Effects of UVB-induced oxidative stress on protein expression and specific protein oxidation in normal human epithelial keratinocytes: A proteomic approach

Proteome Science

Volumn 8, Issue , 2010, Pages

  Perluigi, Marzia ^a   Di Domenico, Fabio ^a   Blarzino, Carla ^a   Foppoli, Cesira ^b   Cini, Chiara ^a,b   Giorgi, Alessandra ^a   Grillo, Caterina ^a   De Marco, Federico ^c   Butterfield, David A ^d   Schininà, Maria E ^a   Coccia, Raffaella ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b CNR   (Italy)

^c REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

26S PROTEASOME SUBUNIT 7; ACTIN; ALPHA ENOLASE; ALPHA3 INTEGRIN; CARBONYL DERIVATIVE; CYTOKERATIN 5; GLUCOSE REGULATED PROTEIN 78; HEAT SHOCK COGNATE PROTEIN 71; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; LIPOCORTIN 2; ORNITHINE OXOACID AMINOTRANSFERASE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PROHIBITIN; PROTEASOME; PROTEASOME SUBUNIT ALPHA 1; PROTEASOME SUBUNIT ALPHA 5; PROTEASOME SUBUNIT ALPHA 6; PROTEIN DISULFIDE ISOMERASE; PROTEIN DISULFIDE ISOMERASE A3; REACTIVE OXYGEN METABOLITE; SEROTRANSFERRIN; TRANSFERRIN; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL INTERACTION; CHILD; CONTROLLED STUDY; CYTOSKELETON; FUNCTIONAL PROTEOMICS; HEAT SHOCK RESPONSE; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VIVO STUDY; KERATINOCYTE; MALE; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN METABOLISM; PROTEIN MODIFICATION; SKIN EPITHELIUM; ULTRAVIOLET B RADIATION; VALIDATION STUDY;

EID: 77952922104     PISSN: None     EISSN: 14775956     Source Type: Journal    
DOI: 10.1186/1477-5956-8-13     Document Type: Article

References (52)

1. Attar M, Lloyd JR, Bickers DR, Mukhtar H. Malignant conversion of UV radiation and chemically induced mouse skin benign tumors by free-radical-generating compounds. Carcinogenesis 1989, 10:1841-1845. 10.1093/carcin/10.10.1841, 2507187.
2. Paz ML, González Maglio DH, Weill FS, Bustamante J, Leoni J. Mitochondrial dysfunction and cellular stress progression after ultraviolet B irradiation in human keratinocytes. Photodermatol Photoimmunol Photomed 2008, 24:115-122. 10.1111/j.1600-0781.2008.00348.x, 18477129.
3. Kovacs D, Raffa S, Flori E, Aspite N, Briganti S, Cardinali G, Torrisi MR, Picardo M. Keratinocyte growth factor down-regulates intracellular ROS production induced by UVB. J Dermatol Sci 2009, 54:106-113. 10.1016/j.jdermsci.2009.01.005, 19250802.
4. D'Autréaux B, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 2007, 8:813-824. 10.1038/nrm2256, 17848967.
5. Kamata H, Hirata H. Redox regulation of cellular signalling. Cell Signal 1999, 11:1-14. 10.1016/S0898-6568(98)00037-0, 10206339.
6. Thannickal VJ, Fanburg BL. Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 2000, 279:L1005-1028.
7. Marnett LJ. Oxyradicals and DNA damage. Carcinogenesis 2000, 21:361-370. 10.1093/carcin/21.3.361, 10688856.
8. Toyokuni S, Okamoto K, Yodoi J, Hiai H. Persistent oxidative stress in cancer. FEBS Lett 1995, 358:1-3. 10.1016/0014-5793(94)01368-B, 7821417.
9. Punnonen K, Puntala A, Jansén CT, Ahotupa M. UVB irradiation induces lipid peroxidation and reduces antioxidant enzyme activities in human keratinocytes in vitro. Acta Derm Venereol 1991, 71:239-242.
10. Stadtman ER, Berlett BS. Reactive oxygen-mediated protein oxidation in aging and disease. Drug Metab Rev 1998, 30:225-243. 10.3109/03602539808996310, 9606602.
11. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991, 11:81-128. 10.1016/0891-5849(91)90192-6, 1937131.
12. LeBlanc WG, Vidal L, Kirsner RS, Lee DJ, Caban-Martinez AJ, McCollister KE, Arheart KL, Chung-Bridges K, Christ S, Clark J, Lewis JE, Davila EP, Rouhani P, Fleming LE. Reported skin cancer screening of US adult workers. J Am Acad Dermatol 2008, 59:55-63. 10.1016/j.jaad.2008.03.013, 18436338.
13. Perluigi M, Giorgi A, Blarzino C, De Marco F, Foppoli C, Di Domenico F, Butterfield DA, Schininà ME, Cini C, Coccia R. Proteomics analysis of protein expression and specific protein oxidation in human papillomavirus transformed keratinocytes upon UVB irradiation. J Cell Mol Med 2009, 13:1809-1822. 10.1111/j.1582-4934.2008.00465.x, 19267883.
14. Jung T, Grune T. The proteasome and its role in the degradation of oxidized proteins. IUBMB Life 2008, 60:743-752. 10.1002/iub.114, 18636510.
15. Dahlmann B. Role of proteasomes in disease. BMC Biochem 2007, 8(Suppl 1):S3. 10.1186/1471-2091-8-S1-S3, 2106367, 18047740.
16. Keller JN, Hanni KB, Markesbery WR. Impaired proteasome function in Alzheimer's disease. J Neurochem 2000, 75:436-9. 10.1046/j.1471-4159.2000.0750436.x, 10854289.
17. Petropoulos I, Conconi M, Wang X, Hoenel B, Brégégère F, Milner Y, Friguet B. Increase of oxidatively modified protein is associated with a decrease of proteasome activity and content in aging epidermal cells. J Gerontol A Biol Sci Med Sci 2000, 55:B220-227.
18. Timperio AM, Egidi MG, Zolla L. Proteomics applied on plant abiotic stresses: Role of heat shock proteins (HSP). J Proteomics 2008, 71:391-411. 10.1016/j.jprot.2008.07.005, 18718564.
19. Arrigo AP, Virot S, Chaufour S, Firdaus W, Kretz-Remy C, Diaz-Latoud C. Hsp27 consolidates intracellular redox homeostasis by upholding glutathione in its reduced form and by decreasing iron intracellular levels. Antioxid Redox Signal 2005, 7:414-422. 10.1089/ars.2005.7.414, 15706088.
20. McClung JK, King RL, Walker LS, Danner DB, Nuell MJ, Stewart CA, Dell'Orco RT. Expression of prohibitin, an antiproliferative protein. Exp Gerontol 1992, 27:413-418. 10.1016/0531-5565(92)90074-A, 1459218.
21. Nuell MJ, Stewart DA, Walker L, Friedman V, Wood CM, Owens GA, Smith JR, Schneider EL, Dell' Orco R, Lumpkin CK, Danner DB, Mc-Clung JK. Prohibitin, an evolutionarily conserved intracellular protein that blocks DNA synthesis in normal fibroblasts and HeLa cells. Mol Cell Biol 1991, 11:1372-1381. 369408, 1996099.
22. Carter WG, Wayner EA, Bouchard TS, Kaur P. The role of integrins α2 β1 and α3 β1 in cell-cell and cell-substrate adhesion of human epidermal cells. J Cell Biol 1990, 110:1387-1404. 10.1083/jcb.110.4.1387, 2116091, 1691191.
23. Manohar A, Shome SG, Lamar J, Stirling L, Iyer V, Pumiglia K, DiPersio CM. Alpha 3 beta 1 integrin promotes keratinocyte cell survival through activation of a MEK [?]/ERK [?] signaling pathway. J Cell Sci 2004, 117:4043-4054. 10.1242/jcs.01277, 15280429.
24. Pignatelli M, Hanby AM, Stamp GW. Low expression of β1, α2 and α3 subunits of VLA integrins in malignant mammary tumours. J Pathol 1991, 165:25-32. 10.1002/path.1711650106, 1659627.
25. Moll R, Franke WW, Schiller DL, Geiger B, Krepler R. The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell 1982, 3:11-24.
26. Rao KS, Babu KK, Gupta PD. Keratins and skin disorders. Cell Biol Int 1996, 20:261-74. 10.1006/cbir.1996.0029, 8664850.
27. Aplin AE, Howe A, Alahari SK, Juliano RL. Signal transduction and signal modulation by cell adhesion receptors: the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins. Pharmacol Rev 1998, 50:197-263.
28. De Marco F, Perluigi M, Foppoli C, Blarzino C, Cini C, Coccia R, Venuti A. UVB irradiation down-regulates HPV-16 RNA expression: implications for malignant progression of transformed cells. Virus Res 2007, 130:249-259. 10.1016/j.virusres.2007.06.018, 17683822.
29. Mann M, Jensen ON. Proteomic analysis of post-translational modifications. Nat Biotechnol 2003, 21:255-261. 10.1038/nbt0303-255, 12610572.
30. Elliott JG, Oliver JD, High S. The thiol-dependent reductase ERp57 interacts specifically with N-glycosylated integral membrane proteins. J Biol Chem 1997, 272:13849-13855. 10.1074/jbc.272.21.13849, 9153243.
31. Antoniou AN, Ford S, Alphey M, Osborne A, Elliott T, Powis SJ. The oxidoreductase ERp57 efficiently reduces partially folded in preference to fully folded MHC class I molecules. EMBO J 2002, 21:2655-2663. 10.1093/emboj/21.11.2655, 126025, 12032078.
32. Kang SJ, Cresswell P. Regulation of intracellular trafficking of human CD1d by association with MHC class II molecules. EMBO J 2002, 21:1650-1660. 10.1093/emboj/21.7.1650, 125936, 11927549.
33. Lahav J, Wijnen EM, Hess O, Hamaia SW, Griffiths D, Makris M, Knight CG, Essex DW, Farndale RW. Enzymatically catalyzed disulfide exchange is required for platelet adhesion to collagen via integrin a2h1. Blood 2003, 102:2085-2092. 10.1182/blood-2002-06-1646, 12791669.
34. Uebara T, Nakamura T, Yao D, Shi ZQ, Gu Z, Ma Y, Masliah E, Nomura Y, Lipton SA. S-nitrosylated protein disulphide isomerase links protein misfolding to neurodegeneration. Nature 2006, 441:513-517. 10.1038/nature04782, 16724068.
35. Falahatpisheh H, Nanez A, Montoya-Durango D, Qian Y, Tiffany-Castiglioni E, Ramos KS. Activation profiles of HSPA5 during the glomerular mesangial cell stress response to chemical injury. Cell Stress Chaperones 2007, 12:209-218. 10.1379/CSC-259.1, 1971237, 17915553.
36. Millard TH, Sharp SJ, Machesky LM. Signalling to actin assembly via the WASP (Wiskott-Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem J 2004, 380:1-17. 10.1042/BJ20040176, 1224166, 15040784.
37. Pelletier MF, Marcil A, Sevigny G, Jakob CA, Tessier DC, Chevet E, Menard R, Bergeron JJ, Thomas DY. The heterodimeric structure of glucosidase II is required for its activity, solubility, and localization in vivo. Glycobiology 2000, 10:815-827. 10.1093/glycob/10.8.815, 10929008.
38. Waisman DM. Annexin II tetramer: structure and function. Mol Cell Biochem 1995, 149-150:301-322. 10.1007/BF01076592, 8569746.
39. Moss SE. Annexins. Trends Cell Biol 1997, 7:87-89. 10.1016/S0962-8924(96)10049-0, 17708913.
40. Tanaka T, Akatsuka S, Ozeki M, Shirase TH, Toyokuni S. Redox regulation of Annexin 2 and its implications for oxidative stress-induced renal carcinogenesis and metastasis. Oncogene 2004, 23:3980-3989. 10.1038/sj.onc.1207555, 15048081.
41. Haley B, Paunesku T, Protić M, Woloschak GE. Response of heterogeneous ribonuclear proteins (hnRNP) to ionising radiation and their involvement in DNA damage repair. Int J Radiat Biol 2009, 85:643-655. 10.1080/09553000903009548, 2785495, 19579069.
42. Castegna A, Aksenov M, Thongboonkerd V, Klein JB, Pierce WM, Booze R, Markesbery WR, Butterfield DA. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J Neurochem 2002, 82:1524-1532. 10.1046/j.1471-4159.2002.01103.x, 12354300.
43. Tamarit J, Cabiscol E, Ros J. Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J Biol Chem 1998, 273:3027-3032. 10.1074/jbc.273.5.3027, 9446617.
44. Levine RL, Stadtman ER. Oxidative modification of proteins during aging. Exp Gerontol 2001, 36:1495-1502. 10.1016/S0531-5565(01)00135-8, 11525872.
45. Pirisi L, Yasumoto S, Feller M, Doniger J, Di Paolo JA. Transformation of human fibroblasts and keratinocytes with human papillomavirus type 16 DNA. J Virol 1987, 61:1061-1066. 254063, 2434663.
46. Conrad CC, Talent JM, Malakowsky CA, Gracy RW. Post-Electrophoretic Identification of Oxidized Proteins. Biol Proced Online 2000, 2:39-45. 10.1251/bpo17, 140127, 12734585.
47. Maurer HH, Peters FT. Toward high-throughput drug screening using mass spectrometry. Ther Drug Monit 2005, 27:686-688. 10.1097/01.ftd.0000180224.19384.f0, 16404794.
48. Mignogna G, Giorgi A, Stefanelli P, Neri A, Colotti G, Maras B, Schininà ME. Inventory of the proteins in Neisseria meningitidis serogroup B strain MC58. J Proteome 2005, 4:1361-1370.
49. Pappin DJ. Peptide mass fingerprinting using MALDI-TOF mass spectrometry. Methods Mol Biol 2003, 211:211-219.
50. Lauderback CM, Hackett JM, Huang FF, Keller JN, Szweda LI, Markesbery WR, Butterfield DA. The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer's disease brain: the role of Abeta1-42. J Neurochem 2001, 78:413-416. 10.1046/j.1471-4159.2001.00451.x, 11461977.
51. Jessop CE, Bulleid NJ. Glutathione directly reduces an oxidoreductase in the endoplasmic reticulum of mammalian cells. J Biol Chem 2004, 279:55341-55347. 10.1074/jbc.M411409200, 15507438.
52. Kim-Han JS, O'Malley KL. Cell stress induced by parkynsonian mimetic, 6-hydroxydopamine, is concurrent with oxidation of the chaperone, ERp57, and aggresome formation. Antioxid Redox Signal 2007, 9:2255-2264. 10.1089/ars.2007.1791, 17848102.