An update on natural products with carbonic anhydrase inhibitory activity

Current Pharmaceutical Design

Volumn 22, Issue 12, 2016, Pages 1570-1591

  Karioti, Anastasia ^a   Carta, Fabrizio ^b   Supuran, Claudiu T ^b  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Carbonic anhydrase inhibitors (CAIs); Flavonoids; Metalloenzymes; Natural products; Polyphenols

Indexed keywords

ALKALOID; CARBONATE DEHYDRATASE INHIBITOR; COUMARIN DERIVATIVE; FLAVONOID; NATURAL PRODUCT; POLYAMINE; POLYPHENOL; SULFONAMIDE; TERPENE; BIOLOGICAL PRODUCT; CARBONATE DEHYDRATASE;

CELLULAR DISTRIBUTION; CLINICAL PRACTICE; CONVERGENT EVOLUTION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; HUMAN; IN VITRO STUDY; INHIBITION CONSTANT; NONHUMAN; PHYSICAL CHEMISTRY; PRIMARY TUMOR; PRIORITY JOURNAL; REVIEW; TUMOR GROWTH; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR MODEL; STRUCTURE ACTIVITY RELATION;

ANIMALS; BIOLOGICAL PRODUCTS; CARBONIC ANHYDRASE INHIBITORS; CARBONIC ANHYDRASES; HUMANS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84964300535     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612822666151211094235     Document Type: Review

References (97)

1. Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008; 7: 168-81.
2. Neri D, Supuran CT. Interfering with pH regulation in tumors as a therapeutic strategy. Nat Rev Drug Discov 2011; 10: 767-77.
3. Supuran CT, Scozzafava A, Casini A. Carbonic anhydrase inhibitors. Med Res Rev 2003; 23: 146-89.
4. Ferry JG. The gamma class of carbonic anhydrases. Biochim Biophys Acta 2010; 1804: 374-81.
5. Nishimori I, Onishi S, Takeuchi H, Supuran CT. The alpha and beta classes carbonic anhydrases from Helicobacter pylori as novel drug targets. Curr Pharm Des 2008; 14: 622-30.
6. Krishnamurthy VM, Kaufman GK, Urbach AR, et al. Carbonic anhydrase as a model for biophysical and physical-organic studies of proteins and protein-ligand binding. Chem Rev 2008; 108: 946-1051.
7. Xu Y, Feng L, Jeffrey PD, Shi Y, Morel FM. Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 2008; 452: 56-61.
8. Del Prete S, Vullo D, Fisher GM, et al. Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum--the-carbonic anhydrases. Bioorg Med Chem Lett 2014; 18: 4389-96.
9. Alterio V, Hilvo M, Di Fiore A, et al. Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX. Proc Natl Acad Sci USA 2009; 106: 16233-8.
10. Alterio V, Di Fiore A, D’Ambrosio K, Supuran CT, De Simone G. X-Ray crystallography of CA inhibitors and its importance in drug design. In: Supuran CT, Winum JY. Eds. Drug design of zincenzyme inhibitors: Functional, Structural, and disease applications. Hoboken: Wiley 2009; pp. 73-138.
11. Alterio V, Di Fiore A, D’Ambrosio K, Supuran CT, De Simone G. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev 2012; 8: 4421-68.
12. Carta F, Supuran CT, Scozzafava A. Sulfonamides and their isosters as carbonic anhydrase inhibitors. Future Med Chem 2014; 10: 1149-65.
13. Masini E, Carta F, Scozzafava A, Supuran CT. Antiglaucoma carbonic anhydrase inhibitors: a patent review. Expert Opin Ther Pat 2013; 6: 705-16.
14. Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin Ther Pat 2013; 6: 725-35.
15. Carta F, Supuran CT. Diuretics with carbonic anhydrase inhibitory action: a patent and literature review (2005-2013). Expert Opin Ther Pat 2013; 6: 681-91.
16. Supuran CT, Carta F, Scozzafava A. Metalloenzyme inhibitors for the treatment of Gram-negative bacterial infections: a patent review (2009-2012). Expert Opin Ther Pat 2013; 7: 777-88.
17. Aggarwal M, Kondeti B, McKenna R. Anticonvulsant/antiepileptic carbonic anhydrase inhibitors: a patent review. Expert Opin Ther Pat 2013; 6: 717-24.
18. Supuran CT, Carbonic anhydrase inhibition with natural products: novel chemotypes and inhibition mechanisms. Mol Divers 2011; 15: 305-16.
19. Poulsen S.-A, Davis R.A. Natural products that inhibit carbonic anhydrase. SubCell Biochem 2014; 75: 325-34.
20. Borges F, Roleira F, Milhazes N, Santana L, Uriarte E. Simple Coumarins: Privileged scaffolds in medicinal chemistry. In: Santana L, Uriarte E, Eds. Frontiers in Medicinal Chemistry Bussum, Netherlands: Bentham Science 2009; pp. 23-85.
21. Begum SA, Sahai M, Ray AB. Non-conventional lignans: coumarinolignans, flavonolignans, and stilbenolignans. Fortschr Chem Org Natural 2010; 93: 1-70.
22. Baxter H, Harborne JB, Moss GP. Phytochemical dictionary: A handbook of bioactive compounds from Plants. 2nd ed. London: Taylor and Francis 1998.
23. Assessment report on Citrus bergamia Risso et Poiteau, aetheroleum, EMA/HMPC/56155/2011.
24. Jameel E, Umar T, Kumar J, Hoda N. Coumarin: A privileged scaffold for the design and development of antineurodegenerative Agents. Chem Biol Drug Des 2016; 87(1): 21-38.
25. Lacy A, O’Kennedy R. Studies on coumarins and coumarin-related compounds to determine their therapeutic role in the treatment of cancer. Curr Pharm Des 2004; 10: 3797-811.
26. Maresca A, Temperini C, Vu H, et al. Non-Zinc Mediated Inhibition of Carbonic Anhydrases: Coumarins Are a New Class of Suicide Inhibitors. J Am Chem Soc 2009; 131: 3057-62.
27. Maresca A, Temperini C, Pochet L, Masereel B, Scozzafava A, Supuran CT. Deciphering the mechanism of carbonic anhydrase inhibition with coumarins and thiocoumarins. J Med Chem 2010; 53: 335-44.
28. Maresca A, Supuran CT. Coumarins incorporating hydroxy-and chloro-moieties selectively inhibit the transmembrane, tumorassociated carbonic anhydrase isoforms IX and XII over the cytosolic ones I and II. Bioorg Med Chem Lett 2010; 20: 4511-4.
29. Davis RA, Vullo D, Maresca A, Supuran CT, Poulsen S-A. Natural product coumarins that inhibit human carbonic anhydrases. Bioorg Med Chem 2013; 21: 1539-43.
30. Sharma A, Tiwari M,. Supuran CT. Novel coumarins and benzocoumarins acting as isoform-selective inhibitors against the tumorassociated carbonic anhydrase IX. J Enzyme Inhib Med Chem 2014; 29: 292-6.
31. Morris JC, Chiche J, Grellier C, et al. Targeting hypoxic tumor cell viability with carbohydrate-based carbonic anhydrase IX and XII inhibitors. J Med Chem. 2011; 54: 6905-18.
32. Salmon AJ, Williams ML, Maresca A, Supuran CT, Poulsen SA. Synthesis of glycoconjugate carbonic anhydrase inhibitors by ruthenium-catalysed azide-alkyne 1,3-dipolar cycloaddition. Bioorg Med Chem Lett 2011; 21: 6058-61.
33. Winum JY, Colinas PA, Supuran CT. Glycosidic carbonic anhydrase IX inhibitors: A sweet approach against cancer. Bioorg Med Chem 2013; 21: 1419-26.
34. Touisni N, Maresca A, McDonald PC, et al. Glycosyl coumarin carbonic anhydrase IX and XII inhibitors strongly attenuate the growth of primary breast tumors. J Med Chem 2011; 54: 8271-7.
35. Quideau S, Deffieux D, Douat-Casassus C, Pouységu L. Plant polyphenols: chemical properties, biological activities, and synthesis. Angew Chem Int Ed 2011; 50: 586-621.
36. Gülçin I. Antioxidant activity of food constituents: an overview. Arch Toxicol 2012; 86: 345-91.
37. López-Malo Vigil A, Palou E, Alzamora SM. Naturally Occurring Compounds In: Davidson PM, John N. Sofos JN, A. L. Branen AL Eds. Plant Sources in Antimicrobials in food. 3rd Ed. Boca Raton: CRC Press Taylor & Francis Group 2005; pp. 429-51.
38. Issaa AY, Volatea SR, Wargovich MJ. The role of phytochemicals in inhibition of cancer and inflammation: New directions and perspectives. J Food Compos Anal 2006; 19: 405-19.
39. Kelsey NA, Wilkins HM, Linseman DA. Nutraceutical antioxidants as novel neuroprotective agents. Molecules 2010; 15: 7792-814.
40. Simonsson I, Jonsson B H, Lindskog S. Phenol, a competitive inhibitor of CO2 hydration catalyzed by carbonic anhydrase. Biochem Biophys Res Commun 1982; 108: 1406-12.
41. Tibell L, Forsman C, Simonsson I, Lindskog S. The inhibition of human carbonic anhydrase II by some organic compounds. Biochim Biophys Acta 198; 829: 202-8.
42. Sahin H, Can Z, Yildiz O, Kolayli S, Innocenti A, Scozzafava G, Supuran CT. Inhibition of carbonic anhydrase isozymes and II with natural products extracted from plants, mushrooms and honey. J Enzyme Inhib Med Chem 2012; 27: 395-402.
43. Scozzafava A, Passaponti M, Supuran C T, Gülçin . Carbonic anhydrase inhibitors: guaiacol and catechol derivatives effectively inhibit certain human carbonic anhydrase isoenzymes (hCA I, II, IX and XII). J Enzyme Inhib Med Chem 2015; 30: 586-91.
44. Riafrecha LE, Rodriguez OM, Vullo D, Supuran CT, Colinas PA. Synthesis of C-cinnamoyl glycosides and their inhibitory activity against mammalian carbonic anhydrases. Bioorg Med Chem 2013: 21: 1489-94.
45. Carreyre H, Coustard JM, Carré G, et al. Natural product hybrid and its superacid synthesized analogues: Dodoneine and its derivatives show selective inhibition of carbonic anhydrase isoforms I, III, XIII and XIV. Bioorg Med Chem 2013; 21: 3790-4.
46. Carré G, Ouédraogo M, Magaud C, et al. Vasorelaxation induced by dodoneine is mediated by calcium channels blockade and carbonic anhydrase inhibition on vascular smooth muscle cells. J Ethnopharmacol 2015; 169: 8-17.
47. Topal M, Gülçin I. Rosmarinic acid: a potent carbonic anhydrase isoenzymes inhibitor. Turk J Chem 2014; 38: 894-902.
48. Petersen M, Simmonds MS. Rosmarinic acid. Phytochemistry 2003; 62: 121-5.
49. Wang M, Karioti A, Bergonzi MC, et al. International Symposium. Traditional Chinese Medicine, Modernization of Acupuncture and Herbal Medicine Research, May 14-16, Graz, Austria 2009.
50. Karioti A, Ceruso M, Carta F, Bilia AR, Supuran CT. New natural product carbonic anhydrase inhibitors incorporating phenol moieties. Bioorg Med Chem 2015; 23(22): 7219-25.
51. Bonaccini L, Karioti A, Bergonzi MC, Bilia AR. Effects of Salvia miltiorrhiza on cns neuronal injury and degeneration: a plausible complementary role of tanshinones and depsides. Planta Med 2015; 81: 1003-16.
52. Ho JHC, Hong CY. Salvianolic acids: small compounds with multiple mechanisms for cardiovascular protection. J Biomed Sci 2011; 18: 1-5.
53. Wu WY, Wang YP. Pharmacological actions and therapeutic applications of Salvia miltiorrhiza depside salt and its active components. Acta Pharmacol Sin 2012; 33: 1119-30.
54. Khalifah RG. The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J Biol Chem 1971; 246: 2561-73.
55. Maresca A, Akyuz G, Osman SM, AlOthman Z, Supuran CT. Inhibition of mammalian carbonic anhydrase isoforms I-XIV with a series of phenolic acid esters. Bioorg Med Chem 2015; 23(22): 7181-8.
56. Andersen ØM, Markham KR. Flavonoids-chemistry, biochemistry and applications. Boca Raton: CRC/Taylor & Francis 2006.
57. Falcone Ferreyra ML, Rius SP, Casati P. Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci 2012; 3: article ID: 222.
58. Lin JK, Weng MS. Flavonoids as nutraceuticals. In: Grotewold, E. Ed. The Science of Flavonoids. New York: Springer 2006; pp. 213-238.
59. Harborne JB, Williams CA. Advances in flavonoid research since 1992. Phytochemistry 2000: 55: 481-504.
60. Balboni G, Congiu C, Onnis V, et al. Flavones and structurally related 4-chromenones inhibit carbonic anhydrases by a different mechanism of action compared to coumarins. Bioorg Med Chem Lett 2012; 22: 3063-66.
61. Ekinci D, Karagoz L, Ekinci D, Senturk M, Supuran CT. Carbonic anhydrase inhibitors: in vitro inhibition of α isoforms (hCA I, hCA II, bCA III, hCA IV) by flavonoids. J Enzyme Inhib Med Chem 2013; 28: 283-8.
62. Sentürk M, Gülçin I, Beydemir S, Küfrevioglu OI, Supuran CT. In vitro inhibition of human carbonic anhydrase I and II isozymes with natural phenolic compounds. Chem Biol Drug Des 2011; 77: 494-9.
63. Koz Ö, Ekinci D, Perrone A, et al. Analysis of saponins and phenolic compounds as inhibitors of α-carbonic anhydrase isoenzymes J Enzyme Inhib Med Chem 2013; 28: 412-7.
64. Innocenti A, Beyza Oztork Sarikaya S, Gülçin I, Supuran CT. Carbonic anhydrase inhibitors. Inhibition of mammalian isoforms I-XIV with a series of natural product polyphenols and phenolic acids. Bioorg Med Chem 2010; 18: 2159-64.
65. Gidaro MC, Alcaro F, Carradori S, et al. Eriocitrin and apigenin as new carbonic anhydrase VA inhibitors from a virtual screening of calabrian natural products. Planta Med 2015; 81: 533-40.
66. Rahman TU, Khatta KF, Liaqa W, Zama K, Musharra SG. Characterization of one novel flavone and four new source compounds from the bark of millettia ovalifolia and in-vitro inhibition of carbonic anhydrase-II by the novel flavonoid. Rec Nat Prod 2015; 9: 553-60.
67. Karioti A, Bilia AR, Skaltsa H. Quercus ilex: A rich source of polyacylated flavonoid glucosides. Food Chem 2010; 123: 131-42.
68. Miroddi, M, Calapai G, Navarra M, Minciullo PL, Gangemi S. Passiflora incarnata L.: ethnopharmacology, clinical application, safety and evaluation of clinical trials. J Ethnopharmacol 2013; 150: 791-804.
69. Huang H, Chen AY, Rojanasakul Y, Ye X, Rankin GO, Chen YC. Dietary compounds galangin and myricetin suppress ovarian cancer cell angiogenesis. J Funct Foods 2015; 15: 464-75.
70. González-Gallego J, García-Mediavilla MV, Sánchez-Campos S, Tuñón MJ. Fruit polyphenols, immunity and inflammation. Br J Nutr 2010; 104: S15-27.
71. Kamran KM, Huma ZE, Dangles O. A comprehensive review on flavanones, the major citrus polyphenols. J Food Compost Anal 2014; 33: 85-104.
72. Taku K, Melby MK, Nishi N, Omori T, Kurzer MS. Soy isoflavones for osteoporosis: An evidence-based approach. Maturitas 2011; 70: 333-8.
73. Vitale DC, Piazza C, Melilli B, Drago F, Salomone S. Isoflavones: estrogenic activity, biological effect and bioavailability. Eur J Drug Metab Pharmacokinet 2013; 38: 15-25.
74. Zhou YX, Zhang H, Peng H. Puerarin: A review of pharmacological effects. Phytother Res 2014; 28: 961-75.
75. Kaur-Sawhney R, Tiburcio AF, Altabella T, Galston AW. Polyamines in plants: An overview. J Cell Mol Biol 2003; 2: 1-12.
76. Clare BW, Supuran CT. Carbonic anhydrase activators. Part 3. Structure-activity correlations for a series of isozyme II activators. J Pharm Sci 1994; 83: 768-79.
77. Temperini C, Vullo D, Scozzafava A, Supuran CT. Carbonic anhydrase activators. Activation of isoforms I, II, IV, VA, VII, and XIV with L-and D-phenylalanine and crystallographic analysis of their adducts with isozyme II: sterospecific recognition within the active site of an enzyme and its consequences for the drug design. J Med Chem 2006; 49: 3019-27.
78. Supuran CT, Scozzafava A. Activation of carbonic anhydrase isozymes. In: Chegwidden WR, Carter N, Edwards Y, Eds. The Carbonic Anhydrases-New Horizons. Basel: Birkhauser Verlag 2000; pp 197-219.
79. Ilies M, Scozzafava A, Supuran CT. Carbonic anhydrase activators. In: Supuran, CT, Scozzafava A, Conway J, Eds. Carbonic anhydrase; Its Inhibitors and Activators. Boca Raton: CRC Press 2004; pp. 317-52.
80. Scozzafava A, Supuran CT. Carbonic anhydrase activators: high affinity isozymes I, II, and IV activators, incorporating a β-alanylhistidine scaffold. Carbonic anhydrase activators: human isozyme II is strongly activated by oligopeptides incorporating the carboxyterminal sequence of the bicarbonate anion exchanger AE1. J Med Chem 2002; 45: 284-91.
81. Ilies M, Banciu MD, Ilies MA, Scozzafava A, Caproiu MT, Supuran CT. Carbonic anhydrase activators: design of high affinity isozymes I, II, and IV activators, incorporating tri-/tetrasubstitutedpyridinium-azole moieties. J Med Chem 2002; 45: 504-10.
82. Carta F, Temperini C, Innocenti A, Scozzafava A, Kaila K, Supuran CT. Polyamines inhibit carbonic anhydrases by anchoring to the zinc-coordinated water molecule. J Med Chem 2010; 53: 5511-22.
83. Arabaci B, I. Gulcin, S. Alwasel. Capsaicin: a potent inhibitor of carbonic anhydrase isoenzymes. Molecules 2014; 19: 10103-14.
84. EMA assessment report. Assessment report on Capsicum annuum L. var. minimum (Miller) Heiser and small fruited varieties of Capsicum frutescens L., fructus. EMA/HMPC/674138/2013].
85. Kumar Sharma S, Vij AS, Sharma M. Mechanisms and clinical uses of capsaicin. Eur J Pharmacol 2013; 720: 55-62.
86. Sethi KK, Sahoo SK, Pichikala JN, Suresh P. Carbonic anhydrase I and II inhibition with natural products: Caffeine and piperine. J Enzyme Inhib Med Chem 2012; 27: 97-100.
87. Thulasiram HV, Erickson HK, Poulter CD. Chimeras of two isoprenoid synthases catalyze all four coupling reactions in isoprenoid biosynthesis. Science 2007: 316: 73-6.
88. Croteau R, Kutchan TM, Lewis NG. Natural Products (Secondary Metabolites). In: Buchanan B, Gruissem W, Jones R, Eds. Biochemistry & Molecular Biology of Plants. West Sussex UK: John Wiley & Sons 2000; pp. 1250-317.
89. Durdagi S, Scozzafava G, Vullo D, Sahin H, Kolayli S, Supuran CT. Inhibition of mammalian carbonic anhydrases I-XIV with grayanotoxin III: Solution and in silico studies. J Enzyme Inhib Med Chem 2014; 29: 469-75.
90. Radix Astragali. WHO Monographs on Selected Medicinal Plants. Vol.1, Geneva 1999.
91. Ionkova I, Shkondrov A, Krasteva I, Ionkov T. Recent progress in phytochemistry, pharmacology and biotechnology of Astragalus saponins. Phytochem Rev 2014; 13: 343-74.
92. Innocenti A, Vullo D, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors: inhibition of mammalian isoforms I-XIV. with a series of substituted phenols including paracetamol and salicylic acid. Bioorg Med Chem 2008; 16: 7424-8.
93. Schwarz S, Sommerwerk S, Lucas SD, Heller L, Csu R. Sulfamates of methyl triterpenoates are effective and competitive inhibitors of carbonic anhydrase II. Eur J Med Chem 2014; 86: 95-102.
94. Jiménez C, Crews P. Novel marine sponge derived amino acids 13. Additional psammaplin derivatives from Psammaplysilla purpurea. Tetrahedron 1991; 47: 2097-102.
95. Mujumdar P, Poulsen SA. Natural product primary sulfonamides and primary sulfamates. J Nat Prod 2015; 78: 1470-7.
96. Mujumdar P, Vullo D, Supuran CT, Peat TS, Poulsen SA. An unusual natural product primary sulfonamide: Synthesis, carbonic anhydrase inhibition and protein X-ray structure of psammaplin C J. Med. Chem. Submitted.
97. Kottakota SK, Benton M, Evangelopoulos D, et al. Versatile routes to marine sponge metabolites through benzylidene rhodanines. Org Lett 2012; 14: 6310-3.