Cyclic AMP is both a pro-apoptotic and anti-apoptotic second messenger

Acta Physiologica

Volumn 204, Issue 2, 2012, Pages 277-287

  Insel, P A ^a   Zhang, L ^a   Murray, F ^a   Yokouchi, H ^a   Zambon, A C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Epac; Protein kinase A; Rap1; S49 cell

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; ISOENZYME; RAP1 PROTEIN;

ACINAR CELL; ADRENAL CORTEX CELL; APOPTOSIS; AUTOPHAGY; BREAST CELL; CANCER CELL; CARCINOMA CELL; CELL DEATH; CELL TYPE; CORNEA ENDOTHELIUM; FIBROBLAST; GENE EXPRESSION; GLIA CELL; HEART MUSCLE CELL; HUMAN; INTESTINE EPITHELIUM CELL; KERATINOCYTE; LEUKOCYTE; LIVER CELL; LYMPHOMA CELL; MACROPHAGE; MELANOCYTE; MELANOMA CELL; MESANGIUM CELL; MICROVASCULAR ENDOTHELIAL CELL; MOLECULAR WEIGHT; OLIGODENDROGLIA; OSTEOBLAST; OSTEOCYTE; PANCREAS ISLET BETA CELL; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SMOOTH MUSCLE FIBER; STEM CELL;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MITOCHONDRIA; PHOSPHORYLATION; RAP1 GTP-BINDING PROTEINS; SECOND MESSENGER SYSTEMS;

EID: 84855350974     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2011.02273.x     Document Type: Review

References (164)

1. Adissu, H.A. & Schuller, H.M. 2004. Antagonistic growth regulation of cell lines derived from human lung adenocarcinomas of Clara cell and aveolar type II cell lineage: implications for chemoprevention. Int J Oncol24, 1467-1472.
2. Altucci, L., Rossin, A., Hirsch, O., Nebbioso, A., Vitoux, D., Wilhelm, E., Guidez, F., De Simone, M., Schiavone, E.M., Grimwade, D., Zelent, A., deThe, H. & Gronemeyer, H. 2005. Rexinoid-triggered differentiation and tumor-selective apoptosis of acute myeloid leukemia by protein kinase-mediated desubordination of retinoid X receptor. Cancer Res65, 8754-8765.
3. Al-Wadei, H.A. & Schuller, H.M. 2006. Cyclic adenosine monophosphate-dependent cell type-specific modulation of mitogenic signaling by retinoids in normal and neoplastic lung cells. Cancer Detect Prev30, 403-411.
4. Amsterdam, A., Keren-Tal, I., Aharoni, D., Dantes, A., Land-Bracha, A., Rimon, E., Sasson, R. & Hirsh, L. 2003a. Steroidogenesis and apoptosis in the mammalian ovary. Steroids68, 861-867.
5. Amsterdam, A., Sasson, R., Keren-Tal, I., Aharoni, D., Dantes, A., Rimon, E., Land, A., Cohen, T., Dor, Y. & Hirsh, L. 2003b. Alternative pathways of ovarian apoptosis: death for life. Biochem Pharmacol66, 1355-1362.
6. Andrade da Costa, B.L., Kang, K.D., Rittenhouse, K.D. & Osborne, N.N. 2009. The localization of PGE2 receptor subtypes in rat retinal cultures and the neuroprotective effect of the EP2 agonist butaprost. Neurochem Int55, 199-207.
7. Balhuizen, A., Kumar, R., Amisten, S., Lundquist, I. & Salehi, A. 2010. Activation of G protein-coupled receptor 30 modulates hormone secretion and counteracts cytokine-induced apoptosis in pancreatic islets of female mice. Mol Cell Endocrinol320, 16-24.
8. Barlow, C.A., Kitiphongspattana, K., Siddiqui, N., Roe, M.W., Mossman, B.T. & Lounsbury, K.M. 2008. Protein kinase A-mediated CREB phosphorylation is an oxidant-induced survival pathway in alveolar type II cells. Apoptosis13, 681-692.
9. Basile, D.V., Wood, H.N. & Braun, A.C. 1973. Programming of cells for death under experimental conditions: relevance to the tumor problem. Proc Natl Acad Sci USA70, 3055-3059.
10. Benz, P.M., Feller, S.M., Sickmann, A., Walter, U. & Renne, T. 2008. Prostaglandin-induced VASP phosphorylation controls alpha II-spectrin breakdown in apoptotic cells. Int Immunopharmacol8, 319-324.
11. Bouizar, Z., Ragazzon, B., Viou, L., Hortane, M., Bertherat, J. & Rizk-Rabin, M. 2010. Cl-cAMP modifies the balance between PKAR1 and PKAR2 and modulates the cell cycle, growth and apoptosis in human adreoncortical H295R cells. J Mol Endocrinol44, 331-347.
12. Brown, J.A., Gianino, S.M. & Gutmann, D.H. 2010. Defective cAMP generation underlies the sensitivity of CNS neurons to neurofibromatosis-1 heterozygosity. J Neurosci30, 5579-5589.
13. Brubaker, P.L. & Drucker, D.J. 2004. Minireview: glucagon-like peptides regulate cell proliferation in the pancreas, gut and central nervous system. Endocrinology145, 2653-2659.
14. Budovskaya, Y.V., Stephan, J.S., Deminoff, S.J. & Herman, P.K. 2005. An evolutionary proteomics approach identifies substrates of the cAMP-dependent protein kinase. Proc Natl Acad Sci USA102, 13933-13938.
15. Calafat, M., Larocca, L., Roca, V., Hauk, V., Pregi, N., Nesse, A. & Perez Leiros, C. 2009. Vasoactive intestinal peptide inhibits TNF-alpha-induced apoptotic events in acinar cells from nonobese diabetic mice submandibular glands. Arthritis Res Ther11, R53.
16. Carie, A.E. & Sebti, S.M. 2007. A chemical biology approach identified a beta-2 adrenergic receptor agonist that causes human tumor regression by blocking the Raf-1/Mek-1/Erk 1/2 pathway. Oncogene26, 3777-3788.
17. Chai, B., Li, J.Y., Zhang, W., Newman, E., Ammori, J. & Mulholland, M.W. 2006. Melanocortin-4 receptor-mediated inhibition of apoptosis in immortalized hypothalamic neurons via mitogen-activated protein kinase. Peptides27, 2846-2857.
18. Chan, A.S., Ng, L.W., Poon, L.S., Chan, W.W. & Wong, Y.H. 2007. Dopaminergic and adrenergic toxicities on SK-N-MC human neuroblastoma cells are mediated through G protein signaling and oxidative stress. Apoptosis12, 167-179.
19. Chen, T.C., Hinton, D.R., Zidovetzki, R. & Hofman, F.M. 1998. Up-regulation of the cAMP/PKA pathway inhibits proliferation, induces differentiation and leads to apoptosis in malignant gliomas. Lab Invest78, 165-174.
20. Chen, H.L., Demiralp, B., Schneider, A., Koh, A.J., Silva, C., Wang, C.Y. & McCauley, L.K. 2002. Parathyroid hormone and parathyroid hormone-related protein exert both pro- and anti-apoptotic effects in mesenchymal cells. J Biol Chem277, 19374-19381.
21. Chen, C.P., Kuhn, P., Chaturvedi, K., Boyadjieva, N. & Sarkar, D.K. 2006. Ethanaol induces apoptotic death of developing beta-endorphrin neurons via suppression of cyclic adenosine monophosphate production and activation of transforming growth factor beta1-linked apoptotic signaling. Mol Pharmacol69, 706-717.
22. Chen, S.U., Chen, R.J., Shieh, J.Y., Chou, C.H., Lin, C.W., Lu, H.F. & Yang, Y.S. 2010. Human chorionic gonadotropin up-regulates expression of myeloid cell leukemia-1 protein in human granulose-lutein cells: implication of corpus luteum rescue and ovarian hyperstimulation syndrome. J Clin Endocrinol Metab95, 3982-3992.
23. Chin, T.Y., Kao, C.H., Wang, H.Y., Huang, W.P., Ma, K.H. & Chueh, S.H. 2010. Inhibition of the mammalian target of rapamycin promotes cyclic AMP-induced differentiation of NG108-15 cells. Autophagy6, 1139-1156.
24. Choi, Y.J., Kim, S.Y., Oh, J.M. & Juhnn, Y.S. 2009. Stimulatory heterotrimeric G protein augments gamma ray-induced apoptosis by up-regulation of Bak expression via CREB and AP-1 in H1299 human lung cancer cells. Exp Mol Med41, 592-600.
25. Coffino, P., Bourne, H.R. & Tomkins, G.M. 1975. Mechanism of lymphoma cell death induced by cyclic AMP. Am J Pathol81, 199-204.
26. Conran, N., Almeida, C.B., Lanaro, C., Ferreira, R.P., Traina, F., Saad, S.T. & Costa, F.F. 2007. Inhibition of caspase-dependent spontaneous apoptosis via a cAMP-protein kinase A dependent pathway in neutrophils from sickle cell disease patients. Br J Haematol139, 148-158.
27. Cornu, M., Modi, H., Kawamori, D., Kulkarni, R.N., Joffraud, M. & Thorens, B. 2010. Glucagon-like peptide-1 increases beta-cell glucose competence and proliferation by translational induction of insulin-like growth factor-1 receptor expression. J Biol Chem285, 10538-10545.
28. Counts, S.E. & Mufson, E.J. 2010. Noradrenaline activation of neurotrophic pathways protects against neuronal amyloid toxicity. J Neurochem113, 649-660.
29. Cribbs, J.T. & Strack, S. 2007. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep8, 939-944.
30. Cross, T.G., Scheel-Toellner, D., Henriquez, N.V., Deacon, E., Salmon, M. & Lord, J.M. 2000. Serine/threonine kinases and apoptosis. Exp Cell Res256, 34-41.
31. Dai, H., Zhang, Z., Zhu, Y., Shen, Y., Hu, W., Huang, Y., Luo, J., Timmerman, H., Leurs, R. & Chen, Z. 2006. Histamine protects against NMDA- induced necrosis in cultured cortical neurons through H receptor/cyclic AMP/protein kinase A and H receptor/GABA release pathways. J Neurochem96, 1390-1400.
32. Desiniotis, A., Schafer, G., Clocker, H. & Eder, I.E. 2010. Enhanced antiproliferative and proapoptotic effects on prostate cancer cells by simultaneously inhibiting androgen receptor and cAMP-dependent protein kinase A. Int J Cancer126, 775-789.
33. Ding, B., Abe, J., Wei, H., Xu, H., Che, W., Aizawa, T., Liu, W., Molina, C.A., Sadoshima, J., Blaxall, B.C., Berk, B.C. & Yan, C. 2005. A positive feedback loop of phosphodiesterase 3 (PDE3) and inducible cAMP early repressor (ICER) leads to cardiomyocyte apoptosis. Proc Natl Acad Sci USA102, 14771-14776.
34. Dong, H., Zitt, C., Auriga, C., Hatzelmann, A. & Epstein, P.M. 2010. Inhibition of PDE3, PDE4 and PDE7 potentiates glucocorticoid-induced apoptosis and overcomes glucocorticoid resistance in CEM T leukemic cells. Biochem Pharmacol79, 321-329.
35. Dou, A.X. & Wang, X. 2010. Cyclic adenosine monophosphate signal pathway in targeted therapy of lymphoma. Chin Med J123, 95-99.
36. Elberg, G., Elberg, D., Lewis, T.V., Guruswamy, S., Chen, L., Logan, C.J., Chan, M.D. & Turman, M.A. 2007. EP2 receptor mediates PGE2-induced cystogenesis of human renal epithelial cells. Am J Physiol Renal Physiol293, F1622-F1632.
37. Faglia, G. & Spada, A. 2001. Genesis of pituitary adenomas: state of the art. J Neurooncol54, 95-101.
38. Ferdaoussi, M., Abdelli, S., Yang, J.Y., Cornu, M., Niederhauser, G., Favre, D., Widmann, C., Regazzi, R., Thorens, B., Waeber, G. & Abderrahmani, A. 2008. Exendin-4 protects beta-cells from interleukin-1 beta-induced apoptosis by interfering with the c-Jun NH2-terminal kinase pathway. Diabetes57, 1205-1215.
39. Gallo-Payet, N. & Payet, M.D. 2003. Mechanism of action of ACTH: beyond cAMP. Microsc Res Tech61, 275-287.
40. Gao, N., Hibi, Y., Cueno, M., Asamitsu, K. & Okamoto, T. 2010. A-kinase-interacting protein 1 (AKIP2) acts as a molecular determinant of PKA in NF-kappaB signaling. J Biol Chem285, 28097-28104.
41. Gates, A., Hohenester, S., Anwer, M.S. & Webster, C.R. 2009. cAMP-GEF cytoprotection by Src tyrosine kinase activation of phosphoinositide-3-kinase p110 beta/alpha in rat hepatocytes. Am J Physiol Gastrointest Liver Physiol296, G764-G774.
42. Gloerich, M. & Bos, J.L. 2010. Epac: defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol50, 355-375.
43. Granata, R., Settanni, F., Gallo, D., Trovato, L., Biancone, L., Cantaluppi, V., Nano, R., Annunziata, M., Campiglia, P., Arnoletti, E., Ghe, C., Volante, M., Papotti, M., Muccioli, G. & Ghigo, E. 2008. Obestatin promotes survival of pancreatic beta-cells and human islets and induces expression of genes involved in the regulation of beta-cell mass and function. Diabetes57, 967-979.
44. Grandoch, M., Bujok, V., Fleckenstein, D., Schmidt, M., Fischer, J.W. & Weber, A.A. 2009a. Epac inhibits apoptosis of human leukocytes. J Leukoc Biol86, 847-849.
45. Grandoch, M., Lopez de Jesus, M., Oude Weernink, P.A., Weber, A.A., Jakobs, K.H. & Schmidt, M. 2009b. B cell receptor-induced growth arrest and apoptosis in WEHI-231 immature B lymphoma cells involve cyclic AMP and Epac proteins. Cell Signal21, 609-621.
46. Grandoch, M., Roscioni, S.S. & Schmidt, M. 2010. The role of Epac proteins, novel cAMP mediators, in the regulation of immune, lung and neuronal function. Br J Pharmacol159, 265-284.
47. Growcott, E.J., Spink, K.G., Ren, X., Afzal, S., Banner, K.H. & Wharton, J. 2006. Phosphodiesterase type 4 expression and anti-proliferative effects in human pulmonary artery smooth muscle cells. Resp Res7, 9.
48. Hasegawa, K., Iwai-Kanai, E. & Sasayama, S. 2001. Neurohormonal regulation of myocardial cell apoptosis during the development of heart failure. J Cell Physiol186, 11-18.
49. Hawcroft, G., Ko, C.W. & Hull, M.A. 2007. Prostaglandin E2-EP4 receptor signaling promotes tumorigenic behaviour of HT-29 human colorectal cancer cells. Oncogene26, 3006-3019.
50. Holen, I., Gordon, P.B., Stormhaug, P.E. & Seglen, P.O. 1996. Role of cAMP in the regulation of hepatocytic autophagy. Eur J Biochem236, 163-170.
51. Holla, V.R., Mann, J.R., Shi, Q. & DuBois, R.N. 2006. Prostaglandin E2 regulates the nuclear receptor NR4A2 in colorectal cancer. J Biol Chem281, 2676-2682.
52. Horiuchi, M., Lindsten, T., Pleasure, D. & Itoh, T. 2010. Differing in vitro survival dependency of mouse and rat NG2+ oligoderoglial progenitor cells. J Neurosci Res88, 957-970.
53. Houslay, M.D. & Christian, F. 2010. p62(SQSTM1) forms part of a novel, reversible aggregate containing a specific conformer of the cAMP-degrading phosphodiesterase, PDE4A4. Autophagy6, 1198-1200.
54. Insel, P.A., Bourne, H.R., Coffino, P. & Tomkins, G.M. 1975. Cyclic AMP-dependent protein kinase: pivotal role in regulation of enzyme induction and growth. Science190, 896-898.
55. Iwai-Kanai, E. & Hasegawa, K. 2004. Intracellular signaling pathways for norepinephrine- and endothelin-1-mediated regulation of myocardial cell apoptosis. Mol Cell Biochem259, 163-168.
56. Jasinska, A., Strakova, Z., Szmidt, M. & Fazleabas, A.T. 2006. Human chorionic gonadotropin and decidualization in vitro inhibits cytochalasin-D-induced apoptosis in cultured endometrial stromal fibroblasts. Endocrinology147, 4112-4121.
57. Ji, Z., Mei, F.C., Miller, A.L., Thompson, E.B. & Cheng, X. 2008. Protein kinase A (PKA) isoform RIIbeta mediates the synergistic killing effect of cAMP and glucocorticoid in acute lymphoblastic leukemia cells. J Biol Chem283, 21920-21925.
58. Jiang, J.L., Peng, Y.P., Qiu, Y.H. & Wang, J.J. 2009. Adrenoreceptor-coupled signal-transduction mechanisms mediating lymphocyte apoptosis induced by endogenous catecholamines. J Neuroimmunol213, 100-111.
59. Jiao, S., Liu, Z., Ren, W.H., Ding, Y., Zhang, Y.Q., Zhang, Z.H. & Mei, Y.A. 2007. cAMP/protein kinase A signaling pathway protects against neuronal apoptosis and is associated with modulation of Kv2/1 in cerebellar granule cells. J Neurochem100, 979-991.
60. Joseph, R.R., Yazer, E., Hanakawa, Y. & Stadnyk, A.W. 2005. Prostaglandins and activation of AC/cAMP prevents anoikis in IEC-18. Apoptosis10, 1221-1233.
61. Journot, L., Villalba, M. & Bockaert, J. 1998. PACAP-38 protects cerebellar granule cells from apoptosis. Ann NY Acad Sci865, 100-110.
62. Kamrava, M., Simpkins, F., Alejandro, E., Michener, C., Meltzer, E. & Kohn, E.C. 2005. Lysophosphatidic acid and endothelin-induced proliferation of ovarian cancer cell lines is mitigated by neurtralization of granulin-epithelin precursor (GEP), a prosurvival factor for ovarian cancer. Oncogene24, 7084-7093.
63. Kang, K.D., Andrade da Costa, B.L. & Osborne, N.N. 2010. Stimulation of prostaglandin EP2 receptors on RGC-5 cells in culture blunts the negative effect of serum withdrawal. Neurochem Res35, 820-829.
64. Kerr, J.F., Wylie, A.H. & Currie, A.R. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer26, 239-257.
65. Kim, S.W., Rai, D., McKeller, M.R. & Aguilar, R.C. 2009. Rational combined targeting of phosphodiesterase 4B and SYK in DLBCL. Blood113, 6153-6160.
66. Kim, J.E., Song, S.E., Kim, Y.K., Kim, J.Y., Park, S.C., Park, Y.K., Baek, S.H., Lee, I.K. & Park, S.Y. 2010a. Adiponectin inhibits palmitate-induced apoptosis through suppression of reactive oxygen species in endothelial cells: involvement of cAMP/protein kinase A and AMP-activated protein kinase. J Endocrinol207, 35-44.
67. Kim, Y.K., Park, J.H., Park, S.H., Lim, B., Baek, W.K., Suh, S.I., Lim, J.G., Ryu, G.R. & Song, D.K. 2010b. Protective role of glucagon-like peptide-1 against glucosamine-induced cytotoxicity in pancreatic beta cells. Cell Physiol Biochem25, 211-220.
68. Kitase, Y., Barragan, L., Qing, H., Kondoh, S., Jiang, J.X., Johnson, M.L. & Bonewald, L.F. 2010. Mechanical induction of PGE2 in osteocytes blocks glucocorticoid-induced apoptosis through both the β-catenin and PKA pathways. J Bone Miner Res25, 2381-2392.
69. Kloster, M.M., Hafte, T.T., Moltzau, L.R., Naderi, E.H., Dahle, M.K., Skalhegg, B.S., Gaudernack, G., Levy, F.O., Naderi, S. & Blomhoff, H.K. 2008. EBV infection renders B cell resistant to growth inhibition via adenylyl cyclase. Cell Signal20, 1169-1178.
70. Kostylina, G., Simon, D., Fey, M.F., Yousefi, S. & Simon, H.U. 2008. Neutrophil apoptosis mediated by nicotinic acid receptors (GPR109A). Cell Death Differ15, 134-142.
71. Kottyan, L.C., Collier, A.R., Cao, K.H., Niese, K.A., Hedgebeth, M., Radu, C.G., Witte, O.N., Khurana Hershey, G.K., Rothenberg, M.E. & Zimmermann, N. 2009. Eosinophil viability is increased by acidic pH in a cAMP- and GPR65-dependent manner. Blood114, 2774-2782.
72. Koyama, H., Bornfeldt, K.E., Fukumoto, S. & Nishizawa, Y. 2001. Molecular pathways of cyclic nucleotide-induced inhibition of arterial smooth muscle cell proliferation. J Cell Physiol186, 1-10.
73. Krakstad, C., Christensen, A.E. & Doskeland, S.O. 2004. cAMP protects neutrophils agains TNF-alpha-induced apoptosis by activation of cAMP-dependent protein kinase, independently of exchange protein directly activated by cAMP (Epac). J Leukoc Biol76, 641-647.
74. Kumar, B., Hanson, A.J. & Prasad, K.N. 2004. Sensitivity to proteasome to its inhibitors increases during cAMP-induced differentiation of neuroblastoma cells in culture and causes decreased viability. Cancer Lett204, 53-59.
75. Kumar, S., Kostin, S., Flacke, J.P., Reusch, H.P. & Ladilov, Y. 2009. Soluble adenylyl cyclase controls mitochondria-dependent apoptosis in coronary endothelial cells. J Biol Chem284, 14760-14768.
76. Kwak, H.J., Park, K.M., Choi, H.E., Chung, K.S., Lim, H.U. & Park, H.Y. 2008. PDE4 inhibitor, roflumilast protects cardiomyocytes against NO-induced apoptosis via activation of PKA and Epac dual pathways. Cell Signal20, 803-814.
77. Lee, J.Y., Kim, J.H., Chae, G., Lee, B.K., Ha, K.S., Kwon, Y.G. & Kim, Y.M. 2010. Cyclic AMP prolongs graft survival by suppressing apoptosis and inflammatory gene expression in acute cardiac allograft rejection. Exp Mol Med42, 69-79.
78. Leone, V., di Palma, A., Ricchi, P., Acquaviva, F., Giannouli, M., Di Prisco, A.M., Iuliano, F. & Acquaviva, A.M. 2007. PGE2 inhibits apoptosis in human adenocarcinoma Caco-2 cell line through Ras-PI3K association and cAMP-dependent kinase A activation. Am J Physiol Gastrointest Liver Physiol293, G673-G681.
79. Lerner, A. & Epstein, P.M. 2006. Cyclic nucleotide phosphodiesterases as targets for treatment of haematological malignancies. Biochem J393, 21-41.
80. Lerner, A., Kim, D.H. & Lee, R. 2000. The cAMP signaling pathway as a therapeutic target in lymphoid malignancies. Leuk Lymphoma37, 39-51.
81. Levine, B. & Yuan, J. 2005. Autophagy in cell death: an innocent convict? J Clin Invest115, 2679-2688.
82. Li, R.C., Cindrova-Davies, T., Skepper, J.N. & Sellers, L.A. 2004. Prostacyclin induces apoptosis of vascular smooth muscle cells by a cAMP-mediated inhibition of extracellular signal-regulated kinase activity and can counteract the mitogenic activity of endothelin-1 or basic fibroblast growth factor. Circ Res94, 759-767.
83. Li, S., Allen, K.T. & Bonanno, J.A. 2011. Soluble adenylyl cyclase mediates bicarbonate-dependent corneal endothelial cell protection. Am J Physiol-Cell Physiol300, C368-C374.
84. Linden, R., Martins, R.A. & Silveira, M.S. 2005. Control of programmed cell death by neurotransmitters and neuropeptides in the developing mammalian retina. Prog Retin Eye Res24, 457-491.
85. Liu, J., Li, X.D., Ora, A., Heikkila, P., Vaheri, A. & Voutilainen, R. 2004. cAMP-dependent protein kinase activation inhibits proliferation and enhances apoptotic effect of tumor necrosis factor-alpha in NCI-H295R adrenocortical cells. J Mol Endocrinol33, 511-522.
86. Loffler, I., Grun, M., Bohmer, F.D. & Rubio, I. 2008. Role of cAMP in the promotion of colorectal cancer cell growth by prostaglandin E2. BMC Cancer19, 380.
87. Mantovani, G., Bondioni, S., Lania, A.G., Rodolfo, M., Peverelli, E., Polentarutti, N., Veliz Rodriguez, T., Ferrero, S., Bosari, S., Beck-Peccoz, P. & Spada, A. 2008a. High expression of PKA regulatory subunit 1A protein is related to proliferation of human melanoma cells. Oncogene27, 1834-1843.
88. Mantovani, G., Lania, A.G., Bondioni, S., Peverelli, E., Pedroni, C., Ferrero, S., Pellegrini, C., Vicentini, L., Arnaldi, G., Bosari, S., Beck-Peccoz, P. & Spada, A. 2008b. Different expression of protein kinase A (PKA) regulatory subunits in cortisol-secreting adrenocortical tumors: relationship with cell proliferation. Exp Cell Res314, 123-130.
89. Martorana, P.A. 1971. The role of cyclic AMP in isoprenaline-induced cardiac necroses in the rat. J Pharm Pharmacol23, 200-203.
90. McEwan, D.G., Brunton, V.G., Baillie, G.S., Leslie, N.R., Houslay, M.D. & Frame, M.C. 2007. Chemoresistant KM12C colon cancer cells are addicted to low cyclic AMP levels in a phosphodiesterase 4-regulated compartment via effects on phosphoinositide 3-kinase. Cancer Res67, 5248-5257.
91. McMurray, J.J. 2010. Clinical Practice. Systolic heart failure. N Engl J Med362, 228-238.
92. Misra, U.K. & Pizzo, S.V. 2005. Coordinate regulation of forskolin-induced cellular proliferation in macrophages by protein kinase A/cAMP-response element-binding protein (CREB) and Epac1-Rap1 signaling: effects of silencing CREB gene expression on Akt activation. J Biol Chem280, 38276-38289.
93. Moghadam, K.K., Kessler, C.A., Schroeder, J.K., Buckley, A.R., Brar, A.K. & Handwerger, S. 2005. Cannabinoid receptor 1 activatioin markedly inhibits human decidualization. Mol Cell Endocrinol229, 65-74.
94. Muhl, H., Nitsch, D., Sandau, K., Brune, B., Varga, Z. & Pfeilschifter, J. 1996. Apoptosis is triggered by the cyclic AMP signaling pathway in renal mesangial cells. FEBS Lett382, 271-275.
95. Naderi, E.H., Findley, H.W., Ruud, E., Blomhoff, H.K. & Naderi, S. 2009. Activation of cAMP signaling inhibits DNA damage-induced apoptosis in BCP-ALL cells through abrogation of p53 accumulation. Blood114, 608-618.
96. Naviglio, S., Di Gesto, D., Romano, M., Sorrention, A., Illiano, F., Sorvillo, L., Abbruzzese, A., Marra, M., Caraglia, M., Chiosi, E., Spina, A. & Illiano, G. 2009. Leptin enhances growth inhibition by cAMP elevating agents through apoptosis of MDA-MB-231 breast cancer cells. Cancer Biol Ther8, 1183-1190.
97. Nishihara, H., Kizaka-Kondoh, S., Insel, P.A. & Eckmann, L. 2003. Inhibition of apoptosis in normal and transformed intestinal epithelial cells by cAMP through induction of inhibitor of apoptosis protein (IAP)-2. Proc Natl Acad Sci USA100, 8921-8926.
98. Nishihara, H., Hwang, M., Kizaka-Kondoh, S., Eckmann, L. & Insel, P.A. 2004. Cyclic AMP promotes cAMP-responsive element-binding protein-dependent induction of cellular inhibitor of apoptosis protein-2 and suppresses apoptosis of colon cancer cells through ERK 1/2 and p38 MAPK. J Biol Chem279, 26176-26183.
99. Ohtsubo, H., Ichiki, T., Miyazaki, R., Inanaga, K., Imayama, I., Hashiguchi, Y., Sadoshima, J. & Sunagawa, K. 2007. Inducible cAMP early repressor inhibits growth of vascular smooth muscle cell. Arterioscler Thromb Vasc Biol27, 1549-1555.
100. Park, M.K., Kang, Y.J., Ha, Y.M., Jeong, J.J., Kim, H.J., Seo, H.G., Lee, J.H. & Chang, K.C. 2009. EP2 receptor activation by prostaglandin E2 leads to induction of HO-1 via PKA and PI3K pathways in C6 cells. Biochem Biophys Res Commun379, 1043-1047.
101. Parkkonnen, J., Hasala, H., Moilanen, E., Giembycz, M.A. & Kankaanranta, H. 2008. Phosphodiesterase 4 inhibitors delay human eosinophil and neutrophil apoptosis in the absence and presence of salbutamol. Pulm Pharmacol Ther21, 499-506.
102. Passeron, T., Namiki, T., Passeron, H.J., Le Pape, E. & Hearing, V.J. 2009. Forskolin protects keratinocytes from UVB-induced apoptosis and increases DNA repair independent of its effects on melanogenesis. Invest Dermatol129, 162-166.
103. Patel, H.H., Hamuro, L.L., Chun, B.J., Kawaraguchi, Y., Quick, A., Rebolledo, B., Pennypacker, J., Thurston, J., Rodriquez-Pinto, N., Self, C., Olson, G., Insel, P.A., Giles, W.R., Taylor, S.S. & Roth, D.M. 2010. Disruption of protein kinase A localization using a trans-activator of transcription (TAT)-conjugated A-kinase-anchoring peptide reduces cardiac function. J Biol Chem285, 27632-27640.
104. Perrino, C., Felicello, A., Schiattarella, G.G., Esposito, G., Guerriero, R., Zaccaro, L., Del Gatto, A., Saviano, M., Garbi, C., Carangi, R., Di Lorenzo, E., Donato, G., Indolfi, C., Avveedimento, V.E. & Chiariello, M. 2010. AKAP121 downregulation impairs protective cAMP signals, promotes mitochondrial dysfunction and increases oxidative stress. Cardiovasc Res88, 101-110.
105. Pon, Y.L., Auersperg, N. & Wong, A.S. 2005. Gonadotropins regulate N-cadherin-mediated human ovarian surface epithelial cell survival at both post-translational and transcriptional levels through a cyclic AMP/protein kinase A pathway. J Biol Chem280, 15438-15448.
106. Porcellini, A., Messina, S., De Gregorio, G., Feliciello, A., Carlucci, A., Barone, M., Picascia, A., De Blasi, A. & Avvedimento, E.V. 2003. The expression of the thyroid-stimulating hormone (TSH) receptor and the cAMP-dependent protein kinase RII beta regulatory subunit confers TSH-cAMP-dependent growth to mouse fibroblasts. J Biol Chem278, 40621-40630.
107. Pratt, R.M. & Martin, G.R. 1975. Epithelial cell death and cyclic AMP increase during palatal development. Proc Natl Acad Sci USA72, 874-877.
108. Pugh, P.C. & Margiotta, J.E. 2006. PACAP support of neuronal survival requires MAPK- and activity-generated signals. Mol Cell Neurosci31, 586-595.
109. Qin, Z., Sun, Z., Huang, J., Hu, Y., Wu, Z. & Mei, B. 2008. Mutated recombinant glucagon-like peptide-1 protects SH-SY5Y cells from apoptosis induced by amyloid-beta peptide (1-42). Neurosci Lett444, 217-221.
110. Quinteros Villarruel, E., Borda, E., Sterin-Borda, L. & Orman, B. 2010. Lidocaine-induced apoptosis of gingival fibroblasts. Participation of cAMP and PKC activity. Cell Biol Int. In press.
111. Raskovalova, T., Lokshin, A., Huang, X., Jackson, E.K. & Gorelik, E. 2006. Adenosine-mediated inhibition of cytotoxic activity and cytokine production by IL-2/NKp46-activated NK cells: involvement of protein kinase A isozyme (PKA I). Immunol Res36, 91-99.
112. Safa, M., Kazemi, A., Zand, H., Azarkeivan, A., Zaker, F. & Hayat, P. 2010. Inhibitory role of cAMP on doxorubicin-induced apoptosis in pre-B ALL cells through dephosphorylation of p53 serine residues. Apoptosis15, 196-203.
113. Sastry, K.S., Karpova, Y., Prokopovich, S., Smith, A.J., Essau, B., Gersappe, A., Carson, J.P., Weber, M.J., Register, T.C., Chen, Y.Q., Penn, R.B. & Kulik, G. 2007. Epinephrine protects cancer cells from apoptosis via activation of cAMP-dependent protein kinase and BAD phosphorylation. J Biol Chem282, 14094-14100.
114. Savai, R., Pullamsetti, S.S., Banat, G.A., Weissmann, N., Ghofrani, H.A., Grimminger, F. & Schermuly, R.T. 2010. Targeting cancer with phosphodiesterase inhbitors. Expert Opin Investig Drugs19, 117-131.
115. Shafer, S.H., Phelps, S.H. & Williams, C.L. 1998. Reduced DNA synthesis and cell viability in small cell lung carcinoma by treatment with cyclic AMP phosphodiesterase inhibitors. Biochem Pharmacol56, 1229-1236.
116. Shao, W., Yu, Z., Fantus, I.G. & Jin, T. 2010. Cyclic AMP signaling stimulates proteasome degradation of thioredoxin interacting protein (TxNIP) in pancreatic beta-cells. Cell Signal22, 1240-1246.
117. Shao, J.L., Wan, X.H., Chen, Y., Bi, C., Chen, H.M., Zhong, Y., Heng, X.H. & Qian, J.Q. 2011. H(2)S protects hippocampal neurons from anoxia-reoxygenation through cAMP-mediated PI3K/Akt/p70S6K cell-survival signaling pathways. J Mol Neurosci43, 453-460.
118. Sinclair, E.M., Yusta, B., Streutker, C., Baggio, L.L., Koehler, J., Charron, M.J. & Drucker, D.J. 2008. Glucagon receptor signaling is essential for control of murine hepatocyte survival. Gastroenterology135, 2096-2106.
119. Singh, K., Xiao, L., Sawyer, D.B. & Colucci, W.S. 2001. Adrenergic regulation of cardiac myocyte apoptosis. J Cell Physiol189, 257-265.
120. Slominski, A., Zbytek, B., Pisarchik, A., Slominski, R.M., Smijewski, M.A. & Wortsman, J. 2006. CRH functions as a growth factor/cytokine in the skin. J Cell Physiol206, 780-791.
121. Slot, K.A., de Boer-Brouwer, M., Houweling, M., Vaandrager, A.B., Dorrington, J.H. & Teerds, K.J. 2006. Luteinizing hormone inhibits Fas-induced apoptosis in ovarian surface epithelial cell lines. J Endocrinol188, 227-239.
122. Smith, P.G., Wang, F., Wilkinson, K.N., Savage, K.J., Klein, U., Neuberg, D.S., Bollag, G., Shipp, M.A. & Aquilar, R.C. 2005. The phosphodiesterase PDE4B limits cAMP-associated PI3K/AKT-dependent apoptosis in diffuse large B-cell lymphoma. Blood105, 308-316.
123. Soleimanpour, S.A., Crutchlow, M.F., Ferrari, A.M., Raum, J.C., Groff, D.N., Rankin, M.M., Liu, C., De Leon, D.D., Naji, A., Kushner, J.A. & Stoffers, D.A. 2010. Calcineurin signaling regulated human islet β-cell survival. J Biol Chem285, 40050-40059.
124. Sousa, L.P., Carmo, A.F., Rezende, B.M., Lopes, F., Silva, D.M., Alessandri, A.L., Bonjardim, C.A., Rossi, A.G., Teixeira, M.M. & Pinho, V. 2009. Cyclic AMP enhances resolution of allergic pleurisy by promoting inflammatory cell apoptosis via inhibition of PI3K/Akt and NF-kappaB. Biochem Pharmacol78, 396-405.
125. Sousa, L.P., Lopes, F., Silva, D.M., Tavares, L.P., Vieira, A.T., Rezende, B.M., Carmo, A.F., Russo, R.C., Garcia, C., Bonjardim, C.A., Alessandri, A.L., Rossi, A.G., Pinho, V. & Teixeira, M.M. 2010. PDE4 inhibition drives resolution of neutrophilic inflammation by inducing apoptosis in a PKA-PI3K/Akt-dependent and NF-kappaB-independent manner. J Leukoc Biol87, 895-904.
126. Steinert, D., Kuper, C., Bartels, H., Beck, F.X. & Neuhofer, W. 2009. PGE2 potentiates tonicity-induced COX-2 expression in renal medullary cells in a positive feedback look involving EP2-cAMP-PKA signaling. Am J Physiol Cell Physiol296, 75-87.
127. Stephan, J.S., Yeh, Y.Y., Ramachandran, V., Deminoff, S.J. & Herman, P.K. 2009. The Tor and PKA signaling pathways independently target the Atg1/Atg13 protein kinase complex to control autophagy. Proc Natl Acad Sci USA10, 17049-17054.
128. Stetler, R.A., Gao, Y., Zukin, R.S., Vosler, P.S., Zhang, L., Zhang, F., Cao, G., Bennett, M.V. & Chen, J. 2010. Apurinic/apyrimidinic endonuclease APE1 is required for PACAP-induced neuroprotection against global cerebral ischemia. Proc Natl Acad Sci USA107, 3204-3209.
129. Suzuki, S., Yokoyama, U., Abe, T., Kiyonari, H., Yamashita, N., Kato, Y., Kurotani, R., Sato, M., Okumura, S. & Ishikawa, Y. 2010. Differential roles of Epac in regulating cell death in neuronal and myocardial cells. J Biol Chem285, 24248-24259.
130. Svoboda, N., Zierler, S. & Kerschbaum, H.H. 2007. cAMP mediates ammonia-induced programmed cell death in the microglial cell line BV-2. Eur J Neurosci25, 2285-2295.
131. Szatmari, E., Kalita, K.B., Kharebava, G. & Hetman, M. 2007. Role of kinase suppressor of Ras-1 in neuronal survival signaling by extracellular signal-regulated kinase 1/2. J Neurosci17, 11389-11400.
132. Tada, M., Kobayashi, H. & Moriuchi, T. 1999. Molecular basis of pituitary oncogenesis. J Neuroncol45, 83-96.
133. Takadera, T. & Ohyashiki, T. 2006a. Prostaglandin E2 deteriorates N-methyl-D-aspartate receptor-mediated cytotoxicity possibly by activating EP2 receptors in cultured cortical neurons. Life Sci78, 1878-1883.
134. Takadera, T. & Ohyashiki, T. 2006b. Prevention of rat cortical neurons from prostaglandin E2-induced apoptosis by glycogen synthase kinase-3 inhibitors. Neurosci Lett400, 105-109.
135. Thompson, E.B., Medh, R.D., Zhou, F., Ayala-Torres, S., Ansari, N., Zhang, W. & Johnson, B.H. 1999. Glucocorticoids, oxysterols, and cAMP with glucocorticoids each cause apoptosis of CEM cells and suppress c-myc. J Steroid Biochem Mol Biol69, 453-461.
136. Tiwari, S., Felekkis, K., Moon, E.Y., Flies, A., Sherr, D.H. & Lerner, A. 2004. Among circulating hematopoietic cells, B-CLL uniquely expressed functional EPAC1, but EPAC1-mediated Rap1 activation does not account for PDE4 inhibitor-induced apoptosis. Blood103, 2661-2667.
137. Torella, D., Gasparri, C., Ellison, G.M., Curcio, A., Leone, A., Vicinanza, C., Galuppo, V., Mendicino, I., Sacco, W., Aquila, I. et al. 2009. Differential regulation of vascular smooth muscle and endothelial cell proliferation in vitro and in vivo by cAMP/PKA-activated p85alphPI3K. Am J Physiol Heart Circ Physiol297, H2015-H2025.
138. Torgersen, K.M., Vagge, J.T., Levy, F.O., Hansson, V., Rolstad, B. & Tasken, K. 1997. Selective activation of cAMP-dependent protein kinase type I inhibits rat natural killer cell cytotoxicity. J Biol Chem272, 5495-5500.
139. Ugland, H., Boquest, A.C., Naderi, S., Collas, P. & Blomhoff, H.K. 2008. cAMP-mediated induction of cyclin E sensitizes growth arrested adipose stem cells to DNA damage-induced apoptosis. Mol Biol Cell19, 5082-5092.
140. Uzan, B., Ea, H.K., Launay, J.M., Garel, J.M., Champy, R., Cressent, M. & Liote, F. 2006. A critical rrole for adrenomedullin-calcitonin receptor-like receptor in regulating rheumatoid fibroblast-like synoviocyte apoptosis. J Immunol176, 5548-5558.
141. Valente, E.G., Vernet, D., Ferrini, M.G., Qian, A., Raifer, J. & Gonzalez-Cadavid, N.F. 2003. L-arginine and phosphodiesterase inhibitors counteract fibrosis in the Peyronie's fibrotic plaque and related fibroblast cultures. Nitric Oxide9, 229-244.
142. Vaudry, D., Falluel-Morel, A., Bourgault, S., Basille, M., Burel, D., Wurtz, O., Fournier, A., Chow, B.K., Hashimoto, H., Galas, L. & Vaudry, H. 2009. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20years after the discovery. Pharmacol Rev61, 283-357.
143. Vaughan, K.R., Stokes, L., Prince, L.R., Marriott, H.M., Meis, S., Kassack, M.U., Bingle, C.D., Sabroe, I., Surprenant, A. & Whyte, M.K. 2007. Inhibition of neutrophil apoptosis by ATP is mediated by the P2Y11 receptor. J Immunol179, 8544-8553.
144. Walker, N.I., Harmon, B.V., Gobe, G.C. & Kerr, J.F. 1988. Patterns of cell death. Methods Achiev Exp Pathol13, 18-54.
145. Wang, S.M. & Yang, W.L. 2009. Circulating hormone adrenomedullin and its binding protein protect neural cells from hypoxia-induced apoptosis. Biochim Biophys Acta1790, 361-367.
146. Werstiuk, E.S. & Lee, R.M.K.W. 2000. Vascular β-adrenoceptor function in hypertension and in ageing. Can J Physiol Pharmacol78, 433-452.
147. Whitaker, C.M., Beaumont, E., Wells, M.J., Magnuson, D.S., Hetman, M. & Onifer, S.M. 2008. Rolipram attenuates acute oligodendrocyte death in the adult rat ventrolateral funiculus following contusive cervical spinal cord injury. Neurosci Lett438, 200-204.
148. Xiao, R.P. 2001. Beta-adrenergic signaling in the heart: dual coupling of the beta2-adrenergic receptor to G(s) and G(i) proteins. Sci STKE104, re15.
149. Yan, L., Hermann, V., Hofer, J.I. & Insel, P.A. 2000. Beta-adrenergic receptor/cAMP-mediated signaling an apoptosis of S49 lymphoma cells. Am J Physiol Cell Physiol279, 1665-1674.
150. Yan, C., Miller, C.L. & Abe, J. 2007. Regulation of phosphodiesterase 3 and inducible cAMP early repressor in the heart. Circ Res100, 489-501.
151. Yano, T., Itoh, Y., Kubota, T., Sendo, T., Koyama, T., Fujita, T., Saeki, K., You, A. & Oishi, R. 2005. A prostacyclin analog prevents radiocontrast nephropathy via phosphorylation of cyclic AMP response element binding protein. Am J Pathol166, 1333-1342.
152. Yu, Z. & Jin, T. 2010. New insights into the role of cAMP in the production and function of the incretin hormone glucagon-like peptide-1 (GLP-1). Cell Signal22, 1-8.
153. Yu, R. & Melmed, S. 2001. Oncogene activation in pituitary tumors. Brain Pathol11, 328-341.
154. Yusta, B., Boushev, R.P. & Drucker, D.J. 2000. The glucagon-like peptide receptor mediates inhibition of cellular apoptosis via a cAMP-dependent protein kinase-independent pathway. J Biol Chem275, 35345-35352.
155. Zambon, A.C., Zhang, L., Minovitsky, S., Kanter, J.R., Prabhakar, S., Salomonis, N., Vranizan, K., Dubchak, I., Conklin, B.R. & Insel, P.A. 2005. Gene expression patterns define key transcriptional events in cell cycle regulation by cAMP and protein kinase A. Proc Natl Acad Sci USA102, 8561-8566.
156. Zhang, L. & Insel, P.A. 2001. Bcl-2 protects lymphoma cells from apoptosis but not growth arrest promoted by cAMP and dexamethosone. Am J Physiol Cell Physiol281, 1642-1647.
157. Zhang, L. & Insel, P.A. 2004. The pro-apoptotic protein Bim is a convergence point for cAMP/protein kinase A- and glucocorticoid-promoted apoptosis of lymphoid cells. J Biol Chem279, 20858-20865.
158. Zhang, L., Murray, F., Zahno, A., Kanter, J.R., Chou, D., Suda, R., Fenlon, M., Rassenti, L., Cottam, H., Kipps, T.J. & Insel, P.A. 2008a. Cyclic nucleotide phosphodiesterase profiling reveals increased expression of phosphodiesterase 7B in chronic lymphocytic leukemia. Proc Natl Acad Sci USA105, 19532-19537.
159. Zhang, L., Zambon, A.C., Vranizan, K., Pothula, K., Conklin, B.R. & Insel, P.A. 2008b. 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 Chem283, 4304-4313.
160. Zhang, J., Wang, Q., Zhu, N., Yu, M., Shen, B., Xiang, J. & Lin, A. 2008c. Cyclic AMP inhibits JNK activation by CREB-mediated induction of c-FLIP(L) and MKP-1, thereby antagonizing UV-induced apoptosis. Cell Death Differ15, 1654-1662.
161. Zhao, L., Qian, Z.M., Zhang, C., Wing, H.Y., Du, F. & Ya, K. 2007. Amyloid beta-peptide 31-35-induced neuronal apoptosis is mediated by caspase-dependent pathways via cAMP-dependent protein kinase A activation. Aging Cell7, 47-57.
162. Zheng, M., Zhu, W., Han, Q. & Xiao, R.P. 2005. Emerging concepts and therapeutic implications of beta-adrenergic receptor subtype signaling. Pharmacol Ther108, 257-268.
163. Zhou, B., Li, F., Chen, H. & Song, J. 2005. The modulation of apoptosis involves Akt and epidermal factor receptor. Intl J Biochem Cell Biol37, 1483-1495.
164. Zhu, Y., Yao, J., Meng, Y., Kasai, A., Hiamatsu, N., Hayakawa, K., Miida, T., Takeda, M., Okada, M. & Kitamura, M. 2006. Profiling of functional phosphodiesterase in mesangial cells using a CRE-SEAP-based reporting system. Br J Pharmacol148, 833-844.