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ER Stress, Human Health and Role of Ca2+-Binding Chaperones

  • Sasirekha Narayanasamy
  • Gopala Krishna Aradhyam
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 13)

Abstract

The Endoplasmic Reticulum (ER) is a dynamic and versatile organelle involved in many critical functions of the cell. It is the major Ca2+ storehouse of the cell and the intra luminal [Ca2+] influences several cellular processes including synthesis of protein, lipids and sterols. Therefore, the concentration of Ca2+ is tightly controlled and buffered by several Ca2+-binding proteins in the ER. Several physiological and pathological disturbances can also perturb ER homeostasis, leading to the accumulation of misfolded or unfolded proteins, a condition termed as ER stress. The ER responds well to the stress by activating a series of signaling cascades known as unfolded protein response (UPR) in order to rescue ER functions. The adaptive response of the UPR pathway activates the transcription of several genes including molecular chaperones which aid in the folding of misfolded proteins. In addition to Ca2+-binding (that regulates their function), these ER-resident calcium binding proteins play a major role in folding, post translational processing and quality control of other nascent polypeptide chains and hence can be classified as calcium-binding chaperones (CaBC). The role of CaBC in the UPR pathway is quite indispensable and will be discussed in this chapter.

Keywords

Ca2+-Binding proteins Ca2+ Signaling Chaperones Endoplasmic reticulum ER stress Unfolded protein response 

Notes

Acknowledgements

The work of the authors presented herein was funded by DST, ICMR, CSIR and DBT. The authors also gratefully thank IIT Madras for the facility and financial support.

References

  1. Aghajani, A., Rahimi, A., Fadai, F., Ebrahimi, A., Najmabadi, H., & Ohadi, M. (2006). A point mutation at the calreticulin gene core promoter conserved sequence in a case of schizophrenia. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics, 141B, 294–295.CrossRefGoogle Scholar
  2. Ali, M. M., Bagratuni, T., Davenport, E. L., et al. (2011). Structure of the Ire1 autophosphorylation complex and implications for the unfolded protein response. The EMBO Journal, 30, 894–905.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Aragon, T., van Anken, E., Pincus, D., et al. (2009). Messenger RNA targeting to endoplasmic reticulum stress signalling sites. Nature, 457, 736–740.PubMedCrossRefGoogle Scholar
  4. Argon, Y., & Simen, B. B. (1999). GRP94, an ER chaperone with protein and peptide binding properties. Seminars in Cell & Developmental Biology, 10, 495–505.CrossRefGoogle Scholar
  5. Arosio, P., Michaels, T. C., Linse, S., et al. (2016). Kinetic analysis reveals the diversity of microscopic mechanisms through which molecular chaperones suppress amyloid formation. Nature Communications, 7, 10948.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Ashby, M. C., & Tepikin, A. V. (2001). ER calcium and the functions of intracellular organelles. Seminars in Cell & Developmental Biology, 12, 11–17.CrossRefGoogle Scholar
  7. Baksh, S., & Michalak, M. (1991). Expression of calreticulin in Escherichia coli and identification of its Ca2+ binding domains. The Journal of Biological Chemistry, 266, 21458–21465.PubMedGoogle Scholar
  8. Baksh, S., Burns, K., Andrin, C., & Michalak, M. (1995). Interaction of calreticulin with protein disulfide isomerase. The Journal of Biological Chemistry, 270, 31338–31344.PubMedCrossRefGoogle Scholar
  9. Baumann, O., & Walz, B. (2001). Endoplasmic reticulum of animal cells and its organization into structural and functional domains. International Review of Cytology, 205, 149–214.PubMedCrossRefGoogle Scholar
  10. Beckmann, R. P., Mizzen, L. E., & Welch, W. J. (1990). Interaction of Hsp 70 with newly synthesized proteins: Implications for protein folding and assembly. Science, 248, 850–854.PubMedCrossRefGoogle Scholar
  11. Bergeron, J. J., Brenner, M. B., Thomas, D. Y., & Williams, D. B. (1994). Calnexin: A membrane-bound chaperone of the endoplasmic reticulum. Trends in Biochemical Sciences, 19, 124–128.PubMedCrossRefGoogle Scholar
  12. Bernard-Marissal, N., Sunyach, C., Marissal, T., Raoul, C., & Pettmann, B. (2015). Calreticulin levels determine onset of early muscle denervation by fast motoneurons of ALS model mice. Neurobiology of Disease, 73, 130–136.PubMedCrossRefGoogle Scholar
  13. Berridge, M. J., Bootman, M. D., & Roderick, H. L. (2003). Calcium signalling: Dynamics, homeostasis and remodelling. Nature Reviews. Molecular Cell Biology, 4, 517–529.PubMedCrossRefGoogle Scholar
  14. Bonito-Oliva, A., Barbash, S., Sakmar, T. P., & Graham, W. V. (2017). Nucleobindin 1 binds to multiple types of pre-fibrillar amyloid and inhibits fibrillization. Scientific Reports, 7, 42880.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bourdi, M., Demady, D., Martin, J. L., et al. (1995). cDNA cloning and baculovirus expression of the human liver endoplasmic reticulum P58: Characterization as a protein disulfide isomerase isoform, but not as a protease or a carnitine acyltransferase. Archives of Biochemistry and Biophysics, 323, 397–403.PubMedCrossRefGoogle Scholar
  16. Braakman, I., Helenius, J., & Helenius, A. (1992). Role of ATP and disulphide bonds during protein folding in the endoplasmic reticulum. Nature, 356, 260–262.PubMedCrossRefGoogle Scholar
  17. Brodsky, J. L., & McCracken, A. A. (1997). ER-associated and proteasome mediated protein degradation: How two topologically restricted events came together. Trends in Cell Biology, 7, 151–156.PubMedCrossRefGoogle Scholar
  18. Bukau, B., & Horwich, A. L. (1998). The Hsp70 and Hsp60 chaperone machines. Cell, 92, 351–366.PubMedCrossRefGoogle Scholar
  19. Cao, S. S., & Kaufman, R. J. (2012). Unfolded protein response. Current Biology, 22, R622–R626.PubMedCrossRefGoogle Scholar
  20. Chen, Y., & Brandizzi, F. (2012). AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis. The Plant Journal, 69, 266–277.PubMedCrossRefGoogle Scholar
  21. Chen, Y., & Brandizzi, F. (2013). IRE1: ER stress sensor and cell fate executor. Trends in Cell Biology, 23, 547–555.PubMedCrossRefGoogle Scholar
  22. Chen, X., Shen, J., & Prywes, R. (2002). The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. The Journal of Biological Chemistry, 277, 13045–13052.PubMedCrossRefGoogle Scholar
  23. Chen, W., Shang, W. H., Adachi, Y., Hirose, K., Ferrari, D. M., & Kamata, T. (2008). A possible biochemical link between NADPH oxidase (Nox) 1 redox-signalling and ERp72. The Biochemical Journal, 416, 55–63.PubMedCrossRefGoogle Scholar
  24. Coe, H., & Michalak, M. (2009). Calcium binding chaperones of the endoplasmic reticulum. General Physiology and Biophysics, 28, F96–F103.PubMedGoogle Scholar
  25. Cooper, A. A., Gitler, A. D., Cashikar, A., et al. (2006). Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson’s models. Science, 313, 324–328.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Corbett, E. F., & Michalak, M. (2000). Calcium, a signaling molecule in the endoplasmic reticulum? Trends in Biochemical Sciences, 25, 307–311.PubMedCrossRefGoogle Scholar
  27. Corbett, E. F., Michalak, K. M., Oikawa, K., et al. (2000). The conformation of calreticulin is influenced by the endoplasmic reticulum luminal environment. The Journal of Biological Chemistry, 275, 27177–27185.PubMedGoogle Scholar
  28. Credle, J. J., Finer-Moore, J. S., Papa, F. R., Stroud, R. M., & Walter, P. (2005). On the mechanism of sensing unfolded protein in the endoplasmic reticulum. Proceedings of the National Academy of Sciences of the United States of America, 102, 18773–18784.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Delaunay, A., Bromberg, K. D., Hayashi, Y., et al. (2008). The ER-bound RING finger protein 5 (RNF5/RMA1) causes degenerative myopathy in transgenic mice and is deregulated in inclusion body myositis. PLoS One, 3, e1609.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Denisov, A. Y., Maattanen, P., Dabrowski, C., Kozlov, G., Thomas, D. Y., & Gehring, K. (2009). Solution structure of the bb’ domains of human protein disulfide isomerase. The FEBS Journal, 276, 1440–1449.PubMedCrossRefGoogle Scholar
  31. Denzel, A., Molinari, M., Trigueros, C., et al. (2002). Early postnatal death and motor disorders in mice congenitally deficient in calnexin expression. Molecular and Cellular Biology, 22, 7398–7404.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Dorner, A. J., Wasley, L. C., & Kaufman, R. J. (1990). Protein dissociation from GRP78 and secretion are blocked by depletion of cellular ATP levels. Proceedings of the National Academy of Sciences of the United States of America, 87, 7429–7432.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Eletto, D., Dersh, D., & Argon, Y. (2010). GRP94 in ER quality control and stress responses. Seminars in Cell & Developmental Biology, 21, 479–485.CrossRefGoogle Scholar
  34. Ellgaard, L., & Ruddock, L. W. (2005). The human protein disulphide isomerase family: Substrate interactions and functional properties. EMBO Reports, 6, 28–32.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Fels, D. R., & Koumenis, C. (2006). The PERK/eIF2alpha/ATF4 module of the UPR in hypoxia resistance and tumor growth. Cancer Biology & Therapy, 5, 723–728.CrossRefGoogle Scholar
  36. Ferri, K. F., & Kroemer, G. (2001). Organelle-specific initiation of cell death pathways. Nature Cell Biology, 3, E255–E263.PubMedCrossRefGoogle Scholar
  37. Fliegel, L., Burns, K., MacLennan, D. H., Reithmeier, R. A., & Michalak, M. (1989). Molecular cloning of the high affinity calcium-binding protein (calreticulin) of skeletal muscle sarcoplasmic reticulum. The Journal of Biological Chemistry, 264, 21522–21528.PubMedGoogle Scholar
  38. Forster, M. L., Sivick, K., Park, Y. N., Arvan, P., Lencer, W. I., & Tsai, B. (2006). Protein disulfide isomerase-like proteins play opposing roles during retrotranslocation. The Journal of Cell Biology, 173, 853–859.PubMedPubMedCentralCrossRefGoogle Scholar
  39. Frand, A. R., Cuozzo, J. W., & Kaiser, C. A. (2000). Pathways for protein disulphide bond formation. Trends in Cell Biology, 10, 203–210.PubMedCrossRefGoogle Scholar
  40. Gaut, J. R., & Hendershot, L. M. (1993). The modification and assembly of proteins in the endoplasmic reticulum. Current Opinion in Cell Biology, 5, 589–595.PubMedCrossRefGoogle Scholar
  41. Gonzalez-Perez, P., Woehlbier, U., Chian, R. J., et al. (2015). Identification of rare protein disulfide isomerase gene variants in amyotrophic lateral sclerosis patients. Gene, 566, 158–165.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Graham, W. V., Bonito-Oliva, A., & Sakmar, T. P. (2017). Update on Alzheimer’s disease therapy and prevention strategies. Annual Review of Medicine, 68, 413–430.PubMedCrossRefGoogle Scholar
  43. Groenendyk, J., Agellon, L. B., & Michalak, M. (2013). Coping with endoplasmic reticulum stress in the cardiovascular system. Annual Review of Physiology, 75, 49–67.PubMedCrossRefGoogle Scholar
  44. Gupta, R., Kapoor, N., Raleigh, D. P., & Sakmar, T. P. (2012). Nucleobindin 1 caps human islet amyloid polypeptide protofibrils to prevent amyloid fibril formation. Journal of Molecular Biology, 421, 378–389.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Haas, I. G., & Wabl, M. (1983). Immunoglobulin heavy chain binding protein. Nature, 306, 387–389.PubMedCrossRefGoogle Scholar
  46. Halperin, L., Jung, J., & Michalak, M. (2014). The many functions of the endoplasmic reticulum chaperones and folding enzymes. IUBMB Life, 66, 318–326.PubMedCrossRefGoogle Scholar
  47. Hammond, C., & Helenius, A. (1995). Quality control in the secretory pathway. Current Opinion in Cell Biology, 7, 523–529.PubMedCrossRefGoogle Scholar
  48. Harding, H. P., Zhang, Y., Bertolotti, A., Zeng, H., & Ron, D. (2000). Perk is essential for translational regulation and cell survival during the unfolded protein response. Molecular Cell, 5, 897–904.PubMedCrossRefGoogle Scholar
  49. Hartl, F. U., Martin, J., & Neupert, W. (1992). Protein folding in the cell: The role of molecular chaperones Hsp70 and Hsp60. Annual Review of Biophysics and Biomolecular Structure, 21, 293–322.PubMedCrossRefGoogle Scholar
  50. Hebert, D. N., & Molinari, M. (2007). In and out of the ER: Protein folding, quality control, degradation, and related human diseases. Physiological Reviews, 87, 1377–1408.PubMedCrossRefGoogle Scholar
  51. Helenius, A., & Aebi, M. (2004). Roles of N-linked glycans in the endoplasmic reticulum. Annual Review of Biochemistry, 73, 1019–1049.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hendershot, L. M. (2004). The ER function BiP is a master regulator of ER function. Mount Sinai Journal of Medicine, 71, 289–297.PubMedPubMedCentralGoogle Scholar
  53. Hetz, C. (2012). The unfolded protein response: Controlling cell fate decisions under ER stress and beyond. Nature Reviews. Molecular Cell Biology, 13, 89–102.PubMedCrossRefGoogle Scholar
  54. Hetz, C., & Glimcher, L. H. (2009). Fine-tuning of the unfolded protein response: Assembling the IRE1alpha interactome. Molecular Cell, 35, 551–561.PubMedPubMedCentralCrossRefGoogle Scholar
  55. Hetz, C., Martinon, F., Rodriguez, D., & Glimcher, L. H. (2011). The unfolded protein response: Integrating stress signals through the stress sensor IRE1alpha. Physiological Reviews, 91, 1219–1243.PubMedCrossRefGoogle Scholar
  56. Honore, B. (2009). The rapidly expanding CREC protein family: Members, localization, function, and role in disease. BioEssays, 31, 262–277.PubMedCrossRefGoogle Scholar
  57. Hurtley, S. M., & Helenius, A. (1989). Protein oligomerization in the endoplasmic reticulum. Annual Review of Cell Biology, 5, 277–307.PubMedCrossRefGoogle Scholar
  58. Irvine, A. G., Wallis, A. K., Sanghera, N., et al. (2014). Protein disulfide-isomerase interacts with a substrate protein at all stages along its folding pathway. PLoS One, 9, e82511.PubMedPubMedCentralCrossRefGoogle Scholar
  59. Jiang, J., Prasad, K., Lafer, E. M., & Sousa, R. (2005). Structural basis of interdomain communication in the Hsc70 chaperone. Molecular Cell, 20, 513–524.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Jin, H., Mimura, N., Kashio, M., Koseki, H., & Aoe, T. (2014). Late-onset of spinal neurodegeneration in knock-in mice expressing a mutant BiP. PLoS One, 9, e112837.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Kakiuchi, C., Ishiwata, M., Nanko, S., et al. (2005). Functional polymorphisms of HSPA5: Possible association with bipolar disorder. Biochemical and Biophysical Research Communications, 336, 1136–1143.PubMedCrossRefGoogle Scholar
  62. Kakiuchi, C., Ishiwata, M., Nanko, S., et al. (2007). Association analysis of HSP90B1 with bipolar disorder. Journal of Human Genetics, 52, 794–803.PubMedCrossRefGoogle Scholar
  63. Kakuyama, H., Soderberg, L., Horigome, K., et al. (2005). CLAC binds to aggregated Abeta and Abeta fragments, and attenuates fibril elongation. Biochemistry, 44, 15602–15609.PubMedCrossRefGoogle Scholar
  64. Kanuru, M., & Aradhyam, G. K. (2017). Chaperone-like activity of Calnuc prevents amyloid aggregation. Biochemistry, 56, 149–159.PubMedCrossRefGoogle Scholar
  65. Kanuru, M., Samuel, J. J., Balivada, L. M., & Aradhyam, G. K. (2009). Ion-binding properties of Calnuc, Ca2+ versus Mg2+-Calnuc adopts additional and unusual Ca2+-binding sites upon interaction with G-protein. The FEBS Journal, 276, 2529–2546.PubMedCrossRefGoogle Scholar
  66. Kaufman, R. J. (2002). Orchestrating the unfolded protein response in health and disease. The Journal of Clinical Investigation, 110, 1389–1398.PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kawano, J., Kotani, T., Ogata, Y., et al. (2000). CALNUC (nucleobindin) is localized in the Golgi apparatus in insect cells. European Journal of Cell Biology, 79, 208–217.PubMedCrossRefGoogle Scholar
  68. Kim, I., Xu, W., & Reed, J. C. (2008). Cell death and endoplasmic reticulum stress: Disease relevance and therapeutic opportunities. Nature Reviews Drug Discovery, 7, 1013–1030.PubMedCrossRefGoogle Scholar
  69. Klappa, P., Ruddock, L. W., Darby, N. J., & Freedman, R. B. (1998). The b’ domain provides the principal peptide-binding site of protein disulfide isomerase but all domains contribute to binding of misfolded proteins. The EMBO Journal, 17, 927–935.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Korennykh, A. V., Egea, P. F., Korostelev, A. A., et al. (2009). The unfolded protein response signals through high-order assembly of Ire1. Nature, 457, 687–693.PubMedCrossRefGoogle Scholar
  71. Kozlov, G., Maattanen, P., Schrag, J. D., et al. (2006). Crystal structure of the bb’ domains of the protein disulfide isomerase ERp57. Structure, 14, 1331–1339.PubMedCrossRefGoogle Scholar
  72. Kozlov, G., Määttänen, P., Schrag, J. D., et al. (2009). Structure of the noncatalytic domains and global fold of the protein disulfide isomerase ERp72. Structure, 17, 651–659.PubMedCrossRefGoogle Scholar
  73. Kozlov, G., Bastos-Aristizabal, S., Maattanen, P., et al. (2010). Structural basis of cyclophilin B binding by the calnexin/calreticulin P-domain. The Journal of Biological Chemistry, 285, 35551–35557.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Kozutsumi, Y., Segal, M., Normington, K., Gething, M. J., & Sambrook, J. (1988). The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature, 332, 462–464.PubMedCrossRefGoogle Scholar
  75. Kraus, A., Groenendyk, J., Bedard, K., et al. (2010). Calnexin deficiency leads to dysmyelination. The Journal of Biological Chemistry, 285, 18928–18938.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Krause, K. H., & Michalak, M. (1997). Calreticulin. Cell, 88, 439–443.PubMedCrossRefGoogle Scholar
  77. Lavoie, C., Meerloo, T., Lin, P., & Farquhar, M. G. (2002). Calnuc, an EF-hand Ca2+-binding protein, is stored and processed in the Golgi and secreted by the constitutive-like pathway in AtT20 cells. Molecular Endocrinology, 16, 2462–2474.PubMedCrossRefGoogle Scholar
  78. Leach, M. R., Cohen-Doyle, M. F., Thomas, D. Y., & Williams, D. B. (2002). Localization of the lectin, ERp57 binding, and polypeptide binding sites of calnexin and calreticulin. The Journal of Biological Chemistry, 277, 29686–29697.PubMedCrossRefGoogle Scholar
  79. Lebeche, D., Lucero, H. A., & Kaminer, B. (1994). Calcium binding properties of rabbit liver protein disulfide isomerase. Biochemical and Biophysical Research Communications, 202, 556–561.PubMedCrossRefGoogle Scholar
  80. Lee, A. H., Iwakoshi, N. N., & Glimcher, L. H. (2003). XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Molecular and Cellular Biology, 23, 7448–7459.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Lee, J. H., Kwon, E. J., & Kim, D. H. (2013). Calumenin has a role in the alleviation of ER stress in neonatal rat cardiomyocytes. Biochemical and Biophysical Research Communications, 439, 327–332.PubMedCrossRefGoogle Scholar
  82. Leustek, T., Toledo, H., Brot, N., & Weissbach, H. (1991). Calcium-dependent autophosphorylation of the glucose-regulated protein, Grp78. Archives of Biochemistry and Biophysics, 289, 256–261.PubMedCrossRefGoogle Scholar
  83. Li, Y., & Camacho, P. (2004). Ca2+-dependent redox modulation of SERCA2b by ERp57. The Journal of Cell Biology, 164, 35–46.PubMedCrossRefGoogle Scholar
  84. Li, G., Mongillo, M., Chin, K. T., et al. (2009). Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. The Journal of Cell Biology, 186, 783–792.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Lievremont, J. P., Rizzuto, R., Hendershot, L., & Meldolesi, J. (1997). BiP, a major chaperone protein of the endoplasmic reticulum lumen, plays a direct and important role in the storage of the rapidly exchanging pool of Ca2+. The Journal of Biological Chemistry, 272, 30873–30879.PubMedCrossRefGoogle Scholar
  86. Lin, P., Le-Niculescu, H., Hofmeister, R., et al. (1998). The mammalian calcium-binding protein, nucleobindin (CALNUC), is a Golgi resident protein. The Journal of Cell Biology, 141, 1515–1527.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Lin, P., Yao, Y., Hofmeister, R., Tsien, R. Y., & Farquhar, M. G. (1999). Overexpression of CALNUC (nucleobindin) increases agonist and thapsigargin releasable Ca2+ storage in the Golgi. The Journal of Cell Biology, 145, 279–289.PubMedPubMedCentralCrossRefGoogle Scholar
  88. Lin, J. H., Li, H., Yasumura, D., et al. (2007a). IRE1 signaling affects cell fate during the unfolded protein response. Science, 318, 944–949.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Lin, P., Li, F., Zhang, Y. W., et al. (2007b). Calnuc binds to Alzheimer's beta-amyloid precursor protein and affects its biogenesis. Journal of Neurochemistry, 100, 1505–1514.PubMedGoogle Scholar
  90. Lipskaia, L., Hulot, J. S., & Lompre, A. M. (2009). Role of sarco/endoplasmic reticulum calcium content and calcium ATPase activity in the control of cell growth and proliferation. Pflügers Archiv, 457, 673–685.PubMedCrossRefGoogle Scholar
  91. Logue, S. E., & Gorman, A. M. (2013). Current Concepts in ER Stress-Induced Apoptosis. Journal of Carcinogenesis & Mutagenesis, s6.Google Scholar
  92. Lucero, H. A., & Kaminer, B. (1999). The role of calcium on the activity of ER calcistorin/protein-disulfide isomerase and the significance of the Cterminal and its calcium binding. A comparison with mammalian protein-disulfide isomerase. The Journal of Biological Chemistry, 274, 3243–3251.PubMedCrossRefGoogle Scholar
  93. Luo, S., Mao, C., Lee, B., & Lee, A. S. (2006). GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Molecular and Cellular Biology, 26, 5688–5697.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Ma, Y., & Hendershot, L. M. (2004). ER chaperone functions during normal and stress conditions. Journal of Chemical Neuroanatomy, 28, 51–65.PubMedPubMedCentralCrossRefGoogle Scholar
  95. Ma, T., & Klann, E. (2014). PERK: A novel therapeutic target for neurodegenerative diseases? Alzheimer’s Research & Therapy, 6, 30.CrossRefGoogle Scholar
  96. Maattanen, P., Kozlov, G., Gehring, K., & Thomas, D. Y. (2006). ERp57 and PDI: Multifunctional protein disulfide isomerases with similar domain architectures but differing substrate-partner associations. Biochemistry and Cell Biology, 84, 881–889.PubMedCrossRefGoogle Scholar
  97. Macer, D. R., & Koch, G. L. (1988). Identification of a set of calcium-binding proteins in reticuloplasm, the luminal content of the endoplasmic reticulum. Journal of Cell Science, 91, 61–70.PubMedGoogle Scholar
  98. Malhotra, J. D., & Kaufman, R. J. (2007a). The endoplasmic reticulum and the unfolded protein response. Seminars in Cell & Developmental Biology, 18, 716–731.CrossRefGoogle Scholar
  99. Malhotra, J. D., & Kaufman, R. J. (2007b). Endoplasmic reticulum stress and oxidative stress: A vicious cycle or a double-edged sword? Antioxidants & Redox Signaling, 9, 2277–2293.CrossRefGoogle Scholar
  100. Mansson, C., Kakkar, V., Monsellier, E., et al. (2014). DNAJB6 is a peptide-binding chaperone which can suppress amyloid fibrillation of polyglutamine peptides at substoichiometric molar ratios. Cell Stress & Chaperones, 19, 227–239.CrossRefGoogle Scholar
  101. Mao, C., Wang, M., Luo, B., et al. (2010). Targeted mutation of the mouse Grp94 gene disrupts development and perturbs endoplasmic reticulum stress signaling. PLoS One, 5, e10852.PubMedPubMedCentralCrossRefGoogle Scholar
  102. Marciniak, S. J., Yun, C. Y., Oyadomari, S., et al. (2004). CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes & Development, 18, 3066–3077.CrossRefGoogle Scholar
  103. Martin, V., Groenendyk, J., Steiner, S. S., et al. (2006). Identification by mutational analysis of amino acid residues essential in the chaperone function of calreticulin. The Journal of Biological Chemistry, 281, 2338–2346.PubMedCrossRefGoogle Scholar
  104. Mayer, M. P., & Bukau, B. (2005). Hsp70 chaperones: Cellular functions and molecular mechanism. Cellular and Molecular Life Sciences, 62, 670–684.PubMedPubMedCentralCrossRefGoogle Scholar
  105. McCracken, A. A., & Brodsky, J. L. (2003). Evolving questions and paradigm shifts in endoplasmic-reticulum-associated degradation (ERAD). BioEssays, 25, 868–877.PubMedCrossRefGoogle Scholar
  106. McCullough, K. D., Martindale, J. L., Klotz, L. O., Aw, T. Y., & Holbrook, N. J. (2001). Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Molecular and Cellular Biology, 21, 1249–1259.PubMedPubMedCentralCrossRefGoogle Scholar
  107. Mesaeli, N., Nakamura, K., Zvaritch, E., et al. (1999). Calreticulin is essential for cardiac development. The Journal of Cell Biology, 144, 857–868.PubMedPubMedCentralCrossRefGoogle Scholar
  108. Meunier, L., Usherwood, Y. K., Chung, K. T., & Hendershot, L. M. (2002). A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Molecular Biology of the Cell, 13, 4456–4469.PubMedPubMedCentralCrossRefGoogle Scholar
  109. Michalak, M., Corbett, E. F., Mesaeli, N., Nakamura, K., & Opas, M. (1999). Calreticulin: One protein, one gene, many functions. The Biochemical Journal, 344, 281–292.PubMedPubMedCentralCrossRefGoogle Scholar
  110. Michalak, M., Robert Parker, J. M., & Opas, M. (2002). Ca2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium, 32, 269–278.PubMedCrossRefGoogle Scholar
  111. Michalak, M., Groenendyk, J., Szabo, E., Gold, L. I., & Opas, M. (2009). Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. The Biochemical Journal, 417, 651–666.PubMedCrossRefGoogle Scholar
  112. Minamino, T., & Kitakaze, M. (2010). ER stress in cardiovascular disease. Journal of Molecular and Cellular Cardiology, 48, 1105–1110.PubMedCrossRefGoogle Scholar
  113. Molinari, M., & Helenius, A. (2000). Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science, 288, 331–333.PubMedCrossRefGoogle Scholar
  114. Morito, D., & Nagata, K. (2015). Pathogenic hijacking of ER-associated degradation: Is ERAD flexible? Molecular Cell, 59, 335–344.PubMedCrossRefGoogle Scholar
  115. Muchowski, P. J., & Wacker, J. L. (2005). Modulation of neurodegeneration by molecular chaperones. Nature Reviews. Neuroscience, 6, 11–22.PubMedCrossRefGoogle Scholar
  116. Muchowski, P. J., Schaffar, G., Sittler, A., Wanker, E. E., Hayer-Hartl, M. K., & Hartl, F. U. (2000). Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proceedings of the National Academy of Sciences of the United States of America, 97, 7841–7846.PubMedPubMedCentralCrossRefGoogle Scholar
  117. Nagashima, Y., Mishiba, K., Suzuki, E., Shimada, Y., Iwata, Y., & Koizumi, N. (2011). Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Scientific Reports, 1(29).  https://doi.org/10.1038/srep00029.
  118. Naidoo, N. (2009). ER and aging-protein folding and the ER stress response. Ageing Research Reviews, 8, 150–159.PubMedCrossRefGoogle Scholar
  119. Nakamura, K., Zuppini, A., Arnaudeau, S., et al. (2001). Functional specialization of calreticulin domains. The Journal of Cell Biology, 154, 961–972.PubMedPubMedCentralCrossRefGoogle Scholar
  120. Navid, F., & Colbert, R. A. (2017). Causes and consequences of endoplasmic reticulum stress in rheumatic disease. Nature Reviews Rheumatology, 13, 25–40.PubMedCrossRefGoogle Scholar
  121. Nigam, S. K., Goldberg, A. L., Ho, S., Rohde, M. F., Bush, K. T., & Sherman, M. (1994). A set of endoplasmic reticulum proteins possessing properties of molecular chaperones includes Ca(2+)-binding proteins and members of the thioredoxin superfamily. The Journal of Biological Chemistry, 269, 1744–1749.PubMedGoogle Scholar
  122. Nishikawa, S., Brodsky, J. L., & Nakatsukasa, K. (2005). Roles of molecular chaperones in endoplasmic reticulum (ER) quality control and ER-associated degradation (ERAD). Journal of Biochemistry, 137(5), 551.PubMedCrossRefGoogle Scholar
  123. Nishitoh, H., Saitoh, M., Mochida, Y., et al. (1998). ASK1 is essential for JNK/SAPK activation by TRAF2. Molecular Cell, 2, 389–395.PubMedCrossRefGoogle Scholar
  124. Nishitoh, H., Matsuzawa, A., Tobiume, K., et al. (2002). ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes & Development, 16, 1345–1355.CrossRefGoogle Scholar
  125. Normington, K., Kohno, K., Kozutsumi, Y., Gething, M. J., & Sambrook, J. (1989). S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell, 57, 1223–1236.PubMedPubMedCentralCrossRefGoogle Scholar
  126. Okada, T., Haze, K., Nadanaka, S., et al. (2003). A serine protease inhibitor prevents endoplasmic reticulum stress-induced cleavage but not transport of the membrane-bound transcription factor ATF6. The Journal of Biological Chemistry, 278, 31024–31032.PubMedCrossRefGoogle Scholar
  127. Oliver, J. D., van der Wal, F. J., Bulleid, N. J., & High, S. (1997). Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins. Science, 275, 86–88.PubMedCrossRefGoogle Scholar
  128. Oslowski, C. M., & Urano, F. (2011). Measuring ER stress and the unfolded protein response using mammalian tissue culture system. Methods in Enzymology, 490, 71–92.PubMedPubMedCentralCrossRefGoogle Scholar
  129. Ostrovsky, O., Makarewich, C. A., Snapp, E. L., & Argon, Y. (2009). An essential role for ATP binding and hydrolysis in the chaperone activity of GRP94 in cells. Proceedings of the National Academy of Sciences of the United States of America, 106, 11600–11605.PubMedPubMedCentralCrossRefGoogle Scholar
  130. Ostwald, T. J., & MacLennan, D. H. (1974). Isolation of a high affinity calcium-binding protein from sarcoplasmic reticulum. The Journal of Biological Chemistry, 249, 974–979.PubMedGoogle Scholar
  131. Otero, J. H., Lizak, B., & Hendershot, L. M. (2010). Life and death of a BiP substrate. Seminars in Cell & Developmental Biology, 21, 472–478.CrossRefGoogle Scholar
  132. Oyadomari, S., & Mori, M. (2004). Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death and Differentiation, 11, 381–389.PubMedCrossRefGoogle Scholar
  133. Oyadomari, S., Koizumi, A., Takeda, K., et al. (2002). Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. The Journal of Clinical Investigation, 109, 525–532.PubMedPubMedCentralCrossRefGoogle Scholar
  134. Park, S. W., & Ozcan, U. (2013). Potential for therapeutic manipulation of the UPR in disease. Seminars in Immunopathology, 35, 351–373.PubMedPubMedCentralCrossRefGoogle Scholar
  135. Pollock, S., Kozlov, G., Pelletier, M. F., et al. (2004). Specific interaction of ERp57 and calnexin determined by NMR spectroscopy and an ER two-hybrid system. The EMBO Journal, 23, 1020–1029.PubMedPubMedCentralCrossRefGoogle Scholar
  136. Primm, T. P., Walker, K. W., & Gilbert, H. F. (1996). Facilitated protein aggregation. Effects of calcium on the chaperone and anti-chaperone activity of protein disulfide-isomerase. The Journal of Biological Chemistry, 271, 33664–33669.PubMedCrossRefGoogle Scholar
  137. Prins, D., Groenendyk, J., Touret, N., & Michalak, M. (2011). Modulation of STIM1 and capacitative Ca2+ entry by the endoplasmic reticulum luminal oxidoreductase ERp57. EMBO Reports, 12, 1182–1188.PubMedPubMedCentralCrossRefGoogle Scholar
  138. Puthalakath, H., O’Reilly, L. A., Gunn, P., et al. (2007). ER stress triggers apoptosis by activating BH3-only protein Bim. Cell, 129, 1337–1349.PubMedCrossRefPubMedCentralGoogle Scholar
  139. Rhodes, J. D., & Sanderson, J. (2009). The mechanisms of calcium homeostasis and signalling in the lens. Experimental Eye Research, 88, 226–234.PubMedCrossRefGoogle Scholar
  140. Rodan, A. R., Simons, J. F., Trombetta, E. S., & Helenius, A. (1996). N-linked oligosaccharides are necessary and sufficient for association of glycosylated forms of bovine RNase with calnexin and calreticulin. The EMBO Journal, 15, 6921–6930.PubMedPubMedCentralCrossRefGoogle Scholar
  141. Ron, D. (2002). Proteotoxicity in the endoplasmic reticulum: Lessons from the Akita diabetic mouse. The Journal of Clinical Investigation, 109, 443–445.PubMedPubMedCentralCrossRefGoogle Scholar
  142. Ron, D., & Hubbard, S. R. (2008). How IRE1 reacts to ER stress. Cell, 132, 24–26.PubMedCrossRefGoogle Scholar
  143. Ron, D., & Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nature Reviews. Molecular Cell Biology, 8, 519–529.PubMedCrossRefGoogle Scholar
  144. Russell, S. J., Ruddock, L. W., Salo, K. E., et al. (2004). The primary substrate binding site in the b' domain of ERp57 is adapted for endoplasmic reticulum lectin association. The Journal of Biological Chemistry, 279, 18861–18869.PubMedCrossRefGoogle Scholar
  145. Rutkowski, D. T., & Kaufman, R. J. (2004). A trip to the ER: Coping with stress. Trends in Cell Biology, 14, 20–28.PubMedCrossRefGoogle Scholar
  146. Sano, R., & Reed, J. C. (2013). ER stress-induced cell death mechanisms. Biochimica et Biophysica Acta, 1833, 3460–3470.PubMedPubMedCentralCrossRefGoogle Scholar
  147. Schonthal, A. H. (2012). Endoplasmic reticulum stress: Its role in disease and novel prospects for therapy. Scientifica, 2012(857516), 1–26.CrossRefGoogle Scholar
  148. Schrag, J. D., Bergeron, J. J., Li, Y., et al. (2001). The structure of calnexin, an ER chaperone involved in quality control of protein folding. Molecular Cell, 8, 633–644.PubMedCrossRefGoogle Scholar
  149. Schrag, J. D., Procopio, D. O., Cygler, M., Thomas, D. Y., & Bergeron, J. J. (2003). Lectin control of protein folding and sorting in the secretory pathway. Trends in Biochemical Sciences, 28, 49–57.PubMedCrossRefGoogle Scholar
  150. Schroder, M. (2008). Endoplasmic reticulum stress responses. Cellular and Molecular Life Sciences, 65, 862–894.PubMedCrossRefGoogle Scholar
  151. Schroder, M., & Kaufman, R. J. (2005a). ER stress and the unfolded protein response. Mutation Research, 569, 29–63.PubMedCrossRefGoogle Scholar
  152. Schroder, M., & Kaufman, R. J. (2005b). The mammalian unfolded protein response. Annual Review of Biochemistry, 74, 739–789.PubMedCrossRefGoogle Scholar
  153. Shamu, C. E., & Walter, P. (1996). Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. The EMBO Journal, 15, 3028–3039.PubMedPubMedCentralCrossRefGoogle Scholar
  154. Shen, J., Chen, X., Hendershot, L., & Prywes, R. (2002). ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Developmental Cell, 3, 99–111.PubMedCrossRefGoogle Scholar
  155. Shi, Y., Vattem, K. M., Sood, R., et al. (1998). Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Molecular and Cellular Biology, 18, 7499–7509.PubMedPubMedCentralCrossRefGoogle Scholar
  156. Song, B., Scheuner, D., Ron, D., Pennathur, S., & Kaufman, R. J. (2008). Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. The Journal of Clinical Investigation, 118, 3378–3389.PubMedPubMedCentralCrossRefGoogle Scholar
  157. Sriram, M., Osipiuk, J., Freeman, B., Morimoto, R., & Joachimiak, A. (1997). Human Hsp70 molecular chaperone binds two calcium ions within the ATPase domain. Structure, 5, 403–414.PubMedCrossRefGoogle Scholar
  158. Szegezdi, E., Logue, S. E., Gorman, A. M., & Samali, A. (2006). Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Reports, 7, 880–885.PubMedPubMedCentralCrossRefGoogle Scholar
  159. Takahashi, K., Niidome, T., Akaike, A., Kihara, T., & Sugimoto, H. (2009). Amyloid precursor protein promotes endoplasmic reticulum stress-induced cell death via C/EBP homologous protein-mediated pathway. Journal of Neurochemistry, 109, 1324–1337.PubMedCrossRefGoogle Scholar
  160. Taylor, C. W., & Laude, A. J. (2002). IP3 receptors and their regulation by calmodulin and cytosolic Ca2+. Cell Calcium, 32, 321–334.PubMedCrossRefGoogle Scholar
  161. Tirasophon, W., Welihinda, A. A., & Kaufman, R. J. (1998). A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes & Development, 12, 1812–1824.CrossRefGoogle Scholar
  162. Tripathi, R., Benz, N., Culleton, B., Trouve, P., & Ferec, C. (2014). Biophysical characterisation of calumenin as a charged F508del-CFTR folding modulator. PLoS One, 9, e104970.PubMedPubMedCentralCrossRefGoogle Scholar
  163. Tsai, B., Ye, Y., & Rapoport, T. A. (2002). Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nature Reviews. Molecular Cell Biology, 3, 246–255.PubMedCrossRefGoogle Scholar
  164. Tsukumo, Y., Tomida, A., Kitahara, O., et al. (2007). Nucleobindin 1 controls the unfolded protein response by inhibiting ATF6 activation. The Journal of Biological Chemistry, 282, 29264–29272.PubMedCrossRefGoogle Scholar
  165. Tsukumo, Y., Tsukahara, S., Saito, S., Tsuruo, T., & Tomida, A. (2009). A novel endoplasmic reticulum export signal: Proline at the +2-position from the signal peptide cleavage site. The Journal of Biological Chemistry, 284, 27500–27510.PubMedPubMedCentralCrossRefGoogle Scholar
  166. Tu, B. P., & Weissman, J. S. (2004). Oxidative protein folding in eukaryotes: Mechanisms and consequences. The Journal of Cell Biology, 164, 341–346.PubMedPubMedCentralCrossRefGoogle Scholar
  167. Tufanli, O., Telkoparan Akillilar, P., Acosta-Alvear, D., et al. (2017). Targeting IRE1 with small molecules counteracts progression of atherosclerosis. Proceedings of the National Academy of Sciences of the United States of America, 114, E1395–EE404.PubMedPubMedCentralCrossRefGoogle Scholar
  168. Uehara, T., Nakamura, T., Yao, D., et al. (2006). S-Nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature, 441, 513.PubMedCrossRefGoogle Scholar
  169. Urano, F., Wang, X., Bertolotti, A., et al. (2000). Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science, 287, 664–666.PubMedCrossRefGoogle Scholar
  170. Urra, H., Dufey, E., Lisbona, F., Rojas-Rivera, D., & Hetz, C. (2013). When ER stress reaches a dead end. Biochimica et Biophysica Acta, 1833, 3507–3517.PubMedCrossRefGoogle Scholar
  171. Vekich, J. A., Belmont, P. J., Thuerauf, D. J., & Glembotski, C. C. (2012). Protein disulfide isomerase-associated 6 is an ATF6-inducible ER stress response protein that protects cardiac myocytes from ischemia/reperfusion-mediated cell death. Journal of Molecular and Cellular Cardiology, 53, 259–267.PubMedPubMedCentralCrossRefGoogle Scholar
  172. Walter, P., & Ron, D. (2011). The unfolded protein response: From stress pathway to homeostatic regulation. Science, 334, 1081–1086.PubMedPubMedCentralCrossRefGoogle Scholar
  173. Wang, M., Ye, R., Barron, E., et al. (2009). Essential role of the unfolded protein response regulator GRP78/BiP in protection from neuronal apoptosis. Cell Death and Differentiation, 17, 488.PubMedPubMedCentralCrossRefGoogle Scholar
  174. Wang, Q., Feng, H., Zheng, P., et al. (2012). The intracellular transport and secretion of calumenin-1/2 in living cells. PLoS One, 7, e35344.PubMedPubMedCentralCrossRefGoogle Scholar
  175. Wang, D. Y., Abbasi, C., El-Rass, S., et al. (2014). Endoplasmic reticulum resident protein 44 (ERp44) deficiency in mice and zebrafish leads to cardiac developmental and functional defects. Journal of the American Heart Association, 3, e001018.PubMedPubMedCentralCrossRefGoogle Scholar
  176. Wang, Q., Groenendyk, J., & Michalak, M. (2015). Glycoprotein quality control and endoplasmic reticulum stress. Molecules, 20, 13689–13704.PubMedCrossRefGoogle Scholar
  177. Wang, Y., Sun, Y., Fu, Y., et al. (2017). Calumenin relieves cardiac injury by inhibiting ERS-initiated apoptosis during viral myocarditis. International Journal of Clinical and Experimental Pathology, 10, 7277–7284.Google Scholar
  178. Wendel, M., Sommarin, Y., Bergman, T., & Heinegard, D. (1995). Isolation, characterization, and primary structure of a calcium-binding 63-kDa bone protein. The Journal of Biological Chemistry, 270, 6125–6133.PubMedCrossRefGoogle Scholar
  179. Williams, D. B. (2006). Beyond lectins: The calnexin/calreticulin chaperone system of the endoplasmic reticulum. Journal of Cell Science, 119, 615–623.PubMedCrossRefGoogle Scholar
  180. Winblad, B., Amouyel, P., Andrieu, S., et al. (2016). Defeating Alzheimer’s disease and other dementias: A priority for European science and society. Lancet Neurology, 15, 455–532.PubMedCrossRefGoogle Scholar
  181. Woehlbier, U., Colombo, A., Saaranen, M. J., et al. (2016). ALS-linked protein disulfide isomerase variants cause motor dysfunction. The EMBO Journal, 35, 845–865.PubMedPubMedCentralCrossRefGoogle Scholar
  182. Xu, C., & Ng, D. T. (2015). Glycosylation-directed quality control of protein folding. Nature Reviews. Molecular Cell Biology, 16, 742–752.PubMedCrossRefGoogle Scholar
  183. Xu, C., Bailly-Maitre, B., & Reed, J. C. (2005). Endoplasmic reticulum stress: Cell life and death decisions. The Journal of Clinical Investigation, 115, 2656–2664.PubMedPubMedCentralCrossRefGoogle Scholar
  184. Yang, L., Zhao, D., Ren, J., & Yang, J. (2015). Endoplasmic reticulum stress and protein quality control in diabetic cardiomyopathy. Biochimica et Biophysica Acta, 1852, 209–218.PubMedCrossRefGoogle Scholar
  185. Ye, J., Rawson, R. B., Komuro, R., et al. (2000). ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Molecular Cell, 6, 1355–1364.PubMedCrossRefGoogle Scholar
  186. Yoshida, H., Haze, K., Yanagi, H., Yura, T., & Mori, K. (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. The Journal of Biological Chemistry, 273, 33741–33749.PubMedCrossRefGoogle Scholar
  187. Zapun, A., Darby, N. J., Tessier, D. C., Michalak, M., Bergeron, J. J., & Thomas, D. Y. (1998). Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. The Journal of Biological Chemistry, 273, 6009–6012.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Sasirekha Narayanasamy
    • 1
  • Gopala Krishna Aradhyam
    • 1
  1. 1.Department of BiotechnologyBhupat and Jyoti Mehta School of Biosciences, Indian Institute of Technology MadrasChennaiIndia

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