Influence of Northern Wild Rice on Gut Dysbiosis and Short Chain Fatty Acids: Correlation with Metabolic and Inflammatory Markers in Mice on High Fat Diet
Abstract
:1. Introduction
2. Materials and Methods
2.1. Dietary Components
2.2. Experimental Animals
2.3. Animal Monitoring and Sample Collection
2.4. Measurements of Circulatory Glucose, Triglycerides and Cholesterol
2.5. Measurements of Plasma Insulin and Pro-Inflammatory Cytokines
2.6. Monocyte Adhesion Assay
2.7. Extration of Mouse Fecal Bacteria DNA and 16S rRNA Gene Sequencing
2.8. Bioinformatics Analyses of Gut Microbiota
2.9. Analysis of Fecal SCFAs
2.10. Extraction and Metabolomics Sample Analysis of WLD
2.11. Metabolomics Data Acquisition
2.12. Statistical Analyses
3. Results
3.1. Macronutrients and Metabolomic Metabolites in WLD versus WHR
3.2. Effects of WLD on Glucose, Lipids and HOMA-IR in HFD-Fed Mice
3.3. Effects of WLD on Circulatory Inflammatory Cytokines and Monocyte Adhesion
3.4. Influence of WLD on Diversities of Gut Microbiota
3.5. Impact of WLD on SCFAs and Relationship with Metabolic or Inflammatory Variables
3.6. Correlation between Fecal SCFAs and Gut Bacteria
3.7. Correlation between Fecal and Body Weights, Metabolic or Inflammatory Markers
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
AMP | adenosine monophosphate. |
AMPA | aminomethylphosphonic acid. |
AMPK | AMP-activated protein kinase. |
ANOVA | analysis of variance assay. |
ELISA | enzyme-linked immunosorbent assay. |
FPG | fasting plasma glucose. |
G1c-1 | 6-BP: α-D-Glucose 1, 6-biphosphate. |
GlcNAc-1P | N-Acetyl-alpha-D-glucosamine 1-phosphate. |
Glu-MI | 6-(alpha-D-Glucosaminyl)-1D-myo-inositol. |
HBSS | Hank’s balanced salt solution. |
HFD | high-fat diet. |
HOMA-IR | Homeostatic model assessment-insulin resistance. |
KAPA | 8-amino-7-oxononanoate. |
MCP-1 | monocyte chemotactic protein-1. |
PAI-1 | plasminogen activator inhibitor-1. |
RGG | α-L-rhamnopyranosyl-(1-2)-β-D-galactopyranosyl-(1)-β-D-glucopyranoside. |
SCFA | short chain fatty acid. |
TNFα | tumor necrosis factor-α. |
WHR | white rice. |
WLD | wild rice. |
WTWD | 13g % of WHR and 13g % of WLD supplemented in HFD. |
wt | weight. |
References
- Stack Whitney, K. Manoomin: The Taming of Wild Rice in the Great Lakes Region. Environment & Society Portal, Arcadia, No.2. Rachel Carson Center for Environment and Society. Available online: https://www.environmentandsociety.org/arcadia/manoomin-taming-wild-rice-great-lakes-region (accessed on 22 March 2024).
- Kellogg, E.A. The Evolutionary History of Ehrhartoideae, Oryzeae, and Oryza. Rice 2009, 2, 1–14. [Google Scholar] [CrossRef]
- U.S. Department of Agriculture. Wild Rice, Cooked. Available online: https://fdc.nal.usda.gov/fdc-app.html#/food-details/168897/nutrients (accessed on 10 May 2024).
- Surendiran, G.; Goh, C.; Le, K.; Zhao, Z.; Askarian, F.; Othman, R.; Nicholson, T.; Moghadasian, P.; Wang, Y.J.; Aliani, M.; et al. Wild rice (Zizania palustris L.) prevents atherogenesis in LDL receptor knockout mice. Atherosclerosis 2013, 230, 284–292. [Google Scholar]
- Moghadasian, M.H.; Alsaif, M.; Le, K.; Gangadaran, S.; Masisi, K.; Beta, T.; Shen, G.X. Combination effects of wild rice and phytosterols on prevention of atherosclerosis in LDL receptor knockout mice. J. Nutr. Biochem. 2016, 33, 128–135. [Google Scholar] [CrossRef]
- Moghadasian, M.H.; Zhao, R.; Ghazawwi, N.; Le, K.; Apea-Bah, F.B.; Beta, T.; Shen, G.X. Inhibitory Effects of North American Wild Rice on Monocyte Adhesion and Inflammatory Modulators in Low-Density Lipoprotein Receptor-Knockout Mice. J. Agric. Food Chem. 2017, 65, 9054–9060. [Google Scholar] [CrossRef]
- Hu, E.A.; Pan, A.; Malik, V.; Sun, Q. White rice consumption and risk of type 2 diabetes: Meta-analysis and systematic review. Br. Med. J. 2012, 344, e1454. [Google Scholar] [CrossRef]
- Jannasch, F.; Kröger, J.; Schulze, M.B. Dietary Patterns and Type 2 Diabetes: A Systematic Literature Review and Meta-Analysis of Prospective Studies. J. Nutr. 2017, 147, 1174–1182. [Google Scholar] [CrossRef]
- Shoelson, S.E.; Herrero, L.; Naaz, A. Obesity, inflammation, and insulin resistance. Gastroenterology 2007, 132, 2169–2180. [Google Scholar] [CrossRef]
- Zhao, R.; Wan, P.; Shariati-Ievari, S.; Michel, A.; Shen, G.X. North American Wild Rice Attenuated Hyperglycemia in High Fat-Induced Obese Mice: Involvement of AMP-Activated Protein Kinase. J. Agri Food Chem. 2020, 68, 8855–8862. [Google Scholar] [CrossRef]
- Netto Candido, T.L.; Bressan, J.; Alfenas, R.C.G. Dysbiosis and metabolic endotoxemia induced by high-fat diet. Nutr. Hosp. 2018, 35, 1432–1440. [Google Scholar] [CrossRef]
- Turnbaugh, P.J.; Backhed, F.; Fulton, L.; Gordon, J.I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008, 3, 213–223. [Google Scholar] [CrossRef]
- Di Tommaso, N.; Gasbarrini, A.; Ponziani, F.R. Intestinal Barrier in Human Health and Disease. Int. J. Environ. Res. Public Health 2021, 18, 12836. [Google Scholar] [CrossRef]
- He, J.; Zhang, P.; Shen, L.; Niu, L.; Tan, Y.; Chen, L.; Zhao, Y.; Bai, L.; Hao, X.; Li, X.; et al. Short-Chain Fatty Acids and Their Association with Signalling Pathways in Inflammation, Glucose and Lipid Metabolism. Int. J. Mol. Sci. 2020, 21, 6356. [Google Scholar] [CrossRef]
- Zhao, R.; Ren, S.; Moghadasain, M.H.; Rempel, J.D.; Shen, G.X. Involvement of Fibrinolytic Regulators in Adhesion of Monocytes to Vascular Endothelial Cells Induced by Glycated LDL and to Aorta from Diabetic Mice. J. Leukocy Biol. 2014, 95, 941–949. [Google Scholar] [CrossRef]
- Zhao, R.; Le, K.; Li, W.; Ren, S.; Moghadasian, M.H.; Beta, T.; Shen, G.X. Effects of Saskatoon Berry Powder on Monocyte Adhesion to Vascular Wall of Leptin Receptor-Deficient Diabetic Mice. J. Nutr. Biochem. 2014, 25, 851–857. [Google Scholar] [CrossRef]
- Huang, F.; Zhao, R.; Xia, M.; Shen, G.X. Impact of Cyanidin-3-Glucoside on Gut Microbiota and Relationship with Metabolism and Inflammation in High Fat-High Sucrose Diet-Induced Insulin Resistant Mice. Microorganisms 2020, 8, 1238. [Google Scholar] [CrossRef]
- Zheng, X.; Qiu, Y.; Zhong, W.; Baxter, S.; Su, M.; Li, Q.; Xie, G.; Ore, B.M.; Qiao, S.; Spencer, M.D.; et al. A targeted metabolomic protocol for short-chain fatty acids and branched-chain amino acids. Metabolomics 2013, 9, 818–827. [Google Scholar] [CrossRef]
- US Department of Agriculture, Agriculture Research Service. FoodData Central. Wild Rice. Available online: https://fdc.nal.usda.gov/fdc-app.html#/food-details/169726/nutrients (accessed on 10 August 2024).
- US Department of Agriculture, Agriculture Research Service. FoodData Central. White Rice Long Strain. Available online: https://fdc.nal.usda.gov/fdc-app.html#/food-details/168877/nutrients (accessed on 10 August 2024).
- Moghadasian, M.H.; Kaur, R.; Kostal, K.; Joshi, A.A.; Molaei, M.; Le, K.; Fischer, G.; Bonomini, F.; Favero, G.; Rezzani, R.; et al. Anti-Atherosclerotic Properties of Wild Rice in Low-Density Lipoprotein Receptor Knockout Mice: The Gut Microbiome, Cytokines, and Metabolomics Study. Nutrients 2019, 11, 2894. [Google Scholar] [CrossRef]
- Hou, X.D.; Yan, N.; Du, Y.M.; Liang, H.; Zhang, Z.F.; Yuan, X.L. Consumption of Wild Rice (Zizania latifolia) Prevents Metabolic Associated Fatty Liver Disease through the Modulation of the Gut Microbiota in Mice Model. Int. J. Mol. Sci. 2020, 21, 5375. [Google Scholar] [CrossRef]
- Łagowska, K.; Malinowska, A.M.; Zawieja, B.; Zawieja, E. Improvement of glucose metabolism in pregnant women through probiotic supplementation depends on gestational diabetes status: Meta-analysis. Sci. Rep. 2020, 10, 17796. [Google Scholar] [CrossRef]
- Álvarez-Arraño, V.; Martín-Peláez, S. Effects of Probiotics and Synbiotics on Weight Loss in Subjects with Overweight or Obesity: A Systematic Review. Nutrients 2021, 13, 3627. [Google Scholar] [CrossRef]
- Zhao, L.; Zhang, F.; Ding, X.; Wu, G.; Lam, Y.Y.; Wang, X.; Fu, H.; Xue, X.; Lu, C.; Ma, J.; et al. Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes. Science 2018, 359, 1151–1156. [Google Scholar] [CrossRef]
- Fu, J.; Xu, K.; Ni, X.; Li, X.; Zhu, X.; Xu, W. Habitual Dietary Fiber Intake, Fecal Microbiota, and Hemoglobin A1c Level in Chinese Patients with Type 2 Diabetes. Nutrients 2022, 14, 1003. [Google Scholar] [CrossRef]
- Mohseni, R.; Teimouri, M.; Safaei, M.; Arab Sadeghabadi, Z. AMP-activated protein kinase is a key regulator of obesity-associated factors. Cell Biochem. Funct. 2023, 41, 20–32. [Google Scholar] [CrossRef] [PubMed]
- Liu, T.; Song, X.; An, Y.; Wu, X.; Zhang, W.; Li, J.; Sun, Y.; Jin, G.; Liu, X.; Guo, Z.; et al. Lactobacillus rhamnosus GG Colonization in Early Life Ameliorates Inflammaging of Offspring by Activating SIRT1/AMPK/PGC-1α Pathway. Oxid. Med. Cell Longev. 2021, 2021, 3328505. [Google Scholar] [CrossRef]
- Zhang, Q.; Koser, S.L.; Bequette, B.J.; Donkin, S.S. Effect of propionate on mRNA expression of key genes for gluconeogenesis in liver of dairy cattle. J. Dairy Sci. 2015, 98, 8698–8709. [Google Scholar] [CrossRef] [PubMed]
- Yoshida, H.; Ishii, M.; Akagawa, M. Propionate suppresses hepatic gluconeogenesis via GPR43/AMPK signaling pathway. Arch. Biochem. Biophys. 2019, 672, 108057. [Google Scholar] [CrossRef]
- Heimann, E.; Nyman, M.; Degerman, E. Propionic acid and butyric acid inhibit lipolysis and de novo lipogenesis and increase insulin-stimulated glucose uptake in primary rat adipocytes. Adipocyte 2014, 4, 81–88. [Google Scholar] [CrossRef] [PubMed]
- Al-Lahham, S.; Roelofsen, H.; Rezaee, F.; Weening, D.; Hoek, A.; Vonk, R.; Venema, K. Propionic acid affects immune status and metabolism in adipose tissue from overweight subjects. Eur. J. Clin. Investig. 2012, 42, 357–364. [Google Scholar] [CrossRef]
- Lin, J.H.; Walter, P.; Yen, T.S. Endoplasmic reticulum stress in disease pathogenesis. Annu. Rev. Pathol. 2008, 3, 399–425. [Google Scholar] [CrossRef] [PubMed]
- Barnes, T.; Di Sebastiano, K.M.; Vlavcheski, F.; Quadrilatero, J.; Tsiani, E.L.; Mourtzakis, M. Glutamate increases glucose uptake in L6 myotubes in a concentration- and time-dependent manner that is mediated by AMPK. Appl. Physiol. Nutr. Metab. 2018, 43, 1307–1313. [Google Scholar] [CrossRef]
- Jayanarayanan, S.; Anju, T.R.; Smijin, S.; Paulose, C.S. Vitamin D3 supplementation increases insulin level by regulating altered IP3 and AMPA receptor expression in the pancreatic islets of streptozotocin-induced diabetic rat. J. Nutr. Biochem. 2015, 26, 1041–1049. [Google Scholar] [CrossRef]
- Fan, S.; Li, D.F.; Wang, D.C.; Fleming, J.; Zhang, H.; Zhou, Y.; Zhou, L.; Zhou, J.; Chen, T.; Chen, G.; et al. Structure and function of Mycobacterium smegmatis 7-keto-8-aminopelargonic acid (KAPA) synthase. Int. J. Biochem. Cell Biol. 2015, 58, 71–80. [Google Scholar] [CrossRef]
- Romero-Navarro, G.; Cabrera-Valladares, G.; German, M.S.; Matschinsky, F.M.; Velazquez, A.; Wang, J.; Fernandez-Mejia, C. Biotin Regulation of Pancreatic Glucokinase and Insulin in Primary Cultured Rat Islets and in Biotin- Deficient Rats1. Endocrinology 2019, 140, 4595–4600. [Google Scholar] [CrossRef]
- Henningsson, R.; Lundquist, I. Arginine-induced insulin release is decreased and glucagon increased in parallel with islet NO production. Am. J. Physiol. 1998, 275, E500–E506. [Google Scholar] [CrossRef]
- Pilz, S.; Meinitzer, A.; Gaksch, M.; Grübler, M.; Verheyen, N.; Drechsler, C.; Hartaigh, B.Ó.; Lang, F.; Alesutan, I.; Voelkl, J.; et al. Homoarginine in the renal and cardiovascular systems. Amino Acids 2015, 47, 1703–1713. [Google Scholar] [CrossRef]
- Katz, A.; Bogardus, C. Relationship between carbohydrate oxidation and G-1,6-P2 in human skeletal muscle during euglycemic hyperinsulinemia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1991, 260, R113–R119. [Google Scholar] [CrossRef]
- Katz, A.; Bogardus, C. Insulin-mediated increase in glucose 1,6-bisphosphate is attenuated in skeletal muscle of insulin-resistant man. Metabolism 1990, 39, 1300–1304. [Google Scholar] [CrossRef]
- Maessen, D.E.; Brouwers, O.; Gaens, K.H.; Wouters, K.; Cleutjens, J.P.; Janssen, B.J.; Miyata, T.; Stehouwer, C.D.; Schalkwijk, C.G. Delayed Intervention With Pyridoxamine Improves Metabolic Function and Prevents Adipose Tissue Inflammation and Insulin Resistance in High-Fat Diet–Induced Obese Mice. Diabetes 2015, 65, 956–966. [Google Scholar] [CrossRef]
- Dakshinamurti, K. Vitamins and their derivatives in the prevention and treatment of metabolic syndrome diseases (diabetes). Can. J. Physiol. Pharmacol. 2015, 93, 355–362. [Google Scholar] [CrossRef]
- Salib, J.; Michael, H.; Eskande, E. Anti-diabetic properties of flavonoid compounds isolated from Hyphaene thebaica epicarp on alloxan induced diabetic rats. Pharmacogn. Res. 2013, 5, 22. [Google Scholar] [CrossRef]
- Litwiniuk, M.; Krejner, A.; Speyrer, M.S.; Gauto, A.R.; Grzela, T. Hyaluronic Acid in Inflammation and Tissue Regeneration. Wounds 2016, 28, 78–88. [Google Scholar]
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Zhao, R.; Fajardo, J.; Shen, G.X. Influence of Northern Wild Rice on Gut Dysbiosis and Short Chain Fatty Acids: Correlation with Metabolic and Inflammatory Markers in Mice on High Fat Diet. Nutrients 2024, 16, 2834. https://doi.org/10.3390/nu16172834
Zhao R, Fajardo J, Shen GX. Influence of Northern Wild Rice on Gut Dysbiosis and Short Chain Fatty Acids: Correlation with Metabolic and Inflammatory Markers in Mice on High Fat Diet. Nutrients. 2024; 16(17):2834. https://doi.org/10.3390/nu16172834
Chicago/Turabian StyleZhao, Ruozhi, Janice Fajardo, and Garry X. Shen. 2024. "Influence of Northern Wild Rice on Gut Dysbiosis and Short Chain Fatty Acids: Correlation with Metabolic and Inflammatory Markers in Mice on High Fat Diet" Nutrients 16, no. 17: 2834. https://doi.org/10.3390/nu16172834