Overexpression of peroxiredoxin I and thioredoxin1 in human breast carcinoma
Mee-Kyung Cha, Kyung-Hoon Suh, Il-Han Kim, Mee-Kyung Cha, Kyung-Hoon Suh, Il-Han Kim
Abstract
Background: Peroxiredoxins (Prxs) are a novel group of peroxidases containing high antioxidant efficiency. The mammalian Prx family has six distinct members (Prx I-VI) in various subcellular locations, including peroxisomes and mitochondria, places where oxidative stress is most evident. The function of Prx I in particular has been implicated in regulating cell proliferation, differentiation, and apoptosis. Since thioredoxin1 (Trx1) as an electron donor is functionally associated with Prx I, we investigated levels of expression of both Prx I and Trx1.
Methods: We investigated levels of expression of both Prx I and Trx1 in breast cancer by real-time polymerase chain reaction (RT-PCR) and Western blot.
Results: Levels of messenger RNA (mRNA) for both Prx I and Trx1 in normal human breast tissue were very low compared to other major human tissues, whereas their levels in breast cancer exceeded that in other solid cancers (colon, kidney, liver, lung, ovary, prostate, and thyroid). Among members of the Prx family (Prx I-VI) and Trx family (Trx1, Trx2), Prx I and Trx1 were preferentially induced in breast cancer. Moreover, the expression of each was associated with progress of breast cancer and correlated with each other. Western blot analysis of different and paired breast tissues revealed consistent and preferential expression of Prx I and Trx1 protein in breast cancer tissue.
Conclusion: Prx I and Trx1 are overexpressed in human breast carcinoma and the expression levels are associated with tumor grade. The striking induction of Prx I and Trx1 in breast cancer may enable their use as breast cancer markers.
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References
- Sundaresan M, Yu ZX, Ferrans VJ, Irani K, Finkel T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science. 1995;270:296–299. doi: 10.1126/science.270.5234.296.
- Finkel T. Oxygen radicals and signaling. Curr Opin Cell Biol. 1998;10:248–253. doi: 10.1016/S0955-0674(98)80147-6.
- Kang SW, Chae HZ, Seo MS, Kim K, Baines IC, Rhee SG. Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-alpha. J Biol Chem . 1998;273(11):6297–6302. doi: 10.1074/jbc.273.11.6297.
- Chae HZ, Robison K, Poole LB, Church G, Storz G, Rhee SG. Cloning and sequencing of thiol-specific antioxidant from mammalian brain, alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc Natl Acad Sci USA. 1994;91:7017–7021. doi: 10.1073/pnas.91.15.7017.
- Klaunig JE, Xu Y, Isenberg JS, Bachowski S, Kolaja KL, Jiang J, Stevenson DE, Walborg EF., Jr The role of oxidative stress in chemical carcinogenesis. Environ Health Perspect. 1998;106:289–295. doi: 10.2307/3433929.
- Dhalla NS, Temsah RM, Netticadan T. Role of oxidative stress in cardiovascular diseases. J Hypertens. 2000;18:655–673. doi: 10.1097/00004872-200018060-00002.
- Ambrosone CB. Oxidants and antioxidants in breast cancer. Antioxid Redox Signal. 2000;2:903–917. doi: 10.1089/ars.2000.2.4-903.
- Kim SH, Fountoulakis M, Cairns N, Lubec G. Protein levels of human peroxiredoxin subtypes in brains of patients with Alzheimer's disease and Down syndrome. J Neural Transm Suppl . 2001;(61):223–235.
- Wright RM, McManaman JL, Repine JE. Alcohol-induced breast cancer: a proposed mechanism. Free Rad Biol Med. 1999;26:348–354. doi: 10.1016/S0891-5849(98)00204-4.
- Haklar G, Sayin-Ozveri E, Yuksel M, Aktan AO, Yalcin AS. Different kinds of reactive oxygen and nitrogen species were detected in colon and breast tumors. Cancer Lett. 2001;165:219–224. doi: 10.1016/S0304-3835(01)00421-9.
- Nelson RL. Dietary iron and colorectal cancer risk. Free Radic Biol Med. 1992;12(2):161–168. doi: 10.1016/0891-5849(92)90010-E.
- Mitsumoto A, Takanezava Y, Okawa K, Iwamatsu A, Nakagawa Y. of peroxiredoxin expression in response to hydroperoxide stress. Free Rad Biol Med. 2001;30:625–635. doi: 10.1016/S0891-5849(00)00503-7.
- Noh DY, Ahn SJ, Lee RA, Kim SW, Park IA, Chae HZ. Overexpression of peroxiredoxin in human breast cancer. Anticancer Res. 2001;21:2085–2090.
- Yanagawa T, Ishikawa T, Ishii T, Tabuchi K, Iwasa S, Bannai S, Omura K, Suzuki H, Yoshida H. Peroxiredoxin I expression in human thyroid tumors. Cancer Lett . 1999;154(1-2):127–132. doi: 10.1016/S0304-3835(99)00243-8.
- Yanagawa T, Iwasa S, Ishii T, Tabuchi K, Yusa H, Onizawa K, Omura K, Harada H, Suzuki H, Yoshida H. Peroxiredoxin I expression in oral cancer: a potential new tumor marker. Cancer Lett. 2000;156:27–35. doi: 10.1016/S0304-3835(00)00434-1.
- Karihtala P, Mäntyniemi A, Kang SW, Kinnula VL, Soini Y. Peroxiredoxins in Breast. Clinical Cancer Research. 2003;9:3418–3424.
- Rhee SG, Chae HZ, Kim K. Carcinoma Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signalling. Free Rad Biol Med. 2005;38:1543–1552. doi: 10.1016/j.freeradbiomed.2005.02.026.
- Mitsui A, Hirakawa T, Yodoi J. Reactive oxygen-reducing and protein-refolding activities of adult T cell leukemia-derived factor/human thioredoxin. Biochem Biophys Res Commun. 1992;186:1220–1226. doi: 10.1016/S0006-291X(05)81536-0.
- Ohira A, Honda O, Gauntt CD, Yamamoto M, Hori K, Masutani H, Yodoi J, Honda Y. Oxidative stress induces adult T cell leukemia derived factor/thioredoxin in the rat retina. Lab Invest. 1994;70:279–285.
- Nakamura H, Matsuda M, Furuke K, Kitaoka Y, Iwata S, Toda K, Inamoto T, Yamaoka Y, Ozawa K, Yodoi J. Adult T cell leukemia-derived factor/human thioredoxin protects endothelial F-2 cell injury caused by activated neutrophils or hydrogen peroxide. Immunol Lett. 1994;42:75–80. doi: 10.1016/0165-2478(94)90038-8.
- Sasada T, Iwata S, Sato N, Kitaoka Y, Hirota K, Nakamura K, Nishiyama Taniguchi A, Takabayashi A, Yodoi J. Redox control of resistance to cis-diamminedichloroplatinum (II) (CDDP): Protective effect of human thioredoxin against CDDP-induced cytotoxicity. J Clin Invest. 1996;97:2268–2276. doi: 10.1172/JCI118668.
- Schenk H, Klein M, Erdbrugger W, Droge W, Schulze OK. Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-κB and AP-1. Proc Natl Acad Sci USA. 1994;91:1672–1676. doi: 10.1073/pnas.91.5.1672.
- Makino Y, Okamoto K, Yoshikawa N, Aoshima M, Hirota K, Yodoi J, Umesono K, Makino I, Tanaka H. Thioredoxin: A redox-regulating cellular cofactor for glucocorticoid hormone action: Crosstalk between endocrine control of stress response and cellular antioxidant defense system. J Clin Invest. 1995;98:2469–2477. doi: 10.1172/JCI119065.
- Ueno M, Masutani H, Arai AJ, Yamauchi A, Hirota K, Sakai T, Inamoto T, Yamaoka J, Yodoi J, Nikaido T. Thioredoxin-dependent redox regulation of p53-mediated p21 activation. J Biol Chem. 1999;274:35809–35815. doi: 10.1074/jbc.274.50.35809.
- Hayashi S, Hajiro NK, Makino Y, Eguchi H, Yodoi Y, Tanaka H. Functional modulation of estrogen receptor by redox state with reference to thioredoxin as a mediator. Nucleic Acids Res. 1997;25:4035–4040. doi: 10.1093/nar/25.20.4035.
- Nakamura H, Masutani H, Tagaya Y, Yamauchi A, Inamoto T, Nanbu Y, Fujii S, Ozawa K, Yodoi Y. Expression and growth-promoting effect of adult T-cell leukemia-derived factor: A human thioredoxin homologue in hepatocellular carcinoma. Cancer. 1992;69:2091–2097. doi: 10.1002/1097-0142(19920415)69:8<2091::AID-CNCR2820690814>;2-X.
- Fujii S, Nanbu Y, Nonogaki H, Konishi I, Mori T, Masutani H, Yodoi Y. Coexpression of adult T-cell leukemia-derived factor, a human thioredoxin homologue, and human papillomavirus DNA in neoplastic cervical squamous epithelium. Cancer. 1991;68:1583–1591. doi: 10.1002/1097-0142(19911001)68:7<1583::AID-CNCR2820680720>;2-N.
- Kobayashi F, Sagawa N, Nanbu Y, Kitaoka Y, Mori T, Fujii S, Nakamura H, Masutani H, Yodoi Y. Biochemical and topological analysis of adult T-cell leukaemia-derived factor, homologous to thioredoxin, in the pregnant human uterus. Hum Reprod. 1995;10:1603–1608.
- Wood ZacharyA, Poole LeslieB, Roy R, Hantgan P, Karplus A. Dimers to Doughnuts: Redox-Sensitive Oligomerization of 2-Cysteine Peroxiredoxins. Biochemistry. 2002;41:5493–5504. doi: 10.1021/bi012173m.
- Seo MS, Kang SW, Kim K, Baines IC, Lee TH, Rhee SG. Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J Biol Chem. 2000;275:20346–20354. doi: 10.1074/jbc.M001943200.
- Wagner E, Luche S, Penna L, Chevallet M, Van Dorsselaer A, Leize-Wagner E, Rabilloud T. A method for detection of overoxidation of cysteines: peroxiredoxins are oxidized in vivo at the active-site cysteine during oxidative stress. Biochem J. 2002;366:777–785.
- Chang TS, Jeong W, Choi SY, Yu S, Kang SW, Rhee SG. Regulation of peroxiredoxin I activity by Cdc2-mediated phosphorylation. J Biol Chem. 2002;277:25370–20376. doi: 10.1074/jbc.M110432200.
- Nakamura H, Bai J, Nishinaka Y, Ueda S, Sasada T, Ohshio G, Imamura M, Takabayashi A, Yamaoka Y, Yodoi Expression of thioredoxin and glutaredoxin, redox-regulating proteins, in pancreatic cancer. Cancer Detect Prev . 2000;24(1):53–60.
- Matsutani Y, Yamauchi A, Takahashi R, Ueno M, Yoshikawa K, Honda K, Nakamura H, Kato H, Kodama H, Inamoto T, Yodoi J, Yamaoka Inverse correlation of thioredoxin expression with estrogen receptor- and p53-dependent tumor growth in breast cancer tissues. Clin Cancer Res. 2001;7:3430–3436.
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