1w9v › Citations

Specificity and affinity of natural product cyclopentapeptide inhibitors against A. fumigatus, human, and bacterial chitinases.

Rao FV, Houston DR, Boot RG, Aerts JM, Hodkinson M, Adams DJ, Shiomi K, Omura S, van Aalten DM
Chem Biol 12 65-76 (2005)
Related entries: 1w9p, 1w9u, 1waw, 1wb0

Cited: 62 times
EuropePMC logo PMID: 15664516

Abstract

Family 18 chitinases play key roles in organisms ranging from bacteria to man. There is a need for specific, potent inhibitors to probe the function of these chitinases in different organisms. Such molecules could also provide leads for the development of chemotherapeuticals with fungicidal, insecticidal, or anti-inflammatory potential. Recently, two natural product peptides, argifin and argadin, have been characterized, which structurally mimic chitinase-chitooligosaccharide interactions and inhibit a bacterial chitinase in the nM-mM range. Here, we show that these inhibitors also act on human and Aspergillus fumigatus chitinases. The structures of these enzymes in complex with argifin and argadin, together with mutagenesis, fluorescence, and enzymology, reveal that subtle changes in the binding site dramatically affect affinity and selectivity. The data show that it may be possible to develop specific chitinase inhibitors based on the argifin/argadin scaffolds.

Articles - 1w9v mentioned but not cited (7)

  1. Structure-based dissection of the natural product cyclopentapeptide chitinase inhibitor argifin. Andersen OA, Nathubhai A, Dixon MJ, Eggleston IM, van Aalten DM. Chem Biol 15 295-301 (2008)
  2. Ligand deconstruction: Why some fragment binding positions are conserved and others are not. Kozakov D, Hall DR, Jehle S, Luo L, Ochiana SO, Jones EV, Pollastri M, Allen KN, Whitty A, Vajda S. Proc Natl Acad Sci U S A 112 E2585-94 (2015)
  3. Deamidation of Amino Acids on the Surface of Adeno-Associated Virus Capsids Leads to Charge Heterogeneity and Altered Vector Function. Giles AR, Sims JJ, Turner KB, Govindasamy L, Alvira MR, Lock M, Wilson JM. Mol Ther 26 2848-2862 (2018)
  4. Natural product-guided discovery of a fungal chitinase inhibitor. Rush CL, Schüttelkopf AW, Hurtado-Guerrero R, Blair DE, Ibrahim AF, Desvergnes S, Eggleston IM, van Aalten DM. Chem Biol 17 1275-1281 (2010)
  5. Solid-phase synthesis of cyclic peptide chitinase inhibitors: SAR of the argifin scaffold. Dixon MJ, Nathubhai A, Andersen OA, van Aalten DM, Eggleston IM. Org Biomol Chem 7 259-268 (2009)
  6. Toward the design of mutation-resistant enzyme inhibitors: further evaluation of the substrate envelope hypothesis. Kairys V, Gilson MK, Lather V, Schiffer CA, Fernandes MX. Chem Biol Drug Des 74 234-245 (2009)
  7. Research Support, Non-U.S. Gov't Exhaustive sampling of the fragment space associated to a molecule leading to the generation of conserved fragments. Heikamp K, Zuccotto F, Kiczun M, Ray P, Gilbert IH. Chem Biol Drug Des 91 655-667 (2018)


Reviews citing this publication (13)

  1. Insect chitinase and chitinase-like proteins. Arakane Y, Muthukrishnan S. Cell Mol Life Sci 67 201-216 (2010)
  2. Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Hartl L, Zach S, Seidl-Seiboth V. Appl Microbiol Biotechnol 93 533-543 (2012)
  3. The chemistry and biology of organic guanidine derivatives. Berlinck RG, Burtoloso AC, Kossuga MH. Nat Prod Rep 25 919-954 (2008)
  4. Biomarkers in the diagnosis of lysosomal storage disorders: proteins, lipids, and inhibodies. Aerts JM, Kallemeijn WW, Wegdam W, Joao Ferraz M, van Breemen MJ, Dekker N, Kramer G, Poorthuis BJ, Groener JE, Cox-Brinkman J, Rombach SM, Hollak CE, Linthorst GE, Witte MD, Gold H, van der Marel GA, Overkleeft HS, Boot RG. J Inherit Metab Dis 34 605-619 (2011)
  5. Recombinant CBM-fusion technology - Applications overview. Oliveira C, Carvalho V, Domingues L, Gama FM. Biotechnol Adv 33 358-369 (2015)
  6. Natural product family 18 chitinase inhibitors. Andersen OA, Dixon MJ, Eggleston IM, van Aalten DM. Nat Prod Rep 22 563-579 (2005)
  7. Chitin Deacetylases: Structures, Specificities, and Biotech Applications. Grifoll-Romero L, Pascual S, Aragunde H, Biarnés X, Planas A. Polymers (Basel) 10 E352 (2018)
  8. Structural Diversity and Biological Activities of Fungal Cyclic Peptides, Excluding Cyclodipeptides. Wang X, Lin M, Xu D, Lai D, Zhou L. Molecules 22 E2069 (2017)
  9. Recent development of two chitinase inhibitors, Argifin and Argadin, produced by soil microorganisms. Hirose T, Sunazuka T, Omura S. Proc Jpn Acad Ser B Phys Biol Sci 86 85-102 (2010)
  10. Microbial chitinases: properties, enhancement and potential applications. Gomaa EZ. Protoplasma 258 695-710 (2021)
  11. Biodegradation and Prospect of Polysaccharide from Crustaceans. Qiu S, Zhou S, Tan Y, Feng J, Bai Y, He J, Cao H, Che Q, Guo J, Su Z. Mar Drugs 20 310 (2022)
  12. Chitinases and peptide mimotopes. Beauvais A, Latgé JP. Chem Biol 12 7-8 (2005)
  13. [Study on the discovery of novel chitinase inhibitors based on natural products]. Hirose T. Yakugaku Zasshi 132 1001-1010 (2012)

Articles citing this publication (42)

  1. Methylxanthine drugs are chitinase inhibitors: investigation of inhibition and binding modes. Rao FV, Andersen OA, Vora KA, Demartino JA, van Aalten DM. Chem Biol 12 973-980 (2005)
  2. Repositioning of an existing drug for the neglected tropical disease Onchocerciasis. Gloeckner C, Garner AL, Mersha F, Oksov Y, Tricoche N, Eubanks LM, Lustigman S, Kaufmann GF, Janda KD. Proc Natl Acad Sci U S A 107 3424-3429 (2010)
  3. Structure of Saccharomyces cerevisiae chitinase 1 and screening-based discovery of potent inhibitors. Hurtado-Guerrero R, van Aalten DM. Chem Biol 14 589-599 (2007)
  4. A novel family of lectins evolutionarily related to class V chitinases: an example of neofunctionalization in legumes. Van Damme EJ, Culerrier R, Barre A, Alvarez R, Rougé P, Peumans WJ. Plant Physiol 144 662-672 (2007)
  5. A structural and biochemical model of processive chitin synthesis. Dorfmueller HC, Ferenbach AT, Borodkin VS, van Aalten DMF. J Biol Chem 289 23020-23028 (2014)
  6. Chitinase inhibitors: extraction of the active framework from natural argifin and use of in situ click chemistry. Hirose T, Sunazuka T, Sugawara A, Endo A, Iguchi K, Yamamoto T, Ui H, Shiomi K, Watanabe T, Sharpless KB, Omura S. J Antibiot (Tokyo) 62 277-282 (2009)
  7. Crystal structure and mutagenesis analysis of chitinase CrChi1 from the nematophagous fungus Clonostachys rosea in complex with the inhibitor caffeine. Yang J, Gan Z, Lou Z, Tao N, Mi Q, Liang L, Sun Y, Guo Y, Huang X, Zou C, Rao Z, Meng Z, Zhang KQ. Microbiology (Reading) 156 3566-3574 (2010)
  8. Kinetic and crystallographic analyses of the catalytic domain of chitinase from Pyrococcus furiosus- the role of conserved residues in the active site. Tsuji H, Nishimura S, Inui T, Kado Y, Ishikawa K, Nakamura T, Uegaki K. FEBS J 277 2683-2695 (2010)
  9. Use of chitin and chitosan to produce new chitooligosaccharides by chitinase Chit42: enzymatic activity and structural basis of protein specificity. Kidibule PE, Santos-Moriano P, Jiménez-Ortega E, Ramírez-Escudero M, Limón MC, Remacha M, Plou FJ, Sanz-Aparicio J, Fernández-Lobato M. Microb Cell Fact 17 47 (2018)
  10. Molecular, Structural and Immunological Characterization of Der p 18, a Chitinase-Like House Dust Mite Allergen. Resch Y, Blatt K, Malkus U, Fercher C, Swoboda I, Focke-Tejkl M, Chen KW, Seiberler S, Mittermann I, Lupinek C, Rodriguez-Dominguez A, Zieglmayer P, Zieglmayer R, Keller W, Krzyzanek V, Valent P, Valenta R, Vrtala S. PLoS One 11 e0160641 (2016)
  11. An efficient synthesis of argifin: a natural product chitinase inhibitor with chemotherapeutic potential. Dixon MJ, Andersen OA, van Aalten DM, Eggleston IM. Bioorg Med Chem Lett 15 4717-4721 (2005)
  12. Chitin-binding proteins of Artemia diapause cysts participate in formation of the embryonic cuticle layer of cyst shells. Ma WM, Li HW, Dai ZM, Yang JS, Yang F, Yang WJ. Biochem J 449 285-294 (2013)
  13. Structure, Catalysis, and Inhibition of OfChi-h, the Lepidoptera-exclusive Insect Chitinase. Liu T, Chen L, Zhou Y, Jiang X, Duan Y, Yang Q. J Biol Chem 292 2080-2088 (2017)
  14. Screening-based discovery of drug-like O-GlcNAcase inhibitor scaffolds. Dorfmueller HC, van Aalten DM. FEBS Lett 584 694-700 (2010)
  15. Comparative molecular evolution of trichoderma chitinases in response to mycoparasitic interactions. Ihrmark K, Asmail N, Ubhayasekera W, Melin P, Stenlid J, Karlsson M. Evol Bioinform Online 6 1-26 (2010)
  16. Fully deacetylated chitooligosaccharides act as efficient glycoside hydrolase family 18 chitinase inhibitors. Chen L, Zhou Y, Qu M, Zhao Y, Yang Q. J Biol Chem 289 17932-17940 (2014)
  17. Mutation of Trp137 to glutamate completely removes transglycosyl activity associated with the Aspergillus fumigatus AfChiB1. Lü Y, Yang H, Hu H, Wang Y, Rao Z, Jin C. Glycoconj J 26 525-534 (2009)
  18. Bent Into Shape: Folded Peptides to Mimic Protein Structure and Modulate Protein Function. Merritt HI, Sawyer N, Arora PS. Pept Sci (Hoboken) 112 e24145 (2020)
  19. Chitinase inhibition by chitobiose and chitotriose thiazolines. Macdonald JM, Tarling CA, Taylor EJ, Dennis RJ, Myers DS, Knapp S, Davies GJ, Withers SG. Angew Chem Int Ed Engl 49 2599-2602 (2010)
  20. Observation of the controlled assembly of preclick components in the in situ click chemistry generation of a chitinase inhibitor. Hirose T, Maita N, Gouda H, Koseki J, Yamamoto T, Sugawara A, Nakano H, Hirono S, Shiomi K, Watanabe T, Taniguchi H, Sharpless KB, Omura S, Sunazuka T. Proc Natl Acad Sci U S A 110 15892-15897 (2013)
  21. New insights into the enzymatic mechanism of human chitotriosidase (CHIT1) catalytic domain by atomic resolution X-ray diffraction and hybrid QM/MM. Fadel F, Zhao Y, Cachau R, Cousido-Siah A, Ruiz FX, Harlos K, Howard E, Mitschler A, Podjarny A. Acta Crystallogr D Biol Crystallogr 71 1455-1470 (2015)
  22. A computational analysis of the binding mode of closantel as inhibitor of the Onchocerca volvulus chitinase: insights on macrofilaricidal drug design. Segura-Cabrera A, Bocanegra-García V, Lizarazo-Ortega C, Guo X, Correa-Basurto J, Rodríguez-Pérez MA. J Comput Aided Mol Des 25 1107-1119 (2011)
  23. Potent family-18 chitinase inhibitors: x-ray structures, affinities, and binding mechanisms. Pantoom S, Vetter IR, Prinz H, Suginta W. J Biol Chem 286 24312-24323 (2011)
  24. Argifin; efficient solid phase total synthesis and evaluation of analogues of acyclic peptide. Sunazuka T, Sugawara A, Iguchi K, Hirose T, Nagai K, Noguchi Y, Saito Y, Yamamoto T, Ui H, Gouda H, Shiomi K, Watanabe T, Omura S. Bioorg Med Chem 17 2751-2758 (2009)
  25. Screening-based discovery of Aspergillus fumigatus plant-type chitinase inhibitors. Lockhart DE, Schuettelkopf A, Blair DE, van Aalten DM. FEBS Lett 588 3282-3290 (2014)
  26. Antifungal activity and expression patterns of extracellular chitinase and β-1,3-glucanase in Wickerhamomyces anomalus EG2 treated with chitin and glucan. Hong SH, Song YS, Seo DJ, Kim KY, Jung WJ. Microb Pathog 110 159-164 (2017)
  27. Molecular cloning and characterization of ech46 endochitinase from Trichoderma harzianum. Sharma V, Salwan R, Sharma PN, Kanwar SS. Int J Biol Macromol 92 615-624 (2016)
  28. Chitinase from Autographa californica multiple nucleopolyhedrovirus: rapid purification from Sf-9 medium and mode of action. Fukamizo T, Sato H, Mizuhara M, Ohnuma T, Gotoh T, Hiwatashi K, Takahashi S. Biosci Biotechnol Biochem 75 1763-1769 (2011)
  29. Glycosidase inhibition by macrolide antibiotics elucidated by STD-NMR spectroscopy. Sadeghi-Khomami A, Lumsden MD, Jakeman DL. Chem Biol 15 739-749 (2008)
  30. Benzoxazepine-Derived Selective, Orally Bioavailable Inhibitor of Human Acidic Mammalian Chitinase. Andryianau G, Kowalski M, Piotrowicz MC, Rajkiewicz AA, Dymek B, Sklepkiewicz PL, Pluta E, Stefaniak F, Czestkowski W, Olejniczak S, Mazur M, Niedziejko P, Koralewski R, Matyszewski K, Gruza M, Zagozdzon A, Salamon M, Rymaszewska A, Welzer M, Dzwonek K, Golab J, Olczak J, Bartoszewicz A, Golebiowski A. ACS Med Chem Lett 11 1228-1235 (2020)
  31. Design and synthesis of a novel inhibitor of T. Viride chitinase through an in silico target fishing protocol. Maccari G, Deodato D, Fiorucci D, Orofino F, Truglio GI, Pasero C, Martini R, De Luca F, Docquier JD, Botta M. Bioorg Med Chem Lett 27 3332-3336 (2017)
  32. Structural dissection reveals a general mechanistic principle for group II chitinase (ChtII) inhibition. Chen W, Zhou Y, Yang Q. J Biol Chem 294 9358-9364 (2019)
  33. Solid-phase total synthesis of the chitinase inhibitor Argadin using a supported acetal resin. Hirose T, Sunazuka T, Sugawara A, Noguchi Y, Tanaka T, Iguchi K, Yamamoto T, Gouda H, Shiomi K, Omura S. J Antibiot (Tokyo) 62 495-500 (2009)
  34. Structural inspection and protein motions modelling of a fungal glycoside hydrolase family 18 chitinase by crystallography depicts a dynamic enzymatic mechanism. Jiménez-Ortega E, Kidibule PE, Fernández-Lobato M, Sanz-Aparicio J. Comput Struct Biotechnol J 19 5466-5478 (2021)
  35. A Plumieridine-Rich Fraction From Allamanda polyantha Inhibits Chitinolytic Activity and Exhibits Antifungal Properties Against Cryptococcus neoformans. Silva E Souza E, Barcellos VA, Sbaraini N, Reuwsaat JCV, Schneider RO, da Silva AC, Garcia AWA, von Poser GL, Barbosa EG, Lima JPMS, Vainstein MH. Front Microbiol 11 2058 (2020)
  36. How to identify a pharmacophore. Prinz H. Chem Biol 15 207-208 (2008)
  37. Crystal structures of the GH18 domain of the bifunctional peroxiredoxin-chitinase CotE from Clostridium difficile. Whittingham JL, Hanai S, Brannigan JA, Ferreira WT, Dodson EJ, Turkenburg JP, Cartwright J, Cutting SM, Wilkinson AJ. Acta Crystallogr F Struct Biol Commun 76 241-249 (2020)
  38. Discovery of Chitin Deacetylase Inhibitors through Structure-Based Virtual Screening and Biological Assays. Liu Y, Ahmed S, Fang Y, Chen M, An J, Yang G, Hou X, Lu J, Ye Q, Zhu R, Liu Q, Liu S. J Microbiol Biotechnol 32 504-513 (2022)
  39. Kinetic characterization of Aspergillus niger chitinase CfcI using a HPAEC-PAD method for native chitin oligosaccharides. van Munster JM, Sanders P, ten Kate GA, Dijkhuizen L, van der Maarel MJ. Carbohydr Res 407 73-78 (2015)
  40. Phage display screening for peptidic chitinase inhibitors. Petter C, Scholz C, Wessner H, Hansen G, Henklein P, Watanabe T, Höhne W. J Mol Recognit 21 401-409 (2008)
  41. Discovery of Octahydroisoindolone as a Scaffold for the Selective Inhibition of Chitinase B1 from Aspergillus fumigatus: In Silico Drug Design Studies. Marbán-González A, Hernández-Mendoza A, Ordóñez M, Razo-Hernández RS, Viveros-Ceballos JL. Molecules 26 7606 (2021)
  42. Total synthesis of the putative structure of the proposed Banyasin A. Gao X, Ren Q, Choi S, Xu Z, Ye T. Front Chem 3 19 (2015)


Quick links