Skip to main content

Advertisement

SpringerLink
Log in

Rice bran protein hydrolysates reduce arterial stiffening, vascular remodeling and oxidative stress in rats fed a high-carbohydrate and high-fat diet

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Rice bran protein hydrolysates (RBPH) contain highly nutritional proteins and antioxidant compounds which show benefits against metabolic syndrome (MetS). Increased arterial stiffness and the components of MetS have been shown to be associated with an increased risk of cardiovascular disease. This study aimed to investigate whether RBPH could alleviate the metabolic disorders, arterial stiffening, vascular remodeling, and oxidative stress in rats fed a high-carbohydrate and high-fat (HCHF) diet.

Methods

Male Sprague–Dawley rats were fed either a standard chow and tap water or a HCHF diet and 15 % fructose solution for 16 weeks. HCHF rats were treated orally with RBPH (250 or 500 mg/kg/day) for the final 6 weeks of the experimental period.

Results

Rats fed with HCHF diet had hyperglycemia, insulin resistance, dyslipidemia, hypertension, increased aortic pulse wave velocity, aortic wall hypertrophy and vascular remodeling with increased MMP-2 and MMP-9 expression. RBPH supplementation significantly alleviated these alterations (P < 0.05). Moreover, RBPH reduced the levels of angiotensin-converting enzyme (ACE) and tumor necrosis factor-alpha in plasma. Oxidative stress was also alleviated after RBPH treatment by decreasing plasma malondialdehyde, reducing superoxide production and suppressing p47phox NADPH oxidase expression in the vascular tissues of HCHF rats. RBPH increased plasma nitrate/nitrite level and up-regulated eNOS expression in the aortas of HCHF-diet-fed rats, indicating that RBPH increased NO production.

Conclusion

RBPH mitigate the deleterious effects of HCHF through potential mechanisms involving enhanced NO bioavailability, anti-ACE, anti-inflammatory and antioxidant properties. RBPH could be used as dietary supplements to minimize oxidative stress and vascular alterations triggered by MetS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Grundy SM (2015) Metabolic syndrome update. Trends Cardiovasc Med. doi:10.1016/j.tcm.2015.10.004

    Google Scholar 

  2. Mottillo S, Filion KB, Genest J, Joseph L, Pilote L, Poirier P, Rinfret S, Schiffrin EL, Eisenberg MJ (2010) The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J Am Coll Cardiol 56(14):1113–1132

    Article  Google Scholar 

  3. Esposito K, Ceriello A, Giugliano D (2007) Diet and the metabolic syndrome. Metab Syndr Relat Disord 5(4):291–296

    Article  CAS  Google Scholar 

  4. Roberts CK, Barnard RJ, Sindhu RK, Jurczak M, Ehdaie A, Vaziri ND (2006) Oxidative stress and dysregulation of NAD(P)H oxidase and antioxidant enzymes in diet-induced metabolic syndrome. Metabolism 55(7):928–934

    Article  CAS  Google Scholar 

  5. Senaphan K, Kukongviriyapan U, Sangartit W, Pakdeechote P, Pannangpetch P, Prachaney P, Greenwald SE, Kukongviriyapan V (2015) Ferulic acid alleviates changes in a rat model of metabolic syndrome induced by high-carbohydrate, high-fat diet. Nutrients 7(8):6446–6464

    Article  CAS  Google Scholar 

  6. Schaalan M, El-Abhar HS, Barakat M, El-Denshary ES (2009) Westernized-like-diet-fed rats: effect on glucose homeostasis, lipid profile, and adipocyte hormones and their modulation by rosiglitazone and glimepiride. J Diabetes Complic 23(3):199–208

    Article  Google Scholar 

  7. Dandona P, Aljada A, Chaudhuri A, Mohanty P, Garg R (2005) Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation 111(11):1448–1454

    Article  Google Scholar 

  8. Renna NF, Diez ER, Lembo C, Miatello RM (2013) Role of Cox-2 in vascular inflammation: an experimental model of metabolic syndrome. Mediat Inflamm 2013:513251

    Article  Google Scholar 

  9. Renna NF, Lembo C, Diez E, Miatello RM (2013) Role of Renin-Angiotensin system and oxidative stress on vascular inflammation in insulin resistence model. Int J Hypertens 2013:420979

    CAS  Google Scholar 

  10. Hopps E, Caimi G (2012) Matrix metalloproteinases in metabolic syndrome. Eur J Intern Med 23(2):99–104

    Article  CAS  Google Scholar 

  11. Mulvany MJ (2012) Small artery remodelling in hypertension. Basic Clin Pharmacol Toxicol 110(1):49–55

    Article  CAS  Google Scholar 

  12. Nakmareong S, Kukongviriyapan U, Pakdeechote P, Kukongviriyapan V, Kongyingyoes B, Donpunha W, Prachaney P, Phisalaphong C (2012) Tetrahydrocurcumin alleviates hypertension, aortic stiffening and oxidative stress in rats with nitric oxide deficiency. Hypertens Res 35(4):418–425

    Article  CAS  Google Scholar 

  13. Payne RA, Wilkinson IB, Webb DJ (2010) Arterial stiffness and hypertension: emerging concepts. Hypertension 55(1):9–14

    Article  CAS  Google Scholar 

  14. Abete I, Goyenechea E, Zulet MA, Martinez JA (2011) Obesity and metabolic syndrome: potential benefit from specific nutritional components. Nutr Metab Cardiovasc Dis 21(Suppl 2):B1–15

    Article  CAS  Google Scholar 

  15. Sirtori CR, Galli C, Anderson JW, Arnoldi A (2009) Nutritional and nutraceutical approaches to dyslipidemia and atherosclerosis prevention: focus on dietary proteins. Atherosclerosis 203(1):8–17

    Article  CAS  Google Scholar 

  16. Wang M, Hettiarachchy NS, Qi M, Burks W, Siebenmorgen T (1999) Preparation and functional properties of rice bran protein isolate. J Agric Food Chem 47(2):411–416

    Article  CAS  Google Scholar 

  17. Islam MS, Nagasaka R, Ohara K, Hosoya T, Ozaki H, Ushio H, Hori M (2011) Biological abilities of rice bran-derived antioxidant phytochemicals for medical therapy. Curr Top Med Chem 11(14):1847–1853

    Article  CAS  Google Scholar 

  18. Justo ML, Candiracci M, Dantas AP, de Sotomayor MA, Parrado J, Vila E, Herrera MD, Rodriguez-Rodriguez R (2013) Rice bran enzymatic extract restores endothelial function and vascular contractility in obese rats by reducing vascular inflammation and oxidative stress. J Nutr Biochem 24(8):1453–1461

    Article  CAS  Google Scholar 

  19. Justo ML, Rodriguez-Rodriguez R, Claro CM, Alvarez de Sotomayor M, Parrado J, Herrera MD (2013) Water-soluble rice bran enzymatic extract attenuates dyslipidemia, hypertension and insulin resistance in obese Zucker rats. Eur J Nutr 52(2):789–797

    Article  CAS  Google Scholar 

  20. Kokkeaw H, Thawornchinsombut S (2007) Process optimization of jasmine rice bran protein hydrolysates and its radical scavenging property. Agric Sci J 38:177–180

    Google Scholar 

  21. Li GH, Qu MR, Wan JZ, You JM (2007) Antihypertensive effect of rice protein hydrolysate with in vitro angiotensin I-converting enzyme inhibitory activity in spontaneously hypertensive rats. Asia Pac J Clin Nutr 16(Suppl 1):275–280

    CAS  Google Scholar 

  22. Wattanasiritham L, Theerakulkait C, Wickramasekara S, Maier CS, Stevens JF (2016) Isolation and identification of antioxidant peptides from enzymatically hydrolyzed rice bran protein. Food Chem 192:156–162

    Article  CAS  Google Scholar 

  23. Boonla O, Kukongviriyapan U, Pakdeechote P, Kukongviriyapan V, Pannangpetch P, Thawornchinsombut S (2015) Peptides-derived from thai rice bran improves endothelial function in 2K-1C renovascular hypertensive rats. Nutrients 7(7):5783–5799

    Article  CAS  Google Scholar 

  24. Boonloh K, Kukongviriyapan U, Pannangpetch P, Kongyingyoes B, Senggunprai L, Prawan A, Thawornchinsombut S, Kukongviriyapan V (2014) Rice bran protein hydrolysates prevented interleukin-6- and high glucose-induced insulin resistance in HepG2 cells. Food Funct 6:566–573

    Article  Google Scholar 

  25. Boonloh K, Kukongviriyapan V, Kongyingyoes B, Kukongviriyapan U, Thawornchinsombut S, Pannangpetch P (2015) Rice bran protein hydrolysates improve insulin resistance and decrease pro-inflammatory cytokine gene expression in rats fed a high carbohydrate-high fat diet. Nutrients 7(8):6313–6329

    Article  CAS  Google Scholar 

  26. Timachai S (2011) Effect of protease on bioactive properties of rice bran protein hydrolysates. Disseertation, Khon Kaen University, Khon Kaen, Thailand

  27. Cunniff P (1999) Association of official analytical chemists, 16th edn. Aspen, Maryland

    Google Scholar 

  28. Boonla O, Kukongviriyapan U, Pakdeechote P, Kukongviriyapan V, Pannangpetch P, Prachaney P, Greenwald SE (2014) Curcumin improves endothelial dysfunction and vascular remodeling in 2K-1C hypertensive rats by raising nitric oxide availability and reducing oxidative stress. Nitric Oxide 42:44–53

    Article  CAS  Google Scholar 

  29. Fitch RM, Vergona R, Sullivan ME, Wang YX (2001) Nitric oxide synthase inhibition increases aortic stiffness measured by pulse wave velocity in rats. Cardiovasc Res 51(2):351–358

    Article  CAS  Google Scholar 

  30. Marque V, Van Essen H, Struijker-Boudier HA, Atkinson J, Lartaud-Idjouadiene I (2001) Determination of aortic elastic modulus by pulse wave velocity and wall tracking in a rat model of aortic stiffness. J Vasc Res 38(6):546–550

    Article  CAS  Google Scholar 

  31. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28(7):412–419

    Article  CAS  Google Scholar 

  32. Nakmareong S, Kukongviriyapan U, Pakdeechote P, Donpunha W, Kukongviriyapan V, Kongyingyoes B, Sompamit K, Phisalaphong C (2011) Antioxidant and vascular protective effects of curcumin and tetrahydrocurcumin in rats with L-NAME-induced hypertension. Naunyn Schmiedebergs Arch Pharmacol 383(5):519–529

    Article  CAS  Google Scholar 

  33. Castro MM, Rizzi E, Rodrigues GJ, Ceron CS, Bendhack LM, Gerlach RF, Tanus-Santos JE (2009) Antioxidant treatment reduces matrix metalloproteinase-2-induced vascular changes in renovascular hypertension. Free Radic Biol Med 46(9):1298–1307

    Article  CAS  Google Scholar 

  34. Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC Jr, Spertus JA, Costa F (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 112(17):2735–2752

    Article  Google Scholar 

  35. Cicero AF, Colletti A (2015) Role of phytochemicals in the management of metabolic syndrome. Phytomedicine. doi:10.1016/j.phymed.2015.11.009

    Google Scholar 

  36. Ardiansyah Shirakawa H, Koseki T, Ohinata K, Hashizume K, Komai M (2006) Rice bran fractions improve blood pressure, lipid profile, and glucose metabolism in stroke-prone spontaneously hypertensive rats. J Agric Food Chem 54(5):1914–1920

    Article  CAS  Google Scholar 

  37. Jung EH, Kim SR, Hwang IK, Ha TY (2007) Hypoglycemic effects of a phenolic acid fraction of rice bran and ferulic acid in C57BL/KsJ-db/db mice. J Agric Food Chem 55(24):9800–9804

    Article  CAS  Google Scholar 

  38. Brunner H, Cockcroft JR, Deanfield J, Donald A, Ferrannini E, Halcox J, Kiowski W, Luscher TF, Mancia G, Natali A, Oliver JJ, Pessina AC, Rizzoni D, Rossi GP, Salvetti A, Spieker LE, Taddei S, Webb DJ (2005) Endothelial function and dysfunction. Part II: association with cardiovascular risk factors and diseases. A statement by the Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension. J Hypertens 23(2):233–246

    Article  CAS  Google Scholar 

  39. Diwan V, Poudyal H, Brown L (2013) Piperine attenuates cardiovascular, liver and metabolic changes in high carbohydrate, high fat-fed rats. Cell Biochem Biophys 67(2):297–304

    Article  CAS  Google Scholar 

  40. Poudyal H, Panchal S, Brown L (2010) Comparison of purple carrot juice and beta-carotene in a high-carbohydrate, high-fat diet-fed rat model of the metabolic syndrome. Br J Nutr 104(9):1322–1332

    Article  CAS  Google Scholar 

  41. Chistiakov DA, Orekhov AN, Bobryshev YV (2015) Endothelial barrier and its abnormalities in cardiovascular disease. Front Physiol 6:365. doi:10.3389/fphys.2015.00365

    Article  Google Scholar 

  42. Vlachopoulos C, Aznaouridis K, Stefanadis C (2010) Prediction of cardiovascular events and all-cause mortality with arterial stiffness: a systematic review and meta-analysis. J Am Coll Cardiol 55(13):1318–1327

    Article  Google Scholar 

  43. Kameyama H, Takeda K, Kusaba T, Narumiya H, Tanda S, Kuwahara N, Yamada K, Tamagaki K, Okigaki M, Hatta T, Sasaki S (2005) Augmentation of pulse wave velocity precedes vascular structural changes of the aorta in rats treated with N(omega)-nitro-l-arginine methyl ester. Hypertens Res 28(5):439–445

    Article  CAS  Google Scholar 

  44. Martinez-Martinez E, Miana M, Jurado-Lopez R, Bartolome MV, Souza Neto FV, Salaices M, Lopez-Andres N, Cachofeiro V (2014) The potential role of leptin in the vascular remodeling associated with obesity. Int J Obes (Lond) 38(12):1565–1572

    Article  CAS  Google Scholar 

  45. Hopps E, Noto D, Caimi G, Averna MR (2010) A novel component of the metabolic syndrome: the oxidative stress. Nutr Metab Cardiovasc Dis 20(1):72–77

    Article  CAS  Google Scholar 

  46. Newby AC (2006) Matrix metalloproteinases regulate migration, proliferation, and death of vascular smooth muscle cells by degrading matrix and non-matrix substrates. Cardiovasc Res 69(3):614–624

    Article  CAS  Google Scholar 

  47. Hayden MR, Sowers JR, Tyagi SC (2005) The central role of vascular extracellular matrix and basement membrane remodeling in metabolic syndrome and type 2 diabetes: the matrix preloaded. Cardiovasc Diabetol 4:9. doi:10.1186/1475-2840-4-9

    Article  Google Scholar 

  48. Goncalves FM, Jacob-Ferreira AL, Gomes VA, Casella-Filho A, Chagas AC, Marcaccini AM, Gerlach RF, Tanus-Santos JE (2009) Increased circulating levels of matrix metalloproteinase (MMP)-8, MMP-9, and pro-inflammatory markers in patients with metabolic syndrome. Clin Chim Acta 403(1–2):173–177

    Article  CAS  Google Scholar 

  49. Miksztowicz V, Muzzio ML, Royer M, Prada M, Wikinski R, Schreier L, Berg G (2008) Increased plasma activity of metalloproteinase 2 in women with metabolic syndrome. Metabolism 57(11):1493–1496

    Article  CAS  Google Scholar 

  50. Harris AK, Hutchinson JR, Sachidanandam K, Johnson MH, Dorrance AM, Stepp DW, Fagan SC, Ergul A (2005) Type 2 diabetes causes remodeling of cerebrovasculature via differential regulation of matrix metalloproteinases and collagen synthesis: role of endothelin-1. Diabetes 54(9):2638–264451

    Article  CAS  Google Scholar 

  51. Unal R, Yao-Borengasser A, Varma V, Rasouli N, Labbate C, Kern PA, Ranganathan G (2010) Matrix metalloproteinase-9 is increased in obese subjects and decreases in response to pioglitazone. J Clin Endocrinol Metab 95(6):2993–3001

    Article  CAS  Google Scholar 

  52. Tan J, Hua Q, Xing X, Wen J, Liu R, Yang Z (2007) Impact of the metalloproteinase-9/tissue inhibitor of metalloproteinase-1 system on large arterial stiffness in patients with essential hypertension. Hypertens Res 30(10):959–963

    Article  CAS  Google Scholar 

  53. Yamamoto D, Takai S (2009) Pharmacological implications of MMP-9 inhibition by ACE inhibitors. Curr Med Chem 16(11):1349–1354

    Article  CAS  Google Scholar 

  54. Mahmud A, Feely J (2002) Effect of angiotensin ii receptor blockade on arterial stiffness: beyond blood pressure reduction. Am J Hypertens 15(12):1092–1095

    Article  CAS  Google Scholar 

  55. Benetos A, Levy BI, Lacolley P, Taillard F, Duriez M, Safar ME (1997) Role of angiotensin II and bradykinin on aortic collagen following converting enzyme inhibition in spontaneously hypertensive rats. Arterioscler Thromb Vasc Biol 17(11):3196–3201

    Article  CAS  Google Scholar 

  56. Uemura S, Matsushita H, Li W, Glassford AJ, Asagami T, Lee KH, Harrison DG, Tsao PS (2001) Diabetes mellitus enhances vascular matrix metalloproteinase activity: role of oxidative stress. Circ Res 88(12):1291–1298

    Article  CAS  Google Scholar 

  57. Uzui H, Harpf A, Liu M, Doherty TM, Shukla A, Chai NN, Tripathi PV, Jovinge S, Wilkin DJ, Asotra K, Shah PK, Rajavashisth TB (2002) Increased expression of membrane type 3-matrix metalloproteinase in human atherosclerotic plaque: role of activated macrophages and inflammatory cytokines. Circulation 106(24):3024–3030

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by grants from the Faculty of Medicine, Khon Kaen University, the Agricultural Research Development Agency, the National Research Council of Thailand and the Thailand Research Fund. Ketmanee Senaphan was supported by a scholarship (PHD/0048/2553) from the Royal Golden Jubilee PhD Program, the Thailand Research Fund.

Author information

Authors and Affiliations

  1. Department of Physiology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand

    Ketmanee Senaphan, Weerapon Sangartit, Poungrat Pakdeechote & Upa Kukongviriyapan

  2. Department of Pharmacology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand

    Veerapol Kukongviriyapan & Patchareewan Pannangpetch

  3. Department of Food Technology, Faculty of Technology, Khon Kaen University, Khon Kaen, 40002, Thailand

    Supawan Thawornchinsombut

  4. Blizard Institute, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London, E1 2ES, UK

    Stephen E. Greenwald

Authors
  1. Ketmanee Senaphan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weerapon Sangartit
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Poungrat Pakdeechote
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Veerapol Kukongviriyapan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patchareewan Pannangpetch
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Supawan Thawornchinsombut
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Stephen E. Greenwald
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Upa Kukongviriyapan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Upa Kukongviriyapan.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Senaphan, K., Sangartit, W., Pakdeechote, P. et al. Rice bran protein hydrolysates reduce arterial stiffening, vascular remodeling and oxidative stress in rats fed a high-carbohydrate and high-fat diet. Eur J Nutr 57, 219–230 (2018). https://doi.org/10.1007/s00394-016-1311-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-016-1311-0

Keywords

Search

Navigation