Manganese superoxide dismutase-mediated inside-out signaling in HaCaT human keratinocytes and SKH-1 mouse skin

Antioxidants and Redox Signaling

Volumn 20, Issue 15, 2014, Pages 2347-2360

  Holley, Aaron K ^a   Xu, Yong ^a   Noel, Teresa ^a   Bakthavatchalu, Vasudevan ^a   Batinic Haberle, Ines ^b   St Clair, Daret K ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; HYDROETHIDINE; MANGANESE MESO TETRAKIS(N,N BUTOXYETHYLPYRIDINIUM 2 YL)PORPHYRIN; MANGANESE SUPEROXIDE DISMUTASE; PEPTIDOMIMETIC AGENT; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; UNCLASSIFIED DRUG; EPIDERMAL GROWTH FACTOR; NOX4 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROTECTION; ENZYME ACTIVATION; GENE SILENCING; HACAT CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INSIDE OUT SIGNALING; INTRACELLULAR SIGNALING; KERATINOCYTE; KNOCKOUT MOUSE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE; ULTRAVIOLET RADIATION; ANIMAL; BIOSYNTHESIS; CELL LINE; GENETICS; METABOLISM; MOLECULAR MIMICRY; SIGNAL TRANSDUCTION; SKIN;

ANIMALS; CELL LINE; EPIDERMAL GROWTH FACTOR; GENE KNOCKDOWN TECHNIQUES; HUMANS; KERATINOCYTES; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR MIMICRY; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SKIN; SRC-FAMILY KINASES; SUPEROXIDE DISMUTASE; ULTRAVIOLET RAYS;

EID: 84899736388     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5204     Document Type: Article

References (67)

1. 2 mediate the differential susceptibility of cancer cells versus normal cells to glucose deprivation. Biochem J 418: 29-37, 2009.
2. Ayli EE, Li W, Brown TT, Witkiewicz A, Elenitsas R, and Seykora JT. Activation of Src-family tyrosine kinases in hyperproliferative epidermal disorders. J Cutan Pathol 35: 273-277, 2007.
3. Aziz MH, Ghotra AS, Shukla Y, and Ahmad N. Ultraviolet-B radiation causes an upregulation of survivin in human keratinocytes and mouse skin. Photochem Photobiol 80: 602-608, 2004.
4. Bakthavatchalu V, Dey S, Xu Y, Noel T, Jungsuwadee P, Holley AK, Dhar SK, Batinic-Haberle I, and St. Clair DK. Manganese superoxide dismutase is a mitochondrial fidelity protein that protects Polc against UV-induced inactivation. Oncogene 31: 2129-2139, 2012.
5. Barnekow A, Paul E, and Schartl M. Expression of the csrc protooncogene in human skin tumors. Cancer Res 47: 235-240, 1987.
6. Batinic-Haberle I, Reboucas JS, and Spasojevic I. Superoxide dismutase mimics: chemistry, pharmacology, and therapeutic potential. Antioxid Redox Signal 13: 877-918, 2010.
7. Bedard K, and Karuse K-H. The NOX family of ROSgenerating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313, 2007.
8. Birch-Machin MA and Swalwell H. How mitochondria record the effects of UV exposure and oxidative stress using human skin as a model tissue. Mutagenesis 25: 101-107, 2010.
9. Bolden A, Noy GP, and Weissbach A. DNA polymerase of mitochondria is a gamma-polymerase. J Biol Chem 252: 3351-3356, 1977.
10. Chamulitrat W, Stremmel W, Kawahara T, Rokutan K, Fujii H, Wingler K, Schmidt HHHW, and Schmidt R. A constitutive NADPH oxidase-like system containing gp91 phox homologs in human keratinocytes. J Invest Dermatol 122: 1000-1009, 2004.
11. Chatzizacharias NA, Kouraklis GP, Giaginis CT, and Theocharis SE. Clinical significance of Src expression and activity in human neoplasia. Histol Histopathol 27: 677-692, 2012.
12. De Gruijl FR. Skin cancer and solar UV radiation. Eur J Cancer 35: 2003-2009, 1999.
13. Devary Y, Gottlieb RA, Smeal T, and Karin M. The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases. Cell 71: 1081-1091, 1992.
14. El-Abaseri TB, Fuhrman J, Trempus C, Shendrik I, Tennant RW, and Hansen LA. Chemoprevention of UV lightinduced skin tumorigenesis by inhibition of the epidermal growth factor receptor. Cancer Res 65: 3958-3965, 2005.
15. El-Abaseri TB, Hammiller B, Repertinger SK, and Hansen LA. The epidermal growth factor receptor increases cytokine production and cutaneous inflammation in response to ultraviolet irradiation. ISRN Dermatol 2013, 2013.
16. El-Abaseri TB and Hansen LA. EGFR activation and ultraviolet light-induced skin carcinogenesis. J Biomed Biotechnol 2007, 2007.
17. El-Abaseri TB, Putta S, and Hansen LA. Ultraviolet irradiation induces keratinocyte proliferation and epidermal hyperplasia through the activation of the epidermal growth factor receptor. Carcinogenesis 27: 225-231, 2006.
18. Frey P, Forand R, Maciag T, and Shooter EM. The biosynthetic precursor of epidermal growth factor and the mechanism of its processing. Proc Natl Acad Sci U S A 76: 6294-6298, 1979.
19. Gniadecki R, Thorn T, Vicanova J, Petersen A, and Wulf HC. Role of mitochondria in ultraviolet-induced oxidative stress. J Cell Biochem 80: 216-222, 2000.
20. Graham KA, Kulawiec M, Owens KM, Li X, Desouki MM, Chandra D, and Singh KK. NADPH oxidase 4 is an oncoprotein localized to mitochondria. Cancer Biol Ther 10: 1-9, 2010.
21. Harris RC, Chung E, and Coffey RJ. EGF receptor ligands. Exp Cell Res 284: 2-13, 2003.
22. Holley AK, Bakthavatchalu V, Velez-Roman JM, and St. Clair DK. Manganese superoxide dismutase: guardian of the powerhouse. Int J Mol Sci 12, 2011.
23. Huang R-P, Wu J-X, Fan Y, and Adamson ED. UV activates growth factor receptors via reactive oxygen intermediates. J Cell Biol 133: 211-220, 1996.
24. Ichihashi M, Ueda M, Budiyanto A, Bito T, Oka M, Fukunaga M, Tsuru K, and Horikawa T. UV-induced skin damage. Toxicology 189: 21-39, 2003.
25. Jagadeesha DK, Takapoo M, Banfi B, Bhalla RC, and Miller Jr FJ. Nox1 transactivation of epidermal growth factor receptor promotes N-cadherin shedding and smooth muscle cell migration. Cardiovasc Res 93: 406-413, 2012.
26. Jandova J, Eshaghian A, Shi M, Li M, King LE, Janda J, and Sligh JE. Identification of an mtDNA mutation hot spot in UV-induced mouse skin tumors producing altered cellular biochemistry. J Invest Dermatol 132: 421-428, 2012.
27. Kitagawa D, Tanemura S, Ohata S, Shimizu N, Seo J, Nishitai G, Watanabe T, Nakagawa K, Kishimoto H, Wada T, Tezuka T, Yamamoto T, Nishina H, and Katada T. Activation of extracellular signal-regulated kinase by ultraviolet is mediated through Src-dependent epidermal growth factor receptor phosphorylation. Its implication in an anti-apoptotitic function. J Biol Chem 277: 366-371, 2002.
28. Le Gall SM, Auger R, Dreux C, and Mauduit P. Regulated cell surface pro-EGF ectodomain shedding is a zinc metalloprotease-dependent process. J Biol Chem 278: 45255-45268, 2003.
29. Lee JH, Pyon J-K, Kim DW, Lee SH, Nam HS, Kim CH, Kang SG, Lee YJ, Park MY, Jeong DJ, and Cho MK. Elevated c-Src and c-Yes expression in malignant skin cancers. J Exp Clin Cancer Res 29: 116, 2010.
30. Lee JK, Edderkaoui M, Truong P, Ohno I, Jang K-T, Berti A, Pandol SJ, and Gukovskaya AS. NADPH oxidase promotes pancreatic cancer cell survival via inhibiting JAK2 dephosphorylation by tyrosine phosphatases. Gastroenterology 133: 1637-1648, 2007.
31. Li Y, Huang T-T, Carlson EJ, Melov S, Ursell PC, Olson JL, Noble LJ, Yoshimura MP, Berger C, Chan PH, Wallace DC, and Epstein CJ. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 11, 1995.
32. Lim JH, Lee JI, Suh YH, Kim W, Song JH, and Jung MH. Mitochondrial dysfunction induces aberrant insulin signalling and glucose utilisation in murine C2C12 myotube cells. Diabetologia 49: 1924-1936, 2006.
33. Madson JG and Hansen LA. Multiple mechanisms of Erbb2 action after ultraviolet irradiation of the skin. Mol Carcinog 46: 624-628, 2007.
34. Matsumura Y and Ananthaswamy HN. Toxic effects of ultraviolet radiation on the skin. Toxicol Appl Pharmacol 195: 298-308, 2004.
35. Mitchell DL, Byrom M, Chiarello S, and Lowery MG. Attenuation of DNA damage in the dermis and epidermis of the albino hairless mouse by chronic exposure to ultraviolet-A and -B radiation. Photochem Photobiol 73: 83-89, 2001.
36. Mochizuki T, Furuta S, Mitsushita J, Shang WH, Ito M, Yokoo Y, Yamaura M, Ishizone S, Nakayama J, Konagai A, Hirose K, Kiyosawa K, and Kamata T. Inhibition of NADPH oxidase 4 activates apoptosis via the AKT/apoptosis signalregulating kinase 1 pathway in pancreatic cancer PANC-1 cells. Oncogene 25: 3699-3707, 2006.
37. Oberley LW. Mechanism of the tumor suppressive effect of MnSOD overexpression. Biomed Pharmacother 59: 143-148, 2005.
38. Owusu-Ansah E, Yavari A, Mandal S, and Banerjee U. Distinct mitochondrial retrograde signals control the G1-S cell cycle checkpoint. Nat Genet 40: 356-361, 2008.
39. Paz ML, Maglio DHG, Weill FS, Bustamante J, and Leoni J. Mitochondrial dysfunction and cellular stress progression after ultraviolet B irradiation in human keratinocytes. Photodermatol Photoimmunol Photomed 24: 115-122, 2008.
40. 2 is an important mediator of UVB-induced EGF-receptor phosphorylation in cultured keratinocytes. J Invest Dermatol 110: 966-971, 1998.
41. Poyton RO and McEwen JE. Crosstalk between nuclear and mitochondrial genomes. Ann Rev Biochem 65: 563-607, 1996.
42. Rajic Z, Tovmasyan A, Spasojevic I, Sheng H, Lu M, Li AM, Gralla EB, Warner DS, Benov L, and Batinic-Haberle I. A new SOD mimetic, Mn(III) ortho N-butoxyethylpyridiylporphyrin, combines superb potency and lipophilicity with low toxicity. Free Radic Biol Med 52: 1828-1834, 2012.
43. Sancho P and Fabregat I. NADPH oxidase NOX1 controls autocrine growth of liver tumor cells through up-regulation of the epidermal growth factor receptor pathway. J Biol Chem 285: 24815-24824, 2010.
44. Sato K-i, Sato A, Aoto M, and Fukami Y. Site-specific association of c-SRC with epidermal growth factor receptor in A431 cells. Biochem Biophys Res Commun 210: 844-851, 1995.
45. Schneider MR, Werner S, Paus R, and Wolf E. Beyond wavy hairs: the epidermal growth factor receptor and its ligands in skin biology and pathology. Am J Pathol 173: 14-24, 2008.
46. Seo M and Juhnn Y-S. Gq protein mediates UVB-induced cyclooxygenase-2 expression by stimulating HB-EGF secretion from HaCaT human keratinocytes. Biochem Biophys Res Commun 393:190-195, 2010.
47. Seo M, Lee M-J, Heo JH, Lee Y-I, Kim Y, Kim S-Y, Lee E-S, and Juhnn Y-S. G protein βγ subunits augment UVBinduced apoptosis by stimulating the release of soluble heparin-binding epidermal growth factor from human keratinocytes. J Biol Chem 282: 24720-24730, 2007.
48. Simeonova PP, Wang S, Hulderman T, and Luster MI. c-Src-dependent activation of the epidermal growth factor receptor and mitogen-activated protein kinase pathway by arsenic. Role in carcinogenesis. J Biol Chem 277: 2945-2950, 2002.
49. Singh AB and Harris RC. Autocrine, paracrine and juxtacrine signaling by EGFR ligands. Cell Signal 17: 1183-1193, 2005.
50. Singh B, Schneider M, Knyazev P, and Ullrich A. UVinduced EGFR signal transactivation is dependent on proligand shedding by activated metalloproteases in skin cancer cell lines. Int J Cancer 124: 531-539, 2009.
51. Takai D, Park S-H, Takada Y, Ichinose S, Kitagawa M, and Akashi M. UV-irradiation induces oxidative damage to mitochondrial DNA primarily through hydrogen peroxide: analysis of 8-oxodGuo by HPLC. Free Radic Res 40: 1138-1148, 2006.
52. Tovmasyan A, Reboucas JS, and Benov L. Simple biological systems for assessing the activity of superoxide dismutase mimics. Antioxid Redox Signal 20: 2416-2436, 2014.
53. Traven A, Wong JMS, Xu D, Sopta M, and Ingles CJ. Interorganellar communication. Altered nuclear gene expression profiles in a yeast mitochondrial DNA mutant. J Biol Chem 276: 4020-4027, 2001.
54. Valerie K, Yacoub A, Hagan MP, Curiel DT, Fisher PB, Grant S, and Dent P. Radiation-induced cell signaling: inside-out and outside-in. Mol Cancer Ther 6: 789-901, 2007.
55. van Duin M, Westerveld A, and Hoeijmakers JHJ. UV stimulation of DNA-mediated transformation of human cells. Mol Cell Biol 5: 734-741, 1985.
56. Vaquero EC, Edderkaoui M, Pandol SJ, Gukovsky I, and Gukovskaya AS. Reactive oxygen species produced by NAD(P)H oxidase inhibit apoptosis in pancreatic cancer cells. J Biol Chem 279: 34643-34654, 2004.
57. Wang R, Dashwood W-M, Nian H, Lohr CV, Fischer KA, Tsuchiya N, Nakagama H, Ashktorab H, and Dashwood RH. NADPH oxidase overexpression in human colon cancers and rat colon tumors induced by 2-amino-1- methyl-6-phenylimidazo[4,5-b] pyridine (PhIP). Int J Cancer 128: 2581-2590, 2011.
58. Weitner T, Kos I, Sheng H, Tovmasyan A, Reboucas JS, Fan P, Waner DS, Vujaskovic Z, Batinic-Haberle I, and Spasojevic I. Comprehensive pharmacokinetic studies and oral bioavailability of two Mn porphyrin-based SOD mimics, MnTE-2-PyP(5 +) and MnTnHex-2-PyP(5 +). Free Radic Biol Med 58: 73-80, 2013.
59. Weyemi U, Caillou B, Talbot M, Ameziane-El-Hassani R, Lacroix L, Lagent-Chevallier O, Ghuzlan AA, Roos D, Bidart J-M, Virion A, Schlumberger M, and Dupuy C. Intracellular expression of reactive oxygen species-generating NADPH oxidase NOX4 in normal and cancer thyroid tissues. Endocr Relat Cancer 17: 27-37, 2010.
60. Wheeler DL, Iida M, and Dunn EF. The role of Src in solid tumors. Oncologist 14: 667-678, 2009.
61. Woo DK, Phang TL, Trawick JD, and Poyton RO. Multiple pathways of mitochondrial-nuclear communication in yeast: intergenomic signaling involves ABF1 and affects a different set of genes than retrograde regulation. Biochim Biophys Acta 1789: 135-145, 2009.
62. Xu Y, Shao Y, Voorhees JJ, and Fisher GJ. Oxidative inhibition of receptor-type protein tyrosine phosphatase κ by ultraviolet irradiation activates epidermal growth factor receptor in human keratinocytes. J Biol Chem 281: 27389-27397, 2006.
63. Xu Y, Shao Y, Zhou J, Voorhees JJ, and Fisher GJ. Ultraviolet irradiation-induces epidermal growth factor receptor (EGFR) nuclear translocation in human keratinocytes. J Cell Biochem 107: 873-880, 2009.
64. Xu Y, Tan L-J, Grachtchouk V, Voorhees JJ, and Fisher GJ. Receptor-type protein-tyrosine phosphatase-κ regulates epidermal growth factor receptor function. J Biol Chem 280: 42694-42700, 2005.
65. Yen H-C, Oberley TD, Vichitbandha S, Ho Y-S, and St. Clair DK. The protective role of manganese superoxide dismutase against adriamycin-induced acute cardiac toxicity in transgenic mice. J Clin Invest 98: 1253-1260, 1996.
66. Zhao Y, Chaiswing L, Oberley TD, Batinic-Haberle I, St. Clair W, Epstein CJ, and St. Clair DK. A mechanism-based antioxidant approach for the reduction of skin carcinogenesis. Cancer Res 65: 1401-1405, 2005.
67. Zhao Y, Xue Y, Oberley TD, Kiningham KK, Lin S-M, Yen H-C, Majima H, Hines J, and St. Clair DK. Overexpression of manganese superoxide dismutase suppresses tumor formation by modulation of activator protein-1 signaling in a multistage skin carcinogenesis model. Cancer Res 61: 6082-6088, 2001.