ER stress and angiogenesis

Cell Metabolism

Volumn 22, Issue 4, 2015, Pages 560-575

  Binet, François ^a   Sapieha, Przemyslaw ^a,b  

^a UNIVERSITY OF MONTREAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; PROTEIN IRE1; PROTEIN IRE1ALPHA; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG; VASCULOTROPIN; ERN1 PROTEIN, HUMAN; RIBONUCLEASE; VASCULOTROPIN A;

ANGIOGENESIS; APOPTOSIS; ATHEROSCLEROSIS; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; HUMAN; MAMMAL CELL; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROLIFERATIVE RETINOPATHY; RETINOPATHY; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; VASCULAR DISEASE; VASCULARIZATION; ANIMAL; ENDOPLASMIC RETICULUM; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY;

ANIMALS; ATHEROSCLEROSIS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84943449172     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2015.07.010     Document Type: Review

References (164)

1. A.P. Adamis, and A.J. Berman Immunological mechanisms in the pathogenesis of diabetic retinopathy Semin. Immunopathol. 30 2008 65 84
2. T. Afonyushkin, O.V. Oskolkova, M. Philippova, T.J. Resink, P. Erne, B.R. Binder, and V.N. Bochkov Oxidized phospholipids regulate expression of ATF4 and VEGF in endothelial cells via NRF2-dependent mechanism: novel point of convergence between electrophilic and unfolded protein stress pathways Arterioscler. Thromb. Vasc. Biol. 30 2010 1007 1013
3. D.A. Antonetti, R. Klein, and T.W. Gardner Diabetic retinopathy N. Engl. J. Med. 366 2012 1227 1239
4. C. Atkins, Q. Liu, E. Minthorn, S.Y. Zhang, D.J. Figueroa, K. Moss, T.B. Stanley, B. Sanders, A. Goetz, N. Gaul, and et al. Characterization of a novel PERK kinase inhibitor with antitumor and antiangiogenic activity Cancer Res. 73 2013 1993 2002
5. G. Auf, A. Jabouille, S. Guérit, R. Pineau, M. Delugin, M. Bouchecareilh, N. Magnin, A. Favereaux, M. Maitre, T. Gaiser, and et al. Inositol-requiring enzyme 1alpha is a key regulator of angiogenesis and invasion in malignant glioma Proc. Natl. Acad. Sci. USA 107 2010 15553 15558
6. J.M. Axten, S.P. Romeril, A. Shu, J. Ralph, J.R. Medina, Y. Feng, W.H. Li, S.W. Grant, D.A. Heerding, E. Minthorn, and et al. Discovery of GSK2656157: an optimized PERK inhibitor selected for preclinical development ACS Med. Chem. Lett. 4 2013 964 968
7. R. Benedito, S.F. Rocha, M. Woeste, M. Zamykal, F. Radtke, O. Casanovas, A. Duarte, B. Pytowski, and R.H. Adams Notch-dependent VEGFR3 upregulation allows angiogenesis without VEGF-VEGFR2 signalling Nature 484 2012 110 114
8. A. Bertolotti, Y. Zhang, L.M. Hendershot, H.P. Harding, and D. Ron Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response Nat. Cell Biol. 2 2000 326 332
9. F. Binet, G. Mawambo, N. Sitaras, N. Tetreault, E. Lapalme, S. Favret, A. Cerani, D. Leboeuf, S. Tremblay, F. Rezende, and et al. Neuronal ER stress impedes myeloid-cell-induced vascular regeneration through IRE1α degradation of netrin-1 Cell Metab. 17 2013 353 371
10. J.D. Blais, C.L. Addison, R. Edge, T. Falls, H. Zhao, K. Wary, C. Koumenis, H.P. Harding, D. Ron, M. Holcik, and J.C. Bell Perk-dependent translational regulation promotes tumor cell adaptation and angiogenesis in response to hypoxic stress Mol. Cell. Biol. 26 2006 9517 9532
11. M. Brownlee, H. Vlassara, and A. Cerami Nonenzymatic glycosylation and the pathogenesis of diabetic complications Ann. Intern. Med. 101 1984 527 537
12. S.S. Cao, and R.J. Kaufman Targeting endoplasmic reticulum stress in metabolic disease Expert Opin. Ther. Targets 17 2013 437 448
13. P. Carmeliet Cardiovascular biology. Creating unique blood vessels Nature 412 2001 868 869
14. P. Carmeliet, and R.K. Jain Molecular mechanisms and clinical applications of angiogenesis Nature 473 2011 298 307
15. S.T. Carmichael Cellular and molecular mechanisms of neural repair after stroke: making waves Ann. Neurol. 59 2006 735 742
16. S.T. Carmichael, I. Archibeque, L. Luke, T. Nolan, J. Momiy, and S. Li Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex Exp. Neurol. 193 2005 291 311
17. A. Cerani, N. Tetreault, C. Menard, E. Lapalme, C. Patel, N. Sitaras, F. Beaudoin, D. Leboeuf, V. De Guire, F. Binet, and et al. Neuron-derived semaphorin 3A is an early inducer of vascular permeability in diabetic retinopathy via neuropilin-1 Cell Metab. 18 2013 505 518
18. J. Chen, and L.E. Smith Retinopathy of prematurity Angiogenesis 10 2007 133 140
19. X. Chen, D. Iliopoulos, Q. Zhang, Q. Tang, M.B. Greenblatt, M. Hatziapostolou, E. Lim, W.L. Tam, M. Ni, Y. Chen, and et al. XBP1 promotes triple-negative breast cancer by controlling the HIF1α pathway Nature 508 2014 103 107
20. N. Cheung, and T.Y. Wong Diabetic retinopathy and systemic vascular complications Prog. Retin. Eye Res. 27 2008 161 176
21. M. Civelek, E. Manduchi, R.J. Riley, C.J. Stoeckert Jr., and P.F. Davies Chronic endoplasmic reticulum stress activates unfolded protein response in arterial endothelium in regions of susceptibility to atherosclerosis Circ. Res. 105 2009 453 461
22. K.M. Connor, N.M. Krah, R.J. Dennison, C.M. Aderman, J. Chen, K.I. Guerin, P. Sapieha, A. Stahl, K.L. Willett, and L.E.H. Smith Quantification of oxygen-induced retinopathy in the mouse: a model of vessel loss, vessel regrowth and pathological angiogenesis Nat. Protoc. 4 2009 1565 1573
23. C. Coulon, M. Georgiadou, C. Roncal, K. De Bock, T. Langenberg, and P. Carmeliet From vessel sprouting to normalization: role of the prolyl hydroxylase domain protein/hypoxia-inducible factor oxygen-sensing machinery Arterioscler. Thromb. Vasc. Biol. 30 2010 2331 2336
24. S.B. Cullinan, D. Zhang, M. Hannink, E. Arvisais, R.J. Kaufman, and J.A. Diehl Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival Mol. Cell. Biol. 23 2003 7198 7209
25. D.J. Davidson, C. Haskell, S. Majest, A. Kherzai, D.A. Egan, K.A. Walter, A. Schneider, E.F. Gubbins, L. Solomon, Z. Chen, and et al. Kringle 5 of human plasminogen induces apoptosis of endothelial and tumor cells through surface-expressed glucose-regulated protein 78 Cancer Res. 65 2005 4663 4672
26. K. De Bock, M. Georgiadou, and P. Carmeliet Role of endothelial cell metabolism in vessel sprouting Cell Metab. 18 2013 634 647
27. K. De Bock, M. Georgiadou, S. Schoors, A. Kuchnio, B.W. Wong, A.R. Cantelmo, A. Quaegebeur, B. Ghesquière, S. Cauwenberghs, G. Eelen, and et al. Role of PFKFB3-driven glycolysis in vessel sprouting Cell 154 2013 651 663
28. F. De Winter, M. Oudega, A.J. Lankhorst, F.P. Hamers, B. Blits, M.J. Ruitenberg, R.J. Pasterkamp, W.H. Gispen, and J. Verhaagen Injury-induced class 3 semaphorin expression in the rat spinal cord Exp. Neurol. 175 2002 61 75
29. Y. Deng, Z.V. Wang, C. Tao, N. Gao, W.L. Holland, A. Ferdous, J.J. Repa, G. Liang, J. Ye, M.A. Lehrman, and et al. The Xbp1s/GalE axis links ER stress to postprandial hepatic metabolism J. Clin. Invest. 123 2013 455 468
30. D. Dong, M. Ni, J. Li, S. Xiong, W. Ye, J.J. Virrey, C. Mao, R. Ye, M. Wang, L. Pen, and et al. Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival, and tumor angiogenesis in transgene-induced mammary tumor development Cancer Res. 68 2008 498 505
31. B. Drogat, P. Auguste, D.T. Nguyen, M. Bouchecareilh, R. Pineau, J. Nalbantoglu, R.J. Kaufman, E. Chevet, A. Bikfalvi, and M. Moenner IRE1 signaling is essential for ischemia-induced vascular endothelial growth factor-A expression and contributes to angiogenesis and tumor growth in vivo Cancer Res. 67 2007 6700 6707
32. Q. Duan, L. Yang, W. Gong, S. Chaugai, F. Wang, C. Chen, P. Wang, M.H. Zou, and D.W. Wang MicroRNA-214 is up-regulated in heart failure patients and suppresses XBP1-mediated endothelial cells angiogenesis J. Cell Physiol. 230 2015 1964 1973
33. J.M. Ebos, and R.S. Kerbel Antiangiogenic therapy: impact on invasion, disease progression, and metastasis Nat. Rev. Clin. Oncol. 8 2011 210 221
34. R.E. Feaver, N.E. Hastings, A. Pryor, and B.R. Blackman GRP78 upregulation by atheroprone shear stress via p38-, alpha2beta1-dependent mechanism in endothelial cells Arterioscler. Thromb. Vasc. Biol. 28 2008 1534 1541
35. D.R. Fels, and C. Koumenis The PERK/eIF2alpha/ATF4 module of the UPR in hypoxia resistance and tumor growth Cancer Biol. Ther. 5 2006 723 728
36. Z. Fu, C.A. Lofqvist, Z. Shao, Y. Sun, J.S. Joyal, C.G. Hurst, R.Z. Cui, L.P. Evans, K. Tian, J.P. SanGiovanni, and et al. Dietary ω-3 polyunsaturated fatty acids decrease retinal neovascularization by adipose-endoplasmic reticulum stress reduction to increase adiponectin Am. J. Clin. Nutr. 101 2015 879 888
37. H. Fujita, B. Zhang, K. Sato, J. Tanaka, and M. Sakanaka Expressions of neuropilin-1, neuropilin-2 and semaphorin 3A mRNA in the rat brain after middle cerebral artery occlusion Brain Res. 914 2001 1 14
38. D. Fukumura, T. Gohongi, A. Kadambi, Y. Izumi, J. Ang, C.O. Yun, D.G. Buerk, P.L. Huang, and R.K. Jain Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability Proc. Natl. Acad. Sci. USA 98 2001 2604 2609
39. Y. Fukushima, M. Okada, H. Kataoka, M. Hirashima, Y. Yoshida, F. Mann, F. Gomi, K. Nishida, S. Nishikawa, and A. Uemura Sema3E-PlexinD1 signaling selectively suppresses disoriented angiogenesis in ischemic retinopathy in mice J. Clin. Invest. 121 2011 1974 1985
40. J. Gao, Y. Ishigaki, T. Yamada, K. Kondo, S. Yamaguchi, J. Imai, K. Uno, Y. Hasegawa, S. Sawada, H. Ishihara, and et al. Involvement of endoplasmic stress protein C/EBP homologous protein in arteriosclerosis acceleration with augmented biological stress responses Circulation 124 2011 830 839
41. B.M. Gardner, and P. Walter Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response Science 333 2011 1891 1894
42. P.S. Gargalovic, M. Imura, B. Zhang, N.M. Gharavi, M.J. Clark, J. Pagnon, W.P. Yang, A. He, A. Truong, S. Patel, and et al. Identification of inflammatory gene modules based on variations of human endothelial cell responses to oxidized lipids Proc. Natl. Acad. Sci. USA 103 2006 12741 12746
43. R. Ghosh, K.L. Lipson, K.E. Sargent, A.M. Mercurio, J.S. Hunt, D. Ron, and F. Urano Transcriptional regulation of VEGF-A by the unfolded protein response pathway PLoS ONE 5 2010 e9575
44. C. Gilbert, J. Rahi, M. Eckstein, J. O'Sullivan, and A. Foster Retinopathy of prematurity in middle-income countries Lancet 350 1997 12 14
45. J. Goveia, P. Stapor, and P. Carmeliet Principles of targeting endothelial cell metabolism to treat angiogenesis and endothelial cell dysfunction in disease EMBO Mol. Med. 6 2014 1105 1120
46. S. Gupta, B. McGrath, and D.R. Cavener PERK regulates the proliferation and development of insulin-secreting beta-cell tumors in the endocrine pancreas of mice PLoS ONE 4 2009 e8008
47. H.P. Hammes, Y. Feng, F. Pfister, and M. Brownlee Diabetic retinopathy: targeting vasoregression Diabetes 60 2011 9 16
48. D. Han, A.G. Lerner, L. Vande Walle, J.P. Upton, W. Xu, A. Hagen, B.J. Backes, S.A. Oakes, and F.R. Papa IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates Cell 138 2009 562 575
49. J. Han, S.H. Back, J. Hur, Y.H. Lin, R. Gildersleeve, J. Shan, C.L. Yuan, D. Krokowski, S. Wang, M. Hatzoglou, and et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death Nat. Cell Biol. 15 2013 481 490
50. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
51. H.P. Harding, Y. Zhang, and D. Ron Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase Nature 397 1999 271 274
52. H.P. Harding, I. Novoa, Y. Zhang, H. Zeng, R. Wek, M. Schapira, and D. Ron Regulated translation initiation controls stress-induced gene expression in mammalian cells Mol. Cell 6 2000 1099 1108
53. H.P. Harding, H. Zeng, Y. Zhang, R. Jungries, P. Chung, H. Plesken, D.D. Sabatini, and D. Ron Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival Mol. Cell 7 2001 1153 1163
54. H.P. Harding, Y. Zhang, H. Zeng, I. Novoa, P.D. Lu, M. Calfon, N. Sadri, C. Yun, B. Popko, R. Paules, and et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress Mol. Cell 11 2003 619 633
55. B. Hardy, A. Battler, C. Weiss, O. Kudasi, and A. Raiter Therapeutic angiogenesis of mouse hind limb ischemia by novel peptide activating GRP78 receptor on endothelial cells Biochem. Pharmacol. 75 2008 891 899
56. M. Hellström, L.K. Phng, J.J. Hofmann, E. Wallgard, L. Coultas, P. Lindblom, J. Alva, A.K. Nilsson, L. Karlsson, N. Gaiano, and et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis Nature 445 2007 776 780
57. C. Hetz, E. Chevet, and H.P. Harding Targeting the unfolded protein response in disease Nat. Rev. Drug Discov. 12 2013 703 719
58. J. Hollien Evolution of the unfolded protein response Biochim. Biophys. Acta 1833 2013 2458 2463
59. J. Hollien, and J.S. Weissman Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response Science 313 2006 104 107
60. P. Hu, Z. Han, A.D. Couvillon, R.J. Kaufman, and J.H. Exton Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression Mol. Cell. Biol. 26 2006 3071 3084
61. W.K. Hu, R. Liu, H. Pei, and B. Li Endoplasmic reticulum stress-related factors protect against diabetic retinopathy Exp. Diabetes Res. 2012 2012 507986
62. T. Iwawaki, R. Akai, S. Yamanaka, and K. Kohno Function of IRE1 alpha in the placenta is essential for placental development and embryonic viability Proc. Natl. Acad. Sci. USA 106 2009 16657 16662
63. C. Johnson, H.J. Sung, S.M. Lessner, M.E. Fini, and Z.S. Galis Matrix metalloproteinase-9 is required for adequate angiogenic revascularization of ischemic tissues: potential role in capillary branching Circ. Res. 94 2004 262 268
64. A.M. Joussen, V. Poulaki, M.L. Le, K. Koizumi, C. Esser, H. Janicki, U. Schraermeyer, N. Kociok, S. Fauser, B. Kirchhof, and et al. A central role for inflammation in the pathogenesis of diabetic retinopathy FASEB J. 18 2004 1450 1452
65. J.-S. Joyal, N. Sitaras, F. Binet, J.C. Rivera, A. Stahl, K. Zaniolo, Z. Shao, A. Polosa, T. Zhu, D. Hamel, and et al. Ischemic neurons prevent vascular regeneration of neural tissue by secreting semaphorin 3A Blood 117 2011 6024 6035
66. E. Karali, S. Bellou, D. Stellas, A. Klinakis, C. Murphy, and T. Fotsis VEGF signals through ATF6 and PERK to promote endothelial cell survival and angiogenesis in the absence of ER stress Mol. Cell 54 2014 559 572
67. Y. Katanasaka, T. Ishii, T. Asai, H. Naitou, N. Maeda, F. Koizumi, S. Miyagawa, N. Ohashi, and N. Oku Cancer antineovascular therapy with liposome drug delivery systems targeted to BiP/GRP78 Int. J. Cancer 127 2010 2685 2698
68. J.H. Kempen, B.J. O'Colmain, M.C. Leske, S.M. Haffner, R. Klein, S.E. Moss, H.R. Taylor, R.F. Hamman Eye Diseases Prevalence Research Group The prevalence of diabetic retinopathy among adults in the United States Arch. Ophthalmol. 122 2004 552 563
69. J. Kern, G. Untergasser, C. Zenzmaier, B. Sarg, G. Gastl, E. Gunsilius, and M. Steurer GRP-78 secreted by tumor cells blocks the antiangiogenic activity of bortezomib Blood 114 2009 3960 3967
70. M.Y. Koh, and G. Powis Passing the baton: the HIF switch Trends Biochem. Sci. 37 2012 364 372
71. A.V. Korennykh, P.F. Egea, A.A. Korostelev, J. Finer-Moore, C. Zhang, K.M. Shokat, R.M. Stroud, and P. Walter The unfolded protein response signals through high-order assembly of Ire1 Nature 457 2009 687 693
72. E.J. Kuiper, F.A. Van Nieuwenhoven, M.D. de Smet, J.C. van Meurs, M.W. Tanck, N. Oliver, I. Klaassen, C.J. Van Noorden, R. Goldschmeding, and R.O. Schlingemann The angio-fibrotic switch of VEGF and CTGF in proliferative diabetic retinopathy PLoS ONE 3 2008 e2675
73. B. Larrivée, C. Freitas, S. Suchting, I. Brunet, and A. Eichmann Guidance of vascular development: lessons from the nervous system Circ. Res. 104 2009 428 441
74. A.S. Lee Glucose-regulated proteins in cancer: molecular mechanisms and therapeutic potential Nat. Rev. Cancer 14 2014 263 276
75. A.H. Lee, N.N. Iwakoshi, and L.H. Glimcher XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response Mol. Cell. Biol. 23 2003 7448 7459
76. Y.Y. Lee, R.C. Cevallos, and E. Jan An upstream open reading frame regulates translation of GADD34 during cellular stresses that induce eIF2alpha phosphorylation J. Biol. Chem. 284 2009 6661 6673
77. A. Li, S. Dubey, M.L. Varney, B.J. Dave, and R.K. Singh IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis J. Immunol. 170 2003 3369 3376
78. J. Li, J.J. Wang, Q. Yu, M. Wang, and S.X. Zhang Endoplasmic reticulum stress is implicated in retinal inflammation and diabetic retinopathy FEBS Lett. 583 2009 1521 1527
79. K.L. Lipson, S.G. Fonseca, S. Ishigaki, L.X. Nguyen, E. Foss, R. Bortell, A.A. Rossini, and F. Urano Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1 Cell Metab. 4 2006 245 254
80. C.Y. Liu, H.N. Wong, J.A. Schauerte, and R.J. Kaufman The protein kinase/endoribonuclease IRE1alpha that signals the unfolded protein response has a luminal N-terminal ligand-independent dimerization domain J. Biol. Chem. 277 2002 18346 18356
81. L. Liu, X. Qi, Z. Chen, L. Shaw, J. Cai, L.H. Smith, M.B. Grant, and M.E. Boulton Targeting the IRE1α/XBP1 and ATF6 arms of the unfolded protein response enhances VEGF blockade to prevent retinal and choroidal neovascularization Am. J. Pathol. 182 2013 1412 1424
82. R. Liu, X. Li, W. Gao, Y. Zhou, S. Wey, S.K. Mitra, V. Krasnoperov, D. Dong, S. Liu, D. Li, and et al. Monoclonal antibody against cell surface GRP78 as a novel agent in suppressing PI3K/AKT signaling, tumor growth, and metastasis Clin. Cancer Res. 19 2013 6802 6811
83. I.B. Lobov, R.A. Renard, N. Papadopoulos, N.W. Gale, G. Thurston, G.D. Yancopoulos, and S.J. Wiegand Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting Proc. Natl. Acad. Sci. USA 104 2007 3219 3224
84. S. Loges, T. Schmidt, and P. Carmeliet Mechanisms of resistance to anti-angiogenic therapy and development of third-generation anti-angiogenic drug candidates Genes Cancer 1 2010 12 25
85. C. Loinard, Y. Zouggari, P. Rueda, B. Ramkhelawon, C. Cochain, J. Vilar, A. Récalde, A. Richart, D. Charue, M. Duriez, and et al. C/EBP homologous protein-10 (CHOP-10) limits postnatal neovascularization through control of endothelial nitric oxide synthase gene expression Circulation 125 2012 1014 1026
86. P.D. Lu, H.P. Harding, and D. Ron Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response J. Cell Biol. 167 2004 27 33
87. M. Lu, D.A. Lawrence, S. Marsters, D. Acosta-Alvear, P. Kimmig, A.S. Mendez, A.W. Paton, J.C. Paton, P. Walter, and A. Ashkenazi Cell death. Opposing unfolded-protein-response signals converge on death receptor 5 to control apoptosis Science 345 2014 98 101
88. S. Luo, P. Baumeister, S. Yang, S.F. Abcouwer, and A.S. Lee Induction of Grp78/BiP by translational block: activation of the Grp78 promoter by ATF4 through and upstream ATF/CRE site independent of the endoplasmic reticulum stress elements J. Biol. Chem. 278 2003 37375 37385
89. Y. Ma, and L.M. Hendershot Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress J. Biol. Chem. 278 2003 34864 34873
90. D.J. Maly, and F.R. Papa Druggable sensors of the unfolded protein response Nat. Chem. Biol. 10 2014 892 901
91. S.J. Marciniak, C.Y. Yun, S. Oyadomari, I. Novoa, Y. Zhang, R. Jungreis, K. Nagata, H.P. Harding, and D. Ron CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum Genes Dev. 18 2004 3066 3077
92. D. Martin, Y. Li, J. Yang, G. Wang, A. Margariti, Z. Jiang, H. Yu, A. Zampetaki, Y. Hu, Q. Xu, and L. Zeng Unspliced X-box-binding protein 1 (XBP1) protects endothelial cells from oxidative stress through interaction with histone deacetylase 3 J. Biol. Chem. 289 2014 30625 30634
93. K.D. McCullough, J.L. Martindale, L.O. Klotz, T.Y. Aw, and N.J. Holbrook Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state Mol. Cell. Biol. 21 2001 1249 1259
94. B.C. McFarland, J. Stewart Jr., A. Hamza, R. Nordal, D.J. Davidson, J. Henkin, and C.L. Gladson Plasminogen kringle 5 induces apoptosis of brain microvessel endothelial cells: sensitization by radiation and requirement for GRP78 and LRP1 Cancer Res. 69 2009 5537 5545
95. P. Mellor, L. Deibert, B. Calvert, K. Bonham, S.A. Carlsen, and D.H. Anderson CREB3L1 is a metastasis suppressor that represses expression of genes regulating metastasis, invasion, and angiogenesis Mol. Cell. Biol. 33 2013 4985 4995
96. N. Mimura, M. Fulciniti, G. Gorgun, Y.T. Tai, D. Cirstea, L. Santo, Y. Hu, C. Fabre, J. Minami, H. Ohguchi, and et al. Blockade of XBP1 splicing by inhibition of IRE1α is a promising therapeutic option in multiple myeloma Blood 119 2012 5772 5781
97. Q. Mohamed, M.C. Gillies, and T.Y. Wong Management of diabetic retinopathy: a systematic review JAMA 298 2007 902 916
98. J.A. Moreno, M. Halliday, C. Molloy, H. Radford, N. Verity, J.M. Axten, C.A. Ortori, A.E. Willis, P.M. Fischer, D.A. Barrett, and G.R. Mallucci Oral treatment targeting the unfolded protein response prevents neurodegeneration and clinical disease in prion-infected mice Sci. Transl. Med. 5 2013 206ra138
99. M. Ni, Y. Zhang, and A.S. Lee Beyond the endoplasmic reticulum: atypical GRP78 in cell viability, signalling and therapeutic targeting Biochem. J. 434 2011 181 188
100. I. Novoa, H. Zeng, H.P. Harding, and D. Ron Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha J. Cell Biol. 153 2001 1011 1022
101. N. Ohoka, S. Yoshii, T. Hattori, K. Onozaki, and H. Hayashi TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death EMBO J. 24 2005 1243 1255
102. O.V. Oskolkova, T. Afonyushkin, A. Leitner, E. von Schlieffen, P.S. Gargalovic, A.J. Lusis, B.R. Binder, and V.N. Bochkov ATF4-dependent transcription is a key mechanism in VEGF up-regulation by oxidized phospholipids: critical role of oxidized sn-2 residues in activation of unfolded protein response Blood 112 2008 330 339
103. U. Ozcan, E. Yilmaz, L. Ozcan, M. Furuhashi, E. Vaillancourt, R.O. Smith, C.Z. Görgün, and G.S. Hotamisligil Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes Science 313 2006 1137 1140
104. L.R. Palam, T.D. Baird, and R.C. Wek Phosphorylation of eIF2 facilitates ribosomal bypass of an inhibitory upstream ORF to enhance CHOP translation J. Biol. Chem. 286 2011 10939 10949
105. I. Papandreou, N.C. Denko, M. Olson, H. Van Melckebeke, S. Lust, A. Tam, D.E. Solow-Cordero, D.M. Bouley, F. Offner, M. Niwa, and A.C. Koong Identification of an Ire1alpha endonuclease specific inhibitor with cytotoxic activity against human multiple myeloma Blood 117 2011 1311 1314
106. E.R. Pereira, N. Liao, G.A. Neale, and L.M. Hendershot Transcriptional and post-transcriptional regulation of proangiogenic factors by the unfolded protein response PLoS ONE 5 2010 5
107. E.R. Pereira, K. Frudd, W. Awad, and L.M. Hendershot Endoplasmic reticulum (ER) stress and hypoxia response pathways interact to potentiate hypoxia-inducible factor 1 (HIF-1) transcriptional activity on targets like vascular endothelial growth factor (VEGF) J. Biol. Chem. 289 2014 3352 3364
108. M. Philippova, D. Ivanov, M.B. Joshi, E. Kyriakakis, K. Rupp, T. Afonyushkin, V. Bochkov, P. Erne, and T.J. Resink Identification of proteins associating with glycosylphosphatidylinositol- anchored T-cadherin on the surface of vascular endothelial cells: role for Grp78/BiP in T-cadherin-dependent cell survival Mol. Cell. Biol. 28 2008 4004 4017
109. M. Potente, H. Gerhardt, and P. Carmeliet Basic and therapeutic aspects of angiogenesis Cell 146 2011 873 887
110. H. Puthalakath, L.A. O'Reilly, P. Gunn, L. Lee, P.N. Kelly, N.D. Huntington, P.D. Hughes, E.M. Michalak, J. McKimm-Breschkin, N. Motoyama, and et al. ER stress triggers apoptosis by activating BH3-only protein Bim Cell 129 2007 1337 1349
111. P. Pyrko, A.H. Schönthal, F.M. Hofman, T.C. Chen, and A.S. Lee The unfolded protein response regulator GRP78/BiP as a novel target for increasing chemosensitivity in malignant gliomas Cancer Res. 67 2007 9809 9816
112. A. Raiter, C. Weiss, Z. Bechor, I. Ben-Dor, A. Battler, B. Kaplan, and B. Hardy Activation of GRP78 on endothelial cell membranes by an ADAM15-derived peptide induces angiogenesis J. Vasc. Res. 47 2010 399 411
113. W. Risau Mechanisms of angiogenesis Nature 386 1997 671 674
114. W. Risau, and I. Flamme Vasculogenesis Annu. Rev. Cell Dev. Biol. 11 1995 73 91
115. L. Romero-Ramirez, H. Cao, M.P. Regalado, N. Kambham, D. Siemann, J.J. Kim, Q.T. Le, and A.C. Koong X box-binding protein 1 regulates angiogenesis in human pancreatic adenocarcinomas Transl. Oncol. 2 2009 31 38
116. D. Ron, and P. Walter Signal integration in the endoplasmic reticulum unfolded protein response Nat. Rev. Mol. Cell Biol. 8 2007 519 529
117. P.J. Rosenfeld, D.M. Brown, J.S. Heier, D.S. Boyer, P.K. Kaiser, C.Y. Chung, R.Y. Kim MARINA Study Group Ranibizumab for neovascular age-related macular degeneration N. Engl. J. Med. 355 2006 1419 1431
118. C.N. Roybal, L.A. Hunsaker, O. Barbash, D.L. Vander Jagt, and S.F. Abcouwer The oxidative stressor arsenite activates vascular endothelial growth factor mRNA transcription by an ATF4-dependent mechanism J. Biol. Chem. 280 2005 20331 20339
119. H.D. Ryoo, P.M. Domingos, M.J. Kang, and H. Steller Unfolded protein response in a Drosophila model for retinal degeneration EMBO J. 26 2007 242 252
120. T. Rzymski, M. Milani, L. Pike, F. Buffa, H.R. Mellor, L. Winchester, I. Pires, E. Hammond, I. Ragoussis, and A.L. Harris Regulation of autophagy by ATF4 in response to severe hypoxia Oncogene 29 2010 4424 4435
121. R. Sano, and J.C. Reed ER stress-induced cell death mechanisms Biochim. Biophys. Acta 1833 2013 3460 3470
122. P. Sapieha Eyeing central neurons in vascular growth and reparative angiogenesis Blood 120 2012 2182 2194
123. P. Sapieha, M. Sirinyan, D. Hamel, K. Zaniolo, J.S. Joyal, J.H. Cho, J.C. Honoré, E. Kermorvant-Duchemin, D.R. Varma, S. Tremblay, and et al. The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis Nat. Med. 14 2008 1067 1076
124. P. Sapieha, D. Hamel, Z. Shao, J.C. Rivera, K. Zaniolo, J.S. Joyal, and S. Chemtob Proliferative retinopathies: angiogenesis that blinds Int. J. Biochem. Cell Biol. 42 2010 5 12
125. P. Sapieha, J.S. Joyal, J.C. Rivera, E. Kermorvant-Duchemin, F. Sennlaub, P. Hardy, P. Lachapelle, and S. Chemtob Retinopathy of prematurity: understanding ischemic retinal vasculopathies at an extreme of life J. Clin. Invest. 120 2010 3022 3032
126. P. Sapieha, A. Stahl, J. Chen, M.R. Seaward, K.L. Willett, N.M. Krah, R.J. Dennison, K.M. Connor, C.M. Aderman, E. Liclican, and et al. 5-Lipoxygenase metabolite 4-HDHA is a mediator of the antiangiogenic effect of ω-3 polyunsaturated fatty acids Sci. Transl. Med. 3 2011 69ra12
127. S. Schoors, K. De Bock, A.R. Cantelmo, M. Georgiadou, B. Ghesquière, S. Cauwenberghs, A. Kuchnio, B.W. Wong, A. Quaegebeur, J. Goveia, and et al. Partial and transient reduction of glycolysis by PFKFB3 blockade reduces pathological angiogenesis Cell Metab. 19 2014 37 48
128. S. Schoors, U. Bruning, R. Missiaen, K.C. Queiroz, G. Borgers, I. Elia, A. Zecchin, A.R. Cantelmo, S. Christen, J. Goveia, and et al. Fatty acid carbon is essential for dNTP synthesis in endothelial cells Nature 520 2015 192 197
129. L.E. Smith Through the eyes of a child: understanding retinopathy through ROP the Friedenwald lecture Invest. Ophthalmol. Vis. Sci. 49 2008 5177 5182
130. L.E. Smith, W. Shen, C. Perruzzi, S. Soker, F. Kinose, X. Xu, G. Robinson, S. Driver, J. Bischoff, B. Zhang, and et al. Regulation of vascular endothelial growth factor-dependent retinal neovascularization by insulin-like growth factor-1 receptor Nat. Med. 5 1999 1390 1395
131. P. Sonveaux, T. Copetti, C.J. De Saedeleer, F. Végran, J. Verrax, K.M. Kennedy, E.J. Moon, S. Dhup, P. Danhier, F. Frérart, and et al. Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis PLoS ONE 7 2012 e33418
132. R. Sriburi, H. Bommiasamy, G.L. Buldak, G.R. Robbins, M. Frank, S. Jackowski, and J.W. Brewer Coordinate regulation of phospholipid biosynthesis and secretory pathway gene expression in XBP-1(S)-induced endoplasmic reticulum biogenesis J. Biol. Chem. 282 2007 7024 7034
133. A. Stahl, P. Sapieha, K.M. Connor, J.P. Sangiovanni, J. Chen, C.M. Aderman, K.L. Willett, N.M. Krah, R.J. Dennison, M.R. Seaward, and et al. Short communication: PPAR gamma mediates a direct antiangiogenic effect of omega 3-PUFAs in proliferative retinopathy Circ. Res. 107 2010 495 500
134. A.N. Stratman, W.B. Saunders, A. Sacharidou, W. Koh, K.E. Fisher, D.C. Zawieja, M.J. Davis, and G.E. Davis Endothelial cell lumen and vascular guidance tunnel formation requires MT1-MMP-dependent proteolysis in 3-dimensional collagen matrices Blood 114 2009 237 247
135. S. Suchting, C. Freitas, F. le Noble, R. Benedito, C. Bréant, A. Duarte, and A. Eichmann The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching Proc. Natl. Acad. Sci. USA 104 2007 3225 3230
136. I. Tabas Macrophage apoptosis in atherosclerosis: consequences on plaque progression and the role of endoplasmic reticulum stress Antioxid. Redox Signal. 11 2009 2333 2339
137. I. Tabas Macrophage death and defective inflammation resolution in atherosclerosis Nat. Rev. Immunol. 10 2010 36 46
138. I. Tabas, and D. Ron Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress Nat. Cell Biol. 13 2011 184 190
139. S. Tajiri, S. Oyadomari, S. Yano, M. Morioka, T. Gotoh, J.I. Hamada, Y. Ushio, and M. Mori Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP Cell Death Differ. 11 2004 403 415
140. M. Tavian, and B. Péault Embryonic development of the human hematopoietic system Int. J. Dev. Biol. 49 2005 243 250
141. J.P. Upton, L. Wang, D. Han, E.S. Wang, N.E. Huskey, L. Lim, M. Truitt, M.T. McManus, D. Ruggero, A. Goga, and et al. IRE1α cleaves select microRNAs during ER stress to derepress translation of proapoptotic Caspase-2 Science 338 2012 818 822
142. F. Urano, X. Wang, A. Bertolotti, Y. Zhang, P. Chung, H.P. Harding, and D. Ron Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1 Science 287 2000 664 666
143. J.J. Virrey, D. Dong, C. Stiles, J.B. Patterson, L. Pen, M. Ni, A.H. Schönthal, T.C. Chen, F.M. Hofman, and A.S. Lee Stress chaperone GRP78/BiP confers chemoresistance to tumor-associated endothelial cells Mol. Cancer Res. 6 2008 1268 1275
144. P. Walter, and D. Ron The unfolded protein response: from stress pathway to homeostatic regulation Science 334 2011 1081 1086
145. Y. Wang, G.N. Alam, Y. Ning, F. Visioli, Z. Dong, J.E. Nör, and P.J. Polverini The unfolded protein response induces the angiogenic switch in human tumor cells through the PERK/ATF4 pathway Cancer Res. 72 2012 5396 5406
146. X. Wang, G. Wang, M. Kunte, V. Shinde, and M. Gorbatyuk Modulation of angiogenesis by genetic manipulation of ATF4 in mouse model of oxygen-induced retinopathy [corrected] Invest. Ophthalmol. Vis. Sci. 54 2013 5995 6002
147. Y. Watatani, K. Ichikawa, N. Nakanishi, M. Fujimoto, H. Takeda, N. Kimura, H. Hirose, S. Takahashi, and Y. Takahashi Stress-induced translation of ATF5 mRNA is regulated by the 5′-untranslated region J. Biol. Chem. 283 2008 2543 2553
148. D.K. Ways, and M.J. Sheetz The role of protein kinase C in the development of the complications of diabetes Vitam. Horm. 60 2000 149 193
149. J. Welti, S. Loges, S. Dimmeler, and P. Carmeliet Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer J. Clin. Invest. 123 2013 3190 3200
150. Z. Xu, Y. Wei, J. Gong, H. Cho, J.K. Park, E.R. Sung, H. Huang, L. Wu, C. Eberhart, J.T. Handa, and et al. NRF2 plays a protective role in diabetic retinopathy in mice Diabetologia 57 2014 204 213
151. H. Yamaguchi, and H.G. Wang CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells J. Biol. Chem. 279 2004 45495 45502
152. K. Yamamoto, H. Ichijo, and S.J. Korsmeyer BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M Mol. Cell. Biol. 19 1999 8469 8478
153. K. Yamamoto, T. Sato, T. Matsui, M. Sato, T. Okada, H. Yoshida, A. Harada, and K. Mori Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1 Dev. Cell 13 2007 365 376
154. K. Yamamoto, K. Takahara, S. Oyadomari, T. Okada, T. Sato, A. Harada, and K. Mori Induction of liver steatosis and lipid droplet formation in ATF6alpha-knockout mice burdened with pharmacological endoplasmic reticulum stress Mol. Biol. Cell 21 2010 2975 2986
155. H. Yang, R. Liu, Z. Cui, Z.Q. Chen, S. Yan, H. Pei, and B. Li Functional characterization of 58-kilodalton inhibitor of protein kinase in protecting against diabetic retinopathy via the endoplasmic reticulum stress pathway Mol. Vis. 17 2011 78 84
156. J. Ye, R.B. Rawson, R. Komuro, X. Chen, U.P. Davé, R. Prywes, M.S. Brown, and J.L. Goldstein ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs Mol. Cell 6 2000 1355 1364
157. T. Yoneda, K. Imaizumi, K. Oono, D. Yui, F. Gomi, T. Katayama, and M. Tohyama Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress J. Biol. Chem. 276 2001 13935 13940
158. H. Yoshida, K. Haze, H. Yanagi, T. Yura, and K. Mori Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors J. Biol. Chem. 273 1998 33741 33749
159. L. Zeng, A. Zampetaki, A. Margariti, A.E. Pepe, S. Alam, D. Martin, Q. Xiao, W. Wang, Z.G. Jin, G. Cockerill, and et al. Sustained activation of XBP1 splicing leads to endothelial apoptosis and atherosclerosis development in response to disturbed flow Proc. Natl. Acad. Sci. USA 106 2009 8326 8331
160. L. Zeng, Q. Xiao, M. Chen, A. Margariti, D. Martin, A. Ivetic, H. Xu, J. Mason, W. Wang, G. Cockerill, and et al. Vascular endothelial cell growth-activated XBP1 splicing in endothelial cells is crucial for angiogenesis Circulation 127 2013 1712 1722
161. P. Zhang, B. McGrath, S. Li, A. Frank, F. Zambito, J. Reinert, M. Gannon, K. Ma, K. McNaughton, and D.R. Cavener The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas Mol. Cell. Biol. 22 2002 3864 3874
162. K. Zhang, H.N. Wong, B. Song, C.N. Miller, D. Scheuner, and R.J. Kaufman The unfolded protein response sensor IRE1alpha is required at 2 distinct steps in B cell lymphopoiesis J. Clin. Invest. 115 2005 268 281
163. A.X. Zhou, and I. Tabas The UPR in atherosclerosis Semin. Immunopathol. 35 2013 321 332
164. J. Zhou, C.Y. Liu, S.H. Back, R.L. Clark, D. Peisach, Z. Xu, and R.J. Kaufman The crystal structure of human IRE1 luminal domain reveals a conserved dimerization interface required for activation of the unfolded protein response Proc. Natl. Acad. Sci. USA 103 2006 14343 14348