Exploring Natural Product Derivatives having Carbonic Anhydrase Inhibitory Activity

Jump To References Section

Authors

  • Department of Pharmaceutical Chemistry, SRM College of Pharmacy, SRMIST, Kattankulanthur - 603203, Tamil Nadu ,IN
  • Department of Pharmaceutical Chemistry, SRM College of Pharmacy, SRMIST, Kattankulanthur - 603203, Tamil Nadu ,IN
  • Department of Pharmaceutical Chemistry, SRM College of Pharmacy, SRMIST, Kattankulanthur - 603203, Tamil Nadu ,IN
  • MVM College of Pharmacy, Bengaluru - 560064, Karnataka ,IN
  • Faculty of Pharmacy, VNS Group of Institutions, Bhopal - 462044, Madhya Pradesh ,IN
  • Dr APJ Abdul Kalam Research Laboratory, Department of Pharmaceutical Chemistry, SRM College of Pharmacy, SRMIST, Kattankulathur - 603203, Tamil Nadu ,IN

DOI:

https://doi.org/10.18311/jnr/2024/36071

Keywords:

Cancer, Carbonic Anhydrase, Natural Product Derivatives, Selective Inhibition

Abstract

Carbonic anhydrase is an enzyme which plays an active role in many biological functions of the human body. It is omnipresent in all the biological organisms with eight different genetic families. Its primary role is to catalyze the reversible hydration of CO2 to bicarbonate and protons. Though it is beneficial in many aspects it is also equally important for the cancer cells because of its pH regulatory nature. For tumor cells to survive and metastasis the regulation of pH and creating a hypoxia condition is very much needed, as Carbonic anhydrase is an extended family of sixteen isozymes, some of them are very essential for tumor cells. Many research is going on to inhibit the selective enzyme which is over expressed in the tumor cells. To be exact Carbonic anhydrase IX and XII are the most important enzymes overexpressed in the tumor cells. Sulfonamides, along with their bioisosters sulfonamides and sulfamates, have been employed for decades in treating conditions like glaucoma, epilepsy, and diuretics. Notably, this class of compounds has been extensively studied for its role as carbonic anhydrase inhibitors, showcasing their significant use and exploration in various therapeutic applications. In recent years, there has been a notable shift in the study of Carbonic anhydrase inhibitors  towards natural products in addition to synthetic derivatives. Traditional drug design methods have historically yielded synthetic CAIs, but the exploration of Natural products derivatives has significantly advanced the field. Natural products, such as psammaplin C and altemicidin, containing primary sulfonamide or sulfamate groups, are gaining attention. The chemical diversity, binding specificity, and interaction tendencies of natural product derivatives make them appealing for molecular probes in research.  

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Downloads

Published

2024-05-28

How to Cite

Packiapalavesam, S. D., Saravanan, V., Ramesh, P., Devarajan, A., Mohan Maruga Raja, M. K., & Kathiravan, M. K. (2024). Exploring Natural Product Derivatives having Carbonic Anhydrase Inhibitory Activity. Journal of Natural Remedies, 24(5), 953–971. https://doi.org/10.18311/jnr/2024/36071

Issue

Section

Review Articles

Categories

Received 2024-01-03
Accepted 2024-02-23
Published 2024-05-28

 

References

Jensen EL, Clement R, Kosta A, Maberly SC, Gontero B. A new widespread subclass of carbonic anhydrase in marine phytoplankton. ISME J. 2019; 13:2094–106. https://doi.org/10.1038/s41396-019-0426-8

Capasso C, Supuran CT. An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria : can bacterial carbonic anhydrases shed new light on the evolution of bacteria? J Enzyme Inhib Med Chem. 2015; 30:325–32. https://doi.org/10.3109/14756366.2014.910202

Del Prete S, Vullo D, De Luca V, Carginale V, Ferraroni M, Osman SM, et al. Sulfonamide inhibition studies of the β-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae. Bioorg Med Chem. 2016; 24:1115–20. https://doi.org/10.1016/j.bmc.2016.01.037

Syrjänen L, Tolvanen M, Hilvo M, Olatubosun A, Innocenti A, Scozzafava A, et al. Characterization of the first beta-class carbonic anhydrase from an arthropod (Drosophila melanogaster) and phylogenetic analysis of beta-class carbonic anhydrases in invertebrates. BMC Biochem. 2010; 11:28. https://doi.org/10.1186/1471-2091-11-28

Ferry JG. The γ class of carbonic anhydrases. Biochim Biophys Acta - Proteins Proteomics. 2010; 1804:374–81. https://doi.org/10.1016/j.bbapap.2009.08.026

Del Prete S, De Luca V, De Simone G, Supuran CT, Capasso C. Cloning, expression and purification of the complete domain of the η -carbonic anhydrase from Plasmodium falciparum. J Enzyme Inhib Med Chem. 2016; 31:54–9. https://doi.org/10.1080/14756366.2016.1217856

Del Prete S, Nocentini A, Supuran CT, Capasso C. Bacterial ι-carbonic anhydrase: a new active class of carbonic anhydrase identified in the genome of the Gram-negative bacterium Burkholderia territorii. J Enzyme Inhib Med Chem. 2020; 35:1060–8. https://doi.org/10.1080/14756366.2020.1755852

Aspatwar A, Tolvanen MEE, Barker H, Syrjänen L, Valanne S, Purmonen S, et al. Carbonic anhydrases in metazoan model organisms: molecules, mechanisms, and physiology. Physiol Rev. 2022; 102:1327–83. https://doi.org/10.1152/physrev.00018.2021

Frost SC. Physiological functions of the alpha class of carbonic anhydrases. 2014; 9–30. https://doi.org/10.1007/978-94-007-7359-2_2

Eldehna WM, Taghour MS, Al-Warhi T, Nocentini A, Elbadawi MM, Mahdy HA, et al. Discovery of 2,4-thiazolidinedione-tethered coumarins as novel selective inhibitors for carbonic anhydrase IX and XII isoforms. J Enzyme Inhib Med Chem. 2022; 37:531–41. https://doi.org/10.1080/14756366.2021.2024528

Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov. 2008; 7:168–81. https://doi.org/10.1038/nrd2467

Thiry A, Dogné J-M, Masereel B, Supuran CT. Targeting tumor-associated carbonic anhydrase IX in cancer therapy. Trends Pharmacol Sci. 2006; 27:566–73. https://doi.org/10.1016/j.tips.2006.09.002

Duda DM, Tu C, Fisher SZ, An H, Yoshioka C, Govindasamy L, et al. Human carbonic anhydrase III: structural and kinetic study of catalysis and proton transfer. Biochemistry. 2005; 44:10046–53. https://doi.org/10.1021/bi050610h

Lindskog S, Silverman DN. The catalytic mechanism of mammalian carbonic anhydrases. Carbon. Anhydrases, Basel: Birkhäuser Basel. 2000; 175–95. https://doi.org/10.1007/978-3-0348-8446-4_10

Maren TH. Carbonic anhydrase: chemistry, physiology, and inhibition. Physiol Rev. 1967; 47:595–781. https://doi.org/10.1152/physrev.1967.47.4.595

Supuran CT, Vullo D, Manole G, Casini A, Scozzafava A. Designing of novel carbonic anhydrase inhibitors and activators. Curr Med Chem Cardiovasc Hematol Agents. 2004; 2:49–68. https://doi.org/10.2174/1568016043477305

Supuran CT, Conroy CW, Maren TH. Is cyanate a carbonic anhydrase substrate? Proteins Struct Funct Genet. 1997; 27:272–8. https://doi.org/10.1002/(SICI)1097-0134(199702)27:2<272::AID-PROT12>3.0.CO;2-J

Guerri A, Briganti F, Scozzafava A, Supuran CT, Mangani S. Mechanism of cyanamide hydration catalyzed by carbonic anhydrase II suggested by cryogenic X-ray diffraction. Biochemistry. 2000; 39:12391–7. https://doi.org/10.1021/bi000937c

Tanc M, Carta F, Scozzafava A, Supuran CT. α-Carbonic anhydrases possess thioesterase activity. ACS Med Chem Lett. 2015; 6:292–5. https://doi.org/10.1021/ml500470b

Clare BW, Supuran CT. A perspective on quantitative structure-activity relationships and carbonic anhydrase inhibitors. Expert Opin Drug Metab Toxicol. 2006; 2:113–37. https://doi.org/10.1517/17425255.2.1.113

Hewett-Emmett D. Evolution and distribution of the carbonic anhydrase gene families. Carbon. Anhydrases, Basel: Birkhäuser Basel. 2000; 29–76. https://doi.org/10.1007/978-3-0348-8446-4_3

Supuran CT. Carbonic anhydrase inhibitors and their potential in a range of therapeutic areas. Expert Opin Ther Pat. 2018; 28:709–12. https://doi.org/10.1080/13543776.2018.1523897

Carta F, Supuran CT. Diuretics with carbonic anhydrase inhibitory action: a patent and literature review (2005 – 2013). Expert Opin Ther Pat. 2013; 23:681–91. https://doi.org/10.1517/13543776.2013.780598

Mincione F, Nocentini A, Supuran CT. Advances in the discovery of novel agents for the treatment of glaucoma. Expert Opin Drug Discov. 2021; 16:1209–25. https://doi.org/10.1080/17460441.2021.1922384

Supuran CT, Scozzafava A, Casini A. Carbonic anhydrase inhibitors. Med Res Rev. 2003; 23:146–89. https://doi.org/10.1002/med.10025

Aggarwal M, Kondeti B, McKenna R. Anticonvulsant/antiepileptic carbonic anhydrase inhibitors: a patent review. Expert Opin Ther Pat. 2013; 23:717–24. https://doi.org/10.1517/13543776.2013.782394

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; 112:4421–68. https://doi.org/10.1021/cr200176r

Canto de Souza L, Provensi G, Vullo D, Carta F, Scozzafava A, Costa A, et al. Carbonic anhydrase activation enhances object recognition memory in mice through phosphorylation of the extracellular signal-regulated kinase in the cortex and the hippocampus. Neuropharmacology. 2017; 118:148–56. https://doi.org/ 10.1016/j.neuropharm.2017.03.009

Blandina P, Provensi G, Passani MB, Capasso C, Supuran CT. Carbonic anhydrase modulation of emotional memory. Implications for the treatment of cognitive disorders. J Enzyme Inhib Med Chem. 2020; 35:1206–14. https://doi.org/10.1080/14756366.2020.1766455

Supuran CT. Carbonic anhydrase activators. Future Med Chem. 2018; 10:561–73. https://doi.org/10.4155/fmc-2017-0223

Supuran CT. Coumarin carbonic anhydrase inhibitors from natural sources. J Enzyme Inhib Med Chem. 2020; 35:1462–70. https://doi.org/10.1080/14756366.2020.1788009

Parkkila S, Kaunisto K, Rajaniemi L, Kumpulainen T, Jokinen K, Rajaniemi H. Immunohistochemical localization of carbonic anhydrase isoenzymes VI, II, and I in human parotid and submandibular glands. J Histochem Cytochem. 1990; 38:941–7. https://doi.org/ 10.1177/38.7.2113069

Aggarwal M, Boone CD, Kondeti B, McKenna R. Structural annotation of human carbonic anhydrases. J Enzyme Inhib Med Chem. 2013; 28:267–77. https://doi.org/10.3109/14756366.2012.737323

Sterling D, Reithmeier RAF, Casey JR. A Transport Metabolon. J Biol Chem. 2001; 276:47886–94. https://doi.org/10.1074/jbc.M105959200

Mitterberger MC, Kim G, Rostek U, Levine RL, Zwerschke W. Carbonic anhydrase III regulates peroxisome proliferator-activated receptor-γ2. Exp Cell Res. 2012; 318:877–86. https://doi.org/10.1016/j.yexcr.2012.02.011

Zimmerman UP, Wang P, Zhang X, Bogdanovich S, Forster RE. Anti‐oxidative response of carbonic anhydrase III in skeletal muscle. IUBMB Life. 2004; 56:343–7. https://doi.org/10.1080/1521-6540400000850

Parkkila S, Parkkila A, Juvonen T, Waheed A, Sly WS, Saarnio J, et al. Membrane-bound carbonic anhydrase IV is expressed in the luminal plasma membrane of the human gallbladder epithelium. Hepatology. 1996; 24:1104–8. https://doi.org/10.1002/hep.510240521

Baird, TT, Waheed A, Okuyama T, Sly WS, Fierke CA. Catalysis and inhibition of human carbonic anhydrase IV. Biochemistry. 1997; 36:2669–78. https://doi.org/10.1021/bi962663s

Idrees D, Shahbaaz M, Bisetty K, Islam A, Ahmad F, Hassan MI. Effect of pH on structure, function, and stability of mitochondrial carbonic anhydrase VA. J Biomol Struct Dyn. 2017; 35:449–61. https://doi.org/10.1080/07391102.2016.1149097

Arechederra RL, Waheed A, Sly WS, Supuran CT, Minteer SD. Effect of sulfonamides as carbonic anhydrase VA and VB inhibitors on mitochondrial metabolic energy conversion. Bioorg Med Chem. 2013; 21:1544–8. https://doi.org/10.1016/j.bmc.2012.06.053

Thatcher BJ, Doherty AE, Orvisky E, Martin BM, Henkin RI. Gustin from human parotid saliva is carbonic anhydrase VI. Biochem Biophys Res Commun. 1998; 250:635–41. https://doi.org/10.1006/bbrc.1998.9356

Henkin RI, Martin BM, Agarwal RP. Decreased parotid saliva Gustin/carbonic anhydrase VI secretion: an enzyme disorder manifested by gustatory and olfactory dysfunction. Am J Med Sci. 1999; 318:380. https://doi.org/10.1097/00000441-199912000-00005

Henkin RI, Martin BM, Agarwal RP. Efficacy of exogenous oral zinc in the treatment of patients with carbonic anhydrase VI deficiency. Am J Med Sci. 1999; 318:392. https://doi.org/10.1097/00000441-199912000-00006

Bootorabi F, Jänis J, Smith E, Waheed A, Kukkurainen S, Hytönen V, et al. Analysis of a shortened form of human carbonic anhydrase VII expressed in vitro compared to the full-length enzyme. Biochimie. 2010; 92:1072–80. https://doi.org/10.1016/j.biochi.2010.05.008

Ruusuvuori E, Huebner AK, Kirilkin I, Yukin AY, Blaesse P, Helmy M, et al. Neuronal carbonic anhydrase VII provides GABAergic excitatory drive to exacerbate febrile seizures. EMBO J. 2013; 32:2275–86. https://doi.org/10.1038/emboj.2013.160

Aspatwar A, E.E. Tolvanen M, Ortutay C, Parkkila S. Carbonic anhydrase-related protein VIII and its role in neurodegeneration and cancer. Curr Pharm Des. 2010; 16:3264–76. https://doi.org/10.2174/138161210793429823

Nocentini A, Supuran CT. Carbonic anhydrase inhibitors as antitumor/antimetastatic agents: a patent review (2008–2018). Expert Opin Ther Pat. 2018; 28:729–40. https://doi.org/10.1080/13543776.2018.1508453

Neri D, Supuran CT. Interfering with pH regulation in tumors as a therapeutic strategy. Nat Rev Drug Discov. 2011; 10:767–77. https://doi.org/10.1038/nrd3554

Queen A, Bhutto HN, Yousuf M, Syed MA, Hassan MI. Carbonic anhydrase IX: A tumor acidification switch in heterogeneity and chemokine regulation. Semin Cancer Biol. 2022; 86:899–913. https://doi.org/10.1016/j.semcancer.2022.01.001

Tam SY, Wu VWC, Law HKW. Hypoxia-induced epithelial-mesenchymal transition in cancers: HIF-1α and beyond. Front Oncol. 2020; 10. https://doi.org/10.3389/fonc.2020.00486

Lee S-H, Griffiths JR. How and why are cancers acidic? Carbonic anhydrase IX and the homeostatic control of tumor extracellular pH. Cancers (Basel). 2020; 12:1616. https://doi.org/10.3390/cancers12061616

Guler O, Simone G, Supuran C. Drug design studies of the novel antitumor targets carbonic anhydrase IX and XII. Curr Med Chem. 2010; 17:1516–26. https://doi.org/10.2174/092986710790979999

Dorai T, Sawczuk IS, Pastorek J, Wiernik PH, Dutcher JP. The role of carbonic anhydrase IX overexpression in kidney cancer. Eur J Cancer. 2005; 41:2935–47. https://doi.org/10.1016/j.ejca.2005.09.011

De Simone G, Supuran CT. Carbonic anhydrase IX: Biochemical and crystallographic characterization of a novel antitumor target. Biochim Biophys Acta - Proteins Proteomics. 2010; 1804:404–9. https://doi.org/10.1016/j.bbapap.2009.07.027

Saravanan V, Chagaleti BK, Packiapalavesam SD, Kathiravan M. Ligand-based pharmacophore modeling and integrated computational approaches in the quest for small molecule inhibitors against hCA IX. RSC Adv. 2024; 14(5):3346-58. https://doi.org/10.1039/D3RA08618F

Robertson N, Potter C, Harris AL. Role of carbonic anhydrase IX in human tumor cell growth, survival, and invasion. Cancer Res. 2004; 64:6160–5. https://doi.org/10.1158/0008-5472.CAN-03-2224

Barnett DH, Sheng S, Howe Charn T, Waheed A, Sly WS, Lin C-Y, et al. Estrogen receptor regulation of carbonic anhydrase XII through a distal enhancer in breast cancer. Cancer Res. 2008; 68:3505–15. https://doi.org/10.1158/0008-5472.CAN-07-6151

Tonissen KF, Poulsen S-A. Carbonic anhydrase XII inhibition overcomes P-glycoprotein-mediated drug resistance: a potential new combination therapy in cancer. Cancer Drug Resist. 2021. https://doi.org/10.20517/cdr.2020.110

Salaroglio IC, Mujumdar P, Annovazzi L, Kopecka J, Mellai M, Schiffer D, et al. Carbonic anhydrase XII inhibitors overcome p–glycoprotein–mediated resistance to temozolomide in glioblastoma. Mol Cancer Ther. 2018; 17:2598–609. https://doi.org/10.1158/1535-7163.MCT-18-0533

Supuran CT. Carbonic anhydrases: from biomedical applications of the inhibitors and activators to biotechnological use for CO2 capture. J Enzyme Inhib Med Chem. 2013; 28:229–30. https://doi.org/10.3109/14756366.2013.761876

Keilin D, Mann T. Carbonic anhydrase. Nature. 1939; 144:442–3. https://doi.org/10.1038/144442b0

Lane TW, Saito MA, George GN, Pickering IJ, Prince RC, Morel FMM. A cadmium enzyme from a marine diatom. Nature. 2005; 435:42–42. https://doi.org/10.1038/435042a

Hirakawa Y, Senda M, Fukuda K, Yu HY, Ishida M, Taira M, et al. Characterization of a novel type of carbonic anhydrase that acts without metal cofactors. BMC Biol. 2021; 19:105. https://doi.org/10.1186/s12915-021-01039-8

Stams T, Christianson DW. X-ray crystallographic studies of mammalian carbonic anhydrase isozymes. Carbon. Anhydrases, Basel: Birkhäuser Basel. 2000; 159–74. https://doi.org/10.1007/978-3-0348-8446-4_9

Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2012; 27:759–72. https://doi.org/10.3109/14756366.2012.672983

Nocentini A, Supuran CT. Advances in the structural annotation of human carbonic anhydrases and impact on future drug discovery. Expert Opin Drug Discov. 2019; 14:1175–97. https://doi.org/10.1080/17460441.2019.1651289

Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov. 2017; 12:61–88. https://doi.org/10.1080/17460441.2017.1253677

Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem. 2016; 31:345–60. https://doi.org/10.3109/14756366.2015.1122001

Supuran CT. Exploring the multiple binding modes of inhibitors to carbonic anhydrases for novel drug discovery. Expert Opin Drug Discov. 2020; 15:671–86. https://doi.org/10.1080/17460441.2020.1743676

Innocenti A, Vullo D, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors: Interactions of phenols with the 12 catalytically active mammalian isoforms (CA I–XIV). Bioorg Med Chem Lett. 2008; 18:1583–7. https://doi.org/10.1016/j.bmcl.2008.01.077

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. https://doi.org/10.1016/j.bmc.2008.06.013

Maresca A, Supuran CT. Coumarins incorporating hydroxy- and chloro-moieties selectively inhibit the transmembrane, tumor-associated carbonic anhydrase isoforms IX and XII over the cytosolic ones I and II. Bioorg Med Chem Lett. 2010; 20:4511–4. https://doi.org/10.1016/j.bmcl.2010.06.040

Sharma A, Tiwari M, Supuran CT. Novel coumarins and benzocoumarins act as isoform-selective inhibitors against the tumor-associated carbonic anhydrase IX. J Enzyme Inhib Med Chem. 2014; 29:292–6. https://doi.org/10.3109/14756366.2013.777334

D'Ambrosio K, Carradori S, Monti SM, Buonanno M, Secci D, Vullo D, et al. Out of the active site binding pocket for carbonic anhydrase inhibitors. Chem Commun. 2015; 51:302–5. https://doi.org/10.1039/C4CC07320G

Galati S, Yonchev D, Rodríguez-Pérez R, Vogt M, Tuccinardi T, Bajorath J. Predicting isoform-selective carbonic anhydrase inhibitors via machine learning and rationalizing structural features important for selectivity. ACS Omega. 2021; 6:4080–9. https://doi.org/10.1021/acsomega.0c06153

Supuran CT. Structure and function of carbonic anhydrases. Biochem J. 2016; 473:2023–32. https://doi.org/10.1042/BCJ20160115

Cuffaro D, Nuti E, Rossello A. An overview of carbohydrate-based carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2020; 35:1906–22. https://doi.org/10.1080/14756366.2020.1825409

Smith DA, Jones RM. The sulfonamide group as a structural alert: A distorted story? Curr Opin Drug Discov Devel. 2008; 11:72–9.

Peerzada MN, Vullo D, Paoletti N, Bonardi A, Gratteri P, Supuran CT, et al. Discovery of novel hydroxylamine-tethered benzenesulfonamides as potential human carbonic anhydrase IX/XII inhibitors. ACS Med Chem Lett. 2023; 14:810–9. https://doi.org/10.1021/acsmedchemlett.3c00094

McDonald PC, Chia S, Bedard PL, Chu Q, Lyle M, Tang L, et al. A phase 1 study of SLC-0111, a novel inhibitor of carbonic anhydrase IX, in patients with advanced solid tumors. Am J Clin Oncol. 2020; 43:484–90. https://doi.org/10.1097/COC.0000000000000691

Liu M, Hansen PE, Lin X. Bromophenols in marine algae and their bioactivities. Mar Drugs. 2011; 9:1273–92. https://doi.org/10.3390/md9071273

Schinke C, Martins T, Queiroz SCN, Melo IS, Reyes FGR. Antibacterial compounds from marine bacteria, 2010–2015. J Nat Prod. 2017; 80:1215–28. https://doi.org/10.1021/acs.jnatprod.6b00235

Mujumdar P, Poulsen S-A. Natural products are primary sulfonamides and primary sulfamates. J Nat Prod. 2015; 78:1470–7. https://doi.org/10.1021/np501015m

Jiménez C, Crews P. Novel marine sponge derived amino acids 13. Additional psammaplin derivatives from Psammaplysilla purpurea. Tetrahedron. 1991; 47:2097–102. https://doi.org/10.1016/S0040-4020(01)96120-4

Mujumdar P, Teruya K, Tonissen KF, Vullo D, Supuran CT, Peat TS, et al. An unusual natural product primary sulfonamide: synthesis, carbonic anhydrase inhibition, and protein x-ray structures of psammaplin C. J Med Chem. 2016; 59:5462–70. https://doi.org/10.1021/acs.jmedchem.6b00443

Mujumdar P, Kopecka J, Bua S, Supuran CT, Riganti C, Poulsen S-A. Carbonic anhydrase XII inhibitors overcome temozolomide resistance in glioblastoma. J Med Chem. 2019; 62:4174–92. https://doi.org/10.1021/acs.jmedchem.9b00282

Karthikeyan A, Joseph A, Nair BG. Promising bioactive compounds from the marine environment and their potential effects on various diseases. J Genet Eng Biotechnol. 2022; 20:14. https://doi.org/10.1186/s43141-021-00290-4

Supuran CT. Carbonic anhydrase inhibitors from marine natural products. Mar Drugs. 2022; 20:721. https://doi.org/10.3390/md20110721

Takahashi A, Ikeda D, Nakamura H, Naganawa H, Kurasawa S, Okami Y, et al. Altemicidin, a new acaricidal and antitumor substance. II. Structure determination. J Antibiot (Tokyo). 1989; 42:1562–6. https://doi.org/10.7164/antibiotics.42.1562

Borges F, Roleira F, Milhazes N, Santana L, Uriarte E. Simple coumarins and analogs in medicinal chemistry: occurrence, synthesis, and biological activity. Curr Med Chem. 2005; 12:887–916. https://doi.org/10.2174/0929867053507315

Maresca A, Temperini C, Vu H, Pham NB, Poulsen S-A, Scozzafava A, 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. https://doi.org/10.1021/ja809683v

Lopez M, Vu H, Wang CK, Wolf MG, Groenhof G, Innocenti A, et al. Promiscuity of carbonic anhydrase II. unexpected ester hydrolysis of carbohydrate-based sulfamate inhibitors. J Am Chem Soc. 2011; 133:18452–62. https://doi.org/10.1021/ja207855c

Fois B, Distinto S, Meleddu R, Deplano S, Maccioni E, Floris C, et al. Coumarins from Magydaris pastinacea as inhibitors of the tumor-associated carbonic anhydrases IX and XII: isolation, biological studies and in silico evaluation. J Enzyme Inhib Med Chem. 2020; 35:539–48. https://doi.org/10.1080/14756366.2020.1713114

Melis C, Distinto S, Bianco G, Meleddu R, Cottiglia F, Fois B, et al. Targeting tumor-associated carbonic anhydrases IX and XII: highly isozyme selective coumarin and psoralen inhibitors. ACS Med Chem Lett. 2018; 9:725–9. https://doi.org/10.1021/acsmedchemlett.8b00170

Xia W, Gooden D, Liu L, Zhao S, Soderblom EJ, Toone EJ, et al. Photo-activated psoralen binds the ErbB2 catalytic kinase domain, blocking ErbB2 signaling and triggering tumor cell apoptosis. PLoS One. 2014; 9:e88983. https://doi.org/10.1371/journal.pone.0088983

Mercer DK, Robertson J, Wright K, Miller L, Smith S, Stewart CS, et al. A prodrug approach to the use of coumarins as potential therapeutics for superficial mycoses. PLoS One. 2013; 8:e80760. https://doi.org/10.1371/journal.pone.0080760