507
Views
21
CrossRef citations to date
0
Altmetric
Reviews

Targeting cAMP in chronic lymphocytic leukemia: a pathway-dependent approach for the treatment of leukemia and lymphoma

, PhD & , MD
Pages 937-949 | Published online: 07 May 2013

Bibliography

  • Gaidano G, Foa R, Dalla-Favera R. Molecular pathogenesis of chronic lymphocytic leukemia. J Clin Invest 2012;122:3432-8
  • Hallek M, Cheson BD, Catovsky D, et al. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute-Working Group 1996 guidelines. Blood 2008;111:5446-56
  • Ma S, Rosen ST. Signal transduction inhibitors in chronic lymphocytic leukemia. Curr Opin Oncol 2011;23:601-8
  • Balakrishnan K, Gandhi V. Protein kinases: emerging therapeutic targets in chronic lymphocytic leukemia. Expert Opin Invest Drug 2012;21:409-23
  • Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004;305:626-9
  • Falschlehner C, Schaefer U, Walczak H. Following TRAIL's path in the immune system. Immunology 2009;127:145-54
  • Packham G, Stevenson FK. Bodyguards and assassins: Bcl-2 family proteins and apoptosis control in chronic lymphocytic leukaemia. Immunology 2005;114:441-9
  • Kitada S, Andersen J, Akar S, et al. Expression of apoptosis-regulating proteins in chronic lymphocytic leukemia: correlations with in vitro and in vivo chemoresponses. Blood 1998;91:3379-89
  • McConkey DJ, Chandra J, Wright S, et al. Apoptosis sensitivity in chronic lymphocytic leukemia is determined by endogenous endonuclease content and relative expression of Bcl-2 and BAX. J Immunol 1996;156:2624-30
  • Petlickovski A, Laurenti L, Li X, et al. Sustained signaling through the B-cell receptor induces Mcl-1 and promotes survival of chronic lymphocytic leukemia B cells. Blood 2005;105:4820-7
  • Cimmino A, Calin GA, Fabbri M, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Nat Acad Sci USA 2005;102:13944-9
  • Calin GA, Dumitru CD, Shimizu M, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Nat Acad Sci USA 2002;99:15524-9
  • Daniel V, Litwack G, Tomkins GM. Induction of cytolysis of cultured lymphoma cells by adenosine 3':5'-cyclic monophosphate and the isolation of resistant variants. Proc Natl Acad Sci USA 1973;70:76-9
  • Insel PA, Bourne HR, Coffino P, et al. Cyclic AMP-dependent protein kinase: pivotal role in regulation of enzyme induction and growth. Science 1975;190:896-8
  • Mentz F, Merle-Beral H, Ouaaz F, et al. Theophylline, a new inducer of apoptosis in B-CLL: role of cyclic nucleotides. Br J Haematol 1995;90:957-9
  • Kim DH, Lerner A. Type 4 cyclic adenosine monophosphate phosphodiesterase as a therapeutic target in chronic lymphocytic leukemia. Blood 1998;92:2484-94
  • Ogawa R, Streiff MB, Bugayenko A, et al. Inhibition of PDE4 phosphodiesterase activity induces growth suppression, apoptosis, glucocorticoid sensitivity, p53, and p21(WAF1/CIP1) proteins in human acute lymphoblastic leukemia cells. Blood 2002;99:3390-7
  • Smith PG, Wang F, Wilkinson KN, et al. The phosphodiesterase PDE4B limits cAMP-associated PI3K/AKT-dependent apoptosis in diffuse large B-cell lymphoma. Blood 2005;105:308-16
  • Insel PA, Zhang L, Murray F, et al. Cyclic AMP is both a pro-apoptotic and anti-apoptotic second messenger. Acta Physiol (Oxf) 2012;204:277-87
  • Tasken K, Andersson KB, Erikstein BK, et al. Regulation of growth in a neoplastic B cell line by transfected subunits of 3',5'-cyclic adenosine monophosphate-dependent protein kinase. Endocrinology 1994;135:2109-19
  • Zhang L, Insel PA. The pro-apoptotic protein Bim is a convergence point for cAMP/protein kinase A- and glucocorticoid-promoted apoptosis of lymphoid cells. J Biol Chem 2004;279:20858-65
  • Ji Z, Mei FC, Miller AL, et al. Protein kinase A (PKA) isoform RIIbeta mediates the synergistic killing effect of cAMP and glucocorticoid in acute lymphoblastic leukemia cells. J Biol Chem 2008;283:21920-5
  • Dong H, Zitt C, Auriga C, et al. Inhibition of PDE3, PDE4 and PDE7 potentiates glucocorticoid-induced apoptosis and overcomes glucocorticoid resistance in CEM T leukemic cells. Biochem Pharmacol 2010;79:321-9
  • Tiwari S, Dong H, Kim EJ, et al. Type 4 cAMP phosphodiesterase (PDE4) inhibitors augment glucocorticoid-mediated apoptosis in B cell chronic lymphocytic leukemia (B-CLL) in the absence of exogenous adenylyl cyclase stimulation. Biochem Pharmacol 2005;69:473-83
  • Meyers JA, Taverna J, Chaves J, et al. Phosphodiesterase 4 inhibitors augment levels of glucocorticoid receptor in B cell chronic lymphocytic leukemia but not in normal circulating hematopoietic cells. Clin Cancer Res 2007;13:4920-7
  • van Daalen Wetters T, Coffino P. Cultured S49 mouse T lymphoma cells. Methods Enzymol 1987;151:9-19
  • Bourne HR, Coffino P, Tomkins GM. Selection of a variant lymphoma cell deficient in adenylate cyclase. Science 1975;187:750-2
  • Coffino P, Bourne HR, Tomkins GM. Somatic genetic analysis of cyclic AMP action: selection of unresponsive mutants. J Cell Physiol 1975;85:603-10
  • Sibley CH, Yamamoto KR. Mouse lymphoma cells: mechanisms of resistance to glucocorticoids. Monogr Endocrinol 1979;12:357-76
  • Ross EM, Howlett AC, Ferguson KM, et al. Reconstitution of hormone-sensitive adenylate cyclase activity with resolved components of the enzyme. J Biol Chem 1978;253:6401-12
  • Gilman AG. Silver spoons and other personal reflections. Annu Rev Pharmacol Toxicol 2012;52:1-19
  • Albert DA. The effect of cyclic-AMP on the regulation of c-myc expression in T lymphoma cells. J Clin Invest 1995;95:1490-6
  • Honeysett JM, Insel PA. Inhibition of ornithine decarboxylase and S-adenosylmethionine decarboxylase activities of S49 lymphoma cells by agents increasing cyclic AMP. J Cyclic Nucleotide Res 1981;7:321-32
  • Lemaire I, Coffino P. Cyclic AMP-induced cytolysis in S49 cells: selection of an unresponsive "deathless" mutant. Cell 1977;11:149-55
  • Hughes RJ, Howard MJ, Allen JM, et al. Decreased beta 2-adrenergic receptor mRNA expression in receptor-deficient S49 lymphoma cells. Mol Pharmacol 1991;40:974-9
  • Johnson GL, Bourne HR, Gleason MK, et al. Isolation and characterization of S49 lymphoma cells deficient in beta-adrenergic receptors: relation of receptor number to activation of adenylate cyclase. Mol Pharmacol 1979;15:16-27
  • Bourne HR, Brothers VM, Kaslow HR, et al. Genetic analysis of cyclic nucleotide phosphodiesterases in S49 mouse lymphoma cells. Adv Cyclic Nucleotide Protein Phosphorylation Res 1984;16:185-94
  • Haga T, Ross EM, Anderson HJ, et al. Adenylate cyclase permanently uncoupled from hormone receptors in a novel variant of S49 mouse lymphoma cells. Proc Natl Acad Sci USA 1977;74:2016-20
  • Zambon AC, Zhang L, Minovitsky S, et al. Gene expression patterns define key transcriptional events in cell-cycle regulation by cAMP and protein kinase A. Proc Natl Acad Sci USA 2005;102:8561-6
  • Zhang L, Insel PA. Bcl-2 protects lymphoma cells from apoptosis but not growth arrest promoted by cAMP and dexamethasone. Am J Physiol Cell Physiol 2001;281:C1642-7
  • Zhang L, Zambon AC, Vranizan K, et al. Gene expression signatures of cAMP/protein kinase A (PKA)-promoted, mitochondrial-dependent apoptosis. Comparative analysis of wild-type and cAMP-deathless S49 lymphoma cells. J Biol Chem 2008;283:4304-13
  • Guo Y, Wilderman A, Zhang L, et al. Quantitative proteomics analysis of the cAMP/protein kinase A signaling pathway. Biochemistry 2012;51:9323-32
  • Zambon AC, Wilderman A, Ho A, et al. Increased expression of the pro-apoptotic protein BIM, a mechanism for cAMP/protein kinase A (PKA)-induced apoptosis of immature T cells. J Biol Chem 2011;286:33260-7
  • Zhang L, Yun H, Murray F, et al. Cytotoxic T lymphocyte antigen-2 alpha induces apoptosis of murine T-lymphoma cells and cardiac fibroblasts and is regulated by cAMP/PKA. Cell Signal 2011;23:1611-16
  • Mentz F, Mossalayi MD, Ouaaz F, et al. Theophylline synergizes with chlorambucil in inducing apoptosis of B-chronic lymphocytic leukemia cells. Blood 1996;88:2172-82
  • Monahan TM, Marchand NW, Fritz RR, et al. Cyclic adenosine 3':5'-monophosphate levels and activities of related enzymes in normal and leukemic lymphocytes. Cancer Res 1975;35(9):2540-7
  • Samuel E, Chung C, Scher N, et al. Protein kinases in chronic lymphocytic leukemia. Blood 1980;55:618-24
  • Overington JP, Al-Lazikani B, Hopkins AL. How many drug targets are there? Nat Rev Drug Discov 2006;5:993-6
  • Insel PA, Snead A, Murray F, et al. GPCR expression in tissues and cells: are the optimal receptors being used as drug targets? Br J Pharmacol 2012;165:1613-16
  • Frey UH, Nuckel H, Sellmann L, et al. The GNAS1 T393C polymorphism is associated with disease progression and survival in chronic lymphocytic leukemia. Clin Cancer Res 2006;12:5686-92
  • Kaderi MA, Murray F, Jansson M, et al. The GNAS1 T393C polymorphism and lack of clinical prognostic value in chronic lymphocytic leukemia. Leuk Res 2008;32:984-7
  • Nuckel H, Frey U, Aralh N, et al. The CC genotype of the C825T polymorphism of the G protein beta3 gene (GNB3) is associated with a high relapse rate in patients with chronic lymphocytic leukaemia. Leuk Lymphoma 2003;44:1739-43
  • Burger JA. Nurture versus nature: the microenvironment in chronic lymphocytic leukemia. Hematol Am Soc Hematol Educ Program 2011;2011:96-103
  • Drost AC, Seitz G, Boehmler A, et al. The G protein-coupled receptor CysLT1 mediates chemokine-like effects and prolongs survival in chronic lymphocytic leukemia. Leuk Lymphoma 2012;53:665-73
  • Burger JA, Burger M, Kipps TJ. Chronic lymphocytic leukemia B cells express functional CXCR4 chemokine receptors that mediate spontaneous migration beneath bone marrow stromal cells. Blood 1999;94:3658-67
  • Cuesta-Mateos C, Lopez-Giral S, Alfonso-Perez M, et al. Analysis of migratory and prosurvival pathways induced by the homeostatic chemokines CCL19 and CCL21 in B-cell chronic lymphocytic leukemia. Exp Hematol 2010;38:756-64; 64 e1-4
  • Ferretti E, Bertolotto M, Deaglio S, et al. A novel role of the CX3CR1/CX3CL1 system in the cross-talk between chronic lymphocytic leukemia cells and tumor microenvironment. Leukemia 2011;25:1268-77
  • Jones D, Benjamin RJ, Shahsafaei A, et al. The chemokine receptor CXCR3 is expressed in a subset of B-cell lymphomas and is a marker of B-cell chronic lymphocytic leukemia. Blood 2000;95:627-32
  • Mahadevan D, Choi J, Cooke L, et al. Gene expression and serum cytokine profiling of low stage CLL identify WNT/PCP, Flt-3L/Flt-3 and CXCL9/CXCR3 as regulators of cell proliferation, survival and migration. Hum Genomics Proteomics 2009;1:453634
  • Wong S, Fulcher D. Chemokine receptor expression in B-cell lymphoproliferative disorders. Leuk Lymphoma 2004;45:2491-6
  • 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;96:2655-63
  • Burger M, Hartmann T, Krome M, et al. Small peptide inhibitors of the CXCR4 chemokine receptor (CD184) antagonize the activation, migration, and antiapoptotic responses of CXCL12 in chronic lymphocytic leukemia B cells. Blood 2005;106:1824-30
  • Burkle A, Niedermeier M, Schmitt-Graff A, et al. Overexpression of the CXCR5 chemokine receptor, and its ligand, CXCL13 in B-cell chronic lymphocytic leukemia. Blood 2007;110:3316-25
  • Mamani-Matsuda M, Moynet D, Molimard M, et al. Long-acting beta2-adrenergic formoterol and salmeterol induce the apoptosis of B-chronic lymphocytic leukaemia cells. Br J Haematol 2004;124:141-50
  • Kamp T, Liebl B, Haen E, et al. Defects of beta 2-adrenergic signal transduction in chronic lymphocytic leukaemia: relationship to disease progression. Eur J Clin Invest 1997;27:121-7
  • Mentz F, Merle-Beral H, Dalloul AH. Theophylline-induced B-CLL apoptosis is partly dependent on cyclic AMP production but independent of CD38 expression and endogenous IL-10 production. Leukemia 1999;13:78-84
  • Ostrom RS, Post SR, Insel PA. Stoichiometry and compartmentation in G protein-coupled receptor signaling: implications for therapeutic interventions involving G(s). J Pharmacol Exp Ther 2000;294:407-12
  • Meyers JA, Su DW, Lerner A. Chronic lymphocytic leukemia and B and T cells differ in their response to cyclic nucleotide phosphodiesterase inhibitors. J Immunol 2009;182:5400-11
  • Carpentieri U, Minguell JJ, Gardner FH. Adenylate cyclase and guanylate cyclase activity in normal and leukemic human lymphocytes. Blood 1981;57:975-8
  • Mendelsohn J, Nordberg J. Adenylate cyclase in thymus-derived and bone marrow-derived lymphocytes from normal donors and patients with chronic lymphocytic leukemia. J Clin Invest 1979;63:1124-32
  • Gao MH, Hammond HK. Unanticipated signaling events associated with cardiac adenylyl cyclase gene transfer. J Mol Cell Cardiol 2011;50:751-8
  • Mabed M, Aref S, Fouda M, et al. Chlorambucil plus theophylline vs chlorambucil alone as a front line therapy for B-cell chronic lymphatic leukemia. Leuk Lymphoma 2004;45:2029-35
  • Willis CR, Goodrich A, Park K, et al. A phase I/II study examining pentostatin, chlorambucil, and theophylline in patients with relapsed chronic lymphocytic leukemia and non-Hodgkin's lymphoma. Ann Hematol 2006;85:301-7
  • Wiernik PH, Paietta E, Goloubeva O, et al. Phase II study of theophylline in chronic lymphocytic leukemia: a study of the Eastern Cooperative Oncology Group (E4998). Leukemia 2004;18:1605-10
  • Moon EY, Lerner A. PDE4 inhibitors activate a mitochondrial apoptotic pathway in chronic lymphocytic leukemia cells that is regulated by protein phosphatase 2A. Blood 2003;101:4122-30
  • Zhang L, Murray F, Zahno A, et al. Cyclic nucleotide phosphodiesterase profiling reveals increased expression of phosphodiesterase 7B in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2008;105:19532-7
  • Moon E, Lee R, Near R, et al. Inhibition of PDE3B augments PDE4 inhibitor-induced apoptosis in a subset of patients with chronic lymphocytic leukemia. Clin Cancer Res 2002;8:589-95
  • Houslay MD. Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem Sci 2010;35:91-100
  • Page CP, Spina D. Selective PDE inhibitors as novel treatments for respiratory diseases. Curr Opin Pharmacol 2012;12:275-86
  • Schett G, Sloan VS, et al. Apremilast: a novel PDE4 inhibitor in the treatment of autoimmune and inflammatory diseases. Ther Adv Musculoskelet Dis 2010;2:271-8
  • Lee R, Wolda S, Moon E, et al. PDE7A is expressed in human B-lymphocytes and is up-regulated by elevation of intracellular cAMP. Cell Signal 2002;14:277-84
  • Bloom TJ, Beavo JA. Identification and tissue-specific expression of PDE7 phosphodiesterase splice variants. Proc Natl Acad Sci USA 1996;93:14188-92
  • Gantner F, Gotz C, et al. Phosphodiesterase profile of human B lymphocytes from normal and atopic donors and the effects of PDE inhibition on B cell proliferation. Br J Pharmacol 1998;123:1031-8
  • Peiro AM, Tang CM, Murray F, et al. Genetic variation in phosphodiesterase (PDE) 7B in chronic lymphocytic leukemia: overview of genetic variants of cyclic nucleotide PDEs in human disease. J Hum Genet 2011;56:676-81
  • Zhang L, Murray F, Rassenti LZ, et al. Cyclic nucleotide phosphodiesterase 7B mRNA: an unfavorable characteristic in chronic lymphocytic leukemia. Int J Cancer 2011;129:1162-9
  • Tiwari S, Felekkis K, Moon EY, et al. Among circulating hematopoietic cells, B-CLL uniquely expresses functional EPAC1, but EPAC1-mediated Rap1 activation does not account for PDE4 inhibitor-induced apoptosis. Blood 2004;103:2661-7
  • Mantovani G, Bondioni S, Lania AG, et al. High expression of PKA regulatory subunit 1A protein is related to proliferation of human melanoma cells. Oncogene 2008;27:1834-43
  • Mantovani G, Lania AG, Bondioni S, et al. Different expression of protein kinase A (PKA) regulatory subunits in cortisol-secreting adrenocortical tumors: relationship with cell proliferation. Exp Cell Res 2008;314:123-30
  • Grandoch M, Roscioni SS, Schmidt M. The role of Epac proteins, novel cAMP mediators, in the regulation of immune, lung and neuronal function. Br J Pharmacol 2010;159:265-84
  • Klein U, Tu Y, Stolovitzky GA, et al. Gene expression profiling of B cell chronic lymphocytic leukemia reveals a homogeneous phenotype related to memory B cells. J Exp Med 2001;194:1625-38
  • Grandoch M, Lopez de Jesus M, Oude Weernink PA, et al. B cell receptor-induced growth arrest and apoptosis in WEHI-231 immature B lymphoma cells involve cyclic AMP and Epac proteins. Cell Signal 2009;21:609-21
  • 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;111:846-55
  • Raymond DR, Wilson LS, Carter RL, et al. Numerous distinct PKA-, or EPAC-based, signalling complexes allow selective phosphodiesterase 3 and phosphodiesterase 4 coordination of cell adhesion. Cell Signal 2007;19:2507-18
  • Almahariq M, Tsalkova T, Mei FC, et al. A novel EPAC-specific inhibitor suppresses pancreatic cancer cell migration and invasion. Mol Pharmacol 2013;83:122-8
  • Courilleau D, Bisserier M, Jullian JC, et al. Identification of a tetrahydroquinoline analog as a pharmacological inhibitor of the cAMP-binding protein Epac. J Biol Chem 2012;287:44192-202
  • Calin GA, Croce CM. Chronic lymphocytic leukemia: interplay between noncoding RNAs and protein-coding genes. Blood 2009;114:4761-70
  • Stangherlin A, Zaccolo M. Phosphodiesterases and subcellular compartmentalized cAMP signaling in the cardiovascular system. Am J Physiol Heart Circ Physiol 2012;302:H379-90
  • Yamamoto S, Sugahara S, Ikeda K, et al. Amelioration of collagen-induced arthritis in mice by a novel phosphodiesterase 7 and 4 dual inhibitor, YM-393059. Eur J Pharmacol 2007;559:219-26
  • Copsel S, Garcia C, Diez F, et al. Multidrug resistance protein 4 (MRP4/ABCC4) regulates cAMP cellular levels and controls human leukemia cell proliferation and differentiation. J Biol Chem 2011;286:6979-88
  • Regard JB, Sato IT, Coughlin SR. Anatomical profiling of G protein-coupled receptor expression. Cell 2008;135:561-71

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.