Bioprocessed Black Rice Bran Potentiates the Growth Inhibitory Activity of an Immune Checkpoint Inhibitor against Murine Colon Carcinoma — Oak Academic Publishing
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Bioprocessed Black Rice Bran Potentiates the Growth Inhibitory Activity of an Immune Checkpoint Inhibitor against Murine Colon Carcinoma
STR Biotech Co., Ltd., Chuncheon, Republic of Korea
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STR Biotech Co., Ltd., Chuncheon, Republic of Korea
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STR Biotech Co., Ltd., Chuncheon, Republic of Korea
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STR Biotech Co., Ltd., Chuncheon, Republic of Korea
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STR Biotech Co., Ltd., Chuncheon, Republic of Korea
,
STR Biotech Co., Ltd., Chuncheon, Republic of Korea
,
STR Biotech Co., Ltd., Chuncheon, Republic of Korea
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U.S. Department of Agriculture, Western Regional Research Center, Agricultural Research Service, Albany, CA, USA
1 STR Biotech Co., Ltd., Chuncheon, Republic of Korea
2 STR Biotech Co., Ltd., Chuncheon, Republic of Korea
3 STR Biotech Co., Ltd., Chuncheon, Republic of Korea
4 STR Biotech Co., Ltd., Chuncheon, Republic of Korea
5 STR Biotech Co., Ltd., Chuncheon, Republic of Korea
6 STR Biotech Co., Ltd., Chuncheon, Republic of Korea
7 STR Biotech Co., Ltd., Chuncheon, Republic of Korea
8 U.S. Department of Agriculture, Western Regional Research Center, Agricultural Research Service, Albany, CA, USA
This study determined the effect of orally fed polysaccharide-rich bioprocessed (fermented) black rice bran produced by culturing with shiitake ( Lentinus edodes ) mushroom mycelium on CT-26 colon cancer cells in vivo in an intracutaneously transplanted mouse tumor alone and in combination with intraperitoneally administered anti-PD-1 immune checkpoint inhibitor. Analysis of the isolated tumor weights at the end of the study shows that the average tumor size in control mice is 3.78 grams, and the average tumor size in mice treated with anti-PD-1 antibody is 2.16 grams. The average tumor size in mice treated with BRB-F alone is 2.25 grams, and the average tumor size in mice treated with anti-PD-1 antibody BRB-F combination is 1.38 grams. Thus, BRB-F or anti-PD-1 antibody alone each reduce tumor size by 40.5% or 42.9%, whereas the combination of BRB-F and anti-PD-1 antibody reduces tumor size by 63.5%, with their cooperative effect being statistically significant. The observed anti-tumor effects were accompanied by a series of biomarkers associated with cancer formation and inhibition. These results indicate that the reported potentiation of cancer therapy using drug-based medical chemotherapies with added checkpoint inhibitors in human patients are mechanistically similar with the functional food evaluated in the present study. These beneficial effects in mice challenge clinicians to investigate if the black rice bran food product can also protect against human cancer.
Ghasemzadeh, A., Karbalaii, M.T., Jaafar, H.Z.E. and Rahmat, A. (2018) Phytochemical Constituents, Antioxidant Activity, and Antiproliferative Properties of Black, Red, and Brown Rice Bran. Chemistry Central Journal, 12, Article No. 17. https://doi.org/10.1186/s13065-018-0382-9
Suttiarporn, P., Chumpolsri, W., Mahatheeranont, S., Luangkamin, S., Teepsawang, S. and Leardkamolkarn, V. (2015) Structures of Phytosterols and Triterpenoids with Potential Anti-Cancer Activity in Bran of Black Non-Glutinous Rice. Nutrients, 7, 1672-1687. https://doi.org/10.3390/nu7031672
Tan, B.L., Norhaizan, M.E. and Chan, L.C. (2023) Rice Bran: From Waste to Nutritious Food Ingredients. Nutrients, 15, Article No. 2503. https://doi.org/10.3390/nu15112503
Bhawamai, S., Lin, S.-H., Hou, Y.-Y. and Chen, Y.-H. (2016) Thermal Cooking Changes the Profile of Phenolic Compounds, but Does Not Attenuate the Anti-Inflammatory Activities of Black Rice. Food & Nutrition Research, 60, Article No. 32941. https://doi.org/10.3402/fnr.v60.32941
Nam, S.H., Choi, S.P., Kang, M.Y., Koh, H.J., Kozukue, N. and Friedman, M. (2005) Bran Extracts from Pigmented Rice Seeds Inhibit Tumor Promotion in Lymphoblastoid B Cells by Phorbol Ester. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association, 43, 741-745. https://doi.org/10.1016/j.fct.2005.01.014
Nam, S.H., Choi, S.P., Kang, M.Y., Kozukue, N. and Friedman, M. (2005) Antioxidative, Antimutagenic, and Anticarcinogenic Activities of Rice Bran Extracts in Chemical and Cell Assays. Journal of Agricultural and Food Chemistry, 53, 816-822. https://doi.org/10.1021/jf0490293
Choi, S.P., Kim, S.P., Kang, M.Y., Nam, S.H. and Friedman, M. (2010) Protective Effects of Black Rice Bran against Chemically-Induced Inflammation of Mouse Skin. Journal of Agricultural and Food Chemistry, 58, 10007-10015. https://doi.org/10.1021/jf102224b
Kim, S.P., Kang, M.Y., Nam, S.H. and Friedman, M. (2012) Dietary Rice Bran Component γ-Oryzanol Inhibits Tumor Growth in Tumor-Bearing Mice. Molecular Nutrition & Food Research, 56, 935-944. https://doi.org/10.1002/mnfr.201200057
Choi, S.P., Kim, S.P., Nam, S.H. and Friedman, M. (2013) Antitumor Effects of Dietary Black and Brown Rice Brans in Tumor-Bearing Mice: Relationship to Composition. Molecular Nutrition & Food Research, 57, 390-400. https://doi.org/10.1002/mnfr.201200515
Tonchaiyaphum, P., Arpornchayanon, W., Khonsung, P., Chiranthanut, N., Pitchakarn, P. and Kunanusorn, P. (2021) Gastroprotective Activities of Ethanol Extract of Black Rice Bran (Oryza sativa L.) in Rats. Molecules, 26, Article No. 3812. https://doi.org/10.3390/molecules26133812
Kim, J.-M., Hong, S.-G., Song, B.-S., Sohn, H.-J., Baik, H. and Sung, M.-K. (2020) Efficacy of Cereal-Based Oral Nutrition Supplement on Nutritional Status, Inflammatory Cytokine Secretion and Quality of Life in Cancer Patients under Cancer Therapy. Journal of Cancer Prevention, 25, 55-63. https://doi.org/10.15430/JCP.2020.25.1.55
Kwon, K.S., Hwang, W.S., Lee, K.H., Kim, K.J., Lee, W.Y., Kim, J., et al. (2023) Protection of Allergic Asthma in Mice by Black Rice Bran Bioprocessed with Shiitake Mushroom Mycelia. Food and Nutrition Sciences, 14, 341-368. https://doi.org/10.4236/fns.2023.144023
Kim, S.P., Lee, J.R., Kwon, K.S., Jang, Y.J., Kim, J., Yu, K.H., et al. (2021). A Bioprocessed Black Rice Bran Glutathione-Enriched Yeast Extract Protects Rats and Mice against Alcohol-Induced Hangovers. Food and Nutrition Sciences, 12, 223-238. https://doi.org/10.4236/fns.2021.123018
Kim, S.P., Park, S.O., Lee, S.J., Nam, S.H. and Friedman, M. (2013) A Polysaccharide Isolated from the Liquid Culture of Lentinus edodes (Shiitake) Mushroom Mycelia Containing Black Rice Bran Protects Mice against a Salmonella Lipopolysaccharide-Induced Endotoxemia. Journal of Agricultural and Food Chemistry, 61, 10987-10994. https://doi.org/10.1021/jf403173k
Kim, S.P., Lee, S.J., Nam, S.H. and Friedman, M. (2018) The Composition of a Bioprocessed Shiitake (Lentinus edodes) Mushroom Mycelia and Rice Bran Formulation and Its Antimicrobial Effects against Salmonella enterica subsp. enterica Serovar Typhimurium Strain SL1344 in Macrophage Cells and in Mice. BMC Complementary and Alternative Medicine, 18, Article No. 322. https://doi.org/10.1186/s12906-018-2365-8
Song, Y., Fu, Y., Xie, Q., Zhu, B., Wang, J. and Zhang, B. (2020) Anti-Angiogenic Agents in Combination with Immune Checkpoint Inhibitors: A Promising Strategy for Cancer Treatment. Frontiers in Immunology, 11, Article No. 1956. https://doi.org/10.3389/fimmu.2020.01956
Bagchi, S., Yuan, R. and Engleman, E.G. (2021) Immune Checkpoint Inhibitors for the Treatment of Cancer: Clinical Impact and Mechanisms of Response and Resistance. Annual Review of Pathology, 16, 223-249. https://doi.org/10.1146/annurev-pathol-042020-042741
Cui, C., Barberi, T., Suresh, R. and Friedman, A.D. (2021) Adoptive Transfer of Immature Myeloid Cells Lacking NF-κB p50 (p50-IMC) Impedes the Growth of MHC-Matched High-Risk Neuroblastoma. Molecular Oncology, 15, 1783-1796. https://doi.org/10.1002/1878-0261.12904
Meybodi, S.M., Farasati Far, B., Pourmolaei, A., Baradarbarjastehbaf, F., Safaei, M., Mohammadkhani, N. and Samadani, A.A. (2023) Immune Checkpoint Inhibitors Promising Role in Cancer Therapy: Clinical Evidence and Immune-Related Adverse Events. Medical Oncology (Northwood, London, England), 40, Article No. 243. https://doi.org/10.1007/s12032-023-02114-6
Hwang, J., Zhang, W., Dhananjay, Y., An, E.-K., Kwak, M., You, S., et al. (2021) Astragalus membranaceus Polysaccharides Potentiate the Growth-Inhibitory Activity of Immune Checkpoint Inhibitors against Pulmonary Metastatic Melanoma in Mice. International Journal of Biological Macromolecules, 182, 1292-1300. https://doi.org/10.1016/j.ijbiomac.2021.05.073
Narumi, S., Finke, J.H. and Hamilton, T.A. (1990) Interferon Gamma and Interleukin 2 Synergize to Induce Selective Monokine Expression in Murine Peritoneal Macrophages. The Journal of Biological Chemistry, 265, 7036-7041.
Fu, Y., Peng, Y., Zhao, S., Mou, J., Zeng, L., Jiang, X., et al. (2021) Combination Foretinib and Anti-PD-1 Antibody Immunotherapy for Colorectal Carcinoma. Frontiers in Cell and Developmental Biology, 9, Article ID: 689727. https://doi.org/10.3389/fcell.2021.689727
Trop, S., Samsonov, D., Gotsman, I., Alper, R., Diment, J. and Ilan, Y. (1999) Liver-Associated Lymphocytes Expressing NK1.1 Are Essential for Oral Immune Tolerance Induction in a Murine Model. Hepatology (Baltimore, Md.), 29, 746-755. https://doi.org/10.1002/hep.510290334
Roden, M.M., Lee, K.H., Panelli, M.C. and Marincola, F.M. (1999) A Novel Cytolysis Assay Using Fluorescent Labeling and Quantitative Fluorescent Scanning Technology. Journal of Immunological Methods, 226, 29-41. https://doi.org/10.1016/s0022-1759(99)00039-3
Xie, Q., Cho, H.J., Calaycay, J., Mumford, R.A., Swiderek, K.M., Lee, T.D., et al. (1992) Cloning and Characterization of Inducible Nitric Oxide Synthase from Mouse Macrophages. Science, 256, 225-228. https://doi.org/10.1126/science.1373522
Duperrier, K., Eljaafari, A., Dezutter-Dambuyant, C., Bardin, C., Jacquet, C., Yoneda, K., et al. (2000) Distinct Subsets of Dendritic Cells Resembling Dermal DCs Can Be Generated in Vitro from Monocytes, in the Presence of Different Serum Supplements. Journal of Immunological Methods, 238, 119-131. https://doi.org/10.1016/s0022-1759(00)00147-2
Finetti, F., Travelli, C., Ercoli, J., Colombo, G., Buoso, E. and Trabalzini, L. (2020) Prostaglandin E2 and Cancer: Insight into Tumor Progression and Immunity. Biology, 9, Article No. 434. https://doi.org/10.3390/biology9120434
Kim, S.P., Kang, M.Y., Kim, J.H., Nam, S.H. and Friedman, M. (2011) Composition and Mechanism of Antitumor Effects of Hericium erinaceus Mushroom Extracts in Tumor-Bearing Mice. Journal of Agricultural and Food Chemistry, 59, 9861-9869. https://doi.org/10.1021/jf201944n
Beers, M.H. (2006) The Merck Manual of Diagnosis and Therapy. 18th Edition, Merck Research Laboratories, Whitehouse Station.
Kusnik, A., Renjithlal, S.L.M., Chodos, A., Shanmukhappa, S.C., Eid, M.M., Renjith, K.M. and Alweis, R. (2023) Trends in Colorectal Cancer Mortality in the United States, 1999-2020. Gastroenterology Research, 16, 217-225. https://doi.org/10.14740/gr.v0i0.1631
Lee, K.H., Jang, Y.J., Hwang, W.S., Kwon, K.S., Lee, W.Y., Kim, J., et al. (2022) Edible Algae (Ecklonia cava) Bioprocessed with Mycelia of Shiitake (Lentinula edodes) Mushrooms in Liquid Culture and Its Isolated Fractions Protect Mice against Allergic Asthma. BMC Complementary Medicine and Therapies, 22, Article No. 242. https://doi.org/10.1186/s12906-022-03705-y
Friedman, M., McQuistan, T., Hendricks, J.D., Pereira, C. and Bailey, G.S. (2007) Protective Effect of Dietary Tomatine against Dibenzo [a,l]pyrene (DBP)-Induced Liver and Stomach Tumors in Rainbow Trout. Molecular Nutrition & Food Research, 51, 1485-1491. https://doi.org/10.1002/mnfr.200700176
Kim, S.P., Nam, S.H. and Friedman, M. (2015) The Tomato Glycoalkaloid α-Tomatine Induces Caspase-Independent Cell Death in Mouse Colon Cancer CT-26 Cells and Transplanted Tumors in Mice. Journal of Agricultural and Food Chemistry, 63, 1142-1150. https://doi.org/10.1021/jf5040288
Kozukue, N., Kim, D.-S., Choi, S.-H., Mizuno, M. and Friedman, M. (2023) Isomers of the Tomato Glycoalkaloids α-Tomatine and Dehydrotomatine: Relationship to Health Benefits. Molecules, 28, Article No. 3621. https://doi.org/10.3390/molecules28083621
Friedman, M. (2015) Chemistry and Anticarcinogenic Mechanisms of Glycoalkaloids Produced by Eggplants, Potatoes, and Tomatoes. Journal of Agricultural and Food Chemistry, 63, 3323-3337. https://doi.org/10.1021/acs.jafc.5b00818
Li, X., Kahlon, T., Wang, S.C. and Friedman, M. (2021) Low Acrylamide Flatbreads Prepared from Colored Rice Flours and Relationship to Asparagine and Proximate Content of Flours and Flatbreads. Foods, 10, Article No. 2909. https://doi.org/10.3390/foods10122909
Friedman, M. (2018) Analysis, Nutrition, and Health Benefits of Tryptophan. International Journal of Tryptophan Research: IJTR, 11, 1-12. https://doi.org/10.1177/1178646918802282
Li, X., Kahlon, T., Wang, S.C. and Friedman, M. (2021). Low Acrylamide Flatbreads from Colored Corn and Other Flours. Foods (Basel, Switzerland), 10, Article No. 2495. https://doi.org/10.3390/foods10102495
Friedman, M. and Brandon, D.L. (2001) Nutritional and Health Benefits of Soy Proteins. Journal of Agricultural and Food Chemistry, 49, 1069-1086. https://doi.org/10.1021/jf0009246
Brandon, D.L. and Friedman, M. (2002) Immunoassays of Soy Proteins. Journal of Agricultural and Food Chemistry, 50, 6635-6642. https://doi.org/10.1021/jf020186g
Juneja, V.K., Friedman, M., Mohr, T.B., Silverman, M. and Mukhopadhyay, S. (2018) Control of Bacillus cereus Spore Germination and Outgrowth in Cooked Rice during Chilling by Nonorganic and Organic Apple, Orange, and Potato Peel Powders. Journal of Food Processing and Preservation, 42, e13558. https://doi.org/10.1111/jfpp.13558
Crawford, L.M., Kahlon, T.S., Chiu, M.M., Wang, S.C. and Friedman, M. (2019) Acrylamide Content of Experimental and Commercial Flatbreads. Journal of Food Science, 84, 659-666. https://doi.org/10.1111/1750-3841.14456
Rounds, L., Cody C.M., Havens X., Feinstein, Y., Friedman, M. and Ravishankar, S. (2013) Concentration-Dependent Inhibition of Escherichia coli O157:H7 and Heterocyclic Amines in Heated Ground Beef Patties by Apple and Olive Extracts, Onion Powder and Clove Bud Oil. Meat Science, 94, 461-467. https://doi.org/10.1016/j.meatsci.2013.03.010