Marine cyanobacteria compounds with anticancer properties: A review on the implication of apoptosis

Marine Drugs

Volumn 10, Issue 10, 2012, Pages 2181-2207

  Costa, Margarida ^a   Costa Rodrigues, João ^b   Fernandes, Maria Helena ^b   Barros, Piedade ^c   Vasconcelos, Vitor ^a,d   Martins, Rosário ^a,c,e  

^a UNIVERSITY OF PORTO   (Portugal)

^b U Porto   (Portugal)

^c POLYTECHNIC INSTITUTE OF PORTO   (Portugal)

^d UNIVERSITY OF PORTO   (Portugal)

^e UNIVERSITY OF PORTO   (Portugal)

Author keywords

Apoptosis; Cancer; Marine cyanobacteria; Natural compounds

Indexed keywords

EID: 84868218952     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md10102181     Document Type: Review

References (137)

1. Tsygankov, A.A. Nitrogen-Fixing cyanobacteria: Producents of hydrogen. Prikl. Biokhim. Mikrobiol. 2007, 43, 279-288.
2. Carmichael, W.W. Cyanobacteria secondary metabolites - the cyanotoxins. J. Appl. Bacteriol. 1992, 72, 445-459.
3. Codd, G.A.; Morrison, L.F.; Metcalf, J.S. Cyanobacterial toxins: Risk management for health protection. Toxicol. Appl. Pharmacol. 2005, 203, 264-272.
4. Blaha, L.; Babica, P.; Marsalek, B. Toxins produced in cyanobacterial water blooms - toxicity and risks. Interdiscip. Toxicol. 2009, 2, 36-41.
5. Singh, R.K.; Tiwari, S.P.; Rai, A.K.; Mohapatra, T.M. Cyanobacteria: An emerging source for drug discovery. J. Antibiot. (Tokyo) 2011, 64, 401-412.
6. Nunnery, J.K.; Mevers, E.; Gerwick, W.H. Biologically active secondary metabolites from marine cyanobacteria. Curr. Opin. Biotechnol. 2010, 21, 787-793.
7. Jones, A.C.; Monroe, E.A.; Eisman, E.B.; Gerwick, L.; Sherman, D.H.; Gerwick, W.H. The unique mechanistic transformations involved in the biosynthesis of modular natural products from marine cyanobacteria. Nat. Prod. Rep. 2010, 27, 1048-1065.
8. Simmons, T.L.; McPhail, K.L.; Ortega-Barria, E.; Mooberry, S.L.; Gerwick, W.H. Belamide A, a new antimitotic tetrapeptide from a Panamanian marine cyanobacterium. Tetrahedron Lett. 2006, 47, 3387-3390.
9. Sisay, M.T.; Hautmann, S.; Mehner, C.; Konig, G.M.; Bajorath, J.; Gutschow, M. Inhibition of human leukocyte elastase by brunsvicamides A-C: Cyanobacterial cyclic peptides. ChemMedChem 2009, 4, 1425-1429.
10. Nogle, L.M.; Okino, T.; Gerwick, W.H. Antillatoxin B, a neurotoxic lipopeptide from the marine cyanobacterium Lyngbya majuscula. J. Nat. Prod. 2001, 64, 983-985.
11. Han, B.; Goeger, D.; Maier, C.S.; Gerwick, W.H. The wewakpeptins, cyclic depsipeptides from a Papua New Guinea collection of the marine cyanobacterium Lyngbya semiplena. J. Org. Chem. 2005, 70, 3133-3139.
12. Soria-Mercado, I.E.; Pereira, A.; Cao, Z.; Murray, T.F.; Gerwick, W.H. Alotamide A, a novel neuropharmacological agent from the marine cyanobacterium Lyngbya bouillonii. Org. Lett. 2009, 11, 4704-4707.
13. Chang, T.T.; More, S.V.; Lu, I.H.; Hsu, J.C.; Chen, T.J.; Jen, Y.C.; Lu, C.K.; Li, W.S. Isomalyngamide A, A-1 and their analogs suppress cancer cell migration in vitro. Eur. J. Med. Chem. 2011, 46, 3810-3819.
14. Andrianasolo, E.H.; Gross, H.; Goeger, D.; Musafija-Girt, M.; McPhail, K.; Leal, R.M.; Mooberry, S.L.; Gerwick, W.H. Isolation of swinholide A and related glycosylated derivatives from two field collections of marine cyanobacteria. Org. Lett. 2005, 7, 1375-1378.
15. Teruya, T.; Sasaki, H.; Kitamura, K.; Nakayama, T.; Suenaga, K. Biselyngbyaside, a macrolide glycoside from the marine cyanobacterium Lyngbya sp. Org. Lett. 2009, 11, 2421-2424.
16. Salvador, L.A.; Paul, V.J.; Luesch, H. Caylobolide B, a macrolactone from symplostatin 1-producing marine cyanobacteria Phormidium spp. from Florida. J. Nat. Prod. 2010, 73, 1606-1609.
17. Montaser, R.; Paul, V.J.; Luesch, H. Pitipeptolides C-F, antimycobacterial cyclodepsipeptides from the marine cyanobacterium Lyngbya majuscula from Guam. Phytochemistry 2011, 72, 2068-2074.
18. Marquez, B.L.; Watts, K.S.; Yokochi, A.; Roberts, M.A.; Verdier-Pinard, P.; Jimenez, J.I.; Hamel, E.; Scheuer, P.J.; Gerwick, W.H. Structure and absolute stereochemistry of hectochlorin, a potent stimulator of actin assembly. J. Nat. Prod. 2002, 65, 866-871.
19. Milligan, K.E.; Marquez, B.L.; Williamson, R.T.; Gerwick, W.H. Lyngbyabellin B, a toxic and antifungal secondary metabolite from the marine cyanobacterium Lyngbya majuscula. J. Nat. Prod. 2000, 63, 1440-1443.
20. Tripathi, A.; Puddick, J.; Prinsep, M.R.; Rottmann, M.; Tan, L.T. Lagunamides A and B: Cytotoxic and antimalarial cyclodepsipeptides from the marine cyanobacterium Lyngbya majuscula. J. Nat. Prod. 2010, 73, 1810-1814.
21. Capper, A.; Cruz-Rivera, E.; Paul, V.; Tibbetts, I. Chemical deterrence of a marine cyanobacterium against sympatric and non-sympatric consumers. Hydrobiologia 2006, 553, 319-326.
22. Tan, L.T.; Goh, B.P. Chemical ecology of marine cyanobacterial secondary metabolites: A mini-review. J. Coast. Dev. 2009, 13, 1-9.
23. Malloy, K.L.; Villa, F.A.; Engene, N.; Matainaho, T.; Gerwick, L.; Gerwick, W.H. Malyngamide 2, an oxidized lipopeptide with nitric oxide inhibiting activity from a Papua New Guinea marine cyanobacterium. J. Nat. Prod. 2011, 74, 95-98.
24. Han, B.; Gross, H.; Goeger, D.E.; Mooberry, S.L.; Gerwick, W.H. Aurilides B and C, cancer cell toxins from a Papua New Guinea collection of the marine cyanobacterium Lyngbya majuscula. J. Nat. Prod. 2006, 69, 572-575.
25. Mooberry, S.L.; Leal, R.M.; Tinley, T.L.; Luesch, H.; Moore, R.E.; Corbett, T.H. The molecular pharmacology of symplostatin 1: A new antimitotic dolastatin 10 analog. Int. J. Cancer 2003, 104, 512-521.
26. Gutierrez, M.; Suyama, T.L.; Engene, N.; Wingerd, J.S.; Matainaho, T.; Gerwick, W.H. Apratoxin D, a potent cytotoxic cyclodepsipeptide from papua new guinea collections of the marine cyanobacteria Lyngbya majuscula and Lyngbya sordida. J. Nat. Prod. 2008, 71, 1099-1103.
27. Linington, R.G.; Edwards, D.J.; Shuman, C.F.; McPhail, K.L.; Matainaho, T.; Gerwick, W.H. Symplocamide A, a potent cytotoxin and chymotrypsin inhibitor from the marine cyanobacterium Symploca sp. J. Nat. Prod. 2008, 71, 22-27.
28. Ulukaya, E.; Acilan, C.; Yilmaz, Y. Apoptosis: Why and how does it occur in biology? Cell Biochem. Funct. 2011, 29, 468-480.
29. Han, S.I.; Kim, Y.S.; Kim, T.H. Role of apoptotic and necrotic cell death under physiologic conditions. BMB Rep. 2008, 41, 1-10.
30. Kim, M.K.; Suh, D.H.; Seoung, J.; Kim, H.S.; Chung, H.H.; Song, Y.S. Autophagy as a target for anticancer therapy and its modulation by phytochemicals. J. Food Drug Anal. 2012, 20, 241-245.
31. Zhang, J.Y. Apoptosis-Based anticancer drugs. Nat. Rev. Drug Discov. 2002, 1, 101-102.
32. Fischer, U.; Schulze-Osthoff, K. Apoptosis-Based therapies and drug targets. Cell Death Differ. 2005, 12, 942-961.
33. Chen, D.; Daniel, K.G.; Chen, M.S.; Kuhn, D.J.; Landis-Piwowar, K.R.; Dou, Q.P. Dietary flavonoids as proteasome inhibitors and apoptosis inducers in human leukemia cells. Biochem. Pharmacol. 2005, 69, 1421-1432.
34. Mao, Y.B.; Song, G.; Cai, Q.F.; Liu, M.; Luo, H.H.; Shi, M.X.; Ouyang, G.; Bao, S.D. Hydrogen peroxide-induced apoptosis in human gastric carcinoma MGC803 cells. Cell Biol. Int. 2006, 30, 332-337.
35. Lytvyn, D.I.; Yemets, A.I.; Blume, Y.B. UV-B overexposure induces programmed cell death in a BY-2 tobacco cell line. Environ. Exp. Bot. 2010, 68, 51-57.
36. Elmore, S. Apoptosis: A review of programmed cell death. Toxicol. Pathol. 2007, 35, 495-516.
37. Martins, R.F.; Ramos, M.F.; Herfindal, L.; Sousa, J.A.; Skaerven, K.; Vasconcelos, V.M. Antimicrobial and cytotoxic assessment of marine cyanobacteria - Synechocystis and Synechococcus. Mar. Drugs 2008, 6, 1-11.
38. Yonezawa, T.; Mase, N.; Sasaki, H.; Teruya, T.; Hasegawa, S.; Cha, B.Y.; Yagasaki, K.; Suenaga, K.; Nagai, K.; Woo, J.T. Biselyngbyaside, isolated from marine cyanobacteria, inhibits osteoclastogenesis and induces apoptosis in mature osteoclasts. J. Cell Biochem. 2012, 113, 440-448.
39. Oftedal, L.; Selheim, F.; Wahlsten, M.; Sivonen, K.; Doskeland, S.O.; Herfindal, L. Marine benthic cyanobacteria contain apoptosis-inducing activity synergizing with daunorubicin to kill leukemia cells, but not cardiomyocytes. Mar. Drugs 2010, 8, 2659-2672.
40. Luesch, H.; Yoshida, W.Y.; Moore, R.E.; Paul, V.J. New apratoxins of marine cyanobacterial origin from Guam and Palau. Bioorg. Med. Chem. 2002, 10, 1973-1978.
41. Luesch, H.; Yoshida, W.Y.; Moore, R.E.; Paul, V.J.; Corbett, T.H. Total structure determination of apratoxin A, a potent novel cytotoxin from the marine cyanobacterium Lyngbya majuscula. J. Am. Chem. Soc. 2001, 123, 5418-5423.
42. Matthew, S.; Schupp, P.J.; Luesch, H. Apratoxin E, a cytotoxic peptolide from a guamanian collection of the marine cyanobacterium Lyngbya bouillonii. J. Nat. Prod. 2008, 71, 1113-1116.
43. Tidgewell, K.; Engene, N.; Byrum, T.; Media, J.; Doi, T.; Valeriote, F.A.; Gerwick, W.H. Evolved diversification of a modular natural product pathway: Apratoxins F and G, two cytotoxic cyclic depsipeptides from a Palmyra collection of Lyngbya bouillonii. ChemBioChem 2010, 11, 1458-1466.
44. Teruya, T.; Sasaki, H.; Fukazawa, H.; Suenaga, K. Bisebromoamide, a potent cytotoxic peptide from the marine cyanobacterium Lyngbya sp.: isolation, stereostructure, and biological activity. Org. Lett. 2009, 11, 5062-5065.
45. Chen, X.X.; Smith, G.D.; Waring, P. Human cancer cell (Jurkat) killing by the cyanobacterial metabolite calothrixin A. J. Appl. Phycol. 2003, 15, 269-277.
46. Khan, Q.A.; Lu, J.; Hecht, S.M. Calothrixins, a new class of human DNA topoisomerase I poisons. J. Nat. Prod. 2009, 72, 438-442.
47. Bernardo, P.H.; Chai, C.L.; Le Guen, M.; Smith, G.D.; Waring, P. Structure-Activity delineation of quinones related to the biologically active Calothrixin B. Bioorg. Med. Chem. Lett. 2007, 17, 82-85.
48. MacMillan, J.B.; Molinski, T.F. Caylobolide A, a unique 36-membered macrolactone from a Bahamian Lyngbya majuscula. Org. Lett. 2002, 4, 1535-1538.
49. Medina, R.A.; Goeger, D.E.; Hills, P.; Mooberry, S.L.; Huang, N.; Romero, L.I.; Ortega-Barria, E.; Gerwick, W.H.; McPhail, K.L. Coibamide A, a potent antiproliferative cyclic depsipeptide from the Panamanian marine cyanobacterium Leptolyngbya sp. J. Am. Chem. Soc. 2008, 130, 6324-6325.
50. Mooberry, S.L.; Busquets, L.; Tien, G. Induction of apoptosis by cryptophycin 1, a new antimicrotubule agent. Int. J. Cancer 1997, 73, 440-448.
51. Wagner, M.M.; Paul, D.C.; Shih, C.; Jordan, M.A.; Wilson, L.; Williams, D.C. In vitro pharmacology of cryptophycin 52 (LY355703) in human tumor cell lines. Cancer Chemother. Pharmacol. 1999, 43, 115-125.
52. Catassi, A.; Cesario, A.; Arzani, D.; Menichini, P.; Alama, A.; Bruzzo, C.; Imperatori, A.; Rotolo, N.; Granone, P.; Russo, P. Characterization of apoptosis induced by marine natural products in non small cell lung cancer A549 cells. Cell. Mol. Life Sci. 2006, 63, 2377-2386.
53. Kalemkerian, G.P.; Ou, X.L.; Adil, M.R.; Rosati, R.; Khoulani, M.M.; Madan, S.K.; Pettit, G.R. Activity of dolastatin 10 against small-cell lung cancer in vitro and in vivo: Induction of apoptosis and bcl-2 modification. Cancer Chemother. Pharm. 1999, 43, 507-515.
54. Turner, T.; Jackson, W.H.; Pettit, G.R.; Wells, A.; Kraft, A.S. Treatment of human prostate cancer cells with dolastatin 10, a peptide isolated from a marine shell-less mollusc. Prostate 1998, 34, 175-181.
55. Beckwith, M.; Urba, W.J.; Longo, D.L. Growth inhibition of human lymphoma cell lines by the marine products, dolastatins 10 and 15. J. Natl. Cancer Inst. 1993, 85, 483-488.
56. Wall, N.R.; Mohammad, R.M.; Al-Katib, A.M. Bax:Bcl-2 ratio modulation by bryostatin 1 and novel antitubulin agents is important for susceptibility to drug induced apoptosis in the human early pre-B acute lymphoblastic leukemia cell line, Reh. Leuk. Res. 1999, 23, 881-888.
57. Jimenez, J.I.; Scheuer, P.J. New lipopeptides from the Caribbean cyanobacterium Lyngbya majuscula. J. Nat. Prod. 2001, 64, 200-203.
58. Engene, N.; Choi, H.; Esquenazi, E.; Byrum, T.; Villa, F.A.; Cao, Z.; Murray, T.F.; Dorrestein, P.C.; Gerwick, L.; Gerwick, W.H. Phylogeny-Guided isolation of ethyl tumonoate A from the marine cyanobacterium cf. Oscillatoria margaritifera. J. Nat. Prod. 2011, 74, 1737-1743.
59. Choi, H.; Pereira, A.R.; Cao, Z.; Shuman, C.F.; Engene, N.; Byrum, T.; Matainaho, T.; Murray, T.F.; Mangoni, A.; Gerwick, W.H. The hoiamides, structurally intriguing neurotoxic lipopeptides from Papua New Guinea marine cyanobacteria. J. Nat. Prod. 2010, 73, 1411-1421.
60. Davies-Coleman, M.T.; Dzeha, T.M.; Gray, C.A.; Hess, S.; Pannell, L.K.; Hendricks, D.T.; Arendse, C.E. Isolation of homodolastatin 16, a new cyclic depsipeptide from a Kenyan collection of Lyngbya majuscula. J. Nat. Prod. 2003, 66, 712-715.
61. Edwards, D.J.; Marquez, B.L.; Nogle, L.M.; McPhail, K.; Goeger, D.E.; Roberts, M.A.; Gerwick, W.H. Structure and biosynthesis of the jamaicamides, new mixed polyketide-peptide neurotoxins from the marine cyanobacterium Lyngbya majuscula. Chem. Biol. 2004, 11, 817-833.
62. White, J.D.; Xu, Q.; Lee, C.S.; Valeriote, F.A. Total synthesis and biological evaluation of (+)-kalkitoxin, a cytotoxic metabolite of the cyanobacterium Lyngbya majuscula. Org. Biomol. Chem. 2004, 2, 2092-2102.
63. Tripathi, A.; Puddick, J.; Prinsep, M.R.; Rottmann, M.; Chan, K.P.; Chen, D.Y.; Tan, L.T. Lagunamide C, a cytotoxic cyclodepsipeptide from the marine cyanobacterium Lyngbya majuscula. Phytochemistry 2011, 72, 2369-2375.
64. Taori, K.; Paul, V.J.; Luesch, H. Structure and activity of largazole, a potent antiproliferative agent from the Floridian marine cyanobacterium Symploca sp. J. Am. Chem. Soc. 2008, 130, 1806-1807.
65. Zeng, X.; Yin, B.; Hu, Z.; Liao, C.; Liu, J.; Li, S.; Li, Z.; Nicklaus, M.C.; Zhou, G.; Jiang, S. Total synthesis and biological evaluation of largazole and derivatives with promising selectivity for cancers cells. Org. Lett. 2010, 12, 1368-1371.
66. Luesch, H.; Yoshida, W.Y.; Moore, R.E.; Paul, V.J.; Mooberry, S.L. Isolation, structure determination, and biological activity of Lyngbyabellin A from the marine cyanobacterium Lyngbya majuscula. J. Nat. Prod. 2000, 63, 611-615.
67. Luesch, H.; Yoshida, W.Y.; Harrigan, G.G.; Doom, J.P.; Moore, R.E.; Paul, V.J. Lyngbyaloside B, a new glycoside macrolide from a Palauan marine cyanobacterium, Lyngbya sp. J. Nat. Prod. 2002, 65, 1945-1948.
68. Pettit, G.R.; Hogan, F.; Xu, J.P.; Tan, R.; Nogawa, T.; Cichacz, Z.; Pettit, R.K.; Du, J.; Ye, Q.H.; Cragg, G.M.; et al. Antineoplastic agents. 536. New sources of naturally occurring cancer cell growth inhibitors from marine organisms, terrestrial plants, and microorganisms (1a,). J. Nat. Prod. 2008, 71, 438-444.
69. Horgen, F.D.; Kazmierski, E.B.; Westenburg, H.E.; Yoshida, W.Y.; Scheuer, P.J. Malevamide D: Isolation and structure determination of an isodolastatin H analogue from the marine cyanobacterium Symploca hydnoides. J. Nat. Prod. 2002, 65, 487-491.
70. Gross, H.; McPhail, K.L.; Goeger, D.E.; Valeriote, F.A.; Gerwick, W.H. Two cytotoxic stereoisomers of malyngamide C, 8-epi-malyngamide C and 8-O-acetyl-8-epi-malyngamide C, from the marine cyanobacterium Lyngbya majuscula. Phytochemistry 2010, 71, 1729-1735.
71. Gutierrez, M.; Tidgewell, K.; Capson, T.L.; Engene, N.; Almanza, A.; Schemies, J.; Jung, M.; Gerwick, W.H. Malyngolide dimer, a bioactive symmetric cyclodepside from the panamanian marine cyanobacterium Lyngbya majuscula. J. Nat. Prod. 2010, 73, 709-711.
72. Golakoti, T.; Yoshida, W.Y.; Chaganty, S.; Moore, R.E. Isolation and structure determination of nostocyclopeptides A1 and A2 from the terrestrial cyanobacterium Nostoc sp. ATCC53789. J. Nat. Prod. 2001, 64, 54-59.
73. Williams, P.G.; Yoshida, W.Y.; Moore, R.E.; Paul, V.J. Isolation and structure determination of obyanamide, a novel cytotoxic cyclic depsipeptide from the marine cyanobacterium Lyngbya confervoides. J. Nat. Prod. 2002, 65, 29-31.
74. Zou, B.; Long, K.; Ma, D.W. Total synthesis and cytotoxicity studies of a cyclic depsipeptide with proposed structure of palau'amide. Org. Lett. 2005, 7, 4237-4240.
75. Williams, P.G.; Yoshida, W.Y.; Quon, M.K.; Moore, R.E.; Paul, V.J. The structure of Palau'amide, a potent cytotoxin from a species of the marine cyanobacterium Lyngbya. J. Nat. Prod. 2003, 66, 1545-1549.
76. Taniguchi, M.; Nunnery, J.K.; Engene, N.; Esquenazi, E.; Byrum, T.; Dorrestein, P.C.; Gerwick, W.H. Palmyramide A, a cyclic depsipeptide from a Palmyra Atoll collection of the marine cyanobacterium Lyngbya majuscula. J. Nat. Prod. 2010, 73, 393-398.
77. Luesch, H.; Pangilinan, R.; Yoshida, W.Y.; Moore, R.E.; Paul, V.J. Pitipeptolides A and B, new cyclodepsipeptides from the marine cyanobacterium Lyngbya majuscula. J. Nat. Prod. 2001, 64, 304-307.
78. Montaser, R.; Abboud, K.A.; Paul, V.J.; Luesch, H. Pitiprolamide, a proline-rich dolastatin 16 analogue from the marine cyanobacterium Lyngbya majuscula from Guam. J. Nat. Prod. 2011, 74, 109-112.
79. Wrasidlo, W.; Mielgo, A.; Torres, V.A.; Barbero, S.; Stoletov, K.; Suyama, T.L.; Klemke, R.L.; Gerwick, W.H.; Carson, D.A.; Stupack, D.G. The marine lipopeptide somocystinamide A triggers apoptosis via caspase 8. Proc. Natl. Acad. Sci. USA 2008, 105, 2313-2318.
80. Harrigan, G.G.; Luesch, H.; Yoshida, W.Y.; Moore, R.E.; Nagle, D.G.; Paul, V.J.; Mooberry, S.L.; Corbett, T.H.; Valeriote, F.A. Symplostatin 1: A dolastatin 10 analogue from the marine cyanobacterium Symploca hydnoides. J. Nat. Prod. 1998, 61, 1075-1077.
81. Williams, P.G.; Yoshida, W.Y.; Moore, R.E.; Paul, V.J. Tasiamide, a cytotoxic peptide from the marine cyanobacterium Symploca sp. J. Nat. Prod. 2002, 65, 1336-1339.
82. 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.
83. Williams, P.G.; Yoshida, W.Y.; Moore, R.E.; Paul, V.J. Tasipeptins A and B: New cytotoxic depsipeptides from the marine cyanobacterium Symploca sp. J. Nat. Prod. 2003, 66, 620-624.
84. Williams, P.G.; Yoshida, W.Y.; Quon, M.K.; Moore, R.E.; Paul, V.J. Ulongapeptin, a cytotoxic cyclic depsipeptide from a Palauan marine cyanobacterium Lyngbya sp. J. Nat. Prod. 2003, 66, 651-654.
85. Mevers, E.; Liu, W.T.; Engene, N.; Mohimani, H.; Byrum, T.; Pevzner, P.A.; Dorrestein, P.C.; Spadafora, C.; Gerwick, W.H. Cytotoxic veraguamides, alkynyl bromide-containing cyclic depsipeptides from the marine cyanobacterium cf. Oscillatoria margaritifera. J. Nat. Prod. 2011, 74, 928-936.
86. Li, W.I.; Berman, F.W.; Okino, T.; Yokokawa, F.; Shioiri, T.; Gerwick, W.H.; Murray, T.F. Antillatoxin is a marine cyanobacterial toxin that potently activates voltage-gated sodium channels. Proc. Natl. Acad. Sci. USA 2001, 98, 7599-7604.
87. Cao, Z.; Gerwick, W.H.; Murray, T.F. Antillatoxin is a sodium channel activator that displays unique efficacy in heterologously expressed rNav1.2, rNav1.4 and rNav1.5 alpha subunits. BMC Neurosci. 2010, 11, 154.
88. Ma, D.; Zou, B.; Cai, G.; Hu, X.; Liu, J.O. Total synthesis of the cyclodepsipeptide apratoxin A and its analogues and assessment of their biological activities. Chemistry 2006, 12, 7615-7626.
89. Liu, Y.; Law, B.K.; Luesch, H. Apratoxin a reversibly inhibits the secretory pathway by preventing cotranslational translocation. Mol. Pharmacol. 2009, 76, 91-104.
90. Sumiya, E.; Shimogawa, H.; Sasaki, H.; Tsutsumi, M.; Yoshita, K.; Ojika, M.; Suenaga, K.; Uesugi, M. Cell-Morphology profiling of a natural product library identifies bisebromoamide and miuraenamide A as actin filament stabilizers. ACS Chem. Biol. 2011, 6, 425-431.
91. Rubio, B.K.; Parrish, S.M.; Yoshida, W.; Schupp, P.J.; Schils, T.; Williams, P.G. Depsipeptides from a Guamanian Marine Cyanobacterium, Lyngbya bouillonii, with selective inhibition of serine proteases. Tetrahedron Lett. 2010, 51, 6718-6721.
92. Gerwick, W.H.; Proteau, P.J.; Nagle, D.G.; Hamel, E.; Blokhin, A.V.; Slate, D.L. Structure of Curacin A, a novel antimitotic, antiproliferative, and brine shrimp toxic natural product from the Marine Cyanobacterium Lyngbya majuscula. J. Org. Chem. 1994, 59, 1243-1245.
93. Mitra, A.; Sept, D. Localization of the antimitotic peptide and depsipeptide binding site on beta-tubulin. Biochemistry 2004, 43, 13955-13962.
94. Harrigan, G.G.; Yoshida, W.Y.; Moore, R.E.; Nagle, D.G.; Park, P.U.; Biggs, J.; Paul, V.J.; Mooberry, S.L.; Corbett, T.H.; Valeriote, F.A. Isolation, structure determination, and biological activity of dolastatin 12 and lyngbyastatin 1 from Lyngbya majuscula/Schizothrix calcicola cyanobacterial assemblages. J. Nat. Prod. 1998, 61, 1221-1225.
95. Kwan, J.C.; Eksioglu, E.A.; Liu, C.; Paul, V.J.; Luesch, H. Grassystatins A-C from marine cyanobacteria, potent cathepsin E inhibitors that reduce antigen presentation. J. Med. Chem. 2009, 52, 5732-5747.
96. De Oliveira, E.O.; Graf, K.M.; Patel, M.K.; Baheti, A.; Kong, H.S.; MacArthur, L.H.; Dakshanamurthy, S.; Wang, K.; Brown, M.L.; Paige, M. Synthesis and evaluation of hermitamides A and B as human voltage-gated sodium channel blockers. Bioorg. Med. Chem. 2011, 19, 4322-4329.
97. Pereira, A.; Cao, Z.; Murray, T.F.; Gerwick, W.H. Hoiamide a, a sodium channel activator of unusual architecture from a consortium of two papua new Guinea cyanobacteria. Chem. Biol. 2009, 16, 893-906.
98. LePage, K.T.; Goeger, D.; Yokokawa, F.; Asano, T.; Shioiri, T.; Gerwick, W.H.; Murray, T.F. The neurotoxic lipopeptide kalkitoxin interacts with voltage-sensitive sodium channels in cerebellar granule neurons. Toxicol. Lett. 2005, 158, 133-139.
99. 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. Prod. 2008, 71, 1625-1629.
100. Matthew, S.; Paul, V.J.; Luesch, H. Largamides A-C, tiglic acid-containing cyclodepsipeptides with elastase-inhibitory activity from the marine cyanobacterium Lyngbya confervoides. Planta Med. 2009, 75, 528-533.
101. Plaza, A.; Bewley, C.A. Largamides A-H, unusual cyclic peptides from the marine cyanobacterium Oscillatoria sp. J. Org. Chem. 2006, 71, 6898-6907.
102. Matthew, S.; Ross, C.; Rocca, J.R.; Paul, V.J.; Luesch, H. Lyngbyastatin 4, a dolastatin 13 analogue with elastase and chymotrypsin inhibitory activity from the marine cyanobacterium Lyngbya confervoides. J. Nat. Prod. 2007, 70, 124-127.
103. Taori, K.; Matthew, S.; Rocca, J.R.; Paul, V.J.; Luesch, H. Lyngbyastatins 5-7, potent elastase inhibitors from Floridian marine cyanobacteria, Lyngbya spp. J. Nat. Prod. 2007, 70, 1593-1600.
104. Kwan, J.C.; Taori, K.; 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.
105. Adams, B.; Porzgen, P.; Pittman, E.; Yoshida, W.Y.; Westenburg, H.E.; Horgen, F.D. Isolation and structure determination of malevamide E, a dolastatin 14 analogue, from the marine cyanobacterium Symploca laete-viridis. J. Nat. Prod. 2008, 71, 750-754.
106. Gunasekera, S.P.; Miller, M.W.; Kwan, J.C.; Luesch, H.; Paul, V.J. Molassamide, a depsipeptide serine protease inhibitor from the marine cyanobacterium Dichothrix utahensis. J. Nat. Prod. 2010, 73, 459-462.
107. Pereira, A.R.; Cao, Z.; Engene, N.; Soria-Mercado, I.E.; Murray, T.F.; Gerwick, W.H. Palmyrolide A, an unusually stabilized neuroactive macrolide from Palmyra Atoll cyanobacteria. Org. Lett. 2010, 12, 4490-4493.
108. Matthew, S.; Ross, C.; Paul, V.J.; Luesch, H. Pompanopeptins A and B, new cyclic peptides from the marine cyanobacterium Lyngbya confervoides. Tetrahedron 2008, 64, 4081-4089.
109. Luesch, H.; Moore, R.E.; Paul, V.J.; Mooberry, S.L.; Corbett, T.H. Isolation of dolastatin 10 from the marine cyanobacterium Symploca species VP642 and total stereochemistry and biological evaluation of its analogue symplostatin 1. J. Nat. Prod. 2001, 64, 907-910.
110. Luesch, H.; Yoshida, W.Y.; Moore, R.E.; Paul, V.J.; Mooberry, S.L.; Corbett, T.H. Symplostatin 3, a new dolastatin 10 analogue from the marine cyanobacterium Symploca sp. VP452. J. Nat. Prod. 2002, 65, 16-20.
111. Matthew, S.; Paul, V.J.; Luesch, H. Tiglicamides A-C, cyclodepsipeptides from the marine cyanobacterium Lyngbya confervoides. Phytochemistry 2009, 70, 2058-2063.
112. Tan, L.T. Filamentous tropical marine cyanobacteria: a rich source of natural products for anticancer drug discovery. J. Appl. Phycol. 2010, 22, 659-676.
113. Drew, L.; Fine, R.L.; Do, T.N.; Douglas, G.P.; Petrylak, D.P. The novel antimicrotubule agent cryptophycin 52 (LY355703) induces apoptosis via multiple pathways in human prostate cancer cells. Clin. Cancer Res. 2002, 8, 3922-3932.
114. Sato, M.; Sagawa, M.; Nakazato, T.; Ikeda, Y.; Kizaki, M. A natural peptide, dolastatin 15, induces G2/M cell cycle arrest and apoptosis of human multiple myeloma cells. Int. J. Oncol. 2007, 30, 1453-1459.
115. Nagarajan, M.; Maruthanayagam, V.; Sundararaman, M. A review of pharmacological and toxicological potentials of marine cyanobacterial metabolites. J. Appl. Toxicol. 2012, 32, 153-155.
116. Han, B.N.; McPhail, K.L.; Gross, H.; Goeger, D.E.; Mooberry, S.L.; Gerwick, W.H. Isolation and structure of five lyngbyabellin derivatives from a Papua New Guinea collection of the marine cyanobacterium Lyngbya majuscula. Tetrahedron 2005, 61, 11723-11729.
117. Paradies, G.; Petrosillo, G.; Paradies, V.; Ruggiero, F.M. Mitochondrial dysfunction in brain aging: role of oxidative stress and cardiolipin. Neurochem. Int. 2011, 58, 447-457.
118. Mammucari, C.; Rizzuto, R. Signaling pathways in mitochondrial dysfunction and aging. Mech. Ageing Dev. 2010, 131, 536-543.
119. Sato, S.; Murata, A.; Orihara, T.; Shirakawa, T.; Suenaga, K.; Kigoshi, H.; Uesugi, M. Marine natural product aurilide activates the OPA1-mediated apoptosis by binding to prohibitin. Chem. Biol. 2011, 18, 131-139.
120. Valko, M.; Leibfritz, D.; Moncol, J.; Cronin, M.T.; Mazur, M.; Telser, J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39, 44-84.
121. Blokhina, O.; Virolainen, E.; Fagerstedt, K.V. Antioxidants, oxidative damage and oxygen deprivation stress: A review. Ann. Bot. 2003, 91, 179-194.
122. Kelman, D.; Ben-Amotz, A.; Berman-Frank, I. Carotenoids provide the major antioxidant defence in the globally significant N2-fixing marine cyanobacterium Trichodesmium. Environ. Microbiol. 2009, 11, 1897-1908.
123. Patel, A.; Mishra, S.; Ghosh, P.K. Antioxidant potential of C-phycocyanin isolated from cyanobacterial species Lyngbya, Phormidium and Spirulina spp. Indian J. Biochem. Biophys. 2006, 43, 25-31.
124. Donepudi, M.; Grutter, M.G. Structure and zymogen activation of caspases. Biophys. Chem. 2002, 101, 145-153.
125. Fuentes-Prior, P.; Salvesen, G.S. The protein structures that shape caspase activity, specificity, activation and inhibition. Biochem. J. 2004, 384, 201-232.
126. Wilkinson, J.C.; Cepero, E.; Boise, L.H.; Duckett, C.S. Upstream regulatory role for XIAP in receptor-mediated apoptosis. Mol. Cell. Biol. 2004, 24, 7003-7014.
127. Okuno, S.; Shimizu, S.; Ito, T.; Nomura, M.; Hamada, E.; Tsujimoto, Y.; Matsuda, H. Bcl-2 prevents caspase-independent cell death. J. Biol. Chem. 1998, 273, 34272-34277.
128. Schrader, K.; Huai, J.; Jockel, L.; Oberle, C.; Borner, C. Non-Caspase proteases: Triggers or amplifiers of apoptosis? Cell. Mol. Life Sci. 2010, 67, 1607-1618.
129. Turk, B. Targeting proteases: Successes, failures and future prospects. Nat. Rev. Drug Discov. 2006, 5, 785-799.
130. Williams, M.S.; Henkart, P.A. Apoptotic cell death induced by intracellular proteolysis. J. Immunol. 1994, 153, 4247-4255.
131. Sagulenko, V.; Muth, D.; Sagulenko, E.; Paffhausen, T.; Schwab, M.; Westermann, F. Cathepsin D protects human neuroblastoma cells from doxorubicin-induced cell death. Carcinogenesis 2008, 29, 1869-1877.
132. Bidere, N.; Lorenzo, H.K.; Carmona, S.; Laforge, M.; Harper, F.; Dumont, C.; Senik, A. Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J. Biol. Chem. 2003, 278, 31401-31411.
133. Zaidi, N.; Kalbacher, H. Cathepsin E: A mini review. Biochem. Biophys. Res. Commun. 2008, 367, 517-522.
134. Ali, M.A.; Rosati, R.; Pettit, G.R.; Kalemkerian, G.P. Dolastatin 15 induces apoptosis and BCL-2 phosphorylation in small cell lung cancer cell lines. Anticancer Res. 1998, 18, 1021-1026.
135. Pedersen, S.F.; Hoffmann, E.K.; Mills, J.W. The cytoskeleton and cell volume regulation. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2001, 130, 385-399.
136. Maeno, E.; Ishizaki, Y.; Kanaseki, T.; Hazama, A.; Okada, Y. Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc. Natl. Acad. Sci. USA 2000, 97, 9487-9492.
137. Fernandez-Segura, E.; Canizares, F.J.; Cubero, M.A.; Warley, A.; Campos, A. Changes in elemental content during apoptotic cell death studied by electron probe X-ray microanalysis. Exp. Cell Res. 1999, 253, 454-462.