Skip to main content

Effects of cyclic nucleotide phosphodiesterases (PDEs) on mitochondrial skeletal muscle functions

Abstract

Mitochondria play a critical role in skeletal muscle metabolism and function, notably at the level of tissue respiration, which conduct muscle strength as well as muscle survival. Pathological conditions induce mitochondria dysfunctions notably characterized by free oxygen radical production disturbing intracellular signaling. In that way, the second messengers, cyclic AMP and cyclic GMP, control intracellular signaling at the physiological and transcription levels by governing phosphorylation cascades. Both nucleotides are specifically and selectively hydrolyzed in their respective 5′-nucleotide by cyclic nucleotide phosphodiesterases (PDEs), which constitute a multi-genic family differently tissue distributed and subcellularly compartmentalized. These PDEs are presently recognized as therapeutic targets for cardiovascular, pulmonary, and neurologic diseases. However, very few data concerning cyclic nucleotides and PDEs in skeletal muscle, specifically in mitochondria, are reported in the literature. The knowledge of PDE implication in mitochondrial signaling would be helpful for resolving critical mitochondrial dysfunctions in skeletal muscle.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

cAMP:

Cyclic adenosine 3′,5′-monophosphate

cGMP:

Cyclic guanosine 3′,5′-monophosphate

PKA:

Protein kinase A

PKG:

Protein kinase G

CREB:

cAMP response element binding protein

PDE:

Cyclic nucleotide phosphodiesterase

AC:

Adenylyl cyclase

GC:

Guanylyl cyclase

ATP:

Adenosine triphosphate

PGC-1α:

Peroxisome proliferator-activated receptor gamma co-activator 1α

PI3K:

Phosphoinositide 3-kinase

IP3:

Inositol trisphosphate

NFK-B :

Nuclear factor-kappa B

COX:

Cytochrome C oxidase

EDL:

Extensor digitorum longus

EPAC:

Exchange protein directly activated by cAMP

PPi:

Inorganic phosphate

MAPK:

Mitogen-activated protein kinases

GSK-3β:

Glycogen synthase kinase 3β

ERK:

Extracellular signal-regulated kinase

PKB/Akt:

Protein kinase B

ROS:

Reactive oxygen species

mKATP:

ATP-dependent mitochondrial potassium channel

mPTP:

Mitochondrial permeability transition pore

TNF-α:

Tumor necrosis factor α

IL-6:

Interleukin-6

SOD:

Superoxide dismutase

mRNA:

Messenger ribonucleic acid

References

  1. Sutherland EW (1972) Studies on the mechanism of hormone action. Science 177:401–408

    CAS  Article  PubMed  Google Scholar 

  2. Sette C, Conti M (1966) Phosphorylation and activation of a cAMP-specific phosphodiesterase by the cAMP-dependent protein kinase. Involvement of serine 54 in the enzyme activation. J Biol Chem 271:16526–16534

    Google Scholar 

  3. Lugnier C (2006) Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol Ther 109:366–398

    CAS  Article  PubMed  Google Scholar 

  4. Azevedo MF, Faucz FR, Bimpaki E, Horvath A, Levy I, de Alexandre RB, Ahmad F, Vincent Manganiello V, Stratakis CA (2014) Clinical and molecular genetics of the phosphodiesterases (PDEs). Endocr Rev 35:195–233

    CAS  Article  PubMed  Google Scholar 

  5. Dousa TP (1999) Cyclic-3′,5′-nucleotide phosphodiesterase isozymes in cell biology and pathophysiology of the kidney. Kidney Int 55:29–62

    CAS  Article  PubMed  Google Scholar 

  6. Ahmad F, Murata T, Simizu K, Degerman E, Maurice D, Manganiello V (2015) Cyclic nucleotide phosphodiesterases: important signaling modulators and therapeutic targets. Oral Dis 21:e25–e50

    CAS  Article  PubMed  Google Scholar 

  7. Bender AT, Beavo JA (2006) Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev 58:488–520

    CAS  Article  PubMed  Google Scholar 

  8. Conti M, Mika D, Richter W (2014) Cyclic AMP compartments and signaling specificity: role of cyclic nucleotide phosphodiesterases. J Gen Physiol 143:29–38

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Wu P, Wang P (2004) Per-Arnt-Sim domain-dependent association of cAMP-phosphodiesterase 8A1 with IkappaB proteins. Proc Natl Acad Sci USA 101:17634–17639

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Fawcett L, Baxendale R, Stacey P, Collette McGrouther C, Harrow I, Soderling S, Hetman J, Beavo JA, Phillips C (2000) Molecular cloning and characterization of a distinct human phosphodiesterase gene family: PDE11A. Proc Natl Acad Sci USA 97:3702–3707

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Schultz JE (2009) Structural and biochemical aspects of tandem GAF domains. Handb Exp Pharmacol 191:93–109

    Article  Google Scholar 

  12. Keravis T, Lugnier C (2012) Cyclic nucleotide phosphodiesterase (PDE) isozymes as targets of the intracellular signalling network: benefits of PDE inhibitors in various diseases and perspectives for future therapeutic developments. Br J Pharmacol 165:1288–1305

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Brescia M, Zaccolo M (2016) Modulation of compartmentalised cyclic nucleotide signalling via local inhibition of phosphodiesterase activity. Int J Mol Sci 17:E1672

    Article  PubMed  Google Scholar 

  14. Bobin P, Belacel-Ouari M, Bedioune I, Zhang L, Leroy J, Leblais V, Fischmeister R, Vandecasteele G (2016) Cyclic nucleotide phosphodiesterases in heart and vessels: a therapeutic perspective. Arch Cardiovasc Dis 109:431–443

    Article  PubMed  Google Scholar 

  15. Wang JH, Sharma RK, Huang CY, Chau V, Chock PB (1980) On the mechanism of activation of cyclic nucleotide phosphodiesterase by calmodulin. Ann NY Acad Sci 356:190–204

    CAS  Article  PubMed  Google Scholar 

  16. Sonnenburg WK, Rybalkin SD, Bornfeldt KE, Kwak KS, Rybalkina IG, Beavo JA (1998) Identification, quantitation, and cellular localization of PDE1 calmodulin-stimulated cyclic nucleotide phosphodiesterases. Methods 14:3–19

    CAS  Article  PubMed  Google Scholar 

  17. Epstein PM, Fiss K, Hachisu R, Andrenyak DM (1982) Interaction of calcium antagonists with cyclic AMP phosphodiesterases and calmodulin. Biochem Biophys Res Commun 105:1142–1149

    CAS  Article  PubMed  Google Scholar 

  18. Lugnier C, Follenius A, Gerard D, Stoclet J-C (1984) Bepridil and flunarizine as calmodulin inhibitors. Eur J Pharmacol 98:157–158

    CAS  Article  PubMed  Google Scholar 

  19. Mumby MC, Martins TJ, Chang ML, Beavo JA (1982) Identification of cGMP-stimulated cyclic nucleotide phosphodiesterase in lung tissue with monoclonal antibodies. J Biol Chem 257:13283–13290

    CAS  PubMed  Google Scholar 

  20. Beavo JA, Hansen RS, Harrison SA, Hurwitz RL, Martins TJ, Mumby MC (1982) Identification and properties of cyclic nucleotide phosphodiesterases. Mol Cell Endocrinol 28:387–410

    CAS  Article  PubMed  Google Scholar 

  21. Cann MJ (2007) Sodium regulation of GAF domain function. Biochem Soc Trans 35:1032–1034

    CAS  Article  PubMed  Google Scholar 

  22. Podzuweit T, Nennstiel P, Müller A (1995) Isozyme selective inhibition of cGMP-stimulated cyclic nucleotide phosphodiesterases by erythro-9-(2-hydroxy-3-nonyl) adenine. Cell Signal 7:733–738

    CAS  Article  PubMed  Google Scholar 

  23. Wunder F, Gnoth MJ, Geerts A, Barufe D (2009) A novel PDE2A reporter cell line: characterization of the cellular activity of PDE inhibitors. Mol Pharm 6:326–336

    CAS  Article  PubMed  Google Scholar 

  24. Degerman E, Belfrage P, Manganiello VC (1997) Structure, localization, and regulation of cGMP-inhibited phosphodiesterase (PDE3). J Biol Chem 272:6823–6826

    CAS  Article  PubMed  Google Scholar 

  25. He R, Komas N, Ekholm D, Murata T, Taira M, Hockman S, Degerman E, Manganiello VC (1998) Expression and characterization of deletion recombinants of two cGMP-inhibited cyclic nucleotide phosphodiesterases (PDE-3). Cell Biochem Biophys 29:89–111

    CAS  Article  PubMed  Google Scholar 

  26. Lugnier C, Komas N (1993) Modulation of vascular cyclic nucleotide phosphodiesterases by cyclic GMP: role in vasodilatation. Eur Heart J 14:141–148

    CAS  Article  PubMed  Google Scholar 

  27. Komas N, Lugnier C, Le Bec A, Serradeil-Le Gal C, Barthelemy G, Stoclet J-C (1989) Differential sensitivity to cardiotonic drugs of cyclic AMP phosphodiesterases III isolated from canine ventricular and sinoatrial enriched tissues. J Cardiovasc Pharmacol 14:213–220

    CAS  Article  PubMed  Google Scholar 

  28. McCahill AC, Huston E, Li X, Houslay MD (2008) PDE4 associates with different scaffolding proteins: modulating interactions as treatment for certain diseases. Handb Exp Pharmacol 186:125–166

    CAS  Article  Google Scholar 

  29. Beard MB, Olsen AE, Jones RE, Erdogan S, Houslay MD, Bolger GB (2000) UCR1 and UCR2 domains unique to the cAMP-specific phosphodiesterase family form a discrete module via electrostatic interactions. J Biol Chem 275:10349–10358

    CAS  Article  PubMed  Google Scholar 

  30. Houslay MD (2010) Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem Sci 35:91–100

    CAS  Article  PubMed  Google Scholar 

  31. Conti M, Richter W, Mehats C, Livera G, Park JY, Jin C (2003) Cyclic AMP-specific PDE4 phosphodiesterases as critical components of cyclic AMP signaling. J Biol Chem 278:5493–5496

    CAS  Article  PubMed  Google Scholar 

  32. Lugnier C, Schoeffter P, Le Bec A, Strouthou E, Stoclet J-C (1986) Selective inhibition of cyclic nucleotide phosphodiesterases of human, bovine and rat aorta. Biochem Pharmacol 35:1743–1751

    CAS  Article  PubMed  Google Scholar 

  33. Tenor H, Hatzelmann A, Beume R, Lahu G, Zech K, Bethke TD (2011) Pharmacology, clinical efficacy, and tolerability of phosphodiesterase-4 inhibitors: impact of human pharmacokinetics. Handb Exp Pharmacol 204:85–119

    CAS  Article  Google Scholar 

  34. Francis SH, Blount MA, Corbin JD (2011) Mammalian cyclic nucleotide phosphodiesterases: molecular mechanisms and physiological functions. Physiol Rev 91:651–690

    CAS  Article  PubMed  Google Scholar 

  35. Gopal VK, Francis SH, Corbin JD (2001) Allosteric sites of phosphodiesterase-5 (PDE5). A potential role in negative feedback regulation of cGMP signaling in corpus cavernosum. Eur J Biochem 268:3304–3312

    CAS  Article  PubMed  Google Scholar 

  36. Das A, Durrant D, Salloum FN, Xi L, Kukreja RC (2015) PDE5 inhibitors as therapeutics for heart disease, diabetes and cancer. Pharmacol Ther 147:12–21

    CAS  Article  PubMed  Google Scholar 

  37. Senft G, Schultz G, Munske K, Hoffmann M (1968) Influence of insulin on cyclic 3′,5′-AMP phosphodiesterase activity in liver, skeletal muscle, adipose tissue, and kidney. Diabetologia 4:322–329

    CAS  Article  PubMed  Google Scholar 

  38. Triner L, Vulliemoz Y, Schwartz I, Nahas GG (1970) Cyclic phosphodiesterase activity and the action of papaverine. Biochem Biophys Res Commun 40:64–69

    CAS  Article  PubMed  Google Scholar 

  39. Toson GC, Carpenedo F (1972) Inhibition by papaverine and eupaverine of 3′, 5′-cyclic AMP phosphodiesterase from rabbit skeletal muscle. Naunyn Schmiedebergs Arch Pharmacol 273:168–171

  40. Gain KR, Appleman MM (1978) Distribution and regulation of the phosphodiesterase of muscle tissues. In: George WJ, Ignarro LJ (eds) Advances in cyclic nucleotide research, vol 9. Raven Press, New York, pp 221–231

  41. Beavo JA (1995) Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol Rev 75:725–748

    CAS  PubMed  Google Scholar 

  42. Enoksson S, Degerman E, Hagström-Toft E, Large V, Arner P (1998) Various phosphodiesterase subtypes mediate the in vivo antilipolytic effect of insulin on adipose tissue and skeletal muscle in man. Diabetologia 41:560–568

    CAS  Article  PubMed  Google Scholar 

  43. Han P, Zhu X, Michaeli T (1997) Alternative splicing of the high affinity cAMP-specific phosphodiesterase (PDE7A) mRNA in human skeletal muscle and heart. J Biol Chem 272:16152–16157

    CAS  Article  PubMed  Google Scholar 

  44. Bingham J, Sudarsanam S, Srinivasan S (2006) Profiling human phosphodiesterase genes and splice isoforms. Biochem Biophys Res Commun 350:25–32

    CAS  Article  PubMed  Google Scholar 

  45. Shimizu-Albergine M, Tsai LC, Patrucco E, Beavo JA (2012) cAMP-specific phosphodiesterases 8A and 8B, essential regulators of Leydig cell steroidogenesis. Mol Pharmacol 81:556–566

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. Genders AJ, Bradley EA, Rattigan S, Richards SM (2011) cGMP phosphodiesterase inhibition improves the vascular and metabolic actions of insulin in skeletal muscle. Am J Physiol Endocrinol Metab 301:E342–E350

    CAS  Article  PubMed  Google Scholar 

  47. Bloom TJ (2002) Cyclic nucleotide phosphodiesterase isozymes expressed in mouse skeletal muscle. Can J Physiol Pharmacol 80:1132–1135

  48. Bloom TJ (2005) Age-related alterations in cyclic nucleotide phosphodiesterase activity in dystrophic mouse leg muscle. Can J Physiol Pharmacol 83:1055–1060

    CAS  Article  PubMed  Google Scholar 

  49. Hinkle RT, Dolan E, Cody DB, Bauer MB, Isfort RJ (2005) Phosphodiesterase 4 inhibition reduces skeletal muscle atrophy. Muscle Nerve 32:775–781

    CAS  Article  PubMed  Google Scholar 

  50. Lira EC, Graca FA, Goncalves DA, Zanon NM, Baviera AM, Strindberg L, Lönnroth P, Migliorini RH, Kettelhut IC, Navegantes LC (2007) Cyclic adenosine monophosphate-phosphodiesterase inhibitors reduce skeletal muscle protein catabolism in septic rats. Shock 27:687–694

    CAS  Article  PubMed  Google Scholar 

  51. Baviera AM, Zanon NM, Carvalho Navegantes LC, Migliorini RH, do Carmo Kettelhut I (2007) Pentoxifylline inhibits Ca2+-dependent and ATP proteasome-dependent proteolysis in skeletal muscle from acutely diabetic rats. Am J Physiol Endocrinol Metab 292:E702–E708

    CAS  Article  PubMed  Google Scholar 

  52. Berdeaux R, Stewart R (2012) cAMP signaling in skeletal muscle adaptation: hypertrophy, metabolism, and regeneration. Am J Physiol Endocrinol Metab 303:E1–E17

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Park SJ, Ahmad F, Philp A, Baar K, Williams T, Luo H, Ke H, Rehmann H, Taussig R, Brown AL, Kim MK, Beaven MA, Burgin AB, Manganiello V, Chung JH (2012) Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 148:421–433

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. Sabatini S, Sgrò P, Duranti G, Ceci R, Di Luigi L (2011) Tadalafil alters energy metabolism in C2C12 skeletal muscle cells. Acta Biochim Pol 58:237–241

    CAS  PubMed  Google Scholar 

  55. Percival JM, Whitehead NP, Adams ME, Candace M, Adamo CM, Joseph A, Beavo JA, Froehner SC (2012) Sildenafil reduces respiratory muscle weakness and fibrosis in the mdx mouse model of Duchenne muscular dystrophy. J Pathol 228:77–87

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Sheffield-Moore M, Wiktorowicz JE, Soman KV, Danesi CP, Kinsky MP, Dillon EL, Randolph KM, Casperson SL, Gore DC, Horstman AM, Lynch JP, Doucet BM, Mettler J, Ryder JW, Ploutz-Snyder LL, Hsu JW, Jahoor F, Jennings K, White GR, McCammon S, Durham WJ (2013) Sildenafil increases muscle protein synthesis and reduces muscle fatigue. Clin Transl Sci 6:463–468

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. Nyberg M, Piil P, Egelund J, Sprague RS, Mortensen SP, Hellsten Y (2015) Potentiation of cGMP signaling increases oxygen delivery and oxidative metabolism in contracting skeletal muscle of older but not young humans. Physiol Rep 3:e12508

    Article  PubMed  PubMed Central  Google Scholar 

  58. Joshi R, Kadeer N, Sheriff S, Friend LA, James JH, Balasubramaniam A (2014) Phosphodiesterase (PDE) inhibitor torbafylline (HWA 448) attenuates burn-induced rat skeletal muscle proteolysis through the PDE4/cAMP/EPAC/PI3K/Akt pathway. Mol Cell Endocrinol 393:152–163

    CAS  Article  PubMed  Google Scholar 

  59. Guillot M, Charles AL, Chamaraux-Tran TN, Bouitbir J, Meyer A, Zoll J, Schneider F, Geny B (2014) Oxidative stress precedes skeletal muscle mitochondrial dysfunction during experimental aortic cross-clamping but is not associated with early lung, heart, brain, liver, or kidney mitochondrial impairment. J Vasc Surg 60(1043–1051):e5

    Google Scholar 

  60. Kalogeris T, Bao Y, Korthuis RJ (2014) Mitochondrial reactive oxygen species: a double edged sword in ischemia/reperfusion vs preconditioning. Redox Biol 2:702–714

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. Lejay A, Meyer A, Schlagowski AI, Charles AL, Singh F, Bouitbir J, Pottecher J, Chakfé N, Zoll J, Geny B (2014) Mitochondria: mitochondrial participation in ischemia–reperfusion injury in skeletal muscle. Int J Biochem Cell Biol 50:101–105

    CAS  Article  PubMed  Google Scholar 

  62. Hamanaka RB, Chandel NS (2010) Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem Sci 35:505–513

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. Bleier L, Wittig I, Heide H, Steger M, Brandt U, Dröse S (2015) Generator-specific targets of mitochondrial reactive oxygen species. Free Radical Biol Med 78:1–10

    CAS  Article  Google Scholar 

  64. Thaveau F, Zoll J, Rouyer O, Chakfe N, Kretz JG, Piquard F, Gény B (2007) Ischemic preconditioning specifically restores complexes I and II activities of the mitochondrial respiratory chain in ischemic skeletal muscle. J Vasc Surg 46:541–547

    Article  PubMed  Google Scholar 

  65. Acin-Perez R, Salazar E, Kamenetsky M, Buck J, Levin LR, Manfredi G (2009) Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab 9:265–276

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. Zhang F, Zhang L, Qi Y, Xu H (2016) Mitochondrial cAMP signaling. Cell Mol Life Sci 73:4577–4590

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. Carlucci A, Lignitto L, Feliciello A (2008) Control of mitochondria dynamics and oxidative metabolism by cAMP, AKAPs and the proteasome. Trends Cell Biol 18:604–613

    CAS  Article  PubMed  Google Scholar 

  68. Romani A, Dowell E, Scarpa A (1991) Cyclic AMP-induced Mg2+ release from rat liver hepatocytes, permeabilized hepatocytes, and isolated mitochondria. J Biol Chem 266:24376–24384

    CAS  PubMed  Google Scholar 

  69. Di Benedetto G, Pendin D, Greotti E, Pizzo P, Pozzan T (2014) Ca2+ and cAMP cross-talk in mitochondria. J Physiol 592:305–312

    Article  PubMed  Google Scholar 

  70. Dent G, Giembycz MA, Evans PM, Rabe KF, Barnes PJ (1994) Suppression of human eosinophil respiratory burst and cyclic AMP hydrolysis by inhibitors of type IV phosphodiesterase: interaction with the beta adrenoceptor agonist albuterol. J Pharmacol Exp Ther 271:1167–1174

    CAS  PubMed  Google Scholar 

  71. Talha S, Bouitbir J, Charles A, Zoll J, Goette-Di Marco P, Meziani F, Piquard F, Geny B (2013) Pretreatment with brain natriuretic peptide reduces skeletal muscle mitochondrial dysfunction and oxidative stress after ischemia–reperfusion. J Appl Physiol 114:172–179

    CAS  Article  PubMed  Google Scholar 

  72. Debska G, Kicinska A, Skalska J, Szewczyk A, May R, Elger CE, Kunz WS (2002) Opening of potassium channels modulates mitochondrial function in rat skeletal muscle. Biochim Biophys Acta 1556:97–105

    CAS  Article  PubMed  Google Scholar 

  73. Gali Ramamoorthy T, Laverny G, Schlagowski AI, Zoll J, Messaddeq N, Bornert JM, Panza S, Ferry A, Geny B, Metzger D (2015) The transcriptional coregulator PGC-1β controls mitochondrial function and anti-oxidant defence in skeletal muscles. Nat Commun 6:10210

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  74. Chanoit G, Zhou J, Lee S, McIntosh R, Shen X, Zvara DA, Xu Z (2011) Inhibition of phosphodiesterases leads to prevention of the mitochondrial permeability transition pore opening and reperfusion injury in cardiac H9c2 Cells. Cardiovasc Drugs Ther 25:299–306

    CAS  Article  PubMed  Google Scholar 

  75. Acin-Perez R, Russwurm M, Gunnewig K, Gertz M, Zoidl G, Ramos L, Buck J, Levin LR, Rassow J, Manfredi G, Steegborn C (2011) A phosphodiesterase 2A isoform localized to mitochondria regulates respiration. J Biol Chem 286:30423–30432

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  76. Módis K, Panopoulos P, Coletta C, Papapetropoulos A, Szabo C (2013) Hydrogen sulfide-mediated stimulation of mitochondrial electron transport involves inhibition of the mitochondrial phosphodiesterase 2A, elevation of cAMP and activation of protein kinase A. Biochem Pharmacol 86:1311–1319

    Article  PubMed  Google Scholar 

  77. Wang B, Zhu L, Sui S, Sun C, Jiang H, Ren D (2014) Cilostazol induces mitochondrial fatty acid β-oxidation in myotubes. Biochem Biophys Res Commun 447:441–445

    CAS  Article  PubMed  Google Scholar 

  78. Chung YW, Lagranha C, Chen Y, Sun J, Tong G, Hockman SC, Ahmad F, Esfahani SG, Bae DH, Polidovitch N, Wu J, Rhee DK, Lee BS, Gucek M, Daniels MP, Brantner CA, Backx PH, Murphy E, Manganiello VC (2015) Targeted disruption of PDE3B, but not PDE3A, protects murine heart from ischemia/reperfusion injury. Proc Natl Acad Sci USA 112:E2253–E2262

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  79. Salloum FN, Ockaili RA, Wittkamp M, Marwaha VR, Kukreja RC (2006) Vardenafil: a novel type 5 phosphodiesterase inhibitor reduces myocardial infarct size following ischemia/reperfusion injury via opening of mitochondrial KATP channels in rabbits. J Mol Cell Cardiol 40:405–411

    CAS  Article  PubMed  Google Scholar 

  80. Fernandes MA, Marques RJ, Vicente JA, Santos MS, Monteiro P, Moreno AJ, Custódio JB (2008) Sildenafil citrate concentrations not affecting oxidative phosphorylation depress H2O2 generation by rat heart mitochondria. Mol Cell Biochem 309:77–85

    CAS  Article  PubMed  Google Scholar 

  81. Fukasawa M, Nishida H, Sato T, Miyazaki M, Nakaya H (2008) 6-[4-(1-Cyclohexyl-1H-tetrazol-5-yl)butoxy]-3,4-dihydro-2-(1H)quinolinone (cilostazol), a phosphodiesterase type 3 inhibitor, reduces infarct size via activation of mitochondrial Ca2+-activated K+ channels in rabbit hearts. J Pharmacol Exp Ther 326:100–104

    CAS  Article  PubMed  Google Scholar 

  82. Whitaker RM, Wills LP, Stallons LJ, Schnellmann RG (2013) cGMP-selective phosphodiesterase inhibitors stimulate mitochondrial biogenesis and promote recovery from acute kidney injury. J Pharmacol Exp Ther 347:626–634

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  83. Takimoto E (2011) cGMP-PKG upregulates PGC1α and improves cardiac function in advanced cardiac hypertrophy independently of RGS2. BMC Pharmacol 11:O18

    Article  PubMed Central  Google Scholar 

  84. Percival JM, Siegel MP, Knowels G, Marcinek DJ (2013) Defects in mitochondrial localization and ATP synthesis in the mdx mouse model of Duchenne muscular dystrophy are not alleviated by PDE5 inhibition. Hum Mol Genet 22:153–167

    CAS  Article  PubMed  Google Scholar 

  85. Charles AL, Guilbert AS, Bouitbir J, Goette-Di Marco P, Enache I, Zoll J, Piquard F, Geny B (2011) Effect of postconditioning on mitochondrial dysfunction in experimental aortic cross-clamping. Br J Surg 98:511–516

    Article  PubMed  Google Scholar 

  86. Lejay A, Choquet P, Thaveau F, Singh F, Schlagowski A, Charles AL, Laverny G, Metzger D, Zoll J, Chakfe N, Geny BA (2015) New murine model of sustainable and durable chronic critical limb ischemia fairly mimicking human pathology. Eur J Vasc Endovasc Surg 49:205–212

    CAS  Article  PubMed  Google Scholar 

  87. Meyer A, Zoll J, Charles AL, Charloux A, de Blay F, Diemunsch P, Sibilia J, Piquard F, Geny B (2013) Skeletal muscle mitochondrial dysfunction during chronic obstructive pulmonary disease: central actor and therapeutic target. Exp Physiol 98:1063–1078

    CAS  Article  PubMed  Google Scholar 

  88. Meyer A, Sibilia J, Geny B (2015) In the idiopathic inflammatory myopathies, reactive oxygen species are at the crossroad between immune and non-immune cell-mediated mechanisms. Ann Rheum Dis 74:e62

    CAS  Article  PubMed  Google Scholar 

  89. Shadrin IY, Khodabukus A, Bursac N (2016) Striated muscle function, regeneration, and repair. Cell Mol Life Sci 73:4175–4202

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We are indebted to Pr. Valérie Wolff for careful language reviewing of the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Claire Lugnier.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tetsi, L., Charles, AL., Paradis, S. et al. Effects of cyclic nucleotide phosphodiesterases (PDEs) on mitochondrial skeletal muscle functions. Cell. Mol. Life Sci. 74, 1883–1893 (2017). https://doi.org/10.1007/s00018-016-2446-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-016-2446-0

Keywords

  • Skeletal muscle
  • Mitochondria functions
  • Cyclic AMP
  • Cyclic GMP
  • Cyclic nucleotide phosphodiesterase