The generation of induced pluripotent stem cells for macular degeneration as a drug screening platform: Identification of curcumin as a protective agent for retinal pigment epithelial cells against oxidative stress

Frontiers in Aging Neuroscience

Volumn 6, Issue JUL, 2014, Pages

  Chang, Yun Ching ^a,b   Chang, Wei Chao ^c,d   Hung, Kuo Hsuan ^b   Yang, Der Ming ^a   Cheng, Yung Hsin ^a,b   Liao, Yi Wen ^a   Woung, Lin Chung ^e   Tsai, Ching Yao ^e   Hsu, Chih Chien ^a   Lin, Tai Chi ^a   Liu, Jorn Hon ^f   Chiou, Shih Hwa ^a,b   Peng, Chi Hsien ^a,g   Chen, Shih Jen ^a  

^a TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^e TAIPEI CITY HOSPITAL   (Taiwan)

^f CHENG HSIN GENERAL HOSPITAL   (Taiwan)

^g FU JEN CATHOLIC UNIVERSITY   (Taiwan)

Author keywords

Age related macular degeneration; Antioxidant; Curcumin; Oxidative stress; Patient specific induced pluripotent stem cells; Retinal pigment epithelial

Indexed keywords

CURCUMIN; GLUTATHIONE PEROXIDASE 1; HEME OXYGENASE 1; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; PLATELET DERIVED GROWTH FACTOR; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN B; VASCULOTROPIN; HO1 PROTEIN; IGFBP 2 PROTEIN; SOD2 PROTEIN; UNCLASSIFIED DRUG;

ADVANCED DRY AGE RELATED MACULAR DEGENERATION; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROTECTION; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG SCREENING; DRY EYE; HUMAN; HUMAN CELL; IN VITRO STUDY; NUCLEAR REPROGRAMMING; OXIDATIVE STRESS; PIGMENT EPITHELIUM; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; RETINA MACULA AGE RELATED DEGENERATION; ANIMAL CELL; CELL DEATH; MOUSE; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PIGMENT CELL; T LYMPHOCYTE;

EID: 84904668706     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00191     Document Type: Article

References (50)

1. Aggarwal, B.B., and Harikumar, K.B. (2009). Potential therapeutic effects of curcumin, the anti-inflammatory agent, against neurodegenerative, cardiovascular, pulmonary, metabolic, autoimmune and neoplastic diseases. Int J Biochem Cell Biol 41, 40-59. doi: 10.1016/j.biocel.2008.06.010.
2. Ammon, H.P., and Wahl, M.A. (1991). Pharmacology of Curcuma longa. Planta Med 57, 1-7. doi: 10.1055/s-2006-960004.
3. Anand, P., Kunnumakkara, A.B., Newman, R.A., and Aggarwal, B.B. (2007). Bioavailability of curcumin: problems and promises. Mol Pharm 4, 807-818. doi: 10.1021/mp700113r.
4. Beatty, S., Koh, H., Phil, M., Henson, D., and Boulton, M. (2000). The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 45, 115-134.
5. Berger, C., Blau, C.A., Clackson, T., Riddell, S.R., and Heimfeld, S. (2003). CD28 costimulation and immunoaffinity-based selection efficiently generate primary gene-modified T cells for adoptive immunotherapy. Blood 101, 476-484. doi: 10.1182/blood-2002-07-2142.
6. Blasiak, J., Petrovski, G., Vereb, Z., Facsko, A., and Kaarniranta, K. (2014). Oxidative stress, hypoxia, and autophagy in the neovascular processes of age-related macular degeneration. Biomed Res Int 2014, 768026. doi: 10.1155/2014/768026.
7. Bowes Rickman, C., Farsiu, S., Toth, C.A., and Klingeborn, M. (2013). Dry age-related macular degeneration: mechanisms, therapeutic targets, and imaging. Invest Ophthalmol Vis Sci 54, ORSF68-80. doi: 10.1167/iovs.13-12757.
8. Chien, Y., Liao, Y.W., Liu, D.M., Lin, H.L., Chen, S.J., Chen, H.L., Peng, C.H., Liang, C.M., Mou, C.Y., and Chiou, S.H. (2012). Corneal repair by human corneal keratocyte-reprogrammed iPSCs and amphiphatic carboxymethyl-hexanoyl chitosan hydrogel. Biomaterials 33, 8003-8016. doi: 10.1016/j.biomaterials.2012.07.029.
9. Dimos, J.T., Rodolfa, K.T., Niakan, K.K., Weisenthal, L.M., Mitsumoto, H., Chung, W., Croft, G.F., Saphier, G., Leibel, R., Goland, R., Wichterle, H., Henderson, C.E., and Eggan, K. (2008). Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321, 1218-1221. doi: 10.1126/science.1158799.
10. Eggenschwiler, R., and Cantz, T. (2009). Induced pluripotent stem cells generated without viral integration. Hepatology 49, 1048-1049. doi: 10.1002/hep.22827.
11. Epstein, J., Sanderson, I.R., and Macdonald, T.T. (2010). Curcumin as a therapeutic agent: the evidence from in vitro, animal and human studies. Br J Nutr 103, 1545-1557. doi: 10.1017/S0007114509993667.
12. Eramudugolla, R., Wood, J., and Anstey, K.J. (2013). Co-morbidity of depression and anxiety in common age-related eye diseases: a population-based study of 662 adults. Front Aging Neurosci 5, 56. doi: 10.3389/fnagi.2013.00056.
13. Friedman, D.S., O'colmain, B.J., Munoz, B., Tomany, S.C., Mccarty, C., De Jong, P.T., Nemesure, B., Mitchell, P., Kempen, J., and Eye Diseases Prevalence Research, G. (2004). Prevalence of age-related macular degeneration in the United States. Arch Ophthalmol 122, 564-572. doi: 10.1001/archopht.122.4.564.
14. Fritsche, L.G., Lauer, N., Hartmann, A., Stippa, S., Keilhauer, C.N., Oppermann, M., Pandey, M.K., Kohl, J., Zipfel, P.F., Weber, B.H., and Skerka, C. (2010). An imbalance of human complement regulatory proteins CFHR1, CFHR3 and factor H influences risk for age-related macular degeneration (AMD). Hum Mol Genet 19, 4694-4704. doi: 10.1093/hmg/ddq399.
15. Fusaki, N., Ban, H., Nishiyama, A., Saeki, K., and Hasegawa, M. (2009). Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc Jpn Acad Ser B Phys Biol Sci 85, 348-362.
16. Haase, A., Olmer, R., Schwanke, K., Wunderlich, S., Merkert, S., Hess, C., Zweigerdt, R., Gruh, I., Meyer, J., Wagner, S., Maier, L.S., Han, D.W., Glage, S., Miller, K., Fischer, P., Scholer, H.R., and Martin, U. (2009). Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell 5, 434-441. doi: 10.1016/j.stem.2009.08.021.
17. Handa, J.T. (2012). How does the macula protect itself from oxidative stress? Mol Aspects Med 33, 418-435. doi: 10.1016/j.mam.2012.03.006.
18. Hollborn, M., Chen, R., Wiedemann, P., Reichenbach, A., Bringmann, A., and Kohen, L. (2013). Cytotoxic effects of curcumin in human retinal pigment epithelial cells. PLoS One 8, e59603. doi: 10.1371/journal.pone.0059603.
19. Jager, R.D., Mieler, W.F., and Miller, J.W. (2008). Age-related macular degeneration. N Engl J Med 358, 2606-2617. doi: 10.1056/NEJMra0801537.
20. Jiang, T.F., Zhang, Y.J., Zhou, H.Y., Wang, H.M., Tian, L.P., Liu, J., Ding, J.Q., and Chen, S.D. (2013). Curcumin ameliorates the neurodegenerative pathology in A53T alpha-synuclein cell model of Parkinson's disease through the downregulation of mTOR/p70S6K signaling and the recovery of macroautophagy. J Neuroimmune Pharmacol 8, 356-369. doi: 10.1007/s11481-012-9431-7.
21. Landa, G., Su, E., Garcia, P.M., Seiple, W.H., and Rosen, R.B. (2011). Inner segment-outer segment junctional layer integrity and corresponding retinal sensitivity in dry and wet forms of age-related macular degeneration. Retina 31, 364-370. doi: 10.1097/IAE.0b013e3181e91132.
22. Loh, Y.H., Agarwal, S., Park, I.H., Urbach, A., Huo, H., Heffner, G.C., Kim, K., Miller, J.D., Ng, K., and Daley, G.Q. (2009). Generation of induced pluripotent stem cells from human blood. Blood 113, 5476-5479. doi: 10.1182/blood-2009-02-204800.
23. Macdonald, I., and Miller, J. (2011). Genetic factors and AMD. Can J Ophthalmol 46, 456-457. doi: 10.1016/j.jcjo.2011.09.024.
24. Maehr, R., Chen, S., Snitow, M., Ludwig, T., Yagasaki, L., Goland, R., Leibel, R.L., and Melton, D.A. (2009). Generation of pluripotent stem cells from patients with type 1 diabetes. Proc Natl Acad Sci U S A 106, 15768-15773. doi: 10.1073/pnas.0906894106.
25. Mandal, M.N., Patlolla, J.M., Zheng, L., Agbaga, M.P., Tran, J.T., Wicker, L., Kasus-Jacobi, A., Elliott, M.H., Rao, C.V., and Anderson, R.E. (2009). Curcumin protects retinal cells from light-and oxidant stress-induced cell death. Free Radic Biol Med 46, 672-679. doi: 10.1016/j.freeradbiomed.2008.12.006.
26. Noorafshan, A., and Ashkani-Esfahani, S. (2013). A review of therapeutic effects of curcumin. Curr Pharm Des 19, 2032-2046.
27. Nowak, J.Z. (2006). Age-related macular degeneration (AMD): pathogenesis and therapy. Pharmacol Rep 58, 353-363.
28. Osakada, F., Jin, Z.B., Hirami, Y., Ikeda, H., Danjyo, T., Watanabe, K., Sasai, Y., and Takahashi, M. (2009). In vitro differentiation of retinal cells from human pluripotent stem cells by small-molecule induction. J Cell Sci 122, 3169-3179. doi: 10.1242/jcs.050393.
29. Park, I.H., Arora, N., Huo, H., Maherali, N., Ahfeldt, T., Shimamura, A., Lensch, M.W., Cowan, C., Hochedlinger, K., and Daley, G.Q. (2008). Disease-specific induced pluripotent stem cells. Cell 134, 877-886. doi: 10.1016/j.cell.2008.07.041.
30. Romano, G., Morales, F., Marino, I.R., and Giordano, A. (2013). A commentary on iPS cell biology: Potential applications in autologous tissue and cell transplantation, development of new models for the study of human pathological conditions and drug screening. J Cell Physiol. doi: 10.1002/jcp.24437.
31. Saha, K., and Jaenisch, R. (2009). Technical challenges in using human induced pluripotent stem cells to model disease. Cell Stem Cell 5, 584-595. doi: 10.1016/j.stem.2009.11.009.
32. Samiec, P.S., Drews-Botsch, C., Flagg, E.W., Kurtz, J.C., Sternberg, P., Jr., Reed, R.L., and Jones, D.P. (1998). Glutathione in human plasma: decline in association with aging, age-related macular degeneration, and diabetes. Free Radic Biol Med 24, 699-704.
33. Schwartz, S.D., Hubschman, J.P., Heilwell, G., Franco-Cardenas, V., Pan, C.K., Ostrick, R.M., Mickunas, E., Gay, R., Klimanskaya, I., and Lanza, R. (2012). Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 379, 713-720. doi: 10.1016/S0140-6736(12)60028-2.
34. Seki, T., Yuasa, S., and Fukuda, K. (2012). Generation of induced pluripotent stem cells from a small amount of human peripheral blood using a combination of activated T cells and Sendai virus. Nat Protoc 7, 718-728. doi: 10.1038/nprot.2012.015.
35. Shahid, H., Khan, J.C., Cipriani, V., Sepp, T., Matharu, B.K., Bunce, C., Harding, S.P., Clayton, D.G., Moore, A.T., Yates, J.R., and Genetic Factors In, A.M.D.S.G. (2012). Age-related macular degeneration: the importance of family history as a risk factor. Br J Ophthalmol 96, 427-431. doi: 10.1136/bjophthalmol-2011-300193.
36. Singh, R., Shen, W., Kuai, D., Martin, J.M., Guo, X., Smith, M.A., Perez, E.T., Phillips, M.J., Simonett, J.M., Wallace, K.A., Verhoeven, A.D., Capowski, E.E., Zhang, X., Yin, Y., Halbach, P.J., Fishman, G.A., Wright, L.S., Pattnaik, B.R., and Gamm, D.M. (2013). iPS cell modeling of Best disease: insights into the pathophysiology of an inherited macular degeneration. Hum Mol Genet 22, 593-607. doi: 10.1093/hmg/dds469.
37. Song, D., and Dunaief, J.L. (2013). Retinal iron homeostasis in health and disease. Front Aging Neurosci 5, 24. doi: 10.3389/fnagi.2013.00024.
38. Sreejayan, and Rao, M.N. (1997). Nitric oxide scavenging by curcuminoids. J Pharm Pharmacol 49, 105-107.
39. Stadtfeld, M., Nagaya, M., Utikal, J., Weir, G., and Hochedlinger, K. (2008). Induced pluripotent stem cells generated without viral integration. Science 322, 945-949. doi: 10.1126/science.1162494.
40. Staerk, J., Dawlaty, M.M., Gao, Q., Maetzel, D., Hanna, J., Sommer, C.A., Mostoslavsky, G., and Jaenisch, R. (2010). Reprogramming of human peripheral blood cells to induced pluripotent stem cells. Cell Stem Cell 7, 20-24. doi: 10.1016/j.stem.2010.06.002.
41. Stanton, C.M., and Wright, A.F. (2014). Inflammatory Biomarkers for AMD. Adv Exp Med Biol 801, 251-257. doi: 10.1007/978-1-4614-3209-8_32.
42. Su, R.J., Baylink, D.J., Neises, A., Kiroyan, J.B., Meng, X., Payne, K.J., Tschudy-Seney, B., Duan, Y., Appleby, N., Kearns-Jonker, M., Gridley, D.S., Wang, J., Lau, K.H., and Zhang, X.B. (2013). Efficient generation of integration-free ips cells from human adult peripheral blood using BCL-XL together with Yamanaka factors. PLoS One 8, e64496. doi: 10.1371/journal.pone.0064496.
43. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872. doi: 10.1016/j.cell.2007.11.019.
44. Tate, D.J., Jr., Miceli, M.V., and Newsome, D.A. (1995). Phagocytosis and H2O2 induce catalase and metallothionein gene expression in human retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 36, 1271-1279.
45. Tokarz, P., Kaarniranta, K., and Blasiak, J. (2013). Role of antioxidant enzymes and small molecular weight antioxidants in the pathogenesis of age-related macular degeneration (AMD). Biogerontology 14, 461-482. doi: 10.1007/s10522-013-9463-2.
46. Winkler, B.S., Boulton, M.E., Gottsch, J.D., and Sternberg, P. (1999). Oxidative damage and age-related macular degeneration. Mol Vis 5, 32.
47. Woo, J.M., Shin, D.Y., Lee, S.J., Joe, Y., Zheng, M., Yim, J.H., Callaway, Z., and Chung, H.T. (2012). Curcumin protects retinal pigment epithelial cells against oxidative stress via induction of heme oxygenase-1 expression and reduction of reactive oxygen. Mol Vis 18, 901-908.
48. Yildirim, Z., Ucgun, N.I., and Yildirim, F. (2011). The role of oxidative stress and antioxidants in the pathogenesis of age-related macular degeneration. Clinics (Sao Paulo) 66, 743-746.
49. Young, R.W. (1987). Pathophysiology of age-related macular degeneration. Surv Ophthalmol 31, 291-306.
50. Yu, J., Vodyanik, M.A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J.L., Tian, S., Nie, J., Jonsdottir, G.A., Ruotti, V., Stewart, R., Slukvin, Ii, and Thomson, J.A. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920. doi: 10.1126/science.1151526.