Therapeutic levels of the hydroxmethylglutaryl-coenzyme A reductase inhibitor lovastatin activate ras signaling via phospholipase D2

Molecular and Cellular Biology

Volumn 31, Issue 6, 2011, Pages 1110-1120

  Cho, Kwang Jin ^a   Hill, Michelle M ^b   Chigurupati, Sravanthi ^a   Du, Guangwei ^a   Parton, Robert G ^b   Hancock, John F ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; EPIDERMAL GROWTH FACTOR RECEPTOR; MEVINOLIN; MITOGEN ACTIVATED PROTEIN KINASE; OXIDOREDUCTASE; PHOSPHOLIPASE D2; RAP PROTEIN; RAS PROTEIN; RHO FACTOR; STATIN;

ANIMAL CELL; ARTICLE; CELL COMMUNICATION; CHOLESTEROL BLOOD LEVEL; COENZYME; HUMAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PRENYLATION; UMBILICAL VEIN ENDOTHELIAL CELL; WILD TYPE;

ANIMALS; ANTICHOLESTEREMIC AGENTS; CELL LINE; CHOLESTEROL; CRICETINAE; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LOVASTATIN; PHOSPHOLIPASE D; PROTEIN PRENYLATION; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

RODENTIA;

EID: 79952274171     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00989-10     Document Type: Article

References (65)

1. Adamson, P., H. F. Paterson, and A. Hall. 1992. Intracellular localization of the P21rho proteins. J. Cell Biol. 119:617-627.
2. Ariotti, N., et al. 2010. Epidermal growth factor receptor activation remodels the plasma membrane lipid environment to induce nanocluster formation. Mol. Cell. Biol. 30:3795-3804.
3. Arnaud, C., V. Braunersreuther, and F. Mach. 2005. Toward immunomodulatory and anti-inflammatory properties of statins. Trends Cardiovasc. Med. 15:202-206.
4. Berzat, A. C., D. C. Brady, J. J. Fiordalisi, and A. D. Cox. 2006. Using inhibitors of prenylation to block localization and transforming activity. Methods Enzymol. 407:575-597.
5. Campbell, M. J., et al. 2006. Breast cancer growth prevention by statins. Cancer Res. 66:8707-8714. (Pubitemid 44449187)
6. Casey, P. J., P. A. Solski, C. J. Der, and J. E. Buss. 1989. p21ras is modified by a farnesyl isoprenoid. Proc. Natl. Acad. Sci. U. S. A. 86:8323-8327.
7. Cerezo-Guisado, M. I., et al. 2007. Lovastatin inhibits the extracellular-signal-regulated kinase pathway in immortalized rat brain neuroblasts. Biochem. J. 401:175-183. (Pubitemid 46114611)
8. Cha, M. S., M. J. Lee, G. H. Je, and J. Y. Kwak. 2001. Endogenous production of nitric oxide by vascular endothelial growth factor down-regulates proliferation of choriocarcinoma cells. Biochem. Biophys. Res. Commun. 282:1061-1066.
9. Chen, J. C., M. L. Wu, K. C. Huang, and W. W. Lin. 2008. HMG-CoA reductase inhibitors activate the unfolded protein response and induce cytoprotective GRP78 expression. Cardiovasc. Res. 80:138-150.
10. Cho, C. H., et al. 2004. Localization of VEGFR-2 and PLD2 in endothelial caveolae is involved in VEGF-induced phosphorylation of MEK and ERK. Am. J. Physiol. Heart Circ. Physiol. 286:H1881-H1888.
11. Diaz, O., et al. 2005. Disruption of lipid rafts stimulates phospholipase d activity in human lymphocytes: implication in the regulation of immune function. J. Immunol. 175:8077-8086. (Pubitemid 41798370)
12. Eisenberg, S., D. E. Shvartsman, M. Ehrlich, and Y. I. Henis. 2006. Clustering of raft-associated proteins in the external membrane leaflet modulates internal leaflet h-ras diffusion and signaling. Mol. Cell. Biol. 26:7190-7200.
13. Emmanuele, L., J. Ortmann, T. Doerflinger, T. Traupe, and M. Barton. 2003. Lovastatin stimulates human vascular smooth muscle cell expression of bone morphogenetic protein-2, a potent inhibitor of low-density lipoprotein- stimulated cell growth. Biochem. Biophys. Res. Commun. 302:67-72.
14. Ghosh-Choudhury, N., C. C. Mandal, and G. G. Choudhury. 2007. Statin-induced Ras activation integrates the phosphatidylinositol 3-kinase signal to Akt and MAPK for bone morphogenetic protein-2 expression in osteoblast differentiation. J. Biol. Chem. 282:4983-4993.
15. Goldstein, J. L., and M. S. Brown. 1990. Regulation of the mevalonate pathway. Nature 343:425-430.
16. Graaf, M. R., A. B. Beiderbeck, A. C. Egberts, D. J. Richel, and H. J. Guchelaar. 2004. The risk of cancer in users of statins. J. Clin. Oncol. 22:2388-2394.
17. Graaf, M. R., D. J. Richel, C. J. van Noorden, and H. J. Guchelaar. 2004. Effects of statins and farnesyltransferase inhibitors on the development and progression of cancer. Cancer Treat. Rev. 30:609-641.
18. Gratton, J. P., et al. 2000. Reconstitution of an endothelial nitric-oxide synthase (eNOS), hsp90, and caveolin-1 complex in vitro. Evidence that hsp90 facilitates calmodulin stimulated displacement of eNOS from caveolin-1. J. Biol. Chem. 275:22268-22272.
19. Grossini, E., C. Molinari, P. P. Caimmi, F. Uberti, and G. Vacca. 2009. Levosimendan induces NO production through p38 MAPK, ERK and Akt in porcine coronary endothelial cells: role for mitochondrial K(ATP) channel. Br. J. Pharmacol. 156:250-261.
20. Grundy, S. M., et al. 2004. Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III guidelines. Circulation 110:227-239. (Pubitemid 38924592)
21. Gupta, S., et al. 2007. Binding of ras to phosphoinositide 3-kinase p110alpha is required for ras-driven tumorigenesis in mice. Cell 129:957-968. (Pubitemid 46802703)
22. Gutierrez, L., A. I. Magee, C. J. Marshall, and J. F. Hancock. 1989. Post-translational processing of p21ras is two-step and involves carboxyl-methylation and carboxy-terminal proteolysis. EMBO J. 8:1093-1098.
23. Hancock, J. F. 2006. Lipid rafts: contentious only from simplistic standpoints. Nat. Rev. Mol. Cell Biol. 7:456-462.
24. Hancock, J. F. 2007. PA promoted to manager. Nat. Cell Biol. 9:615-617.
25. Hancock, J. F. 1995. Prenylation and palmitoylation analysis. Methods Enzymol. 255:237-245.
26. Hancock, J. F. 2003. Ras proteins: different signals from different locations. Nat. Rev. Mol. Cell Biol. 4:373-384.
27. Hancock, J. F., A. I. Magee, J. E. Childs, and C. J. Marshall. 1989. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57: 1167-1177.
28. Hancock, J. F., and R. G. Parton. 2005. Ras plasma membrane signalling platforms. Biochem. J. 389:1-11.
29. Hancock, J. F., H. Paterson, and C. J. Marshall. 1990. A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell 63:133-139.
30. Harding, A. S., and J. F. Hancock. 2008. Using plasma membrane nanoclusters to build better signaling circuits. Trends Cell Biol. 18:364-371.
31. Heasman, S. J., and A. J. Ridley. 2008. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9:690-701.
32. Hochgraf, E., Y. Levy, M. Aviram, J. G. Brook, and U. Cogan. 1994. Lovastatin decreases plasma and platelet cholesterol levels and normalizes elevated platelet fluidity and aggregation in hypercholesterolemic patients. Metabolism 43:11-17. (Pubitemid 24047099)
33. Honda, A., et al. 1999. Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99:521-532.
34. Jenkins, G. M., and M. A. Frohman. 2005. Phospholipase D: a lipid centric review. Cell. Mol. Life Sci. 62:2305-2316.
35. Kita, T., M. S. Brown, and J. L. Goldstein. 1980. Feedback regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase in livers of mice treated with mevinolin, a competitive inhibitor of the reductase. J. Clin. Invest. 66:1094-1100.
36. Laufs, U. 2003. Beyond lipid-lowering: effects of statins on endothelial nitric oxide. Eur. J. Clin. Pharmacol. 58:719-731.
37. Laufs, U., and J. K. Liao. 1998. Post-transcriptional regulation of endothelial nitric oxide synthase mRNA stability by Rho GTPase. J. Biol. Chem. 273: 24266-24271.
38. Lewis, K. A., S. A. Holstein, and R. J. Hohl. 2005. Lovastatin alters the isoprenoid biosynthetic pathway in acute myelogenous leukemia cells in vivo. Leuk. Res. 29:527-533.
39. Liao, J. K., and U. Laufs. 2005. Pleiotropic effects of statins. Annu. Rev. Pharmacol. Toxicol. 45:89-118.
40. Lijnen, P., H. Celis, R. Fagard, J. Staessen, and A. Amery. 1994. Influence of cholesterol lowering on plasma membrane lipids and cationic transport systems. J. Hypertens. 12:59-64. (Pubitemid 24044009)
41. Mantha, A. J., et al. 2005. Targeting the mevalonate pathway inhibits the function of the epidermal growth factor receptor. Clin. Cancer Res. 11:2398-2407.
42. Mason, R. P., M. F. Walter, and R. F. Jacob. 2004. Effects of HMG-CoA reductase inhibitors on endothelial function: role of microdomains and oxidative stress. Circulation 109:II34-41.
43. Michaelson, D., et al. 2001. Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J. Cell Biol. 152:111-126. (Pubitemid 32102441)
44. Michel, J. B., O. Feron, D. Sacks, and T. Michel. 1997. Reciprocal regulation of endothelial nitric-oxide synthase by Ca2+-calmodulin and caveolin. J. Biol. Chem. 272:15583-15586.
45. Mor, A., et al. 2007. The lymphocyte function-associated antigen-1 receptor costimulates plasma membrane Ras via phospholipase D2. Nat. Cell Biol. 9:713-719.
46. Niv, H., O. Gutman, Y. Kloog, and Y. I. Henis. 2002. Activated K-Ras and H-Ras display different interactions with saturable nonraft sites at the surface of live cells. J. Cell Biol. 157:865-872.
47. Ogunwobi, O. O., and I. L. Beales. 2008. Statins inhibit proliferation and induce apoptosis in Barrett's esophageal adenocarcinoma cells. Am. J. Gastroenterol. 103:825-837.
48. Orme, M. H., S. Alrubaie, G. L. Bradley, C. D. Walker, and S. J. Leevers. 2006. Input from Ras is required for maximal PI(3)K signalling in Drosophila. Nat. Cell Biol. 8:1298-1302.
49. Plowman, S. J., N. Ariotti, A. Goodall, R. G. Parton, and J. F. Hancock. 2008. Electrostatic interactions positively regulate K-Ras nanocluster formation and function. Mol. Cell. Biol. 28:4377-4385.
50. Plowman, S. J., C. Muncke, R. G. Parton, and J. F. Hancock. 2005. H-ras, K-ras, and inner plasma membrane raft proteins operate in nanoclusters with differential dependence on the actin cytoskeleton. Proc. Natl. Acad. Sci. U. S. A. 102:15500-15505.
51. Prior, I. A., et al. 2001. GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nat. Cell Biol. 3:368-375.
52. Prior, I. A., C. Muncke, R. G. Parton, and J. F. Hancock. 2003. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J. Cell Biol. 160:165-170.
53. Rikitake, Y., and J. K. Liao. 2005. Rho GTPases, statins, and nitric oxide. Circ. Res. 97:1232-1235.
54. Roy, S., et al. 1999. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat. Cell Biol. 1:98-105.
55. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-39.
56. Sinensky, M., L. A. Beck, S. Leonard, and R. Evans. 1990. Differential inhibitory effects of lovastatin on protein isoprenylation and sterol synthesis. J. Biol. Chem. 265:19937-19941.
57. Smith, S. C., Jr., et al. 2006. AHA/ACC guidelines for secondary prevention for patients with coronary and other atherosclerotic vascular disease: 2006 update: endorsed by the National Heart, Lung, and Blood Institute. Circulation 113:2363-2372.
58. Sukhova, G. K., J. K. Williams, and P. Libby. 2002. Statins reduce inflammation in atheroma of nonhuman primates independent of effects on serum cholesterol. Arterioscler. Thromb. Vasc. Biol. 22:1452-1458.
59. Tian, T., et al. 2007. Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat. Cell Biol. 9:905-914.
60. Vaughan, C. J., and A. M. Gotto, Jr. 2004. Update on statins: 2003. Circulation 110:886-892.
61. Wang, P. Y., J. Weng, and R. G. Anderson. 2005. OSBP is a cholesterol-regulated scaffolding protein in control of ERK 1/2 activation. Science 307: 1472-1476.
62. Yano, M., et al. 2007. Statins activate peroxisome proliferator-activated receptor gamma through extracellular signal-regulated kinase 1/2 and p38 mitogen-activated protein kinase-dependent cyclooxygenase-2 expression in macrophages. Circ. Res. 100:1442-1451.
63. Yeo, E. J., and J. H. Exton. 1995. Stimulation of phospholipase D by epidermal growth factor requires protein kinase C activation in Swiss 3T3 cells. J. Biol. Chem. 270:3980-3988.
64. Yuan, Z., et al. 2009. p38MAPK and ERK promote nitric oxide production in cultured human retinal pigmented epithelial cells induced by high concentration glucose. Nitric Oxide 20:9-15.
65. Zhao, C., G. Du, K. Skowronek, M. A. Frohman, and D. Bar-Sagi. 2007. Phospholipase D2-generated phosphatidic acid couples EGFR stimulation to Ras activation by Sos. Nat. Cell Biol. 9:706-712.