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ER Stress-Induced Secretion of Proteins and Their Extracellular Functions in the Heart

Meyer, Bianca A., Doroudgar, Shirin·2020·Cells
DOI 10.3390/cells9092066PMC PMC7563782
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Abstract

Endoplasmic reticulum (ER) stress is a result of conditions that imbalance protein homeostasis or proteostasis at the ER, for example ischemia, and is a common event in various human pathologies, including the diseased heart. Cardiac integrity and function depend on the active secretion of mature proteins from a variety of cell types in the heart, a process that requires an intact ER environment for efficient protein folding and trafficking to the secretory pathway. As a consequence of ER stress, most protein secretion by the ER secretory pathway is decreased. Strikingly, there is a select group of proteins that are secreted in greater quantities during ER stress. ER stress resulting from the dysregulation of ER Ca2+ levels, for instance, stimulates the secretion of Ca2+-binding ER chaperones, especially GRP78, GRP94, calreticulin, and mesencephalic astrocyte-derived neurotrophic factor (MANF), which play a multitude of roles outside the cell, strongly depending on the cell type and tissue. Here we review current insights in ER stress-induced secretion of proteins, particularly from the heart, and highlight the extracellular functions of these proteins, ranging from the augmentation of cardiac cell viability to the modulation of pro- and anti-apoptotic, oncogenic, and immune-stimulatory cell signaling, cell invasion, extracellular proteostasis, and more. Many of the roles of ER stress-induced protein secretion remain to be explored in the heart. This article is part of a special issue entitled “The Role of Proteostasis Derailment in Cardiac Diseases.”

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Figure 1 Mechanisms of Cardiokine Secretion. Cardiokines (secreted proteins from cardiac cells), such as atrial natriuretic protein (ANP), made at the endoplasmic reticulum (ER), are conventionally transported to the Golgi apparatus, where they are modified and packaged into secretory vesicles and then to the plasma membrane, where they are released into the extracellular space, in what is known as classical protein secretion. Some cardiokines that enter the ER bypass the Golgi apparatus, in some cases entering membrane-bound organelles such as endosomes, on their way to the plasma membrane. Cardiokines secreted via the non-classical secretory pathway are synthesized on cytosolic ribosomes and traffic through various kinds of either vesicle- or nonvesicle-mediated pathways, without transiting through the ER and the Golgi apparatus. Non-classical protein secretion pathways include (1) incorporation into the lysosomal pathway, for example, interleukin 1β (IL1β), (2) cleavage and release from a membrane-bound precursor, for example, tumor necrosis factor α (TNFα), (3) release via exosomes derived from multivesicular bodies, for example, heat shock proteins (HSPs), (4) membrane blebbing and microvesicle shedding, for example, galectins, and (5) direct translocation of proteins across the plasma membrane through membrane transporters, for example fibroblast growth factor 1 and 2. Figures were created with BioRender.com.
Figure 1 Mechanisms of Cardiokine Secretion. Cardiokines (secreted proteins from cardiac cells), such as atrial natriuretic protein (ANP), made at the endoplasmic reticulum (ER), are conventionally transported to the Golgi apparatus, where they are modified and packaged into secretory vesicles and then to the plasma membrane, where they are released into the extracellular space, in what is known as classical protein secretion. Some cardiokines that enter the ER bypass the Golgi apparatus, in some cases entering membrane-bound organelles such as endosomes, on their way to the plasma membrane. Cardiokines secreted via the non-classical secretory pathway are synthesized on cytosolic ribosomes and traffic through various kinds of either vesicle- or nonvesicle-mediated pathways, without transiting through the ER and the Golgi apparatus. Non-classical protein secretion pathways include (1) incorporation into the lysosomal pathway, for example, interleukin 1β (IL1β), (2) cleavage and release from a membrane-bound precursor, for example, tumor necrosis factor α (TNFα), (3) release via exosomes derived from multivesicular bodies, for example, heat shock proteins (HSPs), (4) membrane blebbing and microvesicle shedding, for example, galectins, and (5) direct translocation of proteins across the plasma membrane through membrane transporters, for example fibroblast growth factor 1 and 2. Figures were created with BioRender.com.CC BY · PubMed Central
Figure 2 Regulation of ER Stress by the Unfolded Protein Response and Effects on Cardiokine Secretion. Perturbations of the ER environment result in the activation of the unfolded protein response, mediated by ER-resident integral membrane proteins ATF6 (activating transcription factor 6), PERK (protein kinase RNA (PKR)-like ER kinase), and IRE1α (inositol requiring enzyme 1). Upon ER stress, ATF6 translocates to the Golgi apparatus, where it is cleaved by site-1 and site-2 proteases (S1P, S2P), liberating an N-terminal fragment to translocate to the nucleus, where it is a potent and labile transcription factor that activates the transcription of ER chaperones and the transcription factor X-box binding protein 1 (XBP1). Activation of ATF6 may increase ER secretory capacity [35]. PERK dimerization activates autophosphorylation of its kinase domain, leading to phosphorylation of the α-subunit of translation initiation factor 2 (eIF2α) at Ser51. This inhibits global translational initiation, including translation of mRNAs encoding secretory proteins, reducing the load of unfolded proteins entering the ER. PERK activation also results in the induction of translation of selective mRNAs, including activating transcription factor 4 (ATF4), which activates the transcription of a wide range of genes involved in adaptation to stress conditions. Upon activation, IRE1α oligomerizes and carries out regulated IRE1-dependent decay (RIDD) of ER-targeted transcripts, as well as unconventional RNA splicing, by removing an intron from the XBP1 mRNA, allowing it to become translated into the functional transcription factor, XBP1s. XBP1s activates the transcription of ER chaperones, endoplasmic reticulum associated degradation (ERAD) genes, and genes involved in lipid synthesis.
Figure 2 Regulation of ER Stress by the Unfolded Protein Response and Effects on Cardiokine Secretion. Perturbations of the ER environment result in the activation of the unfolded protein response, mediated by ER-resident integral membrane proteins ATF6 (activating transcription factor 6), PERK (protein kinase RNA (PKR)-like ER kinase), and IRE1α (inositol requiring enzyme 1). Upon ER stress, ATF6 translocates to the Golgi apparatus, where it is cleaved by site-1 and site-2 proteases (S1P, S2P), liberating an N-terminal fragment to translocate to the nucleus, where it is a potent and labile transcription factor that activates the transcription of ER chaperones and the transcription factor X-box binding protein 1 (XBP1). Activation of ATF6 may increase ER secretory capacity [35]. PERK dimerization activates autophosphorylation of its kinase domain, leading to phosphorylation of the α-subunit of translation initiation factor 2 (eIF2α) at Ser51. This inhibits global translational initiation, including translation of mRNAs encoding secretory proteins, reducing the load of unfolded proteins entering the ER. PERK activation also results in the induction of translation of selective mRNAs, including activating transcription factor 4 (ATF4), which activates the transcription of a wide range of genes involved in adaptation to stress conditions. Upon activation, IRE1α oligomerizes and carries out regulated IRE1-dependent decay (RIDD) of ER-targeted transcripts, as well as unconventional RNA splicing, by removing an intron from the XBP1 mRNA, allowing it to become translated into the functional transcription factor, XBP1s. XBP1s activates the transcription of ER chaperones, endoplasmic reticulum associated degradation (ERAD) genes, and genes involved in lipid synthesis.CC BY · PubMed Central
Figure 3 Model of extracellular GRP78 and interacting protein, Cripto, modulation of TGFβ signaling. (A) Transforming growth factor beta (TGFβ) ligand binding to TGFβ receptors (TGFR) leads to activation of genes responsive to Smad2/3 signaling. (B) The 78 kDa glucose regulated protein (GRP78), an ER luminal Ca2+-binding chaperone, is secreted upon ER Ca2+ depletion. Secreted GRP78 is a co-factor required for Cripto-1 growth factor (Cripto) activation. Cripto activates Src, Ras/Raf/MAPK and PI3K/Akt pathways via a mechanism that remains unknown. (C) Cell surface Cripto/GRP78 interaction is required for Cripto modulation of TGFβ signaling.
Figure 3 Model of extracellular GRP78 and interacting protein, Cripto, modulation of TGFβ signaling. (A) Transforming growth factor beta (TGFβ) ligand binding to TGFβ receptors (TGFR) leads to activation of genes responsive to Smad2/3 signaling. (B) The 78 kDa glucose regulated protein (GRP78), an ER luminal Ca2+-binding chaperone, is secreted upon ER Ca2+ depletion. Secreted GRP78 is a co-factor required for Cripto-1 growth factor (Cripto) activation. Cripto activates Src, Ras/Raf/MAPK and PI3K/Akt pathways via a mechanism that remains unknown. (C) Cell surface Cripto/GRP78 interaction is required for Cripto modulation of TGFβ signaling.CC BY · PubMed Central

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Cites

Research works printed but not linked: 134

  1. Kakkar, 2010, Intramyocardial fibroblast myocyte communication, Circ. Res., 106, 47, 10.1161/CIRCRESAHA.109.207456 · DOI
  2. Zhou, 2016, Recounting Cardiac Cellular Composition, Circ. Res., 118, 368, 10.1161/CIRCRESAHA.116.308139 · DOI
  3. Doroudgar, 2011, The cardiokine story unfolds: Ischemic stress-induced protein secretion in the heart, Trends Mol. Med., 17, 207, 10.1016/j.molmed.2010.12.003 · DOI
  4. Lee, 2004, Bi-Directional Protein Transport Between the Er and Golgi, Annu. Rev. Cell Dev. Biol., 20, 87, 10.1146/annurev.cellbio.20.010403.105307 · DOI · Paper page
  5. Nickel, 2009, Mechanisms of regulated unconventional protein secretion, Nat. Rev. Mol. Cell Biol., 10, 148, 10.1038/nrm2617 · DOI
  6. Elvekrog, 2015, Dynamics of co-translational protein targeting, Curr. Opin. Chem. Biol., 29, 79, 10.1016/j.cbpa.2015.09.016 · DOI
  7. Cabrita, 2010, Protein folding on the ribosome, Curr. Opin. Struct. Biol., 20, 33, 10.1016/j.sbi.2010.01.005 · DOI
  8. Gerst, 2010, Addressing mRNAs to the ER: Cis sequences act up!, Trends Biochem. Sci., 35, 459, 10.1016/j.tibs.2010.02.006 · DOI
  9. Weis, 2013, Protein targeting to subcellular organelles via mRNA localization, Biochim. Biophys. Acta Mol. Cell Res., 1833, 260, 10.1016/j.bbamcr.2012.04.004 · DOI
  10. Cohen-Zontag, O., Baez, C., Lim, L.Q.J., Olender, T., Schirman, D., Dahary, D., Pilpel, Y., and Gerst, J.E. (2019). A secretion-enhancing cis regulatory targeting element (SECReTE) involved in mRNA localization and protein synthesis. PLoS Genet., 15. · DOI
  11. Palade, 1975, Intracellular Aspects of the Process of Protein Synthesis, Science, 189, 867, 10.1126/science.1096303 · DOI
  12. Bloch, 1986, Neonatal atria and ventricles secrete atrial natriuretic factor via tissue-specific secretory pathways, Cell, 47, 695, 10.1016/0092-8674(86)90512-X · DOI
  13. Sei, 1992, The cosecretional maturation of atrial natriuretic factor by primary atrial myocytes, Mol. Endocrinol., 6, 309
  14. Maack, 1996, Role of atrial natriuretic factor in volume control, Kidney Int., 49, 1732, 10.1038/ki.1996.257 · DOI
  15. Kim, 2018, Unconventional protein secretion— New insights into the pathogenesis and therapeutic targets of human diseases, J. Cell Sci., 131, jcs213686, 10.1242/jcs.213686 · DOI
  16. Nickel, 2008, Unconventional Mechanisms of Protein Transport to the Cell Surface of Eukaryotic Cells, Annu. Rev. Cell Dev. Biol., 24, 287, 10.1146/annurev.cellbio.24.110707.175320 · DOI
  17. Most, 2005, Distinct subcellular location of the Ca2+-binding protein S100A1 differentially modulates Ca2+-cycling in ventricular rat cardiomyocytes, J. Cell Sci., 118, 421, 10.1242/jcs.01614 · DOI
  18. Balch, 2008, Adapting proteostasis for disease intervention, Science, 319, 916, 10.1126/science.1141448 · DOI · Paper page
  19. Hipp, 2019, The proteostasis network and its decline in ageing, Nat. Rev. Mol. Cell Biol., 20, 421, 10.1038/s41580-019-0101-y · DOI · Paper page
  20. Treaster, S.B., Ridgway, I.D., Richardson, C.A., Gaspar, M.B., Chaudhuri, A.R., and Austad, S.N. (2014). Superior proteome stability in the longest lived animal. Age (Omaha). · DOI
  21. Henning, 2017, Proteostasis in cardiac health and disease, Nat. Rev. Cardiol., 14, 637, 10.1038/nrcardio.2017.89 · DOI · Paper page
  22. Christis, 2008, Protein folding includes oligomerization—Examples from the endoplasmic reticulum and cytosol, FEBS J., 275, 4700, 10.1111/j.1742-4658.2008.06590.x · DOI
  23. Michalak, 2009, Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum, Biochem. J., 417, 651, 10.1042/BJ20081847 · DOI
  24. Mohorko, 2011, Oligosaccharyltransferase: The central enzyme of N-linked protein glycosylation, J. Inherit. Metab. Dis., 34, 869, 10.1007/s10545-011-9337-1 · DOI
  25. Hudson, 2015, Oxidative protein folding: From thiol-disulfide exchange reactions to the redox poise of the endoplasmic reticulum, Free Radic. Biol. Med., 80, 171, 10.1016/j.freeradbiomed.2014.07.037 · DOI
  26. Gidalevitz, 2013, Orchestration of secretory protein folding by ER chaperones, Biochim. Biophys. Acta, 1833, 2410, 10.1016/j.bbamcr.2013.03.007 · DOI
  27. Brodsky, 2012, Cleaning Up: ER-associated degradation to the rescue, Cell, 151, 1163, 10.1016/j.cell.2012.11.012 · DOI
  28. Claessen, 2012, Protein quality control in the ER: Balancing the ubiquitin checkbook, Trends Cell Biol., 22, 22, 10.1016/j.tcb.2011.09.010 · DOI
  29. Chyn, 1979, In vitro synthesis of the Ca2+ transport ATPase by ribosomes bound to sarcoplasmic reticulum membranes, Proc. Natl. Acad. Sci. USA, 76, 1241, 10.1073/pnas.76.3.1241 · DOI
  30. Rossi, 2006, Sarcoplasmic reticulum: The dynamic calcium governor of muscle, Muscle Nerve, 33, 715, 10.1002/mus.20512 · DOI
  31. McLendon, 2015, Proteotoxicity and Cardiac Dysfunction, Circ. Res., 116, 1863, 10.1161/CIRCRESAHA.116.305372 · DOI
  32. Walter, 2011, The Unfolded Protein Response: From Stress Pathway to Homeostatic Regulation, Science, 334, 1081, 10.1126/science.1209038 · DOI
  33. Blackwood, 2019, Pharmacologic ATF6 activation confers global protection in widespread disease models by reprograming cellular proteostasis, Nat. Commun., 10, 187, 10.1038/s41467-018-08129-2 · DOI
  34. Kilberg, 2009, ATF4-dependent transcription mediates signaling of amino acid limitation, Trends Endocrinol. Metab., 20, 436, 10.1016/j.tem.2009.05.008 · DOI
  35. Plemper, 1999, Endoplasmic reticulum degradation. Reverse protein transport and its end in the proteasome, Mol. Biol. Rep., 26, 125, 10.1023/A:1006913215484 · DOI
  36. Ron, 2007, Signal integration in the endoplasmic reticulum unfolded protein response, Nat. Rev. Mol. Cell Biol., 8, 519, 10.1038/nrm2199 · DOI
  37. Harding, 1999, Protein translation and folding are coupled by an endoplasmic- reticulum-resident kinase, Nature, 397, 271, 10.1038/16729 · DOI · Paper page
  38. Shi, 1998, Identification and Characterization of Pancreatic Eukaryotic Initiation Factor 2 α-Subunit Kinase, PEK, Involved in Translational Control, Mol. Cell. Biol., 18, 7499, 10.1128/MCB.18.12.7499 · DOI
  39. Cox, 1993, Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase, Cell, 73, 1197, 10.1016/0092-8674(93)90648-A · DOI
  40. Tirasophon, 1998, A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells, Genes Dev., 12, 1812, 10.1101/gad.12.12.1812 · DOI
  41. Wang, 1998, Cloning of mammalian Ire1 reveals diversity in the ER stress responses, EMBO J., 17, 5708, 10.1093/emboj/17.19.5708 · DOI
  42. Niwa, 1999, A role for presenilin-1 in nuclear accumulation of Ire1 fragments and induction of the mammalian unfolded protein response, Cell, 99, 691, 10.1016/S0092-8674(00)81667-0 · DOI
  43. Zhu, 1997, Interaction of ATF6 and serum response factor, Mol. Cell. Biol., 17, 4957, 10.1128/MCB.17.9.4957 · DOI
  44. Yoshida, 1998, 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, 33741, 10.1074/jbc.273.50.33741 · DOI
  45. Haze, 1999, Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress, Mol. Biol. Cell, 10, 3787, 10.1091/mbc.10.11.3787 · DOI
  46. Wang, 2009, Role of the unfolded protein response regulator GRP78/BiP in development, cancer, and neurological disorders, Antioxidants Redox Signal., 11, 2307, 10.1089/ars.2009.2485 · DOI
  47. Adams, C.J., Kopp, M.C., Larburu, N., Nowak, P.R., and Ali, M.M.U. (2019). Structure and molecular mechanism of ER stress signaling by the unfolded protein response signal activator IRE1. Front. Mol. Biosci., 6. · DOI
  48. Lin, 2007, IRE1 signaling affects cell fate during the unfolded protein response, Science, 318, 944, 10.1126/science.1146361 · DOI
  49. Hetz, 2012, The unfolded protein response: Controlling cell fate decisions under ER stress and beyond, Nat. Rev. Mol. Cell Biol., 13, 89, 10.1038/nrm3270 · DOI
  50. Xu, 2005, Endoplasmic reticulum stress: Cell life and death decisions, J. Clin. Investig., 115, 2656, 10.1172/JCI26373 · DOI
  51. Chang, 2018, Coordination between Two Branches of the Unfolded Protein Response Determines Apoptotic Cell Fate, Mol. Cell, 71, 629.e5, 10.1016/j.molcel.2018.06.038 · DOI
  52. Hofmann, 2019, Protein Misfolding in Cardiac Disease, Circulation, 139, 2085, 10.1161/CIRCULATIONAHA.118.037417 · DOI
  53. Thuerauf, 2006, Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes, Circ. Res., 99, 275, 10.1161/01.RES.0000233317.70421.03 · DOI
  54. Doroudgar, 2009, Ischemia activates the ATF6 branch of the endoplasmic reticulum stress response, J. Biol. Chem., 284, 29735, 10.1074/jbc.M109.018036 · DOI
  55. Groenendyk, 2010, Biology of endoplasmic reticulum stress in the heart, Circ. Res., 107, 1185, 10.1161/CIRCRESAHA.110.227033 · DOI
  56. Buja, 2005, Myocardial ischemia and reperfusion injury, Cardiovasc. Pathol., 14, 170, 10.1016/j.carpath.2005.03.006 · DOI
  57. Doroudgar, 2013, New concepts of endoplasmic reticulum function in the heart: Programmed to conserve, J. Mol. Cell. Cardiol., 55, 85, 10.1016/j.yjmcc.2012.10.006 · DOI
  58. Hill, 2008, Cardiac plasticity, N. Engl. J. Med., 358, 1370, 10.1056/NEJMra072139 · DOI
  59. Blackwood, 2019, ATF6 Regulates Cardiac Hypertrophy by Transcriptional Induction of the mTORC1 Activator, Rheb, Circ. Res., 124, 79, 10.1161/CIRCRESAHA.118.313854 · DOI
  60. Blackwood, 2020, Proteomic analysis of the cardiac myocyte secretome reveals extracellular protective functions for the ER stress response, J. Mol. Cell. Cardiol., 143, 132, 10.1016/j.yjmcc.2020.04.012 · DOI
  61. Maurel, 2014, Getting RIDD of RNA: IRE1 in cell fate regulation, Trends Biochem. Sci., 39, 245, 10.1016/j.tibs.2014.02.008 · DOI
  62. Reid, 2014, The unfolded protein response triggers selective mRNA release from the endoplasmic reticulum, Cell, 158, 1362, 10.1016/j.cell.2014.08.012 · DOI
  63. Peters, 2011, Endoplasmic Reticulum Calcium Depletion Impacts Chaperone Secretion, Innate Immunity, and Phagocytic Uptake of Cells, J. Immunol., 187, 919, 10.4049/jimmunol.1100690 · DOI
  64. Genereux, 2015, Unfolded protein response-induced ER dj3 secretion links ER stress to extracellular proteostasis, EMBO J., 34, 4, 10.15252/embj.201488896 · DOI
  65. Bers, 2008, Calcium Cycling and Signaling in Cardiac Myocytes, Annu. Rev. Physiol., 70, 23, 10.1146/annurev.physiol.70.113006.100455 · DOI
  66. Davlouros, 2016, Calcium Homeostasis and Kinetics in Heart Failure, Med. Chem., 12, 151, 10.2174/157340641202160209094548 · DOI
  67. da Silva, D.C., Valentão, P., Andrade, P.B., and Pereira, D.M. (2020). Endoplasmic reticulum stress signaling in cancer and neurodegenerative disorders: Tools and strategies to understand its complexity. Pharmacol. Res., 155. · DOI
  68. Wetmore, 1996, Roles of the propeptide and metal ions in the folding and stability of the catalytic domain of stromelysin (matrix metalloproteinase 3), Biochemistry, 35, 6549, 10.1021/bi9530752 · DOI
  69. Halperin, 2014, The many functions of the endoplasmic reticulum chaperones and folding enzymes, IUBMB Life, 66, 318, 10.1002/iub.1272 · DOI
  70. Corbett, 1999, Ca2+ Regulation of Interactions between Endoplasmic Reticulum Chaperones, J. Biol. Chem., 274, 6203, 10.1074/jbc.274.10.6203 · DOI
  71. Ou, 1995, Conformational Changes Induced in the Endoplasmic Reticulum Luminal Domain of Calnexin by Mg-ATP and Ca, J. Biol. Chem., 270, 18051, 10.1074/jbc.270.30.18051 · DOI
  72. Suzuki, 1991, Regulating the retention of T-cell receptor alpha chain variants within the endoplasmic reticulum: Ca(2+)-dependent association with BiP, J. Cell Biol., 114, 189, 10.1083/jcb.114.2.189 · DOI
  73. Klappa, 2006, The Endoplasmic Reticulum: Folding, Calcium Homeostasis, Signaling, and Redox Control, Antioxid. Redox Signal., 8, 1391, 10.1089/ars.2006.8.1391 · DOI
  74. Glembotski, 2012, Mesencephalic astrocyte-derived neurotrophic factor protects the heart from ischemic damage and is selectively secreted upon sarco/endoplasmic reticulum calcium depletion, J. Biol. Chem., 287, 25893, 10.1074/jbc.M112.356345 · DOI
  75. Ni, 2011, Beyond the endoplasmic reticulum: Atypical GRP78 in cell viability, signalling and therapeutic targeting, Biochem. J., 434, 181, 10.1042/BJ20101569 · DOI
  76. Gold, 2010, Calreticulin: Non-endoplasmic reticulum functions in physiology and disease, FASEB J., 24, 665, 10.1096/fj.09-145482 · DOI
  77. Marzec, 2012, GRP94: An HSP90-like protein specialized for protein folding and quality control in the endoplasmic reticulum, Biochim. Biophys. Acta Mol. Cell Res., 1823, 774, 10.1016/j.bbamcr.2011.10.013 · DOI · Paper page
  78. Yang, 2019, The ER-localized Ca2+-binding protein calreticulin couples ER stress to autophagy by associating with microtubule-associated protein 1A/1B light chain 3, J. Biol. Chem., 294, 772, 10.1074/jbc.RA118.005166 · DOI
  79. Takemoto, 1992, Heavy chain binding protein (BiP/GRP78) and endoplasmin are exported from the endoplasmic reticulum in rat exocrine pancreatic cells, similar to protein disulfide-isomerase, Arch. Biochem. Biophys., 296, 129, 10.1016/0003-9861(92)90554-A · DOI
  80. Capitani, 2009, The KDEL receptor: New functions for an old protein, FEBS Lett., 583, 3863, 10.1016/j.febslet.2009.10.053 · DOI
  81. Pfeffer, 2007, Unsolved Mysteries in Membrane Traffic, Annu. Rev. Biochem., 76, 629, 10.1146/annurev.biochem.76.061705.130002 · DOI
  82. Zhang, 2010, Cell surface relocalization of the endoplasmic reticulum chaperone and unfolded protein response regulator GRP78/BiP, J. Biol. Chem., 285, 15065, 10.1074/jbc.M109.087445 · DOI
  83. Glembotski, 2011, Functions for the cardiomyokine, MANF, in cardioprotection, hypertrophy and heart failure, J. Mol. Cell. Cardiol., 51, 512, 10.1016/j.yjmcc.2010.10.008 · DOI
  84. Rangel, 2010, Cripto-1: An embryonic gene that promotes tumorigenesis, Future Oncol., 6, 1127, 10.2217/fon.10.68 · DOI
  85. Gray, 2012, Cripto/GRP78 modulation of the TGF-β pathway in development and oncogenesis, FEBS Lett., 586, 1836, 10.1016/j.febslet.2012.01.051 · DOI
  86. Shani, 2008, GRP78 and Cripto Form a Complex at the Cell Surface and Collaborate To Inhibit Transforming Growth Factor β Signaling and Enhance Cell Growth, Mol. Cell. Biol., 28, 666, 10.1128/MCB.01716-07 · DOI
  87. Kelber, 2009, Blockade of Cripto binding to cell surface GRP78 inhibits oncogenic Cripto signaling via MAPK/PI3K and Smad2/3 pathways, Oncogene, 28, 2324, 10.1038/onc.2009.97 · DOI
  88. Tsai, 2015, Characterization and mechanism of stress-induced translocation of 78-kilodalton glucose-regulated protein (GRP78) to the cell surface, J. Biol. Chem., 290, 8049, 10.1074/jbc.M114.618736 · DOI
  89. Selim, 2009, GRP78: A multifunctional receptor on the cell surface, Antioxidants Redox Signal., 11, 2299, 10.1089/ars.2009.2568 · DOI
  90. Bi, 2018, Endoplasmic Reticulum Chaperone GRP78 Protects Heart From Ischemia/Reperfusion Injury Through Akt Activation, Circ. Res., 122, 1545, 10.1161/CIRCRESAHA.117.312641 · DOI
  91. Bhattacharjee, 2005, Regulation of tissue factor-mediated initiation of the coagulatiion cascade by cell surface Grp78, Arterioscler. Thromb. Vasc. Biol., 25, 1737, 10.1161/01.ATV.0000173419.31242.56 · DOI
  92. Zhao, D., Feng, P., Sun, Y., Qin, Z., Zhang, Z., Tan, Y., Gao, E., Lau, W.B., Ma, X., and Yang, J. (2018). Cardiac-derived CTRP9 protects against myocardial ischemia/reperfusion injury via calreticulin-dependent inhibition of apoptosis article. Cell Death Dis., 9. · DOI
  93. Petrova, 2003, MANF, J. Mol. Neurosci., 20, 173, 10.1385/JMN:20:2:173 · DOI
  94. Palgi, 2009, Evidence that DmMANF is an invertebrate neurotrophic factor supporting dopaminergic neurons, Proc. Natl. Acad. Sci. USA, 106, 2429, 10.1073/pnas.0810996106 · DOI
  95. Neves, J., Zhu, J., Sousa-Victor, P., Konjikusic, M., Riley, R., Chew, S., Qi, Y., Jasper, H., and Lamba, D.A. (2016). Immune modulation by MANF promotes tissue repair and regenerative success in the retina. Science, 353. · DOI
  96. Lindström, R., Lindholm, P., Kallijärvi, J., Palgi, M., Saarma, M., and Heino, T.I. (2016). Exploring the Conserved Role of MANF in the Unfolded Protein Response in Drosophila melanogaster. PLoS ONE, 11. · DOI
  97. Tadimalla, 2008, Mesencephalic astrocyte-derived neurotrophic factor is an ischemia-inducible secreted endoplasmic reticulum stress response protein in the heart, Circ. Res., 103, 1249, 10.1161/CIRCRESAHA.108.180679 · DOI
  98. Bai, M., Vozdek, R., Hnízda, A., Jiang, C., Wang, B., Kuchar, L., Li, T., Zhang, Y., Wood, C., and Feng, L. (2018). Conserved roles of C. elegans and human MANFs in sulfatide binding and cytoprotection. Nat. Commun., 9. · DOI
  99. Araujo, 2018, GRP78 Is a Targetable Receptor on Cancer and Stromal Cells, EBioMedicine, 33, 2, 10.1016/j.ebiom.2018.06.030 · DOI
  100. Li, 2012, Glucose regulated protein 78: A critical link between tumor microenvironment and cancer hallmarks, Biochim. Biophys. Acta Rev. Cancer, 1826, 13, 10.1016/j.bbcan.2012.02.001 · DOI
  101. La, 2019, Tumor-secreted GRP78 facilitates the migration of macrophages into tumors by promoting cytoskeleton remodeling, Cell. Signal., 60, 1, 10.1016/j.cellsig.2019.04.004 · DOI
  102. Louessard, 2017, Activation of cell surface GRP78 decreases endoplasmic reticulum stress and neuronal death, Cell Death Differ., 24, 1518, 10.1038/cdd.2017.35 · DOI
  103. Vig, S., Buitinga, M., Rondas, D., Crèvecoeur, I., van Zandvoort, M., Waelkens, E., Eizirik, D.L., Gysemans, C., Baatsen, P., and Mathieu, C. (2019). Cytokine-induced translocation of GRP78 to the plasma membrane triggers a pro-apoptotic feedback loop in pancreatic beta cells. Cell Death Dis., 10. · DOI
  104. Panayi, 2006, BiP regulates autoimmune inflammation and tissue damage, Autoimmun. Rev., 5, 140, 10.1016/j.autrev.2005.08.006 · DOI
  105. Qin, K., Ma, S., Li, H., Wu, M., Sun, Y., Fu, M., Guo, Z., Zhu, H., Gong, F., and Lei, P. (2017). GRP78 impairs production of lipopolysaccharide-induced cytokines by interaction with CD14. Front. Immunol., 8. · DOI
  106. Triantafilou, 2002, GRP78, a Coreceptor for Coxsackievirus A9, Interacts with Major Histocompatibility Complex Class I Molecules Which Mediate Virus Internalization, J. Virol., 76, 633, 10.1128/JVI.76.2.633-643.2002 · DOI
  107. Jindadamrongwech, 2004, Identification of GRP 78 (BiP) as a liver cell expressed receptor element for dengue virus serotype 2, Arch. Virol., 149, 915, 10.1007/s00705-003-0263-x · DOI
  108. Honda, 2009, Molecular Chaperone BiP Interacts with Borna Disease Virus Glycoprotein at the Cell Surface, J. Virol., 83, 12622, 10.1128/JVI.01201-09 · DOI
  109. Nain, M., Mukherjee, S., Karmakar, S.P., Paton, A.W., Paton, J.C., Abdin, M.Z., Basu, A., Kalia, M., and Vrati, S. (2017). GRP78 Is an Important Host Factor for Japanese Encephalitis Virus Entry and Replication in Mammalian Cells. J. Virol., 91. · DOI
  110. Chu, 2018, Middle East respiratory syndrome coronavirus and bat coronavirus HKU9 both can utilize GRP78 for attachment onto host cells, J. Biol. Chem., 293, 11709, 10.1074/jbc.RA118.001897 · DOI
  111. Ibrahim, 2020, COVID-19 spike-host cell receptor GRP78 binding site prediction, J. Infect., 80, 554, 10.1016/j.jinf.2020.02.026 · DOI
  112. Somogyi, 2003, Calreticulin—An endoplasmic reticulum protein with calcium-binding activity is also found in the extracellular matrix, Matrix Biol., 22, 179, 10.1016/S0945-053X(02)00117-8 · DOI
  113. Tufi, 2008, Reduction of endoplasmic reticulum Ca2+ levels favors plasma membrane surface exposure of calreticulin, Cell Death Differ., 15, 274, 10.1038/sj.cdd.4402275 · DOI
  114. Greives, 2012, Exogenous calreticulin improves diabetic wound healing, Wound Repair Regen., 20, 715, 10.1111/j.1524-475X.2012.00822.x · DOI
  115. Obeid, 2007, Calreticulin exposure dictates the immunogenicity of cancer cell death, Nat. Med., 13, 54, 10.1038/nm1523 · DOI · Paper page
  116. Gardai, 2005, Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte, Cell, 123, 321, 10.1016/j.cell.2005.08.032 · DOI · Paper page
  117. Owusu, 2018, The role of the endoplasmic reticulum protein calreticulin in mediating TGF-β-stimulated extracellular matrix production in fibrotic disease, J. Cell Commun. Signal., 12, 289, 10.1007/s12079-017-0426-2 · DOI
  118. Han, A., Li, C., Zahed, T., Wong, M., Smith, I., Hoedel, K., Green, D., and Boiko, A.D. (2019). Calreticulin is a critical cell survival factor in malignant neoplasms. PLoS Biol., 17. · DOI
  119. Schcolnik-Cabrera, A., Oldak, B., Juárez, M., Cruz-Rivera, M., Flisser, A., and Mendlovic, F. (2019). Calreticulin in phagocytosis and cancer: Opposite roles in immune response outcomes. Apoptosis. · DOI
  120. Bowers, 2010, Re-Examination of CD91 Function in GRP94 (Glycoprotein 96) Surface Binding, Uptake, and Peptide Cross-Presentation, J. Immunol., 185, 6819, 10.4049/jimmunol.1000448 · DOI
  121. Bruneau, 1998, Participation of GRP94-related protein in secretion of pancreatic bile salt-dependent lipase and in its internalization by the intestinal epithelium, J. Cell Sci., 111, 2665, 10.1242/jcs.111.17.2665 · DOI
  122. Liu, 2003, Cell surface expression of an endoplasmic reticulum resident heat shock protein gp96 triggers MyD88-dependent systemic autoimmune diseases, Proc. Natl. Acad. Sci. USA, 100, 15824, 10.1073/pnas.2635458100 · DOI
  123. Danilova, T., and Lindahl, M. (2018). Emerging roles for mesencephalic astrocyte-derived neurotrophic factor (MANF) in pancreatic beta cells and diabetes. Front. Physiol., 9. · DOI
  124. 127. Kuhn, T.C., Knobel, J., Burkert-Rettenmaier, S., Li, X., Meyer, I.S., Jungmann, A., Sicklinger, F., Backs, J., Lasitschka, F., and Müller, O.J. (2020). Secretome Analysis of Cardiomyocytes Identifies PCSK6 (Proprotein Convertase Subtilisin/Kexin Type 6) as a Novel Player in Cardiac Remodeling After Myocardial Infarction. Circulation, 141, 1628–1644. · DOI
  125. Shen, 2005, ERdj3, a stress-inducible endoplasmic reticulum DnaJ homologue, serves as a cofactor for BiP’s interactions with unfolded substrates, Mol. Biol. Cell, 16, 40, 10.1091/mbc.e04-05-0434 · DOI
  126. Nizard, 2007, Stress-induced retrotranslocation of clusterin/ApoJ into the cytosol, Traffic, 8, 554, 10.1111/j.1600-0854.2007.00549.x · DOI
  127. Rybak, 1987, Angiogenin abolishes cell-free protein synthesis by specific ribonucleolytic inactivation of ribosomes, Proc. Natl. Acad. Sci. USA, 84, 8330, 10.1073/pnas.84.23.8330 · DOI
  128. Saxena, 1992, Angiogenin is a cytotoxic, tRNA-specific ribonuclease in the RNase A superfamily, J. Biol. Chem., 267, 21982, 10.1016/S0021-9258(19)36710-9 · DOI
  129. Greenway, 2006, ANG mutations segregate with familial and “sporadic” amyotrophic lateral sclerosis, Nat. Genet., 38, 411, 10.1038/ng1742 · DOI
  130. Kieran, 2008, Control of motoneuron survival by angiogenin, J. Neurosci., 28, 14056, 10.1523/JNEUROSCI.3399-08.2008 · DOI
  131. Kieran, 2009, Angiogenin protects motoneurons against hypoxic injury, Cell Death Differ., 16, 1238, 10.1038/cdd.2009.52 · DOI
  132. Skorupa, 2012, Motoneurons secrete angiogenin to induce RNA cleavage in astroglia, J. Neurosci., 32, 5024, 10.1523/JNEUROSCI.6366-11.2012 · DOI
  133. Yamasaki, 2009, Angiogenin cleaves tRNA and promotes stress-induced translational repression, J. Cell Biol., 185, 35, 10.1083/jcb.200811106 · DOI
  134. Mami, 2016, A novel extrinsic pathway for the unfolded protein response in the kidney, J. Am. Soc. Nephrol., 27, 2670, 10.1681/ASN.2015060703 · DOI

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Metadata

Authors
Meyer, B. A., & Doroudgar, S.
Affiliations
Department of Internal Medicine III (Cardiology, Angiology, and Pneumology), Heidelberg University Hospital, Im Neuenheimer Feld 669, 69120 Heidelberg, Germany
ORCID
Doroudgar, Shirin
Venue
Cells
Publisher
MDPI AG
Published
2020-09-10
Volume
9
Issue
9
Pages
2066
ISSN
2073-4409
DOI
10.3390/cells9092066
PMC
PMC7563782
Cited by
51
References
3
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
Deutsches Zentrum für Herz-Kreislaufforschung (FKZ 81X3500109)

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