The inhibition of colon cancer development by black rice bran on BALB/C Mice

Slamet Budijanto; Yeni Kurniati; Lilis Nuraida; Fitriya Nur Annisa Dewi; Bambang Pontjo Priosoeryanto; Nancy Dewi Yuliana; Ardiansyah; Uus Saepuloh; Safrida; Hitoshi Shirakawa; Slamet Budijanto; Yeni Kurniati; Lilis Nuraida; Fitriya Nur Annisa Dewi; Bambang Pontjo Priosoeryanto; Nancy Dewi Yuliana; Ardiansyah; Uus Saepuloh; Safrida; Hitoshi Shirakawa

doi:10.3934/agrfood.2024042

AIMS Agriculture and Food

2024, Volume 9, Issue 3: 789-800. doi: 10.3934/agrfood.2024042

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Research article

The inhibition of colon cancer development by black rice bran on BALB/C Mice

1.
Department of Food Science and Technology, Faculty of Agricultural Technology, IPB University, Dramaga, Bogor, 16680, Indonesia
2.
Southeast Asian Food and Agricultural Science and Technology Center, IPB University, Dramaga, Bogor 16680, Indonesia
3.
Primate Research Center, IPB University, Lodaya II/5, Bogor, 16151, Indonesia
4.
School of Veterinary and Biomedical Medicine, IPB University, Dramaga, Bogor 16680, Indonesia
5.
Department of Veterinary Clinics, Reproduction, and Pathology, IPB University, Dramaga, Bogor, 16680, Indonesia
6.
Department of Food Technology, Universitas Bakrie, Bakrie Tower Kawasan Epicentrum, Jalan HR Rasuna Said, Jakarta, 12920, Indonesia
7.
Department of Nutrition, Faculty of Public Health, University of Teuku Umar, Meureubo, Meulaboh, 23681, Indonesia
8.
International Education and Research Center for Food Agricultural Immunology, Graduate School of Agricultural Science, Tohoku University, Aoba-ku, Sendai 980-0845, Japan

Received: 13 February 2024 Revised: 21 June 2024 Accepted: 02 July 2024 Published: 16 July 2024

Black rice bran (BRB) is well-known for its high antioxidant activity and its pivotal role in preventing colon cancer. The present study aims to investigate the effects of BRB administration on BALB/C mice induced with azoxymethane (AOM) and dextran sodium sulphate (DSS). The 24 mice were divided into three groups: the group induced by colon cancer (C+), the group induced by cancer and given the BRB diet (C+BRB), and the normal group (C−). Both the C− and C+ groups were given a standard AIN-93 M diet containing cellulose fiber. After 16 weeks, the mice were anesthetized, and the colonic tissue was identified for nodule distribution, histopathological observation, and mRNA expression analysis of proliferating cell nuclear antigen (PCNA), caspase-3, and caspase-8 genes using qRT PCR technique. Nodule distribution in the C+BRB group showed a significant decrease compared to the C+ group, with 1.65 ± 0.71 nodule/cm2 vs. 5.73 ± 2.93 nodule/cm². Then, the colon weight was significantly decreased in the C+BRB group, at 0.19 ± 0.04 (g) compared to 0.25 ± 0.03 (g) in the C+ group. Also, the BRB diet in the C+BRB group significantly decreased PCNA mRNA expression compared to the C+ group, with values of 0.58 ± 0.09-fold change vs. 5.22 ± 0.80-fold change. Conversely, increased the mRNA expression of caspase-3 (0.91 ± 0.20-fold change vs. 0.36 ± 0.15-fold change) and caspase-8 (0.51 ± 0.18-fold change vs. 0.13 ± 0.31-fold change). In conclusion, administration of BRB inhibited the rate of cancer development by suppressing cancer cell proliferation and inducing apoptosis.
- AOM/DSS,
- black rice bran,
- caspase-3,
- caspase-8,
- colon cancer,
- PCNA
Citation: Slamet Budijanto, Yeni Kurniati, Lilis Nuraida, Fitriya Nur Annisa Dewi, Bambang Pontjo Priosoeryanto, Nancy Dewi Yuliana, Ardiansyah, Uus Saepuloh, Safrida, Hitoshi Shirakawa. The inhibition of colon cancer development by black rice bran on BALB/C Mice[J]. AIMS Agriculture and Food, 2024, 9(3): 789-800. doi: 10.3934/agrfood.2024042

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Abstract

Black rice bran (BRB) is well-known for its high antioxidant activity and its pivotal role in preventing colon cancer. The present study aims to investigate the effects of BRB administration on BALB/C mice induced with azoxymethane (AOM) and dextran sodium sulphate (DSS). The 24 mice were divided into three groups: the group induced by colon cancer (C+), the group induced by cancer and given the BRB diet (C+BRB), and the normal group (C−). Both the C− and C+ groups were given a standard AIN-93 M diet containing cellulose fiber. After 16 weeks, the mice were anesthetized, and the colonic tissue was identified for nodule distribution, histopathological observation, and mRNA expression analysis of proliferating cell nuclear antigen (PCNA), caspase-3, and caspase-8 genes using qRT PCR technique. Nodule distribution in the C+BRB group showed a significant decrease compared to the C+ group, with 1.65 ± 0.71 nodule/cm2 vs. 5.73 ± 2.93 nodule/cm². Then, the colon weight was significantly decreased in the C+BRB group, at 0.19 ± 0.04 (g) compared to 0.25 ± 0.03 (g) in the C+ group. Also, the BRB diet in the C+BRB group significantly decreased PCNA mRNA expression compared to the C+ group, with values of 0.58 ± 0.09-fold change vs. 5.22 ± 0.80-fold change. Conversely, increased the mRNA expression of caspase-3 (0.91 ± 0.20-fold change vs. 0.36 ± 0.15-fold change) and caspase-8 (0.51 ± 0.18-fold change vs. 0.13 ± 0.31-fold change). In conclusion, administration of BRB inhibited the rate of cancer development by suppressing cancer cell proliferation and inducing apoptosis.

References

[1]	World Health Organization (2017) Cancer. Available from: http://www.who.int/mediacentre/.
[2]	American Cancer Society (2017) Cancer Facts and Figures in 2017. American Cancer Society. Inc. Surveillance Research.
[3]	Datsis A, Tsoga A, Langouretos V (2010) The role of functional foods in the prevention of colorectal cancer. Hellenic J Surg 82: 224–232. https://doi.org/10.1007/s13126-010-0035-5 doi: 10.1007/s13126-010-0035-5
[4]	Moongngarm A, Daomukda N, Khumpika S (2012) Chemical compositions, phytochemicals, and antioxidant capacity of rice bran, rice bran layer, and rice germ. Apcbee Proc 2: 73–79. https://doi.org/10.1016/j.apcbee.2012.06.014 doi: 10.1016/j.apcbee.2012.06.014
[5]	Antczak C, Takagi T, Ramirez CN, et al. (2009) Live cell imaging of caspase activation for high content screening. J Biomol Screen 14: 956–969. https://doi.org/10.1177/1087057109343207 doi: 10.1177/1087057109343207
[6]	Shi Y (2002) Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 9: 459–470. https://doi.org/10.1016/S1097-2765(02)00482-3 doi: 10.1016/S1097-2765(02)00482-3
[7]	Zheng Z, Shetty K (2000) Solid-state bioconversion of phenolics from cranberry pomace and role of Lentinus edodes beta-glucosidase. J Agric Food Chem 48: 895–900. https://doi.org/10.1021/jf990972u doi: 10.1021/jf990972u
[8]	Bravo R, Macdonald-Bravo H (1987) Existence of two populations of cyclin/proliferating cell nuclear antigen during the cell cycle: association with DNA replication sites. J Cell Biol 105: 1549–1554. https://doi.org/10.1083/jcb.105.4.1549 doi: 10.1083/jcb.105.4.1549
[9]	Zulfafamy KE, Ardiansyah, Budijanto S (2018) Antioxidative properties and cytotoxic activity against colon cancer cell WiDr of Rhizopus oryzae and Rhizopus oligosporus-fermented black rice bran extract. Curr Res Nutr Food Sci 6: 23–24. https://doi.org/10.12944/CRNFSJ.6.1.03 doi: 10.12944/CRNFSJ.6.1.03
[10]	Glasauer A, Chandel NS (2014) Targeting antioxidants for cancer therapy. Biochem Pharmacol 92: 90–101. https://doi.org/10.1016/j.bcp.2014.07.017 doi: 10.1016/j.bcp.2014.07.017
[11]	Suzuki R, Kohno H, Sugie S, et al. (2006) Strain differences in the susceptibility to azoxymethane and dextran sodium sulfate-induced colon carcinogenesis in mice. Carcinogenesis 27: 162–169. https://doi.org/10.1093/carcin/bgi205 doi: 10.1093/carcin/bgi205
[12]	Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408. https://doi.org/10.1006/meth.2001.1262 doi: 10.1006/meth.2001.1262
[13]	Phutthaphadoong S, Yamada Y, Hirata A, et al. (2010) Chemopreventive effect of fermented brown rice and rice bran (FBRA) on the inflammation-related colorectal carcinogenesis in ApcMin/+ mice. Oncol Rep 23: 53–59. https://doi.org/10.3892/or_00000605 doi: 10.3892/or_00000605
[14]	Trujillo EB, Bergerson ASL, Graf JC, et al. (2005) Cancer in American society for parenteral and enteral nutrition support practice manual. Nutr Care Org 4: 150–170.
[15]	Norazalina S, Norhaizan ME, Hairuszah I, et al. (2010) Anticarcinogenic efficacy of phytic acid extracted from rice bran on azoxymethane-induced colon carcinogenesis in rats. Exp Toxicol Pathol 62: 259–268. https://doi.org/10.1016/j.etp.2009.04.002 doi: 10.1016/j.etp.2009.04.002
[16]	Tomita H, Kuno T, Yamada Y, et al. (2008) Preventive effect of fermented brown rice and rice bran on N-methyl-N'-nitro-N-nitrosoguanidine-induced gastric carcinogenesis in rats. Oncol Rep 19: 11–15. https://doi.org/10.3892/or.19.1.11 doi: 10.3892/or.19.1.11
[17]	Kampa M, Alexaki VI, Notas G, et al (2004) Antiproliferative and apoptotic effects of selective phenolic acids on T47D human breast cancer cells: potential mechanisms of action. Breast Cancer Res 6: R63–R74. https://doi.org/10.1186/bcr752 doi: 10.1186/bcr752
[18]	Rosenberg DW, Giardina C, Tanaka T (2009) Mouse models for the study of colon carcinogenesis. Carcinogen 30: 183–196. https://doi.org/10.1093/carcin/bgn267 doi: 10.1093/carcin/bgn267
[19]	Lupton JR (2004) Microbial degradation products influence colon cancer risk: the butyrate controversy. J Nutr 134: 479–482. https://doi.org/10.1093/jn/134.2.479 doi: 10.1093/jn/134.2.479
[20]	Andoh A, Fujiyama Y (2004) Anti-inflammatory roles of dietary fiber and short-chain fatty acids as regards inflammatory bowel diseases. Agro Food Ind Hi-Tech 15: 42–43.
[21]	Katyama M, Yoshimi N, Yamda Y, et al. (2002) Preventive effect of fermented black rice and rice bran against colon carcinogenesis in male F344 rats. J Oncol 9: 7–22. https://doi.org/10.3892/or.9.4.817 doi: 10.3892/or.9.4.817
[22]	Yi W, Fischer J, Krewer G, et al. (2005) Phenolic compounds from blueberries can inhibit colon cancer cell proliferation and induce apoptosis. J Agric Food Chem 53: 7320–7329. https://doi.org/10.1021/jf051333o doi: 10.1021/jf051333o
[23]	Yin MC, Lin CC, Wu HC, et al. (2009) Apoptotic effects of protocatechuic acid in human breast, lung, liver, cervix, and prostate cancer cells: potential mechanisms of action. J Agric Food Chem 57: 6468–6473. https://doi.org/10.1021/jf9004466 doi: 10.1021/jf9004466
[24]	Muntana N, Prasong S (2010) Study on total phenolic contents and their antioxidant activities of Thai white, red and black rice bran extracts. Pak J Biol Sci 13: 170–174. https://doi.org/10.3923/pjbs.2010.170.174 doi: 10.3923/pjbs.2010.170.174
[25]	Kim HY, Kim JH, Yang SB, et al. (2007) A polysaccharide extracted from rice bran fermented with Lentinus edodes enhances natural killer cell activity and exhibits anticancer effects. J Med Food 10: 25–31. https://doi.org/10.1089/jmf.2006.116 doi: 10.1089/jmf.2006.116
[26]	Zeng H, Lazarova DL, Bordonaro M (2014) Mechanisms linking dietary fiber, gut microbiota and colon cancer prevention. World J Gastrointest Oncol 6: 41–51. https://doi.org/10.4251/wjgo.v6.i2.41 doi: 10.4251/wjgo.v6.i2.41
[27]	Kuno T, Nagano A, Mori Y et al. (2016) Preventive effect of fermented brown rice and rice bran against Prostate Carcinogenesis in TRAP Rats. Nutrient 87: 421. https://doi.org/10.3390/nu8070421 doi: 10.3390/nu8070421
[28]	Gschwantler M, Kriwanek S, Langner E, et al. (2002) High-grade dysplasia and invasive carcinoma in colorectal adenomas: a multivariate analysis of the impact of adenoma and patient characteristics. Eur J Gastroenterol Hepatol 14: 183–188. https://doi.org/10.1097/00042737-200202000-00013 doi: 10.1097/00042737-200202000-00013
[29]	Rosa LDS, Silva NJA, Soares NCP, et al. (2016) Anticancer properties of phenolic acids in colon cancer—A review. J Nutr Food Sci 6: 1000468.
[30]	Ruemmele FM, Schwartz S, Seidman EG, et al. (2003) Butyrate induced Caco-2 cell apoptosis is mediated via the mitochondrial pathway. Gut 52: 94–100. https://doi.org/10.1136/gut.52.1.94 doi: 10.1136/gut.52.1.94

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