner K, Pope FM, et al. Classification of pseudoxanthoma elasticum: report of a consensus conference. J Am Acad Dermatol 1994;30:103-107.
37. Langmann T, Mauerer R, Schmitz G. Human ATP-binding cassette transporter TaqMan low-density array: analysis of macrophage differentiation and foam cell formation. Clin Chem 2006;52:310-313.
38. Vandesompele J, De Preter K, Pattyn F, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002;3:research0034.1-0034.11.
39. Bodzioch M, Orso E, Klucken J, et al. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat Genet 1999;22:347-351.
40. Lawn RM, Wade DP, Garvin MR, et al. The Tangier disease gene product ABC1 controls the cellular apolipoprotein-mediated lipid removal pathway. J Clin Invest 1999;104:R25-R31.
41. Brousseau ME, Bodzioch M, Schaefer EJ, et al. Common variants in the gene encoding ATP-binding cassette transporter 1 in men with low HDL cholesterol levels and coronary heart disease. Atherosclerosis 2001;154:607-611.
42. Wenzel JJ, Piehler A, Kaminski WE. ABC A-subclass proteins: gatekeepers of cellular phospho- and sphingolipid transport. Front Biosci 2007;12:3177-3193.
43. Frikke-Schmidt R, Nordestgaard BG, Jensen GB, et al. Genetic variation in ABC transporter A1 contributes to HDL cholesterol in the general population. J Clin Invest 2004;114:1343-1353.
44. Wang J, Near S, Young K, et al. ABCC6 gene polymorphism associated with variation in plasma lipoproteins. J Hum Genet 2001;46:699-705.
45. Nagata K, Yamamoto A, Ban N, et al. Human ABCA3, a product of a responsible gene for abca3 for fatal surfactant deficiency in newborns, exhibits unique ATP hydrolysis activity and generates intracellular multilamellar vesicles. Biochem Biophys Res Commun 2004;324:262-268.
46. Denis M, Bissonnette R, Haidar B, et al. Expression, regulation, and activity of ABCA1 in human cell lines. Mol Genet Metab 2003;78:265-274.
47. Goldstein JL, Brown MS. Regulation of the mevalonate pathway. Nature 1990;343:425-430.
48. Borst P, van de Wetering K, Schlingemann R. Does the absence of ABCC6 (Multidrug Resistance Protein 6) in patients with Pseudoxanthoma elasticum prevent the liver from providing sufficient vitamin K to the periphery? Cell Cycle 2008;7:1575-1579.
49. Lu H, Klaassen C. Gender differences in mRNA expression of ATP-binding cassette efflux and bile acid transporters in kidney, liver, and intestine of 5/6 nephrectomized rats. Drug Metab Dispos 2008;36:16-23.
50. Maher JM, Dieter MZ, Aleksunes LM, et al. Oxidative and electrophilic stress induces multidrug resistance-associated protein transporters via the nuclear factor-E2-related factor-2 transcriptional pathway. Hepatology 2007;46:1597-1610.
51. Borst P, de Wolf C, van de Wetering K. Multidrug resistance-associated proteins 3, 4, and 5. Pflugers Arch 2007;453:661-673.
52. Wielinga PR, van der Heijden I, Reid G, et al. Characterization of the MRP4- and MRP5-mediated transport of cyclic nucleotides from intact cells. J Biol Chem 2003;278:17664-17671.
53. Bryan J, Munoz A, Zhang X, et al. ABCC8 and ABCC9: ABC transporters that regulate K+ channels. Pflugers Arch 2007;453:703-718.
54. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001;25:402-408.