Palmitoylation of oncogenic NRAS is essential for leukemogenesis

Blood

Volumn 115, Issue 17, 2010, Pages 3598-3605

  Cuiffo, Benjamin ^a   Ren, Ruibao ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE GRANULOCYTIC LEUKEMIA; ACYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC MYELOMONOCYTIC LEUKEMIA; CONTROLLED STUDY; FARNESYLATION; GENE TARGETING; LEUKEMOGENESIS; MALE; MOUSE; NONHUMAN; ONCOGENE N RAS; PALMITOYLATION; PRIORITY JOURNAL;

EID: 77951729960     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-03-213876     Document Type: Article

References (48)

1. Ulkü AS, Der CJ. Ras signaling, deregulation of gene expression and oncogenesis. Cancer Treat Res. 2003;115:189-208.
2. Bos JL. ras oncogenes in human cancer: a review. Cancer Res. 1989;49(17):4682-4689. (Pubitemid 19213607)
3. Omerovic J, Laude AJ, Prior IA. Ras proteins: paradigms for compartmentalised and isoform-specific signalling. Cell Mol Life Sci. 2007;64(19):2575-2589. (Pubitemid 350035604)
4. Plowman SJ, Hancock JF. Ras signaling from plasma membrane and endomembrane microdomains. Biochim Biophys Acta. 2005;1746(3):274-283. (Pubitemid 41815021)
5. Hancock JF. Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol. 2003;4(5):373-384.
6. Hancock JF, Magee AI, Childs JE, Marshall CJ. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell. 1989;57(7):1167-1177.
7. Wright LP, Philips MR. Thematic review series: lipid posttranslational modifications. CAAX modification and membrane targeting of Ras. J Lipid Res. 2006;47(5):883-891.
8. Rocks O, Peyker A, Kahms M, et al. An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science. 2005;307(5716):1746-1752. (Pubitemid 40388611)
9. Leevers SJ, Marshall CJ. Activation of extracellular signal-regulated kinase, ERK2, by p21ras oncoprotein. EMBO J. 1992;11(2):569-574.
10. Willumsen BM, Christensen A, Hubbert NL, Papageorge AG, Lowy DR. The p21 ras C-terminus is required for transformation and membrane association. Nature. 1984;310(5978):583-586. (Pubitemid 14053901)
11. Harousseau JL. Farnesyltransferase inhibitors in hematologic malignancies. Blood Rev. 2007;21(4):173-182.
12. James GL, Goldstein JL, Brown MS. Polylysine and CVIM sequences of K-RasB dictate specificity of prenylation and confer resistance to benzodiazepine peptidomimetic in vitro. J Biol Chem. 1995;270(11):6221-6226.
13. Ashar HR, James L, Gray K, et al. Farnesyl transferase inhibitors block the farnesylation of CENP-E and CENP-F and alter the association of CENP-E with the microtubules. J Biol Chem. 2000;275(39):30451-30457.
14. Basso AD, Mirza A, Liu G, Long BJ, Bishop WR, Kirschmeier P. The farnesyl transferase inhibitor (FTI) SCH66336 (lonafarnib) inhibits Rheb farnesylation and mTOR signaling: role in FTI enhancement of taxane and tamoxifen anti-tumor activity. J Biol Chem. 2005;280(35):31101-31108. (Pubitemid 41291845)
15. Lebowitz PF, Casey PJ, Prendergast GC, Thissen JA. Farnesyltransferase inhibitors alter the prenylation and growth-stimulating function of RhoB. J Biol Chem. 1997;272(25):15591-15594.
16. Liu A, Du W, Liu JP, Jessell TM, Prendergast GC. RhoB alteration is necessary for apoptotic and antineoplastic responses to farnesyltransferase inhibitors. Mol Cell Biol. 2000;20(16):6105-6113. (Pubitemid 30613058)
17. Lobell RB, Omer CA, Abrams MT, et al. Evaluation of farnesyl:protein transferase and geranylgeranyl: protein transferase inhibitor combinations in preclinical models. Cancer Res. 2001;61(24):8758-8768.
18. Wahlstrom AM, Cutts BA, Karlsson C, et al. Rce1 deficiency accelerates the development of K-RAS-induced myeloproliferative disease. Blood. 2007;109(2):763-768. (Pubitemid 46105979)
19. Wahlstrom AM, Cutts BA, Liu M, et al. Inactivating Icmt ameliorates K-RAS-induced myeloproliferative disease. Blood. 2008;112(4):1357-1365.
20. Hancock JF, Paterson H, Marshall CJ. A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell. 1990;63(1):133-139. (Pubitemid 20359511)
21. Harding A, Hancock JF. Ras nanoclusters: combining digital and analog signaling. Cell Cycle. 2008;7(2):127-134. (Pubitemid 351366508)
22. Henis YI, Hancock JF, Prior IA. Ras acylation, compartmentalization and signaling nanoclusters [Review]. Mol Membr Biol. 2009;26(1):80-92.
23. Prior IA, Hancock JF. Compartmentalization of Ras proteins. J Cell Sci. 2001;114(9):1603-1608.
24. Tian T, Harding A, Inder K, Plowman S, Parton RG, Hancock JF. Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat Cell Biol. 2007;9(8):905-914. (Pubitemid 47190445)
25. Ducker CE, Griffel LK, Smith RA, et al. Discovery and characterization of inhibitors of human palmitoyl acyltransferases. Mol Cancer Ther. 2006;5(7):1647-1659. (Pubitemid 44323232)
26. Bivona TG, Perez De Castro I, Ahearn IM, et al. Phospholipase Cγ activates Ras on the Golgi apparatus by means of RasGRP1. Nature. 2003;424(6949):694-698.
27. Chiu VK, Bivona T, Hach A, et al. Ras signalling on the endoplasmic reticulum and the Golgi. Nat Cell Biol. 2002;4(5):343-350. (Pubitemid 34521029)
28. Eungdamrong NJ, Iyengar R. Compartment-specific feedback loop and regulated trafficking can result in sustained activation of Ras at the Golgi. Biophys J. 2007;92(3):808-815. (Pubitemid 46203211)
29. Perez de Castro I, Bivona TG, Philips MR, Pellicer A. Ras activation in Jurkat T cells following low-grade stimulation of the T-cell receptor is specific to N-Ras and occurs only on the Golgi apparatus. Mol Cell Biol. 2004;24(8):3485-3496. (Pubitemid 38452087)
30. Quatela SE, Philips MR. Ras signaling on the Golgi. Curr Opin Cell Biol. 2006;18(2):162-167.
31. Parikh C, Subrahmanyam R, Ren R. Oncogenic NRAS rapidly and efficiently induces CMML- and AML-like diseases in mice. Blood. 2006;108(7):2349-2357. (Pubitemid 44497519)
32. Gross AW, Zhang X, Ren R. Bcr-Abl with an SH3 deletion retains the ability to induce a myeloproliferative disease in mice, yet c-Abl activated by an SH3 deletion induces only lymphoid malignancy. Mol Cell Biol. 1999;19(10):6918-6928. (Pubitemid 29441874)
33. Parikh C, Subrahmanyam R, Ren R. Oncogenic NRAS, KRAS, and HRAS exhibit different leukemogenic potentials in mice. Cancer Res. 2007;67(15):7139-7146. (Pubitemid 47206541)
34. Zhang X, Ren R. Bcr-Abl efficiently induces a myeloproliferative disease and production of excess interleukin-3 and granulocyte-macrophage colony-stimulating factor in mice: a novel model for chronic myelogenous leukemia. Blood. 1998;92(10):3829-3840. (Pubitemid 28525209)
35. Li W, Zhu T, Guan KL. Transformation potential of Ras isoforms correlates with activation of phosphatidylinositol 3-kinase but not ERK. J Biol Chem. 2004;279(36):37398-37406. (Pubitemid 39195448)
36. Engelman JA, Luo J, Cantley LC. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet. 2006;7(8):606-619. (Pubitemid 44100518)
37. Manning BD, Cantley LC. AKT/PKB signaling: navigating downstream. Cell. 2007;129(7):1261-1274.
38. Hresko RC, Mueckler M. mTOR: RICTOR is the Ser473 kinase for Akt/protein kinase B in 3T3-L1 adipocytes. J Biol Chem. 2005;280(49):40406-40416.
39. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science. 2005;307(5712):1098- 1101.
40. Holland EC, Sonenberg N, Pandolfi PP, Thomas G. Signaling control of mRNA translation in cancer pathogenesis. Oncogene. 2004;23(18):3138-3144. (Pubitemid 38638825)
41. Bodemann BO, White MA. Ral GTPases and cancer: linchpin support of the tumorigenic platform. Nat Rev Cancer. 2008;8(2):133-140.
42. Daley GQ, McLaughlin J, Witte ON, Baltimore D. The CML-specific P210 bcr/abl protein, unlike v-abl, does not transform NIH/3T3 fibroblasts. Science. 1987;237(4814):532-535. (Pubitemid 17125923)
43. Renshaw MW, Kipreos ET, Albrecht MR, Wang JY. Oncogenic v-Abl tyrosine kinase can inhibit or stimulate growth, depending on the cell context. EMBO J. 1992;11(11):3941-3951.
44. Zimmermann S, Moelling K. Phosphorylation and regulation of Raf by Akt (protein kinase B). Science. 1999;286(5445):1741-1744. (Pubitemid 129515882)
45. Jaumot M, Hancock JF. Protein phosphatases 1 and 2A promote Raf-1 activation by regulating 14-3-3 interactions. Oncogene. 2001;20(30):3949-3958. (Pubitemid 32681600)
46. Fukata Y, Iwanaga T, Fukata M. Systematic screening for palmitoyl transferase activity of the DHHC protein family in mammalian cells. Methods. 2006;40(2):177-182. (Pubitemid 44442975)
47. Iwanaga T, Tsutsumi R, Noritake J, Fukata Y, Fukata M. Dynamic protein palmitoylation in cellular signaling. Prog Lipid Res. 2009;48(3):117-127.
48. Swarthout JT, Lobo S, Farh L, et al. DHHC9 and GCP16 constitute a human protein fatty acyltransferase with specificity for H- and N-Ras. J Biol Chem. 2005;280(35):31141-31148. (Pubitemid 41291850)