Sustained inhibition of neovascularization in vldlr-/- mice following intravitreal injection of cerium oxide nanoparticles and the role of the ASK1-P38/JNK-NF-κB pathway

Biomaterials

Volumn 35, Issue 1, 2014, Pages 249-258

  Cai, Xue ^a   Seal, Sudipta ^c   McGinnis, James F ^a,b  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

Nanoceria; Neovascularization; Retinal degeneration; Signal transduction; Vldlr mouse

Indexed keywords

CERIUM OXIDE NANOPARTICLE; GLIAL FIBRILLARY ACIDIC PROTEINS; NANO-CERIA; NEO-VASCULARIZATION; RETINAL DEGENERATIONS; VASCULAR ENDOTHELIAL GROWTH FACTOR; VERY LOW DENSITY LIPOPROTEIN RECEPTORS; VLDLR-/- MOUSE;

BLOOD VESSELS; CELL DEATH; DRUG THERAPY; ENDOTHELIAL CELLS; ENZYME INHIBITION; GENE EXPRESSION; MAMMALS; NANOPARTICLES; OXIDES; REGRESSION ANALYSIS; SIGNAL TRANSDUCTION;

GENE EXPRESSION REGULATION;

ACROLEIN; APOPTOSIS SIGNAL REGULATING KINASE 1; CASPASE 3; CERIUM OXIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METAL NANOPARTICLE; MITOGEN ACTIVATED PROTEIN KINASE P38; NANOCERIA; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; VASCULOTROPIN; VERY LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CHOROID; CONTROLLED STUDY; GENE INACTIVATION; GLIA CELL; MOUSE; MUELLER CELL; NEWBORN; NONHUMAN; OPHTHALMOSCOPY; OXIDATIVE STRESS; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA BLOOD VESSEL; RETINA DEGENERATION; RETINA FLUORESCEIN ANGIOGRAPHY; RETINA NEOVASCULARIZATION; SIGNAL TRANSDUCTION;

MUS;

NANOCERIA; NEOVASCULARIZATION; RETINAL DEGENERATION; SIGNAL TRANSDUCTION; VLDLR(-/-) MOUSE;

ANIMALS; CERIUM; GENE EXPRESSION REGULATION; MAP KINASE KINASE KINASE 5; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NANOPARTICLES; NEOVASCULARIZATION, PATHOLOGIC; NF-KAPPA B; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; POLYMERASE CHAIN REACTION; RECEPTORS, LDL; VITREOUS BODY;

EID: 84887025605     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.10.022     Document Type: Article

References (54)

1. Bird A.C. Age-related macular disease. Br J Ophthalmol 1996, 80:2-3.
2. Bird A.C. Therapeutic targets in age-related macular disease. JClin Invest 2010, 120:3033-3041.
3. Heckenlively J.R., Hawes N.L., Friedlander M., Nusinowitz S., Hurd R., Davisson M., et al. Mouse model of subretinal neovascularization with choroidal anastomosis. Retina 2003, 23:518-522.
4. Hu W., Jiang A., Liang J., Meng H., Chang B., Gao H., et al. Expression of VLDLR in the retina and evolution of subretinal neovascularization in the knockout mouse model's retinal angiomatous proliferation. Invest Ophthalmol Vis Sci 2008, 49:407-415.
5. Frykman P.K., Brown M.S., Yamamoto T., Goldstein J.L., Herz J. Normal plasma lipoproteins and fertility in gene-targeted mice homozygous for a disruption in the gene encoding very low density lipoprotein receptor. Proc Natl Acad Sci U S A 1995, 92:8453-8457.
6. Shen J.K., Dong A., Hackett S.F., Bell W.R., Green W.R., Campochiaro P.A. Oxidative damage in age-related macular degeneration. Histol Histopathol 2007, 22:1301-1308.
7. Cai X., McGinnis J.F. Oxidative stress: the achilles' heel of neurodegenerative diseases of the retina. Front Biosci 2012, 17:1976-1995.
8. Dong A., Xie B., Shen J., Yoshida T., Yokoi K., Hackett S.F., et al. Oxidative stress promotes ocular neovascularization. JCell Physiol 2009, 219:544-552.
9. Salminen A., Kauppinen A., Hyttinen J.M., Toropainen E., Kaarniranta K. Endoplasmic reticulum stress in age-related macular degeneration: trigger for neovascularization. Mol Med 2010, 16:535-542.
10. Chen Y., Hu Y., Moiseyev G., Zhou K.K., Chen D., Ma J.X. Photoreceptor degeneration and retinal inflammation induced by very low-density lipoprotein receptor deficiency. Microvasc Res 2009, 78:119-127.
11. Dorrell M.I., Aguilar E., Jacobson R., Yanes O., Gariano R., Heckenlively J., et al. Antioxidant or neurotrophic factor treatment preserves function in a mouse model of neovascularization-associated oxidative stress. JClin Invest 2009, 119:611-623.
12. Chen Y., Hu Y., Lu K., Flannery J.G., Ma J.X. Very low density lipoprotein receptor, a negative regulator of the wnt signaling pathway and choroidal neovascularization. JBiol Chem 2007, 282:34420-34428.
13. Li C., Huang Z., Kingsley R., Zhou X., Li F., Parke D.W., et al. Biochemical alterations in the retinas of very low-density lipoprotein receptor knockout mice: an animal model of retinal angiomatous proliferation. Arch Ophthalmol 2007, 125:795-803.
14. Penn J.S., Madan A., Caldwell R.B., Bartoli M., Caldwell R.W., Hartnett M.E. Vascular endothelial growth factor in eye disease. Prog Retin Eye Res 2008, 27:331-371.
15. Zhou X., Wong L.L., Karakoti A.S., Seal S., McGinnis J.F. Nanoceria inhibit the development and promote the regression of pathologic retinal neovascularization in the Vldlr knockout mouse. PLoS One 2011, 6:e16733.
16. Kovach J.L., Schwartz S.G., Flynn H.W., Scott I.U. Anti-VEGF treatment strategies for wet AMD. JOphthalmol 2012, 2012:786870.
17. Chakravarthy U., Evans J., Rosenfeld P.J. Age related macular degeneration. BMJ 2010, 340:c981.
18. Chen J., Patil S., Seal S., McGinnis J.F. Rare earth nanoparticles prevent retinal degeneration induced by intracellular peroxides. Nat Nanotechnol 2006, 1:142-150.
19. Perez J.M., Asati A., Nath S., Kaittanis C. Synthesis of biocompatible dextran-coated nanoceria with pH-dependent antioxidant properties. Small 2008, 4:552-556.
20. Vincent A., Inerbaev T.M., Babu S., Karakoti A.S., Self W.T., Masunov A.E., et al. Tuning hydrated nanoceria surfaces: experimental/theoretical investigations of ion exchange and implications in organic and inorganic interactions. Langmuir 2010, 26:7188-7198.
21. Heckert E.G., Karakoti A.S., Seal S., Self W.T. The role of cerium redox state in the SOD mimetic activity of nanoceria. Biomaterials 2008, 29:2705-2709.
22. Das S., Singh S., Dowding J.M., Oommen S., Kumar A., Sayle T.X., et al. The induction of angiogenesis by cerium oxide nanoparticles through the modulation of oxygen in intracellular environments. Biomaterials 2012, 33:7746-7755.
23. 2-X nanocrystalline particles. Appl Surf Sci 1999, 152:53-56.
24. Karakoti A.S., Singh S., Kumar A., Malinska M., Kuchibhatla S.V., Wozniak K., et al. PEGylated nanoceria as radical scavenger with tunable redox chemistry. JAm Chem Soc 2009, 131:14144-14145.
25. Wong L.L., Hirst S.M., Pye Q.N., Reilly C.M., Seal S., McGinnis J.F. Catalytic nanoceria are preferentially retained in the rat retina and are not cytotoxic after intravitreal injection. PLoS One 2013, 8:e58431.
26. Kong L., Cai X., Zhou X., Wong L.L., Karakoti A.S., Seal S., et al. Nanoceria extend photoreceptor cell lifespan in tubby mice by modulation of apoptosis/survival signaling pathways. Neurobiol Dis 2011, 42:514-523.
27. Cai X., Sezate S.A., Seal S., McGinnis J.F. Sustained protection against photoreceptor degeneration in tubby mice by intravitreal injection of nanoceria. Biomaterials 2012, 33:8771-8781.
28. Kyosseva S.V., Chen L., Seal S., McGinnis J.F. Nanoceria inhibit expression of genes associated with inflammation and angiogenesis in the retina of Vldlr null mice. Exp Eye Res 2013, 116C:63-74.
29. Pfaffl M.W. Anew mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
30. Connolly S.E., Hores T.A., Smith L.E., D'Amore P.A. Characterization of vascular development in the mouse retina. Microvasc Res 1988, 36:275-290.
31. Taylor R.C., Acquaah-Mensah G., Singhal M., Malhotra D., Biswal S. Network inference algorithms elucidate Nrf2 regulation of mouse lung oxidative stress. PLoS Comput Biol 2008, 4:e1000166.
32. Bai Y., Ma J.X., Guo J., Wang J., Zhu M., Chen Y., et al. Muller cell-derived VEGF is a significant contributor to retinal neovascularization. JPathol 2009, 219:446-454.
33. Aartsen W.M., van Cleef K.W., Pellissier L.P., Hoek R.M., Vos R.M., Blits B., et al. GFAP-driven GFP expression in activated mouse Muller glial cells aligning retinal blood vessels following intravitreal injection of AAV2/6 vectors. PLoS One 2010, 5:e12387.
34. Izumi Y., Kim-Mitsuyama S., Yoshiyama M., Omura T., Shiota M., Matsuzawa A., et al. Important role of apoptosis signal-regulating kinase 1 in ischemia-induced angiogenesis. Arterioscler Thromb Vasc Biol 2005, 25:1877-1883.
35. Wu G., Luo J., Rana J.S., Laham R., Sellke F.W., Li J. Involvement of COX-2 in VEGF-induced angiogenesis via P38 and JNK pathways in vascular endothelial cells. Cardiovasc Res 2006, 69:512-519.
36. Watari K., Nakamura M., Fukunaga Y., Furuno A., Shibata T., Kawahara A., et al. The antitumor effect of a novel angiogenesis inhibitor (an octahydronaphthalene derivative) targeting both VEGF receptor and NF-kappaB pathway. Int J Cancer 2012, 131:310-321.
37. Furuno A., Watari K., Nakamura M., Fukunaga Y., Jung J.H., Ono M. Anatural anti-inflammatory enone fatty acid inhibits angiogenesis by attenuating nuclear factor-kappaB signaling in vascular endothelial cells. Int J Oncol 2011, 38:493-501.
38. Hirotani S., Otsu K., Nishida K., Higuchi Y., Morita T., Nakayama H., et al. Involvement of nuclear factor-kappaB and apoptosis signal-regulating kinase 1 in G-protein-coupled receptor agonist-induced cardiomyocyte hypertrophy. Circulation 2002, 105:509-515.
39. Pierce E.A., Avery R.L., Foley E.D., Aiello L.P., Smith L.E. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci U S A 1995, 92:905-909.
40. Miller J.W., Adamis A.P., Aiello L.P. Vascular endothelial growth factor in ocular neovascularization and proliferative diabetic retinopathy. Diabetes Metab Rev 1997, 13:37-50.
41. Lu L., Oveson B.C., Jo Y.J., Lauer T.W., Usui S., Komeima K., et al. Increased expression of glutathione peroxidase 4 strongly protects retina from oxidative damage. Antioxid Redox Signal 2009, 11:715-724.
42. Funato Y., Miki H. Redox regulation of Wnt signalling via nucleoredoxin. Free Radic Res 2010, 44:379-388.
43. Funato Y., Terabayashi T., Sakamoto R., Okuzaki D., Ichise H., Nojima H., et al. Nucleoredoxin sustains Wnt/beta-catenin signaling by retaining a pool of inactive dishevelled protein. Curr Biol 2010, 20:1945-1952.
44. Singh S., Kumar A., Karakoti A., Seal S., Self W.T. Unveiling the mechanism of uptake and sub-cellular distribution of cerium oxide nanoparticles. Mol Biosyst 2010, 6:1813-1820.
45. Homma K., Katagiri K., Nishitoh H., Ichijo H. Targeting ASK1 in ER stress-related neurodegenerative diseases. Expert Opin Ther Targets 2009, 13:653-664.
46. Nagai H., Noguchi T., Takeda K., Ichijo H. Pathophysiological roles of ASK1-MAP kinase signaling pathways. JBiochem Mol Biol 2007, 40:1-6.
47. Hattori K., Naguro I., Runchel C., Ichijo H. The roles of ASK family proteins in stress responses and diseases. Cell Commun Signal 2009, 7:9.
48. Ichijo H., Nishida E., Irie K., ten Dijke P., Saitoh M., Moriguchi T., et al. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 1997, 275:90-94.
49. Tobiume K., Matsuzawa A., Takahashi T., Nishitoh H., Morita K., Takeda K., et al. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2001, 2:222-228.
50. Lan W., Petznick A., Heryati S., Rifada M., Tong L. Nuclear Factor-kappaB: central regulator in ocular surface inflammation and diseases. Ocul Surf 2012, 10:137-148.
51. Guma M., Rius J., Duong-Polk K.X., Haddad G.G., Lindsey J.D., Karin M. Genetic and pharmacological inhibition of JNK ameliorates hypoxia-induced retinopathy through interference with VEGF expression. Proc Natl Acad Sci U S A 2009, 106:8760-8765.
52. Umigai N., Tanaka J., Tsuruma K., Shimazawa M., Hara H. Crocetin, a carotenoid derivative, inhibits VEGF-induced angiogenesis via suppression of p38 phosphorylation. Curr Neurovasc Res 2012, 9:102-109.
53. Collet J.F., Messens J. Structure, function, and mechanism of thioredoxin proteins. Antioxid Redox Signal 2010, 13:1205-1216.
54. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 1998, 17:2596-2606.