Citrus limonin and its glucoside inhibit colon adenocarcinoma cell proliferation through apoptosis

Journal of Agricultural and Food Chemistry

Volumn 59, Issue 6, 2011, Pages 2314-2323

  Chidambara Murthy, Kotamballi N ^a   Jayaprakasha, G K ^a   Kumar, Vinod ^a   Rathore, Keerti S ^a   Patil, Bhimanagouda S ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

apoptosis; colon cancer; intracellular calcium; Limonoids; SW480

Indexed keywords

APOPTOSIS; COLON CANCER; INTRACELLULAR CALCIUM; LIMONOIDS; SW480;

CALCIUM; CELL MEMBRANES; CELL PROLIFERATION; DISEASES; MITOCHONDRIA;

CELL DEATH;

CASPASE 3; CYTOCHROME C; GLUCOSIDE; LIMONIN; LIMONOID; PLANT EXTRACT; PROTEIN BAX;

ADENOCARCINOMA; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CHEMISTRY; CITRUS FRUIT; COLON TUMOR; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; PATHOPHYSIOLOGY; TUMOR CELL LINE;

ADENOCARCINOMA; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CELL LINE, TUMOR; CELL PROLIFERATION; CITRUS; COLONIC NEOPLASMS; CYTOCHROMES C; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSIDES; HUMANS; LIMONINS; MITOCHONDRIA; PLANT EXTRACTS;

CITRUS; CITRUS RETICULATA;

EID: 79952759019     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf104498p     Document Type: Article

References (43)

1. Johnson, J. J.; Mukhtar, H. Curcumin for chemoprevention of colon cancer Cancer Lett. 2007, 255 (2) 170-181 (Pubitemid 47268637)
2. Tache, S.; Ladam, A.; Corpet, D. E. Chemoprevention of aberrant crypt foci in the colon of rats by dietary onion Eur. J. Cancer 2007, 43 (2) 454-458 (Pubitemid 46138042)
3. Bingham, S. A.; Day, N. E.; Luben, R.; Ferrari, P.; Slimani, N.; Norat, T.; Clavel-Chapelon, F.; Kesse, E.; Nieters, A.; Boeing, H.; Tjonneland, A.; Overvad, K.; Martinez, C.; Dorronsoro, M.; Gonzalez, C. A.; Key, T. J.; Trichopoulou, A.; Naska, A.; Vineis, P.; Tumino, R.; Krogh, V.; Bueno-de-Mesquita, H. B.; Peeters, P. H. M.; Berglund, G.; Hallmans, G.; Lund, E.; Skeie, G.; Kaaks, R.; Riboli, E. Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study Lancet 2003, 361 (9368) 1496-1501 (Pubitemid 36566339)
4. Block, G.; Patterson, B.; Subar, A. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence Nutr. Cancer 1992, 18 (1) 1-29
5. Marlett, J.; Cheung, T. Database and quick methods of assessing typical dietary fiber intakes using data for 228 commonly consumed foods J. Am. Diet. Assoc. 1997, 97 (10) 1139-1151
6. Girennavar, B.; Jayaprakasha, G. K.; Jadegoud, Y.; Gowda, G. A. N.; Patil, B. S. Radical scavenging and cytochrome P450 3A4 inhibitory activity of bergaptol and geranylcoumarin from grapefruit Bioorg. Med. Chem. 2007, 15 (11) 3684-3691 (Pubitemid 46656345)
7. Jayaprakasha, G. K.; Mandadi, K. K.; Poulose, S. M.; Jadegoud, Y.; Gowda, G. A. N.; Patil, B. S. Inhibition of colon cancer cell growth and antioxidant activity of bioactive compounds from Poncirus trifoliata (L.) Raf Bioorg. Med. Chem. 2007, 15 (14) 4923-4932 (Pubitemid 46836831)
8. Liu, Y.; Ahmad, H.; Luo, Y.; Gardiner, D. T.; Gunasekera, R. S.; McKeehan, W. L.; Patil, B. S. Citrus Pectin: Characterization and Inhibitory Effect on Fibroblast Growth Factor- Receptor Interaction J. Agric. Food Chem. 2001, 49 (6) 3051-3057 (Pubitemid 32826109)
9. Vanamala, J.; Leonardi, T.; Patil, B. S.; Taddeo, S. S.; Murphy, M. E.; Pike, L. M.; Chapkin, R. S.; Lupton, J. R.; Turner, N. D. Suppression of colon carcinogenesis by bioactive compounds in grapefruit Carcinogenesis 2006, 27 (6) 1257-1265 (Pubitemid 43994864)
10. Lee, S.-E.; Kim, M.-R.; Kim, J.-H.; Takeoka, G. R.; Kim, T.-W.; Park, B.-S. Antimalarial activity of anthothecol derived from Khaya anthotheca (Meliaceae) Phytomedicine 2008, 15 (6-7) 533-535 (Pubitemid 351784547)
11. Sun, C.; Chen, K.; Chen, Y.; Chen, Q. Contents and antioxidant capacity of limonin and nomilin in different tissues of citrus fruit of four cultivars during fruit growth and maturation Food Chem. 2005, 93 (4) 599-605 (Pubitemid 40804272)
12. Kelly, C.; Jewell, C.; O'Brien, N. M. The effect of dietary supplementation with the citrus limonoids limonin and nomilin on xenobiotic-metabolizing enzymes in the liver and small intestine of the rat Nutr. Res. (N.Y.) 2003, 23, 681-690 (Pubitemid 36597499)
13. Jayaprakasha, G. K.; Mandadi, K. K.; Poulose, S. M.; Jadegoud, Y. Nagana Gowda, G. A.; Patil, B. S., Novel triterpenoid from Citrus aurantium L. possesses chemopreventive properties against human colon cancer cells Bioorg. Med. Chem. 2008, 16 (11) 5939-5951 (Pubitemid 351758846)
14. Guthri, N.; Morley, K.; Hasegawa, S.; Manner Gary, D.; Vandenberg, T., Inhibition of Human Breast Cancer Cells by Citrus Limonoids. In Citrus Limonoids; American Chemical Society: Washington, DC, 2000; pp 164 - 174.
15. Tian, Q.; Miller, E. G.; Ahmad, H.; Tang, L.; Patil, B. S. Differential inhibition of human cancer cell proliferation by citrus limonoids Nutr. Cancer 2001, 40, 180
16. Poulose, S. M.; Harris, E. D.; Patil, B. S. Antiproliferative Effects of Citrus Limonoids Against Human Neuroblastoma and Colonic Adenocarcinoma Cells Nutr. Cancer 2006, 56 (1) 103-112 (Pubitemid 46173420)
17. Raunio, H.; Husgafvel-Pursiainen, K.; Anttila, S.; Hietanen, E.; Hirvonen, A.; Pelkonen, O. Diagnosis of polymorphisms in carcinogen-activating and inactivating enzymes and cancer susceptibility - a review Gene 1995, 159 (1) 113
18. Khan, S. G.; Katiyar, S. K.; Agarwal, R.; Mukhtar, H. Enhancement of Antioxidant and Phase II Enzymes by Oral Feeding of Green Tea Polyphenols in Drinking Water to SKH-1 Hairless Mice: Possible Role in Cancer Chemoprevention Cancer Res. 1992, 52 (14) 4050-4052
19. Lam, L. K. T.; Zhang, J.; Hasegawa, S.; Schut, H. A. J. Inhibition of Chemically Induced Carcinogenesis by Citrus Limonoids. In Food Phytochemicals for Cancer Prevention I; American Chemical Society: Washington, DC, 1993; pp 209 - 219.
20. Miller, E. G.; Fanous, R.; Rivera-Hidalgo, F.; Binnie, W. H.; Hasegawa, S.; Lam, L. K. T. The effects of citrus limonoids on hamster buccal pouch carcinogenesis Carcinogenesis 1989, 10 (8) 1535-1537 (Pubitemid 19197478)
21. Tanaka, T.; Maeda, M.; Kohno, H.; Murakami, M.; Kagami, S.; Miyake, M.; Wada, K. Inhibition of azoxymethane-induced colon carcinogenesis in male F344 rats by the citrus limonoids obacunone and limonin Carcinogenesis 2001, 22 (1) 193-198 (Pubitemid 32098162)
22. Perez, J. L.; Jayaprakasha, G. K.; Valdivia, V.; Munoz, D.; Dandekar, D. V.; Ahmad, H.; Patil, B. S. Limonin Methoxylation Influences the Induction of Glutathione S-Transferase and Quinone Reductase J. Agric. Food Chem. 2009, 57 (12) 5279-5286
23. Miyagi, Y.; Om, A. S.; Chee, K. M.; Bennink, M. R. Inhibition of Azoxymethane-Induced Colon Cancer by Orange Juice Nutr. Cancer 2000, 36 (2) 224-229 (Pubitemid 30437044)
24. Xie, F.; Zhang, M.; Zhang, C. F.; Wang, Z. T.; Yu, B. Y.; Kou, J. P. Anti-inflammatory and analgesic activities of ethanolic extract and two limonoids from Melia toosendan fruit J. Ethnopharmacol. 2008, 117 (3) 463-466
25. Mandadi, K. K.; Jayaprakasha, G. K.; Bhat, N. G.; Patil, B. S. Red Mexican Grapefruit: A Novel Source for Bioactive Limonoids and their Antioxidant Activity Z. Naturforsch. 2007, 62c, 179-188 (Pubitemid 47226714)
26. Jayaprakasha, G. K.; Patil, B. S.; Bhat, N. G. Patent: A process for the isolation of limonoid glucosides from citrus seeds. US Patent Application. 2007/0237885 A1; WO 2007/118143A2, dated 18th Oct 2007, USA
27. Poulose, S. M.; Jayaprakasha, G. K.; Mayer, R. T.; Girennavar, B.; Patil, B. S. Purification of citrus limonoids and their differential inhibitory effects on human cytochrome P450 enzymes J. Sci. Food Agric. 2007, 87, 1699-1709 (Pubitemid 46983824)
28. Vikram, A.; Jayaprakasha, G. K.; Patil, B. S. Simultaneous determination of citrus limonoid aglycones and glucosides by high performance liquid chromatography Anal. Chim. Acta 2007, 590 (2) 180-186 (Pubitemid 46589373)
29. Ausubel, F. M.; Brent, R.; Kingston, R. E.; Moore, D. D.; Seidman, J. G.; Smith, J. A.; Struhl, K. Short protocols in molecular biology: a compendium of methods from current protocols in molecular biology; Wiley: New York, 2002.
30. Rozen, S.; Skaletsky, H. Primer3 on the WWW for general users and for biologist programmers Methods Mol. Biol. 2000, 132 (3) 365-386
31. Yeung, B.; Huang, D.; Sinicrope, F. PS-341 (bortezomib) induces lysosomal cathepsin B release and a caspase-2-dependent mitochondrial permeabilization and apoptosis in human pancreatic cancer cells J. Biol. Chem. 2006, 281 (17) 11923
32. Lin, H.; Lee, Y.; Chen, B; Tsai, M; Lu, J; Chou, C; Jow, G. Involvement of Bcl-2 family, cytochrome c and caspase 3 in induction of apoptosis by beauvericin in human non-small cell lung cancer cells Cancer Lett. 2005, 230 (2) 248-259 (Pubitemid 41612468)
33. Jacob, R.; Hasegawa, S.; Manners, G. The Potential of Citrus Limonoids as Anticancer Agents Perishables Handl. Q. 2000, 102, 6-8
34. Manners, G. D. Citrus Limonoids: Analysis, Bioactivity, and Biomedical Prospects J. Agric. Food Chem. 2007, 55 (21) 8285-8294 (Pubitemid 350013067)
35. Bonfoco, E.; Krainc, D.; Ankarcrona, M.; Nicotera, P.; Lipton, S. A. Apoptosis and Necrosis: Two Distinct Events Induced, Respectively, by Mild and Intense Insults with N-Methyl-D-Aspartate or Nitric Oxide/Superoxide in Cortical Cell Cultures Proc. Natl. Acad. Sci. U.S.A. 1995, 92 (16) 7162-7166
36. Porter, A. G.; Jänicke, R. U. Emerging roles of caspase-3 in apoptosis Cell Death Differ. 1999, 6 (2) 99-104 (Pubitemid 29082297)
37. Rochaa, G. d. G.; Simõesa, M.; Lúcioa, K. A.; Oliveirab, R. R.; Kaplanb, M. A. C.; Gattass, C. R. Natural triterpenoids from Cecropia lyratiloba are cytotoxic to both sensitive and multidrug resistant leukemia cell lines Bioorg. Med. Chem. 2007, 15 (23) 7355-7360 (Pubitemid 47539142)
38. Zhang, Z.; Li, M.; Wang, H.; Agrawal, S.; Zhang, R. Antisense therapy targeting MDM2 oncogene in prostate cancer: Effects on proliferation, apoptosis, multiple gene expression, and chemotherapy Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (20) 11636
39. Corsetti, G.; Pasini, E.; Assanelli, D.; Bianchi, R. Effects of acute caffeine administration on NOS and Bax/Bcl2 expression in the myocardium of rat Pharmacol. Res. 2008, 57 (1) 19-25
40. Kaiser, N.; Edelman, I. S. Calcium Dependence of Glucocorticoid-Induced Lymphocytolysis Proc. Natl. Acad. Sci. U.S.A. 1977, 74 (2) 638-642
41. 2+ concentration Arch. Biochem. Biophys. 1989, 269 (1) 365-370 (Pubitemid 19052317)
42. Whitfield, J. F. Calcium, calcium-sensing receptor and colon cancer Cancer Lett. 2009, 275 (1) 9-16
43. Macho, A.; Hirsch, T.; Marzo, I.; Marchetti, P.; Dallaporta, B.; Susin, S. A.; Zamzami, N.; Kroemer, G. Glutathione depletion is an early and calcium elevation is a late event of thymocyte apoptosis J. Immunol. 1997, 158 (10) 4612-4619 (Pubitemid 127483779)