Marine Cyanobacteria Compounds with Anticancer Properties: A Review on the Implication of Apoptosis
Abstract
:1. Introduction
Compound | Source | Class of compound | Cytoxicity assay | Human cell line tested | Reference |
---|---|---|---|---|---|
Ankaraholide A | Geitlerinema | Glycosilated swinholide | MTT | NCI-H460 lung tumor | [14] |
SRB | MDA-MB-435 breast carcinoma | [14] | |||
Apratoxin A | Lyngbya majuscula | Cyclic depsipeptide | SRB | KB oral epidermoid cancer and LoVo colon cancer | [40,41] |
MTT | U2OS osteosarcoma, HT29 colon adenocarcinoma and HeLa cervical carcinoma | [42] | |||
Apratoxins B-C | Lyngbya sp. | Cyclic depsipeptides | MTT | KB oral epidermoid cancer and LoVo colon cancer | [40] |
Apratoxin D | Lyngbya majuscula and Lyngbya sordida | Cyclic depsipeptide | MTT | H-460 lung cancer | [26] |
Apratoxin E | Lyngbya bouilloni | Cyclic depsipeptide | MTT | U2OS osteosarcoma, HT29 colon adenocarcinoma and HeLa epithelial carcinoma | [42] |
Apratoxins F and G | Lyngbya bouilloni | Cyclic depsipeptides | MTT | H-460 lung cancer | [43] |
Hemocytometer counting | HCT-116 colorectal cancer cells | [43] | |||
Aurilide B | Lyngbya majuscula | Cyclic depsipeptide | MTT | H-460 lung tumor | [24] |
Aurilide C | Lyngbya majuscula | Cyclic depsipeptide | MTT | NCI-H460 lung tumor | [24] |
Belamide A | Symploca sp. | Linear tetrapeptide | Non-specified | HCT-116 colon cancer | [8] |
Bisebromoamide | Lyngbya sp. | Peptide | SRB | HeLa S3 epithelial carcinoma | [44] |
Biselyngbyaside | Lyngbya sp. | Glicomacrolide | SRB | HeLa S3 epithelial carcinoma, SNB-78 central nervous system cancer and NCI H522 lung cancer | [15] |
Calothrixin A | Calothrix | Pentacyclic indolophenanthridine | 3H-thymidine incorporation | HeLa epithelial carcinoma | [45] |
MTT | Leukemia CEM | [46] | |||
Calothrixin B | Calothrix | Pentacyclic indolophenanthridine | MTT | HeLa epithelial carcinoma | [47] |
Leukemia CEM | [46] | ||||
Caylobolide A | Lyngbya majuscula | Macrolactone | Non-specified | HCT-116 colon tumor | [48] |
Caylobolide B | Phormidium spp. | Macrolactone | MTT | HT29 colorectal adenocarcinoma and HeLa cervical carcinoma | [16] |
Coibamide A | Leptolyngbya sp. | Cyclic depsipeptide | MTT | Lung cancer NCI-H460, breast cancer MDA-MB-231, melanoma LOX IMVI, leukemia HL-60 and astrocytoma SNB75 | [49] |
Cryptophycin 1 | Nostoc spp. | Cyclic depsipeptide | Cell morphology examination | MDA-MB-435 mammary adenocarcinoma and SKOV3 ovarian carcinoma | [50] |
AlamarBlue dye reduction | Leukemia U937, CCRF-CEM and HL-60, colon carcinoma HT-29, GC3 and Caco-2, mammary carcinoma MCF-7 and MDA-MB-231 and cervical carcinoma HeLa | [51] | |||
Dolastatin 10 | Symploca sp. | Linear Pentapeptide | MTT | Lung A549 carcinoma | [52] |
Human lung cancer cells: NCI-H69, -H82, -H446 and -H510 | [53] | ||||
Human DU-145 prostate cancer cell line | [54] | ||||
[3H] Thymidine | Several lymphoma cell lines | [55] | |||
Trypan blue dye | Reh lymphoblastic leukemia | [56] | |||
Dolastatin 12 | Leptolyngbya sp. | Cyclic depsipeptide | MTT | A549 lung carcinoma | [52] |
Dragonamide | Lyngbya majuscula | Lipopeptide | Non-specified | A-549 lung epithelial adenocarcinoma, HT-29 colon adenocarcinoma and MEL-28 melanoma | [57] |
Ethyl Tumonoate A | Oscillatoria margaritifera | Peptide | MTT | H-460 lung cancer | [58] |
Hoiamide A | Assemblage of Lyngbya majuscule and Phormidium gracile | Cyclic depsipeptide | Non-specified | H-460 lung cancer | [59] |
Hoiamide B | Cyanobacterial sample | Cyclic depsipeptide | Non-specified | H-460 lung cancer | [59] |
Homodolastatin 16 | Lyngbya majuscula | Cyclic depsipeptide | MTT | WHCO1 and WHCO6 esophageal cancer and ME180 cervical cancer | [60] |
Isomalyngamide A and A-1 | Lyngbya majuscula | Fatty acid amides | MTT | Breast cancer MCF-7 and MDA-MB-231 | [13] |
Jamaicamides A-C | Lyngbya majuscula | Polyketide-Peptides | MTT | H-460 lung cancer | [61] |
Kalkitoxin | Lyngbya majuscula | Lipopeptide | Trypan blue dye | HCT-116 colon | [62] |
Lagunamide C | Lyngbya majuscula | Cyclic depsipeptide | MTT | Lung adenocarcinoma A549, cancer prostate PC3, ileocecal colorectal cancer HCT8 and ovary cancer SK-OV | [63] |
Largazole | Symploca sp. | Cyclic depsipeptide | MTT | MDA-MB-23I breast cancer and U2OS osteosarcoma | [64] |
A549 lung cancer and HCT-116 colorectal carcinoma | [65] | ||||
Lyngbyabellin A | Lyngbya majuscula | Cyclic depsipeptide | Non-specified | KB nasopharyngeal carcinoma and LoVo colon adenocarcinoma | [66] |
Lyngbyaloside | Lyngbya sp. | Glicomacrolide | Non-specified | KB nasopharyngeal carcinoma and LoVo colon adenocarcinoma | [67] |
Majusculamide C | Lyngbya majuscula | Cyclic depsipeptide | Non-specified | Ovarian carcinoma OVCAR-3, kidney cancer A498, lung cancer NCI-H460, colorectal cancer KM20L2 and glioblastoma SF-295 | [68] |
Malevamide D | Symploca hydnoides | Peptide ester | Non-specified | Lung cancer A-549, colon cancer HT-29 and melanoma MEL-28. | [69] |
Malyngamide 2 | Lyngbya sordida | Fatty acid amine | MTT | H-460 lung cancer | [23] |
Malyngamide C, J and K | Lyngbya majuscula | Fatty acid amines | MTT | H-460 lung cancer | [70] |
Malyngolide dimmer | Lyngbya majuscula | Cyclodepside | MTT | H-460 lung cancer | [71] |
Nostocyclopeptide A1 and A2 | Nostoc sp. | Cyclic heptapeptides | Non-specified | KB oral epidermoid cancer and LoVo colon cancer | [72] |
Obyanamide | Lyngbya confervoides | Cyclic depsipeptide | Non-specified | KB oral epidermoid cancer and LoVo colon cancer | [73] |
Palauamide | Lyngbya sp. | Cyclic depsipeptide | Non-specified | Cervical carcinoma HeLa, lung adenocarcinoma A549 and gastrocarcinoma BGC | [74] |
KB oral epidermoid cancer | [75] | ||||
Palmyramide A | Lyngbya majuscula | Cyclic depsipeptide | MTT | H-460 lung cancer | [76] |
Pitipeptolides A-B | Lyngbya majuscula | Cyclic depsipeptides | Non-specified | LoVo colon cancer | [77] |
MTT | HT29 colon adenocarcinoma and MCF-7 breast cancer | [17] | |||
Pitipeptolide C | Lyngbya majuscula | Cyclic depsipeptide | MTT | HT29 colon adenocarcinoma and MCF-7 breast cancer | [17] |
Pitiprolamide | Lyngbya majuscula | Cyclic depsipeptide | MTT | HCT116 colorectal carcinoma and MCF7 breast adenocarcinoma | [78] |
Pseudodysidenin | Lyngbya majuscula | Lipopeptide | Non-specified | A-549 lung adenocarcinoma, HT-29 colon adenocarcinoma and MEL-28 melanoma | [57] |
Somocystinamide A | Lyngbya majuscula | Lipopeptide | XTT | Jurkat and CEM leukemia, A549 lung carcinoma, Molt4 T leukemia, M21 melanoma and U266 myeloma | [79] |
Symplocamide | Symploca sp. | Cyclic peptide | Non-specified | H-460 lung cancer | [27] |
Symplostatin 1 | Symploca hydnoides | Linear Pentapeptide | SRB | MDA-MB-435 breast carcinoma and NCI/ADR ovarian carcinoma | [25] |
Epidermoid carcinoma cell line | [80] | ||||
Tasiamide | Symploca sp. | Cyclic peptide | Non-specified | KB oral epidermoid cancer and LoVo colon cancer | [81] |
Tasiamide B | Symploca sp. | Peptide | Non-specified | KB oral epidermoid cancer | [82] |
Tasipeptins A-B | Symploca sp. | Cyclic depsipeptides | Non-specified | KB oral epidermoid cancer | [83] |
Ulongapeptin | Lyngbya sp. | Cyclic depsipeptide | Non-specified | KB oral epidermoid cancer | [84] |
Veraguamides A-G | Symploca cf. hydnoides | Cyclic depsipeptides | MTT | H-460 lung cancer | [85] |
Wewakazole | Lyngbya sordida | Cyclic dodecapeptide | MTT | H-460 lung cancer | [23] |
Wewakpeptins | Lyngbya semiplena | Depsipeptides | MTT | H-460 lung cancer | [11] |
Compound | Source | Class of compound | Model tested | Cell effect | Reference |
---|---|---|---|---|---|
Alotamide | Lyngbya bouillonii | Cyclic depsipeptide | Murine cerebrocortical neurons | Calcium influx promotion | [12] |
Ankaraholide A | Geitlerinema | Glycosilated swinholide | Rat aorta A-10 cells | Loss of filamentous (F)-actin | [14] |
Antillatoxin | Lyngbya majuscula | Lipopeptide | Primary rat cerebellar granule cells | Voltage-gated sodium channel activation | [86] |
CHL 1610 Chinese hamster lung cells | [87] | ||||
Antillatoxin B | Lyngbya majuscula | Lipopeptide | neuro-2a mouse neuroblastoma cells | Sodium channel activation | [10] |
Apratoxin A | Lyngbya majuscula | Cyclic depsipeptide | Human HeLa cervical carcinoma cells | Cell cycle inhibition | [88] |
Human U2OS osteosarcoma cells | Secretory pathway inhibition | [89] | |||
Aurilide B | Lyngbya majuscula | Cyclic depsipeptide | Rat aorta A-10 cells | Microfilament disruption | [24] |
Belamide A | Symploca sp. | Linear tetrapeptide | Rat aorta A-10 cells | Microtubule disruption | [8] |
Bisebromoamide | Lyngbya sp. | Peptide | Human HeLa epithelial carcinoma cells | Actin filaments stabilization | [90] |
Normal rat kidney cells extracellular signal regulated protein kinase | Protein kinase inhibition | [44] | |||
Bouillomides A-B | Lyngbya bouillonii | Depsipeptides | Elastase and chymotrypsin | Serine proteases inhibition | [91] |
Calothrixin A | Calothrix | Pentacyclic indolophenanthridine | Human leukemia CEM cells | Cell cycle inhibition | [46] |
Calothrixin B | Calothrix | Pentacyclic indolophenanthridine | Human HeLa epithelial carcinoma cells | Cell cycle inhibition | [45] |
Human HeLa epithelial carcinoma cells | Oxidative stress induction | [45] | |||
Coibamide A | Leptolyngbya sp. | Cyclic depsipeptide | Human NCI-H460 lung cancer cell line | Cell cycle inhibition | [49] |
Cryptophycin 1 | Nostoc spp. | Cyclic depsipeptide | Human MDA-MB-435 mammary adenocarcinoma and SKOV3 ovarian carcinoma cells | Cell cycle inhibition | [50] |
Human MDA-MB-435 mammary adenocarcinoma | Caspase-3 protein activation | [50] | |||
Curacin A | Lyngbya majuscula | Lipopeptide | Tubulin | Tubulin polymerization inhibition | [92] |
Human A549 lung carcinoma cells | Bad protein levels increase | [52] | |||
Human A549 lung carcinoma cells | Caspase-3 protein activation | [52] | |||
Bovine β-tubulin | Tubulin polymerization inhibition | [93] | |||
Dolastatin 10 | Symploca sp. | Linear Pentapeptide | Human Reh lymphoblastic leukemia cells | Bcl-2 protein reduction | [56] |
Human lung cancer cells: NCI-H69 and -H510 | Bcl-2 protein phosphorylation | [53] | |||
Human A549 lung carcinoma cells | Bad protein levels increase | [52] | |||
Human A549 lung carcinoma cells | Caspase-3 protein activation | [52] | |||
Dolastatin 12 | Leptolyngbya sp. | Cyclic depsipeptide | Rat aorta A-10 cells | Microfilament disruptor | [94] |
Grassystatin A-B | Lyngbya confervoides | Linear depsipeptides | Cathepsins D and E | Proteases inhibition | [95] |
Hectochlorin | Lyngbya majuscula | Lipopeptide | Human CA46 Burkitt lymphoma cells | Cell cycle inhibition | [18] |
Hermitamides A-B | Lyngbya majuscula | Lipopeptide | Human HEK embryonic kidney cells | Voltage-gated sodium channel inhibition | [96] |
Hoiamide A | Assemblage of Lyngbya majuscule and Phormidium gracile | Cyclic depsipeptide | Primary cultures of neocortical neurons from embryonic mice | Sodium channel activation | [59,97] |
Hoiamide B | Cyanobacterial sample | Cyclic depsipeptide | Primary cultures of neocortical neurons from embryonic mice | Sodium influx stimulation | [59] |
Kalkitoxin | Lyngbya majuscula | Lipopeptide | Primary rat cerebellar granule neuron cultures | Calcium influx inhibition | [98] |
Kempopeptin A | Lyngbya sp. | Cyclic depsipeptide | Bovine pancreatic α-chymotrypsin, porcine pancreatic elastase | Serine Protease Inhibition | [99] |
Kempopeptin B | Lyngbya sp. | Cyclic depsipeptide | Trypsin | Serine Protease Inhibition | [99] |
Largamides A-C | Lyngbya confervoides | Cyclic depsipeptides | Porcine pancreatic elastase | Serine protease inhibition | [100] |
Largamides D-G | Oscillatoria sp. | Cyclic depsipeptides | α-chymotrypsin | Serine protease inhibition | [101] |
Lyngbyabellin A | Lyngbya majuscula | Cyclic depsipeptide | Human CA46 Burkitt lymphoma cells | Cell cycle inhibition | [18] |
Rat aorta A-10 cells | Microfilament disruption | [66] | |||
Lyngbyabellin B | Lyngbya majuscula | Cyclic depsipeptide | Human CA46 Burkitt lymphoma cells | Cell cycle inhibition | [18] |
Lyngbyastatin 1 | Lyngbya majuscula | Cyclic depsipeptide | Rat aorta A-10 cells | Microfilament disruption | [94] |
Lyngbyastatin 4 | Lyngbya confervoides | Cyclic depsipeptide | Bovine pancreatic α-chymotrypsin and porcine pancreatic elastase | Serine protease inhibition | [102] |
Lyngbyastatin 5-7 | Lyngbya spp. | Cyclic depsipeptides | Porcine pancreatic elastase | Serine protease inhibition | [103] |
Lyngbyastatin 8-10 | Lyngbya semiplena | Cyclic depsipeptides | Porcine pancreatic elastase | Serine protease inhibition | [104] |
Malevamide E | Symploca laete-viridis | Depsipeptide | Human HEK embryonic kidney cells | Calcium influx inhibition | [105] |
Molassamide | Dichothrix utahensis | Depsipeptide | Bovine pancreatic α-chymotrypsin and porcine pancreatic elastase | Serine protease inhibition | [106] |
Palmyramide A | Lyngbya majuscula | Cyclic depsipeptide | Mouse neuroblastoma neuro-2a cells | Sodium channel inhibition | [76] |
Palmyrolide | Assemblage of Leptolyngbya cf. and Oscillatoria spp. | Macrolide | Mouse neuroblastoma neuro-2a cells | Sodium influx inhibition | [107] |
Murine cerebrocortical neurons | Inhibition of calcium oscillations | [107] | |||
Pitipeptolides A and B | Lyngbya majuscula | Cyclic depsipeptides | Elastase | Serine protease stimulation | [77] |
Pompanopeptin A | Lyngbya confervoides | Cyclic peptide | Porcine pancreatic trypsin | Serine protease inhibition | [108] |
Symplocamide | Symploca sp. | Cyclic peptide | Chymotrypsin | Serine protease inhibition | [27] |
Symplostatin 1 | Symploca hydnoides | Linear Pentapeptide | Rat aorta A-10 and human HeLa cervical carcinoma cells | Cell cycle inhibition | [25] |
Rat aorta A-10 cells | Microtubule depolymerization | [109] | |||
Human MDA-MB-435 breast carcinoma cells | Bcl-2 phosphorylation | [25] | |||
Human MDA-MB-435 breast carcinoma cells | Caspase-3 protein activity stimulation | [25] | |||
Symplostatin 3 | Symploca sp. | Rat aorta A-10 cells | Microtubule depolymerization | [110] | |
Tiglicamides A-C | Lyngbya confervoides | Cyclic depsipeptides | Porcine pancreatic elastase | Serine protease inhibition | [111] |
2. Cell Cycle Arrest
3. Mitochondrial Dysfunctions and Oxidative Damage
4. Alterations in Caspase Cascade
5. Non-Caspases Proteases Involvement
Compound | Source | Class of compound | Serine protease inhibition | Reference | ||
---|---|---|---|---|---|---|
Elastase | Chymotripsin | Thrypsin | ||||
Bouillomide A | Lyngbya bouillonii | Depsipeptide | IC50 = 1.9 μM | IC50 = 0.17 μM | No inhibition at 100 μM | [91] |
Bouillomide B | Lyngbya bouillonii | Depsipeptide | IC50 = 1.0 μM | IC50 = 9.3 μM | No inhibition at 100 μM | [91] |
Kempopeptin A | Lyngbya sp. | Cyclic depsipeptide | IC50 = 0.32 μM | IC50 = 2.6 μM | IC50 > 67 μM | [99] |
Kempopeptin B | Lyngbya sp. | Cyclic depsipeptide | IC50 > 67 μM | IC50 > 67 μM | IC50 = 8.4 μM | [99] |
Largamide A | Lyngbya confervoides | Cyclic depsipeptide | IC50 = 1.41 μM | No inhibition at 50 μM | No inhibition at 50 μM | [100] |
Largamide B | Lyngbya confervoides | Cyclic depsipeptide | IC50 = 0.53 μM | No inhibition at 50 μM | No inhibition at 50 μM | [100] |
Largamide C | Lyngbya confervoides | Cyclic depsipeptide | IC50 = 1.15 μM | No inhibition at 50 μM | No inhibition at 50 μM | [100] |
Largamide D | Oscillatoria sp. | Cyclic depsipeptide | Not described | IC50 = 10.0 μM | No inhibition | [101] |
Largamide E | Oscillatoria sp. | Cyclic depsipeptide | Not described | IC50 = 10.0 μM | No inhibition | [101] |
Largamide F | Oscillatoria sp. | Cyclic depsipeptide | Not described | IC50 = 4.0 μM | No inhibition | [101] |
Largamide G | Oscillatoria sp. | Cyclic depsipeptide | Not described | IC50 = 25.0 μM | No inhibition | [101] |
Lyngbyastatin 4 | Lyngbya confervoides | Cyclic depsipeptide | IC50 = 0.03 μM | IC50 = 0.30 μM | No inhibition at 30 μM | [102] |
Lyngbyastatin 5 | Lyngbya spp. | Cyclic depsipeptide | IC50 = 3.2 μM | IC50 = 2.8 μM | No inhibition at 30 μM | [103] |
Lyngbyastatin 6 | Lyngbya spp. | Cyclic depsipeptide | IC50 = 2.0 μM | IC50 = 2.5 μM | No inhibition at 30 μM | [103] |
Lyngbyastatin 7 | Lyngbya spp. | Cyclic depsipeptide | IC50 = 3.3 μMIC50 = 0.47 μM | IC50 = 2.5 μM | No inhibition at 30 μM | [103,104] |
Lyngbyastatin 8 | Lyngbya semiplena | Cyclic depsipeptide | IC50 = 0.12 μM | Not described | Not described | [104] |
Lyngbyastatin 9 | Lyngbya semiplena | Cyclic depsipeptide | IC50 = 0.21 μM | Not described | Not described | [104] |
Lyngbyastatin 10 | Lyngbya semiplena | Cyclic depsipeptide | IC50 = 0.12 μM | Not described | Not described | [104] |
Molassamide | Dichothrix utahensis | Depsipeptide | IC50 = 0.032 μM | IC50 = 0.234 μM | No inhibition at 10 μM | [106] |
Pompanopeptin A | Lyngbya confervoides | Cyclic peptide | Not described | Not described | IC50 = 2.4 μM | [108] |
Symplocamide A | Symploca sp. | Cyclic peptide | Not described | IC50 = 0.38 μM | IC50 = 80.2 μM | [27] |
Somamide B | Lyngbya majuscula and Schizothrix assemblage | Depsipeptide | IC50 = 9.5 μM | IC50 = 4.2 μM | No inhibition at 30 μM | [103] |
Tiglicamide A | Lyngbya confervoides | Cyclic depsipeptide | IC50 = 2.14 μM | Not described | Not described | [111] |
Tiglicamide B | Lyngbya confervoides | Cyclic depsipeptide | IC50 = 6.99 μM | Not described | Not described | [111] |
Tiglicamide C | Lyngbya confervoides | Cyclic depsipeptide | IC50 = 7.28 μM | Not described | Not described | [111] |
6. Alterations in the Bcl-2 Protein Family
7. Alterations in Membrane Sodium Channel Dynamics
8. Conclusions
Acknowledgements
References
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Costa, M.; Costa-Rodrigues, J.; Fernandes, M.H.; Barros, P.; Vasconcelos, V.; Martins, R. Marine Cyanobacteria Compounds with Anticancer Properties: A Review on the Implication of Apoptosis. Mar. Drugs 2012, 10, 2181-2207. https://doi.org/10.3390/md10102181
Costa M, Costa-Rodrigues J, Fernandes MH, Barros P, Vasconcelos V, Martins R. Marine Cyanobacteria Compounds with Anticancer Properties: A Review on the Implication of Apoptosis. Marine Drugs. 2012; 10(10):2181-2207. https://doi.org/10.3390/md10102181
Chicago/Turabian StyleCosta, Margarida, João Costa-Rodrigues, Maria Helena Fernandes, Piedade Barros, Vitor Vasconcelos, and Rosário Martins. 2012. "Marine Cyanobacteria Compounds with Anticancer Properties: A Review on the Implication of Apoptosis" Marine Drugs 10, no. 10: 2181-2207. https://doi.org/10.3390/md10102181