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Glucose-regulated proteins in cancer: molecular mechanisms and therapeutic potential

Lee, Amy S.·2014·Nature Reviews Cancer
DOI 10.1038/nrc3701PMC PMC4158750
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  • GRP94 is a highly abundant ER-resident protein recognized primarily as a luminal molecular chaperone but also as a potent calcium- and peptide-binding protein.

    “GRP94, also known as gp96, is a highly abundant ER-resident protein recognized primarily as a luminal molecular chaperone but also as a potent calcium- and peptide-binding protein”

    From GRP94 Regulates Circulating Cholesterol Levels through Blockade of PCSK9-Induced LDLR Degradation (2015) · cites this paper as Lee, 2014

    The Introduction identifies GRP94 as gp96, describes GRPs as ER chaperones with calcium-binding functions, and discusses their traditional residence in the ER lumen. The Vaccination strategies section describes a GRP94–peptide complex, supporting peptide binding. Our copy does not establish that GRP94 is highly abundant or characterize its calcium- and peptide-binding as potent. (LLM, conf=0.78)

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  1. Ni, M. & Lee, A. S. ER chaperones in mammalian development and human diseases. FEBS Lett. 581, 3641–3651 (2007). · DOI
  2. Wang, X. Y. & Subjeck, J. R. High molecular weight stress proteins: Identification, cloning and utilisation in cancer immunotherapy. Int. J. Hyperthermia 29, 364–375 (2013). · DOI
  3. Wadhwa, R., Taira, K. & Kaul, S. C. An Hsp70 family chaperone, mortalin/mthsp70/PBP74/Grp75: what, when, and where? Cell Stress Chaperones 7, 309–316 (2002). · DOI
  4. Marzec, M., Eletto, D. & Argon, Y. GRP94: An HSP90-like protein specialized for protein folding and quality control in the endoplasmic reticulum. Biochim. Biophys. Acta 1823, 774–787 (2012). · DOI · Paper page
  5. Lee, A. S. GRP78 induction in cancer: therapeutic and prognostic implications. Cancer Res. 67, 3496–3499 (2007). · DOI
  6. Miao, Y. R. et al. Inhibition of established micrometastases by targeted drug delivery via cell surface-associated GRP78. Clin. Cancer Res. 19, 2107–2116 (2013). · DOI
  7. 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. 11, 2307–2316 (2009). · DOI
  8. Kusaczuk, M. & Cechowska-Pasko, M. Molecular chaperone ORP150 in ER stress-related diseases. Curr. Pharm. Des. 19, 2807–2818 (2013). · DOI
  9. Behnke, J. & Hendershot, L. M. The large Hsp70 Grp170 binds to unfolded protein substrates in vivo with a regulation distinct from conventional Hsp70s. J. Biol. Chem. 289, 2899–2907 (2013). · DOI
  10. Wadhwa, R. et al. Hsp70 family member, mot-2/mthsp70/GRP75, binds to the cytoplasmic sequestration domain of the p53 protein. Exp. Cell Res. 274, 246–253 (2002). · DOI
  11. Ni, M., Zhang, Y. & Lee, A. S. Beyond the endoplasmic reticulum: atypical GRP78 in cell viability, signalling and therapeutic targeting. Biochem. J. 434, 181–188 (2011). · DOI
  12. Gonzalez-Gronow, M., Selim, M. A., Papalas, J. & Pizzo, S. V. GRP78: a multifunctional receptor on the cell surface. Antioxid. Redox Signal. 11, 2299–2306 (2009). · DOI
  13. Sato, M., Yao, V. J., Arap, W. & Pasqualini, R. GRP78 signaling hub a receptor for targeted tumor therapy. Adv. Genet. 69, 97–114 (2010). · DOI
  14. Gray, P. C. & Vale, W. Cripto/GRP78 modulation of the TGF-β pathway in development and oncogenesis. FEBS Lett. 586, 1836–1845 (2012). · DOI
  15. Zhang, Y., Liu, R., Ni, M., Gill, P. & Lee, A. S. Cell surface relocalization of the endoplasmic reticulum chaperone and unfolded protein response regulator GRP78/BiP. J. Biol. Chem. 285, 15065–15075 (2010). · DOI
  16. Zhang, Y. et al. Cancer cells resistant to therapy promote cell surface relocalization of GRP78 which complexes with PI3K and enhances PI(3,4,5)P3 production. PLoS ONE 8, e80071 (2013). · DOI
  17. Liu, R. et al. Monoclonal antibody against cell surface GRP78 as a novel agent in suppressing PI3K/AKT signaling, tumor growth and metastasis. Clin. Cancer Res. 19, 6802–6811 (2013). This paper shows that targeting cell surface GRP78 by a therapeutic IgG antibody inhibits the PI3K–AKT pathway without compensatory MAPK pathway activation and suppresses endogenous tumour progression, xenograft growth and metastasis. · DOI
  18. Pfaffenbach, K. T. et al. GRP78/BiP is a novel downstream target of IGF-1 receptor mediated signaling. J. Cell. Physiol. 227, 3803–3811 (2012). · DOI
  19. Gray, M. J. et al. AKT inhibition mitigates GRP78 (glucose-regulated protein) expression and contribution to chemoresistance in endometrial cancers. Int. J. Cancer 133, 21–30 (2013). · DOI
  20. Luo, B. & Lee, A. S. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene 32, 805–818 (2013). · DOI
  21. Li, J. & Lee, A. S. Stress induction of GRP78/BiP and its role in cancer. Curr. Mol. Med. 6, 45–54 (2006). · DOI
  22. Yun, C. O. & Wadhwa, R. in Mortalin Biology: Life, Stress and Death: Life, Stress and Death. Ch. 18 (eds Kaul, S. C. & Wadhwa, R.) (Springer, 2012).
  23. Srivastava, P. K. Identification of chaperones as essential components of the tumor rejection moieties of cancers. Cancer Immun. 12, 5 (2012).
  24. Mori, K. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 101, 451–454 (2000). · DOI
  25. Chang, S. C., Erwin, A. E. & Lee, A. S. Glucose-regulated protein (GRP94 and GRP78) genes share common regulatory domains and are coordinately regulated by common trans-acting factors. Mol. Cell. Biol. 9, 2153–2162 (1989). · DOI
  26. Ma, Y. & Hendershot, L. M. The role of the unfolded protein response in tumour development: friend or foe? Nature Rev. Cancer 4, 966–977 (2004). · DOI
  27. Wu, J. & Kaufman, R. J. From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ. 13, 374–384 (2006). · DOI
  28. Ron, D. & Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nature Rev. Mol. Cell. Biol. 8, 519–529 (2007). · DOI
  29. Hetz, C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nature Rev. Mol. Cell. Biol. 13, 89–102 (2012). · DOI
  30. Luo, S., Baumeister, P., Yang, S., Abcouwer, S. F. & Lee, A. S. Induction of Grp78/BiP by translational block: activation of the Grp78 promoter by ATF4 through an upstream ATF/CRE site independent of the endoplasmic reticulum stress elements. J. Biol. Chem. 278, 37375–37385 (2003). · DOI
  31. Lee, K. et al. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 16, 452–466 (2002). · DOI
  32. Li, J. et al. The unfolded protein response regulator GRP78/BiP is required for endoplasmic reticulum integrity and stress-induced autophagy in mammalian cells. Cell Death Differ. 15, 1460–1471 (2008). · DOI
  33. Wang, M. et al. Essential role of the unfolded protein response regulator GRP78/BiP in protection from neuronal apoptosis. Cell Death Differ. 17, 488–498 (2010). · DOI
  34. Wey, S., Luo, B. & Lee, A. S. Acute inducible ablation of GRP78 reveals its role in hematopoietic stem cell survival, lymphogenesis and regulation of stress signaling. PLoS ONE 7, e39047 (2012). · DOI
  35. Heijmans, J. et al. ER stress causes rapid loss of intestinal epithelial stemness through activation of the unfolded protein response. Cell. Rep. 3, 1128–1139 (2013). · DOI · Paper page
  36. Mathew, R. et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 137, 1062–1075 (2009). · DOI
  37. Baumeister, P., Dong, D., Fu, Y. & Lee, A. S. Transcriptional induction of GRP78/BiP by histone deacetylase inhibitors and resistance to histone deacetylase inhibitor-induced apoptosis. Mol. Cancer Ther. 8, 1086–1094 (2009). · DOI
  38. Pyrko, P., Schonthal, A. H., Hofman, F. M., Chen, T. C. & Lee, A. S. The unfolded protein response regulator GRP78/BiP as a novel target for increasing chemosensitivity in malignant gliomas. Cancer Res. 67, 9809–9816 (2007). · DOI
  39. Dong, D. et al. Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival, and tumor angiogenesis in transgene-induced mammary tumor development. Cancer Res. 68, 498–505 (2008). · DOI
  40. Verras, M., Papandreou, I., Lim, A. L. & Denko, N. C. Tumor hypoxia blocks Wnt processing and secretion through the induction of endoplasmic reticulum stress. Mol. Cell. Biol. 28, 7212–7224 (2008). · DOI
  41. Misra, U. K., Gonzalez-Gronow, M., Gawdi, G. & Pizzo, S. V. The role of MTJ-1 in cell surface translocation of GRP78, a receptor for α 2-macroglobulin-dependent signaling. J. Immunol. 174, 2092–2097 (2005). · DOI
  42. Burikhanov, R. et al. The tumor suppressor Par-4 activates an extrinsic pathway for apoptosis. Cell 138, 377–388 (2009). · DOI
  43. Misra, U. K. et al. The role of Grp 78 in α 2-macroglobulin-induced signal transduction. Evidence from RNA interference that the low density lipoprotein receptor-related protein is associated with, but not necessary for, GRP 78-mediated signal transduction. J. Biol. Chem. 277, 42082–42087 (2002). This paper provides the first evidence that cell surface GRP78 is essential for α2M*-induced signal transduction in both human prostate cancer cells and murine macrophages. · DOI
  44. Misra, U. K. & Pizzo, S. V. Receptor-recognized α(2)-macroglobulin binds to cell surface-associated GRP78 and activates mTORC1 and mTORC2 signaling in prostate cancer cells. PLoS ONE 7, e51735 (2012). · DOI
  45. de Ridder, G. G., Gonzalez-Gronow, M., Ray, R. & Pizzo, S. V. Autoantibodies against cell surface GRP78 promote tumor growth in a murine model of melanoma. Melanoma Res. 21, 35–43 (2011). · DOI
  46. Salmena, L., Carracedo, A. & Pandolfi, P. P. Tenets of PTEN tumor suppression. Cell 133, 403–414 (2008). · DOI
  47. Wey, S. et al. Inducible knockout of GRP78/BiP in the hematopoietic system suppresses Pten-null leukemogenesis and AKT oncogenic signaling. Blood 119, 817–825 (2012). References 47 and 48 show that GRP78 haploinsufficiency is sufficient to suppress PTEN-null-mediated PI3K–AKT oncogenic signalling and tumorigenesis in solid and blood cancer mouse models, with no harmful effect on normal organs. · DOI
  48. Shani, G. et al. 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, 666–677 (2008). · DOI
  49. Kelber, J. A. et al. Blockade of Cripto binding to cell surface GRP78 inhibits oncogenic Cripto signaling via MAPK/PI3K and Smad2/3 pathways. Oncogene 28, 2324–2336 (2009). References 49 and 50 report the identification of GRP78 as a cell surface receptor and cofactor that is required for Cripto signalling via both TGFβ and SRC−MAPK–PI3K pathways that promote the tumorigenic phenotype. · DOI
  50. Wanderling, S. et al. GRP94 is essential for mesoderm induction and muscle development because it regulates insulin-like growth factor secretion. Mol. Biol. Cell 18, 3764–3775 (2007). · DOI
  51. Liu, B. et al. Essential roles of grp94 in gut homeostasis via chaperoning canonical Wnt pathway. Proc. Natl. Acad. Sci. USA 110, 6877–6882 (2013). · DOI
  52. Hua, Y. et al. Molecular chaperone gp96 is a novel therapeutic target of multiple myeloma. Clin. Cancer Res. 19, 6242–6251 (2013). · DOI
  53. Morales, C. et al. Immune chaperone gp96 drives the contributions of macrophages to inflammatory colon tumorigenesis. Cancer Res. 74, 446–459 (2014). References 53 and 54 dissect the essential roles of GRP94 in the development of multiple myeloma and inflammatory colon tumorigenesis, and they show that GRP94 regulates the WNT–LRP–survivin pathway and the expression of crucial inflammatory cytokines. · DOI
  54. Dejeans, N. et al. Overexpression of GRP94 in breast cancer cells resistant to oxidative stress promotes high levels of cancer cell proliferation and migration: implications for tumor recurrence. Free Radic. Biol. Med. 52, 993–1002 (2012). · DOI
  55. Kaul, S. C. et al. Malignant transformation of NIH3T3 cells by overexpression of mot-2 protein. Oncogene 17, 907–911 (1998). · DOI
  56. Wadhwa, R. et al. Inactivation of tumor suppressor p53 by mot-2, a hsp70 family member. J. Biol. Chem. 273, 29586–29591 (1998). · DOI
  57. Mizukoshi, E. et al. Fibroblast growth factor-1 interacts with the glucose-regulated protein GRP75/mortalin. Biochem. J. 343 461–466 (1999). · DOI
  58. Rao, R. V. et al. Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett. 514, 122–128 (2002). · DOI
  59. Reddy, R. K. et al. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J. Biol. Chem. 278, 20915–20924 (2003). · DOI · Paper page
  60. Fu, Y., Li, J. & Lee, A. S. GRP78/BiP inhibits endoplasmic reticulum BIK and protects human breast cancer cells against estrogen-starvation induced apoptosis. Cancer Res. 67, 3734–3740 (2007). · DOI
  61. Zhou, H., Zhang, Y., Fu, Y., Chan, L. & Lee, A. S. Novel mechanism of anti-apoptotic function of 78-kDa glucose-regulated protein (GRP78): endocrine resistance factor in breast cancer, through release of B-cell lymphoma 2 (BCL-2) from BCL-2-interacting killer (BIK). J. Biol. Chem. 286, 25687–25696 (2011). · DOI
  62. Ni, M., Zhou, H., Wey, S., Baumeister, P. & Lee, A. S. Regulation of PERK signaling and leukemic cell survival by a novel cytosolic isoform of the UPR regulator GRP78/BiP. PLoS ONE 4, e6868 (2009). · DOI
  63. Shu, C. W. et al. GRP78 and Raf-1 cooperatively confer resistance to endoplasmic reticulum stress-induced apoptosis. J. Cell. Physiol. 215, 627–635 (2008). · DOI
  64. Luo, S., Mao, C., Lee, B. & Lee, A. S. GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol. Cell. Biol. 26, 5688–5697 (2006). · DOI
  65. Zhu, G. et al. GRP78 plays an essential role in adipogenesis and postnatal growth in mice. FASEB J. 27, 955–964 (2013). · DOI
  66. Misra, U. K., Deedwania, R. & Pizzo, S. V. Activation and cross-talk between Akt, NF-κB, and unfolded protein response signaling in 1-LN prostate cancer cells consequent to ligation of cell surface-associated GRP78. J. Biol. Chem. 281, 13694–13707 (2006). · DOI
  67. Davidson, D. J. et al. Kringle 5 of human plasminogen induces apoptosis of endothelial and tumor cells through surface-expressed glucose-regulated protein 78. Cancer Res. 65, 4663–4672 (2005). · DOI
  68. Martin-Perez, R., Niwa, M. & Lopez-Rivas, A. ER stress sensitizes cells to TRAIL through down-regulation of FLIP and Mcl-1 and PERK-dependent up-regulation of TRAIL-R2. Apoptosis 17, 349–363 (2012). · DOI
  69. Cook, K. L. et al. Glucose-regulated protein 78 controls cross-talk between apoptosis and autophagy to determine antiestrogen responsiveness. Cancer Res. 72, 3337–3349 (2012). · DOI
  70. Reddy, R. K., Lu, J. & Lee, A. S. The endoplasmic reticulum chaperone glycoprotein GRP94 with Ca2+-binding and antiapoptotic properties is a novel proteolytic target of calpain during etoposide-induced apoptosis. J. Biol. Chem. 274, 28476–28483 (1999). · DOI
  71. Patel, P. D. et al. Paralog-selective Hsp90 inhibitors define tumor-specific regulation of HER2. Nature Chem. Biol. 9, 677–684 (2013). · DOI
  72. Namba, T. et al. Up-regulation of 150-kDa oxygen-regulated protein by celecoxib in human gastric carcinoma cells. Mol. Pharmacol. 71, 860–870 (2007). · DOI
  73. Gao, Y. Y. et al. Implication of oxygen-regulated protein 150 (ORP150) in apoptosis induced by proteasome inhibitors in human thyroid cancer cells. J. Clin. Endocrinol. Metab. 95, E319–E326 (2010). · DOI
  74. Sanson, M. et al. Oxidized low-density lipoproteins trigger endoplasmic reticulum stress in vascular cells: prevention by oxygen-regulated protein 150 expression. Circ. Res. 104, 328–336 (2009). · DOI
  75. Sanson, M. et al. Oxygen-regulated protein-150 prevents calcium homeostasis deregulation and apoptosis induced by oxidized LDL in vascular cells. Cell Death Differ. 15, 1255–1265 (2008). · DOI
  76. Virrey, J. J. et al. Stress chaperone GRP78/BiP confers chemoresistance to tumor-associated endothelial cells. Mol. Cancer Res. 6, 1268–1275 (2008). · DOI
  77. McFarland, B. C. et al. Plasminogen Kringle 5 induces apoptosis of brain microvessel endothelial cells: sensitization by radiation and requirement for GRP78 and LRP1. Cancer Res. 69, 5537–5545 (2009). · DOI
  78. Bhattacharjee, G. et al. Regulation of tissue factor—mediated initiation of the coagulation cascade by cell surface grp78. Arterioscler. Thromb. Vasc. Biol. 25, 1737–1743 (2005). · DOI
  79. Philippova, M. et al. Identification of proteins associating with glycosylphosphatidylinositol- anchored T-cadherin on the surface of vascular endothelial cells: role for Grp78/BiP in T-cadherin-dependent cell survival. Mol. Cell. Biol. 28, 4004–4017 (2008). · DOI
  80. Gonzalez-Gronow, M. et al. Plasminogen structural domains exhibit different functions when associated with cell surface GRP78 or the voltage-dependent anion channel. J. Biol. Chem. 282, 32811–32820 (2007). · DOI
  81. Katanasaka, Y. et al. Cancer antineovascular therapy with liposome drug delivery systems targeted to BiP/GRP78. Int. J. Cancer 127, 2685–2698 (2010). · DOI
  82. Ozawa, K. et al. Regulation of tumor angiogenesis by oxygen-regulated protein 150, an inducible endoplasmic reticulum chaperone. Cancer Res. 61, 4206–4213 (2001).
  83. Fu, Y. & Lee, A. S. Glucose regulated proteins in cancer progression, drug resistance and immunotherapy. Cancer Biol. Ther. 5, 741–744 (2006). · DOI
  84. Sun, Q. et al. Expressions of GRP78 and Bax associate with differentiation, metastasis, and apoptosis in non-small cell lung cancer. Mol. Biol. Rep. 39, 6753–6761 (2012). · DOI
  85. Daneshmand, S. et al. Glucose-regulated protein GRP78 is up-regulated in prostate cancer and correlates with recurrence and survival. Hum. Pathol. 38, 1547–1552 (2007). · DOI
  86. Zhang, J. et al. Association of elevated GRP78 expression with increased lymph node metastasis and poor prognosis in patients with gastric cancer. Clin. Exp. Metastasis 23, 401–410 (2006). · DOI
  87. Li, Z. et al. Cell-surface GRP78 facilitates colorectal cancer cell migration and invasion. Int. J. Biochem. Cell. Biol. 45, 987–994 (2013). · DOI
  88. Dong, D. et al. A critical role for GRP78/BiP in the tumor microenvironment for neovascularization during tumor growth and metastasis. Cancer Res. 71, 2848–2857 (2011). This paper shows that GRP78 regulates endothelial cell function and that GRP78 haploinsufficiency in endothelial cells is sufficient to suppress tumour angiogenesis and metastatic growth, with a minimal effect on normal tissue MVD. · DOI
  89. Misra, U. K., Deedwania, R. & Pizzo, S. V. Binding of activated α2-macroglobulin to its cell surface receptor GRP78 in 1-LN prostate cancer cells regulates PAK-2-dependent activation of LIMK. J. Biol. Chem. 280, 26278–26286 (2005). · DOI
  90. Zheng, H. C. et al. Overexpression of GRP78 and GRP94 are markers for aggressive behavior and poor prognosis in gastric carcinomas. Hum. Pathol. 39, 1042–1049 (2008). · DOI
  91. Hong, F., Liu, B., Chiosis, G., Gewirth, D. T. & Li, Z. α7 helix region of αI domain is crucial for integrin binding to endoplasmic reticulum chaperone gp96: a potential therapeutic target for cancer metastasis. J. Biol. Chem. 288, 18243–18248 (2013). · DOI
  92. Yi, X. et al. Association of mortalin (HSPA9) with liver cancer metastasis and prediction for early tumor recurrence. Mol. Cell. Proteomics 7, 315–325 (2008). · DOI
  93. Stojadinovic, A. et al. HYOU1/Orp150 expression in breast cancer. Med. Sci. Monit. 13, BR231–239 (2007).
  94. Mahadevan, N. R. et al. Transmission of endoplasmic reticulum stress and pro-inflammation from tumor cells to myeloid cells. Proc. Natl Acad. Sci. USA 108, 6561–6566 (2011). · DOI
  95. Li, Z. & Li, Z. Glucose regulated protein 78: A critical link between tumor microenvironment and cancer hallmarks. Biochim. Biophys. Acta 1826, 13–22 (2012).
  96. Hori, O. et al. Exposure of astrocytes to hypoxia/reoxygenation enhances expression of glucose-regulated protein 78 facilitating astrocyte release of the neuroprotective cytokine interleukin 6. J. Neurochem. 66, 973–979 (1996). · DOI
  97. Jamora, C., Dennert, G. & Lee, A. S. Inhibition of tumor progression by suppression of stress protein GRP78/BiP induction in fibrosarcoma B/C10ME. Proc. Natl Acad. Sci. USA 93, 7690–7694 (1996). · DOI
  98. Triantafilou, M., Fradelizi, D. & Triantafilou, K. Major histocompatibility class one molecule associates with glucose regulated protein (GRP) 78 on the cell surface. Hum. Immunol. 62, 764–770 (2001). · DOI
  99. Misra, U. K., Chu, C. T., Rubenstein, D. S., Gawdi, G. & Pizzo, S. V. Receptor-recognized α 2-macroglobulin-methylamine elevates intracellular calcium, inositol phosphates and cyclic AMP in murine peritoneal macrophages. Biochem. J. 290, 885–891 (1993). · DOI
  100. Misra, U. K. & Pizzo, S. V. Evidence for a pro-proliferative feedback loop in prostate cancer: the role of Epac1 and COX-2-dependent pathways. PLoS ONE 8, e63150 (2013). · DOI
  101. Oida, T. & Weiner, H. L. TGF-β induces surface LAP expression on murine CD4 T cells independent of Foxp3 induction. PLoS ONE 5, e15523 (2010). · DOI
  102. Corrigall, V. M., Vittecoq, O. & Panayi, G. S. Binding immunoglobulin protein-treated peripheral blood monocyte-derived dendritic cells are refractory to maturation and induce regulatory T-cell development. Immunology 128, 218–226 (2009). · DOI
  103. Yang, Y. et al. Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 26, 215–226 (2007). · DOI · Paper page
  104. Luo, B. et al. The endoplasmic reticulum chaperone protein GRP94 is required for maintaining hematopoietic stem cell interactions with the adult bone marrow niche. PLoS ONE 6, e20364 (2011). · DOI
  105. Luo, B., Tseng, C. C., Adams, G. B. & Lee, A. S. Deficiency of GRP94 in the hematopoietic system alters proliferation regulators in hematopoietic stem cells. Stem Cells Dev. 22, 3062–3073 (2013). · DOI
  106. Wu, M. J. et al. Elimination of head and neck cancer initiating cells through targeting glucose regulated protein78 signaling. Mol. Cancer 9, 283 (2010). · DOI
  107. Chiu, C. C. et al. Grp78 as a therapeutic target for refractory head-neck cancer with CD24CD44 stemness phenotype. Cancer Gene Ther. 20, 606–615 (2013). · DOI
  108. Galicia, V. A. et al. Expansion of hepatic tumor progenitor cells in Pten-null mice requires liver injury and is reversed by loss of AKT2. Gastroenterology 139, 2170–2182 (2010). · DOI
  109. Chen, W. T. et al. GRP78 as a regulator of liver steatosis and cancer progression mediated by loss of the tumor suppressor PTEN. Oncogene, http://dx.doi.org/10.1038/onc.2013.437 (2013). · DOI
  110. Ji, C. et al. Liver-specific loss of glucose-regulated protein 78 perturbs the unfolded protein response and exacerbates a spectrum of liver diseases in mice. Hepatology 54, 229–239 (2011). · DOI
  111. Chen, W. T. et al. Liver-specific knockout of GRP94 in mice disrupts cell adhesion, activates liver progenitor cells, and accelerates liver tumorigenesis. Hepatology, 59, 947–957 (2013). This paper shows that GRP94 is essential in maintaining LPC quiescence and cell adhesion integrity because GRP94 deficiency in the liver leads to ERK activation and acceleration of PTEN-null-driven liver cancer progression. · DOI
  112. Cook, K. L., Clarke, P. A. & Clarke, R. Targeting GRP78 and antiestrogen resistance in breast cancer. Future Med. Chem. 5, 1047–1057 (2013). · DOI
  113. Gomer, C. J. et al. Photodynamic therapy-mediated oxidative stress can induce expression of heat shock proteins. Cancer Res. 56, 2355–2360 (1996).
  114. Li, B., Cheng, X. L., Yang, Y. P. & Li, Z. Q. GRP78 mediates radiation resistance of a stem cell-like subpopulation within the MCF-7 breast cancer cell line. Oncol. Rep. 30, 2119–2126 (2013). · DOI
  115. Roller, C. & Maddalo, D. The molecular chaperone GRP78/BiP in the development of chemoresistance: mechanism and possible treatment. Front. Pharmacol. 4, 10 (2013). · DOI
  116. Kern, J. et al. GRP-78 secreted by tumor cells blocks the antiangiogenic activity of bortezomib. Blood 114, 3960–3967 (2009). · DOI
  117. Yang, L., Li, H., Jiang, Y., Zuo, J. & Liu, W. Inhibition of mortalin expression reverses cisplatin resistance and attenuates growth of ovarian cancer cells. Cancer Lett. 336, 213–221 (2013). · DOI
  118. Thomas, S. et al. Repositioning of Verrucosidin, a purported inhibitor of chaperone protein GRP78, as an inhibitor of mitochondrial electron transport chain complex I. PLoS ONE 8, e65695 (2013). · DOI
  119. Su, S. F. et al. miR-30d, miR-181a and miR-199a-5p cooperatively suppress the endoplasmic reticulum chaperone and signaling regulator GRP78 in cancer. Oncogene 32, 4694–4701 (2013). · DOI
  120. Dong, D. et al. Spontaneous and controllable activation of suicide gene expression driven by the stress-inducible grp78 promoter resulting in eradication of sizable human tumors. Hum. Gene Ther. 15, 553–561 (2004). · DOI
  121. Azatian, A. et al. Effectiveness of HSV-tk suicide gene therapy driven by the Grp78 stress-inducible promoter in esophagogastric junction and gastric adenocarcinomas. J. Gastrointest. Surg. 13, 1044–1051 (2009). · DOI
  122. Kia, A. et al. Dual systemic tumor targeting with ligand-directed phage and Grp78 promoter induces tumor regression. Mol. Cancer Ther. 11, 2566–2577 (2012). · DOI
  123. Reddy, R. K. et al. Cancer-inducible transgene expression by the Grp94 promoter: spontaneous activation in tumors of various origins and cancer-associated macrophages. Cancer Res. 62, 7207–7212 (2002).
  124. Paton, A. W. et al. AB5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP. Nature 443, 548–552 (2006). · DOI
  125. Backer, J. M. et al. Chaperone-targeting cytotoxin and endoplasmic reticulum stress-inducing drug synergize to kill cancer cells. Neoplasia 11, 1165–1173 (2009). · DOI
  126. Prabhu, A., Sarcar, B., Kahali, S., Shan, Y. & Chinnaiyan, P. Targeting the unfolded protein response in glioblastoma cells with the fusion protein EGF-SubA. PLoS ONE 7, e52265 (2012). · DOI
  127. Ermakova, S. P. et al. (-)-Epigallocatechin gallate overcomes resistance to etoposide-induced cell death by targeting the molecular chaperone glucose-regulated protein 78. Cancer Res. 66, 9260–9269 (2006). · DOI
  128. Martin, S. et al. Inducing apoptosis of cancer cells using small-molecule plant compounds that bind to GRP78. Br. J. Cancer 109, 433–443 (2013). · DOI
  129. Deng, W. G., Ruan, K. H., Du, M., Saunders, M. A. & Wu, K. K. Aspirin and salicylate bind to immunoglobulin heavy chain binding protein (BiP) and inhibit its ATPase activity in human fibroblasts. FASEB J. 15, 2463–2470 (2001). · DOI
  130. Maddalo, D. et al. A peptidic unconjugated GRP78/BiP ligand modulates the unfolded protein response and induces prostate cancer cell death. PLoS ONE 7, e45690 (2012). · DOI
  131. Kahali, S. et al. Activation of the unfolded protein response contributes toward the antitumor activity of vorinostat. Neoplasia 12, 80–86 (2010). · DOI
  132. Duerfeldt, A. S. et al. Development of a Grp94 inhibitor. J. Am. Chem. Soc. 134, 9796–9804 (2012). · DOI
  133. Sheu, M. L., Liu, S. H. & Lan, K. H. Honokiol induces calpain-mediated glucose-regulated protein-94 cleavage and apoptosis in human gastric cancer cells and reduces tumor growth. PLoS ONE 2, e1096 (2007). · DOI
  134. Han, J. M. et al. Identification of gp96 as a novel target for treatment of autoimmune disease in mice. PLoS ONE 5, e9792 (2010). · DOI
  135. Kaul, S. C., Aida, S., Yaguchi, T., Kaur, K. & Wadhwa, R. Activation of wild type p53 function by its mortalin-binding, cytoplasmically localizing carboxyl terminus peptides. J. Biol. Chem. 280, 39373–39379 (2005). · DOI
  136. Wadhwa, R. et al. Selective toxicity of MKT-077 to cancer cells is mediated by its binding to the hsp70 family protein mot-2 and reactivation of p53 function. Cancer Res. 60, 6818–6821 (2000).
  137. Lu, W. J. et al. Mortalin-p53 interaction in cancer cells is stress dependent and constitutes a selective target for cancer therapy. Cell Death Differ. 18, 1046–1056 (2011). References 138 and 139 show GRP75 sequesters wild-type p53 in the cytoplasm and that disruption of the interaction between GRP75 and p53 can reactivate p53 function and induce tumour cell-specific apoptosis. · DOI
  138. Utomo, D. H., Widodo, N. & Rifa'i, M. Identifications small molecules inhibitor of p53-mortalin complex for cancer drug using virtual screening. Bioinformation 8, 426–429 (2012). · DOI
  139. Jakobsen, C. G., Rasmussen, N., Laenkholm, A. V. & Ditzel, H. J. Phage display derived human monoclonal antibodies isolated by binding to the surface of live primary breast cancer cells recognize GRP78. Cancer Res. 67, 9507–9517 (2007). · DOI
  140. Arap, M. A. et al. Cell surface expression of the stress response chaperone GRP78 enables tumor targeting by circulating ligands. Cancer Cell 6, 275–284 (2004). This paper provides the first preclinical data showing that GRP78-binding peptide motifs specificallytarget tumour cells and that, when fused to a programmed cell death-inducing sequence, they can suppress tumour growth in xenograft and isogenic mouse models of prostate and breast cancer. · DOI
  141. Kim, Y. et al. Targeting heat shock proteins on cancer cells: selection, characterization, and cell-penetrating properties of a peptidic GRP78 ligand. Biochemistry 45, 9434–9444 (2006). · DOI
  142. Liu, Y. et al. Mechanistic studies of a peptidic GRP78 ligand for cancer cell-specific drug delivery. Mol. Pharm. 4, 435–447 (2007). · DOI
  143. Passarella, R. J. et al. Targeted nanoparticles that deliver a sustained, specific release of Paclitaxel to irradiated tumors. Cancer Res. 70, 4550–4559 (2010). · DOI
  144. Larson, N., Ray, A., Malugin, A., Pike, D. B. & Ghandehari, H. HPMA copolymer-aminohexylgeldanamycin conjugates targeting cell surface expressed GRP78 in prostate cancer. Pharm. Res. 27, 2683–2693 (2010). · DOI
  145. Uckun, F. M. et al. Inducing apoptosis in chemotherapy-resistant B-lineage acute lymphoblastic leukaemia cells by targeting HSPA5, a master regulator of the anti-apoptotic unfolded protein response signalling network. Br. J. Haematol. 153, 741–752 (2011). · DOI
  146. Kang, J. et al. A peptide derived from phage display library exhibits anti-tumor activity by targeting GRP78 in gastric cancer multidrug resistance cells. Cancer Lett. 339, 247–259 (2013). · DOI
  147. Delie, F., Petignat, P. & Cohen, M. GRP78-targeted nanotherapy against castrate-resistant prostate cancer cells expressing membrane GRP78. Target Oncol. 8, 225–230 (2013). · DOI
  148. Li, Z. et al. Reconstructed mung bean trypsin inhibitor targeting cell surface GRP78 induces apoptosis and inhibits tumor growth in colorectal cancer. Int. J. Biochem. Cell. Biol. 47, 68–75 (2014). · DOI
  149. de Ridder, G. G., Ray, R. & Pizzo, S. V. A murine monoclonal antibody directed against the carboxyl-terminal domain of GRP78 suppresses melanoma growth in mice. Melanoma Res. 22, 225–235 (2012). · DOI
  150. Rauschert, N. et al. A new tumor-specific variant of GRP78 as target for antibody-based therapy. Lab. Invest. 88, 375–386 (2008). · DOI
  151. Rasche, L. et al. The natural human IgM antibody PAT-SM6 induces apoptosis in primary human multiple myeloma cells by targeting heat shock protein GRP78. PLoS ONE 8, e63414 (2013). · DOI
  152. Hensel, F., Eckstein, M., Rosenwald, A. & Brandlein, S. Early development of PAT-SM6 for the treatment of melanoma. Melanoma Res. 23, 264–275 (2013). · DOI
  153. Cohen, M. & Petignat, P. Purified autoantibodies against glucose-regulated protein 78 (GRP78) promote apoptosis and decrease invasiveness of ovarian cancer cells. Cancer Lett. 309, 104–109 (2011). · DOI
  154. Al-Hashimi, A. A. et al. Binding of anti-GRP78 autoantibodies to cell surface GRP78 increases tissue factor procoagulant activity via the release of calcium from endoplasmic reticulum stores. J. Biol. Chem. 285, 28912–28923 (2010). · DOI
  155. Arnouk, H. et al. Tumour secreted grp170 chaperones full-length protein substrates and induces an adaptive anti-tumour immune response in vivo. Int. J. Hyperthermia 26, 366–375 (2010). · DOI
  156. Schreiber, T. H., Deyev, V. V., Rosenblatt, J. D. & Podack, E. R. Tumor-induced suppression of CTL expansion and subjugation by gp96-Ig vaccination. Cancer Res. 69, 2026–2033 (2009). · DOI
  157. Randazzo, M., Terness, P., Opelz, G. & Kleist, C. Active-specific immunotherapy of human cancers with the heat shock protein Gp96-revisited. Int. J. Cancer 130, 2219–2231 (2012). · DOI
  158. Reitsma, D. J. & Combest, A. J. Challenges in the development of an autologous heat shock protein based anti-tumor vaccine. Hum. Vaccin. Immunother. 8, 1152–1155 (2012). · DOI
  159. Colaco, C. Autologous heat-shock protein vaccines. Hum. Vaccin. Immunother. 9, 275–276 (2013). · DOI
  160. Li, X. et al. Induction of regulatory T cells by high-dose gp96 suppresses murine liver immune hyperactivation. PLoS ONE 8, e68997 (2013). · DOI
  161. Zhao, B. et al. TAT-mediated gp96 transduction to APCs enhances gp96-induced antiviral and antitumor T cell responses. Vaccine 31, 545–552 (2013). · DOI
  162. Wang, X. Y. et al. Superior antitumor response induced by large stress protein chaperoned protein antigen compared with peptide antigen. J. Immunol. 184, 6309–6319 (2010). This paper shows that GRP170, which is a high molecular weight chaperone, is superior to conventional chaperones as a vaccine platform to deliver large protein antigens to augment antitumour immune responses. · DOI
  163. Wang, X. Y. et al. Extracellular targeting of endoplasmic reticulum chaperone glucose-regulated protein 170 enhances tumor immunity to a poorly immunogenic melanoma. J. Immunol. 177, 1543–1551 (2006). · DOI
  164. Gao, P., Sun, X., Chen, X., Subjeck, J. & Wang, X. Y. Secretion of stress protein grp170 promotes immune-mediated inhibition of murine prostate tumor. Cancer Immunol. Immunother. 58, 1319–1328 (2009). · DOI
  165. Yu, X. et al. A multifunctional chimeric chaperone serves as a novel immune modulator inducing therapeutic antitumor immunity. Cancer Res. 73, 2093–2103 (2013). · DOI
  166. Tamura, Y. et al. Tumor-produced secreted form of binding of immunoglobulin protein elicits antigen-specific tumor immunity. J. Immunol. 186, 4325–4330 (2011). · DOI
  167. Lee, A. S. in Protein Discovery Technologies (eds Pasqualini, R., & Arap, W.) 129–140 (CRC Press, 2009).
  168. Pouyssegur, J., Shiu, R. P. & Pastan, I. Induction of two transformation-sensitive membrane polypeptides in normal fibroblasts by a block in glycoprotein synthesis or glucose deprivation. Cell 11, 941–947 (1977). · DOI
  169. Hightower, L. E. Cultured animal cells exposed to amino acid analogues or puromycin rapidly synthesize several polypeptides. J. Cell. Physiol. 102, 407–427 (1980). · DOI
  170. Munro, S. & Pelham, H. R. An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46, 291–300 (1986). · DOI
  171. Bole, D. G., Hendershot, L. M. & Kearney, J. F. Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J. Cell Biol. 102, 1558–1566 (1986). · DOI
  172. Haas, I. G. & Wabl, M. Immunoglobulin heavy chain binding protein. Nature 306, 387–389 (1983). · DOI
  173. Hendershot, L. M. et al. In vivo expression of mammalian BiP ATPase mutants causes disruption of the endoplasmic reticulum. Mol. Biol. Cell 6, 283–296 (1995). · DOI
  174. Lee, A. S., Bell, J. & Ting, J. Biochemical characterization of the 94- and 78-kilodalton glucose-regulated proteins in hamster fibroblasts. J. Biol. Chem. 259, 4616–4621 (1984). · DOI
  175. Koch, G., Smith, M., Macer, D., Webster, P. & Mortara, R. Endoplasmic reticulum contains a common, abundant calcium-binding glycoprotein, endoplasmin. J. Cell Sci. 86, 217–232 (1986). · DOI
  176. Mazzarella, R. A. & Green, M. ERp99, an abundant, conserved glycoprotein of the endoplasmic reticulum, is homologous to the 90-kDa heat shock protein (hsp90) and the 94-kDa glucose regulated protein (GRP94). J. Biol. Chem. 262, 8875–8883 (1987). · DOI
  177. Maki, R. G., Old, L. J. & Srivastava, P. K. Human homologue of murine tumor rejection antigen gp96: 5′-regulatory and coding regions and relationship to stress-induced proteins. Proc. Natl Acad. Sci. USA 87, 5658–5662 (1990). · DOI
  178. Johnson, J. L. Evolution and function of diverse Hsp90 homologs and cochaperone proteins. Biochim. Biophys. Acta 1823, 607–613 (2012). · DOI
  179. Schild, H. & Rammensee, H. G. gp96—the immune system's Swiss army knife. Nature Immunol. 1, 100–101 (2000). · DOI
  180. Wadhwa, R., Kaul, S. C., Ikawa, Y. & Sugimoto, Y. Identification of a novel member of mouse hsp70 family. Its association with cellular mortal phenotype. J. Biol. Chem. 268, 6615–6621 (1993). · DOI
  181. Sciandra, J. J. & Subjeck, J. R. The effects of glucose on protein synthesis and thermosensitivity in Chinese hamster ovary cells. J. Biol. Chem. 258, 12091–12093 (1983). · DOI
  182. Chen, X. et al. The 170 kDa glucose regulated stress protein is a large HSP70-, HSP110-like protein of the endoplasmic reticulum. FEBS Lett. 380, 68–72 (1996). · DOI
  183. Kuwabara, K. et al. Purification and characterization of a novel stress protein, the 150-kDa oxygen-regulated protein (ORP150), from cultured rat astrocytes and its expression in ischemic mouse brain. J. Biol. Chem. 271, 5025–5032 (1996). · DOI
  184. Sciandra, J. J., Subjeck, J. R. & Hughes, C. S. Induction of glucose-regulated proteins during anaerobic exposure and of heat-shock proteins after reoxygenation. Proc. Natl Acad. Sci. USA 81, 4843–4847 (1984). · DOI
  185. Yoshida, H., Haze, K., Yanagi, H., Yura, T. & Mori, K. 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, 33741–33749 (1998). · DOI
  186. 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. 27, 1437–1443 (1999). · DOI
  187. Baumeister, P. et al. Endoplasmic reticulum stress induction of the Grp78/BiP promoter: activating mechanisms mediated by YY1 and its interactive chromatin modifiers. Mol. Cell. Biol. 25, 4529–4540 (2005). · DOI
  188. Hong, M. et al. Transcriptional regulation of the Grp78 promoter by endoplasmic reticulum stress: role of TFII-I and its tyrosine phosphorylation. J. Biol. Chem. 280, 16821–16828 (2005). · DOI
  189. Lee, A. H., Iwakoshi, N. N. & Glimcher, L. H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23, 7448–7459 (2003). · DOI
  190. Kaneda, S., Yura, T. & Yanagi, H. Production of three distinct mRNAs of 150 kDa oxygen-regulated protein (ORP150) by alternative promoters: preferential induction of one species under stress conditions. J. Biochem. 128, 529–538 (2000). · DOI
  191. Giorgi, C., De Stefani, D., Bononi, A., Rizzuto, R. & Pinton, P. Structural and functional link between the mitochondrial network and the endoplasmic reticulum. Int. J. Biochem. Cell. Biol. 41, 1817–1827 (2009). · DOI
  192. Hayashi, T., Rizzuto, R., Hajnoczky, G. & Su, T. P. MAM: more than just a housekeeper. Trends Cell Biol. 19, 81–88 (2009). · DOI · Paper page
  193. Hetz, C. A. ER stress signaling and the BCL-2 family of proteins: from adaptation to irreversible cellular damage. Antioxid. Redox Signal. 9, 2345–2355 (2007). · DOI
  194. Ouyang, Y. B., Xu, L. J., Emery, J. F., Lee, A. S. & Giffard, R. G. Overexpressing GRP78 influences Ca2+ handling and function of mitochondria in astrocytes after ischemia-like stress. Mitochondrion 11, 279–286 (2011). · DOI
  195. Sun, F. C. et al. Localization of GRP78 to mitochondria under the unfolded protein response. Biochem. J. 396, 31–39 (2006). · DOI
  196. Ye, R. et al. Grp78 heterozygosity promotes adaptive unfolded protein response and attenuates diet-induced obesity and insulin resistance. Diabetes 59, 6–16 (2010). · DOI
  197. Mao, C. et al. Targeted mutation of the mouse Grp94 gene disrupts development and perturbs endoplasmic reticulum stress signaling. PLoS ONE 5, e10852 (2010). · DOI

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Metadata

Authors
Lee, A. S.
Venue
Nature Reviews Cancer
Publisher
Springer Science and Business Media LLC
Published
2014-03-24
Volume
14
Issue
4
Pages
263-276
ISSN
  • 1474-175X
  • 1474-1768
DOI
10.1038/nrc3701
PMC
PMC4158750
Cited by
587
References
3
Language
en
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