Journal of Breast Cancer

Korean Breast Cancer Society (한국유방암학회)
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New Insights into the Role of Endoplasmic Reticulum Stress in Breast Cancer Metastasis

  • Han, Chang-chang (Department of Biochemistry and Molecular Biology, School of Basic Medicine, Nanchang University) ;
  • Wan, Fu-sheng (Department of Biochemistry and Molecular Biology, School of Basic Medicine, Nanchang University)
  • Received : 2017.11.25
  • Accepted : 2018.09.24
  • Published : 2018.12.31
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Abstract

Cellular stress severely disrupts endoplasmic reticulum (ER) function, leading to the abnormal accumulation of unfolded or misfolded proteins in the ER and subsequent development of endoplasmic reticulum stress (ERS). To accommodate the occurrence of ERS, cells have evolved a highly conserved, selfprotecting signal transduction pathway called the unfolded protein response. Notably, ERS signaling is involved in the development of a variety of diseases and is closely related to tumor development, particularly in breast cancer. This review discusses recent research regarding associations between ERS and tumor metastasis. The information presented here will help researchers elucidate the precise mechanisms underlying ERS-mediated tumor metastasis and provide new directions for tumor therapies.

Keywords

Acknowledgement

Supported by : National Natural Science Foundation of China

References

  1. DeSantis C, Ma J, Bryan L, Jemal A. Breast cancer statistics, 2013. CA Cancer J Clin 2014;64:52-62. https://doi.org/10.3322/caac.21203
  2. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin 2015;65:87-108. https://doi.org/10.3322/caac.21262
  3. Wang M, Kaufman RJ. Protein misfolding in the endoplasmic reticulum as a conduit to human disease. Nature 2016;529:326-35. https://doi.org/10.1038/nature17041
  4. Yu H, Su J, Xu Y, Kang J, Li H, Zhang L, et al. p62/SQSTM1 involved in cisplatin resistance in human ovarian cancer cells by clearing ubiquitinated proteins. Eur J Cancer 2011;47:1585-94. https://doi.org/10.1016/j.ejca.2011.01.019
  5. Li Y, Guo Y, Tang J, Jiang J, Chen Z. New insights into the roles of CHOP-induced apoptosis in ER stress. Acta Biochim Biophys Sin (Shanghai) 2014;46:629-40. https://doi.org/10.1093/abbs/gmu048
  6. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001;107:881-91. https://doi.org/10.1016/S0092-8674(01)00611-0
  7. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000;5:897-904. https://doi.org/10.1016/S1097-2765(00)80330-5
  8. Rodrigues LM, Theodoro TR, Matos LL, Mader AM, Milani C, Pinhal MA. Heparanase isoform expression and extracellular matrix remodeling in intervertebral disc degenerative disease. Clinics (Sao Paulo) 2011;66:903-9. https://doi.org/10.1590/S1807-59322011000500030
  9. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010;141:52-67. https://doi.org/10.1016/j.cell.2010.03.015
  10. Malek AV, Bershtein LM, Filatov MV, Beliaev AM. Exosomal intercellular communication system and its role in the process of metastatic dissemination. Vopr Onkol 2014;60:429-36.
  11. Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med 2006;12:895-904. https://doi.org/10.1038/nm1469
  12. Lee AS. Glucose-regulated proteins in cancer: molecular mechanisms and therapeutic potential. Nat Rev Cancer 2014;14:263-76. https://doi.org/10.1038/nrc3701
  13. Bobrovnikova-Marjon E, Grigoriadou C, Pytel D, Zhang F, Ye J, Koumenis C, et al. PERK promotes cancer cell proliferation and tumor growth by limiting oxidative DNA damage. Oncogene 2010;29:3881-95. https://doi.org/10.1038/onc.2010.153
  14. Huber AL, Lebeau J, Guillaumot P, Petrilli V, Malek M, Chilloux J, et al. p58(IPK)-mediated attenuation of the proapoptotic PERK-CHOP pathway allows malignant progression upon low glucose. Mol Cell 2013;49:1049-59. https://doi.org/10.1016/j.molcel.2013.01.009
  15. Qin XJ, Ling BX. Proteomic studies in breast cancer (Review). Oncol Lett 2012;3:735-43.
  16. Gnant M, Balic M, Petru E, Raunik W, Singer CF, Steger GG, et al. Treatment of bone metastases in patients with advanced breast cancer. Breast Care (Basel) 2012;7:92-8. https://doi.org/10.1159/000338650
  17. Li Y, Liu H, Huang YY, Pu LJ, Zhang XD, Jiang CC, et al. Suppression of endoplasmic reticulum stress-induced invasion and migration of breast cancer cells through the downregulation of heparanase. Int J Mol Med 2013;31:1234-42. https://doi.org/10.3892/ijmm.2013.1292
  18. Zhang Y, Liao S, Fan W, Wei W, Wang C, Sun S. Tunicamycin-induced ER stress regulates chemokine CCL5 expression and secretion via STAT3 followed by decreased transmigration of MCF-7 breast cancer cells. Oncol Rep 2014;32:2769-76. https://doi.org/10.3892/or.2014.3479
  19. Duffy MJ, Maguire TM, Hill A, McDermott E, O'Higgins N. Metalloproteinases: role in breast carcinogenesis, invasion and metastasis. Breast Cancer Res 2000;2:252-7. https://doi.org/10.1186/bcr65
  20. Trimboli AJ, Fukino K, de Bruin A, Wei G, Shen L, Tanner SM, et al. Direct evidence for epithelial-mesenchymal transitions in breast cancer. Cancer Res 2008;68:937-45. https://doi.org/10.1158/0008-5472.CAN-07-2148
  21. Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell 2007;25:193-205. https://doi.org/10.1016/j.molcel.2006.12.009
  22. Ishikawa K, Takenaga K, Akimoto M, Koshikawa N, Yamaguchi A, Imanishi H, et al. ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 2008;320:661-4. https://doi.org/10.1126/science.1156906
  23. Lee AS. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem Sci 2001;26:504-10. https://doi.org/10.1016/S0968-0004(01)01908-9
  24. Monnerjahn C, Techel D, Meyer U, Rensing L. The grp78 promoter of Neurospora crassa: constitutive, stress and differentiation-dependent protein-binding patterns. Curr Genet 2001;39:319-26. https://doi.org/10.1007/s002940100202
  25. Ni M, Lee AS. ER chaperones in mammalian development and human diseases. FEBS Lett 2007;581:3641-51. https://doi.org/10.1016/j.febslet.2007.04.045
  26. Little E, Ramakrishnan M, Roy B, Gazit G, Lee AS. The glucose-regulated proteins (GRP78 and GRP94): functions, gene regulation, and applications. Crit Rev Eukaryot Gene Expr 1994;4:1-18. https://doi.org/10.1615/CritRevEukarGeneExpr.v4.i1.10
  27. Haas IG. BiP (GRP78), an essential hsp70 resident protein in the endoplasmic reticulum. Experientia 1994;50:1012-20. https://doi.org/10.1007/BF01923455
  28. Lee E, Nichols P, Spicer D, Groshen S, Yu MC, Lee AS. GRP78 as a novel predictor of responsiveness to chemotherapy in breast cancer. Cancer Res 2006;66:7849-53. https://doi.org/10.1158/0008-5472.CAN-06-1660
  29. Scriven P, Coulson S, Haines R, Balasubramanian S, Cross S, Wyld L. Activation and clinical significance of the unfolded protein response in breast cancer. Br J Cancer 2009;101:1692-8. https://doi.org/10.1038/sj.bjc.6605365
  30. Fernandez PM, Tabbara SO, Jacobs LK, Manning FC, Tsangaris TN, Schwartz AM, et al. Overexpression of the glucose-regulated stress gene GRP78 in malignant but not benign human breast lesions. Breast Cancer Res Treat 2000;59:15-26. https://doi.org/10.1023/A:1006332011207
  31. Liang Y, O'Driscoll L, McDonnell S, Doolan P, Oglesby I, Duffy K, et al. Enhanced in vitro invasiveness and drug resistance with altered gene expression patterns in a human lung carcinoma cell line after pulse selection with anticancer drugs. Int J Cancer 2004;111:484-93. https://doi.org/10.1002/ijc.20230
  32. Liu R, Li X, Gao W, Zhou Y, Wey S, Mitra SK, et al. Monoclonal antibody against cell surface GRP78 as a novel agent in suppressing PI3K/AKT signaling, tumor growth, and metastasis. Clin Cancer Res 2013;19:6802-11. https://doi.org/10.1158/1078-0432.CCR-13-1106
  33. Lee E, Nichols P, Groshen S, Spicer D, Lee AS. GRP78 as potential predictor for breast cancer response to adjuvant taxane therapy. Int J Cancer 2011;128:726-31. https://doi.org/10.1002/ijc.25370
  34. Kuang XY, Jiang HS, Li K, Zheng YZ, Liu YR, Qiao F, et al. The phosphorylation-specific association of STMN1 with GRP78 promotes breast cancer metastasis. Cancer Lett 2016;377:87-96. https://doi.org/10.1016/j.canlet.2016.04.035
  35. Yuan XP, Dong M, Li X, Zhou JP. GRP78 promotes the invasion of pancreatic cancer cells by FAK and JNK. Mol Cell Biochem 2015;398:55-62. https://doi.org/10.1007/s11010-014-2204-2
  36. Decock J, Thirkettle S, Wagstaff L, Edwards DR. Matrix metalloproteinases: protective roles in cancer. J Cell Mol Med 2011;15:1254-65. https://doi.org/10.1111/j.1582-4934.2011.01302.x
  37. Turpeenniemi-Hujanen T. Gelatinases (MMP-2 and -9) and their natural inhibitors as prognostic indicators in solid cancers. Biochimie 2005;87:287-97. https://doi.org/10.1016/j.biochi.2005.01.014
  38. Hsu FN, Yang MS, Lin E, Tseng CF, Lin H. The significance of Her2 on androgen receptor protein stability in the transition of androgen requirement in prostate cancer cells. Am J Physiol Endocrinol Metab 2011;300:E902-8. https://doi.org/10.1152/ajpendo.00610.2010
  39. Lynch CC, Hikosaka A, Acuff HB, Martin MD, Kawai N, Singh RK, et al. MMP-7 promotes prostate cancer-induced osteolysis via the solubilization of RANKL. Cancer Cell 2005;7:485-96. https://doi.org/10.1016/j.ccr.2005.04.013
  40. Indelicato M, Pucci B, Schito L, Reali V, Aventaggiato M, Mazzarino MC, et al. Role of hypoxia and autophagy in MDA-MB-231 invasiveness. J Cell Physiol 2010;223:359-68.
  41. Park GY, Han YK, Han JY, Lee CG. Tauroursodeoxycholic acid reduces the invasion of MDA-MB-231 cells by modulating matrix metalloproteinases 7 and 13. Oncol Lett 2016;12:2227-31. https://doi.org/10.3892/ol.2016.4842
  42. Zhu H, Chen X, Chen B, Chen B, Song W, Sun D, et al. Activating transcription factor 4 promotes esophageal squamous cell carcinoma invasion and metastasis in mice and is associated with poor prognosis in human patients. PLoS One 2014;9:e103882. https://doi.org/10.1371/journal.pone.0103882
  43. Pei S, Yang X, Wang H, Zhang H, Zhou B, Zhang D, et al. Plantamajoside, a potential anti-tumor herbal medicine inhibits breast cancer growth and pulmonary metastasis by decreasing the activity of matrix metalloproteinase-9 and -2. BMC Cancer 2015;15:965. https://doi.org/10.1186/s12885-015-1960-z
  44. Li H, Huang F, Fan L, Jiang Y, Wang X, Li J, et al. Phosphatidylethanolamine-binding protein 4 is associated with breast cancer metastasis through Src-mediated Akt tyrosine phosphorylation. Oncogene 2014;33:4589-98. https://doi.org/10.1038/onc.2013.408
  45. Cardiff RD. Epithelial to mesenchymal transition tumors: fallacious or snail's pace? Clin Cancer Res 2005;11(24 Pt 1):8534-7. https://doi.org/10.1158/1078-0432.CCR-05-2250
  46. Gjerdrum C, Tiron C, Hoiby T, Stefansson I, Haugen H, Sandal T, et al. Axl is an essential epithelial-to-mesenchymal transition-induced regulator of breast cancer metastasis and patient survival. Proc Natl Acad Sci U S A 2010;107:1124-9. https://doi.org/10.1073/pnas.0909333107
  47. Oliveras-Ferraros C, Cufi S, Vazquez-Martin A, Torres-Garcia VZ, Del Barco S, Martin-Castillo B, et al. Micro(mi)RNA expression profile of breast cancer epithelial cells treated with the anti-diabetic drug metformin: induction of the tumor suppressor miRNA let-7a and suppression of the TGFbeta-induced oncomiR miRNA-181a. Cell Cycle 2011;10:1144-51. https://doi.org/10.4161/cc.10.7.15210
  48. Shah PP, Dupre TV, Siskind LJ, Beverly LJ. Common cytotoxic chemotherapeutics induce epithelial-mesenchymal transition (EMT) downstream of ER stress. Oncotarget 2017;8:22625-39.
  49. Zhong Q, Zhou B, Ann DK, Minoo P, Liu Y, Banfalvi A, et al. Role of endoplasmic reticulum stress in epithelial-mesenchymal transition of alveolar epithelial cells: effects of misfolded surfactant protein. Am J Respir Cell Mol Biol 2011;45:498-509. https://doi.org/10.1165/rcmb.2010-0347OC
  50. Li H, Chen X, Gao Y, Wu J, Zeng F, Song F. XBP1 induces snail expression to promote epithelial-to-mesenchymal transition and invasion of breast cancer cells. Cell Signal 2015;27:82-9. https://doi.org/10.1016/j.cellsig.2014.09.018
  51. Cubillos-Ruiz JR, Bettigole SE, Glimcher LH. Tumorigenic and immunosuppressive effects of endoplasmic reticulum stress in cancer. Cell 2017;168:692-706. https://doi.org/10.1016/j.cell.2016.12.004
  52. Feng YX, Sokol ES, Del Vecchio CA, Sanduja S, Claessen JH, Proia TA, et al. Epithelial-to-mesenchymal transition activates PERK-eIF2alpha and sensitizes cells to endoplasmic reticulum stress. Cancer Discov 2014;4:702-15. https://doi.org/10.1158/2159-8290.CD-13-0945
  53. Zhang D, Richardson DR. Endoplasmic reticulum protein 29 (ERp29): an emerging role in cancer. Int J Biochem Cell Biol 2011;43:33-6. https://doi.org/10.1016/j.biocel.2010.09.019
  54. Bambang IF, Xu S, Zhou J, Salto-Tellez M, Sethi SK, Zhang D. Overexpression of endoplasmic reticulum protein 29 regulates mesenchymalepithelial transition and suppresses xenograft tumor growth of invasive breast cancer cells. Lab Invest 2009;89:1229-42. https://doi.org/10.1038/labinvest.2009.87
  55. Zweitzig DR, Smirnov DA, Connelly MC, Terstappen LW, O'Hara SM, Moran E. Physiological stress induces the metastasis marker AGR2 in breast cancer cells. Mol Cell Biochem 2007;306:255-60. https://doi.org/10.1007/s11010-007-9562-y
  56. Liu D, Rudland PS, Sibson DR, Platt-Higgins A, Barraclough R. Human homologue of cement gland protein, a novel metastasis inducer associated with breast carcinomas. Cancer Res 2005;65:3796-805. https://doi.org/10.1158/0008-5472.CAN-04-3823
  57. Berardi DE, Campodonico PB, Diaz Bessone MI, Urtreger AJ, Todaro LB. Autophagy: friend or foe in breast cancer development, progression, and treatment. Int J Breast Cancer 2011;2011:595092.
  58. Akar U, Chaves-Reyez A, Barria M, Tari A, Sanguino A, Kondo Y, et al. Silencing of Bcl-2 expression by small interfering RNA induces autophagic cell death in MCF-7 breast cancer cells. Autophagy 2008;4:669-79. https://doi.org/10.4161/auto.6083
  59. Chiavarina B, Whitaker-Menezes D, Migneco G, Martinez-Outschoorn UE, Pavlides S, Howell A, et al. HIF1-alpha functions as a tumor promoter in cancer associated fibroblasts, and as a tumor suppressor in breast cancer cells: autophagy drives compartment-specific oncogenesis. Cell Cycle 2010;9:3534-51. https://doi.org/10.4161/cc.9.17.12908
  60. Vanderlaag K, Su Y, Frankel AE, Burghardt RC, Barhoumi R, Chadalapaka G, et al. 1,1-Bis(3'-indolyl)-1-(p-substituted phenyl)methanes induce autophagic cell death in estrogen receptor negative breast cancer. BMC Cancer 2010;10:669. https://doi.org/10.1186/1471-2407-10-669
  61. Koren I, Kimchi A. Cell biology: promoting tumorigenesis by suppressing autophagy. Science 2012;338:889-90. https://doi.org/10.1126/science.1230577
  62. Schroder M, Sutcliffe L. Consequences of stress in the secretory pathway: the ER stress response and its role in the metabolic syndrome. Methods Mol Biol 2010;648:43-62.
  63. White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer 2012;12:401-10. https://doi.org/10.1038/nrc3262
  64. Shimada Y, Kobayashi H, Kawagoe S, Aoki K, Kaneshiro E, Shimizu H, et al. Endoplasmic reticulum stress induces autophagy through activation of p38 MAPK in fibroblasts from Pompe disease patients carrying c.546G>T mutation. Mol Genet Metab 2011;104:566-73. https://doi.org/10.1016/j.ymgme.2011.09.005
  65. Zismanov V, Lishner M, Tartakover-Matalon S, Radnay J, Shapiro H, Drucker L. Tetraspanin-induced death of myeloma cell lines is autophagic and involves increased UPR signalling. Br J Cancer 2009;101:1402-9. https://doi.org/10.1038/sj.bjc.6605291
  66. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, et al. ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamineinduced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 2007;14:230-9. https://doi.org/10.1038/sj.cdd.4401984
  67. Fujita E, Kouroku Y, Isoai A, Kumagai H, Misutani A, Matsuda C, et al. Two endoplasmic reticulum-associated degradation (ERAD) systems for the novel variant of the mutant dysferlin: ubiquitin/proteasome ERAD(I) and autophagy/lysosome ERAD(II). Hum Mol Genet 2007;16:618-29. https://doi.org/10.1093/hmg/ddm002
  68. Kim KW, Moretti L, Mitchell LR, Jung DK, Lu B. Endoplasmic reticulum stress mediates radiation-induced autophagy by perk-eIF2alpha in caspase-3/7-deficient cells. Oncogene 2010;29:3241-51. https://doi.org/10.1038/onc.2010.74
  69. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 2006;26:9220-31. https://doi.org/10.1128/MCB.01453-06
  70. Milani M, Rzymski T, Mellor HR, Pike L, Bottini A, Generali D, et al. The role of ATF4 stabilization and autophagy in resistance of breast cancer cells treated with Bortezomib. Cancer Res 2009;69:4415-23. https://doi.org/10.1158/0008-5472.CAN-08-2839
  71. Park MA, Walker T, Martin AP, Allegood J, Vozhilla N, Emdad L, et al. MDA-7/IL-24-induced cell killing in malignant renal carcinoma cells occurs by a ceramide/CD95/PERK-dependent mechanism. Mol Cancer Ther 2009;8:1280-91. https://doi.org/10.1158/1535-7163.MCT-09-0073
  72. Li Z, Li Z. Glucose regulated protein 78: a critical link between tumor microenvironment and cancer hallmarks. Biochim Biophys Acta 2012;1826:13-22.
  73. Luo B, Lee AS. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene 2013;32:805-18. https://doi.org/10.1038/onc.2012.130
  74. Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 2011;36:30-8. https://doi.org/10.1016/j.tibs.2010.07.007
  75. McAllister SD, Murase R, Christian RT, Lau D, Zielinski AJ, Allison J, et al. Pathways mediating the effects of cannabidiol on the reduction of breast cancer cell proliferation, invasion, and metastasis. Breast Cancer Res Treat 2011;129:37-47. https://doi.org/10.1007/s10549-010-1177-4
  76. Wu W, Ye H, Wan L, Han X, Wang G, Hu J, et al. Millepachine, a novel chalcone, induces G2/M arrest by inhibiting CDK1 activity and causing apoptosis via ROS-mitochondrial apoptotic pathway in human hepatocarcinoma cells in vitro and in vivo. Carcinogenesis 2013;34:1636-43. https://doi.org/10.1093/carcin/bgt087
  77. Cho SG, Woo SM, Ko SG. Butein suppresses breast cancer growth by reducing a production of intracellular reactive oxygen species. J Exp Clin Cancer Res 2014;33:51. https://doi.org/10.1186/1756-9966-33-51
  78. Xiong Y, Ye T, Wang M, Xia Y, Wang N, Song X, et al. A novel cinnamide YLT26 induces breast cancer cells apoptosis via ROS-mitochondrial apoptotic pathway in vitro and inhibits lung metastasis in vivo. Cell Physiol Biochem 2014;34:1863-76. https://doi.org/10.1159/000366385
  79. Hung JY, Hsu YL, Ni WC, Tsai YM, Yang CJ, Kuo PL, et al. Oxidative and endoplasmic reticulum stress signaling are involved in dehydrocostuslactone-mediated apoptosis in human non-small cell lung cancer cells. Lung Cancer 2010;68:355-65. https://doi.org/10.1016/j.lungcan.2009.07.017
  80. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, et al. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 2004;18:3066-77. https://doi.org/10.1101/gad.1250704
  81. Auf G, Jabouille A, Guerit S, Pineau R, Delugin M, Bouchecareilh M, et al. Inositol-requiring enzyme 1alpha is a key regulator of angiogenesis and invasion in malignant glioma. Proc Natl Acad Sci U S A 2010;107:15553-8. https://doi.org/10.1073/pnas.0914072107
  82. Jamison S, Lin Y, Lin W. Pancreatic endoplasmic reticulum kinase activation promotes medulloblastoma cell migration and invasion through induction of vascular endothelial growth factor A. PLoS One 2015;10:e0120252. https://doi.org/10.1371/journal.pone.0120252
  83. Lin W, Lin Y, Li J, Harding HP, Ron D, Jamison S. A deregulated integrated stress response promotes interferon-gamma-induced medulloblastoma. J Neurosci Res 2011;89:1586-95. https://doi.org/10.1002/jnr.22693
  84. Chen X, Iliopoulos D, Zhang Q, Tang Q, Greenblatt MB, Hatziapostolou M, et al. XBP1 promotes triple-negative breast cancer by controlling the HIF1alpha pathway. Nature 2014;508:103-7. https://doi.org/10.1038/nature13119
  85. Mujcic H, Rzymski T, Rouschop KM, Koritzinsky M, Milani M, Harris AL, et al. Hypoxic activation of the unfolded protein response (UPR) induces expression of the metastasis-associated gene LAMP3. Radiother Oncol 2009;92:450-9. https://doi.org/10.1016/j.radonc.2009.08.017
  86. Nagelkerke A, Bussink J, Mujcic H, Wouters BG, Lehmann S, Sweep FC, et al. Hypoxia stimulates migration of breast cancer cells via the PERK/ATF4/LAMP3-arm of the unfolded protein response. Breast Cancer Res 2013;15:R2. https://doi.org/10.1186/bcr3373
  87. Dey S, Sayers CM, Verginadis II, Lehman SL, Cheng Y, Cerniglia GJ, et al. ATF4-dependent induction of heme oxygenase 1 prevents anoikis and promotes metastasis. J Clin Invest 2015;125:2592-608. https://doi.org/10.1172/JCI78031
  88. Park SH, Kim J, Do KH, Park J, Oh CG, Choi HJ, et al. Activating transcription factor 3-mediated chemo-intervention with cancer chemokines in a noncanonical pathway under endoplasmic reticulum stress. J Biol Chem 2014;289:27118-33. https://doi.org/10.1074/jbc.M114.568717
  89. Gu F, Nguyen DT, Stuible M, Dube N, Tremblay ML, Chevet E. Proteintyrosine phosphatase 1B potentiates IRE1 signaling during endoplasmic reticulum stress. J Biol Chem 2004;279:49689-93. https://doi.org/10.1074/jbc.C400261200
  90. Julien SG, Dube N, Read M, Penney J, Paquet M, Han Y, et al. Protein tyrosine phosphatase 1B deficiency or inhibition delays ErbB2-induced mammary tumorigenesis and protects from lung metastasis. Nat Genet 2007;39:338-46. https://doi.org/10.1038/ng1963
  91. Bentires-Alj M, Neel BG. Protein-tyrosine phosphatase 1B is required for HER2/Neu-induced breast cancer. Cancer Res 2007;67:2420-4. https://doi.org/10.1158/0008-5472.CAN-06-4610

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