Non-thermal plasma treatment is associated with changes in transcriptome of human epithelial skin cells

Free Radical Research

Volumn 47, Issue 8, 2013, Pages 577-592

  Schmidt, Anke ^a,b   Wende, Kristian ^a,b   Bekeschus, Sander ^a,b   Bundscherer, Lena ^a,b   Barton, Annemarie ^a,b   Ottmüller, Katja ^a,b   Weltmann, Klaus Dieter ^b   Masur, Kai ^a,b  

^a Centre for Innovation Competence Plasmatis   (Germany)

^b INP Greifswald eV   (Germany)

Author keywords

Antioxidative defense; Epithelial skin cells; Gene expression; Non thermal plasma; Oxidative stress; Plasma medicine; ROS; Wound healing

Indexed keywords

ANTIOXIDANT; TRANSCRIPTOME;

ARGON PLASMA COAGULATION; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; CULTURE MEDIUM; DETOXIFICATION; DNA MODIFICATION; DOWN REGULATION; EPITHELIUM CELL; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOME; HUMAN; HUMAN CELL; KERATINOCYTE; MICROARRAY ANALYSIS; OXIDATIVE STRESS; PLASMA GAS; PREDICTION; SKIN EPITHELIUM; UPREGULATION; WOUND HEALING;

CELLS, CULTURED; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; HELA CELLS; HUMANS; OXIDATIVE STRESS; PLASMA GASES; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKIN; TRANSCRIPTOME;

EID: 84880558884     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2013.804623     Document Type: Article

References (92)

1. Burm KTAL. Plasma: The Fourth State of Matter Plasma Chemistry and Plasma Processing. Plasma Chem Plasma Process 2012;32:401-407.
2. Ahn HJ, Kim KI, Kim G, Moon E, Yang SS, Lee JS. Atmospheric-pressure plasma jet induces apoptosis involving mitochondria via generation of free radicals. PLoS One 2011;6:e28154.
3. Heinlin J, Isbary G, Stolz W, Morfi ll G, Landthaler M, Shimizu T, Steffes B, Nosenko T, Zimmermann J, Karrer S. Plasma applications in medicine with a special focus on dermatology. J Eur Acad Dermatol Venereol 2011; 25: 1-11.
4. Weltmann KD, Kindel E, Brandenburg R, Meyer C, Bussiahn R, Wilke C, von Woedtke T. Atmospheric pressure plasma jet for medical therapy: plasma parameters and risk estimation. Contrib Plasma Phys 2009;49:631-640.
5. Graves DB. The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology. J Phys D Appl Phys 2012;45.
6. Bender C, Partecke LI, Kindel E, Doring F, Lademann J, Heidecke CD, et al. The modifi ed HET-CAM as a model for the assessment of the infl ammatory response to tissue tolerable plasma. Toxicol In Vitro 2011; 25: 530-537.
7. Rupf S, Idlibi AN, Marrawi FA, Hannig M, Schubert A, von Mueller L, et al. Removing biofi lms from microstructured titanium ex vivo: a novel approach using atmospheric plasma technology. PLoS One 6:e25893.
8. Fricke K, Koban I, Tresp H, Jablonowski L, Schroder K, Kramer A, et al. Atmospheric pressure plasma: a highperformance tool for the effi cient removal of biofi lms. PLoS One 2012;7:e42539.
9. Matthes R, Bekeschus S, Bender C, Koban I, Hbner NO, Kramer A. Pilot-study on the infl uence of carrier gas and plasma application (open resp. delimited) modifi cations on physical plasma and its antimicrobial eff ect against Pseudomonas aeruginosa and Staphylococcus aureus. GMS Krankenhaushyg Interdiszip 2012; 7.
10. Kalghatgi S, Kelly CM, Cerchar E, Torabi B, Alekseev O, Fridman A, et al. Eff ects of non-thermal plasma on mammalian cells. Plos One 2011;6:e16270.
11. Sensenig R, Kalghatgi S, Cerchar E, Fridman G, Shereshevsky A, Torabi B, et al. Non-thermal plasma induces apoptosis in melanoma cells via production of intracellular reactive oxygen species. Ann Biomed Eng 2011;39:674-687.
12. Partecke LI, Evert K, Haugk J, Doring F, Normann L, Diedrich S, et al. Tissue Tolerable Plasma (TTP) induces apoptosis in pancreatic cancer cells in vitro and in vivo. BMC Cancer 2012;12:473.
13. Kim CH, Bahn JH, Lee SH, Kim GY, Jun SI, Lee K, Baek SJ. Induction of cell growth arrest by atmospheric nonthermal plasma in colorectal cancer cells. J Biotechnol 2010;150:530-538.
14. Gharaee-Kermani M, Phan SH. Role of cytokines and cytokine therapy in wound healing and fi brotic diseases. Curr Pharm Des 2001;7:1083-1103.
15. Becker J. Institut f ?r Gesundheits-und Pfl ege ?konomie (IGP), Hochschule Bremen. Wund Management 2011;1.
16. Melchionna R, Bellavia G, Romani M, Straino S, Germani A, Di Carlo A, et al. C/EBP regulates wound repair and EGF receptor signaling. J Invest Dermatol 2012; 132: 1908-1917.
17. Rezvani HR, Ali N, Serrano-Sanchez M, Dubus P, Varon C, Ged C, et al. Loss of epidermal hypoxia-inducible factor-1-accelerates epidermal aging and aff ects re-epithelialization in human and mouse. J Cell Sci 2011;124:4172-4183.
18. Nauta A, Gurtner GC, Longaker MT. Wound healing and regenerative strategies. Oral Dis 17: 541-549.
19. Jiang WG, Sanders AJ, Ruge F, Harding KG. Infl uence of interleukin-8 (IL-8) and IL-8 receptors on the migration of human keratinocytes, the role of PLC-gamma and potential clinical implications. Exp Ther Med 2012; 3: 231-236.
20. Sen CK, Roy S. Redox signals in wound healing. Biochim Biophys Acta 2008;1780:1348-1361.
21. White-Chu EF, Reddy M. Dry skin in the elderly: complexities of a common problem. Clin Dermatol 2011;29:37-42.
22. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell-line. J Cell Biol 1988;106:761-771.
23. Brandner JM, Zacheja S, Houdek P, Moll I, Lobmann R. Expression of matrix metalloproteinases, cytokines, and connexins in diabetic and nondiabetic human keratinocytes before and after transplantation into an ex vivo wound-healing model. Diabetes Care 2008;31:114-120.
24. Vockel M, Pollok S, Breitenbach U, Ridderbusch I, Kreienkamp HJ, Brandner JM. Somatostatin inhibits cell migration and reduces cell counts of human keratinocytes and delays epidermal wound healing in an ex vivo wound model. PLoS One 2011;6:e19740.
25. Moll I, Houdek P, Schmidt H, Moll R. Characterization of epidermal wound healing in a human skin organ culture model: acceleration by transplanted keratinocytes. J Invest Dermatol 1998;111:251-258.
26. Adair-Kirk TL, Griffi n GL, Meyer MJ, Kelley DG, Miner JH, Keene DR, et al. Keratinocyte-targeted expression of human laminin β2 rescues skin blistering and early lethality of laminin β2 defi cient mice. PLoS One 2012;7:e45546.
27. Usui ML, Mansbridge JN, Carter WG, Fujita M, Olerud JE. Keratinocyte migration, proliferation, and diff erentiation in chronic ulcers from patients with diabetes and normal wounds. J Histochem Cytochem 2008; 56: 687-696.
28. Park HB YJ, Chung KH. Characterization of the cytokine profi le of platelet rich plasma (PRP) and PRP-induced cell proliferation and migration: upregulation of matrix metalloproteinase-1 and-9 in HaCaT cells. Korean J Hematol 2011;46:265-273.
29. Santoro MM GG. Cellular and molecular facets of keratinocyte reepithelization during wound healing. Exp Cell Res 2005;304:274-286.
30. Isbary G, Morfi ll G, Schmidt HU, Georgi M, Ramrath K, Heinlin J, et al. A fi rst prospective randomized controlled trial to decrease bacterial load using cold atmospheric argon plasma on chronic wounds in patients. Br J Dermatol 2010;163:78-82.
31. Ermolova N, Kudryashova E, DiFranco M, Vergara J, Kramerova I, Spencer MJ. Pathogenity of some limb girdle muscular dystrophy mutations can result from reduced anchorage to myofi brils and altered stability of calpain 3. Hum Mol Genet 2011;20:3331-3345.
32. Kieft IE, Darios D, Roks AJM, Stoffels E. Plasma treatment of mammalian vascular cells: a quantitative description. IEEE Trans Plasma Sci 2005;33:771-775.
33. Stoff els E, Kieft IE, Sladek REJ, van den Bedem LJM, van der Laan EP, Steinbuch M. Plasma needle for in vivo medical treatment: recent developments and perspectives. Plasma Sources Sci Technol 2006;15:S169-S180.
34. Stoff els E, Kieft AIE, Sladek AREJ, Zandvoort V, Slaaf DW. Cold gas plasma in biology and medicine. In: d ' Agostino R, Favia P, Kawai Y, Ikegami H, Sato N, et al. (eds.). Advanced Plasma Technology. Weinheim: Wiley-VCH; 2008. pp. 301-318.
35. Winter T, Winter J, Polak M, Kusch K, Mader U, Sietmann R, et al. Characterization of the global impact of low temperature gas plasma on vegetative microorganisms. Proteomics 2011;11:3518-3530.
36. Haertel B, Hhnel M, Blackert S, Wende K, von Woedtke T, Lindequist U. Surface molecules on HaCaT keratinocytes after interaction with non-thermal atmospheric pressure plasma. Cell Biol Int 2012;36:1217-1222.
37. Ji LL. Antioxidants and oxidative stress in exercise. Proc Soc Exp Biol Med 1999;222:283-292.
38. Black AT, Gray JP, Shakarjian MP, Laskin DL, Heck DE, Laskin JD. Increased oxidative stress and antioxidant expression in mouse keratinocytes following exposure to paraquat. Toxicol Appl Pharmacol 2008;231:384-392.
39. Blasig IE, Bellmann C, Cording J, Del Vecchio G, Zwanziger D, Huber O, Haseloff RF. Occludin protein family: oxidative stress and reducing conditions. Antioxid Redox Signal 2011;15:1195-1219.
40. Kaneto H, Katakami N, Matsuhisa M, Matsuoka TA. Role of reactive oxygen species in the progression of type 2 diabetes and atherosclerosis. Mediators Infl amm 2010;2010:453892.
41. Kozina LS, Borzova IV, Arutiunov VA, Ryzhak GA. The role of oxidative stress in skin aging. Adv Gerontol 2012;25:217-222.
42. Lockhart DJ, Winzeler EA. Genomics, gene expression and DNA arrays. Nature 2000; 405: 827-836.
43. von Woedtke T, Kramer A, Weltmann KD. Plasma sterilization: What are the conditions to meet this claim? Plasma Process Polym 2008;5:534-539.
44. Reuter S WJ, Schmidt-Bleker A, Tresp H, Hammer M U and Weltmann K D. Controlling the ambient air aff ected reactive species composition in the effl uent of an argon plasma jet. IEEE Trans Plasma Sci 2012 (Special Issue on Atmospheric Pressure Plamsa Jet Applications).
45. von Woedtke T, Junger M, Kocher T, Kramer A, Lademann J, Lindequist U, Weltmann KD. Plasma medicine-therapeutic application of physical plasmas. World Congress on Medical Physics and Biomedical Engineering, Springer Berlin Heidelberg, 2009:82-83.
46. Reuter S, Tresp H, Wende K, Hammer MU, Winter J, Masur K, et al. From RONS to ROS: tailoring plasma jet treatment of skin cells. IEEE Trans Plasma Sci 2012 (Special Issue on Plasma Medicine).
47. Reuter S, Winter J, Schmidt-Bleker A, Schroeder D, Lange H, Knake N, et al. Atomic oxygen in a cold argon plasma jet: TALIF spectroscopy in ambient air with modelling and measurements of ambient species diff usion. Plasma Sources Sci Technol 2012;21:1-7.
48. Bekeschus S, Kolata J, Wende K, Schmidt A, Bundscherer L, Barton A, Kramer A, Brer B, Weltmann KD, Masur K. Non-thermal atmospheric pressure plasma jet treatment impacting viability and proliferation of human peripheral blood mononuclear cells. Plasma Process Polym 2013;accept.
49. McCall MN, Bolstad B, Irizarry RA. Frozen robust multiarray analysis (fRMA). Biostatistics 2010;11:242-253.
50. Green GH, Diggle PJ. On the operational characteristics of the Benjamini and Hochberg False Discovery Rate procedure. Stat Appl Genet Mol Biol 2007;6:Article27.
51. Schroder K, Busse B, Steff en H, Ohl A, Quade A, Weltmann KD. Confi guration of plasma processes for the generation of a chemical triple pattern for cell-based RNA arrays. Plasma Process Polym 2009;6:S46-S50.
52. Morris JH, Apeltsin L, Newman AM, Baumbach J, Wittkop T, Su G, et al. clusterMaker: a multi-algorithm clustering plugin for Cytoscape. BMC Bioinformatics 2011;12:436.
53. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998;95:14863-14868.
54. Baeuerle PA, Baichwal VR. NF-kappa B as a frequent target for immunosuppressive and anti-infl ammatory molecules. Adv Immunol 1997;65:111-137.
55. Kaplansky G, Bongrand P. Cytokines and chemokines. Cell Mol Biol (Noisy-le-grand) 2001;47:569-574.
56. Egwuagu CE, Yu CR, Zhang M, Mahdi RM, Kim SJ, Gery I. Suppressors of cytokine signaling proteins are diff erentially expressed in Th1 and Th2 cells: implications for Th cell lineage commitment and maintenance. J Immunol 2002;168:3181-3187.
57. Wong CK, Ho CY, Ko FW, Chan CH, Ho AS, Hui DS, Lam CW. Proinfl ammatory cytokines (IL-17, IL-6, IL-18 and IL-12) and Th cytokines (IFN-gamma, IL-4, IL-10 and IL-13) in patients with allergic asthma. Clin Exp Immunol 2001;125:177-183.
58. Kalmes M, Hennen J, Clemens J, Blmeke B. Impact of aryl hydrocarbon receptor (AhR) knockdown on cell cycle progression in human HaCaT keratinocytes. Biol Chem 2011;392:643-651.
59. Abbas A BJ, Rude J, Elfar A, Mukherjee D. PPAR-γ agonist in treatment of diabetes: cardiovascular safety considerations. Cardiovasc Hematol Agents Med Chem 2012;10:124-134.
60. Hong YC, Uhm HS. Microplasma jet at atmospheric pressure. Appl Phys Lett 2006;89:221504.
61. Fridman G, Shereshevsky A, Jost MM, Brooks AD, Fridman A. Floating electrode dielectric barrier discharge plasma in air promoting apoptotic behavior in melanoma skin cancer cell lines. Plasma Chem Plasma Process 2007;27:163-176.
62. Kim K, Geunyoung Kim, Hong YC, Yang SS. A cold micro plasma jet device suitable for bio-medical applications. Microelectron Eng 2010;87:1177-1180.
63. Weltmann KD, Polak M, Masur K, von Woedtke T, Winter J, Reuter S. Plasma processes and plasma sources in medicine. Contrib Plasma Phys 2012;52:644-654.
64. Lee SH, Zahoor M, Hwang JK, Mindo S, Choi KY. Valproic acid induces cutaneous wound healing in vivo and enhances keratinocyte motility. PLoS One 2012;7:e48791.
65. Blumenberg M. SKINOMICS: transcriptional profi ling in dermatology and skin biology. Curr Genomics 2012;13:363-368.
66. Keidar M, Walk R, Shashurin A, Srinivasan P, Sandler A, Dasgupta S, et al. Cold plasma selectivity and the possibility of a paradigm shift in cancer therapy. Br J Cancer 2011;105:1295-1301.
67. Gebicki S, Gebicki JM. Formation of peroxides in amino acids and proteins exposed to oxygen free radicals. Biochem J 1993;289:743-749.
68. Suzuki N, Mittler R. Reactive oxygen species-dependent wound responses in animals and plants. Free Radic Biol Med 2012;53:2269-2276.
69. Guan LM, Scandalios JG. Hydrogen-peroxide-mediated catalase gene expression in response to wounding. Free Radic Biol Med 2000;28:1182-1190.
70. Khodr B, Khalil Z. Modulation of infl ammation by reactive oxygen species: implications for aging and tissue repair. Free Radic Biol Med 2001; 30: 1-8.
71. Reuter S, Niemi K, Schulz-von der Gathen V, Dobele HF. Generation of atomic oxygen in the effl uent of an atmospheric pressure plasma jet. Plasma Sources Sci Technol 2009; 18.
72. Gao X, Dinkova-Kostova AT, Talalay P. Powerful and prolonged protection of human retinal pigment epithelial cells, keratinocytes, and mouse leukemia cells against oxidative damage: the indirect antioxidant eff ects of sulforaphane. Proc Natl Acad Sci USA 2001;98:15221-15226.
73. Halliwell B. Antioxidant defence mechanisms: from the beginning to the end (of the beginning). Free Radic Res 1999;31:261-272.
74. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci 2004;9:490-498.
75. Brown DI, Griendling KK. Nox proteins in signal transduction. Free Radic Biol Med 2009; 47: 1239-1253.
76. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 2002;82:47-95.
77. Takahashi K, Avissar N, Whitin J, Cohen H. Purifi cation and characterization of human plasma glutathione peroxidase: a selenoglycoprotein distinct from the known cellular enzyme. Arch Biochem Biophys 1987; 256: 677-686.
78. Mullenbach GT, Tabrizi A, Irvine BD, Bell GI, Hallewell RA. Sequence of a cDNA coding for human glutathione peroxidase confi rms TGA encodes active site selenocysteine. Nucleic Acids Res 1987;15:5484.
79. Radyuk SN, Michalak K, Klichko VI, Benes J, Rebrin I, Sohal RS, Orr WC. Peroxiredoxin 5 confers protection against oxidative stress and apoptosis and also promotes longevity in Drosophila. Biochem J 2009;419:437-445.
80. Hochstrasser DF, Frutiger S, Paquet N, Bairoch A, Ravier F, Pasquali C, et al. Human liver protein map: a reference database established by microsequencing and gel comparison. Electrophoresis 1992;13:992-1001.
81. Kumin A, Huber C, Rulicke T, Wolf E, Werner S. Peroxiredoxin 6 is a potent cytoprotective enzyme in the epidermis. Am J Pathol 2006;169:1194-1205.
82. Cole-Ezea P, Swan D, Shanley D, Hesketh J. Glutathione peroxidase 4 has a major role in protecting mitochondria from oxidative damage and maintaining oxidative phosphorylation complexes in gut epithelial cells. Free Radic Biol Med 2012;53:488-497.
83. Brauer AU, Savaskan NE, Kuhn H, Prehn S, Ninnemann O, Nitsch R. A new phospholipid phosphatase, PRG-1, is involved in axon growth and regenerative sprouting. Nat Neurosci 2003;6:572-578.
84. Hayes JD, McLellan LI. Glutathione and glutathionedependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic Res 1999;31:273-300.
85. Loos H, Roos D, Weening R, Houwerzijl J. Familial defi ciency of glutathione reductase in human blood cells. Blood 1976;48:53-62.
86. Sen S, Kawahara B, Chaudhuri G. Maintenance of higher H(2) O(2) levels, and its mechanism of action to induce growth in breast cancer cells: important roles of bioactive catalase and PP2A. Free Radic Biol Med 2012; 53: 1541-1551.
87. Bai J, Cederbaum AI. Catalase protects HepG2 cells from apoptosis induced by DNA-damaging agents by accelerating the degradation of p53. J Biol Chem 2003;278:4660-4667.
88. Yu L, Wan F, Dutta S, Welsh S, Liu Z, Freundt E, et al. Autophagic programmed cell death by selective catalase degradation. Proc Natl Acad Sci USA 2006;103:4952-4957.
89. Huang P, Feng L, Oldham EA, Keating MJ, Plunkett W. Superoxide dismutase as a target for the selective killing of cancer cells. Nature 2000;407:390-395.
90. Pryor WA. Oxy-radicals and related species: their formation, lifetimes, and reactions. Annu Rev Physiol 1986;48:657-667.
91. Kang JS, Kim HN, Jung da J, Kim JE, Mun GH, Kim YS, et al. Regulation of UVB-induced IL-8 and MCP-1 production in skin keratinocytes by increasing vitamin C uptake via the redistribution of SVCT-1 from the cytosol to the membrane. J Invest Dermatol 2007; 127: 698-706.
92. Duarte TL, Cooke MS, Jones GD. Gene expression profi ling reveals new protective roles for vitamin C in human skin cells. Free Radic Biol Med 2009; 46: 78-87.