2,176
Views
13
CrossRef citations to date
0
Altmetric
Review

Research Advances in Kinase Enzymes and Inhibitors for Cardiovascular Disease Treatment

, , , &
Article: FSO204 | Received 18 Jan 2017, Accepted 29 Mar 2017, Published online: 08 Aug 2017

References

  • Mozaffarian D, Benjamin EJ, Go AS et al. Heart Disease and Stroke Statistics-2015 Update. A report From the American Heart Association. Circulation 131(4), e29–e322 (2014).
  • Centers for Disease Control and Prevention. Heart disease facts. www.cdc.gov/heartdisease/facts.htm
  • Xu J, Murphy SL, Kochanek KD, Bastian BA. Deaths: final data for 2013. Natl Vital Stat. Rep. 64(2), 1–119 (2016).
  • Kumar R, Singh VP, Baker KM. Kinase inhibitors for cardiovascular disease. J. Mol. Cell Cardiol. 42(1), 1–11 (2007).
  • Vagnozzi RJ, Hoffman NE, Elrod JW, Madesh M, Force T. Protein kinase signaling at the crossroads of myocyte life and death in ischemic heart disease. Drug Discov. Today Ther. Strateg. 9(4), e173–e182 (2012).
  • Roskoski R Jr. USFDA approved protein kinase inhibitors (2015). www.brimr.org/PKI/PKIs.htm
  • Kolluru GK, Majumder S, Chatterjee S. Rho-kinase as a therapeutic target in vascular diseases: striking nitric oxide signaling. Nitric Oxide 43, 45–54 (2014).
  • Kumar R, Singh VP, Baker KM. Kinase inhibitors for cardiovascular disease. J. Mol. Cell Cardiol. 42(1), 1–11 (2007).
  • Hidalgo CG, Chung CS, Saripalli C et al. The multifunctional Ca2+/calmodulin-dependent protein kinase II delta (CaMKIIδ) phosphorylates cardiac titin’s spring elements. J. Mol. Cell Cardiol. 54, 90–97 (2013).
  • Levy De, Wang DX, Lu Q et al. Aryl–indolyl maleimides as inhibitors of CaMKIIδ. Part 1: SAR of the aryl region. Bioorg. Med. Chem. Lett. 18(7), 2390–2394 (2008).
  • Mavunkel B, Xu YJ, Goyal B et al. Pyrimidine-based inhibitors of CaMKIIδ. Bioorg. Med. Chem. Lett. 18(7), 2404–2408 (2008).
  • Liu Q, Molkentin JD. Protein kinase Cα as a heart failure therapeutic target. J. Mol. Cell. Cardiol. 51(4), 474–478 (2011).
  • Walker JW. Protein kinase C, troponin I and heart failure: overexpressed, hyperphosphorylated and underappreciated? J. Mol. Cell. Cardiol. 40(4), 446–450 (2006).
  • Niizuma S, Inuzuka Y, Okuda J et al. Effect of persistent activation of phosphoinositide 3-kinase on heart. Life Sci. 90(15–16), 619–628 (2012).
  • Rose BA, Force T, Wang Y. Mitogen-activated protein kinase signaling in the heart: angels versus demons in a heart-breaking tale. Physiol. Rev. 90(4), 1507–1546 (2010).
  • Abraham ST, Benscoter HA, Schworer CM, Schworer CM, Singer HA. A role for Ca2+/calmodulin-dependent protein kinase II in the mitogen-activated protein kinase signaling cascade of cultured rat aortic vascular smooth muscle cells. Circ. Res. 81(4), 575–584 (1997).
  • Hidalgo CG, Chung CS, Saripalli C et al. The multifunctional Ca(2+)/calmodulin-dependent protein kinase II delta (CaMKIIdelta) phosphorylates cardiac titin’s spring elements. J. Mol. Cell. Cardiol. 54, 90–97 (2013).
  • Picht E, Desantiago J, Huke S, Kaetzel MA, Dedman JR, Bers DM. CaMKII inhibition targeted to the sarcoplasmic reticulum inhibits frequency dependent acceleration of relaxation and Ca(2+) current facilitation. J. Mol. Cell. Cardiol. 42(1), 196–205 (2007).
  • Swulius MT, Waxham MN. Ca(2+)/calmodulin-dependent protein kinases. Cell. Mol. Life Sci. 65(17), 2637–2657 (2008).
  • Barabutis N, Verin A, Catravas JD. Regulation of pulmonary endothelial barrier function by kinases. Am. J. Physiol. Lung Cell. Mol. Physiol. 311(5), L832 (2016).
  • Mayadevi M, Sherin DR, Keerthi VS, Rajasekharan KN, Omkumar RV. Curcumin is an inhibitor of calcium/calmodulin dependent protein kinase II. Bioorg. Med. Chem. 20(20), 6040–6047 (2012).
  • Mayadevi M, Sherin DR, Keerthi VS, Rajasekharan KN, Omkumar RV. Curcumin is an inhibitor of calcium/calmodulin dependent protein kinase II. Bioorg. Med. Chem. 20(20), 6040–6047 (2012).
  • Tokumitsu H, Chijiwa T, Hagiwara M, Mizutani A, Terasawa M, Hidaka H. KN-62, 1-[N,O-bis(5-isoquinolinesulfonyl)-N-methyl-L-tyrosyl]-4-phenylpiperazine, a specific inhibitor of Ca2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 265(8), 4315–4320 (1990).
  • Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95–105 (2000).
  • Yokokura H, Okada Y, Terada O, Hidaka H. HMN-709, a chlorobenzenesulfonamide derivative, is a new membrane-permeable calmodulin antagonist. Jpn J. Pharmacol. 72(2), 127–135 (1996).
  • Lu Q, Chen Z, Perumattam J et al. Aryl–indolyl maleimides as inhibitors of CaMKIIδ. Part 3: importance of the indole orientation. Bioorg. Med. Chem. Lett. 18(7), 2399–2403 (2008).
  • Komiya M, Asano S, Koike N et al. Synthesis and structure based optimization of 2-(4-phenoxybenzoyl)-5-hydroxyindole as a novel CaMKII inhibitor. Bioorg. Med. Chem. 20(23), 6840–6847 (2012).
  • Beauverger P, Gegis G, Biscarrat S, Duclos O, Mccort G. (2012). 5-Oxo-5,8-dihydropyridol [2,3-d] pyrimidine derivatives as CAMKII kinase inhibitors for treating cardiovascular disease. US patent, 0277220, 2012-11-01
  • Shahin R, Taha MO. Elaborate ligand-based modeling and subsequent synthetic exploration unveil new nanomolar Ca2+/calmodulin-dependent protein kinase II inhibitory leads. Bioorg. Med. Chem. 20(1), 377–400 (2012).
  • Shahin R, Taha MO. Elaborate ligand-based modeling and subsequent synthetic exploration unveil new nanomolar Ca2+/calmodulin-dependent protein kinase II inhibitory leads. ( 1464–3391 (Electronic)) (2012).
  • Erickson JR. Mechanisms of CaMKII activation in the heart. Front. Pharmacol. 5, 59 (2014).
  • Knight ZA, Shokat KM. Features of selective kinase inhibitors. Chem. Biol. 12(6), 621–637 (2005).
  • Wu P, Clausen MH, Nielsen TE. Allosteric small-molecule kinase inhibitors. Pharmacol. Ther. 156, 59–68 (2015).
  • Oh KS, Oh BK, Park CH et al. Cardiovascular effects of a novel selective Rho kinase inhibitor, 2-(1H-indazole-5-yl)amino-4-methoxy-6-piperazino triazine (DW1865). Eur. J. Pharmacol. 702(1–3), 218–226 (2013).
  • Noma K, Oyama N, Liao JK. Physiological role of ROCKs in the cardiovascular system. Am. J. Phsyiol. Cell Physiol. 290(3), C661–C668 (2006).
  • Schroter T, Minond D, Weiser A et al. Comparison of miniaturized time-resolved fluorescence resonance energy transfer and enzyme-coupled luciferase high-throughput screening assays to discover inhibitors of Rho-kinase II (ROCK-II). J. Biomol. Screen. 13(1), 17–28 (2008).
  • Feng Y, Yin Y, Weiser A et al. Discovery of substituted 4-(pyrazol-4-yl)-phenylbenzodioxane-2-carboxamides as potent and highly selective Rho kinase (ROCK-II) inhibitors. J. Med. Chem. 51(21), 6642–6645 (2008).
  • Ono-Saito N, Niki I, Hidaka H. H-series protein kinase inhibitors and potential clinical applications. Pharmacol. Ther. 82, 123 (1999).
  • Uehata M, Ishizaki T, Satoh H et al. Calcium sensitization of smooth muscle mediated by a rho-associated protein kinase in hypertension. Nature 389, 990 (1997).
  • Feng Y, Lograsso PV, Defert O, Li R. Rho kinase (ROCK) inhibitors and their therapeutic potential. J. Med. Chem. 59(6), 2269–2300 (2016).
  • Cerebral Vasospasm. Seiler RW, Steiger HJ ( Eds). Springer-Verlag Wien, Vienna, Austria (2001).
  • Mueller BK, Mack H, Teusch N. Rho kinase, a promising drug target for neurological disorders. Nat. Rev. Drug Discov. 4(5), 387–398 (2005).
  • Garnock-Jones KP. Ripasudil: first global approval. Drugs 74, 2211 (2014).
  • Tanihara H, Inoue T, Yamamoto T et al. Phase II randomized clinical study of a rho kinase inhibitor, K-115, in primary open-angle glaucoma and ocular hypertension. Am. J. Ophthalmol. 156, 731 (2013).
  • Tanihara H, Inoue T, Yamamoto T et al. Phase II clinical trials of a selective rho kinase inhibitor, K-115. JAMA Ophthalmol. 131, 1288 (2013).
  • Ikenoya M, Hidaka H, Hosoya T, Suzuki M, Yamamoto N, Sasaki Y. Inhibition of rho-kinase-induced myristoylated alanine-rich C kinase substrate (MARCKS) phosphorylation in human neuronal cells by H-1152, a novel and specific rho-kinase inhibitor. J. Neurochem. 81, 9 (2002).
  • Sasaki Y, Suzuki M, Hidaka H. The novel and specific rho-kinase inhibitor (S)-(+)-2-methyl-1-[(4-methyl-5-isoquinoline)sulfonyl]-homopiperazine as a probing molecule for rho-kinase-involved pathway. Pharmacol. Ther. 93, 225 (2002).
  • Lavogina D, Kalind K, Bredihhina J et al. Conjugates of 5-isoquinolinesulfonylamides and oligo-D-arginine possess high affinity and selectivity towards Rho kinase (ROCK). Bioorg. Med. Chem. Lett. 22(10), 3425–3430 (2012).
  • Ishizaki T, Uehata M, Tamechika I et al. Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol. Pharmacol. 57, 976 (2000).
  • Tokushige H, Waki M, Takayama Y, Tanihara H. Effects of Y-39983, a selective rho-associated protein kinase inhibitor, on blood flow in optic nerve head in rabbits and axonal regeneration of retinal ganglion cells in rats. Curr. Eye Res. 36, 964 (2011).
  • Feng Y, Cameron MD, Frackowiak B et al. Structure–activity relationships, and drug metabolism and pharmacokinetic properties for indazole piperazine and indazole piperidine inhibitors of ROCK-II. Bioorg. Med. Chem. Lett. 17, 2355 (2007).
  • Feng Y, Yin Y, Weiser A et al. Discovery of substituted 4-(pyrazol-4-yl)-phenylbenzodioxane-2-carboxamides as potent and highly selective rho kinase (ROCK-II) inhibitors. J. Med. Chem. 51, 6642 (2008).
  • Fang X, Yin Y, Wang B et al. Tetrahydroisoquinoline derivatives as potent and selective rho kinase inhibitors. J. Med. Chem. 53, 5727 (2010).
  • Mimi L, Quan Z, Wang C. Tricyclic pyrido-carboxamide derivatives as rock inhibitors WO 2015002926 A1 (2015).
  • Mishra RK, Alokam R, Singhal SM et al. Design of novel rho kinase inhibitors using energy based pharmacophore modeling, shape-based screening, in silico virtual screening, and biological evaluation. J. Chem. Inf. Model. 54(1), 2876–2886 (2014).
  • Oh KS, Oh BK, Park CH et al. Cardiovascular effects of a novel selective rho kinase inhibitor, 2-(1H-indazole-5-yl)amino-4-methoxy-6-piperazino triazine (DW1865). Eur. J. Pharmacol. 702, 218 (2013).
  • Shahin R, Alqtaishat S, Taha MO. Elaborate ligand-based modeling reveal new submicromolar Rho kinase inhibitors. J. Comput. Aided Mol. Des. 26(2), 249–266 (2012).
  • Feng Y, Lograsso P. Rho kinase inhibitors: a patent review (2012–2013). Expert Opin. Ther. Pat. 24, 295 (2014).
  • Feng Y, Lograsso PV, Defert O, Li R. Rho kinase (ROCK) inhibitors and their therapeutic potential. J. Med. Chem. 59(6), 2269–2300 (2016).
  • Churchill E, Budas G, Vallentin A, Koyanagi T, Mochly-Rosen D. PKC isozymes in chronic cardiac disease: possible therapeutic targets? Annu. Rev. Pharmacol. Toxicol. 48, 569–599 (2008).
  • Koide Y. Differential induction of protein kinase C isoforms at the cardiac hypertrophy stage and congestive heart failure stage in Dahl salt-sensitive rats. Hypertens. Res. 26, 421–426 (2003).
  • Liu Q, Molkentin JD. Protein kinase Cα as a heart failure therapeutic target. J. Mol. Cell. Cardiol. 51, 474–478 (2011).
  • Mochly-Rosen D. Cardiotrophic effects of protein kinase C epsilon: analysis by in vivo modulation of PKC[epsiv] translocation. Circ. Res. 86, 1173–1179 (2000).
  • Ferreira JC. Pharmacological inhibition of βIIPKC is cardioprotective in late-stage hypertrophy. J. Mol. Cell. Cardiol. 51, 980–987 (2011).
  • Ferreira JC, Boer BN, Grinberg M, Brum PC, Mochly-Rosen D. Protein quality control disruption by PKCβII in heart failure; rescue by the selective PKCβII inhibitor, βIIV5–3. PLoS ONE 7, e33175 (2012).
  • Ferreira JC, Brum PC, Mochly-Rosen D. βIIPKC and ∊PKC isozymes as potential pharmacological targets in cardiac hypertrophy and heart failure. J. Mol. Cell. Cardiol. 51, 479–484 (2011).
  • Omura S, Iwai Y, Hirano A et al. A new alkaloid AM-2282 of Streptomyces origin. Taxonomy, fermentation, isolation and preliminary characterization. J. Antiobiot. (Tokyo) 30(4), 275–282 (1977).
  • Radhika P, Kumar MMK, Nagasree KP. Protein kinase inhibitors from microorganisms. In: Studies in Natural Products Chemistry. Rahman AUr ( Ed.). Elsevier, Amsterdam, The Netherlands 403–445 (2015).
  • Koshino H, Osada H, Isono K. A new inhibitor of protein kinase C, RK-1409 (7-oxostaurosporine). II. Fermentation, isolation, physico-chemical properties and structure. J. Antiobiot. (Tokyo) 45(2), 195–198 (1992).
  • Osada H, Koshino H, Kudo T, Onose R, Isono K. A new inhibitor of protein kinase C, RK-1409 (7-oxostaurosporine). I. Taxonomy and biological activity. J. Antiobiot. (Tokyo) 45(2), 189–194 (1992).
  • Kobayashi E, Nakano H, Morimoto M, Tamaoki T. Calphostin C (UCN-1028C), a novel microbial compound, is a highly potent and specific inhibitor of protein kinase C. Biochem. Biophys. Res. Commun. 159(2), 548–553 (1989).
  • Wagner J, Von Matt P, Sedrani R et al. Discovery of 3-(1H-indol-3-yl)-4-[2-(4-methylpiperazin-1-yl)quinazolin-4-yl]pyrrole-2,5-dione (AEB071), a potent and selective inhibitor of protein kinase C isotypes. J. Med. Chem. 52(20), 6193–6196 (2009).
  • Van Eis MJ, Evenou JP, Floersheim P et al. 2,6-Naphthyridines as potent and selective inhibitors of the novel protein kinase C isozymes. Bioorg. Med. Chem. Lett. 21(24), 7367–7372 (2011).
  • Li H, Hong Y, Nukui S et al. Identification of novel pyrrolopyrazoles as protein kinase C beta II inhibitors. Bioorg. Med. Chem. Lett. 21(1), 584–587 (2011).
  • Mochly-Rosen D, Das K, Grimes KV. Protein kinase C, an elusive therapeutic target? Nat. Rev. Drug Discov. 11(12), 937–957 (2012).
  • Packer M. Double-blind, placebo-controlled study of the efficacy of flosequinan in patients with chronic heart failure. Principal Investigators of the REFLECT Study. J. Am. Coll. Cardiol. 22, 65–72 (1993).
  • Ruboxistaurin: LY 333531. Drugs R D 8(3), 193–199 (2007).
  • Poli A, Mongiorgi S, Cocco L, Follo MY. Protein kinase C involvement in cell cycle modulation. Biochem. Soc. Trans. 42(5), 1471 (2014).
  • Li H. Protein kinase C: novel isozyme-selective peptide inhibitors. Exp. Opin. Therap. Pat. 16(8), 1183–1187 (2006).
  • Alam MA, Uddin SJ, Brown L. Mitogen-activated protein kinase and natural phenolic compounds in cardiovascular remodeling. In: Studies in Natural Products Chemistry. Rahman AUr ( Ed.), Elsevier, 159–190 (2012).
  • Goetze S, Xi XP, Kawano Y et al. TNF-alpha-induced migration of vascular smooth muscle cells is MAPK dependent. Hypertension 33(1 Pt 2), 183–189 (1999).
  • Willette RN, Eybye ME, Olzinski AR et al. Differential effects of p38 mitogen-activated protein kinase and cyclooxygenase 2 inhibitors in a model of cardiovascular disease. J. Pharmacol. Exp. Ther. 330(3), 964 (2009).
  • Ren J, Zhang S, Kovacs A, Wang Y, Muslin AJ. Role of p38 alpha MAPK in cardiac apoptosis and remodeling after myocardial infarction. J. Mol. Cell. Cardiol. 38(4), 617–623 (2005).
  • Chen C, Yu R, Owuor ED, Kong AN. Activation of antioxidant-response element (ARE), mitogen-activated protein kinases (MAPKs) and caspases by major green tea polyphenol components during cell survival and death. Arch. Pharm. Res. 23(6), 605–612 (2000).
  • Cuenda A, Rouse J, Doza YN et al. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364(2), 229–233 (1995).
  • Jackson JR, Bolognese B, Hillegass L et al. Pharmacological effects of SB 220025, a selective inhibitor of P38 mitogen-activated protein kinase, in angiogenesis and chronic inflammatory disease models. J. Pharmacol. Exp. Ther. 284(2), 687–692 (1998).
  • Wadsworth SA, Cavender DE, Beers SA et al. RWJ 67657, a potent, orally active inhibitor of p38 mitogen-activated protein kinase. J. Pharmacol. Exp. Ther. 291(2), 680–687 (1998).
  • Clinical Trials Database: NCT00996840 (2015). https://clinicaltrials.gov/ct2/show/NCT00996840
  • Laufer SA, Wagner GK, Kotschenreuther DA, Albrecht W. Novel substituted pyridinyl imidazoles as potent anticytokine agents with low activity against hepatic cytochrome P450 enzymes. J. Med. Chem. 46(15), 3230–3244 (2003).
  • Das J, Moquin RV, Pitt S et al. Pyrazolo-pyrimidines: A novel heterocyclic scaffold for potent and selective p38α inhibitors. Bioorg. Med. Chem. Lett. 18(8), 2652–2657 (2008).
  • Clinical Trials Database: NCT00570752 (2015). https://clinicaltrials.gov/ct2/show/NCT00570752
  • Clinical Trials Database: NCT00399906 (2015). https://clinicaltrials.gov/ct2/show/NCT00399906
  • Collis AJ, Foster ML, Halley F et al. RPR203494 a pyrimidine analogue of the p38 inhibitor RPR200765A with an improved in vitro potency. Bioorg. Med. Chem. Lett. 11(5), 693–696 (2001)
  • Haddad JJ. VX-745. Vertex Pharmaceuticals. Curr. Opin. Investig. Drugs 2(8), 1070–1076 (2001).
  • Sokol L, Cripe L, Kantarjian H et al. Randomized, dose-escalation study of the p38 alpha MAPK inhibitor SCIO-469 in patients with myelodysplastic syndrome. Leukemia 27(4), 977–980 (2013).
  • Skurk C, Maatz H, Rocnik E, Bialik A, Force T, Walsh K. Glycogen-synthase kinase3beta/beta-catenin axis promotes angiogenesis through activation of vascular endothelial growth factor signaling in endothelial cells. Circ. Res. 96(3), 308–318 (2005).
  • Juhaszova M, Zorov DB, Yaniv Y, Nuss HB, Wang S, Sollott SJ. Role of glycogen synthase kinase-3beta in cardioprotection. Circ. Res. 104(11), 1240–1252 (2009).
  • Meijer L, Thunnissen AM, White AW et al. Inhibition of cyclin-dependent kinases, GSK-3beta and CK1 by hymenialdisine, a marine sponge constituent. Chem. Biol. 7(1), 51–63 (2000).
  • Leclerc S, Garnier M, Hoessel R et al. Indirubins inhibit glycogen synthase kinase-3 beta and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer’s disease. A property common to most cyclin-dependent kinase inhibitors? J. Biol. Chem. 276(1), 251–260 (2001).
  • Leost M, Schultz C, Link A et al. Paullones are potent inhibitors of glycogen synthase kinase-3beta and cyclin-dependent kinase 5/p25. Eur. J. Biochem. 267(19), 5983–5994 (2000)
  • Mettey Y, Gompel M, Thomas V et al. Aloisines, a new family of CDK/GSK-3 inhibitors. SAR study, crystal structure in complex with CDK2, enzyme selectivity, and cellular effects. J. Med. Chem. 46(2), 22–236 (2003).
  • Zhang HC, White KB, Ye H et al. Macrocyclic bisindolylmaleimides as inhibitors of protein kinase C and glycogen synthase kinase-3. Bioorg Med. Chem. Lett. 13(18), 3049–3053 (2003).
  • Duan Q, Madan ND, Wu J et al. Role of phosphoinositide 3-kinase IA (PI3K-IA) activation in cardioprotection induced by ouabain preconditioning. J. Mol. Cell. Cardiol. 80, 114–125 (2015).
  • Pretorius L, Du XJ, Woodcock EA et al. Reduced phosphoinositide 3-kinase (p110 alpha) activation increases the susceptibility to atrial fibrillation. Am. J. Pathol. 175(3), 998–1009 (2001).
  • Mcmullen JR, Amirahmadi F, Woodcock EA et al. Protective effects of exercise and phosphoinositide 3-kinase(p110 alpha) signaling in dilated and hypertrophic cardiomyopathy. Proc. Natl Acad. Sci. USA 104(2), 612–617 (2007).
  • Jasiński M, Jasińska L, Ogrodowczyk M. Resveratrol in prostate diseases – a short review. Central European J. Urol. 66(2), 144–149 (2013).
  • Chong E, Chang SL, Hsiao YW et al. Resveratrol, a red wine antioxidant, reduces atrial fibrillation susceptibility in the failing heart by PI3K/AKT/eNOS signaling pathway activation.. Heart Rhythm. 12(5), 1046–1056 (2015).
  • Liu P, Cheng H, Roberts TM, Zhao JJ. Targeting the phosphoinositide 3-kinase (PI3K) pathway in cancer. Nat. Rev. Drug Discov. 8(8), 627–644 (2009).
  • Zhang J, Fan G, Zhao H et al. Targeted inhibition of focal adhesion kinase attenuates cardiac fibrosis and preserves heart function in adverse cardiac remodeling. Sci. Rep. 7, 43146 (2017).
  • Fang Y, Wang D, Xu X et al. Synthesis, biological evaluation, and molecular dynamics (MD) simulation studies of three novel F-18 labeled and focal adhesion kinase (FAK) targeted 5-bromo pyrimidines as radiotracers for tumor. Eur. J. Med. Chem. 127, 493–508 (2017).