Role of Phosphodiesterase in the Biology and Pathology of Diabetes
Abstract
:1. Introduction
2. The Second Messengers cAMP and cGMP—The Roles in Pancreas
3. PDEs in Basic Research—GENERAL Outline
3.1. The PDE1 Family
3.2. The PDE3 Family
3.3. The PDE4 Family
3.4. Other PDE
3.5. The PDE2 Family
3.6. The PDE5 Family
3.7. The PDE7 Family
3.8. The PDE8 Family
3.9. The PDE9 Family
3.10. The PDE10 Family
3.11. The PDE11 Family
4. The Potential Role of PDEs Inhibition in Regeneration and Diabetes Mellitus (Type 1 and 2)
5. Regeneration
6. Type 1 Diabetes Mellitus
7. Diabetes Type 2
Author Contributions
Funding
Conflicts of Interest
Abbreviations
AC | Adenylyl cyclase |
ADP | Adenosine diphosphate |
AKAP | A-kinase anchoring proteins |
AMPK | AMP-activated protein kinase |
ATP | Adenosine triphosphate |
BMI | Body mass index |
CAM | Calmodulin |
[Ca2+]i | Intracellular calcium |
cAMP | Cyclic AMP |
[cAMP]i | Intracellular camp |
[cAMP]pm | cAMP in the sub-plasma-membrane space |
cGMP | Cyclic GMP |
CYP | Cyclophosphamide |
DB-cAMP | Dibutyryl camp |
EC | Endothelial cell |
EPAC | Exchange protein directly activated by camp |
ERK | Extracellular signal-regulated kinases |
FDA | Food and Drug Administration |
GAD | Glutamic acid decarboxylase |
GAF | Guanylate cyclase |
GC | G protein coupled receptors |
GCPRs | G protein-coupled receptors |
GDP | Guanosine diphosphate |
GLP-1 | Glucagon-like peptide-1 |
GLUT | Glucose transporter |
GSIS | Glucose- stimulated insulin secretion |
GSK3 | Glycogen synthase kinase |
GTP | Guanosine-5’-triphosphate |
Hba1C | Glycated hemoglobin |
IGF | Insulin-like growth factor |
IFN | Interferon |
IL | Interleukin |
IRS | Insulin receptor substrate |
KATP | Channels, ATP-sensitive K+ channels |
NO | Nitric oxide |
NOD | Nondiabetic |
PAS | Per-arnt-sim domain |
PCNA | Proliferating cell nuclear antigen |
PDE | Phosphodiesterase |
PDX-1 | Insulin promoter factor 1 |
RNS | Reactive forms of nitrogen |
ROS | Reactive oxygen species |
p42MAPK | Mitogen-activated protein kinases |
PIK3 | Phosphatidylinositol 3-kinase |
PKA | Protein kinase A |
PKB | Protein kinase B |
PKG | Protein kinase G |
PPAR | Peroxisome proliferator-activated receptors |
SIRT1 | Sirtuin 1 |
STZ | Streptozotocin |
T2D | Type 2 diabetes |
TNF | Tumor necrosis factor |
UCR | Up-stream conserved region |
VGCC | Voltage-gated Ca2+ channel |
VLDL | Very-low-density lipoprotein |
WHO | World health organization |
References
- Mourad, N.I.; Nenquin, M.; Henquin, J. cAMP-Mediated and Metabolic Amplification of Insulin Secretion Are Distinct Pathways Sharing Independence of β-Cell Microfilaments. Endocrinology 2012, 153, 4644–4654. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Straub, S.G.; Sharp, G.W.G. Hypothesis: One rate-limiting step controls the magnitude of both phases of glucose-stimulated insulin secretion. Am. J. Physiol. Cell Physiol. 2004, 565–571. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Henquin, J.C. Regulation of insulin secretion: A matter of phase control and amplitude modulation. Diabetologia 2009, 52, 739–751. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tengholm, A. Cyclic AMP dynamics in the pancreatic β-cell. Ups. J. Med. Sci. 2012, 117, 355–369. [Google Scholar] [CrossRef] [PubMed]
- Hellman, B.O. Pulsatility of insulin release—A clinically important phenomenon. Ups. J. Med. Sci. 2009, 114, 193–205. [Google Scholar] [CrossRef] [PubMed]
- Renstrom, E.; Eliasson, L.; Rorsman, P. Protein kinase A-dependent and -independent stimulation of exocytosis by cAMP in mouse pancreatic B-cells. J. Physiol. 1997, 502, 105–118. [Google Scholar] [CrossRef] [PubMed]
- Harndahl, L.; Jing, X.-J.; Ivarsson, R.; Degerman, E.; Ahre, B.; Manganiello, V.C.; Renstro, E.; Holst, L.S. Important Role of Phosphodiesterase 3B for the Stimulatory Action of cAMP on Pancreatic beta -Cell Exocytosis and Release of Insulin. J. Biol. Chem. 2002, 277, 37446–37455. [Google Scholar] [CrossRef] [Green Version]
- Collins, S.; Surwit, R. The β-Adrenergic Receptors and the Control of Adipose Tissue Metabolism and Thermogenesis. Recent Prog. Horm. Res. 2001, 56, 309–328. [Google Scholar] [CrossRef]
- Tian, G.; Sågetorp, J.; Xu, Y.; Shuai, H.; Degerman, E.; Tengholm, A. Role of phosphodiesterases in the shaping of sub-plasma-membrane cAMP oscillations and pulsatile insulin secretion. J. Cell Sci. 2012, 125, 5084–5095. [Google Scholar] [CrossRef] [Green Version]
- Härndahl, L.; Wierup, N.; Enerbäck, S.; Mulder, H.; Manganiello, V.C.; Sundler, F.; Degerman, E.; Ahrén, B.; Holst, L.S. β-Cell-targeted Overexpression of Phosphodiesterase 3B in Mice Causes Impaired Insulin Secretion, Glucose Intolerance, and Deranged Islet Morphology. J. Biol. Chem. 2004, 279, 15214–15222. [Google Scholar] [CrossRef] [Green Version]
- Walz, H.A.; Härndahl, L.; Wierup, N.; Zmuda-Trzebiatowska, E.; Svennelid, F.; Manganiello, V.C.; Ploug, T.; Sundler, F.; Degerman, E.; Ahrén, B.; et al. Early and rapid development of insulin resistance, islet dysfunction and glucose intolerance after high-fat feeding in mice overexpressing phosphodiesterase 3B. J. Endocrinol. 2006, 189, 629–641. [Google Scholar] [CrossRef]
- Yang, H.; Yang, L. Targeting cAMP/PKA pathway for glycemic control and type 2 diabetes therapy. J. Mol. Endocrinol. 2016, 57, R93–R108. [Google Scholar] [CrossRef] [Green Version]
- Pratt, E.P.S.; Harvey, K.E.; Salyer, A.E.; Hockerman, G.H. Regulation of cAMP accumulation and activity by distinct phosphodiesterase subtypes in INS-1 cells and human pancreatic β-cells. PLoS ONE 2019, 14, e215188. [Google Scholar] [CrossRef] [Green Version]
- Seino, S.; Shibasaki, T. PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol. Rev. 2005, 85, 1303–1342. [Google Scholar] [CrossRef]
- Kalwat, M.A.; Cobb, M.H. Mechanisms of the Amplifying Pathway of Insulin Secretion in the β Cell. Pharmacol. Ther. 2017, 179, 17–30. [Google Scholar] [CrossRef] [PubMed]
- Dou, H.; Wang, C.; Wu, X.; Yao, L.; Zhang, X.; Teng, S. Calcium influx activates adenylyl cyclase 8 for sustained insulin secretion in rat pancreatic beta cells. Diabetologia 2015, 58, 324–333. [Google Scholar] [CrossRef] [Green Version]
- Idevall-Hagren, O.; Barg, S.; Gylfe, E.; Tengholm, A. cAMP mediators of pulsatile insulin secretion from glucose-stimulated single β-cells. J. Biol. Chem. 2010, 285, 23007–23018. [Google Scholar] [CrossRef] [Green Version]
- Beshay, E.; Prud’homme, G.J. Inhibitors of phosphodiesterase isoforms III or IV suppress islet-cell nitric oxide production. Lab. Investig. 2001, 81, 1109–1117. [Google Scholar] [CrossRef] [Green Version]
- Azevedo, M.F.; Faucz, F.R.; Bimpaki, E.; Horvath, A.; Levy, I.; De Alexandre, R.B.; Ahmad, F.; Manganiello, V.; Stratakis, C.A.; Genetics, E.; et al. Clinical and Molecular Genetics of the phosphodiesterases (PDEs). Endocr. Rev. 2014, 35, 195–233. [Google Scholar] [CrossRef]
- Ho, J.E.; Arora, P.; Walford Geoffrey, A.; Ghorbani, A.; Guanga, D.P.; Dhakal, B.P.; Nathan, D.I.; Buys, E.S.; Florez, J.C.; Newton-Cheh, C.; et al. Effect of Phosphodiesterase Inhibition on Insulin Resistance in Obese Individuals. J. Am. Hear. Assoc. 2014, 3, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Russell, M.A.; Morgan, N.G. Expression and functional roles of guanylate cyclase isoforms in BRIN-BD11 β-cells. Islets 2010, 2, 374–382. [Google Scholar] [CrossRef] [Green Version]
- Undank, S.; Kaiser, J.; Sikimic, J.; Düfer, M.; Krippeit-Drews, P.; Drews, G. Atrial Natriuretic Peptide Affects Stimulus-Secretion Coupling of Pancreatic β-Cells. Diabetes 2017, 66, 2840–2848. [Google Scholar] [CrossRef] [Green Version]
- Brescia, M.; Zaccolo, M. Modulation of compartmentalised cyclic nucleotide signalling via local inhibition of phosphodiesterase activity. Int. J. Mol. Sci. 2016, 17, 1672. [Google Scholar] [CrossRef]
- Shao, Y.X.; Huang, M.; Cui, W.; Feng, L.J.; Wu, Y.; Cai, Y.; Li, Z.; Zhu, X.; Liu, P.; Wan, Y.; et al. Discovery of a phosphodiesterase 9A inhibitor as a potential hypoglycemic agent. J. Med. Chem. 2014, 57, 10304–10313. [Google Scholar] [CrossRef] [Green Version]
- Heimann, E.; Jones, H.A.; Resjö, S.; Manganiello, V.C.; Stenson, L.; Degerman, E. Expression and regulation of cyclic nucleotide phosphodiesterases in human and rat pancreatic islets. PLoS ONE 2010, 5, e14191. [Google Scholar] [CrossRef] [Green Version]
- Pyne, N.J.; Furman, B.L. Cyclic nucleotide phosphodiesterases in pancreatic islets. Diabetologia 2003, 46, 1179–1189. [Google Scholar] [CrossRef] [Green Version]
- Conti, M. Phosphodiesterases and cyclic nucleotide signaling in endocrine cells. Mol. Endocrinol. 2000, 14, 1317–1327. [Google Scholar] [CrossRef]
- Conti, M.; Mika, D.; Richter, W. Cyclic AMP compartments and signaling specificity: Role of cyclic nucleotide phosphodiesterases. J. Gen. Physiol. 2014, 29–38. [Google Scholar] [CrossRef] [Green Version]
- Pinto, E.M.; Faucz, F.R.; Paza, L.Z.; Wu, G.; Fernandes, E.S.; Bertherat, J.; Stratakis, C.A.; Lalli, E.; Ribeiro, R.C.; Rodriguez-galindo, C.; et al. Germline Variants in Phosphodiesterase Genes and Genetic Predisposition to Pediatric Adrenocortical Tumors. Cancers 2020, 12, 506. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Degerman, E.; Belfrage, P.; Manganiello, V.C. Structure, Localization, and Regulation of cGMP-inhibited Phosphodiesterase (PDE3). J. Biol. Chem. 1997, 272, 6823–6826. [Google Scholar] [CrossRef] [Green Version]
- Bender, A.T.; Beavo, J.A. Cyclic nucleotide phosphodiesterases: Molecular regulation to clinical use. Pharmacol. Rev. 2006, 58, 488–520. [Google Scholar] [CrossRef] [PubMed]
- Barone, I.; Giordano, C.; Bonofiglio, D.; Andò, S.; Catalano, S. Phosphodiesterase type 5 and cancers: Progress and challenges. Oncotarget 2017, 8, 99179–99202. [Google Scholar] [CrossRef] [Green Version]
- Ahmad, F.; Shen, W.; Vandeput, F.; Szabo-fresnais, N.; Krall, J.; Degerman, E.; Goetz, F.; Klussmann, E.; Movsesian, M.; Manganiello, V. Regulation of Sarcoplasmic Reticulum Ca2+ ATPase 2 ( SERCA2 ) Activity by Phosphodiesterase 3A (PDE3A) in Human Myocardium. J. Biol. Chem. 2015, 290, 6763–6776. [Google Scholar] [CrossRef] [Green Version]
- Ai, Y.; He, H.; Chen, P.; Yan, B.; Zhang, W.; Ding, Z.; Li, D.; Chen, J.; Ma, Y.; Cao, Y.; et al. An alkaloid initiates phosphodiesterase 3A–schlafen 12 dependent apoptosis without affecting the phosphodiesterase activity. Nat. Commun. 2020, 3236. [Google Scholar] [CrossRef]
- Bolger, G.B. Molecular biology of the cyclic amp-specific cyclic nucleotide phosphodiesterases: A diverse family of regulatory enzymes. Cell. Signal. 1994, 6, 851–859. [Google Scholar] [CrossRef]
- Conti, M.; Jin, S.L. The molecular biology of cyclic nucleotide phosphodiesterase.pdf. Prog. Nucleic Acid. Res. Mol. Biol. 1999, 63, 1–38. [Google Scholar] [CrossRef]
- Ahmad, F.; Murata, T.; Simizu, K.; Degermann, E.; Maurice, D.; Manganiello, V. Cyclic Nucleotide Phosphodiesterases: Important signaling modulators and therapeutic targets. Oral. Dis. 2015, 21, 25–50. [Google Scholar] [CrossRef] [Green Version]
- Świerczek, A.; Pociecha, K.; Ślusarczyk, M.; Chłoń-Rzepa, G.; Baś, S.; Mlynarski, J.; Więckowski, K.; Zadrożna, M.; Nowak, B.; Wyska, E. Comparative Assessment of the New PDE7 Inhibitor–GRMS-55 and Lisofylline in Animal Models of Immune-Related Disorders: A PK/PD Modeling Approach. Pharm. Res. 2020, 37. [Google Scholar] [CrossRef] [Green Version]
- Dov, A.; Abramovitch, E.; Warwar, N.; Nesher, R. Insulin Response to Glucose. Endocrinology 2008, 149, 741–748. [Google Scholar] [CrossRef]
- Lugnier, C.; Meyer, A.; Talha, S.; Geny, B. Cyclic nucleotide phosphodiesterases: New targets in the metabolic syndrome? Pharmacol. Ther. 2020, 208, 107475. [Google Scholar] [CrossRef]
- Waddleton, D.; Wu, W.; Feng, Y.; Thompson, C.; Wu, M.; Zhou, Y.P.; Howard, A.; Thornberry, N.; Li, J.; Mancini, J.A. Phosphodiesterase 3 and 4 comprise the major cAMP metabolizing enzymes responsible for insulin secretion in INS-1 (832/13) cells and rat islets. Biochem. Pharmacol. 2008, 76, 884–893. [Google Scholar] [CrossRef] [PubMed]
- Keravis, T.; Lugnier, C. 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. 2012, 165, 1288–1305. [Google Scholar] [CrossRef] [Green Version]
- Beavo, J.A. Cyclic nucleotide phosphodiesterases: Functional implications of multiple isoforms. Physiol. Rev. 1995, 75, 725–748. [Google Scholar] [CrossRef] [PubMed]
- Francis, S.H.; Busch, J.L.; Corbin, J.D. cGMP-Dependent Protein Kinases and cGMP Phosphodiesterases in Nitric Oxide and cGMP Action. Pharmacol. Rev. 2010, 62, 525–563. [Google Scholar] [CrossRef]
- Sugden, M.C.; Ashcroft, S.J.H. Cyclic nucleotide phosphodiesterase of rat pancreatic islets. Effects of Ca2+, calmodulin and trifluoperazine. Biochem. J. 1981, 197, 459–464. [Google Scholar] [CrossRef] [Green Version]
- Lipson, L.G.; Oldham, S.B. The role of calmodulin in insulin secretion: The presence of a calmodulin-stimulatable phosphodiesterase in pancreatic islets of normal and pregnant rats. Life Sci. 1983, 32, 775–780. [Google Scholar] [CrossRef]
- Capito, K.; Hedeskov, C.J.; Thams, P. Cyclic AMP phosphodiesterase activity in mouse pancreatic islets. Effects of calmodulin and phospholipids. Acta Endocrinol (Copenh) 1986, 111, 533–541. [Google Scholar] [CrossRef] [Green Version]
- Parker, J.C.; VanVolkenburg, M.A.; Ketchum, R.J.; Brayman, K.L.; Andrews, K.A. cAMP PDEs of human and rat islets of langerhans contributions of types 3 i 4 to the modulation od insulin secretion. Biochem. Biophys. Res. Commun. 1995, 217, 916–923. [Google Scholar] [CrossRef] [PubMed]
- Han, P.; Werber, J.; Surana, M.; Fleischer, N.; Michaeli, T. The calcium/calmodulin-dependent phosphodiesterase PDE1C down-regulates glucose-induced insulin secretion. J. Biol. Chem. 1999, 274, 22337–22344. [Google Scholar] [CrossRef] [Green Version]
- Ahmad, M.; Abdel-Wahab, Y.H.A.; Tate, R.; Flatt, P.R.; Pyne, N.J.; Furman, B.L. Effect of type-selective inhibitors on cyclic nucleotide phosphodiesterase activity and insulin secretion in the clonal insulin secreting cell line BRIN-BD11. Br. J. Pharmacol. 2000, 129, 1228–1234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shafiee-Nick, R.; Pyne, N.J.; Furman, B.L. Effects of type-selective phosphodiesterase inhibitors on glucose-induced insulin secretion and islet phosphodiesterase activity. Br. J. Pharmacol. 1995, 115, 1486–1492. [Google Scholar] [CrossRef] [Green Version]
- Wechsler, J.; Choi, Y.; Krall, J.; Ahmad, F.; Manganiello, V.C.; Movsesian, M.A. Isoforms of Cyclic Nucleotide Phosphodiesterase PDE3A in Cardiac Myocytes Isoforms of Cyclic Nucleotide Phosphodiesterase PDE3A in Cardiac Myocytes. J. Biol. Chem. 2002. [Google Scholar] [CrossRef] [Green Version]
- Xu, J.; Jia, Y.F.; Tapadar, S.; Weaver, J.D.; Raji, I.O.; Pithadia, D.J.; Javeed, N.; García, A.J.; Choi, D.S.; Matveyenko, A.V.; et al. Inhibition of TBK1/IKKε Promotes Regeneration of Pancreatic β-cells. Sci. Rep. 2018, 8, 1–14. [Google Scholar] [CrossRef] [Green Version]
- Zmuda-Trzebiatowska, E.; Oknianska, A.; Manganiello, V.; Degerman, E. Role of PDE3B in insulin-induced glucose uptake, GLUT-4 translocation and lipogenesis in primary rat adipocytes. Cell. Signal. 2006, 18, 382–390. [Google Scholar] [CrossRef] [Green Version]
- Degerman, E.; Ahmad, F.; Chung, Y.W.; Guirguis, E.; Omar, B.; Stenson, L.; Manganiello, V. From PDE3B to the regulation of energy homeostasis. Curr. Opin. Pharmacol. 2011, 11, 676–682. [Google Scholar] [CrossRef] [Green Version]
- Zhao, A.Z.; Zhao, H.; Teague, J.; Fujimoto, W.; Beavo, J.A. Attenuation of insulin secretion by insulin-like growth factor 1 is mediated through activation of phosphodiesterase 3B. Proc. Natl. Acad. Sci. USA 1997, 94, 3223–3228. [Google Scholar] [CrossRef] [Green Version]
- Choi, Y.H.; Park, S.; Hockman, S.; Zmuda-trzebiatowska, E.; Svennelid, F.; Haluzik, M.; Gavrilova, O.; Haluzik, M.; Ahmad, F.; Pepin, L.; et al. Alterations in regulation of energy homeostasis in cyclic nucleotide phosphodiesterase 3B–null mice Find the latest version: Alterations in regulation of energy homeostasis in cyclic nucleotide phosphodiesterase 3B–null mice. J. Clin. Investig. 2006, 116, 3240–3251. [Google Scholar] [CrossRef] [Green Version]
- Tang, Y.; Osawa, H.; Onuma, H.; Hasegawa, M.; Nishimiya, T.; Ochi, M. Adipocyte-specific reduction of phosphodiesterase 3B gene expression and its restoration by JTT-501 in the obese, diabetic KKAy mouse. Eur. J. Endocrinol. 2001, 145, 93–99. [Google Scholar] [CrossRef] [Green Version]
- Hasegawa, M.; Tang, Y.; Osawa, H.; Onuma, H.; Nishimiya, T.; Ochi, M.; Terauchi, Y.; Kadowaki, T.; Makino, H. Differential regulation of gene expression and insulin-induced activation of phosphodiesterase 3B in adipocytes of lean insulin-resistant IRS-1 (−/−) mice. Diabetes Res. Clin. Pr. 2002, 58, 79–85. [Google Scholar] [CrossRef]
- Zywert, A.; Szkudelska, K.; Szkudelski, T. Inhibition of phosphodiesterase 3b in insulin-secreting cells of normal and streptozotocin-nicotinamide-induced diabetic rats: Implications for insulin secretion. J. Physiol. Pharmacol. 2014, 65, 425–433. [Google Scholar]
- Kilanowska, A.; Szkudelski, T. Effects of inhibition of phosphodiesterase 3B in pancreatic islets on insulin secretion: A potential link with some stimulatory pathways. Arch. Physiol. Biochem. 2019, 2019, 1–8. [Google Scholar] [CrossRef]
- Muhammed, S.J.; Lundquist, I.; Salehi, A. Pancreatic β-cell dysfunction, expression of iNOS and the effect of phosphodiesterase inhibitors in human pancreatic islets of type 2 diabetes. Diabetes Obes. Metab. 2012, 14, 1010–1019. [Google Scholar] [CrossRef] [PubMed]
- Fujimoto, S.; Tsuura, Y.; Ishida, H.; Tsuji, K.; Mukai, E.; Kajikawa, M.; Hamamoto, Y.; Takeda, T.; Yamada, Y.; Seino, Y. Augmentation of basal insulin release from rat islets by preexposure to a high concentration of glucose. Am. J. Physiol. Endocrinol. Metab. 2000, 279. [Google Scholar] [CrossRef] [PubMed]
- Fujimoto, S.; Ishida, H.; Kato, S.; Okamoto, Y.; Tsuji, K.; Mizuno, N.; Ueda, S.; Mukai, E.; Seino, Y. The Novel Insulinotropic Mechanism of Pimobendan: Direct Enhancement of the Exocytotic Process of Insulin Secretory Granules by Increased Ca2+ Sensitivity in β -Cells. Endocrinology 1998, 139, 1133–1140. [Google Scholar] [CrossRef]
- Parker, J.C.; Vanvolkenburg, M.A.; Nardone, N.A.; Hargrove, D.M.; Andrews, K.M. Modulation of Insulin Secretion and Glycemia by Selective Inhibition of Cyclic AMP Phosphodiesterase III. Biochem. Biophys. Res. Commun. 1997, 236, 665–669. [Google Scholar] [CrossRef]
- Cheung, P.; Yang, G.; Boden, G. Milrinone, a selective phosphodiesterase 3 inhibitor, stimulates lipolysis, endogenous glucose production, and insulin secretion. Metabolism 2003, 52, 1496–1500. [Google Scholar] [CrossRef]
- Sullivan, M.; Rena, G.; Begg, F.; Gordon, L.; Olsen, A.S.; Houslay, M.D. Identification and characterization of the human homologue of the short PDE4A cAMP-specific phosphodiesterase RD1 (PDE4A1) by analysis of the human HSPDE4A gene locus located at chromosome 19p13.2. Biochem. J. 1998, 333, 693–703. [Google Scholar] [CrossRef] [Green Version]
- Bolger, G.B.; Bizzi, M.F.; Pinheiro, S.V.B.; Trivellin, G.; Smoot, L.; Accavitti, M.-A.; Korbonits, M.; Ribeiro-Oliveira, A. cAMP-specific PDE4 Phosphodiesterases and AIP in the Pathogenesis of Pituitary Tumors. Endocr Relat Cancer. 2016, 23, 419–431. [Google Scholar] [CrossRef] [Green Version]
- D’Sa, C.; Tolbert, L.M.; Conti, M.; Duman, R.S. Regulation of cAMP-specific phosphodiesterases type 4B and 4D (PDE4) splice variants by cAMP signaling in primary cortical neurons. J. Neurochem. 2002, 81, 745–757. [Google Scholar] [CrossRef]
- Fertig, B.A.; Baillie, G.S. PDE4-Mediated cAMP Signalling. J. Cardiovasc. Dev. Dis. Rev. 2018, 4, 8. [Google Scholar] [CrossRef] [Green Version]
- Bolger, G.; Michaeli, T.; Martins, T.; John, T.; Steiner, B.; Rodgers, L.; Riggs, M.; Wigler, M.; Ferguson, K. A Family of Human Phosphodiesterases Homologous to the dunce Learning and Memory Gene Product of Drosophila melanogaster Are Potential Targets for Antidepressant Drugs. Mol. Cell. Biol. 1993, 13, 6558–6571. [Google Scholar] [CrossRef]
- Sette, C.; Conti, M.; Chem, M.J.B. Phosphorylation and Activation of a cAMP-specific Phosphodiesterase by the cAMP-dependent Protein Kinase. J. Biol. Chem. 1996, 271, 16526–16534. [Google Scholar] [CrossRef] [Green Version]
- Mackenzie, S.J.; Baillie, G.S.; Mcphee, I.; Bolger, G.B.; Houslay, M.D. ERK2 Mitogen-activated Protein Kinase Binding, Phosphorylation, and Regulation of the PDE4D cAMP-specific Phosphodiesterases. J. Biol. Chem. 2000, 275, 16609–16617. [Google Scholar] [CrossRef] [Green Version]
- Klussmann, E. Repository of the Max Delbrück Center for Molecular Medicine (MDC) in the Helmholtz Association Protein-protein interactions of PDE4 family members-Functions, interactions and therapeutic value. Cell. Signal. 2016, 2, 713–718. [Google Scholar] [CrossRef] [Green Version]
- Willoughby, D.; Wong, W.; Schaack, J.; Scott, J.D.; Cooper, D.M.F. An anchored PKA and PDE4 complex regulates. EMBO J. 2006, 25, 2051–2061. [Google Scholar] [CrossRef] [Green Version]
- Francis, S.H.; Blount, M.A.; Corbin, J.D. Mammalian Cyclic Nucleotide Phosphodiesterases: Molecular Mechanisms and Physiological Functions. Physiol. Rev. 2011, 91, 651–690. [Google Scholar] [CrossRef] [Green Version]
- Kelly, M.P. Cyclic nucleotide signaling changes associated with normal aging and age-related diseases of the brain. Cell Signal. 2019, 42, 281–291. [Google Scholar] [CrossRef]
- Tibbo, A.J.; Baillie, G.S. Phosphodiesterase 4B: Master Regulator of Brain Signaling. Cells 2020, 9, 1254. [Google Scholar] [CrossRef]
- Baliga, R.S.; Preedy, M.E.J.J.; Dukinfield, M.S.; Chu, S.M.; Aubdool, A.A.; Bubb, K.J.; Moyes, A.J.; Tones, M.A.; Hobbs, A.J. Phosphodiesterase 2 inhibition preferentially promotes NO/guanylyl cyclase/cGMP signaling to reverse the development of heart failure. Proc. Natl. Acad. Sci. USA 2018, 115, E7428–E7437. [Google Scholar] [CrossRef] [Green Version]
- Turko, I.V.; Francis, S.H.; Corbin, J.D. phosphodiesterase (PDE5) is required for its phosphorylation. Biochem. J. 1998, 329, 505–510. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ayala, J.E.; Bracy, D.P.; Julien, B.M.; Rottman, J.N.; Fueger, P.T.; Wasserman, D.H. Chronic Treatment With Sildenafil Improves Energy Balance and Insulin Action in High Fat–Fed Conscious Mice. Diabetes 2007, 56, 1025–1033. [Google Scholar] [CrossRef] [Green Version]
- Behr-Roussel, D.; Oudot, A.; Caisey, S.; Coz, O.L.E.; Gorny, D.; Bernabé, J.; Wayman, C.; Alexandre, L.; Giuliano, F.A. Daily Treatment with Sildenafil Reverses Endothelial Dysfunction and Oxidative Stress in an Animal Model of Insulin Resistance. Sex. Med. 2008, 53, P1272–P1281. [Google Scholar] [CrossRef]
- Lee, R.; Wolda, S.; Moon, E.; Esselstyn, J.; Hertel, C.; Lerner, A. PDE7A is expressed in human B-lymphocytes and is up-regulated by elevation of intracellular cAMP. Cell Signal. 2002, 14, 277–284. [Google Scholar] [CrossRef]
- Wu, P.; Wang, P. Per-Arnt-Sim domain-dependent association of cAMP-phosphodiesterase 8A1 with IκB proteins. PNAS 2004, 101, 17634–17639. [Google Scholar] [CrossRef] [Green Version]
- Brown, K.M.; Lee, L.C.Y.; Findlay, J.E.; Day, J.P.; Baillie, G.S. Cyclic AMP-specific phosphodiesterase, PDE8A1, is activated by protein kinase A-mediated phosphorylation. FEBS Lett. 2012, 586, 1631–1637. [Google Scholar] [CrossRef] [Green Version]
- Horvath, A.; Giatzakis, C.; Tsang, K.; Greene, E.; Boikos, S.; Libè, R.; Patronas, Y.; Robinson-white, A.; Remmers, E.; Bertherat, J.; et al. A cAMP-specific phosphodiesterase (PDE8B) that is mutated in adrenal hyperplasia is expressed widely in human and mouse tissues: A novel PDE8B isoform in human adrenal cortex. Eur. J. Hum. Genet. 2008, 16, 1245–1253. [Google Scholar] [CrossRef]
- Huai, Q.; Wang, H.; Zhang, W.; Colman, R.W.; Robinson, H.; Ke, H. Crystal structure of phosphodiesterase 9 shows orientation variation of inhibitor 3-isobutyl-1- methylxanthine binding. PNAS 2004, 101, 9624–9629. [Google Scholar] [CrossRef] [Green Version]
- Halpin, D.M.G. ABCD of the phosphodiesterase family: Interaction and differential activity in COPD. Int. J. COPD 2008, 3, 543–561. [Google Scholar] [CrossRef] [Green Version]
- Harms, J.F.; Menniti, F.S.; Schmidt, C.J. Phosphodiesterase 9A in brain regulates cGMP signaling independent of nitric-oxide. Front. Neurosci. 2019, 13. [Google Scholar] [CrossRef]
- Reneerkens, O.A.H.; Rutten, K.; Steinbusch, H.W.M.; Blokland, A.; Prickaerts, J. Selective phosphodiesterase inhibitors: A promising target for cognition enhancement. Psychopharmacology (Berl) 2009, 202, 419–443. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sandner, P. From molecules to patients: Exploring the therapeutic role of soluble guanylate cyclase stimulators. Biol. Chem. 2018, 399, 679–690. [Google Scholar] [CrossRef]
- Soderling, S.H.; Beavo, J.A. Regulation of cAMP and cGMP signaling: New phosphodiesterases and new functions. Curr. Opin. Cell Biol. 2000, 12, 174–179. [Google Scholar] [CrossRef]
- Russwurm, C.; Koesling, D.; Russwurm, M. Phosphodiesterase 10A is tethered to a synaptic signaling complex in striatum. J. Biol. Chem. 2015, 290, 11936–11947. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nawrocki, A.R.; Rodriguez, C.G.; Toolan, D.M.; Price, O.; Henry, M.; Forrest, G.; Szeto, D.; Keohane, C.A.; Pan, Y.; Smith, K.M.; et al. Genetic deletion and pharmacological inhibition of phosphodiesterase 10A protects mice from diet-induced obesity and insulin resistance. Diabetes 2014, 63, 300–311. [Google Scholar] [CrossRef] [Green Version]
- Rouse, M.; Younès, A.; Egan, J.M. Resveratrol and curcumin enhance pancreatic β-cell function by inhibiting phosphodiesterase activity. J. Endocrinol. 2014, 223, 107–117. [Google Scholar] [CrossRef] [PubMed]
- Cantin, L.D.; Magnuson, S.; Gunn, D.; Barucci, N.; Breuhaus, M.; Bullock, W.H.; Burke, J.; Claus, T.H.; Daly, M.; DeCarr, L.; et al. PDE-10A inhibitors as insulin secretagogues. Bioorg. Med. Chem. Lett. 2007, 17, 2869–2873. [Google Scholar] [CrossRef]
- Jäger, R.; Russwurm, C.; Schwede, F.; Genieser, H.G.; Koesling, D.; Russwurm, M. Activation of PDE10 and PDE11 phosphodiesterases. J. Biol. Chem. 2012, 287, 1210–1219. [Google Scholar] [CrossRef] [Green Version]
- Omori, K.; Kotera, J. Overview of PDEs and their regulation. Circ. Res. 2007, 100, 309–327. [Google Scholar] [CrossRef]
- Ceyhan, O.; Birsoy, K.; Hoffman, C.S. Article Identification of Biologically Active PDE11-Selective Inhibitors Using a Yeast-Based High-Throughput Screen. Chem. Biol. 2012, 19, 155–163. [Google Scholar] [CrossRef] [Green Version]
- Boland, B.B.; Alarcón, C.; Ali, A.; Rhodes, C.J. Monomethylated-adenines potentiate glucose-induced insulin production and secretion via inhibition of phosphodiesterase activity in rat pancreatic islets. Islets 2015, 7, e1073435. [Google Scholar] [CrossRef] [Green Version]
- Holst, J.J.; Gromada, J. Role of incretin hormones in the regulation of insulin secretion in diabetic and nondiabetic humans. Am. J. Physiol Endocrinol. Metab 2004, 287, E199–E206. [Google Scholar] [CrossRef]
- Sheehy, D.; Quinnell, S.; Vegas, A.J. Targeting Type 1 Diabetes: Selective Approaches for New Therapies. Biochemistry 2019, 58, 214–233. [Google Scholar] [CrossRef]
- Nicholls, D.G. The Pancreatic β-Cell: A Bioenergetic Perspective. Physiol. Rev. 2016, 96, 1385–1447. [Google Scholar] [CrossRef] [Green Version]
- Doyle, M.E.; Egan, J.M. Mechanisms of Action of GLP-1 in the Pancreas. Pharmacol. Ther. 2008, 113, 546–593. [Google Scholar] [CrossRef] [Green Version]
- Chepurny, O.G.; Hussain, M.A.; Holz, G.G. Exendin-4 as a Stimulator of Rat Insulin I Gene Promoter Activity via bZIP/CRE Interactions Sensitive to Serine/Threonine Protein Kinase Inhibitor Ro 31-8220. Endocrinology 2002, 143, 2303–2313. [Google Scholar] [CrossRef]
- Furman, B.; Ong, W.K.; Pyne, N. Cyclic AMP signaling in pancreatic islets. Adv. Exp. Med. Biol. 2010, 654, 281–304. [Google Scholar] [CrossRef]
- Ong, W.K.; Gribble, F.M.; Reimann, F.; Lynch, M.J.; Houslay, M.D.; Baillie, G.S.; Furman, B.L.; Pyne, N.J. The role of the PDE4D cAMP phosphodiesterase in the regulation of glucagon-like peptide-1 release. Br. J. Pharmacol. 2009, 157, 633–644. [Google Scholar] [CrossRef] [Green Version]
- Baillie, G.S.; Tejeda, G.S.; Kelly, M.P. Therapeutic targeting of 3′,5′-cyclic nucleotide phosphodiesterases: Inhibition and beyond. Nat. Rev. Drug Discov. 2019, 18, 770–796. [Google Scholar] [CrossRef] [PubMed]
- Xie, T.; Chen, M.; Zhang, Q.; Ma, Z.; Weinstein, L.S. Beta cell-specific deficiency of the stimulatory G protein alpha-subunit Gsalpha leads to reduced beta cell mass and insulin-deficient diabetes. PNAS 2007, 104, 19601–19606. [Google Scholar] [CrossRef] [Green Version]
- Xie, W.; Ye, Y.; Feng, Y.; Xu, T.; Huang, S.; Shen, J.; Leng, Y. Linderane suppresses hepatic gluconeogenesis by inhibiting the cAMP/PKA/CREB pathway through indirect activation of PDE 3 via ERK/STAT3. Front. Pharmacol. 2018, 9, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Johanns, M.; Lai, Y.; Hsu, M.; Jacobs, R.; Vertommen, D.; Van Sande, J.; Dumont, J.E.; Woods, A. AMPK antagonizes hepatic glucagon-stimulated cyclic AMP signalling via phosphorylation-induced activation of cyclic nucleotide phosphodiesterase 4B. Nat. Commun. 2016, 7, 10856. [Google Scholar] [CrossRef]
- Meng, S.; Cao, J.; He, Q.; Xiong, L.; Chang, E.; Radovick, S.; Wondisford, F.E.; He, L. Metformin activates AMP-activated protein kinase by promoting formation of the αβγheterotrimeric complex. J. Biol. Chem. 2015, 290, 3393–3802. [Google Scholar] [CrossRef] [Green Version]
- Miller, R.A.; Chu, Q.; Xie, J.; Foretz, M.; Viollet, B.; Birnbaum, M.J. Biguanides suppress hepatic glucagon signaling by decreasing production of cyclic AMP. Nature 2013, 494, 256–260. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Andersson, O.; Adams, B.A.; Yoo, D.; Ellis, G.C.; Gut, P.; Anderson, R.M.; German, M.S.; Stainier, D.Y.R. Article Adenosine Signaling Promotes Regeneration of Pancreatic b Cells In Vivo. Cell Metab. 2012, 15, 885–894. [Google Scholar] [CrossRef] [Green Version]
- Zhao, Z.; Low, Y.S.; Armstrong, N.A.; Ryu, J.H.; Sun, S.A.; Arvanites, A.C.; Hollister-lock, J.; Shah, N.H.; Weir, G.C.; Annes, J.P. Repurposing cAMP-Modulating Medications to Promote β-Cell Replication. Mol. Endocrinol. 2014, 28, 1682–1697. [Google Scholar] [CrossRef]
- Abdollahi, M.; Chan, T.; Subrahmanyam, V.; O’Brien, P. Effects of phosphodiesterase 3,4,5 inhibitors on hepatocyte cAMP levels, glycogenolysis, gluconeogenesis and suceptibility to a mitochondrial toxin. Mol. Cell. Biochem. 2003, 252, 205–211. [Google Scholar] [CrossRef]
- Haak, T.; Gölz, S.; Fritsche, A.; Füchtenbusch, M.; Siegmund, T.; Schnellbächer, E.; Klein, H.H.; Uebel, T.; Droßel, D.; Clinic, I.; et al. Therapy of Type 1 Diabetes Abridged Version of the S3 Guideline (AWMF Register Number: 057–013; 2 nd Edition) Authors Diabetes. Exp. Clin. Endocrinol. Diabetes 2019, 127, S27–S38. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rojas, J.; Bermudez, V.; Palmar, J.; Martínez, M.S.; Olivar, L.C.; Nava, M.; Tomey, D.; Rojas, M.; Salazar, J.; Garicano, C.; et al. Review Article Pancreatic Beta Cell Death: Novel Potential Mechanisms in Diabetes Therapy. J. Diabetes Res. 2018, 2018, 1–19. [Google Scholar] [CrossRef] [Green Version]
- Malik, A.; Morya, R.K.; Bhadada, S.K.; Rana, S. Type 1 diabetes mellitus: Complex interplay of oxidative stress, cytokines, gastrointestinal motility and small intestinal bacterial overgrowth. Eur. J. Clin. Invest. 2018, 48. [Google Scholar] [CrossRef]
- Cnop, M.; Welsh, N.; Jonas, J.; Jorns, A.; Lenzen, S.; Eizirik, D.L. Many Differences, Few Similarities. Diabetes 2005, 54, 97–107. [Google Scholar] [CrossRef] [Green Version]
- Souness, J.E.; Aldous, D.; Sargent, C. Immunosuppressive and anti-inflammatory effects of cyclic AMP phosphodiesterase (PDE) type 4 inhibitors. Immunopharmacology 2000, 47, 127–162. [Google Scholar] [CrossRef]
- Li, H.; Zuo, J.; Tang, W. Phosphodiesterase-4 inhibitors for the treatment of inflammatory diseases. Front. Pharmacol. 2018, 9, 1048. [Google Scholar] [CrossRef] [Green Version]
- Agrawal, N.K.; Maiti, R.; Dash, D.; Pandey, B.L. Cilostazol reduces inflammatory burden and oxidative stress in hypertensive type 2 diabetes mellitus patients. Pharmacol. Res. 2007, 56, 118–123. [Google Scholar] [CrossRef] [PubMed]
- Miller, M.S. Phosphodiesterase inhibition in the treatment of autoimmune and inflammatory diseases: Current status and potential. J. Receptor. Ligand Channel Res. 2015, 15, 19–30. [Google Scholar] [CrossRef] [Green Version]
- Boswell-Smith, V.; Spina, D.; Page, C.P. Phosphodiesterase inhibitors. Br. J. Pharmacol. 2006, 147, 252–257. [Google Scholar] [CrossRef]
- Byun, H.R.; Choi, J.A.; Koh, J.Y. The role of metallothionein-3 in streptozotocin-induced beta-islet cell death and diabetes in mice. Metallomics 2014, 6, 1748–1757. [Google Scholar] [CrossRef] [PubMed]
- Malekifard, F.; Delirezh, N.; Hobbenaghi, R.; Malekinejad, H. Immunotherapeutic effects of pentoxifylline in type 1 diabetic mice and its role in the response of T-helper lymphocytes. Iran J. Basic Med. Sci. 2015, 18, 2–7. [Google Scholar]
- Liang, L.; Beshay, E.; Prud’homme, G. The phosphodiesterase inhibitors pentoxifylline and rolipram prevent diabetes in NOD mice. Diabetes 1998, 47, 570–575. [Google Scholar] [CrossRef]
- Wensheng, L.; Zhangzhili; Zhaoying, L. Effects of rlipram on apoptosis of T lymphocytes in non-obese diabetic mice. Mod. Med. J. 2003, 31, 77–80. [Google Scholar]
- Stosic-Grujicic, S.D.; Maksimovic, D.D.; Mostarica Stojkovic, M.B.; Miodrag, L.L. Pentoxifylline Prevents Autoimmune Mediated Inflammation in Low Dose Streptozotocin Induced Diabetes. Dev. Immunol. 2001, 8, 213–221. [Google Scholar] [CrossRef]
- Fang, L.; Radovits, T.; Szabó, G.; Mózes, M.M.; Rosivall, L.; Kökény, G. Selective phosphodiesterase-5 (PDE-5) inhibitor vardenafil ameliorates renal damage in type 1 diabetic rats by restoring cyclic 3′,5′ guanosine monophosphate (cGMP) level in podocytes. Nephrol. Dial. Transplant. 2013, 28, 1751–1761. [Google Scholar] [CrossRef] [Green Version]
- Berman, B.; Duncan, M.R. Pentoxifylline inhibits the proliferation of human fibroblasts derived from keloid, scleroderma and morphoea skin and their production of collagen, glycosaminoglycans and fibronectin. Br. J. Pharmacol. 1990, 123, 339–346. [Google Scholar] [CrossRef]
- Hosseini, F.; Mohammadbeigi, A.; Aghaali, M.; Borujerdi, R.; Parham, M. Effect of pentoxifylline on diabetic distal polyneuropathy in type 2 diabetic patients: A randomized trial. J. Res. Med. Sci. 2019, 24, 1–6. [Google Scholar] [CrossRef]
- MacDonald, M.J.; Shahidi, N.T.; Allen, D.B.; Lustig, R.H.; Mitchell, T.L.; Susan, T. Cornwell Pentoxifylline in the Treatment of Children With New-Onset Type I Diabetes Mellitus. JAMA 1994, 271, 27–28. [Google Scholar] [CrossRef]
- Solerte, S.B.; Fioravanti, M.; Cerutti, N.; Severgnini, S.; Locatelli, M.; Pezza, N.; Rondanelli, M.; Trecate, L.; Balza, G.; Ferrari, E. Retrospective analysis of long-term hemorheologic effects of pentoxifylline in diabetic patients with angiopathic complications. Acta Diabetol. 1997, 34, 67–74. [Google Scholar] [CrossRef]
- Rendell, M.S.; Rajfer, J.; Wicker, P.A.; Michael, D. Smith Sildenafil for treatment of erectile dysfunction. JAMA 1999, 21, 366–370. [Google Scholar]
- Behrend, L.; Vibe-Petersen, J.; Perrild, H. Sildenafil in the treatment of erectile dysfunction in men with diabetes: Demand, efficacy and patient satisfaction. Int. J. Impot. Res. 2005, 17, 264–269. [Google Scholar] [CrossRef]
- Fu, Z.; Gilbert, E.R.; Liu, D. Regulation of Insulin Synthesis and Secretion and Pancreatic Beta-Cell Dysfunction in Diabetes. Curr. Diabetes Rev. 2013, 9, 25–53. [Google Scholar] [CrossRef]
- Petersen, M.C.; Shulman, G.I. Mechanisms of Insulin Action and Insulin Resistance. Physiol. Rev. 2018, 98, 2133–2223. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kahn, S.E.; Hull, R.L.; Utzschneider, K.M. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 2006, 444, 840–846. [Google Scholar] [CrossRef]
- Hill, K.D.; Eckhauser, A.W.; Marney, A.; Brown, N.J. Phosphodiesterase 5 Inhibition Improves β -Cell Function in Metabolic Syndrome. Diabetes Care 2009, 32, 857–859. [Google Scholar] [CrossRef] [Green Version]
- Aamodt, K.I.; Aramandla, R.; Brown, J.J.; Fiaschi-Taesch, N.; Wang, P.; Stewart, A.F.; Brissova, M.; Powers, A.C. Development of a reliable automated screening system to identify small molecules and biologics that promote human β-cell regeneration. Am. J. Physiol. Endocrinol. Metab. 2016, 311, E859–E868. [Google Scholar] [CrossRef] [Green Version]
- Kushi, R.; Hirota, Y.; Ogawa, W. Insulin resistance and exaggerated insulin sensitivity triggered by single-gene mutations in the insulin signaling pathway. Diabetol. Int. 2020, 1–6. [Google Scholar] [CrossRef]
- Erukainure, O.L.; Ijomone, O.M.; A.Oyebode, O.; I.Chukwuma, C.; Aschner, M.; Islama, M.S. Hyperglycemia-induced oxidative brain injury: Therapeutic effects of Cola nitida infusion against redox imbalance, cerebellar neuronal insults, and upregulated Nrf2 expression in type 2 diabetic rats. Food Chem. Toxicol. 2019, 127, 206–217. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Wang, H. Oxidative stress in pancreatic beta cell regeneration. Oxid. Med. Cell. Longev. 2017, 2017. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, J.S.; Chuang, T.J.; Chen, J.H.; Lee, C.H.; Hsieh, C.H.; Lin, T.K.; Hsiao, F.C.; Hung, Y.J. Cilostazol attenuates the severity of peripheral arterial occlusive disease in patients with type 2 diabetes: The role of plasma soluble receptor for advanced glycation end-products. Endocrine 2015, 703–710. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hsieh, C.; Wang, P. Effect of Cilostazol Treatment on Adiponectin and Soluble CD40 Ligand Levels in Diabetic Patients With Peripheral Arterial Occlusion Disease. Circ. J. 2009, 73, 948–954. [Google Scholar] [CrossRef] [Green Version]
- Chapman, T.M.; Goa, K.L. A Review of its Use in Intermittent Claudication. Am. J. Cardiovasc. Drugs 2003, 3, 117–138. [Google Scholar] [CrossRef] [PubMed]
- Park, S.Y.; Shin, H.K.; Lee, J.; Kim, C.D.; Lee, W.S.; Rhim, B.Y.; Hong, K.W. Cilostazol Ameliorates Metabolic Abnormalities with Suppression of Proinflammatory Markers in a db/db Mouse Model of Type 2 Diabetes via Activation of Peroxisome Proliferator-Activated Receptor γ Transcription. J. Pharmacol. Exp. Ther. 2009, 374, 571–579. [Google Scholar] [CrossRef] [Green Version]
- Chang, S.A.; Cha, B.Y.; Yoo, S.J.; Ahn, Y.B.; Song, K.H.; Han, J.H.; Lee, J.M.; Son, H.S.; Yoon, K.H.; Kang, M.I.; et al. The effect of cilostazol on glucose tolera ce and insulin resistance in a rat model of non-insulin dependent diabetes mellitus. Korean J. Intern. Med. 2001, 16, 87–92. [Google Scholar] [CrossRef]
- Nakaya, Y.; Minami, A.; Sakamoto, S.; Niwa, Y.; Ohnaka, M.; Harada, N.; Nakamura, T. Cilostazol, a phosphodiesterase inhibitor, improves insulin sensitivity in the Otsuka Long-Evans Tokushima Fatty Rat, a model of spontaneous NIDDM. Diabetes Obes. Metab. 1999, 1, 37–41. [Google Scholar] [CrossRef]
- Wada, T.; Onogia, Y.; Kimura, Y.; Nakano, T.; Fusanobori, H.; Ishii, Y.; Sasahara, M.; Tsuneki, H.; Sasaoka, T. Cilostazol ameliorates systemic insulin resistance in diabetic db/db mice by suppressing chronic inflammation in adipose tissue via modulation of both adipocyte and macrophage functions. Eur. J. Pharmacol. 2013, 707, 120–129. [Google Scholar] [CrossRef] [PubMed]
- Aoki, Y.; Shimizu, M.; Watanabe, N. The Blood Glucose Level Increased in Parallel with the Heart Rate Following Cilostazol Administration in Three Diabetic Patients. Intern. Med. 2014, 53, 859–863. [Google Scholar] [CrossRef] [Green Version]
- Asal, N.J.; Wojciak, K.A. Effect of cilostazol in treating diabetes-associated microvascular complications. Endocrine 2017, 56, 240–244. [Google Scholar] [CrossRef] [Green Version]
- Tang, W.-H.; Lin, F.-H.; Lee, C.-H.; Kuo, F.-C.; Hsieh, C.-H.; Hsiao, F.-C.; Hung, Y.-J. Cilostazol effectively attenuates deterioration of albuminuria in patients with type 2 diabetes: A randomized, placebo-controlled trial. Endocrine 2014, 45, 293–301. [Google Scholar] [CrossRef]
- Rosales, R.L.; Delgado-Delos Santos, M.M.S.; Mercado-Asis, L.B. Cilostazol: A Pilot Study on Safety and Clinical Efficacy in Neuropathies of Diabetes Mellitus Type 2 (ASCEND). Angiology 2011, 62, 625–635. [Google Scholar] [CrossRef]
- Ma, X.; Guo, X.; Xiao, X.; Guo, L.; Lv, X.; Li, Q.; Gao, Y. A randomized, open-label, multicentre study to evaluate plasma atherosclerotic biomarkers in patients with type 2 diabetes mellitus and arteriosclerosis obliterans when treated with Probucol and Cilostazol. J. Geriatr. Cardiol. 2012, 1, 228–236. [Google Scholar] [CrossRef] [Green Version]
- Lee, J.; Lee, H.; Yoo, H.B.; Choi, J.; Jung, H.; Yoon, E.J.; Kim, H.; Jung, Y.; Lee, H.; Kim, Y.K. Efficacy of Cilostazol Administration in Alzheimer’s Disease Patients with White Matter Lesions: A Positron-Emission Tomography Study. Neurotherapeutics 2019, 16, 394–403. [Google Scholar] [CrossRef] [Green Version]
- Wu, C.; Rajagopalan, S. Phosphodiesterase-4 inhibition as a therapeutic strategy for metabolic disorders. Obes Rev. 2016, 17, 429–441. [Google Scholar] [CrossRef]
- Plock, N.; Vollert, S.; Mayer, M.; Hanauer, G.; Lahu, G. Pharmacokinetic/Pharmacodynamic Modeling of the PDE4 Inhibitor TAK-648 in Type 2 Diabetes: Early Translational Approaches for Human Dose Prediction. Clin. Transl. Sci. 2017, 10, 185–193. [Google Scholar] [CrossRef] [Green Version]
- Zhang, R.; Maratos-flier, E.; Flier, J.S. Adipose Inflammation in Mice Deficient for. Endocrinology 2009, 150, 3076–3082. [Google Scholar] [CrossRef] [Green Version]
- Park, S.; Ahmad, F.; Philp, A.; Baar, K.; Williams, T.; Ke, H.; Rehmann, H.; Taussig, R.; Brown, A.L.; Myung, K.; et al. Resveratrol Ameliorates Aging-Related Metabolic Phenotypes by Inhibiting cAMP Phosphodiesterases. Cell 2012, 148, 421–433. [Google Scholar] [CrossRef] [Green Version]
- Vollert, S.; Kaessner, N.; Heuser, A.; Hanauer, G.; Dieckmann, A.; Knaack, D.; Kley, H.P.; Beume, R.; Weiss-Haljiti, C. The glucose-lowering effects of the PDE4 inhibitors roflumilast and roflumilast-N-oxide in db/db mice. Diabetologia 2012, 55, 2779–2788. [Google Scholar] [CrossRef]
- Wouters, E.F.M.; Bredenbröker, D.; Teichmann, P.; Brose, M.; Rabe, K.F.; Fabbri, L.M.; Göke, B. Effect of the phosphodiesterase 4 inhibitor roflumilast on glucose metabolism in patients with treatment-naive, newly diagnosed type 2 diabetes mellitus. J. Clin. Endocrinol. Metab. 2012, 97, 1720–1725. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fabbri, L.M.; Calverley, P.M.; Izquierdo-Alonso, J.L.; Bundschuh, D.S.; Brose, M.; Martinez, F.J.; Rabe, K.F. Roflumilast in moderate-to-severe chronic obstructive pulmonary disease treated with longacting bronchodilators: Two randomised clinical trials. Lancet 2009, 374, P695–P703. [Google Scholar] [CrossRef]
- Calverley, P.M.; Rabe, K.F.; Goehring, U.-M.; Kristiansen, S.; Fabbri, L.M.; Fernando, J.M. Roflumilast 2009 second trials.pdf. Lancet 2009, 374, P685–P694. [Google Scholar] [CrossRef]
- Aversa, A. Systemic and metabolic effects of PDE5-inhibitor drugs. World J. Diabetes 2010, 1, 3–7. [Google Scholar] [CrossRef]
- Ramirez, C.E.; Nian, H.; Yu, C.; Gamboa, J.L.; Luther, J.M.; Brown, N.J.; Shibao, C.A. Treatment with Sildenafil Improves Insulin Sensitivity. J. Clin. Endocrinol. Metab. 2015, 100, 4533–4540. [Google Scholar] [CrossRef] [Green Version]
- Marampon, F.; Antinozzi, C.; Corinaldesi, C.; Vannelli, G.B.; Sarchielli, E.; Migliaccio, S.; Di Luigi, L.; Lenzi, A.; Crescioli, C. The phosphodiesterase 5 inhibitor tadalafil regulates lipidic homeostasis in human skeletal muscle cell metabolism. Endocrine 2018, 59, 602–613. [Google Scholar] [CrossRef]
- Aversa, A.; Fittipaldi, S.; Francomano, D.; Bimonte, V.M.; Greco, E.A.; Crescioli, C.; Luigi, L.D.; Lenzi, A.; Migliaccio, S. Tadalafil improves lean mass and endothelial function in nonobese men with mild ED/LUTS: In vivo and in vitro characterization. Endocrine 2017, 56, 639–648. [Google Scholar] [CrossRef]
- Mammi, C.; Pastore, D.; Lombardo, M.F.; Ferrelli, F.; Caprio, M.; Consoli, C.; Tesauro, M.; Gatta, L.; Fini, M.; Federici, M.; et al. Sildenafil Reduces Insulin-Resistance in Human Endothelial Cells. PLoS ONE 2011, 6, e14542. [Google Scholar] [CrossRef] [Green Version]
- Santi, D.; Locaso, M.; Granata, A.R.; Trenti, T.; Roli, L.; Pacchioni, C.; Rochira, V.; Carani, C.; Simoni, M. Could chronic Vardenafil administration influence the cardiovascular risk in men with type 2 diabetes mellitus? PLoS ONE 2018, 13, e199299. [Google Scholar] [CrossRef] [PubMed]
- Tzoumas, N.; Farrah, T.E.; Dhaun, N.; Webb, D.J. Established and emerging therapeutic uses of PDE type 5 inhibitors in cardiovascular disease. Br. J. Pharmacol. 2019, 1–22. [Google Scholar] [CrossRef] [Green Version]
- Antinozzi, C.; Sgrò, P.; Di Luigi, L. Advantages of Phosphodiesterase Type 5 Inhibitors in the Management of Glucose Metabolism Disorders: A Clinical and Translational Issue. Int. J. Endocrinol. 2020, 2020, 1–8. [Google Scholar] [CrossRef]
- Armani, A.; Marzolla, V.; Rosano, G.M.C.; Fabbri, A.; Caprio, M. Phosphodiesterase type 5 (PDE5) in the adipocyte: A novel player in fat metabolism? Trends Endocrinol. Metab. 2011, 22, P404–P411. [Google Scholar] [CrossRef] [PubMed]
- Jansson, P.; Murdolo, G.; Sjögren, L.; Nyström, B. Tadalafil increases muscle capillary recruitment and forearm glucose uptake in women with type 2 diabetes. Diabetologia 2010, 53, 2205–2208. [Google Scholar] [CrossRef] [Green Version]
- Nyströma, T.; Ortsätera, H.; Huang, Z.; Zhang, F.; Larsen, F.J.; Weitzberg, E.; Lundberg, J.O.; Sjöholm, Å. Inorganic nitrite stimulates pancreatic islet blood flow and insulin secretion. Free Radic. Biol. Med. 2012, 53, 1017–1023. [Google Scholar] [CrossRef]
- Bergandi, L.; Silvagno, F.; Russo, I.; Riganti, C.; Anfossi, G.; Aldieri, E.; Ghigo, D.; Trovati, M.; Bosia, A. Insulin Stimulates Glucose Transport Via Nitric Muscle Cells. Arter. Thromb. Vasc Biol. 2003, 23, 2215–2221. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johann, K.; Reis, M.C.; Harder, L.; Herrmann, B.; Gachkar, S.; Mittag, J.; Oelkrug, R. Effects of sildena fi l treatment on thermogenesis and glucose homeostasis in diet-induced obese mice. Nutr. Diabetes 2018. [Google Scholar] [CrossRef]
- Mandosi, E.; Giannetta, E.; Filardi, T.; Lococo, M.; Bertolini, C.; Fallarino, M.; Gianfrilli, D.; Venneri, M.A.; Lenti, L.; Lenzi, A.; et al. treatment and effects on metabolic control in type 2 diabetes Endothelial dysfunction markers as a therapeutic target for Sildenafil treatment and effects on metabolic control in type 2 diabetes. Expert Opin. Ther. Targets 2015, 19, 1–6. [Google Scholar] [CrossRef]
- Grover-Páez, F.; Rivera, G.V.; Ortíz, R.G. Sildenafil citrate diminishes microalbuminuria and the percentage of A1c in male patients with type 2 diabetes.pdf. Diabetes Res. Clin. Pract. 2007, 78, 136–140. [Google Scholar] [CrossRef] [PubMed]
- Scheele, W.; Diamond, S.; Gale, J.; Clerin, V.; Tamimi, N.; Le, V.; Walley, R.; Grover-páez, F.; Perros-huguet, C.; Rolph, T.; et al. Phosphodiesterase Type 5 Inhibition Reduces Albuminuria in Subjects with Overt Diabetic Nephropathy. J. Am. Soc. Nephrol. 2016, 27, 3459–3468. [Google Scholar] [CrossRef] [Green Version]
- Sherifali, D.; Nerenberg, K.; Pullenayegum, E.; Cheng, J.E.; Gernstein, H.C. The Effect of Oral Antidiabetic Agents on A1C Levels. A systematic review and meta-analysis. Diabetes Care 2010, 33, 1859–1864. [Google Scholar] [CrossRef] [Green Version]
- Murdolo, G.; Sjo, M.; Strindberg, L.; Lo, P. Diabetic Postmenopausal Females. J. Clin. Endocrinol. Metab. 2013, 98, 245–254. [Google Scholar] [CrossRef] [Green Version]
- González-Ortiz, M.; Martínez-Abundis, E.; Hernández-Corona, D.; Ramírez-Rodríguez, A. Effect of tadalafil administration on insulin secretion and insulin sensitivity in obese men. Acta Clin. Belgic. 2017, 72, 326–330. [Google Scholar] [CrossRef]
- Sbardella, E.; Minnetti, M.; Aluisio, D.D.; Rizza, L.; Rosaria, M.; Giorgio, D.; Vinci, F.; Pofi, R.; Giannetta, E.; Venneri, M.A.; et al. Cardiovascular features of possible autonomous cortisol secretion in patients with adrenal incidentalomas. Eur. J. Endocrinol. 2018, 178, 501–511. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Califano, J.A.; Khan, Z.; Noonan, K.A.; Rudraraju, L.; Wang, H.; Goodman, S.; Gourin, C.G.; Ha, P.K.; Saunders, J.; Levine, M.; et al. Tadalafil augments tumor specific immunity in patients with head and neck squamous cell carcinoma. Clin. Cancer Res. 2015, 21, 30–38. [Google Scholar] [CrossRef] [Green Version]
- Fiore, D.; Gianfrilli, D.; Giannetta, E.; Galea, N.; Panio, G.; Dato, C.; Pofi, R.; Pozza, C.; Sbardella, E.; Carbone, I.; et al. PDE5 Inhibition Ameliorates Visceral Adiposity Targeting the miR-22/SIRT1 Pathway: Evidence From the CECSID Trial. J. Clin. Endocrinol. Meta 2016, 101, 1525–1534. [Google Scholar] [CrossRef] [Green Version]
- Anderson, S.G.; Hutchings, D.C.; Woodward, M.; Rahimi, K.; Rutter, M.K.; Kirby, M.; Hackett, G.; Trafford, A.W.; Heald, A.H. Phosphodiesterase type-5 inhibitor use in type 2 diabetes is associated with a reduction in all-cause mortality. Card. Risk Factors Prev. 2016, 102, 1750–1756. [Google Scholar] [CrossRef] [Green Version]
- West, T.M.; Wang, Q.; Deng, B.; Zhang, Y.; Barbagallo, F.; Reddy, G.R.; Chen, D.; Phan, K.S.; Xu, B.; Isidori, A.; et al. Phosphodiesterase 5 Associates With β2 Adrenergic Receptor to Modulate Cardiac Function in Type 2 Diabetic Hearts. J. Am. Heart Assoc. 2019, 8, 1–19. [Google Scholar] [CrossRef] [Green Version]
- Das, A.; Durrant, D.; Salloum, F.N.; Xi, L.; Kukreja, R.C. PDE5 inhibitors as therapeutics for heart disease, diabetes and cancer. Pharmacol. Ther. 2015, 147, 12–21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Radovits, T.; Bömicke, T.; Kökény, G.; Arif, R.; Loganathan, S.; Kécsán, K.; Korkmaz, S.; Barnucz, E.; Sandner, P.; Karck, M.; et al. The phosphodiesterase-5 inhibitor vardenafil improves cardiovascular dysfunction in experimental diabetes mellitus. Br. J. Pharmacol. 2009, 156, 909–919. [Google Scholar] [CrossRef] [Green Version]
- Mátyás, C.; Németh, B.T.; Oláh, A.; Török, M.; Ruppert, M.; Kellermayer, D.; Barta, B.A.; Szabó, G.; Kökény, G.; Horváth, E.M.; et al. Prevention of the development of heart failure with preserved ejection fraction by the phosphodiesterase-5A inhibitor vardenafil in rats with type 2 diabetes. Eur. J. Heart Fail. 2017, 19, 326–336. [Google Scholar] [CrossRef]
- Owan, T.E.; Hodge, D.O.; Herges, R.M.; Jacobsen, S.J.; Roger, V.L.; Redfield, M.M. Trends in Prevalence and Outcome of Heart Failure with Preserved Ejection Fraction. N. Engl. J. Med. 2006, 355, 251–259. [Google Scholar] [CrossRef] [Green Version]
- Eskesen, K.; Olsen, N.T.; Dimaano, V.L.; Fritz-Hansen, T.; Sogaard, P.; Chakir, K.; Steenbergen, C.; Kass, D.; Abraham, T.P. Sildenafil treatment attenuates ventricular remodeling in an experimental model of aortic regurgitation. Springerplus 2015, 4, 592. [Google Scholar] [CrossRef] [Green Version]
- Prysyazhna, O.; Burgoyne, J.R.; Scotcher, J.; Grover, S.; Kass, D.; Eaton, P. Phosphodiesterase 5 Inhibition Limits Doxorubicin-induced Heart Failure by Attenuating Protein Kinase G Iα Oxidation. J. Biol. Chem 2016, 291, 17427–17436. [Google Scholar] [CrossRef] [Green Version]
- Luigi, L.D.; Corinaldesi, C.; Colletti, M.; Scolletta, S.; Antinozzi, C.; Vannelli, G.B.; Giannetta, E.; Gianfrilli, D.; Isidori, A.M.; Migliaccio, S.; et al. Phosphodiesterase Type 5 Inhibitor Sildenafil Decreases the Proinflammatory Chemokine CXCL10 in Human Cardiomyocytes and in Subjects with Diabetic Cardiomyopathy. Inflammation 2016, 39, 1238–1252. [Google Scholar] [CrossRef] [Green Version]
- Giannattasio, S.; Corinaldesi, C.; Colletti, M.; Di Luigi, L.; Antinozzi, C.; Filardi, T.; Scolletta, S.; Basili, S.; Lenzi, A.; Morano, S.; et al. The phosphodiesterase 5 inhibitor sildenafil decreases the proinflammatory chemokine IL-8 in diabetic cardiomyopathy: In vivo and in vitro evidence. J. Endocrinol. Investig. 2019, 42, 715–725. [Google Scholar] [CrossRef] [Green Version]
- Clark, M.G. Impaired microvascular perfusion: A consequence of vascular dysfunction and a potential cause of insulin resistance in muscle. Am. J. Physiol. Endocrinol. Metab. 2008, 295, 732–750. [Google Scholar] [CrossRef] [Green Version]
- Genders, A.J.; Bradley, E.A.; Rattigan, S.; Richards, S.M. cGMP phosphodiesterase inhibition improves the vascular and metabolic actions of insulin in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2011, 301, 342–350. [Google Scholar] [CrossRef]
- Jonathan Posner, J.A.; Russell, B.S.P. Structure-based discovery of highly selective phosphodiesterase-9A inhibitors and implications for inhibitor design. J. Med. Chem. 2008, 23, 1–7. [Google Scholar] [CrossRef] [Green Version]
- Meng, F.; Hou, J.; Shao, Y.-X.; Wu, P.-Y.; Huang, M.; Zhu, X.; Cai, Y.; Li, Z.; Xu, J.; Liu, P.; et al. Structure-Based Discovery of Highly Selective Phosphodiesterase-9A Inhibitors and Implications for Inhibitor Design. J. Med. Chem. 2012, 55, 8549–8558. [Google Scholar] [CrossRef] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kilanowska, A.; Ziółkowska, A. Role of Phosphodiesterase in the Biology and Pathology of Diabetes. Int. J. Mol. Sci. 2020, 21, 8244. https://doi.org/10.3390/ijms21218244
Kilanowska A, Ziółkowska A. Role of Phosphodiesterase in the Biology and Pathology of Diabetes. International Journal of Molecular Sciences. 2020; 21(21):8244. https://doi.org/10.3390/ijms21218244
Chicago/Turabian StyleKilanowska, Agnieszka, and Agnieszka Ziółkowska. 2020. "Role of Phosphodiesterase in the Biology and Pathology of Diabetes" International Journal of Molecular Sciences 21, no. 21: 8244. https://doi.org/10.3390/ijms21218244