Amplification of B cell receptor–Erk signaling by Rasgrf-1 overexpression in chronic lymphocytic leukemia

References

• Wickremasinghe RG, Prentice AG, Steele AJ. Aberrantly activated anti-apoptotic signalling mechanisms in chronic lymphocytic leukaemia cells: clues to the identification of novel therapeutic targets. Br J Haematol 2011;153:545–556.
   PubMed Web of Science ®Google Scholar
• Stevenson FK, Krysov S, Davies AJ, et al. B-cell receptor signaling in chronic lymphocytic leukemia. Blood 2011;118:4313–4320.
   PubMed Web of Science ®Google Scholar
• Hamblin TJ, Davis Z, Gardiner A, et al. Unmutated Ig V(H) genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood 1999;94:1848–1854.
   PubMed Web of Science ®Google Scholar
• Chen L, Widhopf G, Huynh L, et al. Expression of ZAP-70 is associated with increased B-cell receptor signaling in chronic lymphocytic leukemia. Blood 2002;100:4609–4614.
   PubMed Web of Science ®Google Scholar
• Efremov DG, Gobessi S, Longo PG. Signaling pathways activated by antigen-receptor engagement in chronic lymphocytic leukemia B-cells. Autoimmun Rev 2007;7:102–108.
   PubMed Web of Science ®Google Scholar
• Ma S, Rosen ST. Signal transduction inhibitors in chronic lymphocytic leukemia. Curr Opin Oncol 2011;23:601–608.
   PubMed Web of Science ®Google Scholar
• Longo PG, Laurenti L, Gobessi S, et al. The Akt/Mcl-1 pathway plays a prominent role in mediating antiapoptotic signals downstream of the B-cell receptor in chronic lymphocytic leukemia B cells. Blood 2008;111:846–855.
   PubMed Web of Science ®Google Scholar
• Krysov S, Dias S, Paterson A, et al. Surface IgM stimulation induces MEK1/2-dependent MYC expression in chronic lymphocytic leukemia cells. Blood 2012;119:170–179.
   PubMedGoogle Scholar
• Burger JA, Tsukada N, Burger M, et al. Blood-derived nurse-like cells protect chronic lymphocytic leukemia B cells from spontaneous apoptosis through stromal cell-derived factor-1. Blood 2000;96: 2655–2663.
   PubMed Web of Science ®Google Scholar
• Buchner M, Fuchs S, Prinz G, et al. Spleen tyrosine kinase is overexpressed and represents a potential therapeutic target in chronic lymphocytic leukemia. Cancer Res 2009;69:5424–5432.
   PubMed Web of Science ®Google Scholar
• Messmer D, Fecteau JF, O’Hayre M, et al. Chronic lymphocytic leukemia cells receive RAF-dependent survival signals in response to CXCL12 that are sensitive to inhibition by sorafenib. Blood 2011;117:882–889.
   PubMed Web of Science ®Google Scholar
• Herman SE, Gordon AL, Hertlein E, et al. Bruton tyrosine kinase represents a promising therapeutic target for treatment of chronic lymphocytic leukemia and is effectively targeted by PCI-32765. Blood 2011;117:6287–6296.
   PubMed Web of Science ®Google Scholar
• Talab F, Allen JC, Thompson V, et al. LCK is an important mediator of B-cell receptor signaling in chronic lymphocytic leukemia cells. Mol Cancer Res 2013;11:541–554.
   PubMed Web of Science ®Google Scholar
• Fecteau JF, Bharati IS, O’Hayre M, et al. Sorafenib-induced apoptosis of chronic lymphocytic leukemia cells is associated with downregulation of RAF and myeloid cell leukemia sequence 1 (Mcl-1). Mol Med 2012;18:19–28.
   PubMed Web of Science ®Google Scholar
• Gold MR, Crowley MT, Martin GA, et al. Targets of B lymphocyte antigen receptor signal transduction include the p21ras GTPase-activating protein (GAP) and two GAP-associated proteins. J Immunol 1993;150:377–386.
   PubMed Web of Science ®Google Scholar
• Yagura H, Oyaizu N, Pahwa S. Tyrosine phosphorylation of guanosine triphosphatase activating protein by activation via surface IgG in human B cells. Blood 1993;81:1535–1539.
   PubMed Web of Science ®Google Scholar
• Milburn MV, Tong L, deVos AM, et al. Molecular switch for signal transduction:structural differences between active and inactive forms of protooncogenic ras proteins. Science 1990;247:939–945.
   PubMed Web of Science ®Google Scholar
• Bos JL, Rehmann H, Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 2007;129: 865–877.
   PubMed Web of Science ®Google Scholar
• Ebinu JO, Stang SL, Teixeira C, et al. RasGRP links T-cell receptor signaling to Ras. Blood 2000;95:3199–3203.
   PubMed Web of Science ®Google Scholar
• Stone JC. Regulation and functi on of the RasGRP family of Ras activators in blood cells. Genes Cancer 2011;2:320–334.
   PubMedGoogle Scholar
• Coughlin JJ, Stang SL, Dower NA, et al. RasGRP1 and RasGRP3 regulate B cell proliferation by facilitating B cell receptor-Ras signaling. J Immunol 2005;175:7179–7184.
   PubMed Web of Science ®Google Scholar
• Lin H, Chen C, Li X, et al. Activation of the MEK/MAPK pathway is involved in bryostatin1-induced monocytic differenciation and up-regulation of X-linked inhibitor of apoptosis protein. Exp Cell Res 2002;272:192–198.
   PubMed Web of Science ®Google Scholar
• Carter BZ, Milella M, Tsao T, et al. Regulation and targeting of antiapoptotic XIAP in acute myeloid leukemia. Leukemia 2003;17:2081–2089.
   PubMed Web of Science ®Google Scholar
• Harada H, Quearry B, Ruiz-Vela A, et al. Survival factor-induced extracellular signal-regulated kinase phosphorylates BIM, inhibiting its association with BAX and proapoptotic activity. Proc Natl Acad Sci USA 2004;101:15313–15317.
   PubMed Web of Science ®Google Scholar
• Pepper C, Thomas A, Fegan C, et al. Flavopiridol induces apoptosis in B-cell chronic lymphocytic leukaemia cells through a p38 and ERK MAP kinase-dependent mechanism. Leuk Lymphoma 2003;44:337–342.
   PubMed Web of Science ®Google Scholar
• Fernandez-Medarde A, Santos E. The RasGrf family of mammalian guanine nucleotide exchange factors. Biochem Biophys Acta 2011;1815:170–188.
   PubMed Web of Science ®Google Scholar
• Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:e45.
   PubMed Web of Science ®Google Scholar
• Roecklein BA, Torok-Storb B. Functionally distinct human marrow stromal cell lines immortalized by transduction with the human papilloma virus E6/E7 genes. Blood 1995;85:997–1005.
   PubMed Web of Science ®Google Scholar
• Guerrero C, Rojas JM, Chedid M, et al. Expression of alternative forms of Ras exchange factors GRF and SOS1 in different human tissues and cell lines. Oncogene 1996;12:1097–1107.
   PubMed Web of Science ®Google Scholar
• Schweighoffer F, Faure M, Fath I, et al. Identification of a human guanine nucleotide-releasing factor (H-GRF55) specific for Ras proteins. Oncogene 1993;8:1477–1485.
   PubMed Web of Science ®Google Scholar
• Baouz S, Jacquet E, Bernardi A, et al. The N-terminal moiety of CDC25(Mm), a GDP/GTP exchange factor of Ras proteins, controls the activity of the catalytic domain. Modulation by calmodulin and calpain. J Biol Chem 1997;272:6671–6676.
   PubMed Web of Science ®Google Scholar
• Leaner VD, Donninger H, Ellis CA, et al. p75-Ras-GRF1 is a c-Jun/AP-1 target protein: its up regulation results in increased Ras activity and is necessary for c-Jun-induced nonadherent growth of Rat1a cells. Mol Cell Biol 2005;25:3324–3337.
   PubMedGoogle Scholar
• Cen H, Papageorge AG, Vass WC, et al. Regulated and constitutive activity by CDC25Mm (GRF), a Ras-specific exchange factor. Mol Cell Biol 1993;13:7718–7724.
   PubMed Web of Science ®Google Scholar
• Mattingly RR, Macara IG. Phosphorylation-dependent activation of the Ras-GRF/CDC25Mm exchange factor by muscarinic receptors and G-protein beta gamma subunits. Nature 1996;382:268–272.
   PubMed Web of Science ®Google Scholar
• Baouz S, Jacquet E, Accorsi K, et al. Sites of phosphorylation by protein kinase A in CDC25Mm/GRF1, a guanine nucleotide exchange factor for Ras. J Biol Chem 2001;276:1742–1749.
   PubMed Web of Science ®Google Scholar
• Veldurthy A, Patz M, Hagist S, et al. The kinase inhibitor dasatinib induces apoptosis in chronic lymphocytic leukemia cells in vitro with preference for a subgroup of patients with unmutated IgVH genes. Blood 2008;112:1443–1452.
   PubMed Web of Science ®Google Scholar
• McCaig AM, Cosimo E, Leach MT, et al. Dasatinib inhibits CXCR4 signaling in chronic lymphocytic leukaemia cells and impairs migration towards CXCL12. PLoS One 2012;7:e48929.
   PubMed Web of Science ®Google Scholar
• de Rooij MF, Kuil A, Geest CR, et al. The clinically active BTK inhibitor PCI-32765 targets B-cell receptor- and chemokine-controlled adhesion and migration in chronic lymphocytic leukemia. Blood 2012;119:2590–2594.
   PubMed Web of Science ®Google Scholar
• Falt S, Merup M, Gahrton G, et al. Identification of progression markers in B-CLL by gene expression profiling. Exp Hematol 2005;33:883–893.
   PubMed Web of Science ®Google Scholar
• Haslinger C, Schweifer N, Stilgenbauer S, et al. Microarray gene expression profiling of B-cell chronic lymphocytic leukemia subgroups defined by genomic aberrations and VH mutation status. J Clin Oncol 2004;22:3937–3949.
   PubMed Web of Science ®Google Scholar
• Jelinek DF, Tschumper RC, Stolovitzky GA, et al. Identification of a global gene expression signature of B-chronic lymphocytic leukemia. Mol Cancer Res 2003;1:346–361.
   PubMed Web of Science ®Google Scholar
• Basso K, Margolin AA, Stolovitzky G, et al. Reverse engineering of regulatory networks in human B cells. Nat Genet 2005;37:382–390.
   PubMed Web of Science ®Google Scholar
• Haferlach T, Kohlmann A, Wieczorek L et al. Clinical utility of microarray-based gene expression profiling in the diagnosis and subclassification of leukemia: report from the International Microarray Innovations in Leukemia Study Group. J Clin Oncol 2010;28:2529–2537.
   PubMed Web of Science ®Google Scholar
• Soo C, Hu FY, Zhang X, et al. Differential expression of fibromodulin, a transforming growth factor-beta modulator, in fetal skin development and scarless repair. Am J Pathol 2000;157:423–433.
   PubMed Web of Science ®Google Scholar
• Choudhury A, Derkow K, Daneshmanesh AH, et al. Silencing of ROR1 and FMOD with siRNA results in apoptosis of CLL cells. Br J Haematol 2010;151:327–335.
   PubMed Web of Science ®Google Scholar
• Jordaan G, Liao W, Sharma S. E-cadherin gene re-expression in chronic lymphocytic leukemia cells by HDAC inhibitors. BMC Cancer 2013;13:88.
   PubMed Web of Science ®Google Scholar
• Calvo F, Crespo P. Structural and spatial determinants regulating TC21 activation by RasGRF family nucleotide exchange factors. Mol Biol Cell 2009;20:4289–4302.
   PubMed Web of Science ®Google Scholar
• Tarnowski M, Schneider G, Amann G, et al. RasGRF1 regulates proliferation and metastatic behavior of human alveolar rhabdomyosarcomas. Int J Oncol 2012;41:995–1004.
   PubMed Web of Science ®Google Scholar
• Yoon B, Herman H, Hu B, et al. Rasgrf1 imprinting is regulated by a CTCF-dependent methylation-sensitive enhancer blocker. Mol Cell Biol 2005;25:11184–11190.
   PubMed Web of Science ®Google Scholar
• Zhu TN, He HJ, Kole S, et al. Filamin A-mediated down-regulation of the exchange factor Ras-GRF1 correlates with decreased matrix metalloproteinase-9 expression in human melanoma cells. J Biol Chem 2007;282:14816–14826.
   PubMed Web of Science ®Google Scholar
• Coccetti P, Mauri I, Alberghina L, et al. The minimal active domain of the mouse ras exchange factor CDC25Mm. Biochem Biophys Res Commun 1995;206:253–259.
   PubMed Web of Science ®Google Scholar
• Limnander A, Depeille P, Freedman TS, et al. STIM1, PKC-delta and RasGRP set a threshold for proapoptotic Erk signaling during B cell development. Nat Immunol 2011;12:425–433.
   PubMed Web of Science ®Google Scholar
• Pepper C, Thomas A, Hoy T, et al. The vitamin D3 analog EB1089 induces apoptosis via a p53-independent mechanism involving p38 MAP kinase activation and suppression of ERK activity in B-cell chronic lymphocytic leukemia cells in vitro. Blood 2003;101:2454–2460.
   PubMed Web of Science ®Google Scholar
• Richardson SJ, Matthews C, Catherwood MA, et al. ZAP-70 expression is associated with enhanced ability to respond to migratory and survival signals in B-cell chronic lymphocytic leukemia (B-CLL). Blood 2006;107:3584–3592.
   PubMed Web of Science ®Google Scholar
• Rossman KL, Der CJ, Sondek J. GEF means go:turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 2005;6:167–180.
   PubMed Web of Science ®Google Scholar
• Crespo P, Schuebel KE, Ostrom AA, et al. Phosphotyrosine-dependent activation of Rac-1 GDP/GTP exchange by the vav proto-oncogene product. Nature 1997;385:169–172.
   PubMed Web of Science ®Google Scholar
• Kiyono M, Kaziro Y, Satoh T. Induction of rac-guanine nucleotide exchange activity of Ras-GRF1/CDC25(Mm) following phosphorylation by the nonreceptor tyrosine kinase Src. J Biol Chem 2000;275:5441–5446.
   PubMed Web of Science ®Google Scholar
• Browett PJ, Ganeshaguru K, Hoffbrand AV, et al. Absence of Kirsten-ras oncogene activation in B-cell chronic lymphocytic leukemia. Leuk Res 1988;12:25–31.
   PubMed Web of Science ®Google Scholar