Non-canonical GLI1/2 activation by PI3K/AKT signaling in renal cell carcinoma: A novel potential therapeutic target

Cancer Letters

Volumn 370, Issue 2, 2016, Pages 313-323

  Zhou, Jiancheng ^a   Zhu, Guodong ^a   Huang, Jun ^a   Li, Lei ^a   Du, Yuefeng ^a   Gao, Yang ^a   Wu, Dapeng ^a   Wang, Xinyang ^a   Hsieh, Jer Tsong ^b   He, Dalin ^a   Wu, Kaijie ^a  

^a THE FIRST AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Hedgehog pathway; PI3K AKT; Renal cell carcinoma; Therapeutic target; VHL

Indexed keywords

ANTINEOPLASTIC AGENT; GANT61; MESSENGER RNA; PERIFOSINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN; G PROTEIN COUPLED RECEPTOR; GANT 61; GLI1 PROTEIN, HUMAN; GLI2 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; NUCLEAR PROTEIN; PYRIDINE DERIVATIVE; PYRIMIDINE DERIVATIVE; SMO PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER PROGNOSIS; CARCINOGENESIS; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DRUG POTENCY; DRUG POTENTIATION; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CARCINOMA; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; RENAL CELL CARCINOMA CELL LINE; TUMOR GROWTH; UPREGULATION; ANTAGONISTS AND INHIBITORS; CARCINOMA, RENAL CELL; CELL CULTURE; KIDNEY NEOPLASMS; MORTALITY; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

CARCINOMA, RENAL CELL; CELLS, CULTURED; HUMANS; KIDNEY NEOPLASMS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PYRIDINES; PYRIMIDINES; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84949505624     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.11.006     Document Type: Article

References (51)

1. Cohen H.T., McGovern F.J. Renal-cell carcinoma. N. Engl. J. Med 2005, 353:2477-2490.
2. Sato Y., Yoshizato T., Shiraishi Y., Maekawa S., Okuno Y., Kamura T., et al. Integrated molecular analysis of clear-cell renal cell carcinoma. Nat. Genet 2013, 45:860-867.
3. Ohh M., Kaelin W.G. VHL and kidney cancer. Methods Mol. Biol 2003, 222:167-183.
4. Zhang H., Gao P., Fukuda R., Kumar G., Krishnamachary B., Zeller K.I., et al. HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 2007, 11:407-420.
5. Sudarshan S., Karam J.A., Brugarolas J., Thompson R.H., Uzzo R., Rini B., et al. Metabolism of kidney cancer: from the lab to clinical practice. Eur. Urol 2013, 63:244-251.
6. Gordan J.D., Bertout J.A., Hu C.J., Diehl J.A., Simon M.C. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 2007, 11:335-347.
7. Cancer Genome Atlas Research Network Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 2013, 499:43-49.
8. Gesk S., Siebert R., Wacker H.H., Nurnberg N., Harder L., Lehman J., et al. Lack of deletions of the PTEN/MMAC1 and MXI1 loci in renal cell carcinoma by interphase cytogenetics. Cancer Genet. Cytogenet 2000, 118:87-88.
9. Pena-Llopis S., Vega-Rubin-de-Celis S., Liao A., Leng N., Pavia-Jimenez A., Wang S., et al. BAP1 loss defines a new class of renal cell carcinoma. Nat. Genet 2012, 44:751-759.
10. Kucejova B., Pena-Llopis S., Yamasaki T., Sivanand S., Tran T.A., Alexander S., et al. Interplay between pVHL and mTORC1 pathways in clear-cell renal cell carcinoma. Mol. Cancer Res 2011, 9:1255-1265.
11. Varela I., Tarpey P., Raine K., Huang D., Ong C.K., Stephens P., et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 2011, 469:539-542.
12. Sosman J.A., Puzanov I., Atkins M.B. Opportunities and obstacles to combination targeted therapy in renal cell cancer. Clin. Cancer Res 2007, 13:764s-769s.
13. Karhadkar S.S., Bova G.S., Abdallah N., Dhara S., Gardner D., Maitra A., et al. Hedgehog signalling in prostate regeneration, neoplasia and metastasis. Nature 2004, 431:707-712.
14. Goodrich L.V., Milenkovic L., Higgins K.M., Scott M.P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 1997, 277:1109-1113.
15. Xie J., Murone M., Luoh S.M., Ryan A., Gu Q., Zhang C., et al. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 1998, 391:90-92.
16. Taipale J., Beachy P.A. The Hedgehog and Wnt signalling pathways in cancer. Nature 2001, 411:349-354.
17. Zhou J., Wu K., Gao D., Zhu G., Wu D., Wang X., et al. Reciprocal regulation of hypoxia-inducible factor 2alpha and GLI1 expression associated with the radioresistance of renal cell carcinoma. Int. J. Radiat. Oncol. Biol. Phys 2014, 90:942-951.
18. Wu K., Xie D., Zou Y., Zhang T., Pong R.C., Xiao G., et al. The mechanism of DAB2IP in chemoresistance of prostate cancer cells. Clin. Cancer Res 2013, 19:4740-4749.
19. Zhou J., Deng Z., Chen Y., Gao Y., Wu D., Zhu G., et al. Overexpression of FABP7 promotes cell growth and predicts poor prognosis of clear cell renal cell carcinoma. Urol. Oncol 2015, 33:113.e9-113.e17.
20. Berman D.M., Karhadkar S.S., Maitra A., Montes De Oca R., Gerstenblith M.R., Briggs K., et al. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature 2003, 425:846-851.
21. He X., Zhang L., Chen Y., Remke M., Shih D., Lu F., et al. The G protein alpha subunit Galphas is a tumor suppressor in Sonic hedgehog-driven medulloblastoma. Nat. Med 2014, 20:1035-1042.
22. Lauth M., Bergstrom A., Shimokawa T., Toftgard R. Inhibition of GLI-mediated transcription and tumor cell growth by small-molecule antagonists. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:8455-8460.
23. Riobo N.A., Lu K., Ai X., Haines G.M., Emerson C.P. Phosphoinositide 3-kinase and Akt are essential for Sonic Hedgehog signaling. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4505-4510.
24. Wei L., Xu Z. Cross-signaling among phosphinositide-3 kinase, mitogen-activated protein kinase and sonic hedgehog pathways exists in esophageal cancer. Int. J. Cancer 2011, 129:275-284.
25. Nilsson M., Unden A.B., Krause D., Malmqwist U., Raza K., Zaphiropoulos P.G., et al. Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:3438-3443.
26. Grachtchouk M., Mo R., Yu S., Zhang X., Sasaki H., Hui C.C., et al. Basal cell carcinomas in mice overexpressing Gli2 in skin. Nat. Genet 2000, 24:216-217.
27. Wasson J.C., Saylors R.L., Zeltzer P., Friedman H.S., Bigner S.H., Burger P.C., et al. Oncogene amplification in pediatric brain tumors. Cancer Res 1990, 50:2987-2990.
28. Zunich S.M., Douglas T., Valdovinos M., Chang T., Bushman W., Walterhouse D., et al. Paracrine sonic hedgehog signalling by prostate cancer cells induces osteoblast differentiation. Mol. Cancer 2009, 8:12.
29. Zhu G., Zhau H.E., He H., Zhang L., Shehata B., Wang X., et al. Sonic and desert hedgehog signaling in human fetal prostate development. Prostate 2007, 67:674-684.
30. Stecca B., Mas C., Clement V., Zbinden M., Correa R., Piguet V., et al. Melanomas require HEDGEHOG-GLI signaling regulated by interactions between GLI1 and the RAS-MEK/AKT pathways. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:5895-5900.
31. Wang Y., Ding Q., Yen C.J., Xia W., Izzo J.G., Lang J.Y., et al. The crosstalk of mTOR/S6K1 and Hedgehog pathways. Cancer Cell 2012, 21:374-387.
32. Jiang J., Hui C.C. Hedgehog signaling in development and cancer. Dev. Cell 2008, 15:801-812.
33. Yoon J.W., Kita Y., Frank D.J., Majewski R.R., Konicek B.A., Nobrega M.A., et al. Gene expression profiling leads to identification of GLI1-binding elements in target genes and a role for multiple downstream pathways in GLI1-induced cell transformation. J. Biol. Chem 2002, 277:5548-5555.
34. Arjumand W., Sultana S. Role of VHL gene mutation in human renal cell carcinoma. Tumour Biol 2012, 33:9-16.
35. Herman J.G., Latif F., Weng Y., Lerman M.I., Zbar B., Liu S., et al. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:9700-9704.
36. Tyers M., Rottapel R. VHL: a very hip ligase. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:12230-12232.
37. Hergovich A., Lisztwan J., Barry R., Ballschmieter P., Krek W. Regulation of microtubule stability by the von Hippel-Lindau tumour suppressor protein pVHL. Nat. Cell Biol 2003, 5:64-70.
38. Kurban G., Duplan E., Ramlal N., Hudon V., Sado Y., Ninomiya Y., et al. Collagen matrix assembly is driven by the interaction of von Hippel-Lindau tumor suppressor protein with hydroxylated collagen IV alpha 2. Oncogene 2008, 27:1004-1012.
39. Roe J.S., Kim H.R., Hwang I.Y., Cho E.J., Youn H.D. von Hippel-Lindau protein promotes Skp2 destabilization on DNA damage. Oncogene 2011, 30:3127-3138.
40. Roe J.S., Youn H.D. The positive regulation of p53 by the tumor suppressor VHL. Cell Cycle 2006, 5:2054-2056.
41. Wang J., Zhang W., Ji W., Liu X., Ouyang G., Xiao W. The von Hippel-Lindau protein suppresses androgen receptor activity. Mol. Endocrinol 2014, 28:239-248.
42. Cho H.K., Kim S.Y., Kim K.H., Kim H.H., Cheong J. Tumor suppressor protein VHL inhibits Hedgehog-Gli activation through suppression of Gli1 nuclear localization. FEBS Lett 2013, 587:826-832.
43. Potter C.J., Pedraza L.G., Xu T. Akt regulates growth by directly phosphorylating Tsc2. Nat. Cell Biol 2002, 4:658-665.
44. Rini B.I., Atkins M.B. Resistance to targeted therapy in renal-cell carcinoma. Lancet Oncol 2009, 10:992-1000.
45. Wander S.A., Hennessy B.T., Slingerland J.M. Next-generation mTOR inhibitors in clinical oncology: how pathway complexity informs therapeutic strategy. J. Clin. Invest 2011, 121:1231-1241.
46. Greenwald R.J., Freeman G.J., Sharpe A.H. The B7 family revisited. Annu. Rev. Immunol 2005, 23:515-548.
47. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med 2012, 366:2443-2454.
48. von Roemeling C.A., Marlow L.A., Wei J.J., Cooper S.J., Caulfield T.R., Wu K., et al. Stearoyl-CoA desaturase 1 is a novel molecular therapeutic target for clear cell renal cell carcinoma. Clin. Cancer Res 2013, 19:2368-2380.
49. Kubo M., Nakamura M., Tasaki A., Yamanaka N., Nakashima H., Nomura M., et al. Hedgehog signaling pathway is a new therapeutic target for patients with breast cancer. Cancer Res 2004, 64:6071-6074.
50. Amakye D., Jagani Z., Dorsch M. Unraveling the therapeutic potential of the Hedgehog pathway in cancer. Nat. Med 2013, 19:1410-1422.
51. Filbin M.G., Dabral S.K., Pazyra-Murphy M.F., Ramkissoon S., Kung A.L., Pak E., et al. Coordinate activation of Shh and PI3K signaling in PTEN-deficient glioblastoma: new therapeutic opportunities. Nat. Med 2013, 19:1518-1523.