IKK2 inhibition attenuates laser-induced choroidal neovascularization

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Lu, Huayi ^a,b   Lu, Qingxian ^a   Gaddipati, Subhash ^a   Kasetti, Ramesh Babu ^a   Wang, Wei ^a   Pasparakis, Manolis ^c   Kaplan, Henry J ^a   Li, Qiutang ^a  

^a University of Louisville School of Medicine   (United States)

^b THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE A; HYPOXIA INDUCIBLE FACTOR 1ALPHA; I KAPPA B ALPHA; I KAPPA B KINASE; I KAPPA B KINASE 2; I KAPPA B KINASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; PLATELET DERIVED GROWTH FACTOR A; RNA; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREEDING; CELL VIABILITY; CHOROID; ENZYME INHIBITION; FLOW CYTOMETRY; FLUORESCENCE ANGIOGRAPHY; HEAT SHOCK; HISTOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; KNOCKOUT MOUSE; LASER; MOUSE; NONHUMAN; PATHOGENESIS; POLYMERASE CHAIN REACTION; PROTEIN DEGRADATION; RETINA; RNA ISOLATION; SIGNAL TRANSDUCTION; SUBRETINAL NEOVASCULARIZATION; THERMAL INJURY; WESTERN BLOTTING;

ANIMALS; CHOROIDAL NEOVASCULARIZATION; I-KAPPA B KINASE; LASERS; MICE; MICE, KNOCKOUT; NF-KAPPA B; SIGNAL TRANSDUCTION;

EID: 84900312987     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087530     Document Type: Article

References (69)

1. Haines JL, Spencer KM, Pericak-Vance MA (2007) Bringing the genetics of macular degeneration into focus. Proc Natl Acad Sci U S A 104: 16725-16726. (Pubitemid 350210932)
2. Rattner A, Nathans J (2006) Macular degeneration: recent advances and therapeutic opportunities. Nat Rev Neurosci 7: 860-872. (Pubitemid 44624178)
3. Brown DM, Kaiser PK, Michels M, Soubrane G, Heier JS, et al. (2006) Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N Engl J Med 355: 1432-1444. (Pubitemid 44511558)
4. Gragoudas ES, Adamis AP, Cunningham ET, Jr., Feinsod M, Guyer DR (2004) Pegaptanib for neovascular age-related macular degeneration. N Engl J Med 351: 2805-2816. (Pubitemid 40051904)
5. Rosenfeld PJ, Brown DM, Heier JS, Boyer DS, Kaiser PK, et al. (2006) Ranibizumab for neovascular age-related macular degeneration. N Engl J Med 355: 1419-1431. (Pubitemid 44511557)
6. Lommatzsch A, Hermans P, Muller KD, Bornfeld N, Bird AC, et al. (2008) Are low inflammatory reactions involved in exudative age-related macular degeneration? Morphological and immunhistochemical analysis of AMD associated with basal deposits. Graefes Arch Clin Exp Ophthalmol 246: 803-810.
7. Grossniklaus HE, Miskala PH, Green WR, Bressler SB, Hawkins BS, et al. (2005) Histopathologic and ultrastructural features of surgically excised subfoveal choroidal neovascular lesions: submacular surgery trials report no. 7. Arch Ophthalmol 123: 914-921. (Pubitemid 41057987)
8. Seddon JM, Gensler G, Milton RC, Klein ML, Rifai N (2004) Association between C-reactive protein and age-related macular degeneration. JAMA 291: 704-710. (Pubitemid 38543790)
9. Hageman GS, Anderson DH, Johnson LV, Hancox LS, Taiber AJ, et al. (2005) A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc Natl Acad Sci U S A 102: 7227-7232. (Pubitemid 40696361)
10. Haines JL, Hauser MA, Schmidt S, Scott WK, Olson LM, et al. (2005) Complement factor H variant increases the risk of age-related macular degeneration. Science 308: 419-421. (Pubitemid 40530081)
11. Li Q, Verma IM (2002) NF-kappaB regulation in the immune system. Nat Rev Immunol 2: 725-734.
12. Li Q, Van Antwerp D, Mercurio F, Lee KF, Verma IM (1999) Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science 284: 321-325. (Pubitemid 129523450)
13. Hacker H, Karin M (2006) Regulation and function of IKK and IKK-related kinases. Sci STKE 2006: re13.
14. Yang XM, Wang YS, Zhang J, Li Y, Xu JF, et al. (2009) Role of PI3K/Akt and MEK/ERK in mediating hypoxia-induced expression of HIF-1alpha and VEGF in laser-induced rat choroidal neovascularization. Invest Ophthalmol Vis Sci 50: 1873-1879.
15. Grossniklaus HE, Kang SJ, Berglin L (2010) Animal models of choroidal and retinal neovascularization. Prog Retin Eye Res 29: 500-519.
16. Semenza GL (2001) HIF-1, O(2), and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 107: 1-3.
17. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, et al. (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23: 99-103. (Pubitemid 29418797)
18. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L (2007) A global double-fluorescent Cre reporter mouse. Genesis 45: 593-605. (Pubitemid 350013057)
19. Bora PS, Hu Z, Tezel TH, Sohn JH, Kang SG, et al. (2003) Immunotherapy for choroidal neovascularization in a laser-induced mouse model simulating exudative (wet) macular degeneration. Proc Natl Acad Sci U S A 100: 2679-2684. (Pubitemid 36297558)
20. Prusky GT, Alam NM, Beekman S, Douglas RM (2004) Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci 45: 4611-4616. (Pubitemid 39564690)
21. Franco LM, Zulliger R, Wolf-Schnurrbusch UE, Katagiri Y, Kaplan HJ, et al. (2009) Decreased visual function after patchy loss of retinal pigment epithelium induced by low-dose sodium iodate. Invest Ophthalmol Vis Sci 50: 4004-4010.
22. Hu W, Criswell MH, Ottlecz A, Cornell TL, Danis RP, et al. (2005) Oral administration of lumiracoxib reduces choroidal neovascular membrane development in the rat laser-trauma model. Retina 25: 1054-1064. (Pubitemid 44735104)
23. Connor KM, Krah NM, Dennison RJ, Aderman CM, Chen J, et al. (2009) Quantification of oxygen-induced retinopathy in the mouse: a model of vessel loss, vessel regrowth and pathological angiogenesis. Nat Protoc 4: 1565-1573.
24. Neuvians TP, Gashaw I, Sauer CG, von Ostau C, Kliesch S, et al. (2005) Standardization strategy for quantitative PCR in human seminoma and normal testis. J Biotechnol 117: 163-171. (Pubitemid 40488706)
25. Luedde T, Assmus U, Wustefeld T, Meyer zu Vilsendorf A, Roskams T, et al. (2005) Deletion of IKK2 in hepatocytes does not sensitize these cells to TNF-induced apoptosis but protects from ischemia/reperfusion injury. J Clin Invest 115: 849-859. (Pubitemid 40489389)
26. Ye F, Han L, Lu Q, Dong W, Chen Z, et al. (2011) Retinal self-antigen induces a predominantly Th1 effector response in Axl and Mertk double-knockout mice. J Immunol 187: 4178-4186.
27. Pasparakis M, Courtois G, Hafner M, Schmidt-Supprian M, Nenci A, et al. (2002) TNF-mediated inflammatory skin disease in mice with epidermis-specific deletion of IKK2. Nature 417: 861-866. (Pubitemid 34670334)
28. Podolin PL, Callahan JF, Bolognese BJ, Li YH, Carlson K, et al. (2005) Attenuation of murine collagen-induced arthritis by a novel, potent, selective small molecule inhibitor of IkappaB Kinase 2, TPCA-1 (2-[(aminocarbonyl)a-mino]- 5-(4-fluorophenyl)-3-thiophenecarboxamide), occurs via reduction of proinflammatory cytokines and antigen-induced T cell Proliferation. J Pharmacol Exp Ther 312: 373-381. (Pubitemid 40096491)
29. Liu J, Jha P, Lyzogubov VV, Tytarenko RG, Bora NS, et al. (2011) Relationship between complement membrane attack complex, chemokine (C-C motif) ligand 2 (CCL2) and vascular endothelial growth factor in mouse model of laser-induced choroidal neovascularization. J Biol Chem 286: 20991-21001.
30. Nagashima K, Sasseville VG, Wen D, Bielecki A, Yang H, et al. (2006) Rapid TNFR1-dependent lymphocyte depletion in vivo with a selective chemical inhibitor of IKKbeta. Blood 107: 4266-4273. (Pubitemid 43801350)
31. Grossmann M, Metcalf D, Merryfull J, Beg A, Baltimore D, et al. (1999) The combined absence of the transcription factors Rel and RelA leads to multiple hemopoietic cell defects. Proc Natl Acad Sci U S A 96: 11848-11853. (Pubitemid 29502821)
32. Senftleben U, Li ZW, Baud V, Karin M (2001) IKKbeta is essential for protecting T cells from TNFalpha-induced apoptosis. Immunity 14: 217-230. (Pubitemid 32289287)
33. Sakamoto K, Maeda S, Hikiba Y, Nakagawa H, Hayakawa Y, et al. (2009) Constitutive NF-kappaB activation in colorectal carcinoma plays a key role in angiogenesis, promoting tumor growth. Clin Cancer Res 15: 2248-2258.
34. Karin M, Ben-Neriah Y (2000) Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol 18: 621-663. (Pubitemid 30365393)
35. Dinh HK, Zhao B, Schuschereba ST, Merrill G, Bowman PD (2001) Gene expression profiling of the response to thermal injury in human cells. Physiol Genomics 7: 3-13.
36. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9: 669-676. (Pubitemid 36749215)
37. Penn JS, Madan A, Caldwell RB, Bartoli M, Caldwell RW, et al. (2008) Vascular endothelial growth factor in eye disease. Prog Retin Eye Res 27: 331-371.
38. Kliffen M, Sharma HS, Mooy CM, Kerkvliet S, de Jong PT (1997) Increased expression of angiogenic growth factors in age-related maculopathy. Br J Ophthalmol 81: 154-162. (Pubitemid 27092496)
39. Lopez PF, Sippy BD, Lambert HM, Thach AB, Hinton DR (1996) Transdifferentiated retinal pigment epithelial cells are immunoreactive for vascular endothelial growth factor in surgically excised age-related macular degeneration-related choroidal neovascular membranes. Invest Ophthalmol Vis Sci 37: 855-868.
40. Aiello LP, Avery RL, Arrigg PG, Keyt BA, Jampel HD, et al. (1994) Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 331: 1480-1487. (Pubitemid 24356306)
41. Adamis AP, Shima DT, Yeo KT, Yeo TK, Brown LF, et al. (1993) Synthesis and secretion of vascular permeability factor/vascular endothelial growth factor by human retinal pigment epithelial cells. Biochem Biophys Res Commun 193: 631-638. (Pubitemid 23214274)
42. Ryuto M, Ono M, Izumi H, Yoshida S, Weich HA, et al. (1996) Induction of vascular endothelial growth factor by tumor necrosis factor alpha in human glioma cells. Possible roles of SP-1. J Biol Chem 271: 28220-28228. (Pubitemid 26374633)
43. Shono T, Ono M, Izumi H, Jimi SI, Matsushima K, et al. (1996) Involvement of the transcription factor NF-kappaB in tubular morphogenesis of human microvascular endothelial cells by oxidative stress. Mol Cell Biol 16: 4231-4239. (Pubitemid 26251224)
44. Yoshida S, Ono M, Shono T, Izumi H, Ishibashi T, et al. (1997) Involvement of interleukin-8, vascular endothelial growth factor, and basic fibroblast growth factor in tumor necrosis factor alpha-dependent angiogenesis. Mol Cell Biol 17: 4015-4023. (Pubitemid 27281877)
45. Levine L, Lucci JA, 3rd, Pazdrak B, Cheng JZ, Guo YS, et al. (2003) Bombesin stimulates nuclear factor kappa B activation and expression of proangiogenic factors in prostate cancer cells. Cancer Res 63: 3495-3502. (Pubitemid 36793027)
46. Yu HG, Yu LL, Yang Y, Luo HS, Yu JP, et al. (2003) Increased expression of RelA/nuclear factor-kappa B protein correlates with colorectal tumorigenesis. Oncology 65: 37-45. (Pubitemid 36829089)
47. Ono M (2008) Molecular links between tumor angiogenesis and inflammation: inflammatory stimuli of macrophages and cancer cells as targets for therapeutic strategy. Cancer Sci 99: 1501-1506.
48. Aggarwal BB, Shishodia S, Sandur SK, Pandey MK, Sethi G (2006) Inflammation and cancer: how hot is the link? Biochem Pharmacol 72: 1605-1621. (Pubitemid 44666739)
49. Shibata A, Nagaya T, Imai T, Funahashi H, Nakao A, et al. (2002) Inhibition of NF-kappaB activity decreases the VEGF mRNA expression in MDA-MB-231 breast cancer cells. Breast Cancer Res Treat 73: 237-243. (Pubitemid 34712997)
50. Ramanathan M, Pinhal-Enfield G, Hao I, Leibovich SJ (2007) Synergistic upregulation of vascular endothelial growth factor (VEGF) expression in macrophages by adenosine A2A receptor agonists and endotoxin involves transcriptional regulation via the hypoxia response element in the VEGF promoter. Mol Biol Cell 18: 14-23. (Pubitemid 46066706)
51. Schofield CJ, Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5: 343-354. (Pubitemid 38579472)
52. Rius J, Guma M, Schachtrup C, Akassoglou K, Zinkernagel AS, et al. (2008) NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 453: 807-811. (Pubitemid 351793778)
53. Koch AE, Halloran MM, Haskell CJ, Shah MR, Polverini PJ (1995) Angiogenesis mediated by soluble forms of E-selectin and vascular cell adhesion molecule-1. Nature 376: 517-519.
54. Taylor BS, de Vera ME, Ganster RW, Wang Q, Shapiro RA, et al. (1998) Multiple NF-kappaB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J Biol Chem 273: 15148-15156. (Pubitemid 28272813)
55. Stetler-Stevenson WG (1999) Matrix metalloproteinases in angiogenesis: a moving target for therapeutic intervention. J Clin Invest 103: 1237-1241.
56. Yasuda M, Shimizu S, Ohhinata K, Naito S, Tokuyama S, et al. (2002) Differential roles of ICAM-1 and E-selectin in polymorphonuclear leukocyte-induced angiogenesis. Am J Physiol Cell Physiol 282: C917-925. (Pubitemid 34663154)
57. Zhou A, Scoggin S, Gaynor RB, Williams NS (2003) Identification of NF-kappa B-regulated genes induced by TNFalpha utilizing expression profiling and RNA interference. Oncogene 22: 2054-2064. (Pubitemid 36523642)
58. Sainson RC, Johnston DA, Chu HC, Holderfield MT, Nakatsu MN, et al. (2008) TNF primes endothelial cells for angiogenic sprouting by inducing a tip cell phenotype. Blood 111: 4997-5007.
59. van Beijnum JR, Buurman WA, Griffioen AW (2008) Convergence and amplification of toll-like receptor (TLR) and receptor for advanced glycation end products (RAGE) signaling pathways via high mobility group B1 (HMGB1). Angiogenesis 11: 91-99.
60. Gupta SC, Sundaram C, Reuter S, Aggarwal BB (2010) Inhibiting NF-kappaB activation by small molecules as a therapeutic strategy. Biochim Biophys Acta 1799: 775-787.
61. Arkan MC, Greten FR (2011) IKK- and NF-kappaB-mediated functions in carcinogenesis. Curr Top Microbiol Immunol 349: 159-169.
62. Mankan AK, Canli O, Schwitalla S, Ziegler P, Tschopp J, et al. (2011) TNF-alpha-dependent loss of IKKbeta-deficient myeloid progenitors triggers a cytokine loop culminating in granulocytosis. Proc Natl Acad Sci U S A 108: 6567-6572.
63. Greten FR, Arkan MC, Bollrath J, Hsu LC, Goode J, et al. (2007) NF-kappaB is a negative regulator of IL-1beta secretion as revealed by genetic and pharmacological inhibition of IKKbeta. Cell 130: 918-931. (Pubitemid 47332565)
64. Wullaert A, Bonnet MC, Pasparakis M (2011) NF-kappaB in the regulation of epithelial homeostasis and inflammation. Cell Res 21: 146-158.
65. Yang P, McKay BS, Allen JB, Jaffe GJ (2004) Effect of NF-kappa B inhibition on TNF-alpha-induced apoptosis in human RPE cells. Invest Ophthalmol Vis Sci 45: 2438-2446. (Pubitemid 38902620)
66. Brown DM, Kaiser PK, Michels M, Soubrane G, Heier JS, et al. (2006) Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N Engl J Med 355: 1432-1444. (Pubitemid 44511558)
67. Rosenfeld PJ, Brown DM, Heier JS, Boyer DS, Kaiser PK, et al. (2006) Ranibizumab for neovascular age-related macular degeneration. N Engl J Med 355: 1419-1431. (Pubitemid 44511557)
68. Regillo CD, Brown DM, Abraham P, Yue H, Ianchulev T, et al. (2008) Randomized, double-masked, sham-controlled trial of ranibizumab for neovascular age-related macular degeneration: PIER Study year 1. Am J Ophthalmol 145: 239-248.
69. Ophthotech's Novel Anti-PDGF Combination Agent Fovista Demonstrated Superior Efficacy Over Lucentis Monotherapy in Large Controlled Wet AMD Trial. (2012) Princeton, NJ: BusinessWire; June 13.