Endoplasmic reticulum stress and angiogenesis: Is there an interaction between them?

Liver International

Volumn 34, Issue 6, 2014, Pages

  Paridaens, Annelies ^a   Laukens, Debby ^a   Vandewynckel, Yves Paul ^a   Coulon, Stephanie ^a   Van Vlierberghe, Hans ^a   Geerts, Anja ^a   Colle, Isabelle ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Angiogenesis; Cirrhosis; Endoplasmic reticulum stress; Liver diseases; Unfolded protein response; Vascular endothelial growth factor A

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; INITIATION FACTOR 2ALPHA; MESSENGER RNA; PLATELET DERIVED GROWTH FACTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; VASCULOTROPIN A; X BOX BINDING PROTEIN 1; SIGNAL PEPTIDE;

ANGIOGENESIS; ATHEROSCLEROSIS; CHRONIC LIVER DISEASE; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM STRESS; HEPATITIS B; HUMAN; KIDNEY ISCHEMIA; NEOPLASM; NONALCOHOLIC FATTY LIVER; NONHUMAN; RETINOPATHY; REVIEW; UNFOLDED PROTEIN RESPONSE; ANIMAL; CHRONIC DISEASE; ENDOPLASMIC RETICULUM; LIVER; LIVER DISEASE; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; VASCULARIZATION;

ANIMALS; CHRONIC DISEASE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER; LIVER DISEASES; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84902546214     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/liv.12457     Document Type: Review

References (74)

1. Vecchi C, Montosi G, Zhang K, et al. ER stress controls iron metabolism through induction of hepcidin. Science 2009; 325: 877-80.
2. Zhang X, Gureasko J, Shen K, Cole PA, Kuriyan J. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 2006; 125: 1137-49.
3. Roybal CN, Yang S, Sun CW, et al. Homocysteine increases the expression of vascular endothelial growth factor by a mechanism involving endoplasmic reticulum stress and transcription factor ATF4. J Biol Chem 2004; 279: 14844-52.
4. Oskolkova OV, Afonyushkin T, Leitner A, et al. 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 2008; 112: 330-9.
5. Afonyushkin T, Oskolkova OV, Philippova M, et al. 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 2010; 30: 1007-13.
6. Bouvier N, Fougeray S, Beaune P, Thervet E, Pallet N. The unfolded protein response regulates an angiogenic response by the kidney epithelium during ischemic stress. J Biol Chem 2012; 18: 14557-68.
7. Malhi H, Kaufman RJ. Endoplasmic reticulum stress in liver disease. J Hepatol 2011; 54: 795-809.
8. Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003; 23: 7448-59.
9. Kaplowitz N, Ji C. Unfolding new mechanisms of alcoholic liver disease in the endoplasmic reticulum. J Gastroenterol Hepatol 2006; 21(Suppl. 3): S7-S9.
10. Hollien J, Lin JH, Li H, et al. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 2009; 186: 323-31.
11. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000; 2: 326-32.
12. DuRose JB, Scheuner D, Kaufman RJ, Rothblum LI, Niwa M. Phosphorylation of eukaryotic translation initiation factor 2 alpha coordinates rRNA transcription and translation inhibition during endoplasmic reticulum stress. Mol Cell Biol 2009; 29: 4295-307.
13. Pereira ER, Liao N, Neale GA, Hendershot LM. Transcriptional and post-transcriptional regulation of proangiogenic factors by the unfolded protein response. PLoS ONE 2010; 5: e12521.
14. Samali A, FitzGerald U, Deegan S, Gupta S. Methods for monitoring endoplasmic reticulum stress and the unfolded protein response. Int J Cell Biol 2010; 2010: 830307.
15. Ghosh R, Lipson KL, Sargent KE, et al. Transcriptional regulation of VEGF-A by the unfolded protein response pathway. PLoS ONE 2010; 5: e9575.
16. Zong WX, Li C, Hatzivassiliou G, et al. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 2003; 162: 59-69.
17. Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003; 4: 552-65.
18. Rao RV, Hermel E, Castro-Obregon S, et al. Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. J Biol Chem 2001; 276: 33869-74.
19. Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 2002; 277: 34287-94.
20. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ. Gadd153 sensitizes cells to endoplasmic reticulum stress by downregulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001; 21: 1249-59.
21. Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000; 287: 664-6.
22. Weston CR, Davis RJ. The JNK signal transduction pathway. Curr Opin Cell Biol 2007; 19: 142-9.
23. Vandewynckel Y-P, Laukens D, Geerts A, et al. The paradox of the unfolded protein response in cancer. Anticancer Res 2013; 33: 3-14.
24. Tazi KA, Bièche I, Paradis V, et al. In vivo altered unfolded protein response and apoptosis in livers from lipopolysaccharide-challenged cirrhotic rats. J Hepatol 2007; 46: 1075-1088.
25. Lusis AJ. Atherosclerosis. Nature 2000; 407: 233-41.
26. Abcouwer SF, Marjon PL, Loper RK, Vander Jagt DL. Response of VEGF expression to amino acid deprivation and inducers of endoplasmic reticulum stress. Invest Ophthalmol Vis Sci 2002; 43: 2791-8.
27. Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol 1995; 11: 73-91.
28. Flamme I, Frölich T, Risau W. Molecular mechanisms of vasculogenesis and embryonic angiogenesis. J Cell Physiol 1997; 173: 206-10.
29. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 2005; 438: 932-6.
30. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003; 9: 669-76.
31. Carmeliet P, Ferreira V, Breier G, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996; 380: 435-39.
32. Ferrara N, Carver-Moore K, Chen H, et al. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996; 380: 439-42.
33. Hickey MM, Simon MC. Regulation of angiogenesis by hypoxia and hypoxia-inducible factors. Curr Top Dev Biol 2006; 76: 217-57.
34. Carmeliet P, Moons L, Luttun A, et al. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 2001; 7: 575-83.
35. Van Steenkiste C, Ribera J, Geerts A, et al. Inhibition of placental growth factor activity reduces the severity of fibrosis, inflammation and portal hypertension in cirrhotic mice. Hepatology 2011; 53: 1629-40.
36. Klein S, Roghani M, Rifkin DB. Fibroblast growth factors as angiogenesis factors: new insights into their mechanism of action. EXS 1997; 79: 159-92.
37. Pöling J, Szibor M, Schimanski S, et al. Induction of smooth muscle cell migration during arteriogenesis is mediated by Rap2. Arterioscler Thromb Vasc Biol 2011; 31: 2297-305.
38. Li A, Dubey S, Varney ML, Dave BJ, Singh RK. IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. J Immunol 2003; 170: 3369-76.
39. Lee AH, Chu GC, Iwakoshi NN, Glimcher LH. XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J 2005; 24: 4368-80.
40. Reimold AM, Etkin A, Clauss I, et al. An essential role in liver development for transcription factor XBP-1. Genes Dev 2000; 14: 153-7.
41. Zeng L, Xiao Q, Chen M, et al. Vascular endothelial cell growth-activated XBP1 splicing in endothelial cells is crucial for angiogenesis. Circulation 2013; 127: 1712-22.
42. Iwawaki T, Akai R, Yamanaka S, Kohno K. Function of IRE1 alpha in the placenta is essential for placental development and embryonic viability. Proc Natl Acad Sci USA 2009; 106: 16657-62.
43. Chaparro M, Sanz-Cameno P, Trapero-Marugan M, Garcia-Buey L, Moreno-Otero R. Mechanisms of angiogenesis in chronic inflammatory liver disease. Ann Hepatol 2007; 6: 208-13.
44. Fernández M, Semela D, Bruix J, et al. Angiogenesis in liver disease. J Hepatol 2009; 50: 604-20.
45. Coulon S, Heindryckx F, Geerts A, et al. Angiogenesis in chronic liver disease and its complications. Liver Int 2010; 31: 146-62.
46. Lazar C, Macovei A, Petrescu S, Branza-Nichita N. Activation of ERAD pathway by human hepatitis B virus modulates viral and subviral particle production. PLoS ONE 2012; 7: e34169.
47. Asselah T, Bièche I, Mansouri A, et al. In vivo hepatic endoplasmic reticulum stress in patients with chronic hepatitis C. J Pathol 2010; 221: 264-74.
48. Yang JC, Teng CF, Wu HC, et al. Enhanced expression of vascular endothelial growth factor-A in ground glass hepatocytes and its implication in hepatitis B virus hepatocarcinogenesis. Hepatology 2009; 49: 1962-71.
49. Wei Y, Wang D, Topczewski F, Pagliassotti MJ. Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells. Am J Physiol Endocrinol Metab 2006; 291: 275-81.
50. Salcedo X, Medina J, Sanz-Cameno P. Review article: angiogenesis soluble factors as liver disease markers. Aliment Pharmacol Ther 2005; 22: 23-30.
51. Coulon S, Legry V, Heindryckx F, et al. Role of vascular endothelial growth factor in the pathophysiology of nonalcoholic steatohepatitis in two rodent models. Hapatology 2013; 57: 1793-805.
52. Nakamura S, Takizawa H, Shimazawa M, et al. Mild endoplasmic reticulum stress promotes retinal neovascularization via induction of BiP/GRP78. PLoS ONE 2013; 8: e60517.
53. Ozcan U, Cao Q, Yilmaz E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004; 306: 457-61.
54. Griffiths B, Lewis CA, Bensaad K, et al. Sterol regulatory element binding protein dependent regulation of lipid synthesis supports cell survival and tumour growth. Cancer Metab 2013; 1: 3.
55. Bobrovnikova-Marjon E, Hatzivassiliou G, Grigoriadou C, et al. PERK-dependent regulation of lipogenesis during mouse mammary gland development and adipocyte differentiation. Proc Natl Acad Sci USA 2008; 105: 16314-9.
56. Ozcan U, Yilmaz E, Ozcan L, et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006; 313: 1137-40.
57. Fu S, Watkins SM, Hotamisligil GS. The role of endoplasmic reticulum in hepatic lipid homeostasis and stress signaling. Cell Metab 2012; 15: 623-34.
58. Drogat B, Auguste P, Nguyen DT, et al. IRE1 signaling is essential for ischemia-induced vascular endothelial growth factor A expression and contributes to angiogenesis and tumour growth in vivo. Cancer Res 2007; 67: 6700-7.
59. Auf G, Jabouille A, Guérit S, et al. IRE1 is a key regulator of angiogenesis and invasion in malignant glioma. Proc Natl Acad Sci U S A 2010; 107: 15553-8.
60. Romero-Ramirez L, Cao H, Nelson D, et al. XBP1 is essential for survival under hypoxic conditions and is required for tumour growth. Cancer Res 2004; 46: 5943-7.
61. Li J, Wang JJ, Yu Q, Wang M, Zhang SX. Endoplasmic reticulum stress is implicated in retinal inflammation and diabetic retinopathy. FEBS Lett 2009; 583: 1521-7.
62. Liu L, Qi X, Chen Z, et al. Targeting the Ire1α/XBP1 and ATF6 arms of the unfolded protein response enhances VEGF blockade to prevent retinal and choroidal neovascularization. Am J Pathol 2013; 182: 1412-24.
63. Wang Y, Alam GN, Ning Y, et al. The unfolded protein response induces the angiogenic switch in human tumor cells through the PERK/ATF4 pathway. Cancer Res 2012; 72: 1-11.
64. Gupta S, McGrath B, Cavener DR. PERK regulates the proliferation and development of insulin-secreting beta-cell tumours in the endocrine pancreas of mice. PLoS ONE 2009; 4: e8008.
65. Puri P, Mirshahi F, Cheung O, et al. Activation and dysregulation of the unfolded protein response in non-alcoholic fatty liver disease. Gastroenterology 2008; 134: 568-76.
66. Galligan JJ, Smathers RL, Shearn CT, et al. Oxidative stress and the ER stress response in a murine model for early stage alcoholic liver disease. J Toxicol 2012; 2012: 207594.
67. Lee GH, Bhandary B, Lee EM, et al. The roles of ER stress and P450 2E1 in CCl4-induced steatosis. Int J Biochem Cell Biol 2011; 43: 1469-82.
68. Ji C, Kaplowitz N. Betaine decreases hyperhomocysteinemia, endoplasmic reticulum stress, and liver injury in alcohol-fed mice. Gastroenterology 2003; 124: 1488-99.
69. Zhong Y, Li Y, Chen Y, et al. Activation of endoplasmic reticulum stress by hyperglycemia is essential for müller cell-derived inflammatory cytokine production in diabetes. Diabetes 2012; 61: 492-504.
70. Gargalovic PS, Imura M, Zhang B, et al. Identification of inflammatory gene modules based on variations of human endothelial cell responses to oxidized lipids. PNAS 2006; 103: 12741-6.
71. Montiea HL, Kayalia F, Haezebroucka AJ, Rossia NF, DeGracia DJ. Renal ischemia and reperfusion activates the eIF2 alpha kinase PERK. Biochim Biophys Acta 2005; 1741: 314-24.
72. Bobrovnikova-Marjon EV, Marjon PL, Barbash O, Vander Jagt DL, Abcouwer SF. Expression of angiogenic factors vascular endothelial growth factor and interleukin-8/CXCL8 is highly responsive to ambient glutamine availability: role of nuclear factor-kappaB and activating protein-1. Cancer Res 2004; 64: 4858-69.
73. Porta C, Paglino C, Imarisio I, et al. Uncovering Pandora's vase: the growing problem of new toxicities from novel anticancer agents. The case of sorafenib and sunitinib. Clin Exp Med 2007; 7: 127-34.
74. Gresset SM, Shah SR. Intricacies of bevacizumab-induced toxicities and their management. Ann Pharmacother 2009; 43: 490-501.