Generic placeholder image

Current Molecular Medicine


ISSN (Print): 1566-5240
ISSN (Online): 1875-5666

Review Article

Anti-diabetic Effects of Macronutrients via Modulation of Angiogenesis: A Comprehensive Review on Carbohydrates and Proteins

Author(s): Mina Khosravifar, Soraya Sajadimajd* and Gholamreza Bahrami*

Volume 23, Issue 3, 2023

Published on: 25 May, 2022

Page: [250 - 265] Pages: 16

DOI: 10.2174/1566524022666220321125548

Price: $65


Background: Diabetes is a major global health concern, manifesting the symptoms of chronic hyperglycemia. Either insufficient or excessive angiogenesis is generally involved in the pathogenesis of diabetes and its complications.

Objective: Given that macronutrients are important dietary players in global health issues, we aimed to review the role of macronutrients, including carbohydrates and proteins, to manage diabetes via angiogenesis modulation.

Methods: Sixteen studies regarding the effects of macronutrients, including carbohydrates and proteins derived from plants, fungus, bacteria, and their derivatives, on angiogenesis in diabetes were included in our study.

Results: Reviewing these studies suggests that carbohydrates, including low molecular weight fucoidan (LMWF), Astragalus polysaccharide (APS), and Ganoderma lucidum polysaccharide (Gl-PS), as well as oligopeptides, like sea cucumber-isolated small molecule oligopeptides (SCCOPs), can induce angiogenesis in the process of wound healing. Considering retinopathy, carbohydrates, including Diphlorethohydroxycarmalol (DPHC), Lyciumbarbarum (LBP), Sulfated K5 Escherichia coli polysaccharide (K5-N, OS (H)), and carnosine suppressed retinal angiogenesis. Furthermore, rice bran protein (RBP) ameliorated angiogenesis in diabetic nephropathy. Carbohydrates, including DPHC, Anoectochilus roxburghii polysaccharide (ARP), and LMWF, showed beneficial effects on endothelial cell dysfunction.

Conclusion: In conclusion, data suggest that a number of macronutrients, including proteins and carbohydrates, could have protective effects against complications of diabetes via modulation of angiogenesis.

Keywords: Diabetes, macronutrient, carbohydrate, protein, angiogenesis, complications.

Ogurtsova K, da Rocha Fernandes JD, Huang Y, et al. IDF diabetes atlas: Global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 2017; 128: 40-50.
[] [PMID: 28437734]
Danaei G, Finucane MM, Lu Y, et al. National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 2011; 378(9785): 31-40.
[] [PMID: 21705069]
Tuomi T, Santoro N, Caprio S, Cai M, Weng J, Groop L. The many faces of diabetes: A disease with increasing heterogeneity. Lancet 2014; 383(9922): 1084-94.
[] [PMID: 24315621]
International diabetes federation (IDF Diabetes Atlas). (7th ed.), Brussels, Belgium: International Diabetes Federation 2015.
Nathan DM. Long-term complications of diabetes mellitus. N Engl J Med 1993; 328(23): 1676-85.
[] [PMID: 8487827]
Gerstein HC, Werstuck GH. Dysglycaemia, vasculopenia, and the chronic consequences of diabetes. Lancet Diabetes Endocrinol 2013; 1(1): 71-8.
[] [PMID: 24622269]
Aronow WS, McClung JA. Translational research in coronary artery disease: pathophysiology to treatment. Academic Press 2015.
Geudens I, Gerhardt H. Coordinating cell behaviour during blood vessel formation. Development 2011; 138(21): 4569-83.
[] [PMID: 21965610]
Tomanek RJ, Schatteman GC. Angiogenesis: New insights and therapeutic potential. Anat Rec 2000; 261(3): 126-35.
[<126::AID-AR7>3.0.CO;2-4] [PMID: 10867630]
Martin A, Komada MR, Sane DC. Abnormal angiogenesis in diabetes mellitus. Med Res Rev 2003; 23(2): 117-45.
[] [PMID: 12500286]
Lin KY, Ito A, Asagami T, et al. Impaired nitric oxide synthase pathway in diabetes mellitus: role of asymmetric dimethylarginine and dimethylarginine dimethylaminohydrolase. Circulation 2002; 106(8): 987-92.
[] [PMID: 12186805]
Cooke JP. NO and angiogenesis. Atheroscler 2003; 4(4): 53-60.
[] [PMID: 14664903]
Dulak J, Józkowicz A, Dembinska-Kiec A, et al. Nitric oxide induces the synthesis of vascular endothelial growth factor by rat vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2000; 20(3): 659-66.
[] [PMID: 10712388]
Nakagawa T, Sato W, Kosugi T, Johnson RJ. Uncoupling of VEGF with endothelial NO as a potential mechanism for abnormal angiogenesis in the diabetic nephropathy. J Diab res 2013; 2013: 184539.
Leeper NJ, Cooke JP. MicroRNA and mechanisms of impaired angiogenesis in diabetes mellitus. Circulation 2011; 123: 236-8.
Wang P-C, Zhao S, Yang B-Y, Wang Q-H, Kuang H-X. Anti-diabetic polysaccharides from natural sources: A review. Carbohydr Polym 2016; 148: 86-97.
[] [PMID: 27185119]
Sharafati-Chaleshtori R, Nickdasti A, Mortezapour E, et al. Artemisia species as a new candidate for diabetes therapy: A comprehensive review. Curr Mol Med 2021; 21(10): 832-49.
[] [PMID: 33397259]
Spinks J, Johnston D, Hollingsworth B. Complementary and alternative medicine (CAM) use and quality of life in people with type 2 diabetes and/or cardiovascular disease. Complement Ther Med 2014; 22(1): 107-15.
[] [PMID: 24559825]
Evert AB, Boucher JL, Cypress M, et al. Nutrition therapy recommendations for the management of adults with diabetes. Diabetes Care 2014; 37 (Suppl. 1): S120-43.
[] [PMID: 24357208]
Koloverou E, Panagiotakos DB. Macronutrient composition and management of non-insulin-dependent diabetes mellitus (NIDDM): A new paradigm for individualized nutritional therapy in diabetes patients. Rev Diabet Stud 2016; 13(1): 6-16.
[] [PMID: 27563693]
Zheng Y, Bai L, Zhou Y, et al. Polysaccharides from Chinese herbal medicine for anti-diabetes recent advances. Int J Biol Macromol 2019; 121: 1240-53.
[] [PMID: 30342938]
Liu ZL, Zhang JG, Liu Q, Yi LT, Li YM, Li Y. The vascular protective effects of Anoectochilus roxburghii polysaccharose under high glucose conditions. J Ethnopharmacol 2017; 202: 192-9.
[] [PMID: 28286103]
Wang Y, Ding L, Li Y, Guan C, Guo J. Lycium barbarum polysaccharides can reduce the oxidative damage of the retinal nerve cells in diabetic rats. Int J Clin Exp Med 2017; 10(3): 5168-74.
Yao Q, Yang Y, Lu X, et al. Lycium barbarum polysaccharides improve retinopathy in diabetic Sprague-Dawley rats. Evid-Based Complem and Alter Med 2018; 2018.
Boonloh K, Lee ES, Kim HM, et al. Rice bran protein hydrolysates attenuate diabetic nephropathy in diabetic animal model. Eur J Nutr 2018; 57(2): 761-72.
[] [PMID: 28004272]
Li D, Li L, Xu T, et al. Effect of low molecular weight oligopeptides isolated from sea cucumber on diabetic wound healing in db/db mice. Mar Drugs 2018; 16(1): 16.
[] [PMID: 29316680]
Simons M. Angiogenesis, arteriogenesis, and diabetes. J Am Coll Cardiol 2005; 46(5): 835-7.
Waltenberger J. VEGF resistance as a molecular basis to explain the angiogenesis paradox in diabetes mellitus. Portland Press Ltd.: London 2009.
Halberg N, Khan T, Trujillo ME, et al. Hypoxia-inducible factor 1α induces fibrosis and insulin resistance in white adipose tissue. Mol Cell Biol 2009; 29(16): 4467-83.
[] [PMID: 19546236]
Unger RH, Scherer PE. Gluttony, sloth and the metabolic syndrome: A roadmap to lipotoxicity. Trends Endocrinol Metab 2010; 21(6): 345-52.
[] [PMID: 20223680]
Sun K, Kusminski CM, Scherer PE. Adipose tissue remodeling and obesity. J Clin Invest 2011; 121(6): 2094-101.
[] [PMID: 21633177]
Cao R, Brakenhielm E, Wahlestedt C, Thyberg J, Cao Y. Leptin induces vascular permeability and synergistically stimulates angiogenesis with FGF-2 and VEGF. Proc Natl Acad Sci USA 2001; 98(11): 6390-5.
[] [PMID: 11344271]
Schneider DJ, Sobel BE. PAI-1 and diabetes: A journey from the bench to the bedside. Diabetes Care 2012; 35(10): 1961-7.
[] [PMID: 22996180]
Xue Y, Petrovic N, Cao R, et al. Hypoxia-independent angiogenesis in adipose tissues during cold acclimation. Cell Metab 2009; 9(1): 99-109.
[] [PMID: 19117550]
Luo X, Jia R, Yao Q, et al. Docosahexaenoic acid attenuates adipose tissue angiogenesis and insulin resistance in high fat diet-fed middle-aged mice via a sirt1-dependent mechanism. Mol Nutr Food Res 2016; 60(4): 871-85.
[] [PMID: 26750093]
Rodrigues T, Matafome P, Sereno J, et al. Methylglyoxal-induced glycation changes adipose tissue vascular architecture, flow and expansion, leading to insulin resistance. Sci Rep 2017; 7(1): 1698.
[] [PMID: 28490763]
Lam KS, Xu A. Adiponectin: Protection of the endothelium. Curr Diab Rep 2005; 5(4): 254-9.
[] [PMID: 16033674]
Ouchi N, Kobayashi H, Kihara S, et al. Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J Biol Chem 2004; 279(2): 1304-9.
[] [PMID: 14557259]
Ishioka K, Omachi A, Sagawa M, et al. Canine adiponectin: cDNA structure, mRNA expression in adipose tissues and reduced plasma levels in obesity. Res Vet Sci 2006; 80(2): 127-32.
[] [PMID: 16051287]
Lillioja S, Young AA, Culter CL, et al. Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 1987; 80(2): 415-24.
[] [PMID: 3301899]
Prior SJ, Goldberg AP, Ortmeyer HK, et al. Increased skeletal muscle capillarization independently enhances insulin sensitivity in older adults after exercise training and detraining. Diabetes 2015; 64(10): 3386-95.
[] [PMID: 26068543]
Gavin TP, Stallings HW III, Zwetsloot KA, et al. Lower capillary density but no difference in VEGF expression in obese vs. lean young skeletal muscle in humans. J Appl Physiol 2005; 98(1): 315-21.
[] [PMID: 15298982]
Waltenberger J. New horizons in diabetes therapy: The angiogenesis paradox in diabetes: description of the problem and presentation of a unifying hypothesis. Immunol Endocr Metab Agents Med Chem 2007; 7(1): 87-93.
Kornowski R, Mintz GS, Kent KM, et al. Increased restenosis in diabetes mellitus after coronary interventions is due to exaggerated intimal hyperplasia. A serial intravascular ultrasound study. Circulation 1997; 95(6): 1366-9.
[] [PMID: 9118501]
Abaci A, Oğuzhan A, Kahraman S, et al. Effect of diabetes mellitus on formation of coronary collateral vessels. Circulation 1999; 99(17): 2239-42.
[] [PMID: 10226087]
Dabelea D, Crume T. Maternal environment and the transgenerational cycle of obesity and diabetes. Diabetes 2011; 60(7): 1849-55.
[] [PMID: 21709280]
Fetita L-S, Sobngwi E, Serradas P, Calvo F, Gautier J-F. Consequences of fetal exposure to maternal diabetes in offspring. J Clin Endocrinol Metab 2006; 91(10): 3718-24.
[] [PMID: 16849402]
Wu H, Xia X, Jiang C, et al. High glucose attenuates insulin-induced VEGF expression in bovine retinal microvascular endothelial cells. Eye (Lond) 2010; 24(1): 145-51.
[] [PMID: 19557019]
Hoshi S, Nomoto K, Kuromitsu J, Tomari S, Nagata M. High glucose induced VEGF expression via PKC and ERK in glomerular podocytes. Biochem Biophys Res Commun 2002; 290(1): 177-84.
[] [PMID: 11779150]
Xia L, Wang H, Munk S, et al. Reactive oxygen species, PKC-β1, and PKC-ζ mediate high-glucose-induced vascular endothelial growth factor expression in mesangial cells. Am J Physiol Endocrinol Metab 2007; 293(5): E1280-8.
[] [PMID: 17711990]
Xu L, Kanasaki K, Kitada M, Koya D. Diabetic angiopathy and angiogenic defects. Fibrogenesis Tissue Repair 2012; 5(1): 13.
[] [PMID: 22853690]
Yilmaz A, Kliche S, Mayr-Beyrle U, Fellbrich G, Waltenberger J. p38 MAPK inhibition is critically involved in VEGFR-2-mediated endothelial cell survival. Biochem Biophys Res Commun 2003; 306(3): 730-6.
[] [PMID: 12810080]
Wardle E. How does hyperglycaemia predispose to diabetic nephropathy? QJM 1996; 89(12): 943-51.
Shi Y, Wan X, Shao N, Ye R, Zhang N, Zhang Y. Protective and anti-angiopathy effects of ginsenoside Re against diabetes mellitus via the activation of p38 MAPK, ERK1/2 and JNK signaling. Mol Med Rep 2016; 14(5): 4849-56.
[] [PMID: 27748921]
Leibson CL, Ransom JE, Olson W, Zimmerman BR, O’fallon WM, Palumbo PJ. Peripheral arterial disease, diabetes, and mortality. Diabetes Care 2004; 27(12): 2843-9.
[] [PMID: 15562195]
Chung AW, Hsiang YN, Matzke LA, McManus BM, van Breemen C, Okon EB. Reduced expression of vascular endothelial growth factor paralleled with the increased angiostatin expression resulting from the upregulated activities of matrix metalloproteinase-2 and -9 in human type 2 diabetic arterial vasculature. Circ Res 2006; 99(2): 140-8.
[] [PMID: 16778129]
Brem H, Tomic-Canic M. Cellular and molecular basis of wound healing in diabetes. J Clin Invest 2007; 117(5): 1219-22.
[] [PMID: 17476353]
Falanga V. Wound healing and its impairment in the diabetic foot. Lancet 2005; 366(9498): 1736-43.
[] [PMID: 16291068]
Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010; 107(9): 1058-70.
[] [PMID: 21030723]
Eming SA, Koch M, Krieger A, et al. Differential proteomic analysis distinguishes tissue repair biomarker signatures in wound exudates obtained from normal healing and chronic wounds. J Proteome Res 2010; 9(9): 4758-66.
[] [PMID: 20666496]
Beidler SK, Douillet CD, Berndt DF, Keagy BA, Rich PB, Marston WA. Inflammatory cytokine levels in chronic venous insufficiency ulcer tissue before and after compression therapy. J Vasc Surg 2009; 49(4): 1013-20.
[] [PMID: 19341889]
Kubo H, Hayashi T, Ago K, Ago M, Kanekura T, Ogata M. Temporal expression of wound healing-related genes in skin burn injury. Leg Med (Tokyo) 2014; 16(1): 8-13.
[] [PMID: 24269074]
Waltenberger J, Lange J, Kranz A. Vascular endothelial growth factor-A-induced chemotaxis of monocytes is attenuated in patients with diabetes mellitus: A potential predictor for the individual capacity to develop collaterals. Circulation 2000; 102(2): 185-90.
[] [PMID: 10889129]
Tchaikovski V, Olieslagers S, Böhmer F-D, Waltenberger J. Clinical perspective. Circulation 2009; 120(2): 150-9.
[] [PMID: 19564559]
Clayton JA, Chalothorn D, Faber JE. Vascular endothelial growth factor-A specifies formation of native collaterals and regulates collateral growth in ischemia. Circ Res 2008; 103(9): 1027-36.
[] [PMID: 18802023]
Ferrara N. Vascular endothelial growth factor: Basic science and clinical progress. Endocr Rev 2004; 25(4): 581-611.
[] [PMID: 15294883]
Sasso FC, Torella D, Carbonara O, et al. Increased vascular endothelial growth factor expression but impaired vascular endothelial growth factor receptor signaling in the myocardium of type 2 diabetic patients with chronic coronary heart disease. J Am Coll Cardiol 2005; 46(5): 827-34.
[] [PMID: 16139132]
Lembo G, Vecchione C, Iaccarino G, Trimarco B. The crosstalk between insulin and the sympathetic nervous system: Possible implications in the pathogenesis of essential hypertension. Blood Press 1996; 1: 38-42.
[PMID: 9162436]
Ushio-Fukai M, Alexander RW. Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase. Mol Cell Biochem 2004; 264(1-2): 85-97.
[] [PMID: 15544038]
Kim JH, Kim KA, Shin YJ, Kim H, Majid A, Bae ON. Methylglyoxal induced advanced glycation end products (AGE)/receptor for AGE (RAGE)-mediated angiogenic impairment in bone marrow-derived endothelial progenitor cells. J Toxicol Environ Health A 2018; 81(9): 266-77.
[] [PMID: 29473788]
Rizzolo LJ, Peng S, Luo Y, Xiao W. Integration of tight junctions and claudins with the barrier functions of the retinal pigment epithelium. Prog Retin Eye Res 2011; 30(5): 296-323.
[] [PMID: 21704180]
Harfouche R, Malak NA, Brandes RP, Karsan A, Irani K, Hussain SN. Roles of reactive oxygen species in angiopoietin-1/tie-2 receptor signaling. FASEB J 2005; 19(12): 1728-30.
[] [PMID: 16049136]
Ribatti D, Vacca A, Roccaro AM, Crivellato E, Presta M. Erythropoietin as an angiogenic factor. Eur J Clin Invest 2003; 33(10): 891-6.
[] [PMID: 14511361]
Hammes H-P, Lin J, Wagner P, et al. Angiopoietin-2 causes pericyte dropout in the normal retina: evidence for involvement in diabetic retinopathy. Diabetes 2004; 53(4): 1104-10.
[] [PMID: 15047628]
Pfister F, Wang Y, Schreiter K, et al. Retinal overexpression of angiopoietin-2 mimics diabetic retinopathy and enhances vascular damages in hyperglycemia. Acta Diabetol 2010; 47(1): 59-64.
[] [PMID: 19238311]
Simon MP, Tournaire R, Pouyssegur J. The angiopoietin-2 gene of endothelial cells is up-regulated in hypoxia by a HIF binding site located in its first intron and by the central factors GATA-2 and Ets-1. J Cell Physiol 2008; 217(3): 809-18.
[] [PMID: 18720385]
Oh H, Takagi H, Suzuma K, Otani A, Matsumura M, Honda Y. Hypoxia and vascular endothelial growth factor selectively up-regulate angiopoietin-2 in bovine microvascular endothelial cells. J Biol Chem 1999; 274(22): 15732-9.
[] [PMID: 10336473]
Nishikawa T, Edelstein D, Du XL, et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000; 404(6779): 787-90.
[] [PMID: 10783895]
Death AK, Fisher EJ, McGrath KC, Yue DK. High glucose alters matrix metalloproteinase expression in two key vascular cells: Potential impact on atherosclerosis in diabetes. Atherosclerosis 2003; 168(2): 263-9.
[] [PMID: 12801609]
Ho FM, Liu SH, Lin WW, Liau CS. Opposite effects of high glucose on MMP-2 and TIMP-2 in human endothelial cells. J Cell Biochem 2007; 101(2): 442-50.
[] [PMID: 17203468]
Van Buren PN, Toto R. Current update in the management of diabetic nephropathy. Curr Diabetes Rev 2013; 9(1): 62-77.
[] [PMID: 23167665]
Costa PZ, Soares R. Neovascularization in diabetes and its complications. Unraveling the angiogenic paradox. Life Sci 2013; 92(22): 1037-45.
[] [PMID: 23603139]
Advani A, Gilbert RE. The endothelium in diabetic nephropathy. In: Semin Nephrology. Elsevier: Amsterdam 2012; Vol. 32: pp. 199-207.
Gu HF, Zheng X, Abu Seman N, et al. Impact of the hypoxia-inducible factor-1 α (HIF1A) Pro582Ser polymorphism on diabetes nephropathy. Diabetes Care 2013; 36(2): 415-21.
[] [PMID: 22991450]
Ziyadeh FN. Mediators of diabetic renal disease: The case for tgf-β as the major mediator. J Am Soc Nephrol 2004; 15(1) (Suppl. 1): S55-7.
[] [PMID: 14684674]
Fukasawa H, Yamamoto T, Suzuki H, et al. Treatment with anti-TGF-β antibody ameliorates chronic progressive nephritis by inhibiting Smad/TGF-β signaling. Kidney Int 2004; 65(1): 63-74.
[] [PMID: 14675037]
Lan HY. Diverse roles of TGF-β/Smads in renal fibrosis and inflammation. Int J Biol Sci 2011; 7(7): 1056-67.
[] [PMID: 21927575]
He X, Kan H, Cai L, Ma Q. Nrf2 is critical in defense against high glucose-induced oxidative damage in cardiomyocytes. J Mol Cell Cardiol 2009; 46(1): 47-58.
[] [PMID: 19007787]
Gao P, Li L, Ji L, et al. Nrf2 ameliorates diabetic nephropathy progression by transcriptional repression of TGFβ1 through interactions with c-Jun and SP1. Biochim Biophys Acta 2014; 1839(11): 1110-20.
[] [PMID: 25046864]
Chung CH, Fan J, Lee EY, et al. Effects of tumor necrosis factor-α on podocyte expression of monocyte chemoattractant protein-1 and in diabetic nephropathy. Nephron Extra 2015; 5(1): 1-18.
[] [PMID: 25852733]
Stone JR, Collins T. The role of hydrogen peroxide in endothelial proliferative responses. Endothelium 2002; 9(4): 231-8.
[] [PMID: 12572854]
Enea NA, Hollis TM, Kern JA, Gardner TW. Histamine H1 receptors mediate increased blood-retinal barrier permeability in experimental diabetes. Arch Ophthalmol 1989; 107(2): 270-4.
[] [PMID: 2521787]
Tang J, Kern TS. Inflammation in diabetic retinopathy. Prog Retin Eye Res 2011; 30(5): 343-58.
[] [PMID: 21635964]
Lu L, Seidel CP, Iwase T, et al. Suppression of GLUT1; A new strategy to prevent diabetic complications. J Cell Physiol 2013; 228(2): 251-7.
[] [PMID: 22717959]
De La Cruz JP, González-Correa JA, Guerrero A, de la Cuesta FS. Pharmacological approach to diabetic retinopathy. Diabetes Metab Res Rev 2004; 20(2): 91-113.
[] [PMID: 15037985]
Ciulla TA, Amador AG, Zinman B. Diabetic retinopathy and diabetic macular edema: pathophysiology, screening, and novel therapies. Diabetes Care 2003; 26(9): 2653-64.
[] [PMID: 12941734]
Yamagishi S, Nakamura K, Matsui T, et al. Pigment epithelium-derived factor inhibits advanced glycation end product-induced retinal vascular hyperpermeability by blocking reactive oxygen species-mediated vascular endothelial growth factor expression. J Biol Chem 2006; 281(29): 20213-20.
[] [PMID: 16707486]
Gariano RF, Gardner TW. Retinal angiogenesis in development and disease. Nature 2005; 438(7070): 960-6.
[] [PMID: 16355161]
Simó R, Carrasco E, García-Ramírez M, Hernández C. Angiogenic and antiangiogenic factors in proliferative diabetic retinopathy. Curr Diabetes Rev 2006; 2(1): 71-98.
[] [PMID: 18220619]
Sherris D. Ocular drug development--future directions. Angiogenesis 2007; 10(2): 71-6.
[] [PMID: 17372850]
Wang S, Park JK, Duh EJ. Novel targets against retinal angiogenesis in diabetic retinopathy. Curr Diab Rep 2012; 12(4): 355-63.
[] [PMID: 22638940]
Li Q, Zemel E, Miller B, Perlman I. Early retinal damage in experimental diabetes: electroretinographical and morphological observations. Exp Eye Res 2002; 74(5): 615-25.
[] [PMID: 12076083]
Kowluru RA, Tang J, Kern TS. Abnormalities of retinal metabolism in diabetes and experimental galactosemia. VII. Effect of long-term administration of antioxidants on the development of retinopathy. Diabetes 2001; 50(8): 1938-42.
[] [PMID: 11473058]
Haskins K, Bradley B, Powers K, et al. Oxidative stress in type 1 diabetes. Ann N Y Acad Sci 2003; 1005(1): 43-54.
Cummings JH, Stephen AM. Carbohydrate terminology and classification. Eur J Clin Nutr 2007; 61(S1) (Suppl. 1): S5-S18.
[] [PMID: 17992187]
Roberfroid M. Inulin-type fructans: Functional food ingredients. CRC Press: Boca Raton 2004.
Sliman SM, Eubank TD, Kotha SR, et al. Hyperglycemic oxoaldehyde, glyoxal, causes barrier dysfunction, cytoskeletal alterations, and inhibition of angiogenesis in vascular endothelial cells: Aminoguanidine protection. Mol Cell Biochem 2010; 333(1-2): 9-26.
[] [PMID: 19585224]
Madonna R, Giovannelli G, Confalone P, Renna FV, Geng Y-J, De Caterina R. High glucose-induced hyperosmolarity contributes to COX-2 expression and angiogenesis: implications for diabetic retinopathy. Cardiovasc Diabetol 2016; 15(1): 18.
[] [PMID: 26822858]
Cumashi A, Ushakova NA, Preobrazhenskaya ME, et al. Consorzio Interuniversitario Nazionale per la Bio-Oncologia, Italy. A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 2007; 17(5): 541-52.
[] [PMID: 17296677]
Liu T, Wang Z, Chen X, et al. Low molecular-weight fucoidan protects against hindlimb ischemic injury in type 2 diabetic mice through enhancing endothelial nitric oxide synthase phosphorylation. J Diabetes 2018; 10(11): 820-34.
[] [PMID: 29633569]
Fernando KHN, Yang HW, Jiang Y, Jeon YJ, Ryu B. Diphlorethohydroxycarmalol Isolated from Ishige okamurae represses high glucose-induced angiogenesis in vitro and in vivo. Mar Drugs 2018; 16(10): E375.
[] [PMID: 30308943]
Chung AW, Yang HH, Sigrist MK, et al. Matrix metalloproteinase-2 and -9 exacerbate arterial stiffening and angiogenesis in diabetes and chronic kidney disease. Cardiovasc Res 2009; 84(3): 494-504.
[] [PMID: 19617223]
Luyt C-E, Meddahi-Pellé A, Ho-Tin-Noe B, et al. Low-molecular-weight fucoidan promotes therapeutic revascularization in a rat model of critical Hindlimb ischemia. J Pharmacol Exp Ther 2003; 305(1): 24-30.
[] [PMID: 12649349]
Wang Z, Liu T, Chen X, et al. Low molecular weight fucoidan ameliorates hindlimb ischemic injury in type 2 diabetic rats. J Ethnopharmacol 2018; 210: 434-42.
[] [PMID: 28917976]
Tan JT, Prosser HC, Dunn LL, et al. High-density lipoproteins rescue diabetes-impaired angiogenesis via scavenger receptor class B type I. Diabetes 2016; 65(10): 3091-103.
[] [PMID: 27284113]
Wang YJ, Yu YR. Protective effects of Astragalus membranaceus on free fatty acid-induced vascular endothelial cell dysfunction. Sichuan Da Xue Xue Bao Yi Xue Ban 2011; 42(1): 48-51.
[PMID: 21355300]
Zhu YP, Shen T, Lin YJ, et al. Astragalus polysaccharides suppress ICAM-1 and VCAM-1 expression in TNF-α-treated human vascular endothelial cells by blocking NF-κB activation. Acta Pharmacol Sin 2013; 34(8): 1036-42.
[] [PMID: 23728723]
Yao C, Li A, Gao W, Pallua N, Steffens G. Improving the angiogenic potential of collagen matrices by covalent incorporation of Astragalus polysaccharides. Int J Burns Trauma 2011; 1(1): 17-26.
[PMID: 22928154]
Tu S, Shao A, Ren L, Chen T, Yao D. Angiogenesis effect of Astragalus polysaccharide combined with endothelial progenitor cells therapy in diabetic male rat following experimental hind limb ischemia. Chin Med J (Engl) 2014; 127(11): 2121-8.
[PMID: 24890165]
Sanodiya BS, Thakur GS, Baghel RK, Prasad GB, Bisen PS. Ganoderma lucidum: a potent pharmacological macrofungus. Curr Pharm Biotechnol 2009; 10(8): 717-42.
[] [PMID: 19939212]
Zhou Z-Y, Tang Y-P, Xiang J, et al. Neuroprotective effects of water-soluble Ganoderma lucidum polysaccharides on cerebral ischemic injury in rats. J Ethnopharmacol 2010; 131(1): 154-64.
[] [PMID: 20600765]
Tangpong J, Cole MP, Sultana R, et al. Adriamycin-mediated nitration of manganese superoxide dismutase in the central nervous system: Insight into the mechanism of chemobrain. J Neurochem 2007; 100(1): 191-201.
[] [PMID: 17227439]
Tie L, Yang H-Q, An Y, et al. Ganoderma lucidum polysaccharide accelerates refractory wound healing by inhibition of mitochondrial oxidative stress in type 1 diabetes. Cell Physiol Biochem 2012; 29(3-4): 583-94.
[] [PMID: 22508065]
Rusnati M, Presta M. Interaction of angiogenic basic fibroblast growth factor with endothelial cell heparan sulfate proteoglycans. Biological implications in neovascularization. Int J Clin Lab Res 1996; 26(1): 15-23.
[] [PMID: 8739851]
Vann WF. SCHMIDT MA, JANN B, JANN K. The structure of the capsular polysaccharide (K5 Antigenn) of urinary‐tract‐infective Escherichia coli 010: K5: H4: A polymer similar to desulfo‐heparin. Eur J Biochem 1981; 116(2): 359-64.
[] [PMID: 7018909]
Rezzola S, Dal Monte M, Belleri M, et al. Therapeutic potential of anti-angiogenic multitarget N, O-sulfated E. coli K5 polysaccharide in diabetic retinopathy. Diabetes 2015; 64(7): 2581-92.
[] [PMID: 25695948]
Keller U. Dietary proteins in obesity and in diabetes. Int J Vitam Nutr Res 2011; 81(2-3): 125-33.
[] [PMID: 22139563]
Justo ML, Rodriguez-Rodriguez R, Claro CM, Alvarez de Sotomayor M, Parrado J, Herrera MD. Water-soluble rice bran enzymatic extract attenuates dyslipidemia, hypertension and insulin resistance in obese Zucker rats. Eur J Nutr 2013; 52(2): 789-97.
[] [PMID: 22661284]
Jefferson JA, Shankland SJ, Pichler RH. Proteinuria in diabetic kidney disease: A mechanistic viewpoint. Kidney Int 2008; 74(1): 22-36.
[] [PMID: 18418356]
Olivera-Castillo L, Pérez-Vega J, Gómez-Ruiz JÁ, Hernández-Ledesma B. Release of bioactive peptides by simulated gastrointestinal digestion of sea cucumber protein. (Isostichopus Badionotus) 2011.
He L-X, Zhang Z-F, Sun B, et al. Sea cucumber (Codonopsis pilosula) oligopeptides: immunomodulatory effects based on stimulating Th cells, cytokine secretion and antibody production. Food Funct 2016; 7(2): 1208-16.
[] [PMID: 26838796]
Guo R, Chai L, Chen L, et al. Stromal cell-derived factor 1 (SDF-1) accelerated skin wound healing by promoting the migration and proliferation of epidermal stem cells. In Vitro Cell Dev Biol Anim 2015; 51(6): 578-85.
[] [PMID: 25636237]
Boldyrev A, Bulygina E, Leinsoo T, Petrushanko I, Tsubone S, Abe H. Protection of neuronal cells against reactive oxygen species by carnosine and related compounds. Comp Biochem Physiol B Biochem Mol Biol 2004; 137(1): 81-8.
[] [PMID: 14698913]
Hipkiss AR, Brownson C, Bertani MF, Ruiz E, Ferro A. Reaction of carnosine with aged proteins: Another protective process? Ann N Y Acad Sci 2002; 959(1): 285-94.
[] [PMID: 11976203]
Teufel M, Saudek V, Ledig J-P, et al. Sequence identification and characterization of human carnosinase and a closely related non-specific dipeptidase. J Biol Chem 2003; 278(8): 6521-31.
[] [PMID: 12473676]
Pfister F, Riedl E, Wang Q, et al. Oral carnosine supplementation prevents vascular damage in experimental diabetic retinopathy. Cell Physiol Biochem 2011; 28(1): 125-36.
[] [PMID: 21865855]
de Gooyer TE, Stevenson KA, Humphries P, Simpson DA, Gardiner TA, Stitt AW. Retinopathy is reduced during experimental diabetes in a mouse model of outer retinal degeneration. Invest Ophthalmol Vis Sci 2006; 47(12): 5561-8.
[] [PMID: 17122149]

Rights & Permissions Print Export Cite as
© 2024 Bentham Science Publishers | Privacy Policy