Epithelial to Mesenchymal Transition in Renal Cell Carcinoma: Implications for Cancer Therapy

Molecular Diagnosis and Therapy

Volumn 20, Issue 2, 2016, Pages 111-117

  Piva, Francesco ^a   Giulietti, Matteo ^a   Santoni, Matteo ^a   Occhipinti, Giulia ^a   Scarpelli, Marina ^a   Lopez Beltran, Antonio ^b   Cheng, Liang ^c   Principato, Giovanni ^a   Montironi, Rodolfo ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSITY OF CÓRDOBA   (Spain)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; DCLK1 PROTEIN; INTEGRIN LINKED KINASE; MICRORNA; NATURAL PRODUCT; PROTEIN SERINE THREONINE KINASE; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG;

CANCER IMMUNOTHERAPY; CANCER PATIENT; CANCER THERAPY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; KIDNEY CARCINOMA; KIDNEY DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DEPLETION; REVIEW; SIGNAL TRANSDUCTION; CARCINOMA, RENAL CELL; DRUG EFFECTS; GENE EXPRESSION REGULATION; KIDNEY NEOPLASMS; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PROGNOSIS;

ANTINEOPLASTIC AGENTS; CARCINOMA, RENAL CELL; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KIDNEY NEOPLASMS; MOLECULAR TARGETED THERAPY; PROGNOSIS; SIGNAL TRANSDUCTION;

EID: 84960145229     PISSN: 11771062     EISSN: 11792000     Source Type: Journal    
DOI: 10.1007/s40291-016-0192-5     Document Type: Review

References (46)

1. Sandock DS, Seftel AD, Resnick MI. A new protocol for the follow up of renal cell carcinoma based on pathological stage. J Urol. 1995;154:28–31.
2. He H, Magi-Galluzzi C. Epithelial-to-mesenchymal transition in renal neoplasms. Adv Anat Pathol. 2014;21:174–80.
3. Weygant N, Qu D, May R, Tierney RM, Berry WL, Zhao L, et al. DCLK1 is a broadly dysregulated target against epithelial–mesenchymal transition, focal adhesion, and stemness in clear cell renal carcinoma. Oncotarget. 2015;6:2193–205.
4. Sampson VB, David JM, Puig I, Patil PU, de Herreros PU, Thomas GV, et al. Wilms’ tumor protein induces an epithelial–mesenchymal hybrid differentiation state in clear cell renal cell carcinoma. PLoS One. 2014;9:102041.
5. Pantuck AJ, An J, Liu H, Rettig MB. NF-kappaB-dependent plasticity of the epithelial to mesenchymal transition induced by Von Hippel–Lindau inactivation in renal cell carcinomas. Cancer Res. 2010;70:752–61.
6. Mahalingaiah PK, Ponnusamy L, Singh KP. Chronic oxidative stress leads to malignant transformation along with acquisition of stem cell characteristics, and epithelial to mesenchymal transition in human renal epithelial cells. J Cell Physiol. 2014;230:1916–28.
7. Huang J, Yao X, Zhang J, Dong B, Chen Q, Xue W, et al. Hypoxia-induced downregulation of miR-30c promotes epithelial–mesenchymal transition in human renal cell carcinoma. Cancer Sci. 2013;104:1609–17.
8. Yoshida N, Ikemoto S, Narita K, Sugimura K, Wada S, Yasumoto R, et al. Interleukin-6, tumour necrosis factor alpha and interleukin-1beta in patients with renal cell carcinoma. Br J Cancer. 2002;86:1396–400.
9. Harrison ML, Obermueller E, Maisey NR, Hoare S, Edmonds K, Li NF, et al. Tumor necrosis factor alpha as a new target for renal cell carcinoma: two sequential phase II trials of infliximab at standard and high dose. J Clin Oncol. 2007;25:4542–9.
10. Ho MY, Tang SJ, Chuang MJ, Cha TL, Li JY, Sun GH, et al. TNF-α induces epithelial–mesenchymal transition of renal cell carcinoma cells via a GSK3β-dependent mechanism. Mol Cancer Res. 2012;10:1109–19.
11. Khawam K, Giron-Michel J, Gu Y, Perier A, Giuliani M, Caignard A, et al. Human renal cancer cells express a novel membrane-bound interleukin-15 that induces, in response to the soluble interleukin-15 receptor alpha chain, epithelial-to-mesenchymal transition. Cancer Res. 2009;69:1561–9.
12. Yoshino H, Enokida H, Itesako T, Tatarano S, Kinoshita T, Fuse M, et al. Epithelial–mesenchymal transition-related microRNA-200s regulate molecular targets and pathways in renal cell carcinoma. J Hum Genet. 2013;58:508–16.
13. Ni D, Ma X, Li HZ, Gao Y, Li XT, Zhang Y, et al. Downregulation of FOXO3a promotes tumor metastasis and is associated with metastasis-free survival of patients with clear cell renal cell carcinoma. Clin Cancer Res. 2014;20:1779–90.
14. Gnemmi V, Bouillez A, Gaudelot K, Hémon B, Ringot B, Pottier N, et al. MUC1 drives epithelial–mesenchymal transition in renal carcinoma through Wnt/β-catenin pathway and interaction with SNAIL promoter. Cancer Lett. 2014;346:225–36.
15. Mikami S, Katsube K, Oya M, Ishida M, Kosaka T, Mizuno R, et al. Expression of Snail and Slug in renal cell carcinoma: E-cadherin repressor Snail is associated with cancer invasion and prognosis. Lab Invest. 2011;91:1443–58.
16. Conant JL, Peng Z, Evans MF, Naud S, Cooper K. Sarcomatoid renal cell carcinoma is an example of epithelial–mesenchymal transition. J Clin Pathol. 2011;64:1088–92.
17. Boström AK, Möller C, Nilsson E, Elfving P, Axelson H, Johansson ME. Sarcomatoid conversion of clear cell renal cell carcinoma in relation to epithelial-to-mesenchymal transition. Hum Pathol. 2012;43:708–19.
18. Dumanskiy YV, Kudriashov AG, Vasilenko IV, Kondratyuk RB, Gulkov YK, Cyrillichystiakov RS. Markers of epithelial–mesenchymal transition in renal cell carcinoma. Exp Oncol. 2013;35:325–7.
19. Harada K, Miyake H, Kusuda Y, Fujisawa M. Expression of epithelial–mesenchymal transition markers in renal cell carcinoma: impact on prognostic outcomes in patients undergoing radical nephrectomy. BJU Int. 2012;110:E1131–7.
20. Chen D, Gassenmaier M, Maruschke M, Riesenberg R, Pohla H, Stief CG, et al. Expression and prognostic significance of a comprehensive epithelial–mesenchymal transition gene set in renal cell carcinoma. J Urol. 2014;191:479–86.
21. Fang Y, Wei J, Cao J, Zhao H, Liao B, Qiu S, et al. Protein expression of ZEB2 in renal cell carcinoma and its prognostic significance in patient survival. PLoS One. 2013;8:e62558.
22. Iacovelli R, Alesini D, Palazzo A, Trenta P, Santoni M, De Marchis L, et al. Targeted therapies and complete responses in first line treatment of metastatic renal cell carcinoma. A meta-analysis of published trials. Cancer Treat Rev. 2014;40:271–5.
23. Santoni M, Massari F, Amantini C, Nabissi M, Maines F, Burattini L, et al. Emerging role of tumor-associated macrophages as therapeutic targets in patients with metastatic renal cell carcinoma. Cancer Immunol Immunother. 2013;62:1757–68.
24. Bielecka ZF, Czarnecka AM, Solarek W, Kornakiewicz A, Szczylik C. Mechanisms of acquired resistance to tyrosine kinase inhibitors in clear—cell renal cell carcinoma (ccRCC). Curr Signal Transduct Ther. 2014;8:218–28.
25. Hammers HJ, Verheul HM, Salumbides B, Sharma R, Rudek M, Jaspers J, et al. Reversible epithelial to mesenchymal transition and acquired resistance to sunitinib in patients with renal cell carcinoma: evidence from a xenograft study. Mol Cancer Ther. 2010;9:1525–35.
26. Satelli A, Li S. Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell Mol Life Sci. 2011;68:3033–46.
27. Aubert S, Fauquette V, Hémon B, Lepoivre R, Briez N, Bernard D, et al. MUC1, a new hypoxia inducible factor target gene, is an actor in clear renal cell carcinoma tumor progression. Cancer Res. 2009;69:5707–15.
28. Kondo K, Kohno N, Yokoyama A, Hiwada K. Decreased MUC1 expression induces E-cadherin-mediated cell adhesion of breast cancer cell lines. Cancer Res. 1998;58:2014–9.
29. Yuan Z, Wong S, Borrelli A, Chung MA. Down-regulation of MUC1 in cancer cells inhibits cell migration by promoting E-cadherin/catenin complex formation. Biochem Biophys Res Commun. 2007;362:740–6.
30. Liu X, Caffrey TC, Steele MM, Mohr A, Singh PK, Radhakrishnan P. MUC1 regulates cyclin D1 gene expression through p120 catenin and β-catenin. Oncogenesis. 2014;3:e107.
31. Rokavec M, Li H, Jiang L, Hermeking H. The p53/miR-34 axis in development and disease. J Mol Cell Biol. 2014;6:214–30.
32. Verschueren K, Remacle JE, Collart C, Kraft H, Baker BS, Tylzanowski P, et al. SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5′-CACCT sequences in candidate target genes. J Biol Chem. 1999;274:20489–98.
33. Postigo AA, Depp JL, Taylor JJ, Kroll KL. Regulation of Smad signaling through a differential recruitment of coactivators and corepressors by ZEB proteins. EMBO J. 2003;22:2453–62.
34. Zheng H, Shen M, Zha YL, Li W, Wei Y, Blanco MA, et al. PKD1 phosphorylation-dependent degradation of SNAIL by SCF-FBXO11 regulates epithelial–mesenchymal transition and metastasis. Cancer Cell. 2014;26:358–73.
35. Hannigan G, Troussard AA, Dedhar S. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat Rev Cancer. 2005;5:51–63.
36. Han KS, Li N, Raven PA, Fazli L, Ettinger S, Hong SJ, et al. Targeting integrin-linked kinase suppresses invasion and metastasis through downregulation of epithelial to mesenchymal transition in renal cell carcinoma. Mol Cancer Ther. 2015;14:1024–34.
37. Mikami S, Oya M, Mizuno R, Kosaka T, Katsube K, Okada Y. Invasion and metastasis of renal cell carcinoma. Med Mol Morphol. 2014;47:63–7.
38. Weimer JM, Anton ES. Doubling up on microtubule stabilizers: synergistic functions of doublecortin-like kinase and doublecortin in the developing cerebral cortex. Neuron. 2006;49:3–4.
39. Cancer Genome Atlas Research Network. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature. 2013;499:43–9.
40. Cao J, Liu J, Xu R, Zhu X, Liu L, Zhao X. MicroRNA-21 stimulates epithelial-to-mesenchymal transition and tumorigenesis in clear cell renal cells. Mol Med Rep. 2016;13:75–82.
41. Lu R, Ji Z, Li X, Zhai Q, Zhao C, Jiang Z, et al. miR-145 functions as tumor suppressor and targets two oncogenes, ANGPT2 and NEDD9, in renal cell carcinoma. J Cancer Res Clin Oncol. 2014;140:387–97.
42. Jingushi K, Ueda Y, Kitae K, Hase H, Egawa H, Ohshio I, et al. miRNA-629 targets TRIM33 to promote TGF-beta/Smad signaling and metastatic phenotypes in ccRCC. Mol Cancer Res. 2014;13:565–74.
43. Zhang S, Zhang D, Yi C, Wang Y, Wang H, Wang J. MicroRNA-22 functions as a tumor suppressor by targeting SIRT1 in renal cell carcinoma. Oncol Rep. 2016;35:559–67.
44. Liu Y, Zhang M, Qian J, Bao M, Meng X, Zhang S, et al. miR-134 functions as a tumor suppressor in cell proliferation and epithelial-to-mesenchymal transition by targeting KRAS in renal cell carcinoma cells. DNA Cell Biol. 2015;34:429–36.
45. Li W, Wang Q, Su Q, Ma D, An C, Ma L, et al. Honokiol suppresses renal cancer cells’ metastasis via dual-blocking epithelial–mesenchymal transition and cancer stem cell properties through modulating miR-141/ZEB2 signaling. Mol Cells. 2014;37:383–8.
46. Yamasaki T, Seki N, Yoshino H, Itesako T, Hidaka H, Yamada Y, et al. MicroRNA-218 inhibits cell migration and invasion in renal cell carcinoma through targeting caveolin-2 involved in focal adhesion pathway. J Urol. 2013;190:1059–68.