Deciphering combinations of PI3K/AKT/mTOR pathway drugs augmenting anti-angiogenic efficacy in vivo

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Sasore, Temitope ^a   Kennedy, Breandán ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; 2 MORPHOLINO 8 PHENYLCHROMONE; DACTOLISIB; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAPAMYCIN; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; AFLIBERCEPT; CHROMONE DERIVATIVE; HYBRID PROTEIN; MONOCLONAL ANTIBODY; MORPHOLINE DERIVATIVE; RANIBIZUMAB; TARGET OF RAPAMYCIN KINASE; VASCULOTROPIN RECEPTOR;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL COUNT; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; COMBINATION CHEMOTHERAPY; COMPLEX FORMATION; CONTROLLED STUDY; DRUG SAFETY; EMBRYO; HUMAN; HUMAN CELL; IN VIVO STUDY; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ZEBRA FISH; ANIMAL; CELL LINE; CELL SURVIVAL; DRUG EFFECTS; METABOLISM;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; CELL LINE; CELL SURVIVAL; CHROMONES; HUMANS; MORPHOLINES; PHOSPHATIDYLINOSITOL 3-KINASE; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84929051901     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0105280     Document Type: Article

References (55)

1. Hoeben A, Landuyt B, Highley MS, Wildiers H, Van Oosterom AT, et al. (2004) Vascular endothelial growth factor and angiogenesis. Pharmacol Rev 56: 549-580. (Pubitemid 39658463)
2. Kilarski WW, Petersson L, Fuchs PF, Zielinski MS, Gerwins P (2012) An in vivo neovascularization assay for screening regulators of angiogenesis and assessing their effects on pre-existing vessels. Angiogenesis 15: 643-655.
3. Kim SY, Sadda S, Humayun MS, de Juan E, Jr., Melia BM, et al. (2002) Morphometric analysis of the macula in eyes with geographic atrophy due to age-related macular degeneration. Retina 22: 464-470. (Pubitemid 35025523)
4. Nowak JZ (2006) Age-related macular degeneration (AMD): pathogenesis and therapy. Pharmacol Rep 58: 353-363.
5. Frost and Sullivan (2011) U.S. Retinal Therapeutics Market. www.frost.com. Subscription Required.
6. Gao G, Ma J (2002) Tipping the balance for angiogenic disorders. Drug Discov Today 7: 171-172. (Pubitemid 34123290)
7. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9: 669-676. (Pubitemid 36749215)
8. Chen Y, Wiesmann C, Fuh G, Li B, Christinger HW, et al. (1999) Selection and analysis of an optimized anti-VEGF antibody: crystal structure of an affinity-matured Fab in complex with antigen. J Mol Biol 293: 865-881. (Pubitemid 29527672)
9. Lien S, Lowman HB (2008) Therapeutic anti-VEGF antibodies. Handb Exp Pharmacol: 131-150.
10. Holash J, Davis S, Papadopoulos N, Croll SD, Ho L, et al. (2002) VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc Natl Acad Sci U S A 99: 11393-11398. (Pubitemid 34920936)
11. Rosenfield PJ, Moshfeghi A, Puliafito C (2005) Optical coherence tomography findings after an intravitreal injection of bevacizumab (avastin) for neovascular age-related macular degeneration. Opthalmic Surg Lasers Imaging 36: 331-335. (Pubitemid 41073112)
12. Rosenfeld PJ, Brown DM, Heier JS, Boyer DS, Kaiser PK, et al. (2006) Ranibizumab for Neovascular Age-Related Macular Degeneration. New Eng J of Med 355: 1419-1431. (Pubitemid 44511557)
13. Short BG (2008) Safety evaluation of ocular drug delivery formulations: techniques and practical considerations. Toxicol Pathol 36: 49-62.
14. Georgopoulos M, Polak K, Prager F, Prunte C, Schmidt-Erfurth U (2009) Characteristics of severe intraocular inflammation following intravitreal injection of bevacizumab (Avastin). Br J Ophthalmol 93: 457-462.
15. Sampat KM, Garg SJ (2010) Complications of intravitreal injections. Curr Opin Ophthalmol 21: 178-183.
16. Cai J, Ahmad S, Jiang WG, Huang J, Kontos CD, et al. (2003) Activation of vascular endothelial growth factor receptor-1 sustains angiogenesis and Bcl-2 expression via the phosphatidylinositol 3-kinase pathway in endothelial cells. Diabetes 52: 2959-2968. (Pubitemid 37466866)
17. Alvarez Y, Astudillo O, Jensen L, Reynolds AL, Waghorne N, et al. (2009) Selective inhibition of retinal angiogenesis by targeting PI3 kinase. PLoS One 4: e7867.
18. Marone R, Cmiljanovic V, Giese B, Wymann MP (2008) Targeting phosphoinositide 3-kinase - Moving towards therapy. Biochim Biophys Acta 1784: 159-185.
19. Jiang BH, Zheng JZ, Aoki M, Vogt PK (2000) Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells. Proc Natl Acad Sci U S A 97: 1749-1753. (Pubitemid 30118514)
20. Vanhaesebroeck B, Waterfield MD (1999) Signaling by distinct classes of phosphoinositide 3-kinases. Exp Cell Res 253: 239-254.
21. Cantrell DA (2001) Phosphoinositide 3-kinase signalling pathways. J Cell Sci 114: 1439-1445.
22. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, et al. (2001) Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70: 535-602. (Pubitemid 32662219)
23. Engelman JA, Luo J, Cantley LC (2006) The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 7: 606-619. (Pubitemid 44100518)
24. Hudes G, Carducci M, Tomczak P, Dutcher J, Figlin R, et al. (2007) Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma. N Engl J Med 356: 2271-2281. (Pubitemid 46849157)
25. Motzer RJ, Escudier B, Oudard S, Hutson TE, Porta C, et al. (2010) Phase 3 trial of everolimus for metastatic renal cell carcinoma: final results and analysis of prognostic factors. Cancer 116: 4256-4265.
26. Yao JC, Shah MH, Ito T, Bohas CL, Wolin EM, et al. (2011) Everolimus for advanced pancreatic neuroendocrine tumors. N Engl J Med 364: 514-523.
27. Dalal M, Jacobs-El N, Nicholson B, Tuo J, Chew E, et al. (2013) Subconjunctival Palomid 529 in the treatment of neovascular age-related macular degeneration. Graefes Arch Clin Exp Ophthalmol 251: 2705-2709.
28. Krishnadev N, Forooghian F, Cukras C, Wong W, Saligan L, et al. (2011) Subconjunctival sirolimus in the treatment of diabetic macular edema. Graefes Arch Clin Exp Ophthalmol 249: 1627-1633.
29. Meyer FA, Yaron I, Yaron M (1990) Synergistic, additive, and antagonistic effects of interleukin-1 beta, tumor necrosis factor alpha, and gamma-interferon on prostaglandin E, hyaluronic acid, and collagenase production by cultured synovial fibroblasts. Arthritis Rheum 33: 1518-1525. (Pubitemid 20362095)
30. Chou TC (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58: 621-681.
31. Kidd KR, Weinstein BM (2003) Fishing for novel angiogenic therapies. Br J Pharmacol 140: 585-594. (Pubitemid 37390846)
32. Isogai S, Horiguchi M, Weinstein BM (2001) The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev Biol 230: 278-301. (Pubitemid 32171423)
33. Lawson ND, Weinstein BM (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248: 307-318. (Pubitemid 35002091)
34. Alvarez Y, Cederlund ML, Cottell DC, Bill BR, Ekker SC, et al. (2007) Genetic determinants of hyaloid and retinal vasculature in zebrafish. BMC Dev Biol 7: 114.
35. Marneros AG, Fan J, Yokoyama Y, Gerber HP, Ferrara N, et al. (2005) Vascular endothelial growth factor expression in the retinal pigment epithelium is essential for choriocapillaris development and visual function. Am J Pathol 167: 1451-1459. (Pubitemid 41541430)
36. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
37. Childs S, Chen J-N, Garrity DM, Fishman MC (2002) Patterning of angiogenesis in the zebrafish embryo. Development 129: 973-982. (Pubitemid 34874121)
38. Brockerhoff SE (2006) Measuring the optokinetic response of zebrafish larvae. Nat Protoc 1: 2448-2451.
39. Yin J, McLoughlin S, Jeffery IB, Glaviano A, Kennedy B, et al. (2010) Integrating multiple genome annotation databases improves the interpretation of microarray gene expression data. BMC Genomics 11: 50.
40. Roulin D, Waselle L, Dormond-Meuwly A, Dufour M, Demartines N, et al. (2011) Targeting renal cell carcinoma with NVP-BEZ235, a dual PI3K/mTOR inhibitor, in combination with sorafenib. Mol Cancer 10: 90.
41. Grabinski N, Ewald F, Hofmann BT, Staufer K, Schumacher U, et al. (2012) Combined targeting of AKT and mTOR synergistically inhibits proliferation of hepatocellular carcinoma cells. Mol Cancer 11: 85.
42. Lang I, Brodowicz T, Ryvo L, Kahan Z, Greil R, et al. (2013) Bevacizumab plus paclitaxel versus bevacizumab plus capecitabine as first-line treatment for HER2-negative metastatic breast cancer: interim efficacy results of the randomised, open-label, non-inferiority, phase 3 TURANDOT trial. Lancet Oncol 14: 125-133.
43. Mazzoletti M, Bortolin F, Brunelli L, Pastorelli R, Di Giandomenico S, et al. (2011) Combination of PI3K/mTOR inhibitors: antitumor activity and molecular correlates. Cancer Res 71: 4573-4584.
44. Graupera M, Guillermet-Guibert J, Foukas LC, Phng L-K, Cain RJ, et al. (2008) Angiogenesis selectively requires the p110[agr] isoform of PI3K to control endothelial cell migration. Nature 453: 662-666. (Pubitemid 351769296)
45. Raynaud FI, Eccles SA, Patel S, Alix S, Box G, et al. (2009) Biological properties of potent inhibitors of class I phosphatidylinositide 3-kinases: from PI-103 through PI-540, PI-620 to the oral agent GDC-0941. Mol Cancer Ther 8: 1725-1738.
46. Toledo LI, Murga M, Zur R, Soria R, Rodriguez A, et al. (2011) A cell-based screen identifies ATR inhibitors with synthetic lethal properties for cancer-associated mutations. Nat Struct Mol Biol 18: 721-727.
47. Werzowa J, Koehrer S, Strommer S, Cejka D, Fuereder T, et al. (2011) Vertical inhibition of the mTORC1/mTORC2/PI3K pathway shows synergistic effects against melanoma in vitro and in vivo. J Invest Dermatol 131: 495-503.
48. Bowles DW, Diamond JR, Lam ET, Weekes CD, Astling DP, et al. (2014) Phase I study of oral rigosertib (ON 01910.Na), a dual inhibitor of the PI3K and Plk1 pathways, in adult patients with advanced solid malignancies. Clin Cancer Res 20: 1656-1665.
49. Shimizu T, Tolcher AW, Papadopoulos KP, Beeram M, Rasco DW, et al. (2012) The clinical effect of the dual-targeting strategy involving PI3K/AKT/mTOR and RAS/MEK/ERK pathways in patients with advanced cancer. Clin Cancer Res 18: 2316-2325.
50. Stevens CB, Adamson S, Stenkamp D (2012) Retinal Abnormalities in a Zebrafish Mutant Lacking Retinal and Hyaloid Vasculature. Invest Ophthalmol Vis Sci: ARVO E-Abstract 3960.
51. Dhakal S, Stevens CB, Weiss O, Inbal A, Stenkamp D (2013) Role of the early ocular vasculature in regulation of retinal neurogenesis. Invest Ophthalmol Vis Sci: ARVO E-Abstract 5145.
52. Yu WZ, Zou H, Li XX, Yan Z, Dong JQ (2008) Effects of the phosphatidylinositol 3-kinase inhibitor in a mouse model of retinal neovascularization. Ophthalmic Res 40: 19-25. (Pubitemid 350308299)
53. Dejneka NS, Kuroki AM, Fosnot J, Tang W, Tolentino MJ, et al. (2004) Systemic rapamycin inhibits retinal and choroidal neovascularization in mice. Mol Vis 10: 964-972. (Pubitemid 41358195)
54. Strauss O (2005) The retinal pigment epithelium in visual function. Physiol Rev 85: 845-881.
55. Zhao S, Overbeek PA (2001) Regulation of choroid development by the retinal pigment epithelium. Mol Vis 7: 277-282. (Pubitemid 36153682)