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Virchows Archiv

, Volume 463, Issue 4, pp 553–562 | Cite as

Peroxiredoxins, thioredoxin, and Y-box-binding protein-1 are involved in the pathogenesis and progression of dialysis-associated renal cell carcinoma

  • Fumiyoshi Fushimi
  • Kenichi Taguchi
  • Hiroto Izumi
  • Kimitoshi Kohno
  • Michihiko Kuwano
  • Mayumi Ono
  • Yutaka Nakashima
  • Tetsuro Takesue
  • Seiji Naito
  • Yoshinao OdaEmail author
Original Article

Abstract

Patients with end-stage renal disease are exposed to increased oxidative stress and impairment of antioxidant mechanisms. We focused on dialysis renal cell carcinoma (RCC), including epithelial hyperplasia in acquired cystic disease of the kidney (ACDK). We attempted to obtain insight into the carcinogenesis and tumor progression in terms of cellular defense mechanisms associated with oxidative stress by investigating the expression of antioxidant proteins by immunohistochemistry. We evaluated retrospectively 43 cases of dialysis RCC and, as a control group, 49 cases of sporadic RCC. Peroxiredoxin (Prx) 1, 3, 4, 5, and 6 expression in dialysis RCC was positively correlated with the duration of dialysis. In epithelial hyperplasia, in 17 cases of acquired cystic disease of the kidney, Prxs and thioredoxin were highly expressed. Moreover, in dialysis RCC, Prx 3, 4, and 5 immunoreactivity and nuclear expression of Y-box-binding protein-1 were higher than in sporadic RCC. In dialysis RCC, Prx 3, 4, and 5 immunoreactivity positively correlated with the Fuhrman nuclear grade. These data suggest that oxidative stress during dialysis enhances antioxidant activity, with an inhibiting effect on carcinogenesis. Once cancer has developed, antioxidant activity might have a stimulating effect on the progression of dialysis RCC.

Keywords

Oxidative stress Peroxiredoxin Y-box-binding protein-1 Renal cell carcinoma Acquired cystic disease of kidney 

Notes

Acknowledgments

This study was supported by a Grant-in-Aid for Challenging Exploratory Research (no. 24650646) from the Japan Society for the Promotion of Science, Tokyo, Japan. We are grateful to Mr. Steve Cotton, Aso Corporation, for editing the English language in this manuscript.

Conflict of interest

None.

References

  1. 1.
    Del Vecchio L, Locatelli F, Carini M (2011) What we know about oxidative stress in patients with chronic kidney disease on dialysis—clinical effects, potential treatment, and prevention. Semin Dial 24:56–64PubMedCrossRefGoogle Scholar
  2. 2.
    Kuntz E, Yusenko MV, Nagy A, Kovacs G (2010) Oligoarray comparative genomic hybridization of renal cell tumors that developed in patients with acquired cystic renal disease. Hum Pathol 41:1345–1349PubMedCrossRefGoogle Scholar
  3. 3.
    Hori Y, Oda Y, Kiyoshima K et al (2007) Oxidative stress and DNA hypermethylation status in renal cell carcinoma arising in patients on dialysis. J Pathol 212:218–26PubMedCrossRefGoogle Scholar
  4. 4.
    Morgan MJ, Liu ZG (2011) Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res 21:103–15PubMedCrossRefGoogle Scholar
  5. 5.
    Cossu-Rocca P, Eble JN, Zhang S, Martignoni G, Brunelli M, Cheng L (2006) Acquired cystic disease-associated renal tumors: an immunohistochemical and fluorescence in situ hybridization study. Mod Pathol 19:780–7PubMedGoogle Scholar
  6. 6.
    Cheuk W, Lo ES, Chan AK, Chan JK (2002) Atypical epithelial proliferations in acquired renal cystic disease harbor cytogenetic aberrations. Hum Pathol 33:761–5PubMedCrossRefGoogle Scholar
  7. 7.
    Hofmann B, Hecht HJ, Flohe L (2002) Peroxiredoxins. Biol Chem 383:347–64PubMedGoogle Scholar
  8. 8.
    Arnér ES, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102–9PubMedCrossRefGoogle Scholar
  9. 9.
    Avila PC, Kropotov AV, Krutilina R, Krasnodembskay A, Tomilin NV, Serikov VB (2008) Peroxiredoxin V contributes to antioxidant defense of lung epithelial cells. Lung 186:103–114PubMedCrossRefGoogle Scholar
  10. 10.
    Cha MK, Suh KH, Kim IH (2009) Overexpression of peroxiredoxin I and thioredoxin1 in human breast carcinoma. J Exp Clin Cancer Res 28:93–104PubMedCrossRefGoogle Scholar
  11. 11.
    Burke-Gaffney A, Callister ME, Nakamura H (2005) Thioredoxin: friend or foe in human disease? Trends Pharmacol Sci 26:398–404PubMedCrossRefGoogle Scholar
  12. 12.
    Chen MF, Lee KD, Yeh CH et al (2010) Role of peroxiredoxin I in rectal cancer and related to p53 status. Int J Radiat Oncol Biol Phys 78:868–878PubMedCrossRefGoogle Scholar
  13. 13.
    Wei Q, Jiang H, Xiao Z et al (2011) Sulfiredoxin–peroxiredoxin IV axis promotes human lung cancer progression through modulation of specific phosphokinase signaling. Proc Natl Acad Sci U S A 108:7004–9PubMedCrossRefGoogle Scholar
  14. 14.
    Cohen SB, Ma W, Valova VA et al (2010) Genotoxic stress-induced nuclear localization of oncoprotein YB-1 in the absence of proteolytic processing. Oncogene 29:403–10PubMedCrossRefGoogle Scholar
  15. 15.
    Hayakawa H, Uchiumi T, Fukuda T et al (2002) Binding capacity of human YB-1 protein for RNA containing 8-oxoguanine. Biochemistry 41:12739–44PubMedCrossRefGoogle Scholar
  16. 16.
    Eble JN, Sauter G, Epstein JI, Sesterhenn IA (eds) (2004) World Health Organization classification of tumors. Pathology and genetics of tumors of the urinary system and male genital organs. Lyon, IARCGoogle Scholar
  17. 17.
    Shiota M, Izumi H, Miyamoto N et al (2008) Ets regulates peroxiredoxin1 and 5 expressions through their interaction with the high-mobility group protein B1. Cancer Sci 99:1950–9PubMedGoogle Scholar
  18. 18.
    Ohga T, Koike K, Ono M et al (1996) Role of the human Y box-binding protein YB-1 in cellular sensitivity to the DNA-damaging agents cisplatin, mitomycin C, and ultraviolet light. Cancer Res 56:4224–8PubMedGoogle Scholar
  19. 19.
    Yasunaga M, Ohishi Y, Oda Y et al (2009) Immunohistochemical characterization of mullerian mucinous borderline tumors: possible histogenetic link with serous borderline tumors and low-grade endometrioid tumors. Hum Pathol 40:965–74PubMedCrossRefGoogle Scholar
  20. 20.
    Basaki Y, Hosoi F, Oda Y et al (2007) Akt-dependent nuclear localization of Y-box-binding protein 1 in acquisition of malignant characteristics by human ovarian cancer cells. Oncogene 26:2736–46PubMedCrossRefGoogle Scholar
  21. 21.
    Yang XJ, Tan MH, Kim HL et al (2005) A molecular classification of papillary renal cell carcinoma. Cancer Res 65:5628–37Google Scholar
  22. 22.
    Yoshida M, Yao M, Ishikawa I et al (2002) Somatic von Hippel–Lindau disease gene mutation in clear-cell renal carcinomas associated with end-stage renal disease/acquired cystic disease of the kidney. Genes Chromosomes Cancer 35:359–364PubMedCrossRefGoogle Scholar
  23. 23.
    Nouh MA, Kuroda N, Yamashita M et al (2010) Renal cell carcinoma in patients with end-stage renal disease: relationship between histological type and duration of dialysis. BJU Int 105:620–7PubMedCrossRefGoogle Scholar
  24. 24.
    Oda Y, Kohashi K, Yamamoto H et al (2008) Different expression profiles of Y-box-binding protein-1 and multidrug resistance-associated proteins between alveolar and embryonal rhabdomyosarcoma. Cancer Sci 99:726–32PubMedCrossRefGoogle Scholar
  25. 25.
    Choyke PL (2000) Acquired cystic kidney disease. Eur Radiol 10:1716–1721PubMedCrossRefGoogle Scholar
  26. 26.
    Fuhrman SA, Lasky LC, Limas C (1982) Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol 6:655–63PubMedCrossRefGoogle Scholar
  27. 27.
    Carducci MA, Piantadosi S, Pound CR et al (1999) Nuclear morphometry adds significant prognostic information to stage and grade for renal cell carcinoma. Urology 53:44–9PubMedCrossRefGoogle Scholar
  28. 28.
    Kropotov A, Gogvadze V, Shupliakov O et al (2006) Peroxiredoxin V is essential for protection against apoptosis in human lung carcinoma cells. Exp Cell Res 312:2806–2815PubMedCrossRefGoogle Scholar
  29. 29.
    Karihtala P, Mäntyniemi A, Kang SW, Kinnula VL, Soini Y (2003) Peroxiredoxins in breast carcinoma. Clin Cancer Res 9:3418–24PubMedGoogle Scholar
  30. 30.
    Zhang B, Wang Y, Su Y (2009) Peroxiredoxins, a novel target in cancer radiotherapy. Cancer Lett 286:154–60PubMedCrossRefGoogle Scholar
  31. 31.
    Tickoo SK, dePeralta-Venturina MN, Harik LR et al (2006) Spectrum of epithelial neoplasm in end stage renal disease: an experience from 66 tumor bearing kidneys with emphasis on histologic patterns distinct from those in sporadic adult renal neoplasia. Am J Surg Pathol 30:141–153PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Fumiyoshi Fushimi
    • 1
  • Kenichi Taguchi
    • 2
  • Hiroto Izumi
    • 3
  • Kimitoshi Kohno
    • 3
  • Michihiko Kuwano
    • 4
  • Mayumi Ono
    • 4
  • Yutaka Nakashima
    • 5
  • Tetsuro Takesue
    • 6
  • Seiji Naito
    • 7
  • Yoshinao Oda
    • 1
    Email author
  1. 1.Department of Anatomic Pathology, Graduate School of Medical SciencesKyushu UniversityHigashi-kuJapan
  2. 2.Department of PathologyNational Kyushu Cancer CenterMinami-kuJapan
  3. 3.Department of Molecular BiologyUniversity of Occupational and Environmental HealthKitakyushuJapan
  4. 4.Department of Pharmaceutical Oncology and Laboratory of Molecular Cancer Biology, Graduate School of Pharmaceutical SciencesKyushu UniversityHigashi-kuJapan
  5. 5.Department of PathologyFukuoka Red Cross HospitalMinami-kuJapan
  6. 6.Department of UrologyFukuoka Red Cross HospitalMinami-kuJapan
  7. 7.Department of Urology, Graduate School of Medical SciencesKyushu UniversityHigashi-kuJapan

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