Endoplasmic Reticulum Stress, NRF2 Signalling and Cardiovascular Diseases in a Nutshell

Current Atherosclerosis Reports

Volumn 19, Issue 8, 2017, Pages

  Mozzini, Chiara ^a   Cominacini, Luciano ^a   Garbin, Ulisse ^a   Fratta Pasini, Anna Maria ^a  

^a UNIVERSITY OF VERONA   (Italy)

Author keywords

Atherosclerotic plaque; Coronary artery disease; Diabetes; Endoplasmic reticulum stress; Oxidative stress

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR NRF2; NFE2L2 PROTEIN, HUMAN;

ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ATHEROSCLEROTIC PLAQUE; CARDIOVASCULAR DISEASE; CORONARY ARTERY DISEASE; DIABETES MELLITUS; DIABETOGENESIS; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM STRESS; HUMAN; INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MISFOLDING; PROTEIN UNFOLDING; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; ENDOPLASMIC RETICULUM; METABOLISM; PHYSIOLOGY;

ANIMALS; CARDIOVASCULAR DISEASES; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMANS; INFLAMMATION; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 85019979936     PISSN: 15233804     EISSN: 15346242     Source Type: Journal    
DOI: 10.1007/s11883-017-0669-7     Document Type: Review

References (65)

1. • Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. 2007;8:519–29. It is a complete review about the ER unfolded protein response.
2. Kaufman RJ. Orchestrating the unfolded protein response in health and disease. J Clin Invest. 2002;110:1389–98.
3. 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.
4. Glimcher LH. XBP1: the last two decades. Ann Rheum Dis. 2010;69:67–71.
5. Kaneko M, Niinuma Y, Nomura Y. Activation signal of nuclear factor-kB in response to endoplasmic reticulum stress is transduced via IRE1 and tumor necrosis factor receptor associated factor 2. Biol and Pharm Bull. 2003;10:931–5.
6. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol. 2001;21:1249–59.
7. Gorlach A, Klappa P, Kietzmann T. The endoplasmic reticulum: folding, calcium homeostasis, signalling, and redox control. Antioxid Redox Signal. 2006;8:1391–418.
8. Cullinan SB, Diehl JA. PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. J Biol Chem. 2004;279:20108–17.
9. Singh S, Vrishni S, Singh BK, Rahman I, Kakkar P. Nrf2/ARE stress response mechanism: a control point in oxidative stress mediated dysfunction and chronic inflammatory disease. Free Radic Res. 2010;44:1267–88.
10. Niture SK, Khatri R, Jaiswal AK. Regulation of Nrf2-an update. Free Radic Biol Med. 2014;66:36–44.
11. Kaspar JW, Niture SK, Jaiswal AK. Nrf2: INrf2 (Keap1) signalling in oxidative stress. FRBM. 2009;47:130–1309.
12. Ma Q. Transcriptional responses to oxidative stress: pathological and toxicological implications. Pharmacol Ther. 2010;125:376–93.
13. Motohashi H, Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med. 2004;10:549–57.
14. Ma Q, Battelli L, Hubbs AF. Multiorgan autoimmune inflammation, enhanced lymphoproliferation, and impaired homeostasis of reactive oxygen species in mice lacking the antioxidant-activated transcription factor Nrf2. Am J Pathol. 2006;168:1960–74.
15. Niture SK, Jain AK, Jaiswal AK. Antioxidant-induced modification of INrf2 cysteine 151 and PKC-delta-mediated phosphorylation of Nrf2 serine 40 are both required for stabilization and nuclear translocation of Nrf2 and increased drug resistance. J Cell Sci. 2009;122:4452–64.
16. Lee OH, Jain AK, Papusha V, Jaiswal AK. An auto-regulatory loop between stress sensors INrf2 and Nrf2 controls their cellular abundance. J Biol Chem. 2007;282:36412–20.
17. Hayes JD, Dinkova-Kostova AT. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends Biochem Sci. 2014;39:199–218.
18. Digaleh H, Kiaei M, Khodagholi F. Nrf2 and Nrf1 signalling and ER stress crosstalk: implication for proteasomal degradation and autophagy. Cell Mol Life Sci. 2013;70:4681–94.
19. Cullinan SB, Zhang D, Hannink M, Arvisais E, Kaufman RJ, Diehl JA. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol. 2003;23:7198–209.
20. Wang Q, Mora-Jensen H, Weniger MA, Perez-Galan P, Wolford C, Hai T. ERAD inhibitors integrate ER stress with an epigenetic mechanism to activate BH3-only protein NOXA in cancer cells. Proc Natl Acad Sci. 2009;106:2200–5.
21. •• Cominacini L, Mozzini C, Garbin U, Pasini A, Stranieri C, Solani E, Vallerio P, Tinelli IA, Fratta Pasini A. Endoplasmic reticulum stress and Nrf2 signalling in cardiovascular diseases. Free Radic Biol Med. 2015;S0891-5849(15):00238–5. This review has recently collected data with the aim to connect ER stress and Nrf2 signalling in cardiovascular diseases. It is innovative and updated.
22. Zhu HI, Jia Z, Misra BR, Zhang L, Cao Z, Yamamoto M. Nuclear factor E2-related factor 2-dependent myocardiac cytoprotection against oxidative and electrophilic stress. Cardiovasc Toxicol. 2008;8:71–85.
23. Hafstad AD, Nabeebaccus AA, Shah AM. Novel aspects of ROS signalling in heart failure. Basic Res Cardiol. 2013;108:359.
24. Hayes JD, McMahon M, Chowdhry S, Dinkova-Kostova AT. Cancer chemoprevention mechanisms mediated through the Keap1-Nrf2 pathway. Antioxid Redox Signal. 2010;13:1713–48.
25. Engin F, Hotamisligil GS. Restoring endoplasmic reticulum function by chemical chaperones: an emerging therapeutic approach for metabolic diseases. Diabetes Obes Metab. 2010;12:108–15.
26. Jeong WS, Jun M, Kong AN. Nrf2: a potential molecular target for cancer chemoprevention by natural compounds. Antioxid Redox Signal. 2005;8:99–106.
27. Venkatesan N. Curcumin attenuation of acute adriamycin myocardial toxicity in rats. Br J Pharmacol. 1998;124:425–7.
28. • Minamino T, Komuro I, Kitakaze M. Endoplasmic reticulum stress as a therapeutic target in cardiovascular disease. Circ Res. 2010;107:1071–82. This review open the new concept of the ER stress as a possible therapeutic target in cardiovascular diseases.
29. • Tabas I. The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ Res. 2010;107:839–50. This review explains the role of ER stress focusing on atherosclerosis.
30. Thorp E, Li G, Seimon T, Kuriakose G, Ron D, Tabas I. Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of Apoe−/− and Ldlr−/− mice lacking Chop. Cell Metab. 2009;9:474–81.
31. Praticò D, Iuliano L, Mauriello A, Spagnoli L, Lawson JA, Maclouf J. Localization of distinct F2-isoprostanes in human atherosclerotic lesions. J Clin Invest. 1997;100:2028–34.
32. Comporti M, Signorini C, Arezzini B, Vecchio D, Monaco B, Gardi C. F2-isoprostanes are not just markers of oxidative stress. Free Radic Biol Med. 2008;44:247–56.
33. Garbin U, Baggio E, Stranieri C, Pasini A, Manfro S, Mozzini C, Vallerio P, Lipari G, Merigo F, Guidi G, Cominacini L, Fratta PA. Expansion of necrotic core and shedding of Mertk receptor in human carotid plaques: a role for oxidized polyunsaturated fatty acids? Cardiovasc Res. 2013;97(1):125–33.
34. Garbin U, Stranieri C, Pasini A, Baggio E, Lipari G, Solani E, Mozzini C, Vallerio P, Cominacini L, Fratta Pasini AM. Do oxidized polyunsaturated fatty acids affect endoplasmic reticulum stress-induced apoptosis in human carotid plaques? Antioxid Redox Signal. 2014;21(6):850–8.
35. •• Cominacini L, Garbin U, Mozzini C, Stranieri C, Pasini A, Solani E, Tinelli IA, Pasini AF. The atherosclerotic plaque vulnerability: focus on the roles of oxidative and endoplasmic reticulum stress in orchestrating macrophage apoptosis and the formation of the necrotic core. Curr Med Chem. 2015;22(13):1565–72. This review underlines the role of oxidative and ER stress in the macrophage apoptosis and the formation of the necrotic core, giving possible explanation about the “vulnerable” plaque.
36. Lauber K, Blumenthal SG, Waibel M, Wesselborg S. Clearance of apoptotic cells; getting rid of the corpses. Mol Cell. 2004;14:277–87.
37. Hopkins PN. Molecular biology of atherosclerosis. Physiol Rev. 2013;93:1317–542.
38. Van Vré EA, Ait-Oufella H, Tedgui A, Mallat Z. Apoptotic cell death and efferocytosis in atherosclerosis. Arterioscler Thromb Vasc Biol. 2012;32:887–93.
39. Peter C, Wesselborg S, Herrmann M, Lauber K. Dangerous attraction: phagocyte recruitment and danger signals of apoptotic and necrotic cells. Apoptosis. 2010;15:1007–28.
40. Lisa S, Domingo B, Martinez J, Gilch S, Llopis JF, Schatzl HM, Gasset M. Failure of prion protein oxidative folding guides the formation of toxic transmembrane forms. J Biol Chem. 2012;287:36693–702.
41. Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal. 2007;9:2277–93.
42. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata D. Executive summary: heart disease and stroke statistics - 2013 update: a report from the American Heart Association. Circulation. 2013;127:143–52.
43. •• Myoishi M, Hao H, Minamino T, Watanabe K, Nishihira K, Hatakeyama K, Asada Y, Okada K, Ishibashi-Ueda H, Gabbiani G, Bochaton-Piallat ML, Mochizuki N, Kitakaze M. Increased endoplasmic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome. Circulation. 2007;116:1226–33. This article is the basis of the concept that ER stress is associated with the atherosclerotic plaque vulnerability. It is not so recent, but the study is well-conducted and the results are essential.
44. Hansson G. Inflammation, atherosclerosis and coronary artery disease. N Engl J Med. 2005;352:1685–95.
45. Cominacini L, Anselmi M, Garbin U, Fratta Pasini A, Stranieri C, Fusaro M, Nava C, Agostoni P, Keta D, Zardini P, Sawamura T, Lo Cascio V. Enhanced plasma levels of oxidized low-density lipoprotein increase circulating nuclear factor-kappa B activation in patients with unstable angina. J Am Coll Cardiol. 2005;46:799–806.
46. Anselmi M, Garbin U, Agostoni P, Fusaro M, Fratta Pasini A, Nava C, Keta D, Turri M, Zardini P, Vassanelli C, Lo Cascio V, Cominacini L. Plasma levels of oxidized-low-density lipoproteins are higher in patients with unstable angina and correlated with angiographic coronary complex plaque. Atherosclerosis. 2006;185:114–20.
47. Fratta Pasini A, Anselmi M, Garbin U, Franchi E, Stranieri C, Nava C, Boccioletti V, Vassanelli C, Cominacini L. Enhanced levels of oxidized low density lipoprotein prime monocytes to cytokine overproduction via upregulation of CD14 and toll-like receptor 4 in unstable angina. Arterioscler Thromb Vasc Biol. 2007;27:1991–7.
48. Mozzini C, Fratta Pasini A, Garbin U, Stranieri C, Pasini A, Vallerio P, Cominacini L. Increased endoplasmic reticulum stress and Nrf2 repression in peripheral blood mononuclear cells of patients with stable coronary artery disease. Free Radic Biol Med. 2014;68:178–85.
49. Sanson M, Augé N, Vindis C, Muller C, Bando Y, Thiers JC, Marachet MA, Zarkovic K, Sawa Y, Salvayre R, Nègre-Salvayre A. Oxidized low-density lipoproteins trigger endoplasmic reticulum stress in vascular cells: prevention by oxygen-regulated protein 150 expression. Circ Res. 2009;104:328–36.
50. Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell. 2010;140:900–17.
51. Kim H, Vaziri N. Contribution of impaired Nrf2–Keap1 pathway to oxidative stress and inflammation in chronic renal failure. Am J Physiol Renal Physiol. 2010;298:F662–71.
52. Suzuki M, Betsuyaku T, Ito Y, Nagai K, Nasuhara Y, Kaga K, Kondo S, Nishimura M. Down-regulated NF-E2 related factor 2 in pulmonary macrophages of aged smokers and patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2008;39:673–82.
53. Garbin U, Fratta Pasini A, Stranieri C, Cominacini M, Pasini A, Manfro S, Lugoboni F, Mozzini C, Guidi G, Faccini G. Cominacini L cigarette smoking blocks the protective expression of Nrf2/ARE pathway in peripheral mononuclear cells of young heavy smokers favouring inflammation. PLoS One. 2009;4:e8225.
54. • Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev. 2008;29:42–61. Important data about the relatively-new concept of a role of the ER in diabetes.
55. Wang J, Takeuchi T, Tanaka S, Kubo SK, Kayo T, Lu D, Takata K, Koizumi A, Izumi T. A mutation in the insulin 2 gene induces diabetes with severe pancreatic β cell dysfunction in the Mody mouse. J Clin Invest. 1999;103:27–37.
56. Inoue H, Tanizawa Y, Wasson J, Behn P, Kalidas K, Bernal-Mizrachi E, Mueckler M, Mueckler M, Marshall H, Donis-Kelelr H, Crock P, Rogers D, Mikuni M, Kumashiro H, Higashi K, Sobue G, Opka Y, Permutt MA. A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome). Nat Genet. 1998;20:143–8.
57. Delepine M, Nicolino M, Barrett T, Golamaully M, Lathrop GM, Julier C. EIF2AK3, encoding translation initiation factor 3, is mutated in patients with Wolcott-Rallison syndrome. Nat Gen. 2000;25:406–9.
58. Lipson KL, Fonseca SG, Ishigaki S, Nguyen LX, Foss E, Bortell R, et al. Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1. Cell Metab. 2006;4:245–54.
59. Elouil H, Bansellam M, Guiot Y, Vander Mierde D, Pascal SM, Schuit FC, Jonas JC. Acute nutrient regulation of unfolded protein response and integrated stress response in cultured rat pancreatic islets. Diabetologia. 2007;50:1442–52.
60. De la Cadena SG, Hernandez-Fonseca K, Camacho-Arroyo I, Massieu L. Glucose deprivation induces reticulum stress by the PERK pathway and caspase-7 and calpain-mediated caspase-12 activation. Apoptosis. 2014;19:414–27.
61. Laybutt DR, Preston AM, Akerfeldt MC, Kench JG, Busch AK, Biankin AV, Biden TJ. Endoplasmic reticulum stress contributes to b cell apoptosis in type 2 diabetes. Diabetologia. 2007;50:752–63.
62. Mozzini C, Garbin U, Stranieri C, Pasini A, Solani E, Tinelli IA, Cominacini L. Fratta Pasini AM endoplasmic reticulum stress and Nrf2 repression in circulating cells of type 2 diabetic patients without the recommended glycemic goals. Free Radic Res. 2015;49(3):244–52.
63. Del Rio D, Stewart AJ, Pellegrini N. A review of recent studies on malondialdehyde as a toxic molecule and biological marker of oxidative status. Nutr Metab Cardiovasc Dis. 2005;15:316–28.
64. Dandona P, Alajada A, Mohanty P, Ghanim H, Hsamouda W, Assian E, Ahmad S. Insulin inhibits intranuclear nuclear factor kB in mononuclear cells of obese subjects: evidence for an anti-inflammatory effect? J Clin Endocrinol Metab. 2001;86:3257–65.
65. Hasnain SZ, Prins JB, Mc Guckin MA. Oxidative and endoplasmatic reticulum stress in β-cell dysfunction in diabetes. J Mol Endocrinol. 2016;56:33–54.