A mechanistic review: potential chronic disease-preventive properties of sorghum.


Journal

Journal of the science of food and agriculture
ISSN: 1097-0010
Titre abrégé: J Sci Food Agric
Pays: England
ID NLM: 0376334

Informations de publication

Date de publication:
May 2021
Historique:
revised: 12 10 2020
received: 24 08 2020
accepted: 11 11 2020
pubmed: 13 11 2020
medline: 24 4 2021
entrez: 12 11 2020
Statut: ppublish

Résumé

Sorghum is one of the most widely cultivated crops, and is used in foods, domestic animal feedstuffs, alcohol production, and biofuels. Recently, many research groups have demonstrated that sorghum contains various components that are strongly associated with the prevention of major human chronic diseases such as obesity, diabetes, atherosclerosis, cancer, and inflammation. However, to use sorghum more widely as a food for the potential prevention and treatment of human chronic diseases, more studies will be required to elucidate the biological mechanisms. In this review paper, we highlight multiple findings to propose a mechanistic link between sorghum consumption and reduced risk of chronic diseases. © 2020 Society of Chemical Industry.

Identifiants

pubmed: 33179254
doi: 10.1002/jsfa.10933
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

2641-2649

Subventions

Organisme : National Institute of Food And Agriculture (NIFA), State Agricultural Experiment Station (SAES)
ID : MD-NFSC-201176

Informations de copyright

© 2020 Society of Chemical Industry.

Références

Natural Resources Conservation Service. United States Department of Agriculture, Plant Guide - Sorghum. Available: https://plants.usda.gov/plantguide/pdf/pg_sobi2.pdf [20 July 2020].
Venkateswaran K, Elangovan M and Sivaraj N, Origin, domestication and diffusion of Sorghum bicolor, in Breeding Sorghum for Diverse End Uses, ed. by Aruna C, KBRS V, Bhat BV and Tonapi VT. Woodhead Publishing, Cambridge, pp. 15-31 (2019).
Food and Agriculture Organization of the United Nations, Land and Water - Sorghum. Available: http://www.fao.org/land-water/databases-and-software/crop-information/sorghum/en/ [20 July 2020].
Food and Agriculture Organization of the United Nations, FAOSTAT - Crops. Available: http://www.fao.org/faostat/en/#data/QC [20 July 2020.
National Sorghum Producers, Sorghum 101. Available: https://sorghumgrowers.com/sorghum-101/ [20 July 2020.
Rooney LW and Pflugfelder RL, Factors affecting starch digestibility with special emphasis on sorghum and corn. J Anim Sci 63:1607-1623 (1986).
de Morais Cardoso L, Pinheiro SS, Martino HS and Pinheiro-Sant'Ana HM, Sorghum (Sorghum bicolor L.): nutrients, bioactive compounds, and potential impact on human health. Crit Rev Food Sci Nutr 57:372-390 (2017).
Pontieri P, Mamone G, De Caro S, Tuinstra MR, Roemer E, Okot J et al., Sorghum, a healthy and gluten-free food for celiac patients as demonstrated by genome, biochemical, and immunochemical analyses. J Agric Food Chem 61:2565-2571 (2013).
Grains and Legumes Nutrition Council, Sorghum. Available: https://www.glnc.org.au/grains/types-of-grains/sorghum/ [20 July 2020.
National Research Council, Lost crops of Africa, in Grains, Vol. I. The National Academies Press, Washington, DC (1996).
Dykes L and Rooney LW, Phenolic compounds in cereal grains and their health benefits. Cereal Foods World 52:105-111 (2007).
Siegel RL, Miller KD and Jemal A, Cancer statistics, 2020. CA Cancer J Clin 70:7-30 (2020).
Hanahan D and Weinberg RA, The hallmarks of cancer. Cell 100:57-70 (2000).
Hanahan D and Weinberg RA, Hallmarks of cancer: the next generation. Cell 144:646-674 (2011).
Park MY, Seo DW, Lee JY, Sung MK, Lee YM, Jang HH et al., Effects of Panicum miliaceum L. extract on adipogenic transcription factors and fatty acid accumulation in 3T3-L1 adipocytes. Nutr Res Pract 5:192-197 (2011).
Ofosu FK, Elahi F, Daliri EB, Yeon SJ, Ham HJ, Kim JH et al., Flavonoids in decorticated sorghum grains exert antioxidant, antidiabetic and antiobesity activities. Molecules 25:2854 (2020).
Chung IM, Yeo MA, Kim SJ, Kim MJ, Park DS and Moon HI, Antilipidemic activity of organic solvent extract from Sorghum bicolor on rats with diet-induced obesity. Hum Exp Toxicol 30:1865-1868 (2011).
Al-Mamary M, Molham A-H, Abdulwali A-A and Al-Obeidi A, In vivo effects of dietary sorghum tannins on rabbit digestive enzymes and mineral absorption. Nutr Res 21:1393-1401 (2001).
Barros F, Awika JM and Rooney LW, Interaction of tannins and other sorghum phenolic compounds with starch and effects on in vitro starch digestibility. J Agric Food Chem 60:11609-11617 (2012).
de Sousa AR, de Castro Moreira ME, Toledo RCL, Dos Anjos Benjamin L, Queiroz VAV, Veloso MP et al., Extruded sorghum (Sorghum bicolor L.) reduces metabolic risk of hepatic steatosis in obese rats consuming a high fat diet. Food Res Int 112:48-55 (2018).
Stefoska-Needham A, Beck EJ, Johnson SK, Chu J and Tapsell LC, Flaked sorghum biscuits increase postprandial GLP-1 and GIP levels and extend subjective satiety in healthy subjects. Mol Nutr Food Res 60:1118-1128 (2016).
Anunciação PC, Cardoso LM, Alfenas RCG, Queiroz VAV, Carvalho CWP, Martino HSD et al., Extruded sorghum consumption associated with a caloric restricted diet reduces body fat in overweight men: a randomized controlled trial. Food Res Int 119:693-700 (2019).
Kim M, Kim E, Kwak HS and Jeong Y, The ingredients in Saengshik, a formulated health food, inhibited the activity of α-amylase and α-glucosidase as anti-diabetic function. Nutr Res Pract 8:602-606 (2014).
Nguyen PH, Dung VV, Zhao BT, Kim YH, Min BS and Woo MH, Antithrombotic and antidiabetic flavonoid glycosides from the grains of Sorghum bicolor (L.) Moench var. hwanggeumchal. Arch Pharm Res 37:1394-1402 (2014).
Farrar JL, Hartle DK, Hargrove JL and Greenspan P, A novel nutraceutical property of select sorghum (Sorghum bicolor) brans: inhibition of protein glycation. Phytother res 22:1052-1056 (2008).
Kim J and Park Y, Anti-diabetic effect of sorghum extract on hepatic gluconeogenesis of streptozotocin-induced diabetic rats. Nutr Metabol 9:106 (2012).
Park JH, Lee SH, Chung I-M and Park Y, Sorghum extract exerts an anti-diabetic effect by improving insulin sensitivity via PPAR-γ in mice fed a high-fat diet. Nutr Res Pract 6:322-327 (2012).
Chung IM, Kim EH, Yeo MA, Kim SJ, Seo MC and Moon HI, Antidiabetic effects of three Korean sorghum phenolic extracts in normal and streptozotocin-induced diabetic rats. Food Res Int 44:127-132 (2011).
Mukai Yuuka KS and Shin S, Sorghum (Sorghum bicolor) extract affects plasma lipid metabolism and hepatic macrophage infiltration in diabetic rats. Curr Nutr Food Sci 16:824-832 (2020).
Poquette NM, Gu X and Lee SO, Grain sorghum muffin reduces glucose and insulin responses in men. Food Funct 5:894-899 (2014).
Anunciacao PC, Cardoso LM, Queiroz VAV, de Menezes CB, de Carvalho CWP, Pinheiro-Sant'Ana HM et al., Consumption of a drink containing extruded sorghum reduces glycaemic response of the subsequent meal. Eur J Nutr 57:251-257 (2018).
Francis N, Rao S, Blanchard C and Santhakumar A, Black sorghum phenolic extract regulates expression of genes associated with oxidative stress and inflammation in human endothelial cells. Molecules 24:3321 (2019).
Cho S-B, Choi Y and Ha TY, In vitro and in vivo effects of prosomillet, buckwheat and sorghum on cholesterol metabolism. FASEB J 14:A249 (2000).
Carr TP, Weller CL, Schlegel VL, Cuppett SL, Guderian DM and Johnson KR, Grain sorghum lipid extract reduces cholesterol absorption and plasma non-HDL cholesterol concentration in hamsters. J Nutr 135:2236-2240 (2005).
Martínez I, Wallace G, Zhang C, Legge R, Benson AK, Carr TP et al., Diet-induced metabolic improvements in a hamster model of hypercholesterolemia are strongly linked to alterations of the gut microbiota. Appl Environ Microbiol 75:4175-4184 (2009).
Ed Nignpense B, Chinkwo KA, Blanchard CL and Santhakumar AB, Black sorghum phenolic extract modulates platelet activation and platelet microparticle release. Nutrients 12:1760 (2020).
van Rensburg SJ, Epidemiologic and dietary evidence for a specific nutritional predisposition to esophageal cancer. J Natl Cancer Inst 67:243-251 (1981).
Isaacson C, The change of the staple diet of black South Africans from sorghum to maize (corn) is the cause of the epidemic of squamous carcinoma of the oesophagus. Med Hypotheses 64:658-660 (2005).
Sewram V, Sitas F, O'Connell D and Myers J, Diet and esophageal cancer risk in the Eastern Cape Province of South Africa. Nutr Cancer 66:791-799 (2014).
Yang L, Browning JD and Awika JM, Sorghum 3-deoxyanthocyanins possess strong phase II enzyme inducer activity and cancer cell growth inhibition properties. J Agric Food Chem 57:1797-1804 (2009).
Suganyadevi P, Saravanakumar M and Mohandas S, Identification of 3-deoxyanthocyanins from red sorghum ( Sorghum bicolor ) bran and its biological properties. Afr J Pure Appl Chem 5:181-193 (2011).
Cox S, Noronha L, Herald T, Bean S, Lee SH, Perumal R et al., Evaluation of ethanol-based extraction conditions of sorghum bran bioactive compounds with downstream anti-proliferative properties in human cancer cells. Heliyon 5:e01589 (2019).
Suganyadevi P, Saravanakumar M and Mohandas S, Evaluation of antiproliferative activity of red sorghum bran anthocyanin on a human breast cancer cell line (MCF-7). Int J Breast Cancer 2011:891481-891481 (2011).
Park JH, Darvin P, Lim EJ, Joung YH, Hong DY, Park EU et al., Hwanggeumchal sorghum induces cell cycle arrest, and suppresses tumor growth and metastasis through Jak2/STAT pathways in breast cancer xenografts. PLoS One 7:e40531 (2012).
Shih C-H, Siu NR, Wong E, Chiu LCM, Chu IK and Lo C, Quantitative analysis of anticancer 3-deoxyanthocyanidins in infected sorghum seedlings. J Agric Food Chem 55:254-259 (2007).
Dia VP, Pangloli P, Jones L, McClure A and Patel A, Phytochemical concentrations and biological activities of Sorghum bicolor alcoholic extracts. Food Funct 7:3410-3420 (2016).
Lee DH, Ahn SS, Kim JB, Lim Y, Lee YH and Shin SY, Downregulation of α-melanocyte-stimulating hormone-induced activation of the Pax3-MITF-tyrosinase axis by sorghum ethanolic extract in B16F10 melanoma cells. Int J Mol Sci 19:1640 (2018).
Awika JM and Rooney LW, Sorghum phytochemicals and their potential impact on human health. Phytochemistry 65:1199-1221 (2004).
Kayodé APP, Nout MJR, Linnemann AR, Hounhouigan JD, Berghofer E and Siebenhandl-Ehn S, Uncommonly high levels of 3-deoxyanthocyanidins and antioxidant capacity in the leaf sheaths of dye sorghum. J Agric Food Chem 59:1178-1184 (2011).
Vanamala JKP, Massey AR, Pinnamaneni SR, Reddivari L and Reardon KF, Grain and sweet sorghum (Sorghum bicolor L. Moench) serves as a novel source of bioactive compounds for human health. Crit Rev Food Sci Nutr 58:2867-2881 (2018).
Smolensky D, Rhodes D, McVey DS, Fawver Z, Perumal R, Herald T et al., High-polyphenol sorghum bran extract inhibits cancer cell growth through ROS induction, cell cycle arrest, and apoptosis. J Med Food 21:990-998 (2018).
Okada H and Mak TW, Pathways of apoptotic and non-apoptotic death in tumour cells. Nat Rev Cancer 4:592-603 (2004).
Elmore S, Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495-516 (2007).
Mazewski C, Liang K and Gonzalez de Mejia E, Comparison of the effect of chemical composition of anthocyanin-rich plant extracts on colon cancer cell proliferation and their potential mechanism of action using in vitro, in silico, and biochemical assays. Food Chem 242:378-388 (2018).
Wu H, Medeiros LJ and Young KH, Apoptosis signaling and BCL-2 pathways provide opportunities for novel targeted therapeutic strategies in hematologic malignances. Blood Rev 32:8-28 (2018).
Suganyadevi P, Saravanakumar M and Mohandas S, The antiproliferative activity of 3-deoxyanthocyanins extracted from red sorghum (Sorghum bicolor) bran through P(53)-dependent and Bcl-2 gene expression in breast cancer cell line. Life Sci 92:379-382 (2013).
Woo HJ, Oh IT, Lee JY, Jun DY, Seu MC, Woo KS et al., Apigeninidin induces apoptosis through activation of Bak and Bax and subsequent mediation of mitochondrial damage in human promyelocytic leukemia HL-60 cells. Process Biochem 47:1861-1871 (2012).
Lee S-H, Lee J, Herald T, Cox S, Noronha L, Perumal R et al., Anti-cancer activity of a novel high phenolic sorghum bran in human colon cancer cells. Oxid Med Cell Longev 2020:2890536 (2020). (In press).
Weinberg RA, The Biology of Cancer. Garland Science, Taylor & Francis Group, New York, NY (2014).
Song JL, Lee JS, Kim HY, Jeong BJ, Jeong JS, Huh TG et al., Dietary mixed cereal grains ameliorate the azoxymethane and dextran sodium sulfate-induced colonic carcinogenesis in C57BL/6J mice. J Med Food 23:440-452 (2020).
Kastenhuber ER and Lowe SW, Putting p53 in context. Cell 170:1062-1078 (2017).
Rao S, Chinkwo K, Santhakumar A, Johnson S and Blanchard C, Apoptosis induction pathway in human colorectal cancer cell line SW480 exposed to cereal phenolic extracts. Molecules 24:2465 (2019).
Massey AR, Reddivari L and Vanamala J, The dermal layer of sweet sorghum (Sorghum bicolor) stalk, a byproduct of biofuel production and source of unique 3-deoxyanthocyanidins, has more antiproliferative and proapoptotic activity than the pith in p53 variants of HCT116 and colon cancer stem cells. J Agric Food Chem 62:3150-3159 (2014).
Ferrara N and Kerbel RS, Angiogenesis as a therapeutic target. Nature 438:967-974 (2005).
Bottaro DP and Liotta LA, Cancer: out of air is not out of action. Nature 423:593-595 (2003).
Wu L, Huang Z, Qin P, Yao Y, Meng X, Zou J et al., Chemical characterization of a procyanidin-rich extract from sorghum bran and its effect on oxidative stress and tumor inhibition in vivo. J Agric Food Chem 59:8609-8615 (2011).
Thiery JP and Sleeman JP, Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7:131-142 (2006).
Kalluri R and Weinberg RA, The basics of epithelial-mesenchymal transition. J Clin Invest 119:1420-1428 (2009).
Makanjuola SBL, Ogundaini AO, Ajonuma LC and Dosunmu A, Apigenin and apigeninidin isolates from the Sorghum bicolor leaf targets inflammation via cyclo-oxygenase-2 and prostaglandin-E2 blockade. Int J Rheum Dis 21:1487-1495 (2018).
Benson KF, Beaman JL, Ou B, Okubena A, Okubena O and Jensen GS, West African Sorghum bicolor leaf sheaths have anti-inflammatory and immune-modulating properties in vitro. J Med Food 16:230-238 (2013).
Zhang Y, Li M, Gao H, Wang B, Tongcheng X, Gao B et al., Triacylglycerol, fatty acid, and phytochemical profiles in a new red sorghum variety (Ji Liang no. 1) and its antioxidant and anti-inflammatory properties. Food Sci Nutr 7:949-958 (2019).
Sullivan AC, Pangloli P and Dia VP, Kafirin from Sorghum bicolor inhibition of inflammation in THP-1 human macrophages is associated with reduction of intracellular reactive oxygen species. Food Chem Toxicol 111:503-510 (2018).
Nguyen PH, Zhao BT, Lee JH, Kim YH, Min BS and Woo MH, Isolation of benzoic and cinnamic acid derivatives from the grains of sorghum bicolor and their inhibition of lipopolysaccharide-induced nitric oxide production in RAW 264.7 cells. Food Chem 168:512-519 (2015).
Shim TJ, Kim TM, Jang KC, Ko JY and Kim DJ, Toxicological evaluation and anti-inflammatory activity of a golden gelatinous sorghum bran extract. Biosci Biotechnol Biochem 77:697-705 (2013).
Ritchie LE, Sturino JM, Carroll RJ, Rooney LW, Azcarate-Peril MA and Turner ND, Polyphenol-rich sorghum brans alter colon microbiota and impact species diversity and species richness after multiple bouts of dextran sodium sulfate-induced colitis. FEMS Microbiol Ecol 91:fiv008 (2015).

Auteurs

Darshika Amarakoon (D)

Department of Nutrition and Food Science, College of Agriculture and Natural Resources, University of Maryland, College Park, MD, USA.

Zhiyuan Lou (Z)

Department of Nutrition and Food Science, College of Agriculture and Natural Resources, University of Maryland, College Park, MD, USA.

Wu-Joo Lee (WJ)

Department of Nutrition and Food Science, College of Agriculture and Natural Resources, University of Maryland, College Park, MD, USA.

Dmitriy Smolensky (D)

Grain Quality and Structure Research Unit, Agricultural Research Service, U.S. Department of Agriculture, Manhattan, KS, USA.

Seong-Ho Lee (SH)

Department of Nutrition and Food Science, College of Agriculture and Natural Resources, University of Maryland, College Park, MD, USA.

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