Activation of the cAMP signaling pathway increases apoptosis in human B- precursor cells and is associated with downregulation of Mcl-1 expression

Journal of Cellular Physiology

Volumn 180, Issue 1, 1999, Pages 71-80

  Myklebust, June Helen ^a   Josefsen, Dag ^a   Blomhoff, Heidi Kiil ^b   Levy, Finn Olav ^b   Naderi, Soheil ^b   Reed, John C ^c   Smeland, Erlend B ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; HUMAN; HUMAN CELL; LYMPHOPOIESIS; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ADULT; APOPTOSIS; B-LYMPHOCYTES; BONE MARROW CELLS; CD40 LIGAND; CELL DIFFERENTIATION; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOWN-REGULATION; ENZYME INHIBITORS; FLOW CYTOMETRY; FORSKOLIN; HEMATOPOIETIC STEM CELLS; HUMANS; ILIUM; INTERLEUKIN-4; MEMBRANE GLYCOPROTEINS; NEOPLASM PROTEINS; NEPRILYSIN; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; THIONUCLEOTIDES;

EID: 0032968198     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199907)180:1<71::AID-JCP8>3.0.CO;2-N     Document Type: Article

References (56)

1. Afan AM, Broome CS, Nicholls SE, Whetton AD, Miyan JA. 1997. Bone marrow innervation regulates cellular retention in the murine haemopoietic system. Br J Haematol 98:569-577.
2. Anderson KL, Anderson G, Michell RH, Jenkinson EJ, Owen JJ. 1996. Intracellular signaling pathways involved in the induction of apoptosis in immature thymic T lymphocytes. J Immunol 156:4083-4091.
3. Beebe SJ. 1994. The cAMP-dependent protein kinases and cAMP signal transduction Semin Cancer Biol 5:285-294.
4. Benestad HB, Strom-Gundersen I, Iversen PO, Haug E, Nja A. 1998. No neuronal regulation of murine bone marrow function. Blood 91:1280-1287.
5. Blomhoff HK, Smeland EB, Beiske K, Blomhoff R, Ruud E, Bjoro T, Pfeifer-Ohlsson S, Watt R, Funderud S, Godal T, Ohlsson R. 1987. Cyclic AMP-mediated suppression of normal and neoplastic B cell proliferation is associated with regulation of myc and Ha-ras protooncogenes. J Cell Physiol 131:426-433.
6. Brown DM, Phipps RP. 1995. Characterization and regulation of prostaglandin E2 receptors on normal and malignant murine B lymphocytes. Cell Immunol 161:79-87.
7. Brown DM, Phipps RP. 1996. Bcl-2 expression inhibits prostaglandin E2-mediated apoptosis in B cell lymphomas. J Immunol 157:1359-1370.
8. Chao DT, Korsmeyer SJ. 1998. BCL-2 family: regulators of cell death. Annu Rev Immunol 16:395-419.
9. Chao JR, Wang JM, Lee SF, Peng HW, Lin YH, Chou CH, Li JC, Huang HM, Chou CK, Kuo ML, Yen JJ, Yang-Yen HF. 1998. mcl-1 is an immediate-early gene activated by the granulocyte-macrophage colony-stimulating factor (GM-CSF) signaling pathway and is one component of the GM-CSF viability response. Mol Cell Biol 18:4883-4898.
10. de Rooij J, Zwartkruis FJ, Verheijen MH, Cool RH, Nijman SM, Wittinghofer A, Bos JL. 1998. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396:474-477.
11. DiFrancesco D, Tortora P. 1991. Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 351:145-147.
12. Døskeland SO, Bøe R, Bruland T, Vintermyr OK, Jastorff B, Lanotte M. 1991. Criteria used to judge that a cellular response is mediated by cAMP. In: Reid E, Cook GMW, Luzio JP, editors. Cell signalling: experimental strategies. Cambridge: Royal Society of Chemistry. p 103-114.
13. Fedyk ER, Phipps RP. 1996. Prostaglandin E2 receptors of the EP2 and EP4 subtypes regulate activation and differentiation of mouse B lymphocytes to IgE-secreting cells. Proc Natl Acad Sci USA 93: 10978-10983.
14. Fedyk ER, Ripper JM, Brown DM, Phipps RP. 1996. A molecular analysis of PGE receptor (EP) expression on normal and transformed B lymphocytes: coexpression of EP1, EP2, EP3beta and EP4. Mol Immunol 33:33-45.
15. Felten SY, Madden KS, Bellinger DL, Kruszewska B, Moynihan JA, Felten DL. 1998. The role of the sympathetic nervous system in the modulation of immune responses. Adv Pharmacol 42:583-587.
16. Gibson LF, Piktel D, Narayanan R, Nunez G, Landreth KS. 1996. Stromal cells regulate bcl-2 and bax expression in pro-B cells. Exp Hematol 24:628-637.
17. Gjertsen BT, Mellgren G, Otten A, Maronde E, Genieser HG, Jastorff B, Vintermyr OK, McKnight GS, Døskeland SO. 1995. Novel (Rp)-cAMPS analogs as tools for inhibition of cAMP-kinase in cell culture. Basal cAMP-kinase activity modulates interleukin-1 beta action. J Biol Chem 270:20599-20607.
18. Grillot DA, Merino R, Pena JC, Fanslow WC, Finkelman FD, Thompson CB, Nunez G. 1996. bcl-x exhibits regulated expression during B cell development and activation and modulates lymphocyte survival in transgenic mice. J Exp Med 183:381-391.
19. Kaufmann SH, Karp JE, Svingen PA, Krajewski S, Burke PJ, Gore SD, Reed JC. 1998. Elevated expression of the apoptotic regulator Mcl-1 at the time of leukemic relapse. Blood 91:991-1000.
20. Kitada S, Andersen J, Akar S, Zapata JM, Takayama S, Krajewski S, Wang HG, Zhang X, Bullrich F, Croce CM, Rai K, Hines J, Reed JC. 1998. Expression of apoptosis-regulating proteins in chronic lymphocytic leukemia: correlations with in vitro and in vivo chemoreaponses. Blood 91:3379-3389.
21. Krajewski S, Bodrug S, Gascoyne R, Berean K, Krajewska M, Reed JC. 1994. Immunohistochemical analysis of Mcl-1 and Bcl-2 proteins in normal and neoplastic lymph nodes. Am J Pathol 145:515-525.
22. Krajewski S, Bodrug S, Krajewska M, Shabaik A, Gascoyne R, Berean K, Reed JC. 1995. Immunohistochemical analysis of Mcl-1 protein in human tissues. Differential regulation of Mcl-1 and Bcl-2 protein production suggests a unique role for Mcl-1 in control of programmed cell death in vivo. Am J Pathol 146:1309-1319.
23. Krupinski J. 1991. The adenylyl cyclase family. Mol Cell Biochem 104:73-79.
24. Lalli E, Sassone-Corsi P, Ceredig R. 1996. Block of T lymphocyte differentiation by activation of the cAMP-dependent signal transduction pathway. EMBO J 15:528-537.
25. Levitzki A. 1988. From epinephrine to cyclic AMP. Science 241:800-806.
26. Levy FO, Rasmussen AM, Tasken K, Skalhegg BS, Huitfeldt HS, Funderud S, Smeland EB, Hansson V. 1996. Cyclic AMP-dependent protein kinase (cAK) in human B cells: co-localization of type I cAK (RI alpha 2 C2) with the antigen receptor during anti-immunoglobulin-induced B cell activation. Eur J Immunol 26:1290-1296.
27. Li L, Krajewski S, Reed JC, Choi YS. 1997. The apoptosis and proliferation of SAC-activated B cells by IL-10 are associated with changes in Bcl-2, Bcl-xL, and Mcl-1 expression. Cell Immunol 178: 33-41.
28. Lømo J, Blomhoff HK, Beiske K, Stokke T, Smeland EB. 1995. TGF-beta 1 and cyclic AMP promote apoptosis in resting human B lymphocytes. J Immunol 154:1634-1643.
29. Lømo J, Smeland EB, Krajewski S, Reed JC, Blomhoff HK. 1996. Expression of the Bcl-2 homologue Mcl-1 correlates with survival of peripheral blood B lymphocytes. Cancer Res 56:40-43.
30. Lømo J, Blomhoff HK, Jacobsen SE, Krajewski S, Reed JC, Smeland EB. 1997. Interleukin-13 in combination with CD40 ligand potently inhibits apoptosis in human B lymphocytes: upregulation of Bcl-xL and Mcl-1. Blood 89:4415-4424.
31. Lu L, Osmond DG. 1997. Apoptosis during B lymphopoiesis in mouse bone marrow. J Immunol 158:5136-5145.
32. McConkey DJ, Orrenius S, Jondal M. 1990. Agents that elevate cAMP stimulate DNA fragmentation in thymocytes. J Immunol 145:1227-1230.
33. Mentz F, Mossalayi MD, Ouaaz F, Debre P. 1995. Involvement of cAMP in CD3 T cell receptor complex-and CD2-mediated apoptosis of human thymocytes. Eur J Immunol 25:1798-1801.
34. Moulding DA, Quayle JA, Hart CA, Edwards SW. 1998. Mcl-1 expression in human neutrophils: regulation by cytokines and correlation with cell survival. Blood 92:2495-2502.
35. Muraguchi A, Miyazaki K, Kehrl JH, Fauci AS. 1984. Inhibition of human B cell activation by diterpine forskolin: interference with B cell growth factor-induced G1 to S transition of the B cell cycle. J Immunol 133:1283-1287.
36. Nakamura T, Gold GH. 1987. A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325:442-444.
37. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F, Riccardi C. 1991. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 139:271-279.
38. Nossal G.J. 1994. Negative selection of lymphocytes. Cell 76:229-239.
39. Nunez G, Merino R, Grillot D, Gonzalez-Garcia M. 1994. Bcl-2 and Bcl-x: regulatory switches for lymphoid death and survival. Immunol Today 15:582-588.
40. Opstelten D, Osmond DG. 1983. Pre-B cells in mouse bone marrow: immunofluorescence stathmokinetic studies of the proliferation of cytoplasmic mu-chain-bearing cells in normal mice. J Immunol 131:2635-2640.
41. Osmond DG. 1990. B cell development in the bone marrow. Semin Immunol 2:173-180.
42. Rasmussen AM, Smeland EB, Erikstein BK, Caignault L, Funderud S. 1992. A new method for detachment of Dynabeads from positively selected B lymphocytes. J Immunol Methods 146:195-202.
43. Rolink A, Melchers F. 1991. Molecular and cellular origins of B lymphocyte diversity. Cell 66:1081-1094.
44. Rothenberg EV. 1992. The development of functionally responsive T cells. Adv Immunol 51:117-139, 165-177.
45. Rothermel JD, Stec WJ, Baraniak J, Jastorff B, Botelho LH. 1983. Inhibition of glycogenolysis in isolated rat hepatocytes by the Rp diastereomer of adenosine cyclic 3′,5′-phosphorothioate. J Biol Chem 258:12125-12128.
46. Schneider TJ, Grillot D, Foote LC, Nunez GE, Rothstein TL. 1997. Bcl-x protects primary B cells against Fas-mediated apoptosis. J Immunol 159:4834-4839.
47. Scott JD. 1991. Cyclic nucleotide-dependent protein kinases. Pharmacol Ther 50:123-145.
48. Skalhegg BS, Landmark BF, Doskeland SO, Hansson V, Lea T, Jahnsen T. 1992. Cyclic AMP-dependent protein kinase type I mediates the inhibitory effects of 3′,5′-cyclic adenosine monophosphate on cell replication in human T lymphocytes. J Biol Chem 267:15707-15714.
49. Skalhegg BS, Tasken K, Hansson V, Huitfeldt HS, Jahnsen T, Lea T. 1994. Location of cAMP-dependent protein kinase type I with the TCR-CD3 complex. Science 263:84-87.
50. Smeland EB, Funderud S, Kvalheim G, Gaudernack G, Rasmussen AM, Rusten L, Wang MY, Tindle RW, Blomhoff HK, Egeland T. 1992. Isolation and characterization of human hematopoietic progenitor cells: an effective method for positive selection of CD34+ cells. Leukemia 6:845-852.
51. Swat W, Ignatowicz L, Kisielow P. 1991. Detection of apoptosis of immature CD4+8+ thymocytes by flow cytometry. J Immunol Methods 137:79-87.
52. Tabarowski Z, Gibson-Berry K, Felten SY. 1996. Noradrenergic and peptidergic innervation of the mouse femur bone marrow. Acta Histochem 98:453-457.
53. Tasken K, Andersson KB, Erikstein BK, Hansson V, Jahnsen T, Blomhoff HK. 1994. Regulation of growth in a neoplastic B cell line by transfected subunits of 3′,5′-cyclic adenosine monophosphate-dependent protein kinase. Endocrinology 135:2109-2119.
54. Torgersen KM, Vaage JT, Levy FO, Hansson V, Rolstad B, Tasken K. 1997. Selective activation of cAMP-dependent protein kinase type I inhibits rat natural killer cell cytotoxicity. J Biol Chem 272:5495-5500.
55. Zhou P, Qian L, Kozopas KM, Craig RW. 1997. Mcl-1, a Bcl-2 family member, delays the death of hematopoietic cells under a variety of apoptosis-inducing conditions. Blood 89:630-643.
56. Zhou P, Qian L, Bieszczad CK, Noelle R, Binder M, Levy NB, Craig RW. 1998. Mcl-1 in transgenic mice promotes survival in a spectrum of hematopoietic cell types and immortalization in the myeloid lineage. Blood 92:3226-3239.