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Research Paper

Interactions between TGF-β type I receptor and hypoxia-inducible factor-α mediates a synergistic crosstalk leading to poor prognosis for patients with clear cell renal cell carcinoma

, , , & ORCID Icon
Pages 2141-2156 | Received 08 Mar 2019, Accepted 02 Jul 2019, Published online: 24 Jul 2019

References

  • Ferlay J, Colombet M, Soerjomataram I, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries and 25 major cancers in 2018. Eur J Cancer. 2018;103:356–387.
  • Kovacs G. Molecular genetics of human renal cell tumours. Nephrol Dial Transplant. 1996;11(Suppl 6):62–65.
  • Nelson EC, Evans CP, Lara PN Jr. Renal cell carcinoma: current status and emerging therapies. Cancer Treat Rev. 2007;33(3):299–313.
  • Kim WY, Kaelin WG. Role of VHL gene mutation in human cancer. J Clin Oncol. 2004;22(24):4991–5004.
  • Iwai K, Yamanaka K, Kamura T, et al. Identification of the von Hippel-lindau tumor-suppressor protein as part of an active E3 ubiquitin ligase complex. Proc Natl Acad Sci U S A. 1999;96(22):12436–12441.
  • Maxwell PH, Wiesener MS, Chang G-W, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature. 1999;399(6733):271–275.
  • Dengler VL, Galbraith M, Espinosa JM. Transcriptional regulation by hypoxia inducible factors. Crit Rev Biochem Mol Biol. 2014;49(1):1–15.
  • Hoskin PJ, Sibtain A, Daley FM, et al. GLUT1 and CAIX as intrinsic markers of hypoxia in bladder cancer: relationship with vascularity and proliferation as predictors of outcome of ARCON. Br J Cancer. 2003;89(7):1290–1297.
  • Tostain J, Li G, Gentil-Perret A, et al. Carbonic anhydrase 9 in clear cell renal cell carcinoma: a marker for diagnosis, prognosis and treatment. Eur J Cancer. 2010;46(18):3141–3148.
  • Ambrosetti D, Dufies M, Dadone B, et al. The two glycolytic markers GLUT1 and MCT1 correlate with tumor grade and survival in clear-cell renal cell carcinoma. PLoS One. 2018;13(2):e0193477.
  • Ananth S, Knebelmann B, Grüning W, et al. Transforming growth factor beta1 is a target for the von Hippel-Lindau tumor suppressor and a critical growth factor for clear cell renal carcinoma. Cancer Res. 1999;59(9):2210–2216.
  • Bostrom AK, Lindgren D, Johansson ME, et al. Effects of TGF-beta signaling in clear cell renal cell carcinoma cells. Biochem Biophys Res Commun. 2013;435(1):126–133.
  • Mallikarjuna P, Sitaram RT, Landström M, et al. VHL status regulates transforming growth factor-β signaling pathways in renal cell carcinoma. Oncotarget. 2018;9(23):16297–16310.
  • Massague J. TGF-beta signal transduction. Annu Rev Biochem. 1998;67:753–791.
  • David CJ, Massague J. Contextual determinants of TGFbeta action in development, immunity and cancer. Nat Rev Mol Cell Biol. 2018;19(7):419–435.
  • Massague J. TGFbeta in Cancer. Cell. 2008;134(2):215–230.
  • Massague J. TGFbeta signalling in context. Nat Rev Mol Cell Biol. 2012;13(10):616–630.
  • Mu Y, Gudey SK, Landstrom M. Non-Smad signaling pathways. Cell Tissue Res. 2012;347(1):11–20.
  • Derynck R, Budi EH. Specificity, versatility, and control of TGF-beta family signaling. Sci Signal. 2019 Feb 26;12(570). pii: eaav5183. doi:10.1126/scisignal.aav5183.
  • Dong C, Zhu S, Wang T, et al. Upregulation of PAI-1 is mediated through TGF-beta/Smad pathway in transplant arteriopathy. J Heart Lung Transplant. 2002;21(9):999–1008.
  • Mu Y, Sundar R, Thakur N, et al. TRAF6 ubiquitinates TGFβ type I receptor to promote its cleavage and nuclear translocation in cancer. Nat Commun. 2011;2:330.
  • Gudey SK, Sundar R, Mu Y, et al. TRAF6 stimulates the tumor-promoting effects of TGFbeta type I receptor through polyubiquitination and activation of presenilin 1. Sci Signal. 2014;7(307):ra2.
  • Song J, Mu Y, Li C, et al. APPL proteins promote TGFbeta-induced nuclear transport of the TGFbeta type I receptor intracellular domain. Oncotarget. 2016;7(1):279–292.
  • Sitaram RT, Mallikarjuna P, Landström M, et al. Transforming growth factor-beta promotes aggressiveness and invasion of clear cell renal cell carcinoma. Oncotarget. 2016;7(24):35917–35931.
  • Peinado H, Quintanilla M, Cano A. Transforming growth factor beta-1 induces snail transcription factor in epithelial cell lines: mechanisms for epithelial mesenchymal transitions. J Biol Chem. 2003;278(23):21113–21123.
  • Vincent T, Neve EPA, Johnson JR, et al. A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nat Cell Biol. 2009;11(8):943–950.
  • Thakur N, Gudey SK, Marcusson A, et al. TGFbeta-induced invasion of prostate cancer cells is promoted by c-Jun-dependent transcriptional activation of Snail1. Cell Cycle. 2014;13(15):2400–2414.
  • Gudey SK, Sundar R, Heldin C-H, et al. Pro-invasive properties of Snail1 are regulated by sumoylation in response to TGFbeta stimulation in cancer. Oncotarget. 2017;8(58):97703–97726.
  • Lundgren K, Nordenskjold B, Landberg G. Hypoxia, Snail and incomplete epithelial-mesenchymal transition in breast cancer. Br J Cancer. 2009;101(10):1769–1781.
  • Choi BJ, Park S-A, Lee S-Y, et al. Hypoxia induces epithelial-mesenchymal transition in colorectal cancer cells through ubiquitin-specific protease 47-mediated stabilization of Snail: A potential role of Sox9. Sci Rep. 2017;7(1):15918.
  • Xu X, Tan X, Tampe B, et al. Snail is a direct target of hypoxia-inducible factor 1alpha (HIF1alpha) in Hypoxia-induced endothelial to mesenchymal transition of human coronary endothelial cells. J Biol Chem. 2015;290(27):16653–16664.
  • Yoshino J, Monkawa T, Tsuji M, et al. Snail1 is involved in the renal epithelial-mesenchymal transition. Biochem Biophys Res Commun. 2007;362(1):63–68.
  • Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2014;15(3):178–196.
  • Guaita S, Puig I, Francı́ C, et al. Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression. J Biol Chem. 2002;277(42):39209–39216.
  • Furuta C, Miyamoto T, Takagi T, et al. Transforming growth factor-beta signaling enhancement by long-term exposure to hypoxia in a tumor microenvironment composed of Lewis lung carcinoma cells. Cancer Sci. 2015;106(11):1524–1533.
  • Zhang H, Akman HO, Smith ELP, et al. Cellular response to hypoxia involves signaling via Smad proteins. Blood. 2003;101(6):2253–2260.
  • McMahon S, Charbonneau M, Grandmont S, et al. Transforming growth factor beta1 induces hypoxia-inducible factor-1 stabilization through selective inhibition of PHD2 expression. J Biol Chem. 2006;281(34):24171–24181.
  • Matsuoka J, Yashiro M, Doi Y, et al. Hypoxia stimulates the EMT of gastric cancer cells through autocrine TGFbeta signaling. PLoS One. 2013;8(5):e62310.
  • Dunn LK, Mohammad KS, Fournier PGJ, et al. Hypoxia and TGF-beta drive breast cancer bone metastases through parallel signaling pathways in tumor cells and the bone microenvironment. PLoS One. 2009;4(9):e6896.
  • Copple BL. Hypoxia stimulates hepatocyte epithelial to mesenchymal transition by hypoxia-inducible factor and transforming growth factor-beta-dependent mechanisms. Liver Int. 2010;30(5):669–682.
  • Svenson U, Ljungberg B, Roos G. Telomere length in peripheral blood predicts survival in clear cell renal cell carcinoma. Cancer Res. 2009;69(7):2896–2901.
  • Kovacs G, Akhtar M, Beckwith BJ, et al. The Heidelberg classification of renal cell tumours. J Pathol. 1997;183(2):131–133.
  • Motzer RJ, Agarwal N, Beard C, et al. NCCN clinical practice guidelines in oncology: kidney cancer. J Natl Compr Canc Netw. 2009;7(6):618–630.
  • Fuhrman SA, Lasky LC, Limas C. Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol. 1982;6(7):655–663.
  • Nagy A, Lánczky A, Menyhárt O, et al. Validation of miRNA prognostic power in hepatocellular carcinoma using expression data of independent datasets. Sci Rep. 2018;8(1):9227.
  • Anaya J. OncoLnc: linking TCGA survival data to mRNAs, miRNAs, and lncRNAs. Peer J Comput Sci. 2016;2(e67).
  • Shinojima T, Oya M, Takayanagi A, et al. Renal cancer cells lacking hypoxia inducible factor (HIF)-1alpha expression maintain vascular endothelial growth factor expression through HIF-2alpha. Carcinogenesis. 2007;28(3):529–536.
  • Kucejova B, Peña-Llopis S, Yamasaki T, et al. Interplay between pVHL and mTORC1 pathways in clear-cell renal cell carcinoma. Mol Cancer Res. 2011;9(9):1255–1265.
  • Lai XM, Liu S-Y, Tsai Y-T, et al. HAF mediates the evasive resistance of anti-angiogenesis TKI through disrupting HIF-1α and HIF-2α balance in renal cell carcinoma. Oncotarget. 2017;8(30):49713–49724.
  • Hakimi AA, Chevinsky M, Hsieh JJ, et al. MP23-11 GENOMIC COMPARISON OF RENAL CELL CARCINOMA CELL LINES TO HUMAN TUMORS. J Urol. 2014;191(4S):e247.
  • Schmidt L, Junker K, Nakaigawa N, et al. Novel mutations of the MET proto-oncogene in papillary renal carcinomas. Oncogene. 1999;18(14):2343–2350.
  • Kovacs G, Fuzesi L, Emanual A, et al. Cytogenetics of papillary renal cell tumors. Genes Chromosomes Cancer. 1991;3(4):249–255.
  • Korhonen M, Sariola H, Gould VE, et al. Integrins and laminins in human renal carcinoma cells and tumors grown in nude mice. Cancer Res. 1994;54(16):4532–4538.
  • Furge KA, Dykema K, Petillo D, et al. Combining differential expression, chromosomal and pathway analyses for the molecular characterization of renal cell carcinoma. Can Urol Assoc J. 2007;1(2 Suppl):S21–7.
  • Robb VA, Karbowniczek M, Klein-Szanto AJ, et al. Activation of the mTOR signaling pathway in renal clear cell carcinoma. J Urol. 2007;177(1):346–352.
  • Campbell L, Al-Jayyoussi G, Gutteridge R, et al. Caveolin-1 in renal cell carcinoma promotes tumour cell invasion, and in co-operation with pERK predicts metastases in patients with clinically confined disease. J Transl Med. 2013;11:255.
  • Lovell M, Lott ST, Wong P, et al. The genetic locus NRC-1 within chromosome 3p12 mediates tumor suppression in renal cell carcinoma independently of histological type, tumor microenvironment, and VHL mutation. Cancer Res. 1999;59(9):2182–2189.
  • Siso-Nadal F, Fox JJ, Laporte SA, et al. Cross-talk between signaling pathways can generate robust oscillations in calcium and cAMP. PLoS One. 2009;4(10):e7189.
  • Klatte T, Seligson DB, Riggs SB, et al. Hypoxia-inducible factor 1 alpha in clear cell renal cell carcinoma. Clin Cancer Res. 2007;13(24):7388–7393.
  • Lidgren A, Hedberg Y, Grankvist K, et al. The expression of hypoxia-inducible factor 1alpha is a favorable independent prognostic factor in renal cell carcinoma. Clin Cancer Res. 2005;11(3):1129–1135.
  • Timar J, Szasz AM, Kardos M, et al. Expression of HIF1a and HIF2a in bone metastatic clear cell renal cell cancer and use as prognostic markers. J Clin Oncol. 2013;31(15_suppl):e15523–e15523.
  • Szendroi A, Szász AM, Kardos M, et al. Opposite prognostic roles of HIF1alpha and HIF2alpha expressions in bone metastatic clear cell renal cell cancer. Oncotarget. 2016;7(27):42086–42098.
  • Luo D, Liu H, Lin D, et al. The clinicopathologic and prognostic value of hypoxia-inducible factor-2alpha in cancer patients: a systematic review and meta-analysis. Cancer Epidemiol Biomarkers Prev. 2019;28(5):857–866.
  • Xiong Y, Liu L, Xia Y, et al. Tumor infiltrating mast cells determine oncogenic HIF-2alpha-conferred immune evasion in clear cell renal cell carcinoma. Cancer Immunol Immunother. 2019;68(5):731–741.
  • Fan Y, Sashittal SG, Chatzizacharias NA, et al. Prognostic significance of hypoxia-inducible factor expression in renal cell carcinoma: a PRISMA-compliant systematic review and meta-analysis. Medicine (Baltimore). 2015;94(38):e1646.
  • Hu Y, Liu J, Huang H. Recent agents targeting HIF-1alpha for cancer therapy. J Cell Biochem. 2013;114(3):498–509.
  • Martinez-Saez O, Borau PG, Alonso-Gordoa T, et al. Targeting HIF-2 alpha in clear cell renal cell carcinoma: A promising therapeutic strategy. Crit Rev Oncol Hematol. 2017;111:117–123.
  • Koh MY, Lemos R, Liu X, et al. The hypoxia-associated factor switches cells from HIF-1alpha- to HIF-2alpha-dependent signaling promoting stem cell characteristics, aggressive tumor growth and invasion. Cancer Res. 2011;71(11):4015–4027.
  • Uchida T, Rossignol F, Matthay MA, et al. Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression in lung epithelial cells: implication of natural antisense HIF-1alpha. J Biol Chem. 2004;279(15):14871–14878.
  • Cai J. Roles of transcriptional factor Snail and adhesion factor E-cadherin in clear cell renal cell carcinoma. Exp Ther Med. 2013;6(6):1489–1493.
  • Zaldumbide L, Erramuzpe A, Guarch R, et al. Snail heterogeneity in clear cell renal cell carcinoma. BMC Cancer. 2016;16:194.
  • Liu W, Liu Y, Liu H, et al. Snail predicts recurrence and survival of patients with localized clear cell renal cell carcinoma after surgical resection. Urol Oncol. 2015;33(2):69 e1–10.
  • Kushida N, Nomura S, Mimura I, et al. Hypoxia-inducible factor-1alpha activates the transforming growth factor-beta/SMAD3 pathway in kidney tubular epithelial cells. Am J Nephrol. 2016;44(4):276–285.
  • Wallace EM, Rizzi JP, Han G, et al. A small-molecule antagonist of HIF2alpha is efficacious in preclinical models of renal cell carcinoma. Cancer Res. 2016;76(18):5491–5500.
  • Feng W, Cui G, Tang C-W, et al. Role of glucose metabolism related gene GLUT1 in the occurrence and prognosis of colorectal cancer. Oncotarget. 2017;8(34):56850–56857.