Mitigation of ROS insults by streptomyces secondary metabolites in primary cortical neurons

ACS Chemical Neuroscience

Volumn 5, Issue 1, 2014, Pages 71-80

  Leirós, Marta ^a   Alonso, Eva ^a   Sanchez, Jon A ^a   Rateb, Mostafa E ^b,c   Ebel, Rainer ^b   Houssen, Wael E ^b   Jaspars, Marcel ^b   Alfonso, Amparo ^a   Botana, Luis M ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c Beni Suef University   (Egypt)

Author keywords

Marine natural products; neurodegenerative diseases; neuroprotection; Nrf2; oxidative stress; Streptomyces

Indexed keywords

3 EPI 5 DEOXYENTEROCIN; 5 DEOXYENTEROCIN; ANHYDROEXFOLIAMYCIN; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; CASPASE 3; CATALASE; DEFERROXAMINE E; GLUTATHIONE; HYDROGEN PEROXIDE; METACYCLOPRODIGIOSIN; NAPHTHOPYRANOMYCIN; NATURAL PRODUCT; NOCARDAMINE; PYRROLE DERIVATIVE; QUINONE DERIVATIVE; REACTIVE OXYGEN METABOLITE; STAUROSPORINE; STREPTORUBIN A; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; UNDECYLPRODIGIOSIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DEGENERATIVE DISEASE; DRUG STRUCTURE; ENZYME ACTIVITY; FETUS; IN VITRO STUDY; INHIBITION KINETICS; METABOLITE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; STREPTOMYCES; WESTERN BLOTTING;

ANIMALS; ANTI-BACTERIAL AGENTS; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; CARBOXYLIC ESTER HYDROLASES; CELLS, CULTURED; CEREBRAL CORTEX; CYTOSOL; EMBRYO, MAMMALIAN; ERYTHROMYCIN; HUMANS; L-LACTATE DEHYDROGENASE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; NEUROBLASTOMA; NEURONS; NF-E2-RELATED FACTOR 2; PROTON IONOPHORES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STREPTOMYCES;

EID: 84892752587     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn4001878     Document Type: Article

References (55)

1. Melo, A., Monteiro, L., Lima, R. M., Oliveira, D. M., Cerqueira, M. D., and El-Bacha, R. S. (2011) Oxidative stress in neurodegenerative diseases: mechanisms and therapeutic perspectives Oxid. Med. Cell. Longevity 2011, 467180
2. Gandhi, S. and Abramov, A. Y. (2012) Mechanism of oxidative stress in neurodegeneration Oxid. Med. Cell. Longevity 2012, 428010
3. Bonda, D. J., Wang, X., Perry, G., Nunomura, A., Tabaton, M., Zhu, X., and Smith, M. A. (2010) Oxidative stress in Alzheimer disease: a possibility for prevention Neuropharmacology 59, 290-294
4. Floyd, R. A. (1999) Antioxidants, oxidative stress, and degenerative neurological disorders Proc. Soc. Exp. Biol. Med. 222, 236-245
5. Pratico, D., Clark, C. M., Liun, F., Rokach, J., Lee, V. Y., and Trojanowski, J. Q. (2002) Increase of brain oxidative stress in mild cognitive impairment: a possible predictor of Alzheimer disease Arch. Neurol. 59, 972-976
6. Nunomura, A., Perry, G., Aliev, G., Hirai, K., Takeda, A., Balraj, E. K., Jones, P. K., Ghanbari, H., Wataya, T., Shimohama, S., Chiba, S., Atwood, C. S., Petersen, R. B., and Smith, M. A. (2001) Oxidative damage is the earliest event in Alzheimer disease J. Neuropathol. Exp. Neurol. 60, 759-767
7. Wang, X. and Michaelis, E. K. (2010) Selective neuronal vulnerability to oxidative stress in the brain Front. Aging Neurosci. 2, 12
8. Feng, Y. and Wang, X. (2012) Antioxidant therapies for Alzheimer's disease Oxid. Med. Cell. Longevity 2012, 472932
9. Basli, A., Soulet, S., Chaher, N., Merillon, J. M., Chibane, M., Monti, J. P., and Richard, T. (2012) Wine polyphenols: potential agents in neuroprotection Oxid. Med. Cell. Longevity 2012, 805762
10. Kaspar, J. W., Niture, S. K., and Jaiswal, A. K. (2009) Nrf2:INrf2 (Keap1) signaling in oxidative stress Free Radicals Biol. Med. 47, 1304-1309
11. Joshi, G. and Johnson, J. A. (2012) The Nrf2-ARE pathway: a valuable therapeutic target for the treatment of neurodegenerative diseases Recent Pat. CNS Drug Discovery 7, 218-229
12. Shih, A. Y., Imbeault, S., Barakauskas, V., Erb, H., Jiang, L., Li, P., and Murphy, T. H. (2005) Induction of the Nrf2-driven antioxidant response confers neuroprotection during mitochondrial stress in vivo J. Biol. Chem. 280, 22925-22936
13. Ramsey, C. P., Glass, C. A., Montgomery, M. B., Lindl, K. A., Ritson, G. P., Chia, L. A., Hamilton, R. L., Chu, C. T., and Jordan-Sciutto, K. L. (2007) Expression of Nrf2 in neurodegenerative diseases J. Neuropathol. Exp. Neurol. 66, 75-85
14. Rateb, M. E., Houssen, W. E., Harrison, W. T., Deng, H., Okoro, C. K., Asenjo, J. A., Andrews, B. A., Bull, A. T., Goodfellow, M., Ebel, R., and Jaspars, M. (2011) Diverse metabolic profiles of a Streptomyces strain isolated from a hyper-arid environment J. Nat. Prod. 74, 1965-1971
15. Allenby, N. E., Laing, E., Bucca, G., Kierzek, A. M., and Smith, C. P. (2012) Diverse control of metabolism and other cellular processes in Streptomyces coelicolor by the PhoP transcription factor: genome-wide identification of in vivo targets Nucleic Acids Res. 40, 9543-9556
16. Yamanaka, K., Oikawa, H., Ogawa, H. O., Hosono, K., Shinmachi, F., Takano, H., Sakuda, S., Beppu, T., and Ueda, K. (2005) Desferrioxamine E produced by Streptomyces griseus stimulates growth and development of Streptomyces tanashiensis Microbiology 151, 2899-2905
17. Zhang, H., Wang, Y., and Pfeifer, B. A. (2008) Bacterial hosts for natural product production Mol. Pharmaceutics 5, 212-225
18. Hong, K., Gao, A. H., Xie, Q. Y., Gao, H., Zhuang, L., Lin, H. P., Yu, H. P., Li, J., Yao, X. S., Goodfellow, M., and Ruan, J. S. (2009) Actinomycetes for marine drug discovery isolated from mangrove soils and plants in China Mar. Drugs 7, 24-44
19. Kim, W. G., Ryoo, I. J., Park, J. S., and Yoo, I. D. (2001) Benzastatins H and I, new benzastatin derivatives with neuronal cell protecting activity from Streptomyces nitrosporeus J. Antibiot. 54, 513-516
20. Sunazuka, T., Hirose, T., and Omura, S. (2008) Efficient total synthesis of novel bioactive microbial metabolites Acc. Chem. Res. 41, 302-314
21. Tadtong, S., Meksuriyen, D., Tanasupawat, S., Isobe, M., and Suwanborirux, K. (2007) Geldanamycin derivatives and neuroprotective effect on cultured P19-derived neurons Bioorg. Med. Chem. Lett. 17, 2939-2943
22. Varming, T., Drejer, J., Frandsen, A., and Schousboe, A. (1996) Characterization of a chemical anoxia model in cerebellar granule neurons using sodium azide: protection by nifedipine and MK-801 J. Neurosci. Res. 44, 40-46
23. Liu, R., Cui, C. B., Duan, L., Gu, Q. Q., and Zhu, W. M. (2005) Potent in vitro anticancer activity of metacycloprodigiosin and undecylprodigiosin from a sponge-derived actinomycete Saccharopolyspora sp. nov Arch. Pharm. Res. 28, 1341-1344
24. Triana-Vidal, L. E. and Carvajal-Varona, S. M. (2013) Protective Effect of Galantamine Against Oxidative Damage Using Human Lymphocytes: A Novel In Vitro Model Arch. Med. Res. 44, 85-92
25. Lobner, D. (2000) Comparison of the LDH and MTT assays for quantifying cell death: validity for neuronal apoptosis? J. Neurosci. Methods 96, 147-152
26. Mytilineou, C., Kramer, B. C., and Yabut, J. A. (2002) Glutathione depletion and oxidative stress Parkinsonism Relat. Disord. 8, 385-387
27. Aoyama, K., Watabe, M., and Nakaki, T. (2008) Regulation of neuronal glutathione synthesis J. Pharmacol. Sci. 108, 227-238
28. Zampagni, M., Wright, D., Cascella, R., D'Adamio, G., Casamenti, F., Evangelisti, E., Cardona, F., Goti, A., Nacmias, B., Sorbi, S., Liguri, G., and Cecchi, C. (2012) Novel S-acyl glutathione derivatives prevent amyloid oxidative stress and cholinergic dysfunction in Alzheimer disease models Free Radicals Biol. Med. 52, 1362-1371
29. Armogida, M., Nistico, R., and Mercuri, N. B. (2012) Therapeutic potential of targeting hydrogen peroxide metabolism in the treatment of brain ischaemia Br. J. Pharmacol. 166, 1211-1224
30. Calkins, M. J., Johnson, D. A., Townsend, J. A., Vargas, M. R., Dowell, J. A., Williamson, T. P., Kraft, A. D., Lee, J. M., Li, J., and Johnson, J. A. (2009) The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease Antioxid. Redox Signaling 11, 497-508
31. Friel, D. D. (2000) Mitochondria as regulators of stimulus-evoked calcium signals in neurons Cell Calcium 28, 307-316
32. Potterat, J. J., Woodhouse, D. E., Rothenberg, R. B., Muth, S. Q., Darrow, W. W., Muth, J. B., and Reynolds, J. U. (1993) AIDS in Colorado Springs: is there an epidemic? AIDS 7, 1517-1521
33. Bakowski, D. and Parekh, A. B. (2002) Permeation through store-operated CRAC channels in divalent-free solution: potential problems and implications for putative CRAC channel genes Cell Calcium 32, 379-391
34. Kajta, M., Trotter, A., Lason, W., and Beyer, C. (2006) Impact of 17beta-estradiol on cytokine-mediated apoptotic effects in primary hippocampal and neocortical cell cultures Brain Res. 1116, 64-74
35. Rateb, M. E., Houssen, W. E., Arnold, M., Abdelrahman, M. H., Deng, H., Harrison, W. T., Okoro, C. K., Asenjo, J. A., Andrews, B. A., Ferguson, G., Bull, A. T., Goodfellow, M., Ebel, R., and Jaspars, M. (2011) Chaxamycins A-D, bioactive ansamycins from a hyper-arid desert Streptomyces sp J. Nat. Prod. 74, 1491-1499
36. Zhao, G., Yao-Yue, C., Qin, G. W., and Guo, L. H. (2012) Luteolin from Purple Perilla mitigates ROS insult particularly in primary neurons Neurobiol. Aging 33, 176-186
37. Pasciu, V., Posadino, A. M., Cossu, A., Sanna, B., Tadolini, B., Gaspa, L., Marchisio, A., Dessole, S., Capobianco, G., and Pintus, G. (2010) Akt downregulation by flavin oxidase-induced ROS generation mediates dose-dependent endothelial cell damage elicited by natural antioxidants Toxicol. Sci. 114, 101-112
38. Williams, R. J. and Spencer, J. P. (2012) Flavonoids, cognition, and dementia: actions, mechanisms, and potential therapeutic utility for Alzheimer disease Free Radicals Biol. Med. 52, 35-45
39. Jiang, F., Li, W., Huang, Y., Chen, Y., Jin, B., Chen, N., Ding, Z., and Ding, X. (2013) Antioxidant, antityrosinase and antitumor activity comparison: the potential utilization of fibrous root part of Bletilla striata (Thunb.) Reichb.f PLoS One 8, e58004
40. Kalinovskaya, N. I., Romanenko, L. A., Irisawa, T., Ermakova, S. P., and Kalinovsky, A. I. (2011) Marine isolate Citricoccus sp. KMM 3890 as a source of a cyclic siderophore nocardamine with antitumor activity Microbiol. Res. 166, 654-661
41. Moore, B. S., Kalaitzis, J. A., and Xiang, L. (2005) Exploiting marine actinomycete biosynthetic pathways for drug discovery Antonie Van Leeuwenhoek 87, 49-57
42. Montaner, B. and Perez-Tomas, R. (2003) The prodigiosins: a new family of anticancer drugs Curr. Cancer Drug Targets 3, 57-65
43. Stankovic, N., Radulovic, V., Petkovic, M., Vuckovic, I., Jadranin, M., Vasiljevic, B., and Nikodinovic-Runic, J. (2012) Streptomyces sp. JS520 produces exceptionally high quantities of undecylprodigiosin with antibacterial, antioxidative, and UV-protective properties Appl. Microbiol. Biotechnol. 96, 1217-1231
44. Potterat, O., Zahner, H., Volkmann, C., and Zeeck, A. (1993) Metabolic products of microorganisms. 264. Exfoliamycin and related metabolites, new naphthoquinone antibiotics from Streptomyces exfoliatus J. Antibiot. 46, 346-349
45. Huh, J. E., Yim, J. H., Lee, H. K., Moon, E. Y., Rhee, D. K., and Pyo, S. (2007) Prodigiosin isolated from Hahella chejuensis suppresses lipopolysaccharide-induced NO production by inhibiting p38 MAPK, JNK and NF-kappaB activation in murine peritoneal macrophages Int. Immunopharmacol. 7, 1825-1833
46. Munoz, L. and Ammit, A. J. (2010) Targeting p38 MAPK pathway for the treatment of Alzheimer's disease Neuropharmacology 58, 561-568
47. Eftekharzadeh, B., Hamedi, J., Mohammadipanah, F., Khodagholi, F., Maghsoudi, N., and Klenk, H. P. (2010) Inhibition of oxidative stress-induced amyloid beta formation in NT2 neurons by culture filtrate of a strain of Streptomyces antibioticus Appl. Microbiol. Biotechnol. 86, 1805-1811
48. Shindo, K. and Kawai, H. (1992) A novel antibiotic, naphthopyranomycin J. Antibiot. 45, 584-586
49. Sitachitta, N., Gadepalli, M., and Davidson, B. S. (1996) New α-pyrone-containing metabolites from a marine-derived actinomycete Tetrahedron 52, 8073-8080
50. Lee, H. S., Shin, H. J., Jang, K. H., Kim, T. S., Oh, K. B., and Shin, J. (2005) Cyclic peptides of the nocardamine class from a marine-derived bacterium of the genus Streptomyces J. Nat. Prod. 68, 623-625
51. Vale, C., Alonso, E., Rubiolo, J. A., Vieytes, M. R., LaFerla, F. M., Gimenez-Llort, L., and Botana, L. M. (2010) Profile for amyloid-beta and tau expression in primary cortical cultures from 3xTg-AD mice Cell. Mol. Neurobiol 30, 577-590
52. Alonso, E., Vale, C., Vieytes, M. R., Laferla, F. M., Gimenez-Llort, L., and Botana, L. M. (2011) 13-Desmethyl spirolide-C is neuroprotective and reduces intracellular Abeta and hyperphosphorylated tau in vitro Neurochem. Int. 59, 1056-1065
53. Alonso, E., Vale, C., Vieytes, M. R., Laferla, F. M., Gimenez-Llort, L., and Botana, L. M. (2011) The cholinergic antagonist gymnodimine improves Abeta and tau neuropathology in an in vitro model of Alzheimer disease Cell. Physiol. Biochem. 27, 783-794
54. White, M. G., Wang, Y., Akay, C., Lindl, K. A., Kolson, D. L., and Jordan-Sciutto, K. L. (2011) Parallel high throughput neuronal toxicity assays demonstrate uncoupling between loss of mitochondrial membrane potential and neuronal damage in a model of HIV-induced neurodegeneration Neurosci. Res. 70, 220-229
55. Kim, E. J., Kwon, K. J., Park, J. Y., Lee, S. H., Moon, C. H., and Baik, E. J. (2002) Neuroprotective effects of prostaglandin E2 or cAMP against microglial and neuronal free radical mediated toxicity associated with inflammation J. Neurosci. Res. 70, 97-107