Cyanobacterial peptides as a prototype for the design of potent β-secretase inhibitors and the development of selective chemical probes for other aspartic proteases

Journal of Medicinal Chemistry

Volumn 55, Issue 23, 2012, Pages 10749-10765

  Liu, Yanxia ^a   Zhang, Wei ^a,b   Li, Li ^c   Salvador, Lilibeth A ^a   Chen, Tiantian ^c   Chen, Wuyan ^c   Felsenstein, Kevin M ^d   Ladd, Thomas B ^d   Price, Ashleigh R ^d   Golde, Todd E ^d   He, Jianhua ^e   Xu, Yechun ^c   Li, Yingxia ^b   Luesch, Hendrik ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b FUDAN UNIVERSITY   (China)

^c SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^d UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^e SHANGHAI INSTITUTE OF APPLIED PHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; ASPARTIC PROTEINASE; ASPARTIC PROTEINASE INHIBITOR; BACTERIAL PROTEIN; BETA SECRETASE INHIBITOR; CATHEPSIN D; CATHEPSIN E; CORTICOSTERONE; DRUG METABOLITE; GAMMA SECRETASE; GRASSYSTATIN A; N2 [2 (3,5 DIFLUOROPHENYL) 2 HYDROXYACETYL] N1 (6,7 DIHYDRO 5 METHYL 6 OXO 5H DIBENZ[B,D]AZEPIN 7 YL)ALANINAMIDE; PEPSTATIN; SULFONAMIDE; TASIAMIDE B DERIVATIVE; THEOPHYLLINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CARBOXY TERMINAL SEQUENCE; CELL ASSAY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG DESIGN; DRUG EFFICACY; DRUG FORMULATION; DRUG HALF LIFE; DRUG PENETRATION; DRUG PROTEIN BINDING; DRUG SELECTIVITY; DRUG STABILITY; DRUG TRANSFORMATION; DRUG TRANSPORT; ENZYME INHIBITION; IC 50; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; PROTEIN PROCESSING; STEREOSPECIFICITY; STRUCTURE ACTIVITY RELATION;

AMYLOID PRECURSOR PROTEIN SECRETASES; ASPARTIC ACID PROTEASES; CYANOBACTERIA; DRUG DESIGN; MODELS, MOLECULAR; MOLECULAR PROBES; PEPTIDES; PROTEASE INHIBITORS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84871001564     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm301630s     Document Type: Article

References (51)

1. Tan, L. T. Filamentous tropical marine cyanobacteria: a rich source of natural products for anticancer drug discovery J. Appl. Phycol. 2010, 22, 659-676
2. Chlipala, G. E.; Mo, S.; Orjala, J. Chemodiversity in freshwater and terrestrial cyanobacteria-a source for drug discovery Curr. Drug Targets 2011, 12, 1654-1673
3. Carmeli, S.; Grach-Pogrebinsky, O.; Gesner-Apter, S.; Raveh, A.; Lifshitz, M.; Zafrir, E. Biologically active cyanobacteria metabolites- Ecological and biomedical perspectives Planta Med. 2008, 74
4. Taori, K.; Paul, V. J.; Luesch, H.; Kempopeptins, A and B, serine protease inhibitors with different selectivity profiles from a marine cyanobacterium, Lyngbya sp J. Nat. Products 2008, 71, 1625-1629
5. Kwan, J. C.; Taori, K. T.; Paul, V. J.; Luesch, H. Lyngbyastatins 8-10, elastase inhibitors with cyclic depsipeptide scaffolds isolated from the marine cyanobacterium Lyngbya semiplena Mar. Drugs 2009, 7, 528-538
6. Matthew, S.; Ratnayake, R.; Becerro, M. A.; Ritson-Williams, R.; Paul, V. J.; Luesch, H. Intramolecular modulation of serine protease inhibitor activity in a marine cyanobacterium with antifeedant properties Mar. Drugs 2010, 8, 1803-1816
7. Kwan, J. C.; Eksioglu, E. A.; Liu, C.; Paul, V. J.; Luesch, H.; Grassystatins, A.-C. potent cathepsin E inhibitors that reduce antigen presentation J. Med. Chem. 2009, 52, 5732-5747
8. Williams, P. G.; Yoshida, W. Y.; Moore, R. E.; Paul, V. J. The isolation and structure elucidation of tasiamide B, a 4-amino-3-hydroxy-5-phenylpentanoic acid containing peptide from the marine cyanobacterium Symploca sp J. Nat. Prod. 2003, 66, 1006-1009
9. Sun, T.; Zhang, W.; Zong, C.; Wang, P.; Li, Y. Total synthesis and stereochemical reassignment of tasiamide B J. Pept. Sci. 2010, 16, 364-374
10. Kortum, S. W.; Benson, T. E.; Bienkowski, M. J.; Emmons, T. L.; Prince, D. B.; Paddock, D. J.; Tomasselli, A. G.; Moon, J. B.; LaBorde, A.; TenBrink, R. E. Potent and selective isophtalamide S2 hydroxyethylamine inhibitors of BACE1 Bioorg. Med. Chem. Lett. 2007, 17, 3378-3383
11. Cumming, J. N.; Le, T. X.; Babu, S.; Carroll, C.; Chen, X.; Favreau, L.; Gaspari, P.; Guo, T.; Hobbs, D. W.; Huang, Y.; Iserloh, U.; Kennedy, M. E.; Kuvelkar, R.; Li, G.; Lowrie, J.; McHugh, N. A.; Ozgur, L.; Pan, J.; Parker, E. M.; Saionz, K.; Stamford, A. W.; Strickland, C.; Tadesse, D.; Voigt, J.; Wang, L.; Wu, Y.; Zhang, L.; Zhang, Q. Rational design of novel, potent piperazinone and imidazolidinone BACE1 inhibitors Bioorg. Med. Chem. Lett. 2008, 18, 3236-3241
12. Yang, S.; Zhang, W.; Ding, N.; Lo, J.; Liu, Y.; Clare-Salzler, M. J.; Luesch, H.; Li, Y. Total synthesis of grassystatin A, a probe for cathepsin E function Bioorg. Med. Chem. 2012, 20, 4774-4780
13. Ghosh, A. K.; Brindisi, M.; Tang, J. Developing β-secretase inhibitors for treatment of Alzheimer's disease J. Neurochem. 2012, 120 (Suppl. 1) 71-83
14. Zheng, H.; Koo, E. H. Biology and pathophysiology of the amyloid precursor protein Mol. Neurodegener. 2011, 6, 27-43
15. Hardy, J. A.; Higgins, G. A. Alzheimer's disease: the amyloid cascade hypothesis Science 1992, 256, 184-185
16. Galimberti, D.; Scarpin, E. Alzheimer's disease: from pathogenesis to disease-modifying approaches CNS Neurol. Disord. Drug Targets 2011, 10, 163-174
17. Ghosh, A. K.; Bilcer, G.; Hong, L.; Koelsch, G.; Tang, J. Memapsin 2 (beta-secretase) inhibitor drug, between fantasy and reality Curr. Alzheimer Res. 2007, 4, 418-422
18. Durham, T. B.; Shepherd, T. A. Progress toward the discovery and development of efficacious BACE inhibitors Curr. Opin. Drug Discovery Dev. 2006, 9, 776-791
19. Willem, M.; Garratt, A. N.; Novak, B.; Citron, M.; Kaufmann, S.; Rittger, A.; DeStrooper, B.; Saftig, P.; Birchmeier, C.; Haass, C. Control of peripheral nerve myelination by the β-secretase BACE1 Science 2006, 314, 664-666
20. Dominguez, D.; Tournoy, J.; Hartmann, D.; Huth, T.; Cryns, K.; Deforce, S.; Serneels, L.; Camacho, I. E.; Marjaux, E.; Craessaerts, K.; Roebroek, A. J. M.; Schwake, M.; D'Hooge, R.; Bach, P.; Kalinke, U.; Moechars, D.; Alzheimer, C.; Reiss, K.; Saftig, P.; DeStrooper, B. Phenotypic and biochemical analyses of BACE1- and BACE2-deficient mice J. Biol. Chem. 2005, 280, 30797-30806
21. Shen, J.; Bronson, R. T.; Chen, D. F.; Xia, W.; Selkoe, D. J.; Tonegawa, S. Skeletal and CNS defects in presenilin-1-deficient mice Cell 1997, 80, 629-639
22. McConlogue, L.; Buttini, M.; Anderson, J. P.; Brigham, E. F.; Chen, K. S.; Freedman, S. B.; Games, D.; Johnson-Wood, K.; Lee, M.; Zeller, M.; Liu, W.; Motter, R.; Sinha, S. Partial reduction of BACE1 has dramatic effects on Alzheimer plaque and synaptic pathology in APP transgenic mice J. Biol. Chem. 2007, 282, 26326-26334
23. 3-ligands J. Med. Chem. 2007, 50, 2399-2407
24. Hong, L.; Koelsch, G.; Lin, X.; Wu, S.; Terzyan, S.; Ghosh, A. K.; Zhang, X. C.; Tang, J. Structure of the protease domain of memapsin 2 (β-secretase) complexed with inhibitor Science 2000, 290, 150-153
25. Wallace, A. C.; Laskowski, R. A.; Thornton, J. M. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions Protein Eng. 1995, 8, 127-134
26. Felsenstein, K. M.; Hunihan, L. W.; Roberts, S. B. Altered cleavage and secretion of a recombinant β-APP bearing the Swedish familial Alzheimer's disease mutation Nat. Genet. 1994, 6, 251-256
27. Abbenante, G.; Kovacs, D. M.; Leung, D. L.; Craik, D. J.; Tanzi, R. E.; Fairlie, D. P. Inhibitors of β-amyloid formation based on the β-secretase cleavage site Biochem. Biophys. Res. Commun. 2000, 268, 133-135
28. Stachel, S. J.; Coburn, C. A.; Steele, T. G.; Jones, K. G.; Loutzenhiser, E. F.; Gregro, A. R.; Rajapakse, H. A.; Lai, M. T.; Crouthamel, M. C.; Xu, M.; Tugusheva, K.; Lineberger, J. E.; Pietrak, B. L.; Espeseth, A. S.; Shi, X. P.; Chen-Dodson, E.; Holloway, M. K.; Munshi, S.; Simon, A. J.; Kuo, L.; Vacca, J. P. Structure-based design of potent and selective cell-permeable inhibitors of human β-secretase (BACE-1) J. Med. Chem. 2004, 47, 6447-6450
29. Colombo, A.; Wang, H.; Kuhn, P. H.; Page, R.; Kremmer, E.; Dempsey, P. J.; Crawford, H. C.; Lichtenthaler, S. F. Constitutive α- and β-secretase cleavages of the amyloid precursor protein are partially coupled in neurons, but not in frequently used cell lines Neurobiol. Dis. 2012, 49C, 137-147
30. Hooper, N. M.; Trew, A. J.; Parkin, E. T.; Turner, A. J. The role of proteolysis in Alzheimer's disease Adv. Exp. Med. Biol. 2000, 477, 379-390
31. Parvathy, S.; Hussain, I.; Karran, E. H.; Turner, A. J.; Hooper, N. M. Alzheimer's amyloid precursor protein α-secretase is inhibited by hydroxamic acid-based zinc metalloprotease inhibitors: similarities to the angiotensin converting enzyme secretase Biochemistry 1998, 37, 1680-1685
32. Wu, J.; Tung, J. S.; Thorsett, E. D.; Pleiss, M. A.; Nissen, J. S.; Neitz, J.; Latimer, L. H.; John, V.; Freedman, S. Preparation of cycloalkyl, lactam, lactone and related compounds for inhibiting β-amyloid peptide release and/or its synthesis. PCT Int. Appl. WO 9828268A2 19980702, 1998.
33. Wong, G. T.; Manfra, D.; Poulet, F. M.; Zhang, Q.; Josien, H.; Bara, T.; Engstrom, L.; Pinzon-Ortiz, M.; Fine, J. S.; Lee, H. J.; Zhang, L.; Higgins, G. A.; Parker, E. M. Chronic treatment with the γ-secretase inhibitor LY-411,575 inhibits β-amyloid peptide production and alters lymphopoiesis and intestinal cell differentiation J. Biol. Chem. 2004, 279, 12876-12882
34. Lewis, P. A.; Piper, S.; Baker, M.; Onstead, L.; Murphy, M. P.; Hardy, J.; Wang, R.; McGowan, E.; Golde, T. E. Expression of BRI-amyloid β peptide fusion proteins: a novel method for specific high-level expression of amyloid β peptides Biochim. Biophys. Acta 2001, 1537, 58-62
35. 1-[(7 S)-5-methyl-6-oxo-6,7-dihydro-5 H -dibenzo[ b, d ]azepin-7-yl]-L-alaninamide (LY-411575) J. Pharmacol. Exp. Ther. 2004, 309, 49-55
36. Li, C.; Nair, L.; Liu, T.; Li, F.; Pichardo, J.; Agrawal, S.; Chase, R.; Tong, X.; Uss, A. S.; Bogen, S.; Njoroge, F. G.; Morrison, R. A.; Cheng, K.-C. Correlation between PAMPA permeability and cellular activities of hepatitis C virus protease inhibitors Biochem. Pharmacol. 2008, 75, 2286-1197
37. Fujikawa, M.; Ano, R.; Nakao, K.; Shimizu, R.; Akamatsu, M. Relationships between structure and high-throughput screening permeability of diverse drugs with artificial membranes: application to prediction of Caco-2 cell permeability Bioorg. Med. Chem. 2005, 13, 4721-4732
38. Chang, W.; Huang, X.; Downs, D.; Cirrito, J. R.; Koelsch, G.; Holtzma, D. M.; Ghosh, A. K.; Tang, J. β-secretase inhibitor GRL-8234 rescues age-related cognitive decline in APP transgenic mice FASEB J. 2011, 25, 775-784
39. Stachel, S. J. Progress towards the development of a viable BACE-1 inhibitor Drug Dev. Res. 2009, 70, 101-110
40. Stanton, M. G.; Stauffer, S. R.; Gregro, A. R.; Steinbeiser, M.; Nantermet, P.; Sankaranarayanan, S.; Price, E. A.; Wu, G.; Crouthamel, M.; Ellis, J.; Lai, M.; Espeseth, A. S.; Shi, X.; Jin, L.; Colussi, D.; Pietrak, B.; Huang, Q.; Xu, M.; Simon, A. J.; Graham, S. L.; Vacca, J. P.; Selnick, H. Discovery of isonicotinamide derived β-secretase inhibitors: In vivo reduction of β-amyloid J. Med. Chem. 2007, 50, 3431-3433
41. Xu, Y.; Li, M. J.; Greenblatt, H.; Chen, W.; Paz, A.; Dym, O.; Peleg, Y.; Chen, T.; Shen, X.; He, J.; Jiang, H.; Silman, I.; Sussman, J. L. Flexibility of the flap in the active site of BACE1 as revealed by crystal structures and molecular dynamics simulations Acta Crystallogr. D Biol. Crystallogr. 2012, 68, 13-25
42. Otwinowski, Z.; Minor, W. Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 1997, 276, 307-326
43. Kabsch, W. XDS Acta Crystallogr. D Biol. Crystallogr 2010, 66, 125-132
44. Collaborative-Computational-Project-Number-4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 1994, 50, 760-763.
45. Adams, P. D.; Grosse-Kunstleve, R. W.; Hung, L. W.; Ioerger, T. R.; McCoy, A. J.; Moriarty, N. W.; Read, R. J.; Sacchettini, J. C.; Sauter, N. K.; Terwilliger, T. C. PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr. D Biol. Crystallogr. 2002, 58, 1948-1954
46. Emsley, P.; Cowtan, K. Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 2004, 60, 2126-2132
47. Lanz, T. A.; Schachter, J. B. Solid-phase extraction enhances detection of beta-amyloid peptides in plasma and enables Aβ quantification following passive immunization with Aβ antibodies J. Neurosci. Methods 2008, 169, 16-22
48. Lanz, T. A.; Schachter, J. B. Demonstration of a common artifact in immunosorbent assays of brain extracts: development of a solid-phase extraction protocol to enable measurement of amyloid-beta from wild-type rodent brain J. Neurosci. Methods 2006, 157, 71-81
49. Yohrling, G. J.; Felsenstein, K. M.; Conway, K. A.; Zupa-Fernandez, A.; Brenneman, D. E.; Arnold, H. M. A comparative analysis of brain and plasma Aβ levels in eight common non-transgenic mouse strains: validation of a specific immunoassay for total rodent Aβ Curr. Alzheimer Res. 2007, 4, 297-303
50. Moore, B. D.; Chakrabarty, P.; Levites, Y.; Kukar, T. L.; Baine, A. M.; Moroni, T.; Ladd, T. B.; Das, P.; Dickson, D. W.; Golde, T. E. Overlapping profiles of Aβ peptides in the Alzheimer's disease and pathological aging brains Alzheimer's Res. Ther. 2012, 4, 18
51. Hoff, J. Methods of blood collection in the mouse Lab Anim. 2000, 29, 47-53