Regulating the Ubiquitin/Proteasome Pathway Via cAMP-signaling: Neuroprotective Potential

Cell Biochemistry and Biophysics

Volumn 67, Issue 1, 2013, Pages 55-66

  Huang, He ^a   Wang, Hu ^a   Figueiredo Pereira, Maria E ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

cAMP; Protein aggregation; Therapy; Ubiquitin proteasome pathway

Indexed keywords

CYCLIC AMP; FORSKOLIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; PHOSPHODIESTERASE INHIBITOR; PROTEASOME; UBIQUITIN; VASODILATOR AGENT;

ARTICLE; DEGENERATIVE DISEASE; HUMAN; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

COLFORSIN; CYCLIC AMP; HUMANS; NEURODEGENERATIVE DISEASES; PHOSPHODIESTERASE INHIBITORS; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION; UBIQUITIN; VASODILATOR AGENTS;

EID: 84883453346     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12013-013-9628-2     Document Type: Article

References (126)

1. Kebabian, J. W., Petzold, G. L., & Greengard, P. (1972). Dopamine-sensitive adenylate cyclase in caudate nucleus of rat brain, and its similarity to the "dopamine receptor". Proceedings of the National Academy of Sciences, 69, 2145-2149.
2. Ravindran, S. (2011). Paul Greengard: Signals underlying moods, addictions, and brain disorders. Proceedings of the National Academy of Sciences, 108, 18872-18874.
3. Kamenetsky, M., Middelhaufe, S., Bank, E. M., Levin, L. R., Buck, J., & Steegborn, C. (2006). Molecular details of cAMP generation in mammalian cells: A tale of two systems. Journal of Molecular Biology, 362, 623-639.
4. Pavan, B., Biondi, C., & Dalpiaz, A. (2009). Adenylyl cyclases as innovative therapeutic goals. Drug Discovery Today, 14, 982-991.
5. Tresguerres, M., Levin, L. R., & Buck, J. (2011). Intracellular cAMP signaling by soluble adenylyl cyclase. Kidney International, 79, 1277-1288.
6. Braun, T., & Dods, R. F. (1975). Development of a Mn-2+ -sensitive, "soluble" adenylate cyclase in rat testis. Proceedings of the National Academy of Sciences, 72, 1097-1101.
7. Pierre, S., Eschenhagen, T., Geisslinger, G., & Scholich, K. (2009). Capturing adenylyl cyclases as potential drug targets. Nature Reviews Drug Discovery, 8, 321-335.
8. 2+ -stimulated adenylyl cyclases. Journal of Neuroscience, 31, 10174-10183.
9. Dunn, T. A., Storm, D. R., & Feller, M. B. (2009). Calcium-dependent increases in protein kinase-A activity in mouse retinal ganglion cells are mediated by multiple adenylate cyclases. PLoS ONE, 4, e7877.
10. Schwoch, G., Trinczek, B., & Bode, C. (1990). Localization of catalytic and regulatory subunits of cyclic AMP-dependent protein kinases in mitochondria from various rat tissues. Biochemical Journal, 270, 181-188.
11. Acin-Perez, R., Salazar, E., Kamenetsky, M., Buck, J., Levin, L. R., & Manfredi, G. (2009). Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metabolism, 9, 265-276.
12. Papa, S., Sardanelli, A. M., Scacco, S., & Technikova-Dobrova, Z. (1999). cAMP-dependent protein kinase and phosphoproteins in mammalian mitochondria. An extension of the cAMP-mediated intracellular signal transduction. FEBS Letters, 444, 245-249.
13. Chen, J., Levin, L. R., & Buck, J. (2012). Role of soluble adenylyl cyclase in the heart. American Journal of Physiology Heart and Circulatory Physiology, 302, H538-H543.
14. Appukuttan, A., Kasseckert, S. A., Micoogullari, M., Flacke, J. P., Kumar, S., Woste, A., et al. (2012). Type 10 adenylyl cyclase mediates mitochondrial Bax translocation and apoptosis of adult rat cardiomyocytes under simulated ischaemia/reperfusion. Cardiovascular Research, 93, 340-349.
15. Nunes, A. R., Monteiro, E. C., Johnson, S. M., & Gauda, E. B. (2009). Bicarbonate-regulated soluble adenylyl cyclase (sAC) mRNA expression and activity in peripheral chemoreceptors. Advances in Experimental Medicine and Biology, 648, 235-241.
16. Cooper, D. M., & Crossthwaite, A. J. (2006). Higher-order organization and regulation of adenylyl cyclases. Trends in Pharmacological Sciences, 27, 426-431.
17. Francis, S. H., Blount, M. A., & Corbin, J. D. (2011). Mammalian cyclic nucleotide phosphodiesterases: Molecular mechanisms and physiological functions. Physiological Reviews, 91, 651-690.
18. Hebb, A. L., & Robertson, H. A. (2007). Role of phosphodiesterases in neurological and psychiatric disease. Current Opinion in Pharmacology, 7, 86-92.
19. Schudt, C., Hatzelmann, A., Beume, R., & Tenor, H. (2011). Phosphodiesterase inhibitors: History of pharmacology. Handbook of Experimental Pharmacology, 204, 1-46.
20. Corbin, J. D., & Francis, S. H. (2003). Molecular biology and pharmacology of PDE-5-inhibitor therapy for erectile dysfunction. Journal of Andrology, 24, S38-S41.
21. Walsh, D. A., Perkins, J. P., & Krebs, E. G. (1968). An adenosine 3′, 5′-monophosphate-dependant protein kinase from rabbit skeletal muscle. Journal of Biological Chemistry, 243, 3763-3765.
22. Zhou, M., Fisher, E. A., & Ginsberg, H. N. (1998). Regulated co-translational ubiquitination of apolipoprotein B100. A new paradigm for proteasomal degradation of a secretory protein. Journal of Biological Chemistry, 273, 24649-24653.
23. Kawasaki, H., Springett, G. M., Mochizuki, N., Toki, S., Nakaya, M., Matsuda, M., et al. (1998). A family of cAMP-binding proteins that directly activate Rap1. Science, 282, 2275-2279.
24. Dwivedi, Y., & Pandey, G. N. (2011). Elucidating biological risk factors in suicide: Role of protein kinase A. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 35, 831-841.
25. Cheng, X., Ma, Y., Moore, M., Hemmings, B. A., & Taylor, S. S. (1998). Phosphorylation and activation of cAMP-dependent protein kinase by phosphoinositide-dependent protein kinase. Proceedings of the National Academy Science USA, 95, 9849-9854.
26. Cauthron, R. D., Carter, K. B., Liauw, S., & Steinberg, R. A. (1998). Physiological phosphorylation of protein kinase A at Thr-197 is by a protein kinase A kinase. Molecular and Cellular Biology, 18, 1416-1423.
27. Taylor, S. S., Buechler, J. A., & Yonemoto, W. (1990). cAMP-dependent protein kinase: Framework for a diverse family of regulatory enzymes. Annual Review of Biochemistry, 59, 971-1005.
28. Hidaka, H., Watanabe, M., & Kobayashi, R. (1991). Properties and use of H-series compounds as protein kinase inhibitors. Methods in Enzymology, 201, 328-339.
29. Davies, S. P., Reddy, H., Caivano, M., & Cohen, P. (2000). Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochemical Journal, 351, 95-105.
30. Lochner, A., & Moolman, J. A. (2006). The many faces of H89: A review. Cardiovascular Drug Reviews, 24, 261-274.
31. Wolfl, S., Martinez, C., & Majzoub, J. A. (1999). Inducible binding of cyclic adenosine 3′, 5′-monophosphate (cAMP)-responsive element binding protein (CREB) to a cAMP-responsive promoter in vivo. Molecular Endocrinology, 13, 659-669.
32. Scott, J. D., Stofko, R. E., McDonald, J. R., Comer, J. D., Vitalis, E. A., & Mangili, J. A. (1990). Type II regulatory subunit dimerization determines the subcellular localization of the cAMP-dependent protein kinase. Journal of Biological Chemistry, 265, 21561-21566.
33. Silva, A. J., Kogan, J. H., Frankland, P. W., & Kida, S. (1998). CREB and memory. Annual Review of Neuroscience, 21, 127-148.
34. Springett, G. M., Kawasaki, H., & Spriggs, D. R. (2004). Non-kinase second-messenger signaling: New pathways with new promise. BioEssays, 26, 730-738.
35. de Rooij, J., Rehmann, H., van Triest, M., Cool, R. H., Wittinghofer, A., & Bos, J. L. (2000). Mechanism of regulation of the Epac family of cAMP-dependent RapGEFs. Journal of Biological Chemistry, 275, 20829-20836.
36. Bos, J. L., Rehmann, H., & Wittinghofer, A. (2007). GEFs and GAPs: Critical elements in the control of small G proteins. Cell, 129, 865-877.
37. Gloerich, M., & Bos, J. L. (2010). Epac: Defining a new mechanism for cAMP action. Annual Review of Pharmacology and Toxicology, 50, 355-375.
38. Rehmann, H., Das, J., Knipscheer, P., Wittinghofer, A., & Bos, J. L. (2006). Structure of the cyclic-AMP-responsive exchange factor Epac2 in its auto-inhibited state. Nature, 439, 625-628.
39. Rehmann, H., rias-Palomo, E., Hadders, M. A., Schwede, F., Llorca, O., & Bos, J. L. (2008). Structure of Epac2 in complex with a cyclic AMP analogue and RAP1B. Nature, 455, 124-127.
40. Feliciello, A., Gottesman, M. E., & Avvedimento, E. V. (2001). The biological functions of A-kinase anchor proteins. Journal of Molecular Biology, 308, 99-114.
41. Skroblin, P., Grossmann, S., Schafer, G., Rosenthal, W., & Klussmann, E. (2010). Mechanisms of protein kinase A anchoring. International Review of Cell Molecular Biology, 283, 235-330.
42. Carnegie, G. K., Means, C. K., & Scott, J. D. (2009). A-kinase anchoring proteins: From protein complexes to physiology and disease. IUBMB Life, 61, 394-406.
43. Dessauer, C. W. (2009). Adenylyl cyclase-A-kinase anchoring protein complexes: The next dimension in cAMP signaling. Molecular Pharmacology, 76, 935-941.
44. Scott, J. D., Dessauer, C. W., & Tasken, K. (2013). Creating order from chaos: Cellular regulation by kinase anchoring. Annual Review of Pharmacology and Toxicology, 53, 187-210.
45. Pidoux, G., & Tasken, K. (2010). Specificity and spatial dynamics of protein kinase A signaling organized by A-kinase-anchoring proteins. Journal of Molecular Endocrinology, 44, 271-284.
46. Hundsrucker, C., & Klussmann, E. (2008). Direct AKAP-mediated protein-protein interactions as potential drug targets. Handbook of Experimental Pharmacology, 186, 483-503.
47. Troger, J., Moutty, M. C., Skroblin, P., & Klussmann, E. (2012). A-kinase anchoring proteins as potential drug targets. British Journal of Pharmacology, 166, 420-433.
48. Kovanich, D., Aye, T. T., Heck, A. J., & Scholten, A. (2012). Probing the specificity of protein-protein interactions by quantitative chemical proteomics. Methods in Molecular Biology, 803, 167-181.
49. Vaudry, D., Falluel-Morel, A., Bourgault, S., Basille, M., Burel, D., Wurtz, O., et al. (2009). Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacological Reviews, 61, 283-357.
50. Shneider, Y., Shtrauss, Y., Yadid, G., & Pinhasov, A. (2010). Differential expression of PACAP receptors in postnatal rat brain. Neuropeptides, 44, 509-514.
51. Eiden, L. E., Samal, B., Gerdin, M. J., Mustafa, T., Vaudry, D., & Stroth, N. (2008). Discovery of pituitary adenylate cyclase-activating polypeptide-regulated genes through microarray analyses in cell culture and in vivo. Annals of the New York Academy of Sciences, 1144, 6-20.
52. Gasperini, L., Piubelli, C., & Carboni, L. (2012). Proteomics of rat hypothalamus, hippocampus and pre-frontal/frontal cortex after central administration of the neuropeptide PACAP. Molecular Biology Reports, 39, 2921-2935.
53. Holighaus, Y., Weihe, E., & Eiden, L. E. (2012). STC1 induction by PACAP is mediated through cAMP and ERK1/2 but not PKA in cultured cortical neurons. Journal of Molecular Neuroscience, 46, 75-87.
54. Nakamachi, T., Li, M., Shioda, S., & Arimura, A. (2006). Signaling involved in pituitary adenylate cyclase-activating polypeptide-stimulated ADNP expression. Peptides, 27, 1859-1864.
55. Reglodi, D., Kiss, P., Lubics, A., & Tamas, A. (2011). Review on the protective effects of PACAP in models of neurodegenerative diseases in vitro and in vivo. Current Pharmaceutical Design, 17, 962-972.
56. Wu, K. Y., Zippin, J. H., Huron, D. R., Kamenetsky, M., Hengst, U., Buck, J., et al. (2006). Soluble adenylyl cyclase is required for netrin-1 signaling in nerve growth cones. Nature Neuroscience, 9, 1257-1264.
57. Rat, D., Schmitt, U., Tippmann, F., Dewachter, I., Theunis, C., Wieczerzak, E., et al. (2011). Neuropeptide pituitary adenylate cyclase-activating polypeptide (PACAP) slows down Alzheimer's disease-like pathology in amyloid precursor protein-transgenic mice. FASEB Journal, 25, 3208-3218.
58. Fang, K. M., Chen, J. K., Hung, S. C., Chen, M. C., Wu, Y. T., Wu, T. J., et al. (2010). Effects of combinatorial treatment with pituitary adenylate cyclase activating peptide and human mesenchymal stem cells on spinal cord tissue repair. PLoS ONE, 5, e15299.
59. Tomimatsu, N., & Arakawa, Y. (2008). Survival-promoting activity of pituitary adenylate cyclase-activating polypeptide in the presence of phosphodiesterase inhibitors on rat motoneurons in culture: cAMP-protein kinase A-mediated survival. Journal of Neurochemistry, 107, 628-635.
60. Endo, K., Nakamachi, T., Seki, T., Kagami, N., Wada, Y., Nakamura, K., et al. (2011). Neuroprotective effect of PACAP against NMDA-induced retinal damage in the mouse. Journal of Molecular Neuroscience, 43, 22-29.
61. Botia, B., Jolivel, V., Burel, D., Le Joncour, V., Roy, V., Naassila, M., et al. (2011). Neuroprotective effects of PACAP against ethanol-induced toxicity in the developing rat cerebellum. Neurotoxicity Research, 19, 423-434.
62. Cameron, D. B., Raoult, E., Galas, L., Jiang, Y., Lee, K., Hu, T., et al. (2009). Role of PACAP in controlling granule cell migration. Cerebellum, 8, 433-440.
63. -/- mutant cerebellum. Journal of Molecular Neuroscience, 36, 38-44.
64. Ago, Y., Yoneyama, M., Ishihama, T., Kataoka, S., Kawada, K., Tanaka, T., et al. (2011). Role of endogenous pituitary adenylate cyclase-activating polypeptide in adult hippocampal neurogenesis. Neuroscience, 172, 554-561.
65. Scharf, E., May, V., Braas, K. M., Shutz, K. C., & Mao-Draayer, Y. (2008). Pituitary adenylate cyclase-activating polypeptide (PACAP) and vasoactive intestinal peptide (VIP) regulate murine neural progenitor cell survival, proliferation, and differentiation. Journal of Molecular Neuroscience, 36, 79-88.
66. Masmoudi-Kouki, O., Douiri, S., Hamdi, Y., Kaddour, H., Bahdoudi, S., Vaudry, D., et al. (2011). Pituitary adenylate cyclase-activating polypeptide protects astroglial cells against oxidative stress-induced apoptosis. Journal of Neurochemistry, 117, 403-411.
67. Castorina, A., Tiralongo, A., Giunta, S., Carnazza, M. L., Rasi, G., & D'Agata, V. (2008). PACAP and VIP prevent apoptosis in schwannoma cells. Brain Research, 1241, 29-35.
68. Yang, S., Yang, J., Yang, Z., Chen, P., Fraser, A., Zhang, W., et al. (2006). Pituitary adenylate cyclase-activating polypeptide (PACAP) 38 and PACAP4-6 are neuroprotective through inhibition of NADPH oxidase: Potent regulators of microglia-mediated oxidative stress. Journal of Pharmacology and Experimental Therapeutics, 319, 595-603.
69. Dejda, A., Seaborn, T., Bourgault, S., Touzani, O., Fournier, A., Vaudry, H., et al. (2011). PACAP and a novel stable analog protect rat brain from ischemia: Insight into the mechanisms of action. Peptides, 32, 1207-1216.
70. Doan, N. D., Bourgault, S., Dejda, A., Letourneau, M., Detheux, M., Vaudry, D., et al. (2011). Design and in vitro characterization of PAC1/VPAC1-selective agonists with potent neuroprotective effects. Biochemical Pharmacology, 81, 552-561.
71. Bourgault, S., Vaudry, D., Segalas-Milazzo, I., Guilhaudis, L., Couvineau, A., Laburthe, M., et al. (2009). Molecular and conformational determinants of pituitary adenylate cyclase-activating polypeptide (PACAP) for activation of the PAC1 receptor. Journal of Medicinal Chemistry, 52, 3308-3316.
72. Bourgault, S., Vaudry, D., Guilhaudis, L., Raoult, E., Couvineau, A., Laburthe, M., et al. (2008). Biological and structural analysis of truncated analogs of PACAP27. Journal of Molecular Neuroscience, 36, 260-269.
73. Iwatsubo, K., Okumura, S., & Ishikawa, Y. (2006). Drug therapy aimed at adenylyl cyclase to regulate cyclic nucleotide signaling. Endocrine, Metabolic & Immune Disorders Drug Targets, 6, 239-247.
74. Insel, P. A., & Ostrom, R. S. (2003). Forskolin as a tool for examining adenylyl cyclase expression, regulation, and G protein signaling. Cellular and Molecular Neurobiology, 23, 305-314.
75. Maruoka, H., Sasaya, H., Sugihara, K., Shimoke, K., & Ikeuchi, T. (2011). Low-molecular-weight compounds having neurotrophic activity in cultured PC12 cells and neurons. Journal of Biochemistry, 150, 473-475.
76. Tegenge, M. A., Stern, M., & Bicker, G. (2009). Nitric oxide and cyclic nucleotide signal transduction modulates synaptic vesicle turnover in human model neurons. Journal of Neurochemistry, 111, 1434-1446.
77. Tegenge, M. A., Roloff, F., & Bicker, G. (2011). Rapid differentiation of human embryonal carcinoma stem cells (NT2) into neurons for neurite outgrowth analysis. Cellular and Molecular Neurobiology, 31, 635-643.
78. Hannila, S. S., & Filbin, M. T. (2008). The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Experimental Neurology, 209, 321-332.
79. Posternak, T., Sutherland, E. W., & Henion, W. F. (1962). Derivatives of cyclic 3′, 5′-adenosine monophosphate. Biochimica et Biophysica Acta, 65, 558-560.
80. Schwede, F., Maronde, E., Genieser, H., & Jastorff, B. (2000). Cyclic nucleotide analogs as biochemical tools and prospective drugs. Pharmacology & Therapeutics, 87, 199-226.
81. Szentandrassy, N., Harmati, G., Farkas, V., Horvath, B., Hegyi, B., Magyar, J., et al. (2011). Modified cAMP derivatives: Powerful tools in heart research. Current Medicinal Chemistry, 18, 3729-3736.
82. Jastorff, B., Hoppe, J., & Morr, M. (1979). A model for the chemical interactions of adenosine 3′: 5′-Monophosphate with the R subunit of protein kinase type I. Refinement of the cyclic phosphate binding moiety of protein kinase type I. European Journal of Biochemistry, 101, 555-561.
83. Krass, J. D., Jastorff, B., & Genieser, H. G. (1997). Determination of lipophilicity by gradient elution high-performance liquid chromatography. Analytical Chemistry, 69, 2575-2581.
84. Bertinetti, D., Schweinsberg, S., Hanke, S. E., Schwede, F., Bertinetti, O., Drewianka, S., et al. (2009). Chemical tools selectively target components of the PKA system. BMC Chemical Biology, 9, 3.
85. 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. British Journal of Pharmacology, 159, 265-284.
86. Enserink, J. M., Christensen, A. E., de Rooij, J., van Triest, M., Schwede, F., Genieser, H. G., et al. (2002). A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nature Cell Biology, 4, 901-906.
87. Rehmann, H., Schwede, F., Doskeland, S. O., Wittinghofer, A., & Bos, J. L. (2003). Ligand-mediated activation of the cAMP-responsive guanine nucleotide exchange factor Epac. Journal of Biological Chemistry, 278, 38548-38556.
88. Holz, G. G., Chepurny, O. G., & Schwede, F. (2008). Epac-selective cAMP analogs: New tools with which to evaluate the signal transduction properties of cAMP-regulated guanine nucleotide exchange factors. Cellular Signalling, 20, 10-20.
89. McPhee, I., Gibson, L. C., Kewney, J., Darroch, C., Stevens, P. A., Spinks, D., et al. (2005). Cyclic nucleotide signalling: A molecular approach to drug discovery for Alzheimer's disease. Biochemical Society Transactions, 33, 1330-1332.
90. Borner, S., Schwede, F., Schlipp, A., Berisha, F., Calebiro, D., Lohse, M. J., et al. (2011). FRET measurements of intracellular cAMP concentrations and cAMP analog permeability in intact cells. Nature Protocols, 6, 427-438.
91. Breckler, M., Berthouze, M., Laurent, A. C., Crozatier, B., Morel, E., & Lezoualc'h, F. (2011). Rap-linked cAMP signaling Epac proteins: Compartmentation, functioning and disease implications. Cellular Signalling, 23, 1257-1266.
92. Bos, J. L. (2006). Epac proteins: Multi-purpose cAMP targets. Trends in Biochemical Sciences, 31, 680-686.
93. Ster, J., De, B. F., Bertaso, F., Abitbol, K., Daniel, H., Bockaert, J., et al. (2009). Epac mediates PACAP-dependent long-term depression in the hippocampus. Journal of Physiology, 587, 101-113.
94. Morales-Garcia, J. A., Redondo, M., onso-Gil, S., Gil, C., Perez, C., Martinez, A., et al. (2011). Phosphodiesterase 7 inhibition preserves dopaminergic neurons in cellular and rodent models of Parkinson disease. PLoS ONE, 6, e17240.
95. Yang, L., Calingasan, N. Y., Lorenzo, B. J., & Beal, M. F. (2008). Attenuation of MPTP neurotoxicity by rolipram, a specific inhibitor of phosphodiesterase IV. Experimental Neurology, 211, 311-314.
96. Sasaki, T., Kitagawa, K., Omura-Matsuoka, E., Todo, K., Terasaki, Y., Sugiura, S., et al. (2007). The phosphodiesterase inhibitor rolipram promotes survival of newborn hippocampal neurons after ischemia. Stroke, 38, 1597-1605.
97. Farooq, M. U., Naravetla, B., Moore, P. W., Majid, A., Gupta, R., & Kassab, M. Y. (2008). Role of sildenafil in neurological disorders. Clinical Neuropharmacology, 31, 353-362.
98. Jiang, H., Nucifora, F. C, Jr, Ross, C. A., & DeFranco, D. B. (2003). Cell death triggered by polyglutamine-expanded huntingtin in a neuronal cell line is associated with degradation of CREB-binding protein. Human Molecular Genetics, 12, 1-12.
99. Nucifora, F. C, Jr, Sasaki, M., Peters, M. F., Huang, H., Cooper, J. K., Yamada, M., et al. (2001). Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science, 291, 2423-2428.
100. Steffan, J. S., Bodai, L., Pallos, J., Poelman, M., McCampbell, A., Apostol, B. L., et al. (2001). Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature, 413, 739-743.
101. Castro, L. R., Gervasi, N., Guiot, E., Cavellini, L., Nikolaev, V. O., Paupardin-Tritsch, D., et al. (2010). Type 4 phosphodiesterase plays different integrating roles in different cellular domains in pyramidal cortical neurons. Journal of Neuroscience, 30, 6143-6151.
102. DeMarch, Z., Giampa, C., Patassini, S., Martorana, A., Bernardi, G., & Fusco, F. R. (2007). Beneficial effects of rolipram in a quinolinic acid model of striatal excitotoxicity. Neurobiology of Diseases, 25, 266-273.
103. Giampa, C., Middei, S., Patassini, S., Borreca, A., Marullo, F., Laurenti, D., et al. (2009). Phosphodiesterase type IV inhibition prevents sequestration of CREB binding protein, protects striatal parvalbumin interneurons and rescues motor deficits in the R6/2 mouse model of Huntington's disease. European Journal of Neuroscience, 29, 902-910.
104. DeMarch, Z., Giampa, C., Patassini, S., Bernardi, G., & Fusco, F. R. (2008). Beneficial effects of rolipram in the R6/2 mouse model of Huntington's disease. Neurobiology of Diseases, 30, 375-387.
105. Giampa, C., Laurenti, D., Anzilotti, S., Bernardi, G., Menniti, F. S., & Fusco, F. R. (2010). Inhibition of the striatal specific phosphodiesterase PDE10A ameliorates striatal and cortical pathology in R6/2 mouse model of Huntington's disease. PLoS ONE, 5, e13417.
106. Nijholt, D. A., De Kimpe, L., Elfrink, H. L., Hoozemans, J. J., & Scheper, W. (2011). Removing protein aggregates: The role of proteolysis in neurodegeneration. Current Medicinal Chemistry, 18, 2459-2476.
107. Huang, Q., & Figueiredo-Pereira, M. E. (2010). Ubiquitin/proteasome pathway impairment in neurodegeneration: Therapeutic implications. Apoptosis, 15, 1292-1311.
108. Wang, X., Li, J., Zheng, H., Su, H., & Powell, S. R. (2011). Proteasome functional insufficiency in cardiac pathogenesis. American Journal of Physiology Heart and Circulatory Physiology, 301, H2207-H2219.
109. Rideout, H. J., Larsen, K. E., Sulzer, D., & Stefanis, L. (2001). Proteasomal inhibition leads to formation of ubiquitin/alpha-synuclein-immunoreactive inclusions in PC12 cells. Journal of Neurochemistry, 78, 899-908.
110. Metcalfe, M. J., Huang, Q., & Figueiredo-Pereira, M. E. (2012). Coordination between proteasome impairment and caspase activation leading to TAU pathology: Neuroprotection by cAMP. Cell Death and Disease, 3, e326.
111. Myeku, N., Wang, H., & Figueiredo-Pereira, M. E. (2012). cAMP stimulates the ubiquitin/proteasome pathway in rat spinal cord neurons. Neuroscience Letters, 527, 126-131.
112. 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. Autophagy, 6, 1198-1200.
113. Drews, O., Tsukamoto, O., Liem, D., Streicher, J., Wang, Y., & Ping, P. (2010). Differential regulation of proteasome function in isoproterenol-induced cardiac hypertrophy. Circulation Research, 107, 1094-1101.
114. Asai, M., Tsukamoto, O., Minamino, T., Asanuma, H., Fujita, M., Asano, Y., et al. (2009). PKA rapidly enhances proteasome assembly and activity in in vivo canine hearts. Journal of Molecular and Cellular Cardiology, 46, 452-462.
115. Zong, C., Gomes, A. V., Drews, O., Li, X., Young, G. W., Berhane, B., et al. (2006). Regulation of murine cardiac 20S proteasomes: Role of associating partners. Circulation Research, 99, 372-380.
116. Lu, H., Zong, C., Wang, Y., Young, G. W., Deng, N., Souda, P., et al. (2008). Revealing the dynamics of the 20S proteasome phosphoproteome: A combined CID and electron transfer dissociation approach. Molecular and Cellular Proteomics, 7, 2073-2089.
117. 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. Cellular Signalling, 22, 1240-1246.
118. Hanna, J., & Finley, D. (2007). A proteasome for all occasions. FEBS Letters, 581, 2854-2861.
119. Zhang, F., Paterson, A. J., Huang, P., Wang, K., & Kudlow, J. E. (2007). Metabolic control of proteasome function. Physiology (Bethesda), 22, 373-379.
120. Pereira, M. E., & Wilk, S. (1990). Phosphorylation of the multicatalytic proteinase complex from bovine pituitaries by a copurifying cAMP-dependent protein kinase. Archives of Biochemistry and Biophysics, 283, 68-74.
121. Marambaud, P., Wilk, S., & Checler, F. (1996). Protein kinase A phosphorylation of the proteasome: A contribution to the alpha-secretase pathway in human cells. Journal of Neurochemistry, 67, 2616-2619.
122. Zhang, F., Hu, Y., Huang, P., Toleman, C. A., Paterson, A. J., & Kudlow, J. E. (2007). Proteasome function is regulated by cyclic AMP-dependent protein kinase through phosphorylation of Rpt6. Journal of Biological Chemistry, 282, 22460-22471.
123. Goncalves, D. A., Lira, E. C., Baviera, A. M., Cao, P., Zanon, N. M., Arany, Z., et al. (2009). Mechanisms involved in 3′, 5′-cyclic adenosine monophosphate-mediated inhibition of the ubiquitin-proteasome system in skeletal muscle. Endocrinology, 150, 5395-5404.
124. Lira, E. C., Goncalves, D. A., Parreiras-E-Silva, L. T., Zanon, N. M., Kettelhut, I. C., & Navegantes, L. C. (2011). Phosphodiesterase-4 inhibition reduces proteolysis and atrogenes expression in rat skeletal muscles. Muscle and Nerve, 44, 371-381.
125. Carlucci, A., Lignitto, L., & Feliciello, A. (2008). Control of mitochondria dynamics and oxidative metabolism by cAMP, AKAPs and the proteasome. Trends in Cell Biology, 18, 604-613.
126. Edelmann, M. J., Nicholson, B., & Kessler, B. M. (2011). Pharmacological targets in the ubiquitin system offer new ways of treating cancer, neurodegenerative disorders and infectious diseases. Expert Reviews in Molecular Medicine, 13, e35.