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Original Article

Lipocalin 2 attenuates iron-related oxidative stress and prolongs the survival of ovarian clear cell carcinoma cells by up-regulating the CD44 variant

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Pages 414-425 | Received 23 Jul 2015, Accepted 15 Dec 2015, Published online: 12 Feb 2016

References

  • Flo TH, Smith KD, Sato S, Rodriquez DJ, Holmes MA, Strong RK, et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004;432:917–921.
  • Devireddy LR, Gazin C, Zhu X, Green MR. A cell-surface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell 2005;123:1293–1305.
  • Hvidberg V, Jacobsen C, Strong RK, Cowland JB, Moestrup SK, Borregaard N. The endocytic receptor megalin binds the iron transporting neutrophil-gelatinase-associated lipocalin with high affinity and mediates its cellular uptake. FEBS Lett 2005;579:773–777.
  • Roudkenar MH, Halabian R, Ghasemipour Z, Roushandeh AM, Rouhbakhsh M, Nekogoftar M, et al. Neutrophil gelatinase-associated lipocalin acts as a protective factor against H(2)O(2) toxicity. Arch Med Res 2008;39:560–566.
  • Bahmani P, Halabian R, Rouhbakhsh M, Roushandeh AM, Masroori N, Ebrahimi M, et al. Neutrophil gelatinase-associated lipocalin induces the expression of heme oxygenase-1 and superoxide dismutase 1, 2. Cell Stress Chaperones 2010;15:395–403.
  • Roudkenar MH, Halabian R, Bahmani P, Roushandeh AM, Kuwahara Y, Fukumoto M. Neutrophil gelatinase-associated lipocalin: a new antioxidant that exerts its cytoprotective effect independent on heme oxygenase-1. Free Radic Res 2011;45:810–819.
  • Halabian R, Tehrani HA, Jahanian-Najafabadi A, Roudkenar MH. Lipocalin-2-mediated upregulation of various antioxidants and growth factors protects bone marrow-derived mesenchymal stem cells against unfavorable microenvironments. Cell Stress Chaperones 2013;18:785–800.
  • Catalan V, Gomez-Ambrosi J, Rodriguez A, Ramirez B, Silva C, Rotellar F, et al. Increased adipose tissue expression of lipocalin-2 in obesity is related to inflammation and matrix metalloproteinase-2 and metalloproteinase-9 activities in humans. J Mol Med 2009;87:803–813.
  • Sahinarsian A, Kocaman SA, Bas D, Akyel A, Ercin U, Zengin O, Timurkaynak T. Plasma neutrophil gelatinase-associated lipocalin levels in acute myocardial infarction and stable coronary artery disease. Coron Artery Dis 2011;22:333–338.
  • Viau A, El Karoui K, Laouari D, Burtin M, Nguyen C, Mori K, et al. Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 2010;120:4065–4076.
  • Bauer M, Eickhoff JC, Gould MN, Mundhenke C, Maass N, Friedl A. Neutrophil gelatinase-associated lipocalin (NGAL) is a predictor of poor prognosis in human primary breast cancer. Breast Cancer Res Treat 2008;108:389–397.
  • Leng X, Ding T, Lin H, Wang Y, Hu L, Hu J, et al. Inhibition of lipocalin 2 impairs breast tumorigenesis and metastasis. Cancer Res 2009;69:8579–8584.
  • Barresi V, Reggiani-Bonetti L, Di Gregorio C, Vitarelli E, Ponz De Leon M, Barresi G. Neutrophil gelatinase-associated lipocalin (NGAL) and matrix metalloproteinase-9 (MMP-9) prognostic value in stage I colorectal carcinoma. Pathol Res Pract 2011;207:479–486.
  • Wang HJ, He XJ, Ma YY, Jiang XT, Xia YJ, Ye ZY, et al. Expressions of neutrophil gelatinase-associated lipocalin in gastric cancer: a potential biomarker for prognosis and an ancillary diagnostic test. Anat Rec (Hoboken) 2010;293:1855–1863.
  • Tong Z, Kunnumakkara AB, Wang H, Matsuo Y, Diagaradjane P, Harikumar KB, et al. Neutrophil gelatinase-associated lipocalin: a novel suppressor of invasion and angiogenesis in pancreatic cancer. Cancer Res 2008;68:6100–6108.
  • Miyamoto T, Kashima H, Suzuki A, Kikuchi N, Konishi I, Seki N, Shiozawa T. Laser-captured microdissection-microarray analysis of the genes involved in endometrial carcinogenesis: stepwise up-regulation of lipocalin2 expression in normal and neoplastic endometria and its functional relevance. Hum Pathol 2011;42:1265–1274.
  • Miyamoto T, Asaka R, Suzuki A, Takatsu A, Kashima H, Shiozawa T. Immunohistochemical detection of a specific receptor for lipocalin2 (solute carrier family 22 member 17, SLC22A17) and its prognostic significance in endometrial carcinoma. Exp Mol Pathol 2011;91:563–568.
  • Toyokuni S. Role of iron in carcinogenesis: cancer as a ferrotoxic disease. Cancer Sci 2009;100:9–16.
  • Bradbear RA, Bain C, Siskind V, Schofield FD, Webb S, Axelsen EM, et al. Cohort study of internal malignancy in genetic hemochromatosis and other chronic nonalcoholic liver diseases. J Natl Cancer Inst 1985;75:81–84.
  • Kobayashi H, Sumimoto K, Moniwa N, Imai M, Takakura K, Kuromaki T, et al. Risk of developing ovarian cancer among women with ovarian endometrioma: a cohort study in Shizuoka, Japan. Int J Gynecol Cancer 2007;17:37–43.
  • Yamaguchi K, Mandai M, Toyokuni S, Hamanishi J, Higuchi T, Takakura K, Fujii S. Contents of endometriotic cysts, especially the high concentration of free iron, are a possible cause of carcinogenesis in the cysts through the iron-induced persistent oxidative stress. Clin Cancer Res 2008;14:32–40.
  • Axelsson L, Bergenfeldt M, Ohlsson K. Studies of the release and turnover of a human neutrophil lipocalin. Scand J Clin Lab Invest 1995;55:577–588.
  • Kobara H, Miyamoto T, Suzuki A, Asaka R, Yamada Y, Ishikawa K, et al. Lipocalin2 enhances the matrix metalloproteinase-9 activity and invasion of extravillous trophoblasts under hypoxia. Placenta 2013;34:1036–1043.
  • Lau WM, Teng E, Chong HS, Lopez KA, Tay AY, Salto-Tellez M, et al. CD44v8-10 is a cancer-specific marker for gastric cancer stem cells. Cancer Res 2014;74:2630–2641.
  • Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 2011;19:387–400.
  • Cho H, Kim JH. Lipocalin2 expressions correlate significantly with tumor differentiation in epithelial ovarian cancer. J Histochem Cytochem 2009;57:513–521.
  • Kikuchi N, Horiuchi A, Osada R, Imai T, Wang C, Chen X, Konishi I. Nuclear expression of S100A4 is associated with aggressive behavior of epithelial ovarian carcinoma: an important autocrine/paracrine factor in tumor progression. Cancer Sci 2006;97:1061–1069.
  • Ishiyama M, Tominaga H, Shiga M, Sasamoto K, Ohkura Y, Ueno K. A combined assay of cell viability and in vitro cytotoxicity with a highly water-soluble tetrazolium salt, neutral red and crystal violet. Bio Pharm Bull 1996;11:1518–1520.
  • Brewer CJ, Wood RI, Wood JC. mRNA regulation of cardiac iron transporters and ferritin subunits in a mouse model of iron overload. Exp Hematol 2014;42:1059–1067.
  • Mandai M, Matsumura N, Baba T, Yamaguchi K, Hamanishi J, Konishi I. Ovarian clear cell carcinoma as a stress-responsive cancer: influence of the microenvironment on the carcinogenesis and cancer phenotype. Cancer Lett 2011;310:129–133.
  • Heath JL, Weiss JM, Lavau CP, Wechsler DS. Iron deprivation in cancer-potential therapeutic implications. Nutrients 2013;5:2836–2859.
  • Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 2009;8:579–591.
  • Roudkenar MH, Kuwahara Y, Baba T, Roushandeh AM, Ebishima S, Abe S, et al. Oxidative stress induced lipocalin 2 gene expression: addressing its expression under the harmful conditions. J Radiat Res 2007;48:39–44.
  • Mahadevan MR, Rodvold J, Almanza G, Perez AF, Wheeler MC, Zanetti M. ER stress drives lipocalin 2 upregulation in prostate cancer cells in an NF-κB-dependent manner. BMC Cancer 2011;11:229.
  • Kumandan S, Mahadevan NR, Chiu K, DeLaney A, Zanetti M. Activation of the unfolded protein response bypasses trastuzumab-mediated inhibition of the PI-3K pathway. Cancer Lett 2013;329:236–242.
  • Roudkenar MH, Halabian R, Roushandeh AM, Nourani MR, Masroori N, Ebrahimi M, et al. Lipocalin 2 regulation by thermal stresses: protective role of Lcn2/NGAL against cold and heat stresses. Exp Cell Res 2009;315:3140–3151.
  • Wu G, Fang YZ, Yang S, Lupton JR, Turner ND. Glutathione metabolism and its implications for health. J Nutr 2004;134:489–492.
  • Tanner B, Hengstler JG, Dietrich B, Henrich M, Steinberg P, Weikel W, et al. Glutathione, glutathione S-transferase alpha and pi, and aldehyde dehydrogenase content in relationship to drug resistance in ovarian cancer. Gynecol Oncol 1997;65:54–62.
  • Williams K, Motiani K, Giridhar PV, Kasper S. CD44 integrates signaling in normal stem cell, cancer stem cell and (pre)metastatic niches. Exp Biol Med (Maywood) 2013;238:324–338.
  • Fotiadis D, Kanai Y, Palacín M. The SLC3 and SLC7 families of amino acid transporters. Mol Aspects Med 2013;34:139–158.
  • Bannai S, Tateishi N. Role of membrane transport in metabolism and function of glutathione in mammals. J Membr Biol 1986;89:1–8.
  • Peng ST, Su CH, Kuo CC, Shaw CF, Wang HS. CD44 crosslinking-mediated matrix metalloproteinase-9 relocation in breast tumor cells leads to enhanced metastasis. Int J Oncol 2007;31:1119–1126.
  • Yan L, Borregaard N, Kjeldsen L, Moses MA. The high molecular weight urinary matrix metalloproteinase (MMP) activity is a complex of gelatinase B/MMP-9 and neutrophil gelatinase-associated lipocalin (NGAL). Modulation of MMP-9 activity by NGAL. J Biol Chem 2001;276:37258–37265.
  • Sakakura Y, Sato H, Shiiya A, Tamba M, Sagara J, Matsuda M, et al. Expression and function of cystine/glutamate transporter in neutrophils. J Leukoc Biol 2007;81:974–982.
  • Bao GH, Xu J, Hu FL, Wan XC, Deng SX, Barasch J. EGCG inhibit chemical reactivity of iron through forming an Ngal-EGCG-iron complex. Biometals 2013;26:1041–1050.
  • Lee YC, Tzeng WF, Chiou TJ, Chu ST. MicroRNA-138 suppresses neutrophil gelatinase-associated lipocalin expression and inhibits tumorigenicity. PLoS One 2012;7:e52979.

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