Phenotype-based discovery of 2-[(E)-2-(Quinolin-2-yl)vinyl]phenol as a novel regulator of ocular angiogenesis

Journal of Biological Chemistry

Volumn 291, Issue 14, 2016, Pages 7242-7255

  Reynolds, Alison L ^a   Alvarez, Yolanda ^a   Sasore, Temitope ^a   Waghorne, Nora ^a   Butler, Clare T ^a   Kilty, Claire ^a   Smith, Andrew J ^a   Mcvicar, Carmel ^b   Wong, Vickie H Y ^b   Galvin, Orla ^a   Merrigan, Stephanie ^a   Osman, Janina ^c   Grebnev, Gleb ^a   Sjölander, Anita ^c   Stitt, Alan W ^b   Kennedy, Breandán N ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; EYE PROTECTION; OPHTHALMOLOGY; PHENOLS;

AGE-RELATED MACULAR DEGENERATION; ANGIOGENIC SPROUTING; DIABETIC RETINOPATHY; OXYGEN INDUCED RETINOPATHIES; PHYSIOLOGICAL ROLES; RECEPTOR ANTAGONISTS; RETINAL NEOVASCULARIZATION; THERAPEUTIC AGENTS;

CELL SIGNALING;

ANGIOGENESIS INHIBITOR; CYSTEINYL LEUKOTRIENE RECEPTOR 1; CYSTEINYL LEUKOTRIENE RECEPTOR 2; LEUKOTRIENE RECEPTOR; PHENOL DERIVATIVE; QUININIB; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; AORTIC RING (SLICE); ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG SCREENING; DRUG STRUCTURE; DRUG TOLERABILITY; EMBRYO; EX VIVO STUDY; HUMAN; HUMAN CELL; IC50; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RETINA BLOOD VESSEL; RETINA NEOVASCULARIZATION; RETINOPATHY; SIGNAL TRANSDUCTION; ZEBRA FISH; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CHEMISTRY; DIABETIC RETINOPATHY; DRUG DEVELOPMENT; DRUG EFFECTS; MACULAR DEGENERATION; METABOLISM; PATHOLOGY; RETINAL NEOVASCULARIZATION; TRANSGENIC ANIMAL;

ANGIOGENESIS INHIBITORS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL LINE; DIABETIC RETINOPATHY; DRUG DISCOVERY; HUMANS; MACULAR DEGENERATION; MICE; PHENOLS; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RETINAL NEOVASCULARIZATION; SIGNAL TRANSDUCTION; ZEBRAFISH;

EID: 84963979800     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.710665     Document Type: Article

References (69)

1. Fruttiger, M. (2007) Development of the retinal vasculature. Angiogenesis 10, 77-88.
2. Cheung, N., Mitchell, P., and Wong, T. Y. (2010) Diabetic retinopathy. Lancet 376, 124-136.
3. Jager, R. D., Mieler, W. F., and Miller, J. W. (2008) Age-related macular degeneration. N. Engl. J. Med. 358, 2606-2617.
4. Hellström, A., Smith, L. E., and Dammann, O. (2013) Retinopathy of prematurity. Lancet 382, 1445-1457.
5. Rehak, M., and Wiedemann, P. (2010) Retinal vein thrombosis: pathogenesis and management. J. Thromb. Haemost. 8, 1886-1894.
6. Gariano, R. F., and Gardner, T. W. (2005) Retinal angiogenesis in development and disease. Nature 438, 960-966.
7. Alvarez, Y., Astudillo, O., Jensen, L., Reynolds, A. L., Waghorne, N., Brazil, D. P., Cao, Y., O'Connor, J. J., and Kennedy, B. (2009) Selective inhibition of retinal angiogenesis by targeting PI3 kinase. PLoS ONE 4, e7867.
8. Kitambi, S. S., McCulloch, K. J., Peterson, R. T., and Malicki, J. J. (2009) Small molecule screen for compounds that affect vascular development in the zebrafish retina. Mech. Dev. 126, 464-477.
9. Folkman, J. (1997) in Regulation of Angiogenesis (Goldberg, I., and Rosen, E., eds.) pp. 1-8, Birkhäuser, Basel, Switzerland.
10. Frost & Sullivan (June 7, 2011) Analysis of the US Retinal Therapeutics Market: Improvements in Administration and Efficacy Drive Growth, Frost & Sullivan Report NC77-52.
11. Frost & Sullivan (July 3, 2010) European Ophthalmic Pharmaceuticals Market, Frost & Sullivan Report M4AC-52.
12. CATT Research Group, Martin, D. F., Maguire, M. G., Ying, G. S., Grunwald, J. E., Fine, S. L., and Jaffe, G. J. (2011) Ranibizumab and bevacizumab for neovascular age-related macular degeneration. N. Engl. J. Med. 364, 1897-1908.
13. Heier, J. S., Brown, D. M., Chong, V., Korobelnik, J.-F., Kaiser, P. K., Nguyen, Q. D., Kirchhof, B., Ho, A., Ogura, Y., Yancopoulos, G. D., Stahl, N., Vitti, R., Berliner, A. J., Soo, Y., Anderesi, M., Groetzbach, G., Sommerauer, B., Sandbrink, R., Simader, C., Schmidt-Erfurth, U., and VIEW 1 and VIEW 2 Study Groups. (2012) Intravitreal aflibercept (VEGF trapeye) in wet age-related macular degeneration. Ophthalmology 119, 2537-2548.
14. Rosenfeld, P. J., Brown, D. M., Heier, J. S., Boyer, D. S., Kaiser, P. K., Chung, C. Y., Kim, R. Y., and MARINA Study Group (2006) Ranibizumab for neovascular age-related macular degeneration. N. Engl. J. Med. 355, 1419-1431.
15. Rofagha, S., Bhisitkul, R. B., Boyer, D. S., Sadda, S. R., Zhang, K., and SEVEN-UP Study Group (2013) Seven-year outcomes in ranibizumabtreated patients in ANCHOR, MARINA, and HORIZON: A multicenter cohort study (SEVEN-UP). Ophthalmology 120, 2292-2299.
16. Diabetic Retinopathy Clinical Research Network, Elman, M. J., Qin, H., Aiello, L. P., Beck, R. W., Bressler, N. M., Ferris, F. L. 3rd, Glassman, A. R., Maturi, R. K., and Melia, M. (2012) Intravitreal ranibizumab for diabetic macular edema with prompt vs. deferred laser treatment: 3-year randomized trial results. Ophthalmology 119, 2312-2318.
17. Wangsa-Wirawan, N. D., and Linsenmeier, R. A. (2003) Retinal oxygen: fundamental and clinical aspects. Arch. Ophthalmol. 121, 547-557.
18. Saint-Geniez, M., and D'Amore, P. (2004) Development and pathology of the hyaloid, choroidal and retinal vasculature. Int. J. Dev. Biol. 48, 1045-1058.
19. Fruttiger, M. (2002) Development of the mouse retinal vasculature: Angiogenesis versus vasculogenesis. Invest. Ophthalmol. Vis. Sci. 43, 522-527.
20. Shastry, B. S. (2009) Persistent hyperplastic primary vitreous: congenital malformation of the eye. Clin. Exp. Ophthalmol. 37, 884-890.
21. Alvarez, Y., Cederlund, M. L., Cottell, D. C., Bill, B. R., Ekker, S. C., Torres- Vazquez, J., Weinstein, B. M., Hyde, D. R., Vihtelic, T. S., and Kennedy, B. N. (2007) Genetic determinants of hyaloid and retinal vasculature in zebrafish. BMC Dev. Biol. 7, 114.
22. Hartsock, A., Lee, C., Arnold, V., and Gross, J. M. (2014) In vivo analysis of hyaloid vasculature morphogenesis in zebrafish: A role for the lens in maturation and maintenance of the hyaloid. Dev. Biol. 394, 327-339.
23. Kalén, M., Wallgard, E., Asker, N., Nasevicius, A., Athley, E., Billgren, E., Larson, J. D., Wadman, S. A., Norseng, E., Clark, K. J., He, L., Karlsson- Lindahl, L., Häger, A.-K., Weber, H., Augustin, H., Samuelsson, T., Kemmet, C. K., Utesch, C. M., Essner, J. J., Hackett, P. B., and Hellström, M. (2009) Combination of reverse and chemical genetic screens reveals angiogenesis inhibitors and targets. Chem. Biol. 16, 432-441.
24. Peterson, R. T., Link, B. A., Dowling, J. E., and Schreiber, S. L. (2000) Small molecule developmental screens reveal the logic and timing of vertebrate development. Proc. Natl. Acad. Sci. U.S.A. 97, 12965-12969.
25. Rennekamp, A. J., and Peterson, R. T. (2015) 15 years of zebrafish chemical screening. Curr. Opin. Chem. Biol. 24, 58-70.
26. Kanaoka, Y., Maekawa, A., and Austen, K. F. (2013) Identification of GPR99 protein as a potential third cysteinyl leukotriene receptor with a preference for leukotriene E4 ligand. J. Biol. Chem. 288, 10967-10972.
27. Singh, R. K., Gupta, S., Dastidar, S., and Ray, A. (2010) Cysteinyl leukotrienes and their receptors: molecular and functional characteristics. Pharmacology 85, 336-349.
28. Kanaoka, Y., and Boyce, J. A. (2004) Cysteinyl leukotrienes and their receptors: cellular distribution and function in immune and inflammatory responses. J. Immunol. 173, 1503-1510.
29. Bäck, M., Powell, W. S., Dahlén, S. E., Drazen, J. M., Evans, J. F., Serhan, C. N., Shimizu, T., Yokomizo, T., and Rovati, G. E. (2014) Update on leukotriene, lipoxin and oxoeicosanoid receptors: IUPHAR Review 7. Br. J. Pharmacol. 171, 3551-3574.
30. Ciana, P., Fumagalli, M., Trincavelli, M. L., Verderio, C., Rosa, P., Lecca, D., Ferrario, S., Parravicini, C., Capra, V., Gelosa, P., Guerrini, U., Belcredito, S., Cimino, M., Sironi, L., Tremoli, E., Rovati, G. E., Martini, C., and Abbracchio, M. P. (2006) The orphan receptor GPR17 identified as a new dual uracil nucleotides/cysteinyl-leukotrienes receptor. EMBO J. 25, 4615-4627.
31. Meltzer, E. O., Malmstrom, K., Lu, S., Prenner, B. M., Wei, L. X., Weinstein, S. F., Wolfe, J. D., and Reiss, T. F. (2000) Concomitant montelukast and loratadine as treatment for seasonal allergic rhinitis: A randomized, placebo-controlled clinical trial. J. Allergy Clin. Immunol. 105, 917-922.
32. Reiss, T. F., Altman, L. C., Chervinsky, P., Bewtra, A., Stricker, W. E., Noonan, G. P., Kundu, S., and Zhang, J. (1996) Effects of montelukast (MK-0476), a new potent cysteinyl leukotriene (LTD4) receptor antagonist, in patients with chronic asthma. J. Allergy Clin. Immunol. 98, 528-534.
33. Kyritsis, N., Kizil, C., Zocher, S., Kroehne, V., Kaslin, J., Freudenreich, D., Iltzsche, A., and Brand, M. (2012) Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 338, 1353-1356.
34. Qian, X.-D., Wei, E.-Q., Zhang, L., Sheng, W.-W., Wang, M.-L., Zhang, W.-P., and Chen, Z. (2006) Pranlukast, a cysteinyl leukotriene receptor 1 antagonist, protects mice against brain cold injury. Eur. J. Pharmacol. 549, 35-40.
35. Wang, X. Y., Tang, S. S., Hu, M., Long, Y., Li, Y. Q., Liao, M. X., Ji, H., and Hong, H. (2013) Leukotriene D4 induces amyloid-β generation via CysLT1R-mediated NF-κ-B pathways in primary neurons. Neurochem. Int. 62, 340-347.
36. Kanaoka, Y., and Boyce, J. A. (2014) Cysteinyl leukotrienes and their receptors: emerging concepts. Allergy Asthma Immunol. Res. 6, 288-295.
37. Barajas-Espinosa, A., Ni, N. C., Yan, D., Zarini, S., Murphy, R. C., and Funk, C. D. (2012) The cysteinyl leukotriene 2 receptor mediates retinal edema and pathological neovascularization in a murine model of oxygeninduced retinopathy. FASEB J. 26, 1100-1109.
38. Duah, E., Adapala, R. K., Al-Azzam, N., Kondeti, V., Gombedza, F., Thodeti, C. K., and Paruchuri, S. (2013) Cysteinyl leukotrienes regulate endothelial cell inflammatory and proliferative signals through CysLT(2) and CysLT(1) receptors. Sci. Rep. 3, 3274.
39. Jiang, Y., Borrelli, L. A., Kanaoka, Y., Bacskai, B. J., and Boyce, J. A. (2007) CysLT(2) receptors interact with CysLT(1) receptors and down-modulate cysteinyl leukotriene-dependent mitogenic responses of mast cells. Blood 110, 3263-3270.
40. Lipinski, C., Lombardo, F., Dominy, B., and Feeney, P. (2001) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev. 23, 3-26.
41. Lawson, N. D., and Weinstein, B. M. (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318.
42. Brockerhoff, S. (2006) Measuring the optokinetic response of zebrafish larvae. Nat. Protoc. 1, 2448-2451.
43. Sasore, T., and Kennedy, B. (2014) Deciphering combinations of PI3K/AKT/mTOR pathway drugs augmenting anti-angiogenic efficacy in vivo. Plos One 9, e105280.
44. Baker, M., Robinson, S. D., Lechertier, T., Barber, P. R., Tavora, B., D'Amico, G., Jones, D. T., Vojnovic, B., and Hodivala-Dilke, K. (2012) Use of the mouse aortic ring assay to study angiogenesis. Nat. Protoc. 7, 89-104.
45. Connor, K. M., Krah, N. M., Dennison, R. J., Aderman, C. M., Chen, J., Guerin, K. I., Sapieha, P., Stahl, A., Willett, K. L., and Smith, L. E. (2009) Quantification of oxygen-induced retinopathy in the mouse: A model of vessel loss, vessel regrowth and pathological angiogenesis. Nat. Protoc. 4, 1565-1573.
46. Smith, L. E., Wesolowski, E., McLellan, A., Kostyk, S. K., D'Amato, R., Sullivan, R., and D'Amore, P. A. (1994) Oxygen-induced retinopathy in the mouse. Invest. Ophthalmol. Vis. Sci. 35, 101-111.
47. Gardiner, T. A., Gibson, D. S., de Gooyer, T. E., de la Cruz, V. F., McDonald, D. M., and Stitt, A. W. (2005) Inhibition of tumor necrosis factor-α improves physiological angiogenesis and reduces pathological neovascularization in ischemic retinopathy. Am. J. Pathol. 166, 637-644.
48. Sidman, R. L., Li, J., Lawrence, M., Hu, W., Musso, G. F., Giordano, R. J., Cardó-Vila, M., Pasqualini, R., and Arap, W. (2015) The peptidomimetic Vasotide targets two retinal VEGF receptors and reduces pathological angiogenesis in murine and nonhuman primate models of retinal disease. Sci. Transl. Med. 7, 309ra165-309ra165.
49. Gagnidze, K., Sachchidanand, Rozenfeld, R., Mezei, M., Zhou, M.-M., and Devi, L. A. (2008) Homology modeling and site-directed mutagenesis to identify selective inhibitors of endothelin-converting enzyme-2. J. Med. Chem. 51, 3378-3387.
50. Gupta, A., Gomes, I., Wardman, J., and Devi, L. A. (2014) Opioid receptor function is regulated by post-endocytic peptide processing. J. Biol. Chem. 289, 19613-19626.
51. Zamboni, R., Belley, M., Champion, E., Charette, L., DeHaven, R., Frenette, R., Gauthier, J. Y., Jones, T. R., Leger, S., and Masson, P. (1992) Development of a novel series of styrylquinoline compounds as high-affinity leukotriene D4 receptor antagonists: synthetic and structure-activity studies leading to the discovery of (+-)-3-[[[3-[2-(7-chloro-2-quinolinyl)-(E)-ethenyl]phenyl][[3- (dimethylamino)-3-oxopropyl]thio]methyl]thio]propionic acid. J. Med. Chem. 35, 3832-3844.
52. Lorusso, P. M., Boerner, S. A., and Hunsberger, S. (2011) Clinical development of vascular disrupting agents: what lessons can we learn from ASA404? J. Clin. Oncol. 29, 2952-2955.
53. Dhakal, S., Stevens, C., Weiss, O., Inbal, A., and Stenkamp, D. (2013) Role of the early ocular vasculature in regulation of retinal neurogenesis. Invest. Ophthalmol. Vis. Sci. 54, Abstr. 5145.
54. Dhakal, S., Stevens, C. B., Sebbagh, M., Weiss, O., Frey, R. A., Adamson, S., Shelden, E. A., Inbal, A., and Stenkamp, D. L. (2015) Abnormal retinal development in Cloche mutant zebrafish. Dev. Dyn. 244, 1439-1455.
55. Stahl, A., Connor, K. M., Sapieha, P., Chen, J., Dennison, R. J., Krah, N. M., Seaward, M. R., Willett, K. L., Aderman, C. M., Guerin, K. I., Hua, J., Löfqvist, C., Hellström, A., and Smith, L. E. (2010) The mouse retina as an angiogenesis model. Invest. Ophthalmol. Vis. Sci. 51, 2813-2826.
56. Marschallinger, J., Schaffner, I., Klein, B., Gelfert, R., Rivera, F. J., Illes, S., Grassner, L., Janssen, M., Rotheneichner, P., Schmuckermair, C., Coras, R., Boccazzi, M., Chishty, M., Lagler, F. B., Renic, M., Bauer, H.-C., Singewald, N., Blumcke, I., Bogdahn, U., Couillard-Despres, S., Lie, D. C., Abbracchio, M. P., and Aigner, L. (2015) Structural and functional rejuvenation of the aged brain by an approved anti-asthmatic drug. Nat. Commun. 6, 8466.
57. Maekawa, A., Kanaoka, Y., Xing, W., and Austen, K. F. (2008) Functional recognition of a distinct receptor preferential for leukotriene E(4) in mice lacking the cysteinyl leukotriene 1 and 2 receptors. Proc. Natl. Acad. Sci. U.S.A. 105, 16695-16700.
58. Reynolds, A. L., Kent, D., and Kennedy, B. N. (2014) Ocular neovascularisation: current and emerging therapies. Adv. Exp. Med. Biol. 801, 797-804.
59. Tsopanoglou, N. E., Pipili-Synetos, E., and Maragoudakis, M. E. (1994) Leukotrienes C4 and D4 promote angiogenesis via a receptor-mediated interaction. Eur. J. Pharmacol. 258, 151-154.
60. Kanayasu, T., Nakao-Hayashi, J., Asuwa, N., Morita, I., Ishii, T., Ito, H., and Murota, S. (1989) Leukotriene C4 stimulates angiogenesis in bovine carotid artery endothelial cells in vitro. Biochem. Biophys. Res. Commun. 159, 572-578.
61. Yuan, Y.-M., Fang, S.-H., Qian, X.-D., Liu, L.-Y., Xu, L.-H., Shi, W.-Z., Zhang, L.-H., Lu, Y.-B., Zhang, W.-P., and Wei, E.-Q. (2009) Leukotriene D4 stimulates the migration but not proliferation of endothelial cells mediated by the cysteinyl leukotriene CysLT1 receptor via the extracellular signal-regulated kinase pathway. J. Pharmacol. Sci. 109, 285-292.
62. Xu, L., Zhang, L., Liu, L., Fang, S., Lu, Y., Wei, E., and Zhang, W. (2010) Involvement of cysteinyl leukotriene receptors in angiogenesis in rat thoracic aortic rings. Pharmazie 65, 750-754.
63. Savari, S., Liu, M., Zhang, Y., Sime, W., and Sjölander, A. (2013) CysLT1R antagonists inhibit tumor growth in a xenograft model of colon cancer. PLoS ONE 8, e73466.
64. Balantic, M., Rijavec, M., Skerbinjek Kavalar, M., Suskovic, S., Silar, M., Kosnik, M., and Korosec, P. (2012) Asthma treatment outcome in children is associated with vascular endothelial growth factor A (VEGFA) polymorphisms. Mol. Diagn. Ther. 16, 173-180.
65. Lee, K. S., Kim, S. R., Park, H. S., Jin, G. Y., and Lee, Y. C. (2004) Cysteinyl leukotriene receptor antagonist regulates vascular permeability by reducing vascular endothelial growth factor expression. J. Allergy Clin. Immunol. 114, 1093-1099.
66. Smith, G. A., Rawls, C. M., and Kunka, R. L. (2004) An automated method for the determination of montelukast in human plasma using dual-column HPLC analysis and peak height summation of the parent compound and its photodegradation product. Pharm. Res. 21, 1539-1544.
67. Kim, M. H., Lee, Y. J., Kim, M. O., Kim, J. S., and Han, H. J. (2010) Effect of leukotriene D4 on mouse embryonic stem cell migration and proliferation: involvement of PI3K/Akt as well as GSK-3-/-catenin signaling pathways. J. Cell Biochem. 111, 686-698.
68. Salim, T., Sand-Dejmek, J., and Sjölander, A. (2014) The inflammatory mediator leukotriene D4 induces subcellular -βcatenin translocation and migration of colon cancer cells. Exp. Cell Res. 321, 255-266.
69. Savari, S., Vinnakota, K., Zhang, Y., and Sjölander, A. (2014) Cysteinyl leukotrienes and their receptors: bridging inflammation and colorectal cancer. World J. Gastroenterol. 20, 968-977.