6-Bromoisatin found in muricid mollusc extracts inhibits colon cancer cell proliferation and induces apoptosis, preventing early stage tumor formation in a colorectal cancer rodent model

Marine Drugs

Volumn 12, Issue 1, 2014, Pages 17-35

  Esmaeelian, Babak ^a   Abbott, Catherine A ^a,b   Le Leu, Richard K ^b,c   Benkendorff, Kirsten ^d  

^a FLINDERS UNIVERSITY   (Australia)

^b FLINDERS UNIVERSITY   (Australia)

^c CSIRO   (Australia)

^d SOUTHERN CROSS UNIVERSITY   (Australia)

Author keywords

Apoptosis; Azoxymethane; Bioactive natural product; Colorectal cancer; In vivo model; Isatin; Marine mollusc

Indexed keywords

6 BROMOISATIN; AZOXYMETHANE; CASPASE 3; CASPASE 7; HEMATOXYLIN; ISATIN DERIVATIVE; LIVER ENZYME; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BLOOD ANALYSIS; BODY WEIGHT; CANCER RISK; CANCER STAGING; CARCINOGENESIS; CELL PROLIFERATION; COLORECTAL CANCER; CONTROLLED STUDY; DIURETIC ACTIVITY; DRUG EFFICACY; DRUG SAFETY; DRUG TOXICITY; ENZYME ACTIVITY; IC 50; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLLUSC; MOUSE; NONHUMAN; PROTON NUCLEAR MAGNETIC RESONANCE; RISK REDUCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BODY WEIGHT; CASPASES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SIZE; CELL SURVIVAL; COLON; COLORECTAL NEOPLASMS; DRUG SCREENING ASSAYS, ANTITUMOR; HT29 CELLS; HUMANS; HYDROCARBONS, BROMINATED; IMMUNOHISTOCHEMISTRY; ISATIN; KI-67 ANTIGEN; LIVER; MAGNETIC RESONANCE SPECTROSCOPY; POTASSIUM; SNAILS;

EID: 84892880699     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12010017     Document Type: Article

References (50)

1. Medvedev, A.; Buneeva, O.; Glover, V. Biological targets for isatin and its analogues: Implications for therapy. Biol. Targets Ther. 2007, 1, 151-162.
2. Vine, K.L.; Matesic, L.; Locke, J.; Ranson, M.; Skropeta, D. Cytotoxic and anticancer activities of isatin and its derivatives: A comprehensive review from 2000-2008. Anticancer Agents Med. Chem. 2009, 9, 397-414.
3. Pal, M.; Sharma, N.K.; Priyanka, J.K. Synthetic and biological multiplicity of isatin: A review. J. Adv. Sci. Res. 2011, 2, 35-44.
4. Akgul, O.; Tarikogullari, A.H.; Kose, F.A.; Ballar, P.; Pabuccuoglu, V. Synthesis and cytotoxic activity of some 2-(2,3-dioxo-2, 3-dihydro-1H-indol-1- yl) acetamide derivatives. Turk. J. Chem. 2013, 37, 204-212.
5. Benkendorff, K. The Australian Muricidae Dicathais orbita: A model species for marine natural product research. Mar. Drugs 2013, 11, 1370-1398.
6. Cane, A.; Tournaire, M.-C.; Barritault, D.; Crumeyrolle-Arias, M. The endogenous oxindoles 5-hydroxyoxindole and isatin are antiproliferative and proapoptotic. Biochem. Biophys. Res. Commun. 2000, 276, 379-384.
7. Igosheva, N.; Lorz, C.; O'Conner, E.; Glover, V.; Mehmet, H. Isatin, an endogenous monoamine oxidase inhibitor, triggers a dose-and time-dependent switch from apoptosis to necrosis in human neuroblastoma cells. Neurochem. Int. 2005, 47, 216-224.
8. Vine, K.L.; Locke, J.M.; Ranson, M.; Benkendorff, K.; Pyne, S.G.; Bremner, J.B. In vitro cytotoxicity evaluation of some substituted isatin derivatives. Bioorg. Med. Chem. 2007, 15, 931-938.
9. Motzer, R.J.; Michaelson, M.D.; Redman, B.G.; Hudes, G.R.; Wilding, G.; Figlin, R.A.; Ginsberg, M.S.; Kim, S.T.; Baum, C.M.; DePrimo, S.E. Activity of SU11248, a multitargeted inhibitor of vascular endothelial growth factor receptor and platelet-derived growth factor receptor, in patients with metastatic renal cell carcinoma. J. Clin. Oncol. 2006, 24, 16-24.
10. Prenen, H.; Cools, J.; Mentens, N.; Folens, C.; Sciot, R.; Schöffski, P.; Van Oosterom, A.; Marynen, P.; Debiec-Rychter, M. Efficacy of the kinase inhibitor SU11248 against gastrointestinal stromal tumor mutants refractory to imatinib mesylate. Clin. Cancer Res. 2006, 12, 2622-2627.
11. Kapadia, G.; Shukla, Y.; Basak, S.; Sokoloski, E.; Fales, H. The melosatins - a novel class of alkaloids from Melochia tomentosa. Tetrahedron 1980, 36, 2441-2447.
12. Gräfe, U.; Radics, L. Isolation and structure elucidation of 6-(3′-methylbuten-2′-yl) isatin, an unusual metabolite from Streptomyces albus. J. Antibiot. 1986, 39, 162-163.
13. Cooksey, C. J. Tyrian purple: 6,6′-dibromoindigo and related compounds. Molecules 2001, 6, 736-7693.
14. Edwards, V.; Benkendorff, K.; Young, F. Marine compounds selectively induce apoptosis in female reproductive cancer cells but not in primary-derived human reproductive granulosa cells. Mar. Drugs 2012, 10, 64-83.
15. Esmaeelian, B.; Benkendorff, K.; Johnston, R.M.; Abbott, C.A. Purified brominated indole derivatives from Dicathais orbita induce apoptosis and cell cycle arrest in colorectal cancer cell lines. Mar. Drugs 2013, 11, 3802-3822.
16. Westley, C.B.; McIver, C.M.; Abbott, C.A.; Le Leu, R.K.; Benkendorff, K. Enhanced acute apoptotic response to azoxymethane-induced DNA damage in the rodent colonic epithelium by Tyrian purple precursors: A potential colorectal cancer chemopreventative. Cancer Biol. Ther. 2010, 9, 371-379.
17. McLeod, R.; Schmocker, S.; Kennedy, E. Management of primary colon cancer in older adults. Geriat. Aging 2009, 12, 374-381.
18. Jemal, A.; Bray, F.; Center, M.M.; Ferlay, J.; Ward, E.; Forman, D. Global cancer statistics. CA Cancer J. Clin. 2011, 61, 69-90.
19. Chan, A.T.; Giovannucci, E.L. Primary prevention of colorectal cancer. Gastroenterology 2010, 138, 2029-2043.e10.
20. ACS, American Cancer Society. Colorectal Cancer Facts & Figures 2011-2013; American Cancer Society: Atlanta, GA, USA, 2013.
21. IARC, International Agency for Research on Cancer (IARC). World Cancer Report 2008; World Health Organization Press: Geneva, Switzerland, 2008; pp. 192-193.
22. Rajamanickam, S.; Agarwal, R. Natural products and colon cancer: Current status and future prospects. Drug Dev. Res. 2008, 69, 460-471.
23. Hong, M.Y.; Chapkin, R.S.; Wild, C.P.; Morris, J.S.; Wang, N.; Carroll, R.J.; Turner, N.D.; Lupton, J.R. Relationship between DNA adduct levels, repair enzyme, and apoptosis as a function of DNA methylation by azoxymethane. Cell Growth Differ. 1999, 10, 749-758.
24. Reddy, B.S.; Hirose, Y.; Cohen, L.A.; Simi, B.; Cooma, I.; Rao, C.V. Preventive potential of wheat bran fractions against experimental colon carcinogenesis: implications for human colon cancer prevention. Cancer Res. 2000, 60, 4792-4797.
25. Hu, Y.; Martin, J.; Le Leu, R.; Young, G. The colonic response to genotoxic carcinogens in the rat: regulation by dietary fibre. Carcinogenesis 2002, 23, 1131-1137.
26. Le Leu, R.; Hu, Y.; Young, G. Effects of resistant starch and nonstarch polysaccharides on colonic luminal environment and genotoxin-induced apoptosis in the rat. Carcinogenesis 2002, 23, 713-719.
27. Le Leu, R.K.; Brown, I.L.; Hu, Y.; Young, G.P. Effect of resistant starch on genotoxin-induced apoptosis, colonic epithelium, and lumenal contents in rats. Carcinogenesis 2003, 24, 1347-1352.
28. Vinson, J.; Bose, P. Comparative bioavailability of synthetic and natural Vitamin C in guinea pigs. Nutr. Rep.Int. 1983, 27, 1-5.
29. Lodge, J. K. Vitamin E bioavailability in humans. J. Plant Physiol. 2005, 162, 790-796.
30. Constantinou, C.; Papas, K.; Constantinou, A. Caspase-independent pathways of programmed cell death: The unraveling of new targets of cancer therapy? Curr. Cancer Drug Targets 2009, 9, 717-728.
31. Zhuang, S.; Schnellmann, R.G. A death-promoting role for extracellular signal-regulated kinase. J. Pharmacol. Exp. Ther. 2006, 319, 991-997.
32. Wang, X.; Martindale, J.L.; Holbrook, N.J. Requirement for ERK activation in cisplatin-induced apoptosis. J. Biol. Chem. 2000, 275, 39435-39443.
33. Kim, Y.K.; Kim, H.J.; Kwon, C.H.; Kim, J.H.; Woo, J.S.; Jung, J.S.; Kim, J.M., Role of ERK activation in cisplatin-induced apoptosis in OK renal epithelial cells. J. Appl. Toxicol. 2005, 25, 374-382.
34. Jo, S.-K.; Cho, W.Y.; Sung, S.A.; Kim, H.K.; Won, N.H. MEK inhibitor, U0126, attenuates cisplatin-induced renal injury by decreasing inflammation and apoptosis. Kidney Int. 2005, 67, 458-466.
35. Sinha, D.; Bannergee, S.; Schwartz, J.H.; Lieberthal, W.; Levine, J.S. Inhibition of ligand-independent ERK1/2 activity in kidney proximal tubular cells deprived of soluble survival factors up-regulates Akt and prevents apoptosis. J. Biol. Chem. 2004, 279, 10962-10972.
36. Hu, Y.; McIntosh, G.H.; Le Leu, R.K.; Woodman, R.; Young, G.P. Suppression of colorectal oncogenesis by selenium-enriched milk proteins: apoptosis and K-ras mutations. Cancer Res. 2008, 68, 4936-4944.
37. Le Leu, R.K.; Hu, Y.; Brown, I.L.; Woodman, R.J.; Young, G.P. Synbiotic intervention of Bifidobacterium lactis and resistant starch protects against colorectal cancer development in rats. Carcinogenesis 2010, 31, 246-251.
38. Saini, K.S.; Thompson, C.; Winterford, C.M.; Walker, N.I.; Cameron, D.P. Streptozotocin at low doses induces apoptosis and at high doses causes necrosis in a murine pancreatic β cell line, INS-1. IUBMB Life 1996, 39, 1229-1236.
39. Hewawasam, R.; Jayatilaka, K.; Pathirana, C.; Mudduwa, L. Hepatoprotective effect of Epaltes divaricata extract on carbon tetrachloride induced hepatotoxicity in mice. Indian J. Med. Res. 2004, 120, 30-34.
40. Westley, C.B.; Benkendorff, K.; McIver, C.M.; Le Leu, R.K.; Abbott, C.A. Gastrointestinal and hepatotoxicity assessment of an anticancer extract from muricid molluscs. Evid.-Based Comp. Alt. Med. 2013, 2013, 1-12.
41. Lindeman, R.D. Hypokalemia: causes, consequences and correction. Am. J. Med. Sci. 1976, 272, 5-17.
42. Weiner, I.D.; Wingo, C.S. Hypokalemia - consequences, causes, and correction. J. Am. Soc. Nephrol. 1997, 8, 1179-1188.
43. Gennari, F.J. Disorders of potassium homeostasis: Hypokalemia and hyperkalemia. Crit. Care Clin. 2002, 18, 273-288.
44. Nataraj, K.S.; Rao, J.V.; Jayaveera, K.N. Diuretic activity of some novel isatin derivatives. J. Pharm. Res. 2010, 3, 863.
45. Matheus, M.E.; de Almeida Violante, F.; Garden, S.J.; Pinto, A.C.; Dias Fernandes, P. Isatins inhibit cyclooxygenase-2 and inducible nitric oxide synthase in a mouse macrophage cell line. Eur. J. Pharm. 2007, 556, 200-206.
46. Kim, J.-K.; Park, G.-M. Indirubin-3-monoxime exhibits anti-inflammatory properties by down-regulating NF-κB and JNK signaling pathways in lipopolysaccharide-treated RAW264.7 cells. Inflamm. Res. 2012, 61, 319-325.
47. Jung, H.-L.; Nam, K.N.; Son, M.S.; Kang, H.; Hong, J.W.; Kim, J.W.; Lee, E.H. Indirubin-3′-oxime inhibits inflammatory activation of rat brain microglia. Neurosci. Lett. 2011, 487, 139-143.
48. Hu, Y.; Le Leu, R.K.; Young, G.P. Sulindac corrects defective apoptosis and suppresses azoxymethane-induced colonic oncogenesis in p53 knockout mice. Int. J. Cancer 2005, 116, 870-875.
49. Potten, C.S.; Li, Y.; O'Connor, P.J.; Winton, D. A possible explanation for the differential cancer incidence in the intestine, based on distribution of the cytotoxic effects of carcinogens in the murine large bowel. Carcinogenesis 1992, 13, 2305-2312.
50. Cordes, C.; Munzel, A.N.N.K.; Rudolph, P.; Hoffmann, M.; Leuschner, I.; Gottschlich, S. Immunohistochemical staining of Ki-67 using the monoclonal antibody Ki-S11 is a prognostic indicator for laryngeal squamous cell carcinoma. Anticancer Res. 2009, 29, 1459-1465.