Peroxisome proliferator-activated receptor-β/delta; regulates angiogenic cell behaviors and oxygen-induced retinopathy

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 5, 2013, Pages 4197-4207

  Capozzi, Megan E ^a   McCollum, Gary W ^a   Savage, Sara R ^a   Penn, John S ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Nuclear transcription factor; Peroxisome proliferator activated receptor; Retinopathy of prematurity; Vascular endothelial growth factor

Indexed keywords

3 [(4 ANILINO 2 METHOXYPHENYL) SULFAMOYL] 2 THENOIC ACID METHYL ESTER; 3 [(4 ANILINO 2 METHOXYPHENYL)SULFAMOYL] 2 THENOIC ACID METHYL ESTER; [4 [2 (3 FLUORO 4 TRIFLUOROMETHYLPHENYL) 4 METHYL 5 THIAZOLYLMETHYLTHIO] 2 METHYLPHENOXY] ACETIC ACID; [4 [2 (3 FLUORO 4 TRIFLUOROMETHYLPHENYL) 4 METHYL 5 THIAZOLYLMETHYLTHIO] 2 METHYLPHENOXY]ACETIC ACID; ANGIOPOIETIN RECEPTOR; MESSENGER RNA; MOXIFLOXACIN; OXYGEN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROXYMETACAINE; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RETINA NEOVASCULARIZATION; RETINOPATHY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANGIOGENESIS; NUCLEAR TRANSCRIPTION FACTOR; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; RETINOPATHY OF PREMATURITY; VASCULAR ENDOTHELIAL GROWTH FACTOR;

ANGIOGENESIS INHIBITORS; ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HUMANS; OXYGEN; PPAR DELTA; PPAR-BETA; RATS; RETINAL DISEASES; RETINAL NEOVASCULARIZATION; RETINAL VESSELS; SULFONES; THIAZOLES; THIOPHENES;

EID: 84879261778     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-11608     Document Type: Article

References (74)

1. Klagsbrun M. Regulators of angiogenesis: stimulators, inhibitors, and extracellular matrix. J Cell Biochem. 1991;47:199-200.
2. Folkman J, Shing Y. Angiogenesis. J Biol Chem. 1992;267: 10931-10934.
3. Folkman J, D'Amore PA. Blood vessel formation: what is its molecular basis? Cell. 1996;87:1153-1155.
4. Risau W. Mechanisms of angiogenesis. Nature. 1997;386:671-674.
5. Li J, Zhang YP, Kirsner RS. Angiogenesis in wound repair: angiogenic growth factors and the extracellular matrix. Microsc Res Tech. 2003;60:107-114.
6. Folkman J, Browder T, Palmblad J. Angiogenesis research: guidelines for translation to clinical application. Thromb Haemost. 2001;86:23-33.
7. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995;1:27-31.
8. Penn JS, Madan A, Caldwell RB, Bartoli M, Caldwell RW, Hartnett ME. Vascular endothelial growth factor in eye disease. Prog Retin Eye Res. 2008;27:331-371.
9. Bressler NM, Bressler SB. Preventative ophthalmology. Agerelated macular degeneration. Ophthalmology. 1995;102: 1206-1211.
10. Lee P, Wang CC, Adamis AP. Ocular neovascularization: an epidemiologic review. Surv Ophthalmol. 1998;43:245-269.
11. Ashton N. Retinal vascularization in health and disease: Proctor Award Lecture of the Association for Research in Ophthalmology. Am J Ophthalmol. 1957;44:7-17.
12. Desvergne B, Wahli W. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr Rev. 1999; 20:649-688.
13. Tan NS, Michalik L, Desvergne B, Wahli W. Multiple expression control mechanisms of peroxisome proliferator-activated receptors and their target genes. J Steroid Biochem Mol Biol. 2005;93:99-105.
14. Bishop-Bailey D, Bystrom J. Emerging roles of peroxisome proliferator-activated receptor-beta/delta in inflammation. Pharmacol Ther. 2009;124:141-150.
15. Adhikary T, Kaddatz K, Finkernagel F, et al. Genomewide analyses define different modes of transcriptional regulation by peroxisome proliferator-activated receptor-beta/delta (PPARbeta/delta). PLoS One. 2011;6:e16344.
16. Desvergne B, Michalik L, Wahli W. Transcriptional regulation of metabolism. Physiol Rev. 2006;86:465-514.
17. Kilgore KS, Billin AN. PPARbeta/delta ligands as modulators of the inflammatory response. Curr Opin Investig Drugs. 2008; 9:463-469.
18. Peters JM, Gonzalez FJ. Sorting out the functional role(s) of peroxisome proliferator-activated receptor-beta/delta (PPAR-beta/delta) in cell proliferation and cancer. Biochim Biophys Acta. 2009;1796:230-241.
19. Grimaldi PA. Metabolic and nonmetabolic regulatory functions of peroxisome proliferator-activated receptor beta. Curr Opin Lipidol. 2010;21:186-191.
20. Muoio DM, Way JM, Tanner CJ, et al. Peroxisome proliferatoractivated receptor-alpha regulates fatty acid utilization in primary human skeletal muscle cells. Diabetes. 2002;51: 901-909.
21. Vidal-Puig AJ, Considine RV, Jimenez-Linan M, et al. Peroxisome proliferator-activated receptor gene expression in human tissues. Effects of obesity, weight loss, and regulation by insulin and glucocorticoids. J Clin Invest. 1997;99:2416-2422.
22. Shimaya A, Kurosaki E, Shioduka K, Nakano R, Shibasaki M, Shikama H. YM268 increases the glucose uptake, cell differentiation, and mRNA expression of glucose transporter in 3T3-L1 adipocytes. Horm Metab Res. 1998;30:543-548.
23. Bishop-Bailey D, Swales KE. The role of PPARs in the endothelium: implications for cancer therapy. PPAR Res. 2008;2008:904251.
24. Burdick AD, Kim DJ, Peraza MA, Gonzalez FJ, Peters JM. The role of peroxisome proliferator-activated receptor-beta/delta in epithelial cell growth and differentiation. Cell Signal. 2006; 18:9-20.
25. Peters JM, Hollingshead HE, Gonzalez FJ. Role of peroxisomeproliferator-activated receptor beta/delta (PPARbeta/delta) in gastrointestinal tract function and disease. Clin Sci (Lond). 2008;115:107-127.
26. Müller R, Körnhoff M, Peters JM, Müller-Brüsselbach S. A role for PPARβ/delta; in tumor stroma and tumorigenesis. PPAR Res. 2008;2008:534294.
27. Piqueras L, Reynolds AR, Hodivala-Dilke KM, et al. Activation of PPARbeta/delta induces endothelial cell proliferation and angiogenesis. Arterioscler Thromb Vasc Biol. 2007;27:63-69.
28. Müller-Brüsselbach S, Körnhoff M, Rieck M, et al. Deregulation of tumor angiogenesis and blockade of tumor growth in PPARbeta-deficient mice. EMBO J. 2007;26:3686-3698.
29. Penn JS, Tolman BL, Henry MM. Oxygen-induced retinopathy in the rat: relationship of retinal nonperfusion to subsequent neovascularization. Invest Ophthalmol Vis Sci. 1994;35:3429-3435.
30. Sznaidman ML, Haffner CD, Maloney PR, et al. Novel selective small molecule agonists for peroxisome proliferator-activated receptor delta (PPARdelta)-synthesis and biological activity. Bioorg Med Chem Lett. 2003;13:1517-1521.
31. Shearer BG, Steger DJ, Way JM, et al. Identification and characterization of a selective peroxisome proliferator-activated receptor beta/delta (NR1C2) antagonist. Mol Endocrinol. 2008;22:523-529.
32. Robciuc MR, Skrobuk P, Anisimov A, et al. Angiopoietin-like 4 mediates PPAR delta effect on lipoprotein lipase-dependent fatty acid uptake but not on beta-oxidation in myotubes. PLoS One. 2012;7:e46212.
33. Shirotani M, Yui Y, Hattori R, Kawai C. U-61431F, a stable prostacyclin analogue, inhibits the proliferation of bovine vascular smooth muscle cells with little antiproliferative effect on endothelial cells. Prostaglandins. 1991;41:97-110.
34. Stephen RL, Gustafsson MC, Jarvis M, et al. Activation of peroxisome proliferator-activated receptor delta stimulates the proliferation of human breast and prostate cancer cell lines. Cancer Res. 2004;64:3162-3170.
35. Bullard LE, Qi X, Penn JS. Role for extracellular signal responsive kinase-1 and -2 in retinal angiogenesis. Invest Ophthalmol Vis Sci. 2003;44:1722-1731.
36. Pal M, Tan MJ, Huang RL, et al. Angiopoietin-like 4 regulates epidermal differentiation. PLoS One. 2011;6:e25377.
37. Borland MG, Foreman JE, Girroir EE, et al. Ligand activation of peroxisome proliferator-activated receptor-beta/delta inhibits cell proliferation in human HaCaT keratinocytes. Mol Pharmacol. 2008;74:1429-1442.
38. Burdick AD, Bility MT, Girroir EE, et al. Ligand activation of peroxisome proliferator-activated receptor-beta/delta (PPAR-beta/delta) inhibits cell growth of human N/TERT-1 keratinocytes. Cell Signal. 2007;19:1163-1171.
39. Kim DJ, Bility MT, Billin AN, Willson TM, Gonzalez FJ, Peters JM. PPARbeta/delta selectively induces differentiation and inhibits cell proliferation. Cell Death Differ. 2006;13:53-60.
40. Auerbach R, Akhtar N, Lewis RL, Shinners BL. Angiogenesis assays: problems and pitfalls. Cancer Metastasis Rev. 2000;19: 167-172.
41. Gealekman O, Burkart A, Chouinard M, Nicoloro SM, Straubhaar J, Corvera S. Enhanced angiogenesis in obesity and in response to PPARgamma activators through adipocyte VEGF and ANGPTL4 production. Am J Physiol Endocrinol Metab. 2008;295:E1056-E1064.
42. Penn JS, Tolman BL, Lowery LA. Variable oxygen exposure causes preretinal neovascularization in the newborn rat. Invest Ophthalmol Vis Sci. 1993;34:576-585.
43. Penn JS, Henry MM, Wall PT, Tolman BL. The range of PaO2 variation determines the severity of oxygen-induced retinopathy in newborn rats. Invest Ophthalmol Vis Sci. 1995;36: 2063-2070.
44. Takata Y, Liu J, Yin F, et al. PPARdelta-mediated antiinflammatory mechanisms inhibit angiotensin II-accelerated atherosclerosis. Proc Natl Acad Sci U S A. 2008;105:4277-4282.
45. Quintela AM, Jimenez R, Gomez-Guzman M, et al. Activation of peroxisome proliferator-activated receptor-beta/-delta (PPAR beta/delta) prevents endothelial dysfunction in type 1 diabetic rats. Free Radic Biol Med. 2012;53:730-741.
46. Graham TL, Mookherjee C, Suckling KE, Palmer CN, Patel L. The PPARdelta agonist GW0742X reduces atherosclerosis in LDLR(-/-) mice. Atherosclerosis. 2005;181:29-37.
47. Gaudel C, Schwartz C, Giordano C, Abumrad NA, Grimaldi PA. Pharmacological activation of PPARbeta promotes rapid and calcineurin-dependent fiber remodeling and angiogenesis in mouse skeletal muscle. Am J Physiol Endocrinol Metab. 2008; 295:E297-E304.
48. Wagner N, Jehl-Pietri C, Lopez P, et al. Peroxisome proliferatoractivated receptor beta stimulation induces rapid cardiac growth and angiogenesis via direct activation of calcineurin. Cardiovasc Res. 2009;83:61-71.
49. Robbins SG, Conaway JR, Ford BL, Roberto KA, Penn JS. Detection of vascular endothelial growth factor (VEGF) protein in vascular and non-vascular cells of the normal and oxygen-injured rat retina. Growth Factors. 1997;14:229-241.
50. Sanchez-Siles AA, Ishimura N, Rumi MA, et al. Administration of PPARbeta/delta agonist reduces copper-induced liver damage in mice: possible implications in clinical practice. J Clin Biochem Nutr. 2011;49:42-49.
51. Perdiguero EG, Galaup A, Durand M, et al. Alteration of developmental and pathological retinal angiogenesis in angptl4-deficient mice. J Biol Chem. 2011;286:36841-36851.
52. Yokouchi H, Eto K, Nishimura W, et al. Angiopoietin-like protein 4 (ANGPTL4) is induced by high glucose in retinal pigment epithelial cells and exhibits potent angiogenic activity on retinal endothelial cells. [published online ahead of print February 7, 2013]. Acta Ophthalmol. doi:10.1111/aos.12097.
53. Peters JM, Shah YM, Gonzalez FJ. The role of peroxisome proliferator-activated receptors in carcinogenesis and chemoprevention. Nat Rev Cancer. 2012;12:181-195.
54. Di Paola R, Esposito E, Mazzon E, Paterniti I, Galuppo M, Cuzzocrea S. GW0742, a selective PPAR-beta/delta agonist, contributes to the resolution of inflammation after gut ischemia/reperfusion injury. J Leukoc Biol. 2010;88:291-301.
55. Tan NS, Michalik L, Noy N, et al. Critical roles of PPAR beta/delta in keratinocyte response to inflammation. Genes Dev. 2001;15:3263-3277.
56. Yang X, Kume S, Tanaka Y, et al. GW501516, a PPARdelta agonist, ameliorates tubulointerstitial inflammation in proteinuric kidney disease via inhibition of TAK1-NFkappaB pathway in mice. PLoS One. 2011;6:e25271.
57. Galuppo M, Di Paola R, Mazzon E, et al. GW0742, a high affinity PPAR-beta/delta agonist reduces lung inflammation induced by bleomycin instillation in mice. Int J Immunopathol Pharmacol. 2010;23:1033-1046.
58. Wang N. PPAR-delta in vascular pathophysiology. PPAR Res. 2008;2008:164163.
59. Wu KK. Peroxisome proliferator-activated receptors protect against apoptosis via 14-3-3. PPAR Res. 2010;2010:417646.
60. Hall MG, Quignodon L, Desvergne B. Peroxisome proliferator activated receptor beta/delta in the brain: facts and hypothesis. PPAR Res. 2008;2008:780452.
61. Benetti E, Patel NS, Collino M. The role of PPARbeta/delta in the management of metabolic syndrome and its associated cardiovascular complications. Endocr Metab Immune Disord Drug Targets. 2011;11:273-284.
62. Bonini-Filho MA, Jorge R, Barbosa JC, Calucci D, Cardillo JA, Costa RA. Intravitreal injection versus sub-Tenon's infusion of triamcinolone acetonide for refractory diabetic macular edema: a randomized clinical trial. Invest Ophthalmol Vis Sci. 2005;46:3845-3849.
63. Chieh JJ, Roth DB, Liu M, et al. Intravitreal triamcinolone acetonide for diabetic macular edema. Retina. 2005;25:828-834.
64. Jonas J, Heatley G, Spaide R, Varma R. Intravitreal triamcinolone acetonide and secondary ocular hypertension. J Glaucoma. 2005;14:168-171.
65. Jonas JB, Martus P, Degenring RF, Kreissig I, Akkoyun I. Predictive factors for visual acuity after intravitreal triamcinolone treatment for diabetic macular edema. Arch Ophthalmol. 2005;123:1338-1343.
66. Martidis A, Duker JS, Greenberg PB, et al. Intravitreal triamcinolone for refractory diabetic macular edema. Ophthalmology. 2002;109:920-927.
67. Massin P, Audren F, Haouchine B, et al. Intravitreal triamcinolone acetonide for diabetic diffuse macular edema: preliminary results of a prospective controlled trial. Ophthalmology. 2004;111:218-224; discussion 224-225.
68. Sutter FK, Simpson JM, Gillies MC. Intravitreal triamcinolone for diabetic macular edema that persists after laser treatment: three-month efficacy and safety results of a prospective, randomized, double-masked, placebo-controlled clinical trial. Ophthalmology. 2004;111:2044-2049.
69. Fintak DR, Shah GK, Blinder KJ, et al. Incidence of endophthalmitis related to intravitreal injection of bevacizumab and ranibizumab. Retina. 2008;28:1395-1399.
70. Jonas JB, Kamppeter BA, Harder B, Vossmerbaeumer U, Sauder G, Spandau UH. Intravitreal triamcinolone acetonide for diabetic macular edema: a prospective, randomized study. J Ocul Pharmacol Ther. 2006;22:200-207.
71. Moshfeghi DM, Kaiser PK, Bakri SJ, et al. Presumed sterile endophthalmitis following intravitreal triamcinolone acetonide injection. Ophthalmic Surg Lasers Imaging. 2005;36:24-29.
72. Moshfeghi DM, Kaiser PK, Scott IU, et al. Acute endophthalmitis following intravitreal triamcinolone acetonide injection. Am J Ophthalmol. 2003;136:791-796.
73. Sang DN, D'Amore PA. Is blockade of vascular endothelial growth factor beneficial for all types of diabetic retinopathy? Diabetologia. 2008;51:1570-1573.
74. Wirostko B, Wong TY, Simo R. Vascular endothelial growth factor and diabetic complications. Prog Retin Eye Res. 2008; 27:608-621.