Unfolded Protein Response Signaling in Hepatic Stem Cell Activation in Liver Fibrosis


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Abstract

Frequent exposure to various external and internal adverse forces (stresses) disrupts cell protein homeostasis through endoplasmic reticulum (ER) capacity saturation. This process leads to the unfolded protein response (UPR), which aims to re-establish/maintain optimal cellular equilibrium. This complex mechanism is involved in the pathogenesis of various disorders, such as metabolic syndrome, fibrotic diseases, neurodegeneration, and cancer, by altering cellular metabolic changes integral to activating the hepatic stellate cells (HSCs). The development of hepatic fibrosis is one of the consequences of UPR activation. Therefore, novel therapies that target the UPR pathway effectively and specifically are being studied. This article covers the involvement of the UPR signaling pathway in cellular damage in liver fibrosis. Investigating the pathogenic pathways related to the ER/UPR stress axis that contribute to liver fibrosis can help to guide future drug therapy approaches.

About the authors

Zohreh Salimi

Department of Clinical Biochemistry, School of Pharmacy & Pharmaceutical Sciences, Isfahan University of Medical Sciences

Email: info@benthamscience.net

Mehdi Rostami

Department of Clinical Biochemistry, Faculty of Medicine, Mashhad University of Medical Sciences

Email: info@benthamscience.net

Yaser Milasi

Department of Clinical Biochemistry, School of Pharmacy & Pharmaceutical Sciences, Isfahan University of Medical Sciences

Email: info@benthamscience.net

Alireza Mafi

Department of Clinical Biochemistry, School of Pharmacy & Pharmaceutical Sciences, Isfahan University of Medical Sciences

Email: info@benthamscience.net

Ramin Raoufinia

Medical Genetics and Molecular Medicine Department, School of Medicine, Mashhad University of Medical Science

Email: info@benthamscience.net

Amirhossein Kiani

Department of Immunology, Faculty of Medicine, Ahvaz Jundishapur University of Medical Sciences

Email: info@benthamscience.net

Fariba Sakhaei

Department of Clinical Biochemistry, School of Pharmacy & Pharmaceutical Sciences, Isfahan University of Medical Sciences

Email: info@benthamscience.net

Behrooz Ghezelbash

Department of Immunology, School of Medicine, Isfahan University of Medical Sciences

Email: info@benthamscience.net

Alexandra Butler

Research Department, Royal College of Surgeons in Ireland

Email: info@benthamscience.net

Maryam Mohammad-Sadeghipour

Department of Clinical Biochemistry, Afzalipoor Faculty of Medicine, Kerman University of Medical Sciences

Author for correspondence.
Email: info@benthamscience.net

Amirhossein Sahebkar

Biotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Science

Author for correspondence.
Email: info@benthamscience.net

References

  1. Ozgur, R.; Uzilday, B.; Iwata, Y.; Koizumi, N.; Turkan, I. Interplay between the unfolded protein response and reactive oxygen species: A dynamic duo. J. Exp. Bot., 2018, 69(14), 3333-3345. doi: 10.1093/jxb/ery040 PMID: 29415271
  2. Chen, X.; Cubillos-Ruiz, J.R. Endoplasmic reticulum stress signals in the tumour and its microenvironment. Nat. Rev. Cancer, 2021, 21(2), 71-88. doi: 10.1038/s41568-020-00312-2 PMID: 33214692
  3. Schröder, M. Endoplasmic reticulum stress responses. Cell. Mol. Life Sci., 2008, 65(6), 862-894. doi: 10.1007/s00018-007-7383-5 PMID: 18038217
  4. Kapoor, A.; Sanyal, A.J. Endoplasmic reticulum stress and the unfolded protein response. Clin. Liver Dis., 2009, 13(4), 581-590. doi: 10.1016/j.cld.2009.07.004 PMID: 19818306
  5. Aghaei, M.; Dastghaib, S.; Aftabi, S.; Aghanoori, M.R.; Alizadeh, J.; Mokarram, P.; Mehrbod, P.; Ashrafizadeh, M.; Zarrabi, A.; McAlinden, K.D.; Eapen, M.S.; Sohal, S.S.; Sharma, P.; Zeki, A.A.; Ghavami, S. The ER stress/UPR axis in chronic obstructive pulmonary disease and idiopathic pulmonary fibrosis. Life., 2020, 11(1), 1. doi: 10.3390/life11010001 PMID: 33374938
  6. Salminen, A.; Kaarniranta, K. ER stress and hormetic regulation of the aging process. Ageing Res. Rev., 2010, 9(3), 211-217. doi: 10.1016/j.arr.2010.04.003 PMID: 20416402
  7. Kim, I.; Xu, W.; Reed, J.C. Cell death and endoplasmic reticulum stress: Disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov., 2008, 7(12), 1013-1030. doi: 10.1038/nrd2755 PMID: 19043451
  8. Kim, S.R.; Lee, Y.C. Endoplasmic reticulum stress and the related signaling networks in severe asthma. Allergy Asthma Immunol. Res., 2015, 7(2), 106-117. doi: 10.4168/aair.2015.7.2.106 PMID: 25729617
  9. Kelsen, SG The unfolded protein response in chronic obstructive pulmonary disease. Ann. Am. Thorac. Soc., 2016, 13(S2)
  10. Wang, M.; Wey, S.; Zhang, Y.; Ye, R.; Lee, A.S. Role of the unfolded protein response regulator GRP78/BiP in development, cancer, and neurological disorders. Antioxid. Redox Signal., 2009, 11(9), 2307-2316. doi: 10.1089/ars.2009.2485 PMID: 19309259
  11. Walter, P.; Ron, D. The unfolded protein response: From stress pathway to homeostatic regulation. Science., 2011, 334(6059), 1081-1086. doi: 10.1126/science.1209038 PMID: 22116877
  12. Koo, J.H.; Lee, H.J.; Kim, W.; Kim, S.G. Endoplasmic reticulum stress in hepatic stellate cells promotes liver fibrosis via PERK-Mediated degradation of HNRNPA1 and up-regulation of SMAD2. Gastroenterology., 2016, 150(1), 181-193.e8. doi: 10.1053/j.gastro.2015.09.039 PMID: 26435271
  13. Li, X; Wang, Y; Wang, H; Huang, C; Huang, Y; Li, J Endoplasmic reticulum stress is the crossroads of autophagy, inflammation, and apoptosis signaling pathways and participates in liver fibrosis. Inflamm Res., 2015, 64(1), 1-7. doi: 10.1007/s00011-014-0772-y
  14. Maiers, J.; Malhi, H. Endoplasmic reticulum stress in metabolic liver diseases and hepatic fibrosis. Semin. Liver Dis., 2019, 39(2), 235-248. doi: 10.1055/s-0039-1681032 PMID: 30912096
  15. Iracheta-Vellve, A.; Petrasek, J.; Gyongyosi, B.; Satishchandran, A.; Lowe, P.; Kodys, K.; Catalano, D.; Calenda, C.D.; Kurt-Jones, E.A.; Fitzgerald, K.A.; Szabo, G. Endoplasmic reticulum stress-induced hepatocellular death pathways mediate liver injury and fibrosis via stimulator of interferon genes. J. Biol. Chem., 2016, 291(52), 26794-26805. doi: 10.1074/jbc.M116.736991 PMID: 27810900
  16. Dastghaib, S.; Shojaei, S.; Mostafavi-Pour, Z.; Sharma, P.; Patterson, J.B.; Samali, A.; Mokarram, P.; Ghavami, S. Simvastatin induces unfolded protein response and enhances temozolomide-induced cell death in glioblastoma cells. Cells, 2020, 9(11), 2339. doi: 10.3390/cells9112339 PMID: 33105603
  17. Dastghaib, S.; Kumar, P.S.; Aftabi, S.; Damera, G.; Dalvand, A.; Sepanjnia, A.; Kiumarsi, M.; Aghanoori, M.R.; Sohal, S.S.; Ande, S.R.; Alizadeh, J.; Mokarram, P.; Ghavami, S.; Sharma, P.; Zeki, A.A. Mechanisms targeting the unfolded protein response in asthma. Am. J. Respir. Cell Mol. Biol., 2021, 64(1), 29-38. doi: 10.1165/rcmb.2019-0235TR PMID: 32915643
  18. Arsène, F.; Tomoyasu, T.; Bukau, B. The heat shock response of Escherichia coli. Int. J. Food Microbiol., 2000, 55(1-3), 3-9. doi: 10.1016/S0168-1605(00)00206-3 PMID: 10791710
  19. Anckar, J.; Sistonen, L. Regulation of HSF1 function in the heat stress response: Implications in aging and disease. Annu. Rev. Biochem., 2011, 80(1), 1089-1115. doi: 10.1146/annurev-biochem-060809-095203 PMID: 21417720
  20. Yeganeh, B.; Rezaei Moghadam, A.; Tran, A.T.; Rahim, M.N.; Ande, S.R.; Hashemi, M.; Coombs, K.M.; Ghavami, S. Asthma and influenza virus infection:focusing on cell death and stress pathways in influenza virus replication. Iran. J. Allergy Asthma Immunol., 2013, 12(1), 1-17. PMID: 23454774
  21. Bertolotti, A.; Zhang, Y.; Hendershot, L.M.; Harding, H.P.; Ron, D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol., 2000, 2(6), 326-332. doi: 10.1038/35014014 PMID: 10854322
  22. Oikawa, D.; Kimata, Y.; Kohno, K.; Iwawaki, T. Activation of mammalian IRE1α upon ER stress depends on dissociation of BiP rather than on direct interaction with unfolded proteins. Exp. Cell Res., 2009, 315(15), 2496-2504. doi: 10.1016/j.yexcr.2009.06.009 PMID: 19538957
  23. Carrara, M.; Prischi, F.; Nowak, P.R.; Kopp, M.C.; Ali, M.M.U. Noncanonical binding of BiP ATPase domain to Ire1 and Perk is dissociated by unfolded protein CH1 to initiate ER stress signaling. eLife, 2015, 4, e03522. doi: 10.7554/eLife.03522 PMID: 25692299
  24. Mehrbod, P.; Ande, S.R.; Alizadeh, J.; Rahimizadeh, S.; Shariati, A.; Malek, H.; Hashemi, M.; Glover, K.K.M.; Sher, A.A.; Coombs, K.M.; Ghavami, S. The roles of apoptosis, autophagy and unfolded protein response in arbovirus, influenza virus, and HIV infections. Virulence., 2019, 10(1), 376-413. doi: 10.1080/21505594.2019.1605803 PMID: 30966844
  25. Veyron, S.; Peyroche, G.; Cherfils, J. FIC proteins: from bacteria to humans and back again. Pathog. Dis., 2018, 76(2) doi: 10.1093/femspd/fty012 PMID: 29617857
  26. Preissler, S.; Rato, C.; Perera, L.A.; Saudek, V.; Ron, D. FICD acts bifunctionally to AMPylate and de-AMPylate the endoplasmic reticulum chaperone BiP. Nat. Struct. Mol. Biol., 2017, 24(1), 23-29. doi: 10.1038/nsmb.3337 PMID: 27918543
  27. Ham, H.; Woolery, A.R.; Tracy, C.; Stenesen, D.; Krämer, H.; Orth, K. Unfolded protein response-regulated Drosophila Fic (dFic) protein reversibly AMPylates BiP chaperone during endoplasmic reticulum homeostasis. J. Biol. Chem., 2014, 289(52), 36059-36069. doi: 10.1074/jbc.M114.612515 PMID: 25395623
  28. McMahon, M.; Samali, A.; Chevet, E. Regulation of the unfolded protein response by noncoding RNA. Am. J. Physiol. Cell Physiol., 2017, 313(3), C243-C254. doi: 10.1152/ajpcell.00293.2016 PMID: 28637678
  29. Preissler, S.; Ron, D. Early events in the endoplasmic reticulum unfolded protein response. Cold Spring Harb. Perspect. Biol., 2019, 11(4), a033894. doi: 10.1101/cshperspect.a033894 PMID: 30396883
  30. Casey, A.K.; Moehlman, A.T.; Zhang, J.; Servage, K.A.; Krämer, H.; Orth, K. Fic-mediated deAMPylation is not dependent on homodimerization and rescues toxic AMPylation in flies. J. Biol. Chem., 2017, 292(51), 21193-21204. doi: 10.1074/jbc.M117.799296 PMID: 29089387
  31. Kimata, Y.; Ishiwata-Kimata, Y.; Ito, T.; Hirata, A.; Suzuki, T.; Oikawa, D.; Takeuchi, M.; Kohno, K. Two regulatory steps of ER-stress sensor Ire1 involving its cluster formation and interaction with unfolded proteins. J. Cell Biol., 2007, 179(1), 75-86. doi: 10.1083/jcb.200704166 PMID: 17923530
  32. Fu, J; Tao, T; Li, Z; Chen, Y; Li, J; Peng, L. The roles of ER stress in epilepsy: Molecular mechanisms and therapeutic implications. Biomed. Pharmacother., 2020, 131, 110658..
  33. Sundaram, A.; Plumb, R.; Appathurai, S.; Mariappan, M. The Sec61 translocon limits IRE1α signaling during the unfolded protein response. eLife, 2017, 6, e27187. doi: 10.7554/eLife.27187 PMID: 28504640
  34. Sundaram, A.; Appathurai, S.; Plumb, R.; Mariappan, M. Dynamic changes in complexes of IRE1α, PERK, and ATF6α during endoplasmic reticulum stress. Mol. Biol. Cell, 2018, 29(11), 1376-1388. doi: 10.1091/mbc.E17-10-0594 PMID: 29851562
  35. Sano, R.; Reed, J.C. ER stress-induced cell death mechanisms. Biochim. Biophys. Acta Mol. Cell Res., 2013, 1833(12), 3460-3470. doi: 10.1016/j.bbamcr.2013.06.028 PMID: 23850759
  36. Wang, M.; Kaufman, R.J. Protein misfolding in the endoplasmic reticulum as a conduit to human disease. Nature., 2016, 529(7586), 326-335. doi: 10.1038/nature17041 PMID: 26791723
  37. Rutkowski, D.T.; Arnold, S.M.; Miller, C.N.; Wu, J.; Li, J.; Gunnison, K.M.; Mori, K.; Sadighi Akha, A.A.; Raden, D.; Kaufman, R.J. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol., 2006, 4(11), e374. doi: 10.1371/journal.pbio.0040374 PMID: 17090218
  38. Lin, J.H.; Li, H.; Yasumura, D.; Cohen, H.R.; Zhang, C.; Panning, B.; Shokat, K.M.; LaVail, M.M.; Walter, P. IRE1 signaling affects cell fate during the unfolded protein response. Science., 2007, 318(5852), 944-949. doi: 10.1126/science.1146361 PMID: 17991856
  39. Deegan, S.; Saveljeva, S.; Gorman, A.M.; Samali, A. Stress-induced self-cannibalism: On the regulation of autophagy by endoplasmic reticulum stress. Cell. Mol. Life Sci., 2013, 70(14), 2425-2441. doi: 10.1007/s00018-012-1173-4 PMID: 23052213
  40. Tsuru, A.; Fujimoto, N.; Takahashi, S.; Saito, M.; Nakamura, D.; Iwano, M.; Iwawaki, T.; Kadokura, H.; Ron, D.; Kohno, K. Negative feedback by IRE1β optimizes mucin production in goblet cells. Proc. Natl. Acad. Sci., 2013, 110(8), 2864-2869. doi: 10.1073/pnas.1212484110 PMID: 23386727
  41. 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., 2009, 106(39), 16657-16662. doi: 10.1073/pnas.0903775106 PMID: 19805353
  42. Upton, J.P.; Wang, L.; Han, D.; Wang, E.S.; Huskey, N.E.; Lim, L.; Truitt, M.; McManus, M.T.; Ruggero, D.; Goga, A.; Papa, F.R.; Oakes, S.A. IRE1α cleaves select microRNAs during ER stress to derepress translation of proapoptotic Caspase-2. Science., 2012, 338(6108), 818-822. doi: 10.1126/science.1226191 PMID: 23042294
  43. Han, D.; Lerner, A.G.; Vande Walle, L.; Upton, J.P.; Xu, W.; Hagen, A.; Backes, B.J.; Oakes, S.A.; Papa, F.R. IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell., 2009, 138(3), 562-575. doi: 10.1016/j.cell.2009.07.017 PMID: 19665977
  44. Yeganeh, B.; Rezaei Moghadam, A.; Alizadeh, J.; Wiechec, E.; Alavian, S.M.; Hashemi, M.; Geramizadeh, B.; Samali, A.; Bagheri, L.K.; Post, M.; Peymani, P.; Coombs, K.M.; Ghavami, S. Hepatitis B and C virus-induced hepatitis: Apoptosis, autophagy, and unfolded protein response. World J. Gastroenterol., 2015, 21(47), 13225-13239. doi: 10.3748/wjg.v21.i47.13225 PMID: 26715805
  45. Yanagitani, K.; Imagawa, Y.; Iwawaki, T.; Hosoda, A.; Saito, M.; Kimata, Y.; Kohno, K. Cotranslational targeting of XBP1 protein to the membrane promotes cytoplasmic splicing of its own mRNA. Mol. Cell, 2009, 34(2), 191-200. doi: 10.1016/j.molcel.2009.02.033 PMID: 19394296
  46. Yoshida, H.; Matsui, T.; Yamamoto, A.; Okada, T.; Mori, K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell., 2001, 107(7), 881-891. doi: 10.1016/S0092-8674(01)00611-0 PMID: 11779464
  47. Lee, K.; Tirasophon, W.; Shen, X.; Michalak, M.; Prywes, R.; Okada, T.; Yoshida, H.; Mori, K.; Kaufman, R.J. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev., 2002, 16(4), 452-466. doi: 10.1101/gad.964702 PMID: 11850408
  48. Ghavami, S.; Sharma, P.; Yeganeh, B.; Ojo, O.O.; Jha, A.; Mutawe, M.M.; Kashani, H.H.; Los, M.J.; Klonisch, T.; Unruh, H.; Halayko, A.J. Airway mesenchymal cell death by mevalonate cascade inhibition: Integration of autophagy, unfolded protein response and apoptosis focusing on Bcl2 family proteins. Biochim. Biophys. Acta Mol. Cell Res., 2014, 1843(7), 1259-1271. doi: 10.1016/j.bbamcr.2014.03.006 PMID: 24637330
  49. Ghavami, S.; Yeganeh, B.; Stelmack, G.L.; Kashani, H.H.; Sharma, P.; Cunnington, R.; Rattan, S.; Bathe, K.; Klonisch, T.; Dixon, I.M.C.; Freed, D.H.; Halayko, A.J. Apoptosis, autophagy and ER stress in mevalonate cascade inhibition-induced cell death of human atrial fibroblasts. Cell Death Dis., 2012, 3(6), e330. doi: 10.1038/cddis.2012.61 PMID: 22717585
  50. Scorrano, L.; Oakes, S.A.; Opferman, J.T.; Cheng, E.H.; Sorcinelli, M.D.; Pozzan, T.; Korsmeyer, S.J. BAX and BAK regulation of endoplasmic reticulum Ca2+: A control point for apoptosis. Science., 2003, 300(5616), 135-139. doi: 10.1126/science.1081208 PMID: 12624178
  51. Bultynck, G.; Kiviluoto, S.; Henke, N.; Ivanova, H.; Schneider, L.; Rybalchenko, V.; Luyten, T.; Nuyts, K.; De Borggraeve, W.; Bezprozvanny, I.; Parys, J.B.; De Smedt, H.; Missiaen, L.; Methner, A. The C terminus of Bax inhibitor-1 forms a Ca2+-permeable channel pore. J. Biol. Chem., 2012, 287(4), 2544-2557. doi: 10.1074/jbc.M111.275354 PMID: 22128171
  52. Varadarajan, S.; Bampton, E.T.W.; Smalley, J.L.; Tanaka, K.; Caves, R.E.; Butterworth, M.; Wei, J.; Pellecchia, M.; Mitcheson, J.; Gant, T.W.; Dinsdale, D.; Cohen, G.M. A novel cellular stress response characterised by a rapid reorganisation of membranes of the endoplasmic reticulum. Cell Death Differ., 2012, 19(12), 1896-1907. doi: 10.1038/cdd.2012.108 PMID: 22955944
  53. Ishikawa, T.; Watanabe, N.; Nagano, M.; Kawai-Yamada, M.; Lam, E. Bax inhibitor-1: A highly conserved endoplasmic reticulum-resident cell death suppressor. Cell Death Differ., 2011, 18(8), 1271-1278. doi: 10.1038/cdd.2011.59 PMID: 21597463
  54. Gaddam, D.; Stevens, N.; Hollien, J. Comparison of mRNA localization and regulation during endoplasmic reticulum stress in Drosophila cells. Mol. Biol. Cell, 2013, 24(1), 14-20. doi: 10.1091/mbc.e12-06-0491 PMID: 23135994
  55. Hollien, J.; Weissman, J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science., 2006, 313(5783), 104-107. doi: 10.1126/science.1129631 PMID: 16825573
  56. Srinivasan, V.; Korhonen, L.; Lindholm, D. The unfolded protein response and autophagy as drug targets in neuropsychiatric disorders. Front. Cell. Neurosci., 2020, 14, 554548. doi: 10.3389/fncel.2020.554548 PMID: 33132844
  57. McGrath, E.; Logue, S.; Mnich, K.; Deegan, S.; Jäger, R.; Gorman, A.; Samali, A. The unfolded protein response in breast cancer. Cancers., 2018, 10(10), 344. doi: 10.3390/cancers10100344 PMID: 30248920
  58. Cnop, M.; Toivonen, S.; Igoillo-Esteve, M.; Salpea, P. Endoplasmic reticulum stress and eIF2α phosphorylation: The Achilles heel of pancreatic β cells. Mol. Metab., 2017, 6(9), 1024-1039. doi: 10.1016/j.molmet.2017.06.001 PMID: 28951826
  59. Okamura, K.; Kimata, Y.; Higashio, H.; Tsuru, A.; Kohno, K. Dissociation of Kar2p/BiP from an ER sensory molecule, Ire1p, triggers the unfolded protein response in yeast. Biochem. Biophys. Res. Commun., 2000, 279(2), 445-450. doi: 10.1006/bbrc.2000.3987 PMID: 11118306
  60. Amin-Wetzel, N.; Neidhardt, L.; Yan, Y.; Mayer, M.P.; Ron, D. Unstructured regions in IRE1α specify BiP-mediated destabilisation of the luminal domain dimer and repression of the UPR. eLife, 2019, 8, e50793. doi: 10.7554/eLife.50793 PMID: 31873072
  61. Wang, X.; Ron, D. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP Kinase. Science, 1996, 272(5266), 1347-1349. doi: 10.1126/science.272.5266.1347 PMID: 8650547
  62. Kim, B.J.; Ryu, S.W.; Song, B.J. JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J. Biol. Chem., 2006, 281(30), 21256-21265. doi: 10.1074/jbc.M510644200 PMID: 16709574
  63. Hetz, C.; Bernasconi, P.; Fisher, J.; Lee, A.H.; Bassik, M.C.; Antonsson, B.; Brandt, G.S.; Iwakoshi, N.N.; Schinzel, A.; Glimcher, L.H.; Korsmeyer, S.J. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science., 2006, 312(5773), 572-576. doi: 10.1126/science.1123480 PMID: 16645094
  64. Rizzuto, R.; Pinton, P.; Carrington, W.; Fay, F.S.; Fogarty, K.E.; Lifshitz, L.M.; Tuft, R.A.; Pozzan, T. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science., 1998, 280(5370), 1763-1766. doi: 10.1126/science.280.5370.1763 PMID: 9624056
  65. Roy, B.; Lee, A.S. The mammalian endoplasmic reticulum stress response element consists of an evolutionarily conserved tripartite structure and interacts with a novel stress-inducible complex. Nucleic Acids Res., 1999, 27(6), 1437-1443. doi: 10.1093/nar/27.6.1437 PMID: 10037803
  66. Sano, R.; Hou, Y.C.C.; Hedvat, M.; Correa, R.G.; Shu, C.W.; Krajewska, M.; Diaz, P.W.; Tamble, C.M.; Quarato, G.; Gottlieb, R.A.; Yamaguchi, M.; Nizet, V.; Dahl, R.; Thomas, D.D.; Tait, S.W.; Green, D.R.; Fisher, P.B.; Matsuzawa, S.I.; Reed, J.C. Endoplasmic reticulum protein BI-1 regulates Ca 2+ -mediated bioenergetics to promote autophagy. Genes Dev., 2012, 26(10), 1041-1054. doi: 10.1101/gad.184325.111 PMID: 22588718
  67. Cavener, D.R.; Gupta, S.; McGrath, B.C. PERK in beta cell biology and insulin biogenesis. Trends Endocrinol. Metab., 2010, 21(12), 714-721. doi: 10.1016/j.tem.2010.08.005 PMID: 20850340
  68. Delépine, M.; Nicolino, M.; Barrett, T.; Golamaully, M.; Mark Lathrop, G.; Julier, C. EIF2AK3, encoding translation initiation factor 2-α kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat. Genet., 2000, 25(4), 406-409. doi: 10.1038/78085 PMID: 10932183
  69. Deng, X.; Xiao, L.; Lang, W.; Gao, F.; Ruvolo, P.; May, W.S., Jr Novel role for JNK as a stress-activated Bcl2 kinase. J. Biol. Chem., 2001, 276(26), 23681-23688. doi: 10.1074/jbc.M100279200 PMID: 11323415
  70. Wek, R.C.; Cavener, D.R. Translational control and the unfolded protein response. Antioxid. Redox Signal., 2007, 9(12), 2357-2372. doi: 10.1089/ars.2007.1764 PMID: 17760508
  71. Mahameed, M.; Wilhelm, T.; Darawshi, O.; Obiedat, A.; Tommy, W.S.; Chintha, C.; Schubert, T.; Samali, A.; Chevet, E.; Eriksson, L.A.; Huber, M.; Tirosh, B. The unfolded protein response modulators GSK2606414 and KIRA6 are potent KIT inhibitors. Cell Death Dis., 2019, 10(4), 300. doi: 10.1038/s41419-019-1523-3 PMID: 30931942
  72. Puthalakath, H.; O’Reilly, L.A.; Gunn, P.; Lee, L.; Kelly, P.N.; Huntington, N.D.; Hughes, P.D.; Michalak, E.M.; McKimm-Breschkin, J.; Motoyama, N.; Gotoh, T.; Akira, S.; Bouillet, P.; Strasser, A. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell., 2007, 129(7), 1337-1349. doi: 10.1016/j.cell.2007.04.027 PMID: 17604722
  73. Li, G.; Mongillo, M.; Chin, K.T.; Harding, H.; Ron, D.; Marks, A.R.; Tabas, I. Role of ERO1-α–mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress–induced apoptosis. J. Cell Biol., 2009, 186(6), 783-792. doi: 10.1083/jcb.200904060 PMID: 19752026
  74. Dai, X.; Yan, X.; Wintergerst, K.A.; Cai, L.; Keller, B.B.; Tan, Y. Nrf2: Redox and metabolic regulator of stem cell state and function. Trends Mol. Med., 2020, 26(2), 185-200. doi: 10.1016/j.molmed.2019.09.007 PMID: 31679988
  75. Oyadomari, S.; Mori, M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ., 2004, 11(4), 381-389. doi: 10.1038/sj.cdd.4401373 PMID: 14685163
  76. Novoa, I.; Zeng, H.; Harding, H.P.; Ron, D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J. Cell Biol., 2001, 153(5), 1011-1022. doi: 10.1083/jcb.153.5.1011 PMID: 11381086
  77. McCullough, K.D.; Martindale, J.L.; Klotz, L.O.; Aw, T.Y.; Holbrook, N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol., 2001, 21(4), 1249-1259. doi: 10.1128/MCB.21.4.1249-1259.2001 PMID: 11158311
  78. Rainbolt, T.K.; Saunders, J.M.; Wiseman, R.L. Stress-responsive regulation of mitochondria through the ER unfolded protein response. Trends Endocrinol. Metab., 2014, 25(10), 528-537. doi: 10.1016/j.tem.2014.06.007 PMID: 25048297
  79. Shutt, T.E.; McBride, H.M. Staying cool in difficult times: Mitochondrial dynamics, quality control and the stress response. Biochim. Biophys. Acta Mol. Cell Res., 2013, 1833(2), 417-424. doi: 10.1016/j.bbamcr.2012.05.024 PMID: 22683990
  80. Wai, T.; Langer, T. Mitochondrial dynamics and metabolic regulation. Trends Endocrinol. Metab., 2016, 27(2), 105-117. doi: 10.1016/j.tem.2015.12.001 PMID: 26754340
  81. Lebeau, J.; Saunders, J.M.; Moraes, V.W.R.; Madhavan, A.; Madrazo, N.; Anthony, M.C.; Wiseman, R.L. The PERK arm of the unfolded protein response regulates mitochondrial morphology during acute endoplasmic reticulum stress. Cell Rep., 2018, 22(11), 2827-2836. doi: 10.1016/j.celrep.2018.02.055 PMID: 29539413
  82. Logue, S.E.; McGrath, E.P.; Cleary, P.; Greene, S.; Mnich, K.; Almanza, A.; Chevet, E.; Dwyer, R.M.; Oommen, A.; Legembre, P.; Godey, F.; Madden, E.C.; Leuzzi, B.; Obacz, J.; Zeng, Q.; Patterson, J.B.; Jäger, R.; Gorman, A.M.; Samali, A. Inhibition of IRE1 RNase activity modulates the tumor cell secretome and enhances response to chemotherapy. Nat. Commun., 2018, 9(1), 3267. doi: 10.1038/s41467-018-05763-8 PMID: 30111846
  83. Almanza, A.; Carlesso, A.; Chintha, C.; Creedican, S.; Doultsinos, D.; Leuzzi, B.; Luís, A.; McCarthy, N.; Montibeller, L.; More, S.; Papaioannou, A.; Püschel, F.; Sassano, M.L.; Skoko, J.; Agostinis, P.; de Belleroche, J.; Eriksson, L.A.; Fulda, S.; Gorman, A.M.; Healy, S.; Kozlov, A.; Muñoz-Pinedo, C.; Rehm, M.; Chevet, E.; Samali, A. Endoplasmic reticulum stress signalling - from basic mechanisms to clinical applications. FEBS J., 2019, 286(2), 241-278. doi: 10.1111/febs.14608 PMID: 30027602
  84. Hombach-Klonisch, S.; Mehrpour, M.; Shojaei, S.; Harlos, C.; Pitz, M.; Hamai, A.; Siemianowicz, K.; Likus, W.; Wiechec, E.; Toyota, B.D.; Hoshyar, R.; Seyfoori, A.; Sepehri, Z.; Ande, S.R.; Khadem, F.; Akbari, M.; Gorman, A.M.; Samali, A.; Klonisch, T.; Ghavami, S. Glioblastoma and chemoresistance to alkylating agents: Involvement of apoptosis, autophagy, and unfolded protein response. Pharmacol. Ther., 2018, 184, 13-41. doi: 10.1016/j.pharmthera.2017.10.017 PMID: 29080702
  85. Szegezdi, E.; Logue, S.E.; Gorman, A.M.; Samali, A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep., 2006, 7(9), 880-885. doi: 10.1038/sj.embor.7400779 PMID: 16953201
  86. Shojaei, S.; Suresh, M.; Klionsky, D.J.; Labouta, H.I.; Ghavami, S. Autophagy and SARS-CoV-2 infection: A possible smart targeting of the autophagy pathway. Virulence, 2020, 11(1), 805-810. doi: 10.1080/21505594.2020.1780088 PMID: 32567972
  87. Sureda, A.; Alizadeh, J.; Nabavi, S.F.; Berindan-Neagoe, I.; Cismaru, C.A.; Jeandet, P.; Łos, M.J.; Clementi, E.; Nabavi, S.M.; Ghavami, S. Endoplasmic reticulum as a potential therapeutic target for covid-19 infection management? Eur. J. Pharmacol., 2020, 882, 173288. doi: 10.1016/j.ejphar.2020.173288 PMID: 32561291
  88. Shore, G.C.; Papa, F.R.; Oakes, S.A. Signaling cell death from the endoplasmic reticulum stress response. Curr. Opin. Cell Biol., 2011, 23(2), 143-149. doi: 10.1016/j.ceb.2010.11.003 PMID: 21146390
  89. Senft, D.; Ronai, Z.A. UPR, autophagy, and mitochondria crosstalk underlies the ER stress response. Trends Biochem. Sci., 2015, 40(3), 141-148. doi: 10.1016/j.tibs.2015.01.002 PMID: 25656104
  90. B’chir, W.; Maurin, A.C.; Carraro, V.; Averous, J.; Jousse, C.; Muranishi, Y.; Parry, L.; Stepien, G.; Fafournoux, P.; Bruhat, A. The eIF2α/ATF4 pathway is essential for stress-induced autophagy gene expression. Nucleic Acids Res., 2013, 41(16), 7683-7699. doi: 10.1093/nar/gkt563 PMID: 23804767
  91. Wei, Y.; Pattingre, S.; Sinha, S.; Bassik, M.; Levine, B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol. Cell, 2008, 30(6), 678-688. doi: 10.1016/j.molcel.2008.06.001 PMID: 18570871
  92. Haberzettl, P.; Hill, B.G. Oxidized lipids activate autophagy in a JNK-dependent manner by stimulating the endoplasmic reticulum stress response. Redox Biol., 2013, 1(1), 56-64. doi: 10.1016/j.redox.2012.10.003 PMID: 24024137
  93. Adolph, T.E.; Tomczak, M.F.; Niederreiter, L.; Ko, H.J.; Böck, J.; Martinez-Naves, E.; Glickman, J.N.; Tschurtschenthaler, M.; Hartwig, J.; Hosomi, S.; Flak, M.B.; Cusick, J.L.; Kohno, K.; Iwawaki, T.; Billmann-Born, S.; Raine, T.; Bharti, R.; Lucius, R.; Kweon, M.N.; Marciniak, S.J.; Choi, A.; Hagen, S.J.; Schreiber, S.; Rosenstiel, P.; Kaser, A.; Blumberg, R.S. Paneth cells as a site of origin for intestinal inflammation. Nature., 2013, 503(7475), 272-276. doi: 10.1038/nature12599 PMID: 24089213
  94. Mandic, A.; Hansson, J.; Linder, S.; Shoshan, M.C. Cisplatin induces endoplasmic reticulum stress and nucleus-independent apoptotic signaling. J. Biol. Chem., 2003, 278(11), 9100-9106. doi: 10.1074/jbc.M210284200 PMID: 12509415
  95. Van de Craen, M.; Vandenabeele, P.; Declercq, W.; Van den Brande, I.; Van Loo, G.; Molemans, F.; Schotte, P.; Van Criekinge, W.; Beyaert, R.; Fiers, W. Characterization of seven murine caspase family members. FEBS Lett., 1997, 403(1), 61-69. doi: 10.1016/S0014-5793(97)00026-4 PMID: 9038361
  96. Xie, Q.; Khaoustov, V.I.; Chung, C.C.; Sohn, J.; Krishnan, B.; Lewis, D.E.; Yoffe, B. Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress–induced caspase-12 activation. Hepatology., 2002, 36(3), 592-601. doi: 10.1053/jhep.2002.35441 PMID: 12198651
  97. Morishima, N.; Nakanishi, K.; Tsuchiya, K.; Shibata, T.; Seiwa, E. Translocation of Bim to the endoplasmic reticulum (ER) mediates ER stress signaling for activation of caspase-12 during ER stress-induced apoptosis. J. Biol. Chem., 2004, 279(48), 50375-50381. doi: 10.1074/jbc.M408493200 PMID: 15452118
  98. Shojaei, S.; Koleini, N.; Samiei, E.; Aghaei, M.; Cole, L.K.; Alizadeh, J.; Islam, M.I.; Vosoughi, A.; Albokashy, M.; Butterfield, Y.; Marzban, H.; Xu, F.; Thliveris, J.; Kardami, E.; Hatch, G.M.; Eftekharpour, E.; Akbari, M.; Hombach-Klonisch, S.; Klonisch, T.; Ghavami, S. Simvastatin increases temozolomide-induced cell death by targeting the fusion of autophagosomes and lysosomes. FEBS J., 2020, 287(5), 1005-1034. doi: 10.1111/febs.15069 PMID: 31545550
  99. Kroemer, G.; Mariño, G.; Levine, B. Autophagy and the integrated stress response. Mol. Cell, 2010, 40(2), 280-293. doi: 10.1016/j.molcel.2010.09.023 PMID: 20965422
  100. Alizadeh, J.; Glogowska, A.; Thliveris, J.; Kalantari, F.; Shojaei, S.; Hombach-Klonisch, S.; Klonisch, T.; Ghavami, S. Autophagy modulates transforming growth factor beta 1 induced epithelial to mesenchymal transition in non-small cell lung cancer cells. Biochim. Biophys. Acta Mol. Cell Res., 2018, 1865(5), 749-768. doi: 10.1016/j.bbamcr.2018.02.007 PMID: 29481833
  101. Alizadeh, J.; Shojaei, S.; Sepanjnia, A.; Hashemi, M.; Eftekharpour, E.; Ghavami, S. Simultaneous detection of autophagy and epithelial to mesenchymal transition in the non-small cell lung cancer cells. Methods Mol. Biol., 2017, 1854, 87-103. doi: 10.1007/7651_2017_84 PMID: 29101677
  102. 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(37), 34287-34294. doi: 10.1074/jbc.M204973200 PMID: 12097332
  103. Hitomi, J.; Katayama, T.; Taniguchi, M.; Honda, A.; Imaizumi, K.; Tohyama, M. Apoptosis induced by endoplasmic reticulum stress depends on activation of caspase-3 via caspase-12. Neurosci. Lett., 2004, 357(2), 127-130. doi: 10.1016/j.neulet.2003.12.080 PMID: 15036591
  104. Sakurai, M.; Takahashi, G.; Abe, K.; Horinouchi, T.; Itoyama, Y.; Tabayashi, K. Endoplasmic reticulum stress induced in motor neurons by transient spinal cord ischemia in rabbits. J. Thorac. Cardiovasc. Surg., 2005, 130(3), 640-645. doi: 10.1016/j.jtcvs.2005.01.007 PMID: 16153907
  105. Tinhofer, I.; Anether, G.; Senfter, M.; Pfaller, K.; Bernhard, D.; Hara, M.; Greil, R. Stressful death of T-ALL tumor cells following treatment with the antitumor agent Tetrocarcin-A. FASEB J., 2002, 16(10), 1295-1297. doi: 10.1096/fj.02-0020fje PMID: 12060673
  106. Cullinan, S.B.; Diehl, J.A. Coordination of ER and oxidative stress signaling: The PERK/Nrf2 signaling pathway. Int. J. Biochem. Cell Biol., 2006, 38(3), 317-332. doi: 10.1016/j.biocel.2005.09.018 PMID: 16290097
  107. Belmont, P.J.; Chen, W.J.; Thuerauf, D.J.; Glembotski, C.C. Regulation of microRNA expression in the heart by the ATF6 branch of the ER stress response. J. Mol. Cell. Cardiol., 2012, 52(5), 1176-1182. doi: 10.1016/j.yjmcc.2012.01.017 PMID: 22326432
  108. Cullinan, S.B.; Diehl, J.A. PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. J. Biol. Chem., 2004, 279(19), 20108-20117. doi: 10.1074/jbc.M314219200 PMID: 14978030
  109. Dhar, D.; Baglieri, J.; Kisseleva, T.; Brenner, D.A. Mechanisms of liver fibrosis and its role in liver cancer. Exp. Biol. Med., 2020, 245(2), 96-108. doi: 10.1177/1535370219898141 PMID: 31924111
  110. Toosi, A.E. Liver fibrosis: Causes and methods of assessment, a review. Rev. Roum. Med. Intern., 2015, 53(4), 304-314.
  111. Li, S.; Tan, H.Y.; Wang, N.; Zhang, Z.J.; Lao, L.; Wong, C.W.; Feng, Y. The role of oxidative stress and antioxidants in liver diseases. Int. J. Mol. Sci., 2015, 16(11), 26087-26124. doi: 10.3390/ijms161125942 PMID: 26540040
  112. Cederbaum, A.I.; Lu, Y.; Wu, D. Role of oxidative stress in alcohol-induced liver injury. Arch. Toxicol., 2009, 83(6), 519-548. doi: 10.1007/s00204-009-0432-0 PMID: 19448996
  113. Czaja, A.J. Hepatic inflammation and progressive liver fibrosis in chronic liver disease. World J. Gastroenterol., 2014, 20(10), 2515-2532. doi: 10.3748/wjg.v20.i10.2515 PMID: 24627588
  114. Aboutwerat, A.; Pemberton, P.W.; Smith, A.; Burrows, P.C.; McMahon, R.F.T.; Jain, S.K.; Warnes, T.W. Oxidant stress is a significant feature of primary biliary cirrhosis. Biochim. Biophys. Acta Mol. Basis Dis., 2003, 1637(2), 142-150. doi: 10.1016/S0925-4439(02)00225-9 PMID: 12633902
  115. Tiao, M.M.; Lin, T.K.; Wang, P.W.; Chen, J.B.; Liou, C.W. The role of mitochondria in cholestatic liver injury. Chang Gung Med. J., 2009, 32(4), 346-353. PMID: 19664341
  116. Novo, E.; Cannito, S.; Paternostro, C.; Bocca, C.; Miglietta, A.; Parola, M. Cellular and molecular mechanisms in liver fibrogenesis. Arch. Biochem. Biophys., 2014, 548, 20-37. doi: 10.1016/j.abb.2014.02.015 PMID: 24631571
  117. Parola, M.; Marra, F.; Pinzani, M. Myofibroblast – like cells and liver fibrogenesis: Emerging concepts in a rapidly moving scenario. Mol. Aspects Med., 2008, 29(1-2), 58-66. doi: 10.1016/j.mam.2007.09.002 PMID: 18022682
  118. Friedman, S.L. Mechanisms of hepatic fibrogenesis. Gastroenterology, 2008, 134(6), 1655-1669. doi: 10.1053/j.gastro.2008.03.003 PMID: 18471545
  119. Czochra, P.; Klopcic, B.; Meyer, E.; Herkel, J.; Garcia-Lazaro, J.F.; Thieringer, F.; Schirmacher, P.; Biesterfeld, S.; Galle, P.R.; Lohse, A.W.; Kanzler, S. Liver fibrosis induced by hepatic overexpression of PDGF-B in transgenic mice. J. Hepatol., 2006, 45(3), 419-428. doi: 10.1016/j.jhep.2006.04.010 PMID: 16842882
  120. Jiang, J.X.; Török, N.J. Liver injury and the activation of the hepatic myofibroblasts. Curr. Pathobiol. Rep., 2013, 1(3), 215-223. doi: 10.1007/s40139-013-0019-6 PMID: 23977452
  121. Dorner, A.J.; Wasley, L.C.; Kaufman, R.J. Increased synthesis of secreted proteins induces expression of glucose-regulated proteins in butyrate-treated Chinese hamster ovary cells. J. Biol. Chem., 1989, 264(34), 20602-20607. doi: 10.1016/S0021-9258(19)47105-6 PMID: 2511206
  122. Hernández-Gea, V.; Hilscher, M.; Rozenfeld, R.; Lim, M.P.; Nieto, N.; Werner, S.; Devi, L.A.; Friedman, S.L. Endoplasmic reticulum stress induces fibrogenic activity in hepatic stellate cells through autophagy. J. Hepatol., 2013, 59(1), 98-104. doi: 10.1016/j.jhep.2013.02.016 PMID: 23485523
  123. Heindryckx, F.; Binet, F.; Ponticos, M.; Rombouts, K.; Lau, J.; Kreuger, J.; Gerwins, P. Endoplasmic reticulum stress enhances fibrosis through IRE 1α-mediated degradation of miR-150 and XBP -1 splicing. EMBO Mol. Med., 2016, 8(7), 729-744. doi: 10.15252/emmm.201505925 PMID: 27226027
  124. Kim, R.S.; Hasegawa, D.; Goossens, N.; Tsuchida, T.; Athwal, V.; Sun, X.; Robinson, C.L.; Bhattacharya, D.; Chou, H.I.; Zhang, D.Y.; Fuchs, B.C.; Lee, Y.; Hoshida, Y.; Friedman, S.L. The XBP1 arm of the unfolded protein response induces fibrogenic activity in hepatic stellate cells through autophagy. Sci. Rep., 2016, 6(1), 39342. doi: 10.1038/srep39342 PMID: 27996033
  125. Maiers, J.L.; Kostallari, E.; Mushref, M.; deAssuncao, T.M.; Li, H.; Jalan-Sakrikar, N.; Huebert, R.C.; Cao, S.; Malhi, H.; Shah, V.H. The unfolded protein response mediates fibrogenesis and collagen I secretion through regulating TANGO1 in mice. Hepatology, 2017, 65(3), 983-998. doi: 10.1002/hep.28921 PMID: 28039913
  126. Rutkowski, D.T.; Hegde, R.S. Regulation of basal cellular physiology by the homeostatic unfolded protein response. J. Cell Biol., 2010, 189(5), 783-794. doi: 10.1083/jcb.201003138 PMID: 20513765
  127. de Galarreta, M.R.; Navarro, A.; Ansorena, E.; Garzón, A.G.; Mòdol, T.; López-Zabalza, M.J.; Martínez-Irujo, J.J.; Iraburu, M.J. Unfolded protein response induced by Brefeldin A increases collagen type I levels in hepatic stellate cells through an IRE1α, p38 MAPK and Smad-dependent pathway. Biochim. Biophys. Acta Mol. Cell Res., 2016, 1863(8), 2115-2123. doi: 10.1016/j.bbamcr.2016.05.002 PMID: 27155082
  128. Wei, W.; Zhang, F.; Chen, H.; Tang, Y.; Xing, T.; Luo, Q.; Yu, L.; Du, J.; Shen, J.; Zhang, L. Toxoplasma gondii dense granule protein 15 induces apoptosis in choriocarcinoma JEG-3 cells through endoplasmic reticulum stress. Parasit. Vectors, 2018, 11(1), 251. doi: 10.1186/s13071-018-2835-3 PMID: 29665822
  129. Sato, H.; Shiba, Y.; Tsuchiya, Y.; Saito, M.; Kohno, K. 4µ8C inhibits insulin secretion independent of IRE1α RNase activity. Cell Struct. Funct., 2017, 42(1), 61-70. doi: 10.1247/csf.17002 PMID: 28321016
  130. Darling, N.J.; Cook, S.J. The role of MAPK signalling pathways in the response to endoplasmic reticulum stress. Biochim. Biophys. Acta Mol. Cell Res., 2014, 1843(10), 2150-2163. doi: 10.1016/j.bbamcr.2014.01.009 PMID: 24440275
  131. Huang, Y.; Li, X.; Wang, Y.; Wang, H.; Huang, C.; Li, J. Endoplasmic reticulum stress-induced hepatic stellate cell apoptosis through calcium-mediated JNK/P38 MAPK and Calpain/Caspase-12 pathways. Mol. Cell. Biochem., 2014, 394(1-2), 1-12. doi: 10.1007/s11010-014-2073-8 PMID: 24961950
  132. Zhao, G.; Hatting, M.; Nevzorova, Y.A.; Peng, J.; Hu, W.; Boekschoten, M.V.; Roskams, T.; Muller, M.; Gassler, N.; Liedtke, C.; Davis, R.J.; Cubero, F.J.; Trautwein, C. Jnk1 in murine hepatic stellate cells is a crucial mediator of liver fibrogenesis. Gut, 2014, 63(7), 1159-1172. doi: 10.1136/gutjnl-2013-305507 PMID: 24037431
  133. Shih, Y.C.; Chen, C.L.; Zhang, Y.; Mellor, R.L.; Kanter, E.M.; Fang, Y.; Wang, H.C.; Hung, C.T.; Nong, J.Y.; Chen, H.J.; Lee, T.H.; Tseng, Y.S.; Chen, C.N.; Wu, C.C.; Lin, S.L.; Yamada, K.A.; Nerbonne, J.M.; Yang, K.C. Endoplasmic reticulum protein TXNDC5 augments myocardial fibrosis by facilitating extracellular matrix protein folding and redox-sensitive cardiac fibroblast activation. Circ. Res., 2018, 122(8), 1052-1068. doi: 10.1161/CIRCRESAHA.117.312130 PMID: 29535165
  134. Groenendyk, J.; Lee, D.; Jung, J.; Dyck, J.R.B.; Lopaschuk, G.D.; Agellon, L.B.; Michalak, M. Inhibition of the unfolded protein response mechanism prevents cardiac fibrosis. PLoS One, 2016, 11(7), e0159682. doi: 10.1371/journal.pone.0159682 PMID: 27441395
  135. Wang, C.; Zhang, F.; Cao, Y.; Zhang, M.; Wang, A.; Xu, M.; Su, M.; Zhang, M.; Zhuge, Y. Etoposide induces apoptosis in activated human hepatic stellate cells via ER stress. Sci. Rep., 2016, 6(1), 34330. doi: 10.1038/srep34330 PMID: 27680712
  136. Li, Y.; Chen, Y.; Huang, H.; Shi, M.; Yang, W.; Kuang, J.; Yan, J. Autophagy mediated by endoplasmic reticulum stress enhances the caffeine-induced apoptosis of hepatic stellate cells. Int. J. Mol. Med., 2017, 40(5), 1405-1414. doi: 10.3892/ijmm.2017.3145 PMID: 28949381
  137. He, L.; Hou, X.; Fan, F.; Wu, H. Quercetin stimulates mitochondrial apoptosis dependent on activation of endoplasmic reticulum stress in hepatic stellate cells. Pharm. Biol., 2016, 54(12), 3237-3243. doi: 10.1080/13880209.2016.1223143 PMID: 27572285
  138. Tsubouchi, K.; Araya, J.; Minagawa, S.; Hara, H.; Ichikawa, A.; Saito, N.; Kadota, T.; Sato, N.; Yoshida, M.; Kurita, Y.; Kobayashi, K.; Ito, S.; Fujita, Y.; Utsumi, H.; Yanagisawa, H.; Hashimoto, M.; Wakui, H.; Yoshii, Y.; Ishikawa, T.; Numata, T.; Kaneko, Y.; Asano, H.; Yamashita, M.; Odaka, M.; Morikawa, T.; Nakayama, K.; Nakanishi, Y.; Kuwano, K. Azithromycin attenuates myofibroblast differentiation and lung fibrosis development through proteasomal degradation of NOX4. Autophagy., 2017, 13(8), 1420-1434. doi: 10.1080/15548627.2017.1328348 PMID: 28613983
  139. Kawamura, K.; Ichikado, K.; Yasuda, Y.; Anan, K.; Suga, M. Azithromycin for idiopathic acute exacerbation of idiopathic pulmonary fibrosis: a retrospective single-center study. BMC Pulm. Med., 2017, 17(1), 94. doi: 10.1186/s12890-017-0437-z PMID: 28629448

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