Suppression of Experimental Choroidal Neovascularization by Curcumin in Mice

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Xie, Ping ^a   Zhang, WeiWei ^a   Yuan, Songtao ^a   Chen, Zhiqiang ^b   Yang, Qin ^a   Yuan, DongQing ^a   Wang, Feng ^a   Liu, QingHuai ^a  

^a THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^b Jiangsu Province Official Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

C 1386; CURCUMIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; DRUG ACTIVITY; DRUG DOSE COMPARISON; ENZYME LINKED IMMUNOSORBENT ASSAY; GRANULOCYTE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LASER COAGULATION; MACROPHAGE; MALE; MOUSE; NONHUMAN; PIGMENT EPITHELIUM; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RETINA FLUORESCEIN ANGIOGRAPHY; RETINA MACULA AGE RELATED DEGENERATION; SUBRETINAL NEOVASCULARIZATION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CHOROIDAL NEOVASCULARIZATION; CURCUMIN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; FLUORESCEIN ANGIOGRAPHY; GRANULOCYTES; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL;

MUS;

EID: 84871681400     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053329     Document Type: Article

References (86)

1. Fine SL, Berger JW, Maguire MG, Ho AC, (2000) Age-related macular degeneration. N Engl J Med 342: 483-492.
2. Kulkarni AD, Kuppermann BD, (2005) Wet age-related macular degeneration. Adv Drug Deliv Rev 57: 1994-2009.
3. Sakurai E, Anand A, Ambati BK, van Rooijen N, Ambati J, (2003) Macrophage depletion inhibits experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 44: 3578-3585.
4. Tsutsumi C, Sonoda KH, Egashira K, Qiao H, Hisatomi T, et al. (2003) The critical role of ocular-infiltrating macrophages in the development of choroidal neovascularization. J Leukoc Biol 74: 25-32.
5. Krzystolik MG, Afshari MA, Adamis AP, Gaudreault J, Gragoudas ES, et al. (2002) Prevention of experimental choroidal neovascularization with intravitreal anti-vascular endothelial growth factor antibody fragment. Arch Ophthalmol 120: 338-346.
6. Grossniklaus HE, Ling JX, Wallace TM, Dithmar S, Lawson DH, et al. (2002) Macrophage and retinal pigment epithelium expression of angiogenic cytokines in choroidal neovascularization. Mol Vis 8: 119-126.
7. Xiong M, Elson G, Legarda D, Leibovich SJ, (1998) Production of vascular endothelial growth factor by murine macrophages: regulation by hypoxia, lactate, and the inducible nitric oxide synthase pathway. Am J Pathol 153: 587-598.
8. Ishibashi T, Hata Y, Yoshikawa H, Nakagawa K, Sueishi K, et al. (1997) Expression of vascular endothelial growth factor in experimental choroidal neovascularization. Graefes Arch Clin Exp Ophthalmol 235: 159-167.
9. Espinosa-Heidmann DG, Suner IJ, Hernandez EP, Monroy D, Csaky KG, et al. (2003) Macrophage depletion diminishes lesion size and severity in experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 44: 3586-3592.
10. Zhou J, Pham L, Zhang N, He S, Gamulescu MA, et al. (2005) Neutrophils promote experimental choroidal neovascularization. Mol Vis. 11: 414-424.
11. Hara R, Inomata Y, Kawaji T, Sagara N, Inatani M, et al. (2010) Suppression of choroidal neovascularization by N-acetyl-cysteine in mice. Curr Eye Res. 35: 1012-1020.
12. Yamada K, Sakurai E, Itaya M, Yamasaki S, Ogura Y, (2007) Inhibition of laser-induced choroidal neovascularization by atorvastatin by downregulation of monocyte chemotactic protein-1 synthesis in mice. Invest Ophthalmol Vis Sci 48: 1839-1843.
13. Benny O, Nakai K, Yoshimura T, Bazinet L, Akula JD, et al. (2010) Broad Spectrum Antiangiogenic Treatment for Ocular Neovascular Diseases. PLoS One 5: e12515.
14. Chen H, Liu B, Lukas TJ, Neufeld AH, (2008) The aged retinal pigment epithelium/choroid: a potential substratum for the pathogenesis of age-related macular degeneration. PLoS One 3: e2339.
15. Yeh DC, Bula DV, Miller JW, Gragoudas ES, Arroyo JG, (2004) Expression of leukocyte adhesion molecules in human subfoveal choroidal neovascular membranes treated with and without photodynamic therapy. Invest Ophthalmol Vis Sci 45: 2368-2373.
16. Sakurai E, Taguchi H, Anand A, Ambati BK, Gragoudas ES, et al. (2003) Targeted disruption of the CD18 or ICAM-1 gene inhibits choroidal neovascularization. Invest Ophthalmol Vis Sci 44: 2743-2749.
17. Espinosa-Heidmann DG, Marin-Castano ME, Pereira-Simon S, Hernandez EP, Elliot S, et al. (2005) Gender and estrogen supplementation increases severity of experimental choroidal neovascularization. Exp Eye Res 80: 413-423.
18. Oh H, Takagi H, Takagi C, Suzuma K, Otani A, et al. (1999) The potential angiogenic role of macrophages in the formation of choroidal neovascular membranes. Invest Ophthalmol Vis Sci 40: 1891-1898.
19. Luhmann UF, Robbie S, Munro PM, Barker SE, Duran Y, et al. (2009) The drusenlike phenotype in aging Ccl2-knockout mice is caused by an accelerated accumulation of swollen autofluorescent subretinal macrophages. Invest Ophthalmol Vis Sci 50: 5934-5943.
20. Regatieri CV, Dreyfuss JL, Melo GB, Lavinsky D, Farah ME, et al. (2009) Dual role of intravitreous infliximab in experimental choroidal neovascularization: effect on the expression of sulfated glycosaminoglycans. Invest Ophthalmol Vis Sci 50: 5487-5494.
21. Shi X, Semkova I, Müther PS, Dell S, Kociok N, et al. (2006) Inhibition of TNF-alpha reduces laser-induced choroidal neovascularization. Exp Eye Res 83: 1325-1334.
22. Izumi-Nagai K, Nagai N, Ohgami K, Satofuka S, Ozawa Y, et al. (2007) Macular pigment lutein is antiinflammatory in preventing choroidal neovascularization. Arterioscler Thromb Vasc Biol 27: 2555-2562.
23. Yoshida T, Zhang H, Iwase T, Shen J, Semenza GL, et al. (2010) Digoxin inhibits retinal ischemia-induced HIF-1alpha expression and ocular neovascularization. FASEB J. 24: 1759-1767.
24. Singh S, (2007) From exotic spice to modern drug? Cell 130: 765-768.
25. Sikora E, Scapagnini G, Barbagallo M, (2010) Curcumin, inflammation, ageing and age-related diseases. Immun Ageing 7: 1-4.
26. Zhou H, Beevers CS, Huang S, (2011) The targets of curcumin. Curr Drug Targets 12: 332-347.
27. Mrudula T, Suryanarayana P, Srinivas PN, Reddy GB, (2007) Effect of curcumin on hyperglycemia-induced vascular endothelial growth factor expression in streptozotocin-induced diabetic rat retina. Biochem Biophys Res Commun. 361: 528-532.
28. Deodhar SD, Sethi R, Srimal RC, (1980) Preliminary study on antirheumatic activity of curcumin (diferuloyl methane). Indian J Med Res 71: 632-634.
29. Heng MC, Song MK, Harker J, Heng MK, (2000) Drug-induced suppression of phosphorylase kinase activity correlates with resolution of psoriasis as assessed by clinical, histological and immunohistochemical parameters. Br J Dermatol 143: 937-949.
30. Holt PR, Katz S, Kirshoff R, (2005) Curcumin therapy in inflammatory bowel disease: a pilot study. Dig Dis Sci 50: 2191-2193.
31. Hanai H, Iida T, Takeuchi K, Watanabe F, Maruyama Y, et al. (2006) Curcumin maintenance therapy for ulcerative colitis: randomized, multicenter, double-blind, placebo-controlled trial. Clin Gastroenterol Hepatol 4: 1502-1506.
32. Shoskes D, Lapierre C, Cruz-Correa M, Muruve N, Rosario R, et al. (2005) Beneficial effects of the bioflavonoids curcumin and quercetin on early function in cadaveric renal transplantation: a randomized placebo controlled trial. Transplantation 80: 1556-1559.
33. Lal B, Kapoor AK, Asthana OP, Agrawal PK, Prasad R, et al. (1999) Efficacy of curcumin in the management of chronic anterior uveitis. Phytother Res 13: 318-322.
34. Allegri P, Mastromarino A, Neri P, (2010) Management of chronic anterior uveitis relapses: efficacy of oral phospholipidic curcumin treatment. Long-term follow-up. Clin Ophthalmol 21: 1201-1206.
35. Lal B, Kapoor AK, Agrawal PK, Asthana OP, Srimal RC, (2000) Role of curcumin in idiopathic inflammatory orbital pseudotumours. Phytother Res 14: 443-447.
36. Takehana Y, Kurokawa T, Kitamura T, Tsukahara Y, Akahane S, et al. (1999) Suppression of laser-induced choroidal neovascularization by oral tranilast in the rat. Invest Ophthalmol Vis Sci 40: 459-466.
37. Andrews NC, Faller DV, (1991) A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res 19: 2499.
38. Furie MB, Randolph GJ, (1995) Chemokines and tissue injury. Am J Pathol 146: 1287-1301.
39. Itaya M, Sakurai E, Nozaki M, Yamada K, Yamasaki S, et al. (2007) Upregulation of VEGF in murine retina via monocyte recruitment after retinal scatter laser photocoagulation. Invest Ophthalmol Vis Sci 48: 5677-5683.
40. Curry JM, Eubank TD, Roberts RD, Wang Y, Pore N, et al. (2008) M-CSF signals through the MAPK/ERK pathway via Sp1 to induce VEGF production and induces angiogenesis in vivo. PLoS One 3: e3405.
41. Caicedo A, Espinosa-Heidmann DG, Piña Y, Hernandez EP, Cousins SW, (2005) Blood-derived macrophages infiltrate the retina and activate Muller glial cells under experimental choroidal neovascularization. Exp Eye Res 81: 38-47.
42. Woo HM, Kang JH, Kawada T, Yoo H, Sung MK, et al. (2007) Active spice-derived components can inhibit inflammatory responses of adipose tissue in obesity by suppressing inflammatory actions of macrophages and release of monocyte chemoattractant protein-1 from adipocytes. Life Sci 80: 926-931.
43. Soetikno V, Sari FR, Veeraveedu PT, Thandavarayan RA, Harima M, et al. (2011) Curcumin ameliorates macrophage infiltration by inhibiting NF-κB activation and proinflammatory cytokines in streptozotocin induced-diabetic nephropathy. Nutr Metab (Lond) 8: 35.
44. Kuwabara N, Tamada S, Iwai T, Teramoto K, Kaneda N, et al. (2006) Attenuation of renal fibrosis by curcumin in rat obstructive nephropathy. Urology 67: 440-446.
45. Zhong F, Chen H, Han L, Jin Y, Wang W, (2011) Curcumin attenuates lipopolysaccharide-induced renal inflammation. Biol Pharm Bull 34: 226-232.
46. Pan Y, Wang Y, Cai L, Cai Y, Hu J, et al. (2012) Inhibition of high glucose-induced inflammatory response and macrophage infiltration by a novel curcumin derivative prevents renal injury in diabetic rats. Br J Pharmacol 166: 1169-1182.
47. Takahashi M, Ishiko T, Kamohara H, Hidaka H, Ikeda O, et al. (2007) Curcumin (1,7-bis(4-hydroxy-3-methoxyphenyl)-1,6-heptadiene-3,5-dione) blocks the chemotaxis of neutrophils by inhibiting signal transduction through IL-8 receptors. Mediators Inflamm. 2007: 10767.
48. Larmonier CB, Midura-Kiela MT, Ramalingam R, Laubitz D, Janikashvili N, et al. (2011) Modulation of neutrophil motility by curcumin: implications for inflammatory bowel disease. Inflamm Bowel Dis. 17: 503-515.
49. Gukovsky I, Reyes CN, Vaquero EC, Gukovskaya AS, Pandol SJ, (2003) Curcumin ameliorates ethanol and nonethanol experimental pancreatitis. Am J Physiol Gastrointest Liver Physiol. 284: G85-95.
50. Moghaddam SJ, Barta P, Mirabolfathinejad SG, Ammar-Aouchiche Z, Garza NT, et al. (2009) Curcumin inhibits COPD-like airway inflammation and lung cancer progression in mice. Carcinogenesis. 30: 1949-1956.
51. Jackson JK, Higo T, Hunter WL, Burt HM, (2006) The antioxidants curcumin and quercetin inhibit inflammatory processes associated with arthritis. Inflamm Res. 55: 168-175.
52. Madan B, Ghosh B, (2003) Diferuloylmethane inhibits neutrophil infiltration and improves survival of mice in high-dose endotoxin shock. Shock. 19: 91-96.
53. Kent D, Sheridan C, (2003) Choroidal neovascularization: a wound healing perspective. Mol Vis 9: 747-755.
54. Ferrara N, Houck K, Jakeman L, Leung DW, (1992) Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocr Rev 13: 18-32.
55. Kowluru RA, Kanwar M, (2007) Effects of curcumin on retinal oxidative stress and inflammation in diabetes. Nutr Metab (Lond) 16 4: 8.
56. Gupta SK, Kumar B, Nag TC, Agrawal SS, Agrawal R, et al. (2011) Curcumin prevents experimental diabetic retinopathy in rats through its hypoglycemic, antioxidant, and anti-inflammatory mechanisms. J Ocul Pharmacol Ther 27: 123-130.
57. Kim JS, Choi JS, Chung SK, (2010) The effect of curcumin on corneal neovascularization in rabbit eyes. Curr Eye Res 35: 274-280.
58. Sawatpanich T, Petpiboolthai H, Punyarachun B, Anupunpisit V, (2010) Effect of curcumin on vascular endothelial growth factor expression in diabetic mice kidney induced by streptozotocin. J Med Assoc Thai 93Suppl 2: S1-8.
59. Zhang Y, Cao H, Hu YY, Wang H, Zhang CJ, (2011) Inhibitory effect of curcumin on angiogenesis in ectopic endometrium of rats with experimental endometriosis. Int J Mol Med 27: 87-94.
60. Chen WH, Chen Y, Cui GH, (2005) Effects of TNF-alpha and curcumin on the expression of VEGF in Raji and U937 cells and on angiogenesis in ECV304 cells. Chin Med J (Engl) 118: 2052-2057.
61. Hangai M, He S, Hoffmann S, Lim JI, Ryan SJ, et al. (2006) Sequential induction of angiogenic growth factors by TNF-alpha in choroidal endothelial cells. J Neuroimmunol 171: 45-56.
62. Olson JL, Courtney RJ, Mandava N, (2007) Intravitreal infliximab and choroidal neovascularization in an animal model. Arch Ophthalmol 125: 1221-1224.
63. Lichtlen P, Lam TT, Nork TM, Streit T, Urech DM, (2010) Relative contribution of VEGF and TNF-alpha in the cynomolgus laser-induced CNV model: comparing the efficacy of bevacizumab, adalimumab, and ESBA105. Invest Ophthalmol Vis Sci 51: 4738-4745.
64. Markomichelakis NN, Theodossiadis PG, Sfikakis PP, (2005) Regression of neovascular age-related macular degeneration following infliximab therapy. Am J Ophthalmol 139: 537-540.
65. Theodossiadis PG, Liarakos VS, Sfikakis PP, Vergados IA, Theodossiadis GP (2009) Intravitreal administration of the anti-tumor necrosis factor agent infliximab for neovascular age-related macular degeneration. Am J Ophthalmol 147: 825-30.
66. Kim YS, Ahn Y, Hong MH, Joo SY, Kim KH, et al. (2007) Curcumin attenuates inflammatory responses of TNF-alpha-stimulated human endothelial cells. J Cardiovasc Pharmacol 50: 41-49.
67. Nagai N, Oike Y, Izumi-Nagai K, Urano T, Kubota Y, et al. (2006) Angiotensin II type 1 receptor-mediated inflammation is required for choroidal neovascularization. Arterioscler Thromb Vasc Biol 26: 2252-2259.
68. Bian ZM, Elner SG, Strieter RM, Kunkel SL, Lukacs NW, et al. (1999) IL-4 potentiates IL-1beta- and TNF-alpha-stimulated IL-8 and MCP-1 protein production in human retinal pigment epithelial cells. Curr Eye Res 18: 349-357.
69. Elner SG, Strieter RM, Elner VM, Rollins BJ, Del Monte MA, et al. (1991) Monocyte chemotactic protein gene expression by cytokine-treated human retinal pigment epithelial cells. Lab Invest 64: 819-825.
70. Elner SG, Elner VM, Pavilack MA, Todd RF 3rd, Mayo-Bond L, et al (1992) Modulation and function of intercellular adhesion molecule-1 (CD54) on human retinal pigment epithelial cells. Lab Invest 66: 200-211.
71. Sugimoto H, Shikata K, Hirata K, Akiyama K, Matsuda M, et al. (1997) Increased expression of intercellular adhesion molecule-1 (ICAM-1) in diabetic rat glomeruli: glomerular hyperfiltration is a potential mechanism of ICAM-1 upregulation. Diabetes 46: 2075-2081.
72. Ambati J, Anand A, Fernandez S, Sakurai E, Lynn BC, Kuziel WA, et al. (2003) An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat Med 9: 1390-1397.
73. Shen WY, Yu MJ, Barry CJ, Constable IJ, Rakoczy PE, (1998) Expression of cell adhesion molecules and vascular endothelial growth factor in experimental choroidal neovascularisation in the rat. Br J Ophthalmol 82: 1063-1071.
74. Kunnumakkara AB, Anand P, Aggarwal BB, (2008) Curcumin inhibits proliferation, invasion, angiogenesis and metastasis of different cancers through interaction with multiple cell signaling proteins. Cancer Lett 8 269: 199-225.
75. Hayden MS, Ghosh S, (2008) Shared principles in NF-kappaB signaling. Cell 132: 344-362.
76. Hara R, Inomata Y, Kawaji T, Sagara N, Inatani M, et al. (2010) Suppression of choroidal neovascularization by N-acetyl-cysteine in mice. Curr Eye Res 35: 1012-1020.
77. Chen D, Nie M, Fan MW, Bian Z, (2008) Anti-inflammatory activity of curcumin in macrophages stimulated by lipopolysaccharides from Porphyromonas gingivalis. Pharmacology 82: 264-269.
78. Jain SK, Rains J, Croad J, Larson B, Jones K, (2009) Curcumin supplementation lowers TNF-alpha, IL-6, IL-8, and MCP-1 secretion in high glucose-treated cultured monocytes and blood levels of TNF-alpha, IL-6, MCP-1, glucose, and glycosylated hemoglobin in diabetic rats. Antioxid Redox Signal 11: 241-249.
79. Bian ZM, Elner VM, Yoshida A, Kunkel SL, Elner SG, (2001) Signaling pathways for glycated human serum albumin-induced IL-8 and MCP-1 secretion in human RPE cells. Invest Ophthalmol Vis Sci 42: 1660-1668.
80. Kumar A, Dhawan S, Hardegen NJ, Aggarwal BB, (1998) Curcumin (Diferuloylmethane) inhibition of tumor necrosis factor (TNF)-mediated adhesion of monocytes to endothelial cells by suppression of cell surface expression of adhesion molecules and of nuclear factor-kappaB activation. Biochem Pharmacol 55: 775-783.
81. Lin M, Hu Y, Chen Y, Zhou KK, Jin J, et al. (2012) Impacts of hypoxia-inducible factor-1 knockout in the retinal pigment epithelium on choroidal neovascularization. Invest Ophthalmol Vis Sci. 53: 6197-6206.
82. Inoue Y, Yanagi Y, Matsuura K, Takahashi H, Tamaki Y, et al. (2007) Expression of hypoxia-inducible factor 1α and 2α in choroidal neovascular membranes associated with age-related macular degeneration. Br J Ophthalmol. 91: 1720-1721.
83. Sheridan CM, Pate S, Hiscott P, Wong D, Pattwell DM, et al. (2009) Expression of hypoxia-inducible factor-1alpha and-2alpha in human choroidal neovascular membranes. Graefes Arch Clin Exp Ophthalmol. 247: 1361-1367.
84. Song SJ, Chung H, Yu HG, (2008) Inhibitory effect of YC-1, 3-(5′-hydroxymethyl-2′-furyl)-1-benzylindazole, on experimental choroidal neovascularization in rat. Ophthalmic Res. 40: 35-40.
85. Bae MK, Kim SH, Jeong JW, Lee YM, Kim HS, et al. (2006) Curcumin inhibits hypoxia-induced angiogenesis via down-regulation of HIF-1. Oncol Rep. 15: 1557-1562.
86. Jung HJ, Kim JH, Shim JS, Kwon HJ, (2010) A novel Ca2+/calmodulin antagonist HBC inhibits angiogenesis and down-regulates hypoxia-inducible factor. J Biol Chem. 285: 25867-25874.