The US Department of Agriculture’s MyPyramid guidelines introduced a near doubling of the dietary recommendations for vegetables including dry beans—an important food staple in many traditional diets that can improve public health and nutrition. Populations with high legume (peas, beans, lentils) consumption have a low risk of cancer and chronic degenerative diseases. Common beans ( Phaseolus vulgaris L.) are known as a rich, reliable source of non-digested compounds like fiber, phenolics, peptides and phytochemicals that are associated with health benefits. Emerging evidence indicates that common bean consumption is associated with reduced cancer risk in human populations, inhibiting carcinogenesis in animal models and inducing cell cycle arrest and apoptosis in cell cultures. Fiber may reduce the risk of premature death from all causes, whereas the whole non-digestible fraction from common beans exhibits anti-proliferative activity and induces apoptosis in vitro and in vivo colon cancer. The mechanisms responsible for this apparently protective role may include gene-nutrient interactions and modulation of proteins’ expression. This review investigates the potential health benefits and bioactivity of beans on tumor inhibition, highlighting studies involving functional compounds, mainly non-digestible fractions that modulate genes and proteins, thereby, unraveling their preventive role against the development of cancer.
References
[1]
Beninger, C.W.; Hosfield, G.L. Antioxidant activity of extracts, condensed tannin fractions, and pure flavonoids from Phaseolus vulgaris L. seed coat color genotypes. J. Agric. Food Chem. 2003, 51, 7879–7883, doi:10.1021/jf0304324.
[2]
Campos-Vega, R.; Vergara-Casta？eda, H.A.; Oomah, B.D. Functional Food Sources: Beans in Sight. In Beans: Nutrition, Consumption and Health; Popescu, E., Golubev, I., Eds.; Nova Science Publishers, Inc.: Hauppauge, NY, USA, 2011.
[3]
Report of the 30th Session of the Codex Committee on Nutrition and Foods for Special Dietary Uses. Available online: ftp://ftp.fao.org/codex/Circular_letters/CXCL2008/cl08_35e.pdf (accessed on 17 May 2013).
[4]
McCleary, B.V.; DeVries, J.W.; Rader, J.I.; Cohen, G.; Prosky, L.; Mugford, D.C.; Okuma, K. Determination of insoluble, soluble, and total dietary fiber (CODEX definition) by enzymatic-gravimetric method and liquid chromatography: Collaborative study. J. AOAC Int. 2012, 95, 824–844, doi:10.5740/jaoacint.CS2011_25.
[5]
Bobe, G.; Barrett, K.G.; Mentor-Marcel, R.A.; Saffiotti, U.; Young, M.R.; Colburn, N.H.; Albert, P.S.; Bennink, M.R.; Lanza, E. Dietary cooked navy beans and their fractions attenuate colon carcinogenesis in azoxymethane-induced ob/ob mice. Nutr. Cancer 2008, 60, 373–381, doi:10.1080/01635580701775142.
[6]
Mentor-Marcel, R.A.; Bobe, G.; Barrett, K.G.; Young, M.R.; Albert, P.S.; Bennink, M.R.; Lanza, E.; Colburn, N.H. Inflammation-associated serum and colon markers as indicators of dietary attenuation of colon carcinogenesis in ob/ob mice. Cancer Prev. Res. (Phila) 2009, 2, 60–69.
[7]
Hangen, L.; Bennink, M.R. Consumption of black beans and navy beans (Phaseolus vulgaris) reduced azoxymethane-induced colon cancer in rats. Nutr. Cancer 2002, 44, 60–65, doi:10.1207/S15327914NC441_8.
[8]
Lanza, E.; Hartman, T.J.; Albert, P.S.; Shields, R.; Slattery, M.; Caan, B.; Paskett, E.; Iber, F.; Kikendall, J.W.; Lance, P.; et al. High dry bean intake and reduced risk of advanced colorectal adenoma recurrence among participants in the polyp prevention trial. J. Nutr. 2006, 136, 1896–1903.
[9]
Mills, P.K.; Beeson, W.L.; Phillips, R.L.; Fraser, G.E. Cohort study of diet, lifestyle, and prostate cancer in Adventist men. Cancer 1989, 64, 598–604, doi:10.1002/1097-0142(19890801)64:3<598::AID-CNCR2820640306>3.0.CO;2-6.
[10]
Kolonel, L.N.; Hankin, J.H.; Whittemore, A.S.; Wu, A.H.; Gallagher, R.P.; Wilkens, L.R.; John, E.M.; Howe, G.R.; Dreon, D.M.; West, D.W.; Paffenbarger, R.S., Jr. Vegetables, fruits, legumes and prostate cancer: A multiethnic case-control study. Cancer Epidemiol. Biomarkers Prev. 2000, 9, 795–804.
[11]
Thompson, M.D.; Mensack, M.M.; Jiang, W.; Zhu, Z.; Lewis, M.R.; McGinley, J.N.; Brick, M.A.; Thompson, H.J. Cell signaling pathways associated with a reduction in mammary cancer burden by dietary common bean (Phaseolus vulgaris L.). Carcinogenesis 2012, 33, 226–232.
[12]
Ferlay, J.; Shin, H.R.; Bray, F.; Forman, D.; Mathers, C.; Parkin, D.M. Globocan 2008: Cancer Incidence and Mortality Worldwide. IARC Cancer Base, No. 10; International Agency for Research on Cancer: Lyon, France, 2010.
[13]
Armstrong, B.; Doll, R. Environmental factors and cancer incidence and mortality in different countries, with special reference to dietary practices. Int. J. Cancer 1975, 15, 617–631, doi:10.1002/ijc.2910150411.
[14]
Doll, R.; Peto, R. The causes of cancer: Quantitative estimates of avoidable risks of cancer in the United States today. J. Natl. Cancer Inst. 1981, 66, 1191–1308.
[15]
Food, Nutrition, Physical Activity, and the Prevention of Cancer: A Global Perspective; American Institute for Cancer Research: Washington, DC, USA, 2007.
[16]
Correa, P. Epidemiological correlations between diet and cancer frequency. Cancer Res. 1981, 41, 3685–3690.
[17]
Dahm, C.C.; Keogh, R.H.; Spencer, E.A.; Greenwood, D.C.; Key, T.J.; Fentiman, I.S.; Shipley, M.J.; Brunner, E.J.; Cade, J.E.; Burley, V.J.; et al. Dietary fiber and colorectal cancer risk: A nested case-control study using food diaries. J. Natl. Cancer Inst. 2010, 102, 614–626, doi:10.1093/jnci/djq092.
[18]
Bazzano, L.A.; He, J.; Ogden, L.G.; Loria, C.; Vupputuri, S.; Myers, L.; Whelton, P.K. Legume consumption and risk of coronary heart disease in US men and women: NHANES I Epidemiologic Follow-up Study. Arch. Intern. Med. 2001, 161, 2573–2578, doi:10.1001/archinte.161.21.2573.
[19]
Waldecker, M.; Kautenburger, T.; Daumann, H.; Busch, C.; Schrenk, D. Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon. J. Nutr. Biochem. 2008, 19, 587–593, doi:10.1016/j.jnutbio.2007.08.002.
[20]
Campos-Vega, R.; Guevara-Gonzalez, R.; Guevara-Olvera, B.; Oomah, B.D.; Loarca-Pi？a, G. Bean (Phaseolus vulgaris L.) polysaccharides modulate gene expression in human colon cancer cells (HT-29). Food Res. 2010, 43, 1057–1064.
[21]
Delzenne, N.; Cherbut, C.; Neyrinck, A. Prebiotics: Actual and potential effects in inflammatory and malignant colonic diseases. Curr. Opin. Clin. Nutr. Metab. Care 2003, 6, 581–586, doi:10.1097/00075197-200309000-00013.
[22]
Sengupta, S.; Muir, J.G.; Gibson, P.R. Does butyrate protect from colorectal cancer? J. Gastroenterol. Hepatol. 2006, 21, 209–218, doi:10.1111/j.1440-1746.2006.04213.x.
[23]
Feregrino-Pérez, A.A.; Berumen, L.C.; García-Alcocer, G.; Guevara-González, R.G.; Ramos-Gómez, M.; Reynoso-Camacho, R.; Acosta-Gallegos, J.A.; Loarca-Pi？a, G. Composition and chemopreventive effect of polysaccharides from common beans (Phaseolus vulgaris L.) on azoxymethane-induced colon cancer. J. Agric. Food Chem. 2008, 56, 8737–8744.
[24]
Vergara-Casta？eda, H.A.; Guevara-González, R.G.; Ramos-Gómez, M.; Reynoso-Camacho, R.; Guzmán-Maldonado, H.; Feregrino-Pérez, A.A.; Oomah, B.D.; Loarca-Pi？a, G. Non-digestible fraction of cooked bean (Phaseolus vulgaris L.) cultivar Bayo Madero suppresses colonic aberrant crypt foci in azoxymethane-induced rats. Food Funct. 2010, 1, 294–300.
[25]
Vergara-Casta？eda, H.A.; Guevara-González, R.G.; Guevara-Olvera, B.L.; Oomah, B.D.; Loarca-Pi？a, G.F. Non-digestible fraction of beans (Phaseolus vulgaris L.) modulates signalling pathway genes at an early stage of colon cancer in Sprague-Dawley rats. Br. J. Nutr. 2012, 108, S145–S154.
[26]
Bennink, M.R.; Om, A.S. Inhibition of Colon Cancer (CC) by soy phytochemicals but not by soy protein. FASEB J. 1998, 12, A655.
[27]
Bennink, M.R.; Om, A.S.; Miyagi, Y. Inhibition of colon cancer (CC) by soy flour but not by genistin or a mixture of isoflavones. FASEB J. 1999, 13, A50.
[28]
Rondini, E.A.; Bennink, M.R. Microarray analyses of genes differentially expressed by diet (black beans and soy flour) during azoxymethane-induced colon carcinogenesis in rats. J. Nutr. Metab. 2012, 2012, 351796.
[29]
Cruz-Bravo, R.K.; Guevara-González, R.; Ramos-Gómez, M.; García-Gasca, T.; Campos-Vega, R.; Oomah, B.D.; Loarca-Pi？a, G. Fermented nondigestible fraction from common bean (Phaseolus vulgaris L.) cultivar Negro 8025 modulates HT-29 cell behavior. J. Food Sci. 2011, 76, T41–T47.
[30]
Campos-Vega, R.; Reynoso-Camacho, R.; Pedraza-Aboytes, G.; Acosta-Gallegos, J.A.; Guzman-Maldonado, S.H.; Paredes-Lopez, O.; Oomah, B.D.; Loarca-Pi？a, G.F. Chemical composition and in vitro polysaccharide fermentation of different beans (Phaseolus vulgaris L.). J. Food Sci. 2009, 74, T59–T65.
[31]
Campos-Vega, R.; García-Gasca, T.; Guevara-González, R.; Ramos-Gómez, M.; Oomah, B.D.; Loarca-Pi？a, G. Human gut flora-fermented nondigestible fraction from cooked bean (Phaseolus vulgaris L.) modifies protein expression associated with apoptosis, cell cycle arrest, and proliferation in human adenocarcinoma colon cancer cells. J. Agric. Food Chem. 2012, 60, 12443–12450.
[32]
Lee, Y.K.; Hwang, J.T.; Lee, M.S.; Kim, Y.M.; Park, O.J. Kidney bean husk extracts exert antitumor effect by inducing apoptosis involving AMP-activated protein kinase signaling pathway. Ann. N. Y. Acad. Sci. 2009, 1171, 484–488, doi:10.1111/j.1749-6632.2009.04697.x.
[33]
Murtaugh, M.A.; Sweeney, C.; Giuliano, A.R.; Herrick, J.S.; Hines, L.; Byers, T.; Baumgartner, K.B.; Slattery, M.L. Diet patterns and breast cancer risk in Hispanic and non-Hispanic white women: The Four-Corners Breast Cancer Study. Am. J. Clin. Nutr. 2008, 87, 978–984.
[34]
Thompson, M.D.; Brick, M.A.; McGinley, J.N.; Thompson, H.J. Chemical composition and mammary cancer inhibitory activity of dry bean. Crop Sci. 2009, 49, 179–186, doi:10.2135/cropsci2008.04.0218.
[35]
Marshall, S. Role of insulin, adipocyte hormones, and nutrient-sensing pathways in regulating fuel metabolism and energy homeostasis: A nutritional perspective of diabetes, obesity, and cancer. Sci. STKE 2006, 346, re7, doi:10.1126/stke.3462006re7.
[36]
Um, S.H.; D’Alessio, D.; Thomas, G. Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab. 2006, 3, 393–402, doi:10.1016/j.cmet.2006.05.003.
Hynes, N.E.; Boulay, A. The mTOR pathway in breast cancer. J. Mammary Gland Biol. Neoplasia 2006, 11, 53–61, doi:10.1007/s10911-006-9012-6.
[39]
Mensack, M.M.; McGinley, J.N.; Thompson, H.J. Metabolomic analysis of the effects of edible dry beans (Phaseolus vulgaris L.) on tissue lipid metabolism and carcinogenesis in rats. Br. J. Nutr. 2012, 108, S155–S165.
[40]
Xu, B.; Chang, S.K.C. Comparative study on antiproliferation properties and cellular antioxidant activities of commonly consumed food legumes against nine human cancer cell lines. Food Chem. 2012, 134, 1287–1296, doi:10.1016/j.foodchem.2012.02.212.
[41]
García-Gasca, T.; García-Cruz, M.; Hernández-Rivera, E.; López-Matínez, J.; Casta？eda-Cuevas, A.L.; Yllescas-Gasca, L.; Rodríguez-Méndez, A.J.; Mendiola-Olaya, E.; Castro-Guillén, J.L.; Blanco-Labra, A. Effects of tepary bean (Phaseolus acutifolius) protease inhibitor and semi pure lectin fractions on cancer cells. Nutr. Cancer. 2012, 64, 1269–1278, doi:10.1080/01635581.2012.722246.
[42]
Nakaya, K.; Nabata, Y.; Ichiyanagi, T.; An, W.W. Stimulation of dendritic cell maturation and induction of apoptosis in leukemia cells by a heat-stable extract from azuki bean (Vigna angularis), a promising immunopotentiating food and dietary supplement for cancer prevention. Asian Pac. J. Cancer Prev. 2012, 13, 607–611, doi:10.7314/APJCP.2012.13.2.607.
[43]
Guzmán-Maldonado, S.H.; Paredes-López, O. Biotechnology for the Improvement of Nutritional Quality of Food Crop Plants. In Molecular Biotechnology for Plant Food Production; Paredes-Lopez, O., Ed.; Technomic Publishing: Lancaster, PA, USA, 1999; pp. 553–620.
[44]
De Mejía, E.G.; Casta？o-Tostado, E.; Loarca-Pi？a, G. Antimutagenic effects of natural phenolic compounds in beans. Mutat. Res. 1999, 441, 1–9, doi:10.1016/S1383-5718(99)00040-6.
[45]
Cardador-Martínez, A.; Loarca-Pi？a, G.; Oomah, B.D. Antioxidant activity in common beans (Phaseolus vulgaris L.). J. Agric. Food Chem. 2002, 50, 6975–6980.
[46]
Chan, S.T.; Yang, N.C.; Huang, C.S.; Liao, J.W.; Yeh, S.L. Quercetin enhances the antitumor activity of trichostatin A through upregulation of p53 protein expression in vitro and in vivo. PLoS One 2013, 8, e54255.
[47]
Choi, E.J.; Kim, G.H. Antiproliferative activity of daidzein and genistein may be related to ERα/c-erbB-2 expression in human breast cancer cells. Mol. Med. Rep. 2013, 7, 781–784.
[48]
Campos-Vega, R.; Loarca-Pi？a, G.; Oomah, B.D. Minor components of pulses and their potential impact on human health. Food Res. 2010, 43, 461–482, doi:10.1016/j.foodres.2009.09.004.
[49]
Bandugula, V.R.; N, R.P. 2-Deoxy-d-glucose and ferulic acid modulates radiation response signaling in non-small cell lung cancer cells. Tumour Biol. 2013, 34, 51–59.
[50]
Prabhakar, M.M.; Vasudevan, K.; Karthikeyan, S.; Baskaran, N.; Silvan, S.; Manoharan, S. Anti-cell proliferative efficacy of ferulic acid against 7,12-dimethylbenz(a) anthracene induced hamster buccal pouch carcinogenesis. Asian Pac. J. Cancer Prev. 2012, 13, 5207–5211, doi:10.7314/APJCP.2012.13.10.5207.
[51]
Yuan, B.; Imai, M.; Kikuchi, H.; Fukushima, S.; Hazama, S.; Akaike, T.; Yoshino, Y.; Ohyama, K.; Hu, X.; Pei, X.; Toyoda, H. Cytocidal Effects of Polyphenolic Compounds, Alone or in Combination with, Anticancer Drugs against Cancer Cells: Potential Future Application of the Combinatory Therapy, Apoptosis and Medicine. Available online: http://www.intechopen.com/books/apoptosis-and-medicine/cytocidal-effects-of-polyphenolic-compounds-alone-or-in-combination-with-anticancer-drugs-against-ca (accessed on 21 May 2013).
[52]
Eli, M.; Li, D.S.; Zhang, W.W.; Kong, B.; Du, C.S.; Wumar, M.; Mamtimin, B.; Sheyhidin, I.; Hasim, A. Decreased blood riboflavin levels are correlated with defective expression of RFT2 gene in gastric cancer. World J. Gastroenterol. 2012, 18, 3112–3118, doi:10.3748/wjg.v18.i24.3112.
Noto, J.M.; Gaddy, J.A.; Lee, J.Y.; Piazuelo, M.B.; Friedman, D.B.; Colvin, D.C.; Romero-Gallo, J.; Suarez, G.; Loh, J.; Slaughter, J.C.; et al. Iron deficiency accelerates Helicobacter pylori-induced carcinogenesis in rodents and humans. J. Clin. Invest. 2013, 123, 479–492, doi:10.1172/JCI64373.
[55]
Llaverias, G.; Escolà-Gil, J.C.; Lerma, E.; Julve, J.; Pons, C.; Cabré, A.; Cofán, M.; Ros, E.; Sánchez-Quesada, J.L.; Blanco-Vaca, F. Phytosterols inhibit the tumor growth and lipoprotein oxidizability induced by a high-fat diet in mice with inherited breast cancer. J. Nutr. Biochem. 2013, 24, 39–48, doi:10.1016/j.jnutbio.2012.01.007.
