Potential of dietary non-provitamin A carotenoids in the prevention and treatment of diabetic microvascular complications

Advances in Nutrition

Volumn 7, Issue 1, 2016, Pages 14-24

  Murillo, Ana Gabriela ^a   Fernandez, Maria Luz ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Carotenoids; Diabetes; Inflammation; Microvascular complications; Oxidative stress

Indexed keywords

ANTIOXIDANT; CAROTENOID;

DIABETES MELLITUS; DIABETIC ANGIOPATHIES; DIET THERAPY; DRUG EFFECTS; HUMAN; OXIDATIVE STRESS;

ANTIOXIDANTS; CAROTENOIDS; DIABETES MELLITUS; DIABETIC ANGIOPATHIES; HUMANS; OXIDATIVE STRESS;

EID: 85000352066     PISSN: 21618313     EISSN: 21565376     Source Type: Journal    
DOI: 10.3945/an.115.009803     Document Type: Review

References (108)

1. Maritim AC, Sanders RA, Watkins, III JB. Diabetes, oxidative stress,and antioxidants: a review. J Biochem Mol Toxicol 2003;17:24-38.
2. Dabla PK. Renal function in diabetic nephropathy. World J Diabetes2010;1:48-56.
3. Rahimi R, Nikfar S, Larijani B, Abdollahi M. A review on the role of antioxidants in the management of diabetes and its complications. Biomed Pharmacother 2005;59:365-73.
4. Olokoba AB, Obateru OA, Olokoba LB. Type 2 diabetes mellitus: a review of current trends. Oman Med J 2012;27:269-73.
5. Yang W, Dall TM, Halder P, Gallo P, Kowal SL, Hogan PF, Petersen M.Economic costs of diabetes in the U.S. in 2012. Diabetes Care 2013;36:1033-46.
6. Fowler MJ. Microvascular and macrovascular complications of diabetes.Clin Diabetes 2008;26:77-82.
7. Johansen JS, Harris AK, Rychly DJ, Ergul A. Oxidative stress and theuse of antioxidants in diabetes: linking basic science to clinical practice.Cardiovasc Diabetol 2005;4:5.
8. Chistiakov DA. Diabetic retinopathy: pathogenic mechanisms andcurrent treatments. Diabetes Metab Syndr 2012;5:165-72.
9. Calcutt NA, Cooper ME, Kern TS, Schmidt AM. Therapies forhyperglycaemia-induced diabetic complications: from animal models to clinical trials. Nat Rev Drug Discov 2009;8:417-29.
10. Stahl W, Sies H. Bioactivity and protective effects of natural carotenoids.Biochim Biophys Acta 2005;1740:101-7.
11. Naguib YM. Antioxidant activities of astaxanthin and related carotenoids.J Agric Food Chem 2000;48:1150-4.
12. Ciccone MM, Cortese F, Gesualdo M, Carbonara S, Zito A, Ricci G,De Pascalis F, Scicchitano P, Riccioni G. Dietary intake of carotenoids and their antioxidant and anti-inflammatory effects in cardio vascular care. Mediators Inflamm 2013;2013:782137.
13. Naito Y, Uchiyama K, Aoi W, Hasegawa G, Nakamura N, Yoshida N,Maoka T, Takahashi J, Yoshikawa T. Prevention of diabetic nephropathyby treatment with astaxanthin in diabetic db/db mice. Biofactors2004;20:49-59.
14. Allen DA, Harwood S, Varagunam M, Raftery MJ, Yaqoob MM. Highglucose-induced oxidative stress causes apoptosis in proximal tubularepithelial cells and is mediated by multiple caspases. FASEB J 2003;17:908-10.
15. Kim YJ, Kim YA, Yokozawa T. Protection against oxidative stress, inflammation,and apoptosis of high-glucose-exposed proximal tubularepithelial cells by astaxanthin. J Agric Food Chem 2009;57:8793-7.
16. Tang J, Kern TS. Inflammation in diabetic retinopathy. Prog Retin EyeRes 2011;30:343-58.
17. Tarr JM, Kaul K, Chopra M, Kohner EM, Chibber R. Pathophysiology of diabetic retinopathy. ISRN Ophthalmol 2013;2013:343560.
18. Dong LY, Jin J, Lu G, Kang XL. Astaxanthin attenuates the apoptosis of retinal ganglion cells in db/db mice by inhibition of oxidative stress.Mar Drugs 2013;11:960-74.
19. Nguyen TT, Wong TY. Retinal vascular manifestations of metabolic disorders. Trends Endocrinol Metab 2006;17:262-8.
20. American Diabetes Association. Standards of medical care in diabetes-2007. Diabetes Care 2007;30(Suppl 1):S4-41.
21. American Diabetes Association. Standards of medical care in diabetes-2015. Diabetes Care 2015;38(Suppl 1):S5-89.
22. American Diabetes Association. Microvascular complications and footcare. Diabetes Care 2015;38(Suppl 1):S58-66.
23. Tesfaye S, Selvarajah D. Advances in the epidemiology, pathogenesis and management of diabetic peripheral neuropathy. Diabetes MetabRes Rev 2012;28:8-14.
24. Boulton JM. Management of diabetic peripheral neuropathy. Clin Diabetes2005;23:9-15.
25. Kuhad A, Sharma S, Chopra K. Lycopene attenuates thermal hyperalgesiain a diabetic mouse model of neuropathic pain. Eur J Pain 2008;12:624-32.
26. Pop-Busui R, Lu J, Lopes N, Jones TLZ. Prevalence of diabetic peripheral neuropathy and relation to glycemic control therapies at baselinein the BARI 2D cohort. J Peripher Nerv Syst 2009;14:1-13.
27. Williams MD, Nadler JL. Inflammatory mechanisms of diabetic complications.Curr Diab Rep 2007;7:242-8.
28. Patel S, Santani D. Role of NF- k B in the pathogenesis of diabetes and its associated complications. Pharmacol Rep 2009;61:595-603.
29. Romeo G, Liu W, Asnaghi V, Kern TS, Lorenzi M. Activation of nuclear factor-kappa B induced by diabetes and high glucose regulatesa proapoptotic program in retinal pericytes. Diabetes 2002;51:2241-8.
30. Goldin A, Beckman JA, Schmidt AM, Creager MA. Advanced glycationend products: sparking the development of diabetic vascular injury.Circulation 2006;114:597-605.
31. Stitt AW. AGEs and diabetic retinopathy. Invest Ophthalmol Vis Sci2010;51:4867-74.
32. Kiho T, Usui S, Hirano K, Aizawa K, Inakuma T. Tomato paste fraction inhibiting the formation of advanced glycation end-products. Biosci Biotechnol Biochem 2004;68:200-5.
33. Ramasamy R, Vannucci SJ, Du Yan SS, Herold K, Yan SF, Schmidt AM. Advanced glycation end products and RAGE: a common thread in aging, diabetes,neurode generation, and inflammation. Glycobiology 2005;15:16R-28R.
34. Ola MS, Nawaz MI, Siddiquei MM, Al-Amro S, Abu El-Asrar AM. Recentadvances in understanding the biochemical and molecular mechanism of diabetic retinopathy. J Diabetes Complications 2012;26:56-64.
35. Rahbar S, Figarola JL. Novel inhibitors of advanced glycation endproducts.Arch Biochem Biophys 2003;419:63-79.
36. Schmitt A, Nöller J, Schmitt J. The binding of advanced glycation endproducts to cell surfaces can be measured using bead-reconstituted cellular membrane proteins. Biochim Biophys Acta 2007;1768:1389-99.
37. Wautier MP, Khodabandehlou T, Le C. Modulation of RAGE expression influences the adhesion of red blood cells from diabetic patients.Clin Hemorheol Microcirc 2006;35:379-86.
38. Brownlee M. Advanced protein glycosylation in diabetes and aging.Annu Rev Med 1995;46:223-34.
39. Coulthard LR, White DE, Jones DL, McDermott MF. Burchill S a. p38(MAPK): stress responses from molecular mechanisms to the rapeutics.Trends Mol Med 2009;15:369-79.
40. Du Y, Tang J, Li G, Li G, Berti-Mattera L, Lee CA, Bartkowski D, Gale D, Monahan J, Niesman MR, et al. Effects of p38 MAPK inhibition onearly stages of diabetic retinopathy and sensory nerve function. Invest Ophthalmol Vis Sci 2010;51:2158-64.
41. Kowluru RA, Menon B, Gierhart DL. Beneficial effect of zeaxanthinon retinal metabolic abnormalities in diabetic rats. Invest Ophthalmol Vis Sci 2008;49:1645-51.
42. Etzioni A, Frydman M, Pollack S, Avidor I, Phillips ML, Paulson JC,Gershoni-Baruch R. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insul independent diabetes mellitus. N Engl J Med 1992;327:1789-92.
43. Fiedor J, Burda K. Potential role of carotenoids as antioxidants in human health and disease. Nutrients 2014;6:466-88.
44. Sila A, Ghlissi Z, Kamoun Z, Makni M, Nasri M, Bougatef A, Sahnoun Z. Astaxanthin from shrimp by-products ameliorates nephropathy indiabetic rats. Eur J Nutr 2015;54:301-7.
45. Johnson EJ. The role of carotenoids in human health. Nutr Clin Care2002;5:56-65.
46. Rao AV, Rao LG. Carotenoids and human health. Pharmacol Res 2007;55:207-16.
47. Latowski D, Kuczýnska P, Strza1ka K. Xanthophyll cycle-a mechanism protecting plants against oxidative stress. Redox Rep 2011;16:78-90.
48. Stahl W, Sies H. Antioxidant activity of carotenoids. Mol Aspects Med2003;24:345-51.
49. Maiani G, Castón MJP, Catasta G, Toti E, Cambrodón IG, Bysted A,Granado-Lorencio F, Olmedilla-Alonso B, Knuthsen P, Valoti M,et al. Carotenoids: actual knowledge on food sources, intakes, stability and bio availability and their protective role in humans. Mol Nutr Food Res 2009;53 (Suppl 2):S194-218.
50. Tang G. Bioconversion of dietary provitamin A carotenoids to vitamin A in humans. Am J Clin Nutr 2010;91:1468S-73S.
51. Brazionis L, Rowley K, Itsiopoulos C, O'Dea K. Plasma carotenoids and diabetic retinopathy. Br J Nutr 2009;101:270-7.
52. Rissanen TH, Voutilainen S, Salonen R, Kaplan GA, Salonen JT. Serumlycopene concentrations and carotid atherosclerosis: the Kuopio Ischaemic Heart Disease Risk Factor Study. Am J Clin Nutr 2003;77:133-38.
53. Moeller SM, Voland R, Tinker L, Blodi BA, Klein L, Gehrs KM, Johnson EJ, Snodderly DM, Wallace B, Chappell RJ, et al. Associations betweenage-related nuclear cataract and lutein and zeaxanthin in thediet and serum in the Carotenoids in Age-Related Eye Disease Study(CAREDS), an ancillary study of the Women's Health Initiative.Arch Ophthalmol 2008;126:354-64.
54. Murphy MM, Barraj LM, Herman D, Bi X, Cheatham R, Randolph RK. Phyto nutrient intake by adults in the United States in relationto fruit and vegetable consumption. J Acad Nutr Diet 2012;112:222-9.
55. Sluijs I, Cadier E, Beulens JWJ. van der A DL, Spijkerman AMW, van der Schouw YT. Dietary intake of carotenoids and risk of type 2 diabetes. Nutr Metab Cardiovasc Dis 2015;25:376-81.
56. Perry A, Rasmussen H, Johnson EJ. Xanthophyll (lutein, zeaxanthin)content in fruits, vegetables and corn and egg products. J Food Compost Anal 2009;22:9-15.
57. Kotake-Nara E, Nagao A. Absorption and metabolism of xanthophylls.Mar Drugs 2011;9:1024-37.
58. Lemmens L, Colle I, Van Buggenhout S, Palmero P, Van Loey A,Hendrickx M. Carotenoid bioaccessibility in fruit- and vegetable based food products as affected by product (micro)structural characteristics and the presence of lipids: A review. Trends Food Sci Technol 2014;38:125-35.
59. Alves-Rodrigues A, Shao A. The science behind lutein. Toxicol Lett2004;150:57-83.
60. Yonekura L, Nagao A. Intestinal absorption of dietary carotenoids.Mol Nutr Food Res 2007;51:107-15.
61. Castenmiller JJ, West CE. Bioavailability and bioconversion of carotenoids.Annu Rev Nutr 1998;18:19-38.
62. Odeberg J, Lignell Å, Pettersson A, Höglund P. Oral bio availability of the antioxidant astaxanthin in humans is enhanced by incorporation of lipid based formulations. Eur J Pharm Sci 2003;19:299-304.
63. Kawada T, Kamei Y. Fujita a, Hida Y, Takahashi N, Sugimoto E,Fushiki T. Carotenoids and retinoids as suppressors on adipocyte differentiation via nuclear receptors. Biofactors 2000;13:103-9.
64. Stahl W, Ale-Agha N, Polidori MC. Non-antioxidant properties of carotenoids.Biol Chem 2002;383:553-8.
65. Kaulmann A, Bohn T. Carotenoids, inflammation, and oxidative stress-implications of cellular signaling pathways and relation tochronic disease prevention. Nutr Res 2014;34:907-29.
66. Oku H, Kodama T, Sakagami K, Puro DG. Diabetes-induced disruption of gap junction pathways within the retinal microvasculature. Invest Ophthalmol Vis Sci 2001;42:1915-20.
67. Gandhi GK, Ball KK, Cruz NF, Dienel GA. Hyperglycaemia and diabetesimpair gap junctional communication among astrocytes. ASNNeuro 2010;2:e00030.
68. Jewell C, Brien NMO. Effect of dietary supplementation with carotenoidson xenobiotic metabolizing enzymes in the liver, lung, kidneyand small intestine of the rat. Br J Nutr 1999;81:235-42.
69. Banerjee M, Vats P. Reactive metabolites and antioxidant gene polymorphismsin type 2 diabetes mellitus. Redox Biol 2013;2C:170-7.
70. Dadbinpour A, Sheikhha MH, Darbouy M, Afkhami-Ardekani M. Investigating GSTT1 and GSTM1 null genotype as the risk factor of diabetes type 2 retinopathy. J Diabetes Metab Disord 2013;12:48.
71. Bonet ML, Canas JA, Ribot J, Palou A. Carotenoids and their conversion products in the control of adipocyte function, adiposity and obesity.Arch Biochem Biophys 2015;572:112-25.
72. Roberts RL, Green J, Lewis B. Lutein and zeaxanthin in eye and skinhealth. Clin Dermatol. 2009;27:195-201.
73. Kijlstra A, Tian Y, Kelly ER, Berendschot TTJM. Lutein: more thanjust a filter for blue light. Prog Retin Eye Res 2012;31:303-15.
74. Loane E, Nolan JM, O'Donovan O, Bhosale P, Bernstein PS, Beatty S.Transport and retinal capture of lutein and zeaxanthin with reference to age-related macular degeneration. Surv Ophthalmol 2008;53:68-81.
75. Mozaffarieh M, Sacu S, Wedrich A. The role of the carotenoids, luteinand zeaxanthin, in protecting against age-related macular degeneration:a review based on controversial evidence. Nutr J 2003;2:20.
76. Johnson EJ, Maras JE, Rasmussen HM, Tucker KL. Intake of leuteinand zeaxathin differ with age, sex, and ethnicity. J Am Diet Assoc2010;110:1357-62.
77. Neuringer M, Sandstrom MM, Johnson EJ, Snodderly DM. Nutritional manipulation of primate retinas, I: effects of lutein or zeaxanth insupplements on serum and macular pigment in xanthophyll-freerhesus monkeys. Invest Ophthalmol Vis Sci 2004;45:3234-43.
78. Kalariya NM, Ramana KV. Vankuijk FJGM. Focus on molecules: lutein.Exp Eye Res 2012;102:107-8.
79. Berson EL, Rosner B, Sandberg MA, Weigel C, Brockhurst RJ, Hayes KC, Johnson EJ, Anderson EJ, Johnson CA, Gaudio AR, et al. Clinicaltrial of lutein in patients with retinitis pigmentosa receiving vitamin A. Arch Ophthalmol 2010;128:403-11.
80. Kim EK, Choi E-J. Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta 2010;1802:396-405.
81. Chew BP, Park JS. Functions and actions of retinoids and carotenoids:building on the vision on James Allen Olson. Proceedings of a symposiumto honor the memory of James Allen Olson. June 21-24, 2001,Ames, Iowa, USA. J Nutr 2004;134:220S-93S.
82. Muriach M, Bosch-Morell F, Alexander G, Blomhoff R, Barcia J, Arnal E, Almansa I, Romero FJ, Miranda M. Lutein effect on retina and hippocampusof diabetic mice. Free Radic Biol Med 2006;41:979-84.
83. Kim JE, Clark RM, Park Y, Lee J, Fernandez ML. Lutein decreases oxidative stress and inflammation in liver and eyes of guinea pigs fed a hyper cholesterolemic diet. Nutr Res Pract 2012;6:113-9.
84. Lenzen S. The mechanisms of alloxan- and streptozotocin-induced diabetes.Diabetologia 2008;51:216-26.
85. Sasaki M, Ozawa Y, Kurihara T, Kubota S, Yuki K, Noda K, Kobayashi S, Ishida S, Tsubota K. Neurodegenerative influence of oxidative stressin the retina of a murine model of diabetes. Diabetologia 2010;53:971-9.
86. Hu B-J, Hu Y-N, Lin S, Ma W-J, Li X-R. Application of lutein and zeaxanthinin nonproliferative diabetic retinopathy. Int J Ophthalmol2011;4:303-6.
87. Kalariya NM, Ramana KV, Srivastava SK, van Kuijk FJ. Carotenoid derivedaldehydes-induced oxidative stress causes apoptotic cell death in human retinal pigment epithelial cells. Exp Eye Res 2008;29:997-1003.
88. Seddon J, Ajani U, Sperduto R, Hiller R, Blair N, Burton T, Farber M.Dietary carotenoids, vitamins A, C and E, and advanced age-related macular degeneration. JAMA 1994;35:21-41.
89. Tanumihardjo SA, Li J, Dosti MP. Lutein absorption is facilitated with co supplementation of ascorbic acid in young adults. J Am Diet Assoc2005;105:114-8.
90. Rissanen T, Voutilainen S, Nyyssönen K, Salonen JT. Lycopene, atherosclerosis,and coronary heart rt disease. Exp Biol Med (Maywood)2002;227:900-7.
91. Giovannucci E. A prospective study of tomato products, lycopene, andprostate cancer risk. J Natl Cancer Inst 2002;94:391-8.
92. Rao AV, Agarwal S. Role of antioxidant lycopene in cancer and heart disease. J Am Coll Nutr 2000;19:563-9.
93. Pierine DT, Navarro MEL, Minatel IO, Luvizotto RAM, Nascimento AF, Ferreira ALA, Yeum K-J, Corrêa CR. Lycopene supplementation reduces TNF-a via RAGE in the kidney of obese rats. Nutr Diabetes2014;4:e142.
94. Bae JW, Bae J-S. Barrier protective effects of lycopene in human endothelialcells. Inflamm Res 2011;60:751-8.
95. Oborna I, Malickova K, Fingerova H, Brezinova J, Horka P, Novotny J,Bryndova H, Filipcikova R, Svobodova M. A randomized controlled trial of lycopene treatment on soluble receptor for advanced glycationend products in seminal and blood plasma of normospermic men.Am J Reprod Immunol 2011;66:179-84.
96. Guo Y, Liu Y, Wang Y. Beneficial effect of lycopene on anti-diabeticnephropathy through diminishing inflammatory response and oxidative stress. Food Funct 2015;6:1150-6.
97. Toyama T, Shimizu M, Furuichi K, Kaneko S, Wada T. Treatment andimpact of dyslipidemia in diabetic nephropathy. Clin Exp Nephrol2014;18:201-5.
98. Li W, Wang G, Lu X, Jiang Y, Xu L, Zhao X. Lycopene ameliorates renal function in rats with streptozotocin-induced diabetes. Int J Clin Exp Pathol 2014;7:5008-15.
99. Rao V, Agarwal S. Role of lycopene as antioxidant carotenoid in the prevention of chronic diseases: a review. Nutr Res 1999;19:305-23.
100. Erdman JW, Ford NA, Lindshield BL. Are the health attributes of lycopenerelated to its antioxidant function? Arch Biochem Biophys2009;483:229-35.
101. Lindshield BL, Canene-Adams K, Erdman JW. Lycopenoids: are lycopenemetabolites bioactive? Arch Biochem Biophys 2007;458:136-40.
102. Shi J, Dai Y, Kakuda Y, Mittal G, Xue SJ. Effect of heating and exposureto light on the stability of lycopene in tomato puree. Food Control2008;19:514-20.
103. Xianquan S, Shi J, Kakuda Y, Yueming J. Review stability of lycopeneduring food processing and storage. J Med Food 2005;8:413-22.
104. Rao AV. Lycopene, tomatoes, and the prevention of coronary heart disease. Exp Biol Med (Maywood) 2002;227:908-13.
105. Park CH, Xu FH, Roh S-S, Song YO, Uebaba K, Noh JS, Yokozawa T.Astaxanthin and corni fructus protect against diabetes-induced oxidative Stress, inflammation, and advanced glycation end product inlivers of streptozotocin-induced diabetic rats. J Med Food 2015;18:337-44.
106. Nakajima Y, Inokuchi Y, Shimazawa M, Otsubo K, Ishibashi T, Hara H. Astaxanthin, a dietary carotenoid, protects retinal cells against oxidative stress in-vitro and in mice in-vivo. J Pharm Pharmacol 2008;60:1365-74.
107. Kajimoto Y, Kaneto H. Role of oxidative stress in pancreatic b-celldys function. Ann N Y Acad Sci 2004;1011:168-76.
108. Kidd P. Astaxanthin, cell membrane nutrient with diverse clinical benefits and anti-aging potential. Altern Med Rev 2011;16:355-64.