Downregulation of OCLN and GAS1 in clear cell renal cell carcinoma
- Authors:
- André Luis Giacometti Conceição
- Camila Tainah Da Silva
- Rodolfo Miglioli Badial
- Marina Curado Valsechi
- Bruna Stuqui
- Jéssica Domingues Gonçalves
- Miriam Galvonas Jasiulionis
- Marilia De Freitas Calmon
- Paula Rahal
-
Affiliations: Laboratory of Genomic Studies, Department of Biology, São Paulo State University (UNESP), São José do Rio Preto, SP 15054-000, Brazil, Department of Pharmacology, The Federal University of São Paulo (UNIFESP), São Paulo, SP 15054-000, Brazil - Published online on: January 31, 2017 https://doi.org/10.3892/or.2017.5414
- Pages: 1487-1496
This article is mentioned in:
Abstract
Shuch B, Amin A, Armstrong AJ, Eble JN, Ficarra V, Lopez-Beltran A, Martignoni G, Rini BI and Kutikov A: Understanding pathologic variants of renal cell carcinoma: Distilling therapeutic opportunities from biologic complexity. Eur Urol. 67:85–97. 2015. View Article : Google Scholar : PubMed/NCBI | |
Cohen HT and McGovern FJ: Renal-cell carcinoma. N Engl J Med. 353:2477–2490. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kuroda N, Hosokawa T, Michal M, Hes O, Sima R, Ohe C and Lee GH: Clear cell renal cell carcinoma with focal renal angiomyoadenomatous tumor-like area. Ann Diagn Pathol. 15:202–206. 2011. View Article : Google Scholar : PubMed/NCBI | |
Nagata M, Sakurai-Yageta M, Yamada D, Goto A, Ito A, Fukuhara H, Kume H, Morikawa T, Fukayama M, Homma Y, et al: Aberrations of a cell adhesion molecule CADM4 in renal clear cell carcinoma. Int J Cancer. 130:1329–1337. 2012. View Article : Google Scholar : PubMed/NCBI | |
Baylin SB: DNA methylation and gene silencing in cancer. Nat Clin Pract Oncol. 2 Suppl 1:S4–S11. 2005. View Article : Google Scholar : PubMed/NCBI | |
Tang J and Zhuang S: Epigenetics in acute kidney injury. Curr Opin Nephrol Hypertens. 24:351–358. 2015.PubMed/NCBI | |
Baylin SB and Ohm JE: Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat Rev Cancer. 6:107–116. 2006. View Article : Google Scholar : PubMed/NCBI | |
Feinberg AP and Tycko B: The history of cancer epigenetics. Nat Rev Cancer. 4:143–153. 2004. View Article : Google Scholar : PubMed/NCBI | |
Benard A, Goossens-Beumer IJ, van Hoesel AQ, De Graaf W, Horati H, Putter H, Zeestraten EC, van de Velde CJ and Kuppen PJ: Histone trimethylation at H3K4, H3K9 and H4K20 correlates with patient survival and tumor recurrence in early-stage colon cancer. BMC Cancer. 14:5312014. View Article : Google Scholar : PubMed/NCBI | |
Khakpour G, Pooladi A, Izadi P, Noruzinia M and Bazzaz J Tavakkoly: DNA methylation as a promising landscape: A simple blood test for breast cancer prediction. Tumour Biol. 36:4905–4912. 2015. View Article : Google Scholar : PubMed/NCBI | |
Li J and Mansmann UR: A microRNA molecular modeling extension for prediction of colorectal cancer treatment. BMC Cancer. 15:4722015. View Article : Google Scholar : PubMed/NCBI | |
De Wever O, Pauwels P, De Craene B, Sabbah M, Emami S, Redeuilh G, Gespach C, Bracke M and Berx G: Molecular and pathological signatures of epithelial-mesenchymal transitions at the cancer invasion front. Histochem Cell Biol. 130:481–494. 2008. View Article : Google Scholar : PubMed/NCBI | |
Pierucci-Alves F, Yi S and Schultz BD: Transforming growth factor beta 1 induces tight junction disruptions and loss of transepithelial resistance across porcine vas deferens epithelial cells. Biol Reprod. 86:362012. View Article : Google Scholar : PubMed/NCBI | |
Katoh Y and Katoh M: Hedgehog signaling, epithelial-to-mesenchymal transition and miRNA (Review). Int J Mol Med. 22:271–275. 2008.PubMed/NCBI | |
Kunkel M, Reichert TE, Benz P, Lehr HA, Jeong JH, Wieand S, Bartenstein P, Wagner W and Whiteside TL: Overexpression of Glut-1 and increased glucose metabolism in tumors are associated with a poor prognosis in patients with oral squamous cell carcinoma. Cancer. 97:1015–1024. 2003. View Article : Google Scholar : PubMed/NCBI | |
Sun L, Zeng X, Yan C, Sun X, Gong X, Rao Y and Yan N: Crystal structure of a bacterial homologue of glucose transporters GLUT1-4. Nature. 490:361–366. 2012. View Article : Google Scholar : PubMed/NCBI | |
Sasaki H, Shitara M, Yokota K, Hikosaka Y, Moriyama S, Yano M and Fujii Y: Overexpression of GLUT1 correlates with Kras mutations in lung carcinomas. Mol Med Rep. 5:599–602. 2012.PubMed/NCBI | |
Li W, Wei Z, Liu Y, Li H, Ren R and Tang Y: Increased 18F-FDG uptake and expression of Glut1 in the EMT transformed breast cancer cells induced by TGF-beta. Neoplasma. 57:234–240. 2010. View Article : Google Scholar : PubMed/NCBI | |
Fisseler-Eckhoff A: New TNM classification of malignant lung tumors 2009 from a pathology perspective. Pathologe. 30 Suppl 2:S193–S199. 2009.(In German). View Article : Google Scholar | |
Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e452001. View Article : Google Scholar : PubMed/NCBI | |
Calmon MF, Colombo J, Carvalho F, Souza FP, Filho JF, Fukuyama EE, Camargo AA, Caballero OL, Tajara EH, Cordeiro JA, et al: Methylation profile of genes CDKN2Ap14 and p16), DAPK1CDH1, and ADAM23 in head and neck cancer. Cancer Genet Cytogenet. 173:31–37. 2007. View Article : Google Scholar : PubMed/NCBI | |
Nguyen CT, Weisenberger DJ, Velicescu M, Gonzales FA, Lin JC, Liang G and Jones PA: Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-aza-2′-deoxycytidine. Cancer Res. 62:6456–6461. 2002.PubMed/NCBI | |
Zigeuner R, Hutterer G, Chromecki T, Imamovic A, Kampel-Kettner K, Rehak P, Langner C and Pummer K: External validation of the Mayo Clinic stage, size, grade, and necrosis (SSIGN) score for clear-cell renal cell carcinoma in a single European centre applying routine pathology. Eur Urol. 57:102–109. 2010. View Article : Google Scholar : PubMed/NCBI | |
Gulati S, Martinez P, Joshi T, Birkbak NJ, Santos CR, Rowan AJ, Pickering L, Gore M, Larkin J, Szallasi Z, et al: Systematic evaluation of the prognostic impact and intratumour heterogeneity of clear cell renal cell carcinoma biomarkers. Eur Urol. 66:936–948. 2014. View Article : Google Scholar : PubMed/NCBI | |
Fisel P, Kruck S, Winter S, Bedke J, Hennenlotter J, Nies AT, Scharpf M, Fend F, Stenzl A, Schwab M, et al: DNA methylation of the SLC16A3 promoter regulates expression of the human lactate transporter MCT4 in renal cancer with consequences for clinical outcome. Clin Cancer Res. 19:5170–5181. 2013. View Article : Google Scholar : PubMed/NCBI | |
Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S and Tsukita S and Tsukita S: Occludin: A novel integral membrane protein localizing at tight junctions. J Cell Biol. 123:1777–1788. 1993. View Article : Google Scholar : PubMed/NCBI | |
Balda MS, Whitney JA, Flores C, González S, Cereijido M and Matter K: Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol. 134:1031–1049. 1996. View Article : Google Scholar : PubMed/NCBI | |
Balda MS, Flores-Maldonado C, Cereijido M and Matter K: Multiple domains of occludin are involved in the regulation of paracellular permeability. J Cell Biochem. 78:85–96. 2000. View Article : Google Scholar : PubMed/NCBI | |
Tsukita S, Furuse M and Itoh M: Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol. 2:285–293. 2001. View Article : Google Scholar : PubMed/NCBI | |
Farquhar MG and Palade GE: Junctional complexes in various epithelia. J Cell Biol. 17:375–412. 1963. View Article : Google Scholar : PubMed/NCBI | |
Thiery JP and Sleeman JP: Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol. 7:131–142. 2006. View Article : Google Scholar : PubMed/NCBI | |
Orbán E, Szabó E, Lotz G, Kupcsulik P, Páska C, Schaff Z and Kiss A: Different expression of occludin and ZO-1 in primary and metastatic liver tumors. Pathol Oncol Res. 14:299–306. 2008. View Article : Google Scholar : PubMed/NCBI | |
Martin TA, Mansel RE and Jiang WG: Loss of occludin leads to the progression of human breast cancer. Int J Mol Med. 26:723–734. 2010. View Article : Google Scholar : PubMed/NCBI | |
Tobioka H, Isomura H, Kokai Y, Tokunaga Y, Yamaguchi J and Sawada N: Occludin expression decreases with the progression of human endometrial carcinoma. Hum Pathol. 35:159–164. 2004. View Article : Google Scholar : PubMed/NCBI | |
Tobioka H, Tokunaga Y, Isomura H, Kokai Y, Yamaguchi J and Sawada N: Expression of occludin, a tight-junction-associated protein, in human lung carcinomas. Virchows Arch. 445:472–476. 2004. View Article : Google Scholar : PubMed/NCBI | |
Rachow S, Zorn-Kruppa M, Ohnemus U, Kirschner N, Vidal-y-Sy S, von den Driesch P, Börnchen C, Eberle J, Mildner M, Vettorazzi E, et al: Occludin is involved in adhesion, apoptosis, differentiation and Ca2+-homeostasis of human keratinocytes: Implications for tumorigenesis. PLoS One. 8:e551162013. View Article : Google Scholar : PubMed/NCBI | |
Osanai M, Murata M, Nishikiori N, Chiba H, Kojima T and Sawada N: Epigenetic silencing of occludin promotes tumorigenic and metastatic properties of cancer cells via modulations of unique sets of apoptosis-associated genes. Cancer Res. 66:9125–9133. 2006. View Article : Google Scholar : PubMed/NCBI | |
Ellinger J, Kahl P, Mertens C, Rogenhofer S, Hauser S, Hartmann W, Bastian PJ, Büttner R, Müller SC and von Ruecker A: Prognostic relevance of global histone H3 lysine 4 (H3K4) methylation in renal cell carcinoma. Int J Cancer. 127:2360–2366. 2010. View Article : Google Scholar : PubMed/NCBI | |
Ye D, Guo S, Al-Sadi R and Ma TY: MicroRNA regulation of intestinal epithelial tight junction permeability. Gastroenterology. 141:1323–1333. 2011. View Article : Google Scholar : PubMed/NCBI | |
Munari E, Marchionni L, Chitre A, Hayashi M, Martignoni G, Brunelli M, Gobbo S, Argani P, Allaf M, Hoque MO, et al: Clear cell papillary renal cell carcinoma: micro-RNA expression profiling and comparison with clear cell renal cell carcinoma and papillary renal cell carcinoma. Hum Pathol. 45:1130–1138. 2014. View Article : Google Scholar : PubMed/NCBI | |
White NM, Bao TT, Grigull J, Youssef YM, Girgis A, Diamandis M, Fatoohi E, Metias M, Honey RJ, Stewart R, et al: miRNA profiling for clear cell renal cell carcinoma: Biomarker discovery and identification of potential controls and consequences of miRNA dysregulation. J Urol. 186:1077–1083. 2011. View Article : Google Scholar : PubMed/NCBI | |
Zhou L, Chen J, Li Z, Li X, Hu X, Huang Y, Zhao X, Liang C, Wang Y, Sun L, et al: Integrated profiling of microRNAs and mRNAs: microRNAs located on Xq27.3 associate with clear cell renal cell carcinoma. PLoS One. 5:e152242010. View Article : Google Scholar : PubMed/NCBI | |
Fong MY, Zhou W, Liu L, Alontaga AY, Chandra M, Ashby J, Chow A, O'Connor ST, Li S, Chin AR, et al: Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat Cell Biol. 17:183–194. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ruaro ME, Stebel M, Vatta P, Marzinotto S and Schneider C: Analysis of the domain requirement in Gas1 growth suppressing activity. FEBS Lett. 481:159–163. 2000. View Article : Google Scholar : PubMed/NCBI | |
Stebel M, Vatta P, Ruaro ME, Del Sal G, Parton RG and Schneider C: The growth suppressing gas1 product is a GPI-linked protein. FEBS Lett. 481:152–158. 2000. View Article : Google Scholar : PubMed/NCBI | |
Del Sal G, Ruaro ME, Philipson L and Schneider C: The growth arrest-specific gene, gas1, is involved in growth suppression. Cell. 70:595–607. 1992. View Article : Google Scholar : PubMed/NCBI | |
Beachy PA, Karhadkar SS and Berman DM: Tissue repair and stem cell renewal in carcinogenesis. Nature. 432:324–331. 2004. View Article : Google Scholar : PubMed/NCBI | |
Allen BL, Tenzen T and McMahon AP: The Hedgehog-binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev. 21:1244–1257. 2007. View Article : Google Scholar : PubMed/NCBI | |
Wang H, Zhou X, Zhang Y, Zhu H, Zhao L, Fan L, Wang Y, Gang Y, Wu K, Liu Z, et al: Growth arrest-specific gene 1 is downregulated and inhibits tumor growth in gastric cancer. FEBS J. 279:3652–3664. 2012. View Article : Google Scholar : PubMed/NCBI | |
Jiang Z, Xu Y and Cai S: Down-regulated GAS1 expression correlates with recurrence in stage II and III colorectal cancer. Hum Pathol. 42:361–368. 2011. View Article : Google Scholar : PubMed/NCBI | |
Gobeil S, Zhu X, Doillon CJ and Green MR: A genome-wide shRNA screen identifies GAS1 as a novel melanoma metastasis suppressor gene. Genes Dev. 22:2932–2940. 2008. View Article : Google Scholar : PubMed/NCBI | |
Scaltriti M, Brausi M, Amorosi A, Caporali A, DArca D, Astancolle S, Corti A and Bettuzzi S: Clusterin (SGP-2, ApoJ) expression is downregulated in low- and high-grade human prostate cancer. Int J Cancer. 108:23–30. 2004. View Article : Google Scholar : PubMed/NCBI | |
Sacilotto N, Espert A, Castillo J, Franco L and López-Rodas G: Epigenetic transcriptional regulation of the growth arrest-specific gene 1Gas1) in hepatic cell proliferation at mononucleosomal resolution. PLoS One. 6:e233182011. View Article : Google Scholar : PubMed/NCBI | |
Ma Y, Qin H and Cui Y: MiR-34a targets GAS1 to promote cell proliferation and inhibit apoptosis in papillary thyroid carcinoma via PI3K/Akt/Bad pathway. Biochem Biophys Res Commun. 441:958–963. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhang L, He S, Guo S, Xie W, Xin R, Yu H, Yang F, Qiu J, Zhang D, Zhou S, et al: Down-regulation of miR-34a alleviates mesangial proliferation in vitro and glomerular hypertrophy in early diabetic nephropathy mice by targeting GAS1. J Diabetes Complications. 28:259–264. 2014. View Article : Google Scholar : PubMed/NCBI | |
Liu H, Brannon AR, Reddy AR, Alexe G, Seiler MW, Arreola A, Oza JH, Yao M, Juan D, Liou LS, et al: Identifying mRNA targets of microRNA dysregulated in cancer: With application to clear cell renal cell carcinoma. BMC Syst Biol. 4:512010. View Article : Google Scholar : PubMed/NCBI | |
Yu G, Li H, Wang J, Gumireddy K, Li A, Yao W, Tang K, Xiao W, Hu J, Xiao H, et al: miRNA-34a suppresses cell proliferation and metastasis by targeting CD44 in human renal carcinoma cells. J Urol. 192:1229–1237. 2014. View Article : Google Scholar : PubMed/NCBI | |
Dutta KK, Zhong Y, Liu YT, Yamada T, Akatsuka S, Hu Q, Yoshihara M, Ohara H, Takehashi M, Shinohara T, et al: Association of microRNA-34a overexpression with proliferation is cell type-dependent. Cancer Sci. 98:1845–1852. 2007. View Article : Google Scholar : PubMed/NCBI | |
Yan S, Wang Y, Chen M, Li G and Fan J: Deregulated SLC2A1 promotes tumor cell proliferation and metastasis in gastric cancer. Int J Mol Sci. 16:16144–16157. 2015. View Article : Google Scholar : PubMed/NCBI | |
Amann T, Maegdefrau U, Hartmann A, Agaimy A, Marienhagen J, Weiss TS, Stoeltzing O, Warnecke C, Schölmerich J, Oefner PJ, et al: GLUT1 expression is increased in hepatocellular carcinoma and promotes tumorigenesis. Am J Pathol. 174:1544–1552. 2009. View Article : Google Scholar : PubMed/NCBI | |
Krzeslak A, Wojcik-Krowiranda K, Forma E, Jozwiak P, Romanowicz H, Bienkiewicz A and Brys M: Expression of GLUT1 and GLUT3 glucose transporters in endometrial and breast cancers. Pathol Oncol Res. 18:721–728. 2012. View Article : Google Scholar : PubMed/NCBI | |
Manel N, Kim FJ, Kinet S, Taylor N, Sitbon M and Battini JL: The ubiquitous glucose transporter GLUT-1 is a receptor for HTLV. Cell. 115:449–459. 2003. View Article : Google Scholar : PubMed/NCBI | |
Augustin R: The protein family of glucose transport facilitators: It's not only about glucose after all. IUBMB Life. 62:315–333. 2010.PubMed/NCBI | |
Cifuentes M, García MA, Arrabal PM, Martínez F, Yañez MJ, Jara N, Weil B, Domínguez D, Medina RA and Nualart F: Insulin regulates GLUT1-mediated glucose transport in MG-63 human osteosarcoma cells. J Cell Physiol. 226:1425–1432. 2011. View Article : Google Scholar : PubMed/NCBI | |
Vermeulen JF, van Brussel AS, van der Groep P, Morsink FH, Bult P, van der Wall E and van Diest PJ: Immunophenotyping invasive breast cancer: Paving the road for molecular imaging. BMC Cancer. 12:2402012. View Article : Google Scholar : PubMed/NCBI | |
Vermeulen JF, van der Wall E, Witkamp AJ and van Diest PJ: Analysis of expression of membrane-bound tumor markers in ductal carcinoma in situ of the breast: Paving the way for molecular imaging. Cell Oncol. 36:333–340. 2013. View Article : Google Scholar |