Structure - activity relationship and mechanism of action studies of manzamine analogues for the control of neuroinflammation and cerebral infections

Journal of Medicinal Chemistry

Volumn 53, Issue 1, 2010, Pages 61-76

  Peng, Jiangnan ^a   Kudrimoti, Sucheta ^a   Prasanna, Sivaprakasam ^b,g   Odde, Srinivas ^b   Doerksen, Robert J ^b   Pennaka, Hari K ^a   Choo, Yeun Mun ^a   Rao, Karumanchi V ^a   Tekwani, Babu L ^b   Madgula, Vamsi ^b   Khan, Shabana I ^a,b   Wang, Bin ^a   Mayer, Alejandro M S ^c   Jacob, Melissa R ^b   Tu, Lan Chun ^d   Gertsch, Jürg ^e,f   Hamann, Mark T ^a,b  

^a UNIVERSITY OF MISSISSIPPI   (United States)

^b UNIVERSITY OF MISSISSIPPI   (United States)

^c MIDWESTERN UNIVERSITY   (United States)

^d NATIONAL YANG MING UNIVERSITY   (Taiwan)

^e ETH ZURICH   (Switzerland)

^f UNIVERSITY OF BERN   (Switzerland)

^g BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYMANZAMINE A; AMPHOTERICIN B; ANTIMALARIAL AGENT; CHLOROQUINE; CIPROFLOXACIN; GLYCOGEN SYNTHASE KINASE 3BETA; IRCINAL; LACTATE DEHYDROGENASE; MANZAMINE A; MANZAMINE F; PHORBOL 13 ACETATE 12 MYRISTATE; QUININE; RIFAMPICIN; SUPEROXIDE; THROMBOXANE B2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIFUNGAL ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ANTIMALARIAL ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; BRAIN MALARIA; CONTROLLED STUDY; DRUG ABSORPTION; DRUG PENETRATION; DRUG SYNTHESIS; IC 50; MALARIA; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR DOCKING; MOUSE; NONHUMAN; PLASMODIUM BERGHEI; REACTION ANALYSIS; STRUCTURE ACTIVITY RELATION;

ANIMALS; ANTI-INFECTIVE AGENTS; CARBAZOLES; CEREBELLAR DISEASES; INDOLE ALKALOIDS; MICE; MICROBIAL SENSITIVITY TESTS; MOLECULAR STRUCTURE; NEUROGENIC INFLAMMATION; PORIFERA; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 74849100624     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm900672t     Document Type: Article

References (72)

1. Sakai, R.; Higa, T.; Jefford, C. W.; Bernardinelli, G. Manzamine A, a novel antitumor alkaloid from a sponge. J. Am. Chem. Soc. 1986, 108, 6404-6405.
2. Hu, J. F.; Hamann, M. T.; Hill, R.; Kelly, M. The manzamine alkaloids. Alkaloids Chem. Biol. 2003, 60, 207-285.
3. Peng, J.; Rao, K. V.; Choo, Y. -M.; Hamann, M. T. In, Moden Alakloids; Fattorusso, E. T., S. O., Ed.; Wiley-VCH: Weinheim, Germany: 2008; pp 189-232.
4. Rao, K. V.; Santarsiero, B. D.; Mesecar, A. D.; Schinazi, R. F.; Tekwani, B. L.; Hamann, M. T. New manzamine alkaloids with activity against infectious and tropical parasitic diseases from an Indonesian sponge. J. Nat. Prod. 2003, 66, 823-828.
5. Hamann, M. T.; El-Sayed, K. A. Methods of treating drug-resistant infections through administration of pharmaceutical compositions containing manzamine alkaloids. U.S. Patent US27035, 2002.
6. Nakamura, H.; Deng, S.; Kobayashi, J.; Ohizumi, Y.; Tomotake, Y.; Matsuzaki, T.; Hirata, Y. Physiologically active marine natural products from Porifera. XV. Keramamine-A and -B, novel antimicrobial alkaloids from the Okinawan marine sponge Pellina sp. Tetrahedron Lett. 1987, 28, 621-624.
7. El Sayed, K. A.; Kelly, M.; Kara, U. A.; Ang, K. K.; Katsuyama, I.; Dunbar, D. C.; Khan, A. A.; Hamann, M. T. New manzamine alkaloids with potent activity against infectious diseases. J. Am. Chem. Soc. 2001, 123, 1804-1808.
8. Ang, K. K.; Holmes, M. J.; Higa, T.; Hamann,M. T.; Kara, U. A. In vivo antimalarial activity of the beta-carboline alkaloid manzamine A. Antimicrob. Agents Chemother. 2000, 44, 1645-1649.
9. Longley, R. E.; McConnell, O. J.; Essich, E.; Harmody, D. Evaluation of marine sponge metabolites for cytotoxicity and signal transduction activity. J. Nat. Prod. 1993, 56, 915-920.
10. Mayer, A. M. S.; Gunasekera, S. P.; Pomponi, S. A.; Sennett, S. H. Anti-inflammatory uses of manzamine. U.S. Patent US 20020187999, 2002.
11. Mayer, A. M. S.; Gunasekera, S. P.; Pomponi, S. A.; Sennett, S. H. Anti-inflammatory uses of manzamines. U.S. PatentUS6,602,881, 2003.
12. Yousaf, M.; Hammond, N. L.; Peng, J.; Wahyuono, S.; McIntosh, K. A.; Charman, W. N.; Mayer, A. M.; Hamann, M. T. New manzamine alkaloids from an Indo-Pacific sponge. Pharmacokinetics, oral availability, and the significant activity of several manzamines against HIV-I, AIDS opportunistic infections, and inflammatory diseases. J. Med. Chem. 2004, 47, 3512-3517.
13. Mayer, A. M.; Hall, M. L.; Lynch, S. M.; Gunasekera, S. P.; Sennett, S. H.; Pomponi, S. A. Differential modulation of microglia superoxide anion and thromboxane B2 generation by the marine manzamines. BMC Pharmacol. 2005, 5, 6.
14. Peng, J.; Shen, X.; El Sayed, K. A.; Dunbar, D. C.; Perry, T. L.; Wilkins, S. P.; Hamann, M. T.; Bobzin, S.; Huesing, J.; Camp, R.; Prinsen, M.; Krupa, D.; Wideman, M. A. Marine natural products as prototype agrochemical agents. J. Agric. Food Chem. 2003, 51, 2246-2252.
15. Rao, K. V.; Kasanah, N.; Wahyuono, S.; Tekwani, B. L.; Schinazi, R. F.; Hamann, M. T. Three new manzamine alkaloids from a common Indonesian sponge and their activity against infectious and tropical parasitic diseases. J. Nat. Prod. 2004, 67, 1314-1318.
16. Peng, J.; Hu, J. F.; Kazi, A. B.; Li, Z.; Avery, M.; Peraud, O.; Hill, R. T.; Franzblau, S. G.; Zhang, F.; Schinazi, R. F.; Wirtz, S. S.; Tharnish, P.; Kelly, M.; Wahyuono, S.; Hamann, M. T. Manadomanzamines A and B: a novel alkaloid ring system with potent activity against mycobacteria and HIV-1. J. Am. Chem. Soc. 2003, 125, 13382-13386.
17. Yousaf, M.; El Sayed, K. A.; Rao, K. V.; Lim, C. W.; Hu, J.-F.; Kelly, M.; Franzblau, S. G.; Zhang, F.; Peraud, O.; Hill, R. T.; Hamann, M. T. 12,34-Oxamanzamines, novel biocatalytic and natural products from manzamine producing Indo-Pacific sponges. Tetrahedron 2002, 58, 7397-7402.
18. El Sayed, K. A.; Bartyzel, P.; Shen, X.; Perry, T. L.; Zjawiony, J. K.; Hamann, M. T. Marine natural products as antituberculosis agents. Tetrahedron 2000, 56, 949-953.
19. Kondo, K.; Ohnishi, N.; Takemoto, K.; Yoshida, H.; Yoshida, K. Synthesis of optically quadratic nonlinear phenylpyridylacetylenes. J. Org. Chem. 1992, 57, 1622-1625.
20. Hamann, M.; Alonso, D.; Martin-Aparicio, E.; Fuertes, A.; Perez-Puerto, M. J.; Castro, A.; Morales, S.; Navarro, M. L.; Del Monte-Millan, M.; Medina, M.; Pennaka, H.; Balaiah, A.; Peng, J.; Cook, J.; Wahyuono, S.; Martinez, A. Glycogen synthase kinase-3 (GSK-3) inhibitory activity and structure - activity relationship (SAR) studies of the manzamine alkaloids. Potential for Alzheimer0s disease. J. Nat. Prod. 2007, 70, 1397-1405.
21. Liu, F.; Liang, Z.; Shi, J.; Yin, D.; El-Akkad, E.; Grundke-Iqbal, I.; Iqbal, K.; Gong, C. X. PKA modulates GSK-3beta- and cdk5-catalyzed phosphorylation of tau in site- and kinase-specific manners. FEBS Lett. 2006, 580, 6269-6274.
22. Winkler, J. D.; Axten, J. M. The First Total Syntheses of Ircinol A, Ircinal A, and Manzamines A and D. J. Am. Chem. Soc. 1998, 120, 6425-6426.
23. Martin, S. F.; Humphrey, J. M.; Ali, A.; Hillier, M. C. Enantioselective Total Syntheses of Ircinal A and Related Manzamine Alkaloids. J. Am. Chem. Soc. 1999, 121, 866-867.
24. Humphrey, J. M.; Liao, Y.; Ali, A.; Rein, T.; Wong, Y. L.; Chen, H. J.; Courtney, A. K.; Martin, S. F. Enantioselective total syntheses of manzamine a and related alkaloids. J. Am. Chem. Soc. 2002, 124, 8584-8592.
25. Pandit, U. K.; Overkleeft, H. S.; Borer, B. C.; Bieraugel, H. Synthesis mediated by ring-closing metathesis. Applications in the synthesis of azasugars and alkaloids. Eur. J. Org. Chem. 1999, 5, 959-968.
26. Uchida, H.; Nishida, A.; Nakagawa, M. An efficient access to the optically active manzamine tetracyclic ring system. Tetrahedron Lett. 1999, 40, 113-116.
27. Coldham, I.; Crapnell, K. M.; Fernandez, J. C.; Moseley, J. D.; Rabot, R. Synthesis of the ABC ring system of manzamine A. J. Org. Chem. 2002, 67, 6181-6187.
28. Baldwin, J. E.; Claridge, T. D. W.; Culshaw, A. J.; Heupel, F. A.; Lee, V.; Spring, D. R.; Whitehead, R. C.; Boughtflower, R. J.; Mutton, I. M.; Upton, R. J. Investigations into the manzamine alkaloid biosynthetic hypothesis. Angew. Chem., Int. Ed. 1998, 37, 2661-2663.
29. Winkler, J. D.; Londregan, A. T.; Ragains, J. R.; Hamann, M. T. Synthesis and biological evaluation of manzamine analogues. Org. Lett. 2006, 8, 3407-3409.
30. Winkler, J. D.; Londregan, A. T.; Hamann, M. T. Antimalarial activity of a new family of analogues of manzamine A. Org. Lett. 2006, 8, 2591-2594.
31. Torisawa, Y.; Hashimoto, A.; Okouchi, M.; Iimori, T.; Nagasawa, M.; Hino, T.; Nakagawa, M. Manzamine C congeners with modified azacyclic rings: synthesis and biological evaluation. Bioorg. Med. Chem. Lett. 1996, 6, 2565-2570.
32. Winkler, J. D.; Londregan, A. T.; Hamann, M. T. Synthetic modification of manzamine A via Grubbs metathesis. Novel structures with enhanced antibacterial and antiprotozoal properties. Org. Lett. 2007, 9, 4467-4469.
33. Choo, Y.-M.; Hamann, M. T. An improved Pictet - Spengler condensation: a convenient synthetic route to bioactive manzamine derivatives. Heterocycles 2007, 71, 245-252.
34. Mayer, A. M.; Oh, S.; Ramsey, K. H.; Jacobson, P. B.; Glaser, K. B.; Romanic, A. M. Escherichia coli lipopolysaccharide potentiation and inhibition of rat neonatal microglia superoxide anion generation: correlation with prior lactic dehydrogenase, nitric oxide, tumor necrosis factor-alpha, thromboxane B2, and metalloprotease release. Shock (Augusta, GA) 1999, 11, 180-186.
35. Morgenstern, S.; Flor, R.; Kessler, G.; Klein, B. The automated determination of NAD-coupled enzymes. II. Serum lactate dehydrogenase. Clin. Chem. 1966, 12, 274-281.
36. Deininger, M. H.; Kremsner, P. G.; Meyermann, R.; Schluesener, H. Macrophages/microglial cells in patients with cerebral malaria. Eur. Cytokine Network 2002, 13, 173-185.
37. Van der Heyde, H. C.; Nolan, J.; Combes, V.; Gramaglia, I.; Grau, G. E. A unified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to microcirculatory dysfunction. Trends Parasitol. 2006, 22, 503-508.
38. Schluesener, H. J.; Kremsner, P. G.; Meyermann, R. Widespread expression of MRP8 and MRP14 in human cerebral malaria by microglial cells. Acta Neuropathol. 1998, 96, 575-580.
39. Woodgett, J. R. In Glycogen synthase Kinase 3 (GSK-3) and its Inhibitors; Martinez, A., Castro, A., Medina, M., Eds.; John Wiley & Sons: Hoboken, NJ 2006; pp 3-23.
40. Forde, J. E.; Dale, T. C. Glycogen synthase kinase 3: a key regulator of cellular fate. Cell. Mol. Life Sci. 2007, 64, 1930-1944.
41. Cohen, P.; Frame, S. The renaissance of GSK3. Nat. Rev. Mol. Cell Biol. 2001, 2, 769-776.
42. Meijer, L.; Flajolet, M.; Greengard, P. Pharmacological inhibitors of glycogen synthase kinase 3. Trends Pharmacol. Sci. 2004, 25, 471-480.
43. Rao, K. V.; Donia, M. S.; Peng, J.; Garcia-Palomero, E.; Alonso, D.; Martinez, A.; Medina, M.; Franzblau, S. G.; Tekwani, B. L.; Khan, S. I.; Wahyuono, S.; Willett, K. L.; Hamann, M. T. Manzamine B and E and ircinal A related alkaloids from an Indonesian Acanthostrongylophora sponge and their activity against infectious, tropical parasitic, and Alzheimer0s diseases. J. Nat. Prod. 2006, 69, 1034-1040.
44. Tu, L. C.; Chou, C. K.; Chen, C. Y.; Chang, Y. T.; Shen, Y. C.; Yeh, S. F. Characterization of the cytotoxic mechanism of Mana-Hox, an analog of manzamine alkaloids. Biochim. Biophys. Acta 2004, 1672, 148-156.
45. Verdonk, M. L.; Cole, J. C.; Hartshorn, M. J.; Murray, C. W.; Taylor, R. D. Improved protein-ligand docking using GOLD. Proteins 2003, 52, 609-623.
46. Dajani, R.; Fraser, E.; Roe, S. M.; Young, N.; Good, V.; Dale, T. C.; Pearl, L. H. Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell 2001, 105, 721-732.
47. Bax, B.; Carter, P. S.; Lewis, C.; Guy, A. R.; Bridges, A.; Tanner, R.; Pettman, G.; Mannix, C.; Culbert, A. A.; Brown, M. J.; Smith, D. G.; Reith, A. D. The structure of phosphorylated GSK-3beta complexed with a peptide, FRATtide, that inhibits beta-catenin phosphorylation. Structure 2001, 9, 1143-1152.
48. Martinez, A.; Alonso, M.; Castro, A.; Perez, C.; Moreno, F. J. First non-ATP competitive glycogen synthase kinase 3 beta (GSK-3beta) inhibitors: thiadiazolidinones (TDZD) as potential drugs for the treatment of Alzheimer0s disease. J. Med. Chem. 2002, 45, 1292-1299.
49. Martinez, A.; Alonso, M.; Castro, A.; Dorronsoro, I.; Gelpi, J. L.; Luque, F. J.; Perez, C.; Moreno, F. J. SAR and 3D-QSAR studies on thiadiazolidinone derivatives: exploration of structural requirements for glycogen synthase kinase 3 inhibitors. J. Med. Chem. 2005, 48, 7103-7112.
50. Droucheau, E.; Primot, A.; Thomas, V.; Mattei, D.; Knockaert, M.; Richardson, C.; Sallicandro, P.; Alano, P.; Jafarshad, A.; Baratte, B.; Kunick, C.; Parzy, D.; Pearl, L.; Doerig, C.; Meijer, L. Plasmodium falciparum glycogen synthase kinase-3: molecular model, expression, intracellular localization and selective inhibitors. Biochim. Biophys. Acta, Proteins Proteomics 2004, 1697, 181-196.
51. Martin, M.; Rehani, K.; Jope, R. S.; Michalek, S. M. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 2005, 6, 777-784.
52. Jope, R. S.; Yuskaitis, C. J.; Beurel, E. Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem. Res. 2007, 32, 577-595.
53. Magae, Y.; Magae, J. Effect of staurosporine on growth and hyphal morphology of Pleurotus ostreatus. J. Gen. Microbiol. 1993, 139, 161-164.
54. Park, H. J.; Lee, J. Y.; Hwang, I. S.; Yun, B. S.; Kim, B. S.; Hwang, B. K. Isolation and antifungal and antioomycete activities of staurosporine from Streptomyces roseoflavus strain LS-A24. J. Agric. Food Chem. 2006, 54, 3041-3046.
55. Hunt, N. H.; Golenser, J.; Chan-Ling, T.; Parekh, S.; Rae, C.; Potter, S.; Medana, I. M.; Miu, J.; Ball, H. J. Immunopathogenesis of cerebral malaria. Int. J. Parasitol. 2006, 36, 569-582.
56. Szklarczyk, A.; Stins, M.; Milward, E. A.; Ryu, H.; Fitzsimmons, C.; Sullivan, D.; Conant, K. Glial activation and matrix metalloproteinase release in cerebral malaria. J. Neurovirol. 2007, 13, 2-10.
57. Medana, I. M.; Hunt, N. H.; Chan-Ling, T. Early activation of microglia in the pathogenesis of fatal murine cerebral malaria. Glia 1997, 19, 91-103.
58. Hiestand, P. C.; Petersen, F.; Roggo, S.; Hamann, M. T. Use of manzamines in transplantation and autoimmune diseases. Patent EP7678, 2006.
59. Golenser, J.; McQuillan, J.; Hee, L.; Mitchell, A. J.; Hunt, N. H. Conventional and experimental treatment of cerebral malaria. Int. J. Parasitol. 2006, 36, 583-593.
60. Akiyama, H.; Barger, S.; Barnum, S.; Bradt, B.; Bauer, J.; Cole, G. M.; Cooper, N. R.; Eikelenboom, P.; Emmerling, M.; Fiebich, B. L.; Finch, C. E.; Frautschy, S.; Griffin, W. S.; Hampel, H.; Hull, M.; Landreth, G.; Lue, L.; Mrak, R.; Mackenzie, I. R.; McGeer, P. L.; O'Banion, M. K.; Pachter, J.; Pasinetti, G.; Plata-Salaman, C.; Rogers, J.; Rydel, R.; Shen, Y.; Streit, W.; Strohmeyer, R.; Tooyoma, I.; Van Muiswinkel, F. L.; Veerhuis, R.; Walker, D.; Webster, S.; Wegrzyniak, B.; Wenk, G.; Wyss-Coray, T. Inflammation and Alzheimer0s disease. Neurobiol. Aging 2000, 21, 383-421.
61. Block, M. L.; Hong, J. S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 2005, 76, 77-98.
62. Sastre, M.; Klockgether, T.; Heneka, M. T. Contribution of inflammatory processes to Alzheimer0s disease: molecular mechanisms. Int. J. Dev. Neurosci. 2006, 24, 167-176.
63. Hill, R. T.; Hamann,M. T.; Peraud, O.; Kasanah, N. Manzamineproducing actinomycetes. U.S. Patent US24238, 2004.
64. Shilabin, A. G.; Kasanah, N.; Tekwani, B. L.; Hamann, M. T. Kinetic studies and bioactivity of potential manzamine prodrugs. J. Nat. Prod. 2008, 71, 1218-1221.
65. Ibrahim, M. A.; Shilabin, A. G.; Prasanna, S.; Jacob, M.; Khan, S. I.; Doerksen, R. J.; Hamann, M. T. 2-N-Methyl modifications and SAR studies of manzamine A. Bioorg. Med. Chem. 2008, 16, 6702-6706.
66. Makler, M. T.; Ries, J. M.; Williams, J. A.; Bancroft, J. E.; Piper, R. C.; Gibbins, B. L.; Hinrichs, D. J. Parasite lactate dehydrogenase as an assay for Plasmodium falciparum drug sensitivity. Am. J. Trop. Med. Hyg. 1993, 48, 739-741.
67. Borenfreund, E.; Babich, H.; Martin-Alguacil, N. Rapid chemosensitivity assay with human normal and tumor cells in vitro. In Vitro Cell Dev. Biol. 1990, 26, 1030-1034.
68. NCCLS. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard M27-A2; National Committee on Clinical Laboratory Standards, 2002; Vol. 22, Issue 15.
69. NCCLS. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard M24-T2; National Committee on Clinical Laboratory Standards, 2000, Vol. 20, Issue 26.
70. NCCLS. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically M7-A5; National Committee on Clinical Laboratory Standards, 2000; Vol. 20, Issue 2.
71. Franzblau, S. G.; Witzig, R. S.; McLaughlin, J. C.; Torres, P.; Madico, G.; Hernandez, A.; Degnan, M. T.; Cook, M. B.; Quenzer, V. K.; Ferguson, R. M.; Gilman, R. H. Rapid, low-technology MIC determination with clinical Mycobacterium tuberculosis isolates by using the microplate Alamar Blue assay. J. Clin. Microbiol. 1998, 36, 362-366.
72. Madgula, V. L.; Avula, B.; Reddy, V. L. N.; Khan, I. A.; Khan, S. I. Transport of decursin and decursinol angelate across Caco-2 and MDR-MDCK cell monolayers: in vitro models for intestinal and blood-brain barrier permeability. Planta Med. 2007, 73, 330-335.