Oxidative stress in fibroblasts from patients with pseudoxanthoma elasticum: Possible role in the pathogenesis of clinical manifestations

Journal of Pathology

Volumn 208, Issue 1, 2006, Pages 54-61

  Pasquali Ronchetti, Ivonne ^a   Garcia Fernandez, Maria Inmaculada ^b   Boraldi, Federica ^a   Quaglino, Daniela ^a   Gheduzzi, Dealba ^a   De Vincenzi Paolinelli, Chiara ^a   Tiozzo, Roberta ^a   Bergamini, Stefania ^a   Ceccarelli, Daniela ^a   Muscatello, Umberto ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b UNIVERSITY OF MÁLAGA   (Spain)

Author keywords

Connective tissue; Elastin mineralization; Extracellular matrix; Fibrolast; MRP6; Oxidative stress; Pathogenesis; Pseudoxanthoma elasticum (PXE)

Indexed keywords

ABC TRANSPORTER; ELASTIN; HYDROGEN PEROXIDE; MULTIDRUG RESISTANCE PROTEIN 6; REACTIVE OXYGEN METABOLITE;

ADULT; ARTICLE; CALCIFICATION; CARDIOVASCULAR SYSTEM; CELL CULTURE; CELL RESPIRATION; CLINICAL ARTICLE; CLINICAL FEATURE; CONNECTIVE TISSUE; CONTROLLED STUDY; ELASTIC FIBER; EXTRACELLULAR MATRIX; EYE; FIBROBLAST; GENE MUTATION; GENETIC DISORDER; HISTOPATHOLOGY; HUMAN; HUMAN CELL; MALE; MEMBRANE POTENTIAL; MITOCHONDRION; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN DETERMINATION; PSEUDOXANTHOMA ELASTICUM; SKIN; SKIN BIOPSY;

ADENINE NUCLEOTIDES; ADULT; ANTIOXIDANTS; BIOLOGICAL MARKERS; CELLS, CULTURED; CHRONIC DISEASE; FEMALE; FIBROBLASTS; GLUTATHIONE; GLUTATHIONE DISULFIDE; HUMANS; HYDROGEN PEROXIDE; MALONDIALDEHYDE; MEMBRANE POTENTIALS; MIDDLE AGED; MITOCHONDRIA; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; OXIDATIVE STRESS; PSEUDOXANTHOMA ELASTICUM; SKIN; SUPEROXIDE DISMUTASE;

EID: 29744452435     PISSN: 00223417     EISSN: None     Source Type: Journal    
DOI: 10.1002/path.1867     Document Type: Article

References (59)

1. Neldner KH, Struk B. Pseudoxanthoma elasticum. In Connective Tissue and Its Heritable Disorders: Molecular, Genetic and Medical Aspects, Royce PM, Steinmann B (eds). Wiley-Liss: New York, 2002; 561-583.
2. Gheduzzi D, Sammarco R, Quaglino, D, Bercovitch L, Terry S, Taylor W, Pasquali-Ronchetti I. Extracutaneous ultrastructural alterations in pseudoxanthoma elasticum. Ultrastruct Pathol 2003;27:375-384.
3. Kool M, van der Linden M, de Haas M, Baas F, Borst P. Expression of human MRP6, a homologue of the multidrug resistance protein gene MRP1, in tissues and cancer cells. Cancer Res 1999;59:175-182.
4. Le Saux O, Urban Z, Tschuch C, Csiszar K, Bacchelli B, Quaglino D, et al. Mutations in a gene encoding an ABC transporter cause pseudoxanthoma elasticum. Nat Genet 2000;25:223-227.
5. Gheduzzi D, Guidetti R, Anzivino C, Tarugi P, Di Leo E, Quaglino D, Pasquali-Ronchetti I. ABCC6 mutations in Italian families affected by pseudoxanthoma elasticum (PXE). Hum Mutat 2004;24:438-439.
6. Klein I, Sarkadi B, Varadi A. An inventory of the human ABC proteins. Biochim Biophys Acta 1999;1461:237-262.
7. Ilias A, Urban Z, Seidl TL, Le Saux O, Sinko E, Boyd CD, et al. Loss of ATP-dependent transport activity in pseudoxanthoma elasticum-associated mutants of human ABCC6 (MRP6). J Biol Chem 2002;277:16 860-16 867.
8. Boraldi F, Quaglino D, Croce MA, Garcia Fernandez MI, Tiozzo R, Gheduzzi D, 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.
9. Aessopos A, Farmakis D, Loukopoulos D. Elastic tissue abnormalities resembling pseudoxanthoma elasticum in β-thalassaemia and the sickling syndromes. Blood 2002;99:30-35.
10. Baccarani-Contri M, Bacchelli B, Boraldi F, Quaglino D, Taparelli F, Carnevali E, et al. Characterization of pseudoxanthoma elasticum-like lesions in the skin of patients with β-thalassaemia. J Am Acad Dermatol 2001;44:33-39.
11. Cianciulli P, Sorrentino F, Maffei L, Amadori S, Cappabianca MP, Foglietta E, et al. Cardiovascular involvement in thalassaemic patients with pseudoxanthoma elasticum-like skin lesions: a long-term follow-up study. Eur J Clin Invest 2002;32:700-706.
12. Hamlin N, Beck K, Bacchelli B, Cianciulli P, Pasquali-Ronchetti I, Le Saux O. Acquired pseudoxanthoma elasticum-like syndrome in β-thalassaemia patients. Br J Haematol 2003;122:852-854.
13. Chan AC, Chow CK, Chiu D. Interaction of antioxidants and their implication in genetic anemia. Proc Soc Exp Biol Med 1999;222:274-282.
14. Livrea MA, Tesoriere L, Maggio A, D'Arpa D, Pintaudi AM, Pedone E. Oxidative modification of low-density lipoprotein and atherogenetic risk in β-thalassaemia. Blood 1998;92:3936-3942.
15. Quaglino D, Boraldi F, Barbieri D, Croce A, Tiozzo R, Pasquali Ronchetti I. Abnormal phenotype of in vitro dermal fibroblasts from patients with pseudoxanthoma elasticum (PXE). Biochim Biophys Acta 2000;1501:51-62.
16. Chance B, Williams GR. The respiratory chain and oxidative phosphorylation. Adv Enzymol 1956;17:65-130.
17. Stocchi V, Cucchiarini L, Canestrari F, Piacentini MP, Fornaini G. A very fast ion-pair reversed-phase HPLC method for the separation of the most significant nucleotides and their degradation products in human red blood cells. Anal Biochem 1987;167:181-190.
18. Atkinson DE. The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 1968;7:4030-4034.
19. Cossarizza A, Baccarani-Contri M, Kalashnikova G, Franceschi C. A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5, 5′,6, 6′-tetrachloro-1, 1′,3, 3′-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem Biophys Res Commun 1993;197:40-45.
20. Reers M, Smiley ST, Mottola-Hartshorn C, Chen A, Lin M, Chen LB. Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol 1995;260:406-417.
21. Luo J, Li N, Paul Robinson J, Shi R. Detection of reactive oxygen species by flow cytometry after spinal cord injury. J Neurosci Methods 2002;120:105-112.
22. Boya P, de la Pena A, Beloqui O, Larrea E, Conchillo M, Castelruiz Y, et al. Antioxidant status and glutathione metabolism in peripheral blood mononuclear cells from patients with chronic hepatitis C. J Hepatol 1999;31:808-814.
23. Goth L. A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 1991;196:143-151.
24. Lepage G, Munoz G, Champagne J, Roy CC. Preparative steps necessary for the accurate measurement of malondialdehyde by high-performance liquid chromatography. Anal Biochem 1991;197:277-283.
25. Miller NJ, Rice-Evans C, Davies MJ, Gopinathan V, Milner A. A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin Sci (Colch) 1993;84:407-412.
26. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991;11:81-128.
27. Zhang H, Huang HM, Carson RC, Mahmood J, Thomas HM, Gibson GE. Assessment of membrane potentials of mitochondrial populations in living cells. Anal Biochem 2001;298:170-180.
28. Kaim G, Dimroth P. ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. EMBO J 1999;18:4118-4127.
29. Korshunov SS, Skulachev VP, Starkov AA. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 1997;416:15-18.
30. Arnold S, Kadenbach B. Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome c oxidase. Eur J Biochem 1997;249:350-354.
31. Kadenbach B. Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim Biophys Acta 2003;1604:77-94.
32. Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 2000;29:222-230.
33. Raha S, Robinson BH. Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem Sci 2000;25:502-508.
34. Scharffetter-Kochanek K, Brenneisen P, Wenk J, Herrmann G, Ma W, et al. Photoaging of the skin from phenotype to mechanisms. Exp Gerontol 2000;35:307-316.
35. Iglesias-De La Cruz MC, Ruiz-Torres P, Alcami J, Diez-Marques L, Ortega-Velazquez R, Chen S, et al. Hydrogen peroxide increases extracellular matrix mRNA through TGFβ in human mesangial cells. Kidney Int 2001;59:87-95.
36. Siwik DA, Pagano PJ, Colucci WS. Oxidative stress regulates collagen synthesis and matrix metalloproteinase activity in cardiac fibroblasts. Am J Physiol Cell Physiol 2001;280:C53-60.
37. Quaglino D, Tiozzo R, Passi A, Boraldi F, Croce A, Sartor L, et al. Metalloproteases/antiproteinases imbalance in cultured dermal fibroblasts from pseudoxanthoma elasticum patients. Biochim Biophys Acta 2005;1741:42-47.
38. Kawaguchi Y, Tanaka H, Okada T, Konishi H, Takahashi M, Ito M, Asai J. Effect of reactive oxygen species on the elastin mRNA expression in cultured human dermal fibroblasts. Free Radic Biol Med 1997;23:162-165.
39. Pasquali-Ronchetti I, Volpin D, Baccarani-Contri M, Castellani I, Peserico A. Pseudoxanthoma elasticum. Biochemical and ultrastructural studies. Dermatologica 1981;163:307-325.
40. Uitto J, Paul JL, Brockley K, Pearce RH, Clark JG. Elastic fibers in human skin: quantitation of elastic fibers by computerized digital image analyses and determination of elastin by radioimmunoassay of desmosine. Lab Invest 1983;49:499-505.
41. Hayashi A, Ryu A, Suzuki T, Kawada A, Tajima S. In vitro degradation of tropoelastin by reactive oxygen species. Arch Dermatol Res 1998;290:497-500.
42. Basalyga DM, Simionescu DT, Xiong W, Baxter BT, Starcher BC, Vyavahare NR. Elastin degradation and calcification in an abdominal aorta injury model: role of matrix metalloproteinases. Circulation 2004;110:3480-3487.
43. Kuroki M, Voest EE, Amano S, Beerepoot LV, Takashima S, Tolentino M, et al. Reactive oxygen intermediates increase vascular endothelial growth factor expression in vitro and in vivo. J Clin Invest 1996;98:1667-1675.
44. Maulik N. Redox signaling of angiogenesis. Antioxid Redox Signal 2002;4:805-815.
45. Algvere PV, Seregard S. Age-related maculopathy: pathogenetic features and new treatment modalities. Acta Ophthalmol Scand 2002;80:136-143.
46. Ayalasomayajula SP, Kompella UB. Induction of vascular endothelial growth factor by 4-hydroxynonenal and its prevention by glutathione precursors in retinal pigment epithelial cells. Eur J Pharmacol 2002;449:213-220.
47. Evereklioglu C, Er H, Doganay S, Cekmen M, Turkoz Y, Otlu B, Ozerol E. Nitric oxide and lipid peroxidation are increased and associated with decreased antioxidant enzyme activities in patients with age-related macular degeneration. Doc Ophthalmol 2003;106:129-136.
48. Sarks JP, Sarks SH, Killingsworth MC. Morphology of early choroidal neovascularisation in age-related macular degeneration: correlation with activity. Eye 1997;11:515-522.
49. Tarin JJ, Vendrell FJ, Ten J, Blanes R, van Blerkom J, Cano A. The oxidizing agent tertiary butyl hydroperoxide induces disturbances in spindle organization, c-meiosis, and aneuploidy in mouse oocytes. Mol Hum Reprod 1996;2:895-901.
50. Neely MD, Sidell KR, Graham DG, Montine TJ. The lipid peroxidation product 4-hydroxynonenal inhibits neurite outgrowth, disrupts neuronal microtubules, and modifies cellular tubulin. J Neurochem 1999;72:2323-2333.
51. Chiarugi P, Pani G, Giannoni E, Taddei L, Colavitti R, Raugei G, et al. Reactive oxygen species as essential mediators of cell adhesion: the oxidative inhibition of a FAK tyrosine phosphatase is required for cell adhesion. J Cell Biol 2003;161:933-944.
52. Maccari F, Gheduzzi D, Volpi N. Anomalous structure of urinary glycosaminoglycans in patients with pseudoxanthoma elasticum. Clin Chem 2003;49:380-388.
53. Passi A, Albertini R, Baccarani-Contri M, de Luca G, de Paepe A, Pallavicini G, et al. Proteoglycan alterations in skin fibroblast cultures from patients affected with pseudoxanthoma elasticum. Cell Biochem Funct 1996;14:111-120.
54. Tiozzo-Costa R, Baccarani-Contri M, Cingi MR, Pasquali-Ronchetti I, Salvini R, Rindi S, De Luca G. Pseudoxanthoma elasticum (PXE): ultrastructural and biochemical study on proteoglycan and proteoglycan-associated material produced by skin fibroblasts in vitro. Coll Relat Res 1988;8:49-64.
55. Ha BJ. Oxidative stress in ovariectomy menopause and role of chondroitin sulfate. Arch Pharm Res 2004;27:867-872.
56. Gheduzzi D, Guerra D, Bochicchio B, Pepe A, Tamburro AM, Quaglino D, et al. Heparan sulphate interacts with tropoelastin, with some tropoelastin peptides and is present in human dermis elastic fibers. Matrix Biol 2005;24:15-25.
57. Annovazzi L, Viglio S, Gheduzzi D, Pasquali-Ronchetti I, Zanone C, Cetta G, Iadarola P. High levels of desmosines in urine and plasma of patients with pseudoxanthoma elasticum. Eur J Clin Invest 2004;34:156-164.
58. Cheng ML, Ho HY, Tseng HC, Lee CH, Shih LY, Chiu DT. Antioxidant deficit and enhanced susceptibility to oxidative damage in individuals with different forms of α-thalassaemia. Br J Haematol 2005;128:119-127.
59. Livrea MA, Tesoriere L, Pintaudi AM, Calabrese A, Maggio A, Freisleben HJ, et al. Oxidative stress and antioxidant status in β-thalassaemia major: iron overload and depletion of lipid-soluble antioxidants. Blood 1996;88:3608-3614.