Phosphodiesterase-4 inhibition reduces proteolysis and atrogenes expression in rat skeletal muscles

Muscle and Nerve

Volumn 44, Issue 3, 2011, Pages 371-381

  Lira, Eduardo C ^a   GonçAlves, Dawit A P ^a   Parreiras E Silva, Lucas T ^a   Zanon, Neusa M ^a   Kettelhut, Isis C ^a   Navegantes, Luiz C C ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Atrogenes; Autophagy; Camp; Phosphodiesterase; Proteolysis

Indexed keywords

ATROGIN 1; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; MESSENGER RNA; MUSCLE RING FINGER 1 PROTEIN; PHOSPHODIESTERASE IV; PROTEASOME; PROTEIN KINASE B; ROLIPRAM; TYROSINE; UBIQUITIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HUMAN; MALE; MICRODIALYSIS; MUSCLE ATROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; SKELETAL MUSCLE;

ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; GENE EXPRESSION; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, ANIMAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; PHOSPHODIESTERASE 4 INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; ROLIPRAM; SKP CULLIN F-BOX PROTEIN LIGASES; TYROSINE; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 80052047753     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.22066     Document Type: Article

References (53)

1. Bloom TJ. Cyclic nucleotide phosphodiesterase isozymes expressed in mouse skeletal muscle. Can J Physiol Pharmacol 2002;80: 1132-1135.
2. Omori K, Kotera J. Overview of PDEs and their regulation. Circ Res 2007;100:309-327.
3. Sette C, Conti M. Phosphorylation and activation of a cAMP-specific phosphodiesterase by the cAMP-dependent protein kinase. J Biol Chem 1996;271:16526-16534.
4. Hoffmann R, Baillie GS, MacKenzie SJ, Yarwood SJ, Houslay MD. The MAP kinase ERK2 inhibits the cyclic AMP-specific phosphodies-terase HSPDE4D3 by phosphorylating it at Ser579. EMBO J 1999;18: 893-903.
5. Moher D, Pham B, Ausejo M, Saenz A, Hood S, Barber GG. Pharmacological management of intermittent claudication: a meta-analysis of randomised trials. Drugs 2000;59:1057-1070.
6. Combaret L, Tilignac T, Claustre A, Voisin L, Taillandier D, Obled C et al. Torbafylline (HWA 448) inhibits enhanced skeletal muscle ubiquitin-proteasome-dependent proteolysis in cancer and septic rats. Biochem J 2002;15:185-192.
7. Vary T, Dardevet D, Grizard J, Voisin L, Buffiere C, Denis P, et al. Pentoxifylline improves insulin action limiting skeletal muscle catab-olism after infection. J Endocrinol 1999;163:15-24.
8. 2{thorn}-dependent and ATP pro-teasome-dependent proteolysis in skeletal muscle from acutely diabetic rats. Am J Physiol Endocrinol Metab 2007;292:E702-E708.
9. Endres S, Fülle HJ, Sinha B, Stroll D, Dinarello CA, Gerzer R, et al. Cyclic nucleotides differentially regulate the synthesis of tumour necrosis factor-alpha and interleukin-1 beta by human mononuclear cells. Immunology 1991;72:56-60.
10. Hinkle RT, Dolan E, Cody DB, Bauer MB, Isfort RJ. Phosphodiester-ase 4 inhibition reduces skeletal muscle atrophy. Muscle Nerve 2005; 32:775-781.
11. Lira EC, Graça FA, Gonçalves DA, Zanon NM, Baviera AM, Strind-berg L, et al. Cyclic adenosine monophosphate-phosphodiesterase inhibitors reduce skeletal muscle protein catabolism in septic rats. Shock 2007;27:687-694.
12. Barnette MS, Underwood DC. New phosphodiesterase inhibitors as therapeutics for the treatment of chronic lung disease. Curr Opin Pulm Med 2007;6:164-169.
13. Spina D. Phosphodiesterase-4 inhibitors in the treatment of inflammatory lung disease. Drugs 2003;63:2575-2594.
14. Torphy TJ, Page C. Phosphodiesterases: journey towards therapeutics. Trends Pharm Sci 2000;21:157-159.
15. Scott SV, Klionsky DJ. Delivery of proteins and organelles to the vacuole from the cytoplasm. Curr Opin Cell Biol 1998;10:523-529.
16. Attaix D, Aurousseau E, Combaret L, Kee A, Larbaud D, Ralliere C, et al. Ubiquitin-proteasome dependent proteolysis in skeletal muscle. Reprod Nutr Dev 1998;38:153-168.
17. Jagoe RT, Goldberg AL. What we really know about the ubiquitin- proteasome pathway in muscle atrophy? Curr Opin Clin Nutr Metab Care 2001;4:183-190.
18. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, et al. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 2004;18:39-51.
19. Sacheck JM, Hyatt JP, Raffaello A, Jagoe RT, Roy RR, Edgerton VR, et al. Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 2007;21:140-155.
20. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 2001;294:1704-1708.
21. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL. Atrogin-1, a muscle-specific-F box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 2001;98:14440-14445.
22. Tanida I, Ueno T, Kominami E. LC3 and autophagy. Methods Mol Biol 2008;445:77-88.
23. Bechet D, Tassa A, Taillandier D, Combaret L, Attaix D. Lysosomal proteolysis in skeletal muscle. Int J Biochem Cell Biol 2005;37: 2098-2114.
24. Furuno K, Goodman MN, Goldberg AL. Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J Biol Chem 1990;265:8550-8557.
25. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, et al. FoxO3 coordinately activates protein degradation by the autopha-gic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007;6:472-483.
26. Ungerstedt U. Microdialysis-principles and application for studies in animals and man. J Intern Med 1991;230:365-373.
27. Waalkes TP, Udenfriend SA. A fluorimetric method for stimation of tyrosine in plasma and tissue. J Lab Clin Med 1957;50:733-736.
28. Kettelhut IC, Wing SS, Goldberg AL. Endocrine regulation of protein breakdown in skeletal muscle. Diabetes Metab Rev 1988;4: 751-772.
29. Lönnroth P, Strindberg L. Validation of the internal reference techi-nique for calibrating microdialysis catheters in situ. Acta Physiol Scand 1995;153:375-380.
30. Hickner RC, Rosdahl H, Borg L, Ungerstedt U, Jorfeldt L, Henriks-son J. The ethanol technique of monitoring local blood flow changes in rat skeletal muscle: implications for microdialysis. Acta Physiol Scand 1992;146:87-97.
31. Cikos S, Bukovska A, Koppel J. Relative quantification of mRNA: comparison of methods currently used for real-time PCR data analysis. BMC Mol Biol 2007;8:113-127.
32. Lowry OH, Rosebrough NJ, Farr AL, Randall RF. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-275.
33. Gore DC, Wolfe RR, Chinkes DL. Quantification of amino acid transport through interstitial fluid: assessment of four-compartment modeling for muscle protein kinetics. Am J Physiol Endocrinol Metab 2006;292:E319-E323.
34. Gutierrez A, Anderstam B, Alvestrand A. Amino acid concentration in the interstitium of human skeletal muscle: a microdialysis study. Eur J Clin Invest 1999;29:947-952.
35. Korkmaz S, Maupoil V, Sobry C, Brunet C, Chevalier S, Freslon JL. An increased regional blood flow precedes mesenteric inflammation in rats treated by a phosphodiesterase 4 inhibitor. Toxicol Sci 2009; 107:298-305.
36. Navegantes LC, Resano NM, Migliorini RH, Kettelhut IC. Role of adrenoceptors and cAMP on the catecholamine-induced inhibition of proteolysis in rat skeletal muscle. Am J Physiol Endocrinol Metab 2000;279:E663-E668.
37. Mizrachi K, Aricha R, Feferman T, Kela-Madar N, Mandel I, Papema T, et al. Involvement of phosphodiesterases in autoimmune diseases. J Neuroimmunol 2010;220:43-51.
38. McArdle A, Edwards RH, Jackson MJ. Effects of contractile activity on muscle damage in the dystrophin-deficient mdx mouse. Clin Sci (Lond) 1991;80:367-371.
39. Bingham J, Sudarsanam S, Srinivasan S. Profiling human phosphodi-esterase genes and splice isoforms. Biochem Biophys Res Commun 2006;350:25-32.
40. Kobzik L, Reid MB, Bredt DS, Stamler JS. Nitric oxide in skeletal muscle. Nature 1994;372:546-548.
41. Navegantes LC, Resano NM, Migliorini RH, Kettelhut IC. Catechol-amines inhibit Ca(2{thorn})-dependent proteolysis in rat skeletal muscle through beta(2)-adrenoceptors and cAMP. Am J Physiol Endocrinol Metab 2001;281:E449-E454.
42. Sensky PL, Jewell KK, Ryan KJ, Parr T, Bardsley RG, Buttery PJ. Effect of anabolic agents on calpastatin promoters in porcine skeletal muscle and their responsiveness to cyclic adenosine monophos-phate- and calcium-treated stimuli. J Anim Sci 2006;84:2973-2982.
43. Combaret L, Ralliére C, Taillandier D, Tanaka K, Attaix D. Manipulation of the ubiquitin-proteasome pathway in cachexia: pentoxifyl-line suppresses the activation of 20S and 26S proteasomes in muscles from tumor-bearing rats. Mol Biol Rep 1999;26:95-101.
44. 0-cyclic adenosine monophosphate-mediated inhibition of the ubiquitin-proteasome system in skeletal muscle. Endocrinology 2009;150:5395-5404.
45. Ogata T, Oishi Y, Higuchi M, Muraoka I. Fasting-related autophagic response in slow- and fast-twitch skeletal muscle. Biochem Biophys Res Commun 2010;394:136-140.
46. Stephan JS, Yeh YY, Ramachandran V, Deminoff SJ, Herman PK. The Tor and PKA signaling pathways independently target the Atg1/ Atg13 protein kinase complex to control autophagy. Proc Natl Acad Sci USA 2009;106:17049-17054.
47. De Rooji J, Zwartkruis FJ, Verheijen MH, Cool RH, Nijman SM, Wit-tinghofer A, et al. Epac is a Rap 1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 1998;396:474-477.
48. Navegantes LCC, Migliorini RH, Kettelhut IC. Adrenergic control of protein metabolism in skeletal muscle. Curr Opin Clin Nutr Metab Care 2002;5:281-286.
49. Brennesvik EO, Ktori C, Ruzzin J, Jebens E, Shepherd PR, Jensen J. Adrenaline potentiates insulin-stimulated PKB activation via cAMP and Epac: implication for cross talk between insulin and adrenaline. Cell Signal 2005;17:1551-1559.
50. Rangarajan S, Enserink JM, Kuiperij HB, de Rooji J, Price LS, Schwede F, et al. Cyclic AMP induces integrin-mediated cell adhesion through Epac and Rap1 upon stimulation of the b2-adrenergic receptor. J Cell Biol 2003;160:487-493.
51. Baviera AM, Zanon NM, Navegantes LC, Kettelhut IC. Involvement of cAMP/Epac/PI3K-dependent pathway in the antiproteolytic effect of epinephrine on rat skeletal muscle. Mol Cell Endocrinol 2010; 315:104-112.
52. Stuenaes JT, Bolling A, Ingvaldsen A, Rommundstad C, Sudar E, Lin FC, et al. Beta-adrenoceptor stimulation potentiates insulin-stimulated PKB phosphorylation in rat cardiomyocytes via cAMP and PKA. Br J Pharmacol 2010;160:116-129.
53. Kolnes AJ, Ingvaldsen A, Bollig A, Stuenaes JT, Kreft M, Zorec R, et al. Caffeine and theophylline block insulin-stimulated glucose uptake and PKB phosphorylation in rat skeletal muscles. Acta Physiol (Oxf) 2010;200:65-74.