Platelet-derived growth factor BB induces nuclear export and proteasomal degradation of CREB via phosphatidylinositol 3-kinase/Akt signaling in pulmonary artery smooth muscle cells

Molecular and Cellular Biology

Volumn 26, Issue 13, 2006, Pages 4934-4948

  Garat, Chrystelle V ^b   Fankell, Dana ^b   Erickson, Paul F ^b   Reusch, Jane E B ^a,b   Bauer, Natalie N ^b   McMurtry, Ivan F ^b   Klemm, Dwight J ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; CYAN FLUORESCENT PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DNA; LACTACYSTIN; LEPTOMYCIN B; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR BB; PROTEIN KINASE B; SERINE; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTERY MUSCLE; ARTICLE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME INHIBITION; IMMUNOHISTOCHEMISTRY; MUTATION; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; PULMONARY ARTERY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER; UBIQUITINATION; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACETYLCYSTEINE; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL PROLIFERATION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYSTEINE PROTEINASE INHIBITORS; FATTY ACIDS, UNSATURATED; HUMANS; MUTATION; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; PLATELET-DERIVED GROWTH FACTOR; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-AKT; PULMONARY ARTERY; RATS; RECOMBINANT FUSION PROTEINS; SERINE; SIGNAL TRANSDUCTION; UBIQUITIN;

ANIMALIA;

EID: 33745475138     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.02477-05     Document Type: Article

References (69)

1. Allen, R. T., K. D. Krueger, A. Dhume, and D. K. Agrawal. 2005. Sustained Akt/PKB activation and transient attenuation of c-Jun N-terminal kinase in the inhibition of apoptosis by IGF-1 in vascular smooth muscle cells. Apoptosis 10:525-535.
2. Atkins, J. B., J. Chlan-Fourney, H. E. Nye, N. Hiroi, W. A. Carlezon, and E. J. Nestler. 1999. Region-specific induction of dFosB by repeated administration of typical versus atypical antipsychotic drugs. Synapse 33:118-128.
3. Beals, C. R., C. M. Sheridan, C. W. Turck, P. Gardner, and G. R. Crabtree. 1997. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275:1930-1933.
4. Biggs, W. H., III, J. Meisenhelder, T. Hunter, W. K. Cavenee, and K. C. Arden. 1999. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc. Natl. Acad. Sci. USA 96:7421-7426.
5. Bornfeldt, K. E., and E. G. Krebs. 1999. Crosstalk between protein kinase A and growth factor receptor signaling pathways in arterial smooth muscle. Cell. Signal. 11:465-477.
6. Botney, M. D., L. Bahadori, and L. I. Gold. 1994. Vascular remodeling in primary pulmonary hypertension. Potential role for transforming growth factor-b. Am. J. Pathol. 140:286-295.
7. Brownawell, A. M., G. J. Kops, I. G. Macara, and B. M. T. Burgering. 2001. Inhibition of nuclear import by protein kinase B (Akt) regulates the subcellular distribution and activity of the forkhead transcription factor AFX. Mol. Cell. Biol. 21:3534-3546.
8. Bullock, B. P., and J. F. Habener. 1998. Phosphorylation of the cAMP response element binding protein CREB by cAMP-dependent protein kinase A and glycogen synthase kinase-3 alters DNA-binding affinity, conformation, and increases net charge. Biochemistry 37:3795-3809.
9. Cross, D. A., D. R. Alessi, P. Cohen, M. Andjelkovich, and B. A. Hemmings. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated protein kinase B. Nature 378:785-789.
10. D'Amico, M., J. Hulit, D. F. Amanatullah, B. T. Zafonte, C. Albanese, B. Bouzahzah, M. Fu, L. H. Augenlicht, L. A. Donehower, K.-I. Takemaru, R. T. Moon, R. Davis, M. P. Lisanti, M. Shtutman, J. Zhurinsky, A. Ben-Ze'ev, A. A. Troussard, S. Dedahr, and R. G. Pestell. 2000. The integrin-linked kinase regulates the cyclin D1 gene through glycogen synthase kinase 3β and cAMP-responsive element-binding protein-dependent pathways. J. Biol. Chem. 275:32469-32657.
11. Dawes, K. E., A. J. Peacock, A. J. Gray, J. E. Bishop, and G. J. Laurent. 1994. Characterization of fibroblast mitogens and chemoattractants produced by endothelial cells exposed to hypoxia. Am. J. Respir. Cell Mol. Biol. 10:552-559.
12. Du, K., and M. Montminy. 1998. CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 273:32377-32379.
13. Enslen, H., H. Tokumitsu, and T. R. Soderling. 1995. Phosphorylation of CREB by CaM-kinase IV activated by CaM-kinase IV kinase. Biochem. Biophys. Res. Commun. 207:1038-1043.
14. Faller, D. V. 1999. Endothelial cell responses to hypoxic stress. Clin. Exp. Pharmacol. Physiol. 26:74-84.
15. Fanburg, B., and S.-L. Lee. 2000. A role for the serotonin transporter in hypoxia-induced pulmonary hypertension. J. Clin. Investig. 105:1521-1523.
16. Feng, J., R. Tamaskovic, Z. Yang, D. P. Brazil, A. Merlo, D. Hess, and B. A. Hemmings. 2004. Stabilization of Mdm2 via decreased ubiquitination is mediated by protein kinase B/Akt-dependent phosphorylation. J. Biol. Chem. 279:35510-35517.
17. Fiol, C. J., J. S. Williams, C. H. Chou, Q. M. Wang, P. J. Roach, and O. M. Andrisani. 1994. A secondary phosphorylation of CREB341 at Ser129 is required for the cAMP-mediated control of gene expression. A role for glycogen synthase kinase-3 in the control of gene expression. J. Biol. Chem. 269:32187-32193.
18. Fukuyama, K., T. Ichiki, H. Ono, T. Tokunou, N. Iino, S. Masuda, H. Ohtsubo, and A. Takeshita. 2005. cAMP-response element-binding protein mediates prostaglandin F(2alpha)-induced hypertrophy of vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 338:910-918.
19. Funakoshi, Y., T. Ichiki, K. Takeda, T. Tokuno, N. Iino, and A. Takeshita. 2002. Critical role of cAMP-response element-binding protein for angiotensin II-induced hypertrophy of vascular smooth muscle cells. J. Biol. Chem. 277:18710-18717.
20. Ghofrani, H. A., W. Seeger, and F. Grimminger. 2005. Imatinib for the treatment of pulmonary arterial hypertension. N. Engl. J. Med. 353:1412-1413.
21. Goruppii, S., and J. M. Kyriakis. 2004. The pro-hypertrophic basic helix-loop-helix protein p8 is degraded by the ubiquitin/proteosome system in a protein kinase B/Akt- and glucogen synthase kinase-3-dependent manner, whereas endothelin induction of p8 mRNA and renal mesangial cell hypertrophy require NFAT4. J. Biol. Chem. 279:20950-20958.
22. Graves, L. M., K. E. Bornfeldt, E. W. Raines, B. C. Potts, S. G. Macdonald, R. Ross, and E. G. Krebs. 1993. Protein kinase A antagonizes platelet-derived growth factor-induced signaling by mitogen-activated protein kinase in human arterial smooth muscle cells. Proc. Natl. Acad. Sci. USA 90:10300-10304.
23. Graves, L. M., and J. C. Lawrence, Jr. 1996. Insulin, growth factors, and cAMP. Antagonism in the signal transduction pathways. Trends Endocrinol. Metab. 7:43-50.
24. Gu, J., L. Nie, D. Weiderschain, and Z.-M. Yuan. 2001. Identification of p53 sequence elements that are required for Mdm2-mediated nuclear export. Mol. Cell. Biol. 21:8533-8546.
25. Hayashi, S., R. Morishita, H. Matsushita, H. Nakagami, Y. Taniyama, T. Nakamura, M. Aoki, K. Yamamoto, J. Higaki, and T. Ogihara. 2000. Cyclic AMP inhibited proliferation of human aortic vascular smooth muscle cells, accompanied by induction of p53 and p21. Hypertension 35:237-243.
26. Holtmann, M. H., and M. F. Neurath. 2004. Differential TNF-signaling in chronic inflammatory disorders. Curr. Mol. Med. 4:439-444.
27. Hoshiya, M., and M. Awazu. 1998. Trapidil inhibits platelet-derived growth factor-stimulated mitogen-activated protein kinase cascade. Hypertension 31:665-671.
28. Huang, F., and A. Sorkin. 2005. Growth factor receptor binding protein 2-mediated recruitment of the RING domain of Cbl to the epidermal growth factor receptor is essential and sufficient to support receptor endocytosis. Mol. Biol. Cell 16:1268-1281.
29. Isenovic, E. R., Y. Meng, A. Divald, N. Milivojevic, and J. R. Sowers. 2002. Role of phosphatidylinositol 3-kinase/Akt pathway in angiotensin II and insulin-like growth factor-1 modulation of nitric oxide synthase in vascular smooth muscle cells. Endocrine 19:287-292.
30. Iyengar, R. 1996. Gating by cyclic AMP: expanded role for an old signaling pathway. Science 271:461-463.
31. Kang, Y. J., E. S. Jeon, H. Y. Song, J. S. Woo, J. S. Jung, Y. K. Kim, and J. H. Kim. 2005. Role of c-Jun N-terminal kinase in the PDGF-induced proliferation and migration of human adipose tissue-derived mesenchymal stem cells. J. Cell. Biochem. 95:1135-1145.
32. Kaplan-Albuquerque, N., C. Garat, C. Desseva, P. L. Jones, and R. A. Nemenoff. 2003. Platelet-derived growth factor-BB-mediated activation of Akt suppresses smooth muscle-specific gene expression through inhibition of mitogen-activated protein kinase and redistribution of serum response factor. J. Biol. Chem. 278:39830-39838.
33. Klemm, D. J., P. Watson, M. G. Frid, E. C. Dempsey, J. Schaack, L. A. Colton, A. Nesterova, K. R. Stenmark, and J. E. B. Reusch. 2001. cAMP response element-binding protein content is a molecular determinant of smooth muscle cell proliferation and migration. J. Biol. Chem. 276:46132-46141.
34. Koyama, H., K. E. Bornfeldt, S. Fukumoto, and Y. Nishizawa. 2001. Molecular pathways of cyclic nucleotide-induced inhibition of arterial smooth muscle cell proliferation. J. Cell. Physiol. 186:1-10.
35. Li, F., C. Zhang, S. Schaefer, A. Estes, and K. U. Malik. 2005. ANG II-induced neointimal growth is mediated via cPLA2- and PLD2-activated Akt in balloon-injured rat carotid artery. Am. J. Physiol. Heart Circ. Physiol. 289:H2592-H2601.
36. Lohrum, M. A., D. B. Woods, R. L. Ludwig, E. Balint, and K. H. Vousden. 2001. C-terminal ubiquitination of p53 contributes to nuclear export. Mol. Cell. Biol. 21:8521-8532.
37. Lymn, J. S., K. L. Gallagher, G. F. Clunn, S. E. Fexby, M. K. Patel, and A. D. Hughes. 2003. PDGF stimulates DNA synthesis in human vascular smooth muscle cells via a novel wortmannin-insensitive phosphatidylinositol 3-kinase. FEBS Lett. 555:591-596.
38. Mottet, D., V. Dumont, Y. Deccache, C. Demazy, N. Ninane, M. Raes, and C. Michiels. 2003. Regulation of hypoxia-inducible factor-1a protein level during hypoxic conditions by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3b pathway in HepG2 cells. J. Biol. Chem. 278:31277-31285.
39. Musa, N. L., M. Ramakrishnan, J. Li, S. Kartha, P. Liu, R. G. Pestell, and M. B. Hershenson. 1999. Forskolin inhibits cyclin D1 expression in cultured airway smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 20:352-358.
40. Nagata, D., E. Suzuki, H. Nishimatsu, H. Satonaka, A. Goto, M. Omata, and Y. Hirata. 2001. Transcriptional activation of the cyclin D1 gene is mediated by multiple cis-elements, including SP1 sites and a cAMP-responsive element in vascular endothelial cells. J. Biol. Chem. 276:662-669.
41. Nakata, S., M. Tsutsui, H. Shimokawa, M. Tamura, H. Tasaki, T. Morishita, O. Suda, S. Ueno, Y. Toyohira, Y. Nakashima, and N. Yanagihara. 2005. Vascular neuronal NO synthase is selectively upregulated by platelet-derived growth factor. Involvement of the mitogen-activated protein kinase kinase/extracellular signal-regulated kinase pathway. Arterioscler. Thromb. Vasc. Biol. 25:2502-2508.
42. Newby, A. C., and A. B. Zaltsman. 2000. Molecular mechanisms in intimal hyperplasia. J. Pathol. 190:300-309.
43. Ono, H., T. Ichiki, K. Fukuyama, N. Iino, S. Masuda, K. Egashira, and A. Takeshita. 2004. cAMP-response element-binding protein mediates tumor necrosis factor-alpha-induced vascular smooth muscle cell migration. Arterioscler. Thromb. Vasc. Biol. 24:1634-1639.
44. Osinski, M. T., and K. Schror. 2000. Inhibition of platelet-derived growth factor-induced mitogenesis by phosphodiesterase 3 inhibitors: role of protein kinase A in vascular smooth muscle cell mitogenesis. Biochem. Pharmacol. 60:381-387.
45. Parada, C. A., D. B. Reichling, and J. D. Levine. 2005. Chronic hyperalgesic priming in the rat involves a novel interaction between cAMP and PKCe second messenger pathways. Pain 113:185-190.
46. Perkett, E. A., D. B. Badesch, M. K. Roessler, K. R. Stenmark, and B. Meyrick. 1992. Insulin-like growth factor-1 and pulmonary hypertension induced by continuous air embolism in sheep. Am. Rev. Respir. Cell Mol. Biol. 6:82-87.
47. Radwanska, K., J. Caboche, and L. Kaczmarek. 2005. Extracellular signal-regulated kinases (ERKs) modulate cocaine-induced gene expression in the mouse amygdala. Eur. J. Neurosci. 22:939-948.
48. Rius, J., J. Martinez-Gonzalez, J. Crespo, and L. Badimon. 2004. Involvement of neuron-derived orphan receptor-1 (NOR-1) in LDL-induced mitogenic stimulus in vascular smooth muscle cells: role of CREB. Arterioscler. Thromb. Vasc. Biol. 24:697-702.
49. Rothman, A., B. Wolner, D. Button, and P. Taylor. 1994. Immediate-early gene expression in response to hypertrophic and proliferative stimuli in pulmonary arterial smooth muscle cells. J. Biol. Chem. 269:6399-6404.
50. Rybalkin, S. D., K. E. Bornfeldt, W. K. Sonnenburg, I. G. Rybalkina, K. S. Kwak, K. Hanson, E. G. Krebs, and J. A. Beavo. 1997. Calmodulin-stimulated cyclic nucleotide phosphodiesterase (PDE1C) is induced in the human arterial smooth muscle cells of the synthetic, proliferative phenotype. J. Clin. Investig. 100:2611-2621.
51. Schermuly, R. T., E. Dony, H. A. Ghofrani, S. Pullamsetti, R. Savai, M. Roth, A. Sydykov, Y. J. Lai, N. Weissmann, W. Seeger, and F. Grimminger. 2005. Reversal of experimental pulmonary hypertension by PDGF inhibition. J. Clin. Investig. 115:2691-2694.
52. Seasholtz, T. M., T. Zhang, M. R. Morissette, A. L. Howes, A. H. Yang, and J. H. Brown. 2001. Increased expression and activity of RhoA are associated with increased DNA synthesis and reduced p27(Kip1) expression in the vasculature of hypertensive rats. Circ. Res. 89:488-495.
53. Shaul, P. W., B. Kinanae, M. A. Farrar, M. Buja, and R. R. Magness. 1991. Prostacyclin production and mediation of adenylate cyclase activity in the pulmonary artery: alteration after prolonged hypoxia in the rat. J. Clin. Investig. 88:447-455.
54. Stenmark, K. R., and R. P. Mecham. 1997. Cellular and molecular mechanisms of pulmonary vascular remodeling. Ann. Rev. Physiol. 59:89-144.
55. Stevenson, A. S., L. Cartin, T. L. Wellman, M. H. Dick, M. T. Nelson, and K. M. Lounsbury. 2001. Membrane depolarization mediates phosphorylation and nuclear translocation of CREB in vascular smooth muscle cells. Exp. Cell Res. 263:118-130.
56. Sun, P., H. Enslen, P. S. Myung, and R. A. Maurer. 1994. Differential activation of CREB by Ca2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev. 8:2527-2539.
57. Taylor, C. T., G. T. Furuta, K. Synnestvedt, and S. P. Colgan. 2000. Phosphorylation-dependent targeting of CAMP response element binding protein to the ubiquitin/proteosome pathway in hypoxia. Proc. Natl. Acad. Sci. USA 97:12091-12096.
58. Tokunou, T., T. Ichiki, K. Takeda, Y. Funakoshi, N. Iino, and A. Takeshita. 2001. cAMP response element-binding protein mediates thrombin-induced proliferation of vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 21:1764-1769.
59. Townsend, S. F., V. K. M. Han, and K. R. Stenmark. 1994. Persistence of the fetal pattern of IGF-II expression in the adventitia of small pulmonary arteries in neonatal hypoxic pulmonary hypertension. Growth Regul. 4:S12.
60. Vadiveloo, P. K., E. L. Filonzi, H. R. Stanton, and J. A. Hamilton. 1997. G1 phase arrest of human smooth muscle cells by heparin, IL-4 and cAMP is linked to repression of cyclin D1 and cdk2. Atherosclerosis 133:61-69.
61. van Weeren, P. C., K. M. de Bruyn, A. M. de Vries-Smits, J. van Lint, and B. M. Burgering. 1998. Essential role for protein kinase B (PKB) in insulin-induced glycogen synthase kinase 3 inactivation. Characterization of dominant-negative mutant of PKB. J. Biol. Chem. 273:13150-13156.
62. Vecchione, C., E. Patrucco, G. Marino, L. Barberis, R. Poulet, A. Aretini, A. Maffei, M. T. Gentile, M. Storto, O. Azzolino, M. Brancaccio, G. L. Colussi, U. Bettarini, F. Altruda, L. Silengo, G. Tarone, M. P. Wymann, E. Hirsch, and G. Lembo. 2005. Protection from angiotensin II-mediated vasculotoxic and hypertensive response in mice lacking PI3Kgamma. J. Exp. Med. 18:1217-1228.
63. Weng, Y.-I., and S. D. Shukla. 2003. Effects of chronic ethanol treatment on the angiotensin II-mediated p42/p44 mitogen-activated protein kinase and phosphorylase a activation in rat hepatocytes. Alcohol 29:83-90.
64. Woods, M., E. G. Wood, J. A. Mitchell, and T. D. Warner. 2000. Cyclic AMP regulates cytokine stimulation of endothelin-1 release in human vascular smooth muscle cells. J. Cardiovasc. Pharmacol. 36:5404-5406.
65. Xing, J., D. D. Ginty, and M. E. Greenberg. 1996. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273:959-963.
66. Xing, J., J. M. Kornhauser, Z. Xia, E. A. Thiele, and M. E. Greenberg. 1998. Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol. Cell. Biol. 18:1946-1955.
67. Yamamoto, K. K., G. A. Gonzalez, W. H. Biggs III, and M. R. Montminy. 1988. Phosphorylation-induced binding and transcriptional efficacy of nuclear factor CREB. Nature 334:494-498.
68. Zauli, G., D. Milani, P. Mirandola, M. Mazzoni, P. Secchiero, S. Miscia, and S. Capitani. 2001. HIV-1 Tat protein downregulates CREB transcription factor expression in PC12 neuronal cells through a phosphatidylinositol 3-kinase/Akt/cyclic nucleoside phosphodiesterase pathway. FASEB J. 15:483-491.
69. Zhang, S., C. V. Remillard, I. Fantozzi, and J. X. Yuan. 2004. ATP-induced mitogenesis is mediated by cyclic AMP response element-binding protein-enhanced TRPC4 expression and activity in human pulmonary artery smooth muscle cells. Am. J. Physiol. Cell Physiol. 287:C1192-C1201.