Dietary wolfberry upregulates carotenoid metabolic genes and enhances mitochondrial biogenesis in the retina of db/db diabetic mice

Molecular Nutrition and Food Research

Volumn 57, Issue 7, 2013, Pages 1158-1169

  Yu, Huifeng ^a   Wark, Logan ^a   Ji, Hua ^a,b   Willard, Lloyd ^a   Jaing, Yu ^a   Han, Jing ^a   He, Hui ^b   Ortiz, Edlin ^a   Zhang, Yunong ^a   Medeiros, Denis M ^a,c   Lin, Dingbo ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b INSTITUTE OF CEREAL AND OIL CROPS   (China)

^c UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

Carotenoids; Diabetic retinopathy; Hypoxia; Mitochondrial biogenesis; Wolfberry

Indexed keywords

AMPK ALPHA2 SUBUNIT, MOUSE; BCO2 PROTEIN, MOUSE; CAROTENOID; DIOXYGENASE; DNA BINDING PROTEIN; GLUTATHIONE TRANSFERASE P1; GSTP1 PROTEIN, MOUSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL TRANSCRIPTION FACTOR A; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SCARB1 PROTEIN, MOUSE; SCAVENGER RECEPTOR B; TRANSCRIPTION FACTOR; XANTHOPHYLL; ZEAXANTHIN;

ANIMAL; ARTICLE; CHEMISTRY; DIABETIC RETINOPATHY; DRUG EFFECT; EXPERIMENTAL DIABETES MELLITUS; GENETICS; HYPOXIA; LIVER; LYCIUM; MALE; METABOLISM; MITOCHONDRIAL BIOGENESIS; MITOCHONDRION; MOUSE; RETINA; UPREGULATION;

CAROTENOIDS; DIABETIC RETINOPATHY; HYPOXIA; MITOCHONDRIAL BIOGENESIS; WOLFBERRY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CAROTENOIDS; DIABETES MELLITUS, EXPERIMENTAL; DIOXYGENASES; DNA-BINDING PROTEINS; GLUTATHIONE S-TRANSFERASE PI; LIVER; LUTEIN; LYCIUM; MALE; MICE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PPAR GAMMA; RETINA; SCAVENGER RECEPTORS, CLASS B; TRANSCRIPTION FACTORS; UP-REGULATION; XANTHOPHYLLS;

LYCIUM; MUS;

EID: 84879796122     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200642     Document Type: Article

References (63)

1. Brazionis, L., Rowley, K., Itsiopoulos, C., O'Dea, K., Plasma carotenoids and diabetic retinopathy. Br. J. Nutr. 2009, 101, 270-277.
2. Coyne, T., Ibiebele, T. I., Baade, P. D., Dobson, A. et al., Diabetes mellitus and serum carotenoids: findings of a population-based study in Queensland, Australia. Am. J. Clin. Nutr. 2005, 82, 685-693.
3. Polidori, M. C., Mecocci, P., Stahl, W., Parente, B. et al., Plasma levels of lipophilic antioxidants in very old patients with type 2 diabetes. Diabetes Metab. Res. Rev. 2000, 16, 15-19.
4. Thurnham, D. I., Macular zeaxanthins and lutein - a review of dietary sources and bioavailability and some relationships with macular pigment optical density and age-related macular disease. Nutr. Res. Rev. 2007, 20, 163-179.
5. Chiu, C. J., Taylor, A., Dietary hyperglycemia, glycemic index and metabolic retinal diseases. Prog. Retin. Eye Res. 2011, 30, 18-53.
6. Chucair, A. J., Rotstein, N. P., Sangiovanni, J. P., During, A. et al., Lutein and zeaxanthin protect photoreceptors from apoptosis induced by oxidative stress: relation with docosahexaenoic acid. Invest Ophthalmol. Vis. Sci. 2007, 48, 5168-5177.
7. Kijlstra, A., Tian, Y., Kelly, E. R., Berendschot, T. T., Lutein: more than just a filter for blue light. Prog. Retin. Eye Res. 2012, 31, 303-315.
8. Ozawa, Y., Sasaki, M., Takahashi, N., Kamoshita, M. et al., Neuroprotective effects of lutein in the retina. Curr. Pharm. Des. 2012, 18, 51-56.
9. Borel, P., Genetic variations involved in interindividual variability in carotenoid status. Mol. Nutr. Food Res. 2012, 56, 228-240.
10. Lietz, G., Oxley, A., Boesch-Saadatmandi, C., Kobayashi, D., Importance of β, β-carotene 15, 15'-monooxygenase 1 (BCMO1) and β, β-carotene 9', 10'-dioxygenase 2 (BCDO2) in nutrition and health. Mol. Nutr. Food Res. 2012, 56, 241-250.
11. Ferrucci, L., Perry, J. R., Matteini, A., Perola, M. et al., Common variation in the beta-carotene 15, 15'-monooxygenase 1 gene affects circulating levels of carotenoids: a genome-wide association study. Am. J. Hum. Genet. 2009, 84, 123-133.
12. Borel, P., de Edelenyi, F. S., Vincent-Baudry, S., Malezet-Desmoulin, C. et al., Genetic variants in BCMO1 and CD36 are associated with plasma lutein concentrations and macular pigment optical density in humans. Ann. Med. 2011, 43, 47-59.
13. Provost, A. C., Vede, L., Bigot, K., Keller, N. et al., Morphologic and electroretinographic phenotype of SR-BI knockout mice after a long-term atherogenic diet. Invest. Ophthalmol. Vis. Sci. 2009, 50, 3931-3942.
14. Bhosale, P., Larson, A. J., Frederick, J. M., Southwick, K. et al., Identification and characterization of a Pi isoform of glutathione S-transferase (GSTP1) as a zeaxanthin-binding protein in the macula of the human eye. J. Biol. Chem. 2004, 279, 49447-49454.
15. Bhatti, R. A., Yu, S., Boulanger, A., Fariss, R. N. et al., Expression of beta-carotene 15, 15' monooxygenase in retina and RPE-choroid. Invest. Ophthalmol. Vis. Sci. 2003, 44, 44-49.
16. Morinobu, T., Tamai, H., Beta-carotene 15, 15'-dioxygenase activity in streptozotocin-induced diabetic rats. J. Nutr. Sci. Vitaminol. (Tokyo) 2000, 46, 263-265.
17. Amengual, J., Lobo, G. P., Golczak, M., Li, H. N. et al., A mitochondrial enzyme degrades carotenoids and protects against oxidative stress. FASEB J. 2011, 25, 948-959.
18. Lobo, G. P., Isken, A., Hoff, S., Babino, D. et al., BCDO2 acts as a carotenoid scavenger and gatekeeper for the mitochondrial apoptotic pathway. Development 2012, 139, 2966-2967.
19. Kiefer, C., Hessel, S., Lampert, J. M., Vogt, K. et al., Identification and characterization of a mammalian enzyme catalyzing the asymmetric oxidative cleavage of provitamin A. J. Biol. Chem. 2001, 276, 14110-14116.
20. Funk, R. H., Blood supply of the retina. Ophthalmic Res. 1997, 29, 320-325.
21. Campochiaro, P. A., Retinal and choroidal neovascularization. J. Cell. Physiol. 2000, 184, 301-310.
22. Neely, K. A., Quillen, D. A., Schachat, A. P., Gardner, T. W. et al., Diabetic retinopathy. Med. Clin. North Am. 1998, 82, 847-876.
23. Arden, G. B., Sivaprasad, S., Hypoxia and oxidative stress in the causation of diabetic retinopathy. Curr. Diabetes Rev. 2011, 7, 291-304.
24. Nyengaard, J. R., Ido, Y., Kilo, C., Williamson, J. R., Interactions between hyperglycemia and hypoxia: implications for diabetic retinopathy. Diabetes 2004, 53, 2931-2938.
25. Wong, A., Merritt, S., Butt, A. N., Williams, A. et al., Effect of hypoxia on circulating levels of retina-specific messenger RNA in type 2 diabetes mellitus. Ann. NY Acad. Sci. 2008, 1137, 243-252.
26. Lin, M., Hu, Y., Chen, Y., Zhou, K. K. et al., Impacts of hypoxia-inducible factor-1 knockout in the retinal pigment epithelium on choroidal neovascularization. Invest. Ophthalmol. Vis. Sci. 2012, 53, 6197-6206.
27. Han, X. X., Guo, C. M., Li, Y., Hui, Y. N., Effects of bevacizumab on the neovascular membrane of proliferative diabetic retinopathy: reduction of endothelial cells and expressions of VEGF and HIF-1α. Mol Vis. 2012, 18, 1-9.
28. Dong, X., Wang, Y. S., Dou, G. R., Hou, H. Y. et al., Influence of Dll4 via HIF-1α-VEGF signaling on the angiogenesis of choroidal neovascularization under hypoxic conditions. PLoS One 2011, 6, e18481.
29. Ryan, G. J., New pharmacologic approaches to treating diabetic retinopathy. Am. J. Health Syst. Pharm. 2007, 64, S15-S21.
30. Sivitz, W. I., Yorek, M. A., Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Antioxid. Redox Signal. 2010, 12, 537-577.
31. Kowluru, R. A., Mohammad, G., dos Santos, J. M., Zhong, Q., Abrogation of MMP-9 gene protects against the development of retinopathy in diabetic mice by preventing mitochondrial damage. Diabetes 2011, 60, 3023-3033.
32. Tang, L., Zhang, Y., Jiang, Y., Willard, L. et al., Dietary wolfberry ameliorates retinal structure abnormalities in db/db mice at the early stage of diabetes. Exp. Biol. Med. (Maywood) 2011, 236, 1051-1063.
33. Arden, G. B., Sivaprasad, S., The pathogenesis of early retinal changes of diabetic retinopathy. Doc. Ophthalmol. 2012, 124, 15-26.
34. Lieth, E., Gardner, T. W., Barber, A. J., Antonetti, D. A., Retinal neurodegeneration: early pathology in diabetes. Clin. Exp. Ophthalmol. 2000, 28, 3-8.
35. Ly, A., Yee, P., Vessey, K. A., Phipps, J. A. et al., Early inner retinal astrocyte dysfunction during diabetes and development of hypoxia, retinal stress, and neuronal functional loss. Invest. Ophthalmol. Vis. Sci. 2011, 52, 9316-9326.
36. Obrosova, I. G., Drel, V. R., Kumagai, A. K., Szábo, C. et al., Early diabetes-induced biochemical changes in the retina: comparison of rat and mouse models. Diabetologia 2006, 49, 2525-2533.
37. Cukiernik, M., Hileeto, D., Evans, T., Mukherjee, S. et al., Vascular endothelial growth factor in diabetes induced early retinal abnormalities. Diabetes Res. Clin. Pract. 2004, 65, 197-208.
38. Li, Q., Zemel, E., Miller, B., Perlman, I., Early retinal damage in experimental diabetes: electroretinographical and morphological observations. Exp. Eye Res. 2002, 74, 615-625.
39. Inbaraj, B. S., Lu, H., Hung, C. F., Wu, W. B. et al., Determination of carotenoids and their esters in fruits of Lycium barbarum Linnaeus by HPLC-DAD-APCI-MS. J. Pharm. Biomed. Anal. 2008, 47, 812-818.
40. Ji, H., He, H., Lin, D., Dietary wolfberry protects against retinal degeneration. In: Preedy, V. (Ed.), Nutrition, Diet, the Eye and Vision. Elsevier, Amsterdam 2013 (in press).
41. Santos, J. M., Kowluru, R. A., Role of mitochondria biogenesis in the metabolic memory associated with the continued progression of diabetic retinopathy and its regulation by lipoic acid. Invest. Ophthalmol. Vis. Sci. 2011, 52, 8791-8798.
42. Santos, J. M., Tewari, S., Goldberg, A. F., Kowluru, R. A., Mitochondrial biogenesis and the development of diabetic retinopathy. Free Radic. Biol. Med. 2011, 51, 1849-1860.
43. Musi, N., Hirshman, M. F., Nygren, J., Svanfeldt, M. et al., Metformin increases AMP-activated protein kinase activity in skeletal muscle of subjects with type 2 diabetes. Diabetes 2002, 51, 2074-2081.
44. Dontsov, A. E., Glickman, R. D., Ostrovsky, M. A., Retinal pigment epithelium pigment granules stimulate the photo-oxidation of unsaturated fatty acids. Free Radic. Biol. Med. 1999, 26, 1436-1446.
45. Midena, E., Segato, T., Radin, S., di Giorgio, G. et al., Studies on the retina of the diabetic db/db mouse. I. Endothelial cell-pericyte ratio. Ophthalmic Res. 1989, 21, 106-111.
46. Clements, R. S. Jr., Robison, W. G. Jr., Cohen, M. P., Anti-glycated albumin therapy ameliorates early retinal microvascular pathology in db/db mice. J. Diabetes Complicat. 1998, 12, 28-33.
47. Barile, G. R., Pachydaki, S. I., Tari, S. R., Lee, S. E. et al., The RAGE axis in early diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 2005, 46, 2916-2924.
48. Cheung, A. K., Fung, M. K., Lo, A. C., Lam, T. T. et al., Aldose reductase deficiency prevents diabetes-induced blood-retinal barrier breakdown, apoptosis, and glial reactivation in the retina of db/db mice. Diabetes 2005, 54, 3119-3125.
49. Li, J., Wang, J. J., Chen, D., Mott, R. et al., Systemic administration of HMG-CoA reductase inhibitor protects the blood-retinal barrier and ameliorates retinal inflammation in type 2 diabetes. Exp. Eye Res. 2009, 89, 71-78.
50. Arden, G. B., Sivaprasad, S., Hypoxia and oxidative stress in the causation of diabetic retinopathy. Curr. Diabetes Rev. 2011, 7, 291-304.
51. Reeve, V. E., Allanson, M., Arun, S. J., Domanski, D. et al., Mice drinking goji berry juice (Lycium barbarum) are protected from UV radiation-induced skin damage via antioxidant pathways. Photochem. Photobiol. Sci. 2010, 9, 601-607.
52. Amagase, H., Sun, B., Borek, C., Lycium barbarum (goji) juice improves in vivo antioxidant biomarkers in serum of healthy adults. Nutr. Res. 2009, 29, 19-25.
53. Ren, Z., Na, L., Xu, Y., Rozati, M. et al., Dietary supplementation with lacto-wolfberry enhances the immune response and reduces pathogenesis to influenza infection in mice. J. Nutr. 2012, 142, 1596-1602.
54. Salt, I., Celler, J. W., Hawley, S. A., Prescott, A. et al., AMP-activated protein kinase: greater AMP dependence, and preferential nuclear localization, of complexes containing the alpha2 isoform. Biochem. J. 1998, 334, 177-187.
55. Ju, T. C., Chen, H. M., Lin, J. T., Chang, C. P. et al., Nuclear translocation of AMPK-alpha1 potentiates striatal neurodegeneration in Huntington's disease. J. Cell Biol. 2011, 194, 209-227.
56. Yu, L., Yang, S. J., AMP-activated protein kinase mediates activity-dependent regulation of peroxisome proliferator-activated receptor gamma coactivator-1alpha and nuclear respiratory factor 1 expression in rat visual cortical neurons. Neuroscience 2010, 169, 23-38.
57. Okoshi, R., Ozaki, T., Yamamoto, H., Ando, K. et al., Activation of AMP-activated protein kinase induces p53-dependent apoptotic cell death in response to energetic stress. J. Biol. Chem. 2008, 283, 3979-3987.
58. Qin, S., De Vries, G. W., Alpha2 but not alpha1 AMP-activated protein kinase mediates oxidative stress-induced inhibition of retinal pigment epithelium cell phagocytosis of photoreceptor outer segments. J. Biol. Chem. 2008, 283, 6744-6751.
59. Scarpulla, R. C., Vega, R. B., Kelly, D. P., Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol. Metab. 2012, 23, 459-466.
60. Piantadosi, C. A., Suliman, H. B., Mitochondrial transcription factor A induction by redox activation of nuclear respiratory factor 1. J. Biol. Chem. 2006, 281, 324-333.
61. Corrado, M., Scorrano, L., Campello, S., Mitochondrial dynamics in cancer and neurodegenerative and neuroinflammatory diseases. Int. J. Cell Biol. 2012, doi: 10.1155/2012/2012/729290
62. Overly, C. C., Rieff, H. I., Hollenbeck, P. J., Organelle motility and metabolism in axons vs dendrites of cultured hippocampal neurons. J. Cell Sci. 1996, 109, 971-980.
63. Sparrow, J. R., Hicks, D., Hamel, C. P., The retinal pigment epithelium in health and disease. Curr. Mol. Med. 2010, 10, 802-823.