Suppression of the GTPase-activating protein RGS10 increases Rheb-GTP and mTOR signaling in ovarian cancer cells

Cancer Letters

Volumn 369, Issue 1, 2015, Pages 175-183

  Altman, Molly K ^a   Alshamrani, Ali A ^a   Jia, Wei ^a   Nguyen, Ha T ^a   Fambrough, Jada M ^a   Tran, Sterling K ^a   Patel, Mihir B ^a   Hoseinzadeh, Pooya ^a   Beedle, Aaron M ^a   Murph, Mandi M ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

4E BP1; Lysophosphatidic acid; MTOR; Regulator of G protein Signaling 10 protein (RGS10); Rheb

Indexed keywords

ETOPOSIDE; GROWTH FACTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; INITIATION FACTOR 4E BINDING PROTEIN 1; LYSOPHOSPHATIDIC ACID; MAMMALIAN TARGET OF RAPAMYCIN; REGULATOR OF G PROTEIN SIGNALING 10; RGS PROTEIN; RHEB PROTEIN; S6 KINASE; SAPANISERTIB; TEMSIROLIMUS; UNCLASSIFIED DRUG; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; MTOR PROTEIN, HUMAN; NEUROPEPTIDE; RGS10 PROTEIN, HUMAN; RHEB PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE;

ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; INTRACELLULAR SIGNALING; OVARIAN CANCER CELL LINE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN HYDROLYSIS; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; CELL SURVIVAL; FEMALE; GENETICS; HUMAN; METABOLISM; OVARY TUMOR; PATHOLOGY; PHOSPHORYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL SURVIVAL; FEMALE; HUMANS; MONOMERIC GTP-BINDING PROTEINS; NEUROPEPTIDES; OVARIAN NEOPLASMS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RGS PROTEINS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84943455286     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.08.012     Document Type: Article

References (33)

1. Hunt T.W., Fields T.A., Casey P.J., Peralta E.G. RGS10 is a selective activator of G alpha i GTPase activity. Nature 1996, 383:175-177.
2. Siderovski D.P., Willard F.S. The GAPs, GEFs, and GDIs of heterotrimeric G-protein alpha subunits. Int. J. Biol. Sci 2005, 1:51-66.
3. Sethakorn N., Yau D.M., Dulin N.O. Non-canonical functions of RGS proteins. Cell. Signal 2010, 22:1274-1281.
4. Long X., Lin Y., Ortiz-Vega S., Yonezawa K., Avruch J. Rheb binds and regulates the mTOR kinase. Curr. Biol 2005, 15:702-713.
5. Efeyan A., Sabatini D.M. mTOR and cancer: many loops in one pathway. Curr. Opin. Cell Biol 2010, 22:169-176.
6. Goorden S.M., Hoogeveen-Westerveld M., Cheng C., van Woerden G.M., Mozaffari M., Post L., et al. Rheb is essential for murine development. Mol. Cell. Biol 2011, 31:1672-1678.
7. Inoki K., Li Y., Xu T., Guan K.L. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev 2003, 17:1829-1834.
8. Zhang Y., Gao X., Saucedo L.J., Ru B., Edgar B.A., Pan D. Rheb is a direct target of the tuberous sclerosis tumour suppressor proteins. Nat. Cell Biol 2003, 5:578-581.
9. Tee A.R., Manning B.D., Roux P.P., Cantley L.C., Blenis J. Tuberous sclerosis complex gene products, tuberin and hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr. Biol 2003, 13:1259-1268.
10. Tee A.R., Blenis J., Proud C.G. Analysis of mTOR signaling by the small G-proteins, Rheb and RhebL1. FEBS Lett 2005, 579:4763-4768.
11. Weinberg R. The Biology of Cancer 2014, Garland Science. second ed.
12. Guo Y., Kwiatkowski D.J. Equivalent benefit of rapamycin and a potent mTOR ATP-competitive inhibitor, MLN0128 (INK128), in a mouse model of tuberous sclerosis. Mol. Cancer Res 2013, 11:467-473.
13. Hsieh A.C., Liu Y., Edlind M.P., Ingolia N.T., Janes M.R., Sher A., et al. The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature 2012, 485:55-61.
14. Hooks S.B., Callihan P., Altman M.K., Hurst J.H., Ali M.W., Murph M.M. Regulators of G-protein signaling RGS10 and RGS17 regulate chemoresistance in ovarian cancer cells. Mol. Cancer 2010, 9:289.
15. Ali M.W., Cacan E., Liu Y., Pierce J.Y., Creasman W.T., Murph M.M., et al. Transcriptional suppression, DNA methylation, and histone deacetylation of the regulator of G-protein signaling 10 (RGS10) gene in ovarian cancer cells. PLoS ONE 2013, 8:e60185.
16. Wang X., Seed B. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 2003, 31:e154.
17. Monroy C.A., Mackie D.I., Roman D.L. A high throughput screen for RGS proteins using steady state monitoring of free phosphate formation. PLoS ONE 2013, 8:e62247.
18. Jia W., Eneh J.O., Ratnaparkhe S., Altman M.K., Murph M.M. MicroRNA-30c-2* expressed in ovarian cancer cells suppresses growth factor-induced cellular proliferation and downregulates the oncogene BCL9. Mol. Cancer Res 2011, 9:1732-1745.
19. Alberts B. Molecular Biology of the Cell 2015, Garland Science. sixth ed.
20. Kam Y., Exton J.H. Role of phospholipase D1 in the regulation of mTOR activity by lysophosphatidic acid. FASEB J. 2004, 18:311-319.
21. Shor B., Zhang W.G., Toral-Barza L., Lucas J., Abraham R.T., Gibbons J.J., et al. A new pharmacologic action of CCI-779 involves FKBP12-independent inhibition of mTOR kinase activity and profound repression of global protein synthesis. Cancer Res 2008, 68:2934-2943.
22. Wang C.C., Held R.G., Hall B.J. SynGAP regulates protein synthesis and homeostatic synaptic plasticity in developing cortical networks. PLoS ONE 2013, 8:e83941.
23. Lopez-Rivera E., Jayaraman P., Parikh F., Davies M.A., Ekmekcioglu S., Izadmehr S., et al. Inducible nitric oxide synthase drives mTOR pathway activation and proliferation of human melanoma by reversible nitrosylation of TSC2. Cancer Res 2014, 74:1067-1078.
24. Beaufort C.M., Helmijr J.C., Piskorz A.M., Hoogstraat M., Ruigrok-Ritstier K., Besselink N., et al. Ovarian cancer cell line panel (OCCP): clinical importance of in vitro morphological subtypes. PLoS ONE 2014, 9:e103988.
25. Vezina C., Kudelski A., Sehgal S.N. Rapamycin (AY-22,989), a new antifungal antibiotic. I. Taxonomy of the producing streptomycete and isolation of the active principle. J. Antibiot 1975, 28:721-726.
26. Grunwald V., DeGraffenried L., Russel D., Friedrichs W.E., Ray R.B., Hidalgo M. Inhibitors of mTOR reverse doxorubicin resistance conferred by PTEN status in prostate cancer cells. Cancer Res 2002, 62:6141-6145.
27. Lu C.H., Wyszomierski S.L., Tseng L.M., Sun M.H., Lan K.H., Neal C.L., et al. Preclinical testing of clinically applicable strategies for overcoming trastuzumab resistance caused by PTEN deficiency. Clin. Cancer Res 2007, 13:5883-5888.
28. Beeram M., Tan Q.T., Tekmal R.R., Russell D., Middleton A., DeGraffenried L.A. Akt-induced endocrine therapy resistance is reversed by inhibition of mTOR signaling. Ann. Oncol 2007, 18:1323-1328.
29. Tsurutani J., West K.A., Sayyah J., Gills J.J., Dennis P.A. Inhibition of the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin pathway but not the MEK/ERK pathway attenuates laminin-mediated small cell lung cancer cellular survival and resistance to imatinib mesylate or chemotherapy. Cancer Res 2005, 65:8423-8432.
30. Schewe D.M., Aguirre-Ghiso J.A. ATF6alpha-Rheb-mTOR signaling promotes survival of dormant tumor cells in vivo. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:10519-10524.
31. Mabuchi S., Kawase C., Altomare D.A., Morishige K., Sawada K., Hayashi M., et al. mTOR is a promising therapeutic target both in cisplatin-sensitive and cisplatin-resistant clear cell carcinoma of the ovary. Clin. Cancer Res 2009, 15:5404-5413.
32. Altman M.K., Nguyen D.T., Patel S.B., Fambrough J.M., Beedle A.M., Hardman W.J., et al. Regulator of G-protein signaling 5 reduces HeyA8 ovarian cancer cell proliferation and extends survival in a murine tumor model. Biochem. Res. Int 2012, 2012:518437.
33. Jiang H., Vogt P.K. Constitutively active Rheb induces oncogenic transformation. Oncogene 2008, 27:5729-5740.