ER proteostasis addiction in cancer biology: Novel concepts

Seminars in Cancer Biology

Volumn 33, Issue , 2015, Pages 40-47

  Dufey, Estefanie ^a   Urra, Hery ^a   Hetz, Claudio ^a,b  

^a UNIVERSITY OF CHILE   (Chile)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Cancer; ER stress; Proteostasis; UPR

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; PROTEIN DISULFIDE ISOMERASE; RAD51 PROTEIN; REACTIVE OXYGEN METABOLITE;

ACTIN FILAMENT; ANGIOGENESIS; CELL INVASION; CELL SURVIVAL; DNA DAMAGE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GENOMIC INSTABILITY; HUMAN; HYPOXIA; IMMUNOMODULATION; MACROPHAGE ACTIVATION; MALIGNANT TRANSFORMATION; METASTASIS; NEOPLASM; NUTRIENT AVAILABILITY; PH; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; UNFOLDED PROTEIN RESPONSE; ANIMAL; ANOXIA; APOPTOSIS; GENETICS; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PROTEIN DENATURATION;

ANIMALS; ANOXIA; APOPTOSIS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMANS; HYDROGEN-ION CONCENTRATION; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN DENATURATION; PROTEIN FOLDING; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84938211446     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2015.04.003     Document Type: Review

References (132)

1. Balch W.E., Morimoto R.I., Dillin A., Kelly J.W. Adapting proteostasis for disease intervention. Science 2008, 319:916-919.
2. Lindquist S.L., Kelly J.W. Chemical and biological approaches for adapting proteostasis to ameliorate protein misfolding and aggregation diseases: progress and prognosis. Cold Spring Harb Perspect Biol 2011, 3.
3. Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 2012, 13:89-102.
4. Dufey E., Sepulveda D., Rojas-Rivera D., Hetz C. Cellular mechanisms of endoplasmic reticulum stress signaling in health and disease. 1. An overview. Am J Physiol Cell Physiol 2014, 307:C582-C594.
5. Oakes S.A., Papa F.R. The role of endoplasmic reticulum stress in human pathology. Annu Rev Pathol 2015, 10:173-194.
6. De Raedt T., Walton Z., Yecies J.L., Li D., Chen Y., Malone C.F., et al. Exploiting cancer cell vulnerabilities to develop a combination therapy for ras-driven tumors. Cancer Cell 2011, 20:400-413.
7. Dejeans N., Manie S., Hetz C., Bard F., Hupp T., Agostinis P., et al. Addicted to secrete - novel concepts and targets in cancer therapy. Trends Mol Med 2014, 20:242-250.
8. Wang M., Kaufman R.J. The impact of the endoplasmic reticulum protein-folding environment on cancer development. Nat Rev Cancer 2014, 14:581-597.
9. Hetz C., Chevet E., Harding H.P. Targeting the unfolded protein response in disease. Nat Rev Drug Discov 2013, 12:703-719.
10. Maly D.J., Papa F.R. Druggable sensors of the unfolded protein response. Nat Chem Biol 2014, 10:892-901.
11. Ma Y., Hendershot L.M. The role of the unfolded protein response in tumour development: friend or foe. Nat Rev Cancer 2004, 4:966-977.
12. Clarke H.J., Chambers J.E., Liniker E., Marciniak S.J. Endoplasmic reticulum stress in malignancy. Cancer Cell 2014, 25:563-573.
13. Gutierrez T., Simmen T. Endoplasmic reticulum chaperones and oxidoreductases: critical regulators of tumor cell survival and immunorecognition. Front Oncol 2014, 4:291.
14. Feldman D.E., Chauhan V., Koong A.C. The unfolded protein response: a novel component of the hypoxic stress response in tumors. Mol Cancer Res: MCR 2005, 3:597-605.
15. Harding H.P., 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.
16. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 2003, 11:619-633.
17. Urra H., Dufey E., Lisbona F., Rojas-Rivera D., Hetz C. When ER stress reaches a dead end. Biochim Biophys Acta 2013, 1833:3507-3517.
18. Marciniak S.J., Yun C.Y., 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, 18:3066-3077.
19. Han J., Back S.H., Hur J., Lin Y.H., Gildersleeve R., Shan J., et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol 2013, 15:481-490.
20. Walter P., Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334:1081-1086.
21. 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, 107:881-891.
22. Calfon M., Zeng H., Urano F., Till J.H., Hubbard S.R., Harding H.P., et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002, 415:92-96.
23. Lee K., Tirasophon W., Shen X., Michalak M., Prywes R., Okada T., et al. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev 2002, 16:452-466.
24. 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 2003, 23:7448-7459.
25. Acosta-Alvear D., Zhou Y., Blais A., Tsikitis M., Lents N.H., Arias C., et al. XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol Cell 2007, 27:53-66.
26. Maurel M., Chevet E., Tavernier J., Gerlo S. Getting RIDD of RNA: IRE1 in cell fate regulation. Trends Biochem Sci 2014, 39:245-254.
27. Shen J., Chen X., Hendershot L., Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 2002, 3:99-111.
28. Haze K., Yoshida H., Yanagi H., Yura T., Mori K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 1999, 10:3787-3799.
29. Adachi Y., Yamamoto K., Okada T., Yoshida H., Harada A., Mori K. ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum. Cell Struct Funct 2008, 33:75-89.
30. Shoulders M.D., Ryno L.M., Genereux J.C., Moresco J.J., Tu P.G., Wu C., et al. Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep 2013, 3:1279-1292.
31. Reid D.W., Chen Q., Tay A.S., Shenolikar S., Nicchitta C.V. The unfolded protein response triggers selective mRNA release from the endoplasmic reticulum. Cell 2014, 158:1362-1374.
32. Graeber T.G., Osmanian C., Jacks T., Housman D.E., Koch C.J., Lowe S.W., et al. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 1996, 379:88-91.
33. Blais J.D., Addison C.L., Edge R., Falls T., Zhao H., Wary K., et al. Perk-dependent translational regulation promotes tumor cell adaptation and angiogenesis in response to hypoxic stress. Mol Cell Biol 2006, 26:9517-9532.
34. Koritzinsky M., Levitin F., van den Beucken T., Rumantir R.A., Harding N.J., Chu K.C., et al. Two phases of disulfide bond formation have differing requirements for oxygen. J Cell Biol 2013, 203:615-627.
35. Xu S., Butkevich A.N., Yamada R., Zhou Y., Debnath B., Duncan R., et al. Discovery of an orally active small-molecule irreversible inhibitor of protein disulfide isomerase for ovarian cancer treatment. Proc Natl Acad Sci U S A 2012, 109:16348-16353.
36. Zhu G., Lee A.S. Role of the unfolded protein response, GRP78 and GRP94 in organ homeostasis. J Cell Physiol 2015, 230:1413-1420.
37. Li Z. Glucose regulated protein 78: a critical link between tumor microenvironment and cancer hallmarks. Biochim Biophys Acta 2012, 1826:13-22.
38. Roller C., Maddalo D. The molecular Chaperone GRP78/BiP in the development of chemoresistance: mechanism and possible treatment. Front Pharmacol 2013, 4:10.
39. Gazit G., Lu J., Lee A.S. De-regulation of GRP stress protein expression in human breast cancer cell lines. Breast Cancer Res Treat 1999, 54:135-146.
40. Song M.S., Park Y.K., Lee J.H., Park K. Induction of glucose-regulated protein 78 by chronic hypoxia in human gastric tumor cells through a protein kinase C-epsilon/ERK/AP-1 signaling cascade. Cancer Res 2001, 61:8322-8330.
41. Dong D., Ni M., Li J., Xiong S., Ye W., Virrey J.J., 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 2008, 68:498-505.
42. Fernandez P.M., Tabbara S.O., Jacobs L.K., Manning F.C., Tsangaris T.N., Schwartz A.M., 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.
43. Li J., Lee A.S. Stress induction of GRP78/BiP and its role in cancer. Curr Mol Med 2006, 6:45-54.
44. Arap M.A., Lahdenranta J., Mintz P.J., Hajitou A., Sarkis A.S., Arap W., et al. Cell surface expression of the stress response chaperone GRP78 enables tumor targeting by circulating ligands. Cancer Cell 2004, 6:275-284.
45. Lee A.S. GRP78 induction in cancer: therapeutic and prognostic implications. Cancer Res 2007, 67:3496-3499.
46. Romero-Ramirez L., Cao H., Nelson D., Hammond E., Lee A.H., Yoshida H., et al. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res 2004, 64:5943-5947.
47. Chen X., Iliopoulos D., Zhang Q., Tang Q., Greenblatt M.B., Hatziapostolou M., et al. XBP1 promotes triple-negative breast cancer by controlling the HIF1alpha pathway. Nature 2014, 508:103-107.
48. Pereira E.R., Frudd K., Awad W., Hendershot L.M. Endoplasmic reticulum (ER) stress and hypoxia response pathways interact to potentiate hypoxia-inducible factor 1 (HIF-1) transcriptional activity on targets like vascular endothelial growth factor (VEGF). J Biol Chem 2014, 289:3352-3364.
49. Bi M., Naczki C., Koritzinsky M., Fels D., Blais J., Hu N., et al. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J 2005, 24:3470-3481.
50. Rouschop K.M., Dubois L.J., Keulers T.G., van den Beucken T., Lambin P., Bussink J., et al. PERK/eIF2alpha signaling protects therapy resistant hypoxic cells through induction of glutathione synthesis and protection against ROS. Proc Natl Acad Sci U S A 2013, 110:4622-4627.
51. Koumenis C., Naczki C., Koritzinsky M., Rastani S., Diehl A., Sonenberg N., et al. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 2002, 22:7405-7416.
52. Tay K.H., Luan Q., Croft A., Jiang C.C., Jin L., Zhang X.D., et al. Sustained IRE1 and ATF6 signaling is important for survival of melanoma cells undergoing ER stress. Cell Signal 2014, 26:287-294.
53. Tang C.H., Ranatunga S., Kriss C.L., Cubitt C.L., Tao J., Pinilla-Ibarz J.A., et al. Inhibition of ER stress-associated IRE-1/XBP-1 pathway reduces leukemic cell survival. J Clin Invest 2014, 124:2585-2598.
54. Lin J.H., Li H., Zhang Y., Ron D., Walter P. Divergent effects of PERK and IRE1 signaling on cell viability. PloS ONE 2009, 4:e4170.
55. Greenman C., Stephens P., Smith R., Dalgliesh G.L., Hunter C., Bignell G., et al. Patterns of somatic mutation in human cancer genomes. Nature 2007, 446:153-158.
56. Kan Z., Jaiswal B.S., Stinson J., Janakiraman V., Bhatt D., Stern H.M., et al. Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 2010, 466:869-873.
57. Xue Z., He Y., Ye K., Gu Z., Mao Y., Qi L. A conserved structural determinant located at the interdomain region of mammalian inositol-requiring enzyme 1alpha. J Biolo Chem 2011, 286:30859-30866.
58. Carrasco D.R., Sukhdeo K., Protopopova M., Sinha R., Enos M., Carrasco D.E., et al. The differentiation and stress response factor XBP-1 drives multiple myeloma pathogenesis. Cancer Cell 2007, 11:349-360.
59. Niederreiter L., Fritz T.M., Adolph T.E., Krismer A.M., Offner F.A., Tschurtschenthaler M., et al. ER stress transcription factor Xbp1 suppresses intestinal tumorigenesis and directs intestinal stem cells. J Exp Med 2013, 210:2041-2056.
60. 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, 29:3881-3895.
61. Huber A.L., 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, 49:1049-1059.
62. Nakagawa H., Umemura A., Taniguchi K., Font-Burgada J., Dhar D., Ogata H., et al. ER stress cooperates with hypernutrition to trigger TNF-dependent spontaneous HCC development. Cancer Cell 2014, 26:331-343.
63. Arai M., Kondoh N., Imazeki N., Hada A., Hatsuse K., Kimura F., et al. Transformation-associated gene regulation by ATF6alpha during hepatocarcinogenesis. FEBS Lett 2006, 580:184-190.
64. Wang W.A., Groenendyk J., Michalak M. Endoplasmic reticulum stress associated responses in cancer. Biochim Biophys Acta 2014, 1843:2143-2149.
65. Jain R.K. Molecular regulation of vessel maturation. Nat Med 2003, 9:685-693.
66. Wang Y., Alam G.N., Ning Y., Visioli F., Dong Z., Nor J.E., et al. The unfolded protein response induces the angiogenic switch in human tumor cells through the PERK/ATF4 pathway. Cancer Res 2012, 72:5396-5406.
67. Ghosh R., Lipson K.L., Sargent K.E., Mercurio A.M., Hunt J.S., Ron D., et al. Transcriptional regulation of VEGF-A by the unfolded protein response pathway. PloS ONE 2010, 5:e9575.
68. Oskolkova O.V., Afonyushkin T., Leitner A., von Schlieffen E., Gargalovic P.S., Lusis A.J., et al. ATF4-dependent transcription is a key mechanism in VEGF up-regulation by oxidized phospholipids: critical role of oxidized sn-2 residues in activation of unfolded protein response. Blood 2008, 112:330-339.
69. Romero-Ramirez L., Cao H., Regalado M.P., Kambham N., Siemann D., Kim J.J., et al. X box-binding protein 1 regulates angiogenesis in human pancreatic adenocarcinomas. Transl Oncol 2009, 2:31-38.
70. 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, 107:15553-15558.
71. Virrey J.J., Dong D., Stiles C., Patterson J.B., Pen L., Ni M., et al. Stress chaperone GRP78/BiP confers chemoresistance to tumor-associated endothelial cells. Mol Cancer Res: MCR 2008, 6:1268-1275.
72. Karali E., Bellou S., Stellas D., Klinakis A., Murphy C., Fotsis T. VEGF signals through ATF6 and PERK to promote endothelial cell survival and angiogenesis in the absence of ER stress. Mol Cell 2014, 54:559-572.
73. Urra H., Hetz C. A novel ER stress-independent function of the UPR in angiogenesis. Mol Cell 2014, 54:542-544.
74. Friedberg E.C. DNA damage and repair. Nature 2003, 421:436-440.
75. Lord C.J., Ashworth A. The DNA damage response and cancer therapy. Nature 2012, 481:287-294.
76. Negrini S., Gorgoulis V.G., Halazonetis T.D. Genomic instability - an evolving hallmark of cancer. Nat Rev Mol Cell Biol 2010, 11:220-228.
77. He L., Kim S.O., Kwon O., Jeong S.J., Kim M.S., Lee H.G., et al. ATM blocks tunicamycin-induced endoplasmic reticulum stress. FEBS Lett 2009, 583:903-908.
78. Dioufa N., Chatzistamou I., Farmaki E., Papavassiliou A.G., Kiaris H. p53 antagonizes the unfolded protein response and inhibits ground glass hepatocyte development during endoplasmic reticulum stress. Exp Biol Med (Maywood) 2012, 237:1173-1180.
79. Duplan E., Giaime E., Viotti J., Sevalle J., Corti O., Brice A., et al. ER-stress-associated functional link between Parkin and DJ-1 via a transcriptional cascade involving the tumor suppressor p53 and the spliced X-box binding protein XBP-1. J Cell Sci 2013, 126:2124-2133.
80. Senovilla L., Galluzzi L., Marino G., Vitale I., Castedo M., Kroemer G. Immunosurveillance against cancer-associated hyperploidy. Oncotarget 2012, 3:1270-1271.
81. Torres E.M., Sokolsky T., Tucker C.M., Chan L.Y., Boselli M., Dunham M.J., et al. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 2007, 317:916-924.
82. Oromendia A.B., Dodgson S.E., Amon A. Aneuploidy causes proteotoxic stress in yeast. Genes Dev 2012, 26:2696-2708.
83. Pavelka N., Rancati G., Zhu J., Bradford W.D., Saraf A., Florens L., et al. Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 2010, 468:321-325.
84. Pollack J.R., Sorlie T., Perou C.M., Rees C.A., Jeffrey S.S., Lonning P.E., et al. Microarray analysis reveals a major direct role of DNA copy number alteration in the transcriptional program of human breast tumors. Proc Natl Acad Sci U S A 2002, 99:12963-12968.
85. Ganem N.J., Storchova Z., Pellman D., Tetraploidy Aneuploidy and cancer. Curr Opin Genetics Dev 2007, 17:157-162.
86. Papp B., Pal C., Hurst L.D. Dosage sensitivity and the evolution of gene families in yeast. Nature 2003, 424:194-197.
87. Torres E.M., Dephoure N., Panneerselvam A., Tucker C.M., Whittaker C.A., Gygi S.P., et al. Identification of aneuploidy-tolerating mutations. Cell 2010, 143:71-83.
88. Denoyelle C., Abou-Rjaily G., Bezrookove V., Verhaegen M., Johnson T.M., Fullen D.R., et al. Anti-oncogenic role of the endoplasmic reticulum differentially activated by mutations in the MAPK pathway. Nat Cell Biol 2006, 8:1053-1063.
89. Henry K.A., Blank H.M., Hoose S.A., Polymenis M. The unfolded protein response is not necessary for the G1/S transition, but it is required for chromosome maintenance in Saccharomyces cerevisiae. PloS ONE 2010, 5:e12732.
90. Strome E.D., Wu X., Kimmel M., Plon S.E. Heterozygous screen in Saccharomyces cerevisiae identifies dosage-sensitive genes that affect chromosome stability. Genetics 2008, 178:1193-1207.
91. Malhotra J.D., Miao H., Zhang K., Wolfson A., Pennathur S., Pipe S.W., et al. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc Natl Acad Sci U S A 2008, 105:18525-18530.
92. Song B., Scheuner D., Ron D., Pennathur S., Kaufman R.J. Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Investig 2008, 118:3378-3389.
93. Mlynarczyk C., Fahraeus R. Endoplasmic reticulum stress sensitizes cells to DNA damage-induced apoptosis through p53-dependent suppression of p21(CDKN1A.). Nat Commun 2014, 5:5067.
94. Yamamori T., Meike S., Nagane M., Yasui H., Inanami O. ER stress suppresses DNA double-strand break repair and sensitizes tumor cells to ionizing radiation by stimulating proteasomal degradation of Rad51. FEBS Lett 2013, 587:3348-3353.
95. Nagelkerke A., Bussink J., van der Kogel A.J., Sweep F.C., Span P.N. The PERK/ATF4/LAMP3-arm of the unfolded protein response affects radioresistance by interfering with the DNA damage response. Radiother Oncol: J Eur Soc Ther Radiol Oncol 2013, 108:415-421.
96. Bourougaa K., Naski N., Boularan C., Mlynarczyk C., Candeias M.M., Marullo S., et al. Endoplasmic reticulum stress induces G2 cell-cycle arrest via mRNA translation of the p53 isoform p53/47. Mol Cell 2010, 38:78-88.
97. Candeias M.M., Powell D.J., Roubalova E., Apcher S., Bourougaa K., Vojtesek B., et al. Expression of p53 and p53/47 are controlled by alternative mechanisms of messenger RNA translation initiation. Oncogene 2006, 25:6936-6947.
98. Sivan G., Elroy-Stein O. Regulation of mRNA translation during cellular division. Cell Cycle 2008, 7:741-744.
99. Sharma S., Kelly T.K., Jones P.A. Epigenetics in cancer. Carcinogenesis 2010, 31:27-36.
100. Baumeister P., Luo S., Skarnes W.C., Sui G., Seto E., Shi Y., et al. Endoplasmic reticulum stress induction of the Grp78/BiP promoter: activating mechanisms mediated by YY1 and its interactive chromatin modifiers. Mol Cell Biol 2005, 25:4529-4540.
101. Ohoka N., Hattori T., Kitagawa M., Onozaki K., Hayashi H. Critical and functional regulation of CHOP (C/EBP homologous protein) through the N-terminal portion. J Biol Chem 2007, 282:35687-35694.
102. Wang Q., Mora-Jensen H., Weniger M.A., Perez-Galan P., Wolford C., Hai T., et al. ERAD inhibitors integrate ER stress with an epigenetic mechanism to activate BH3-only protein NOXA in cancer cells. Proc Natl Acad Sci U S A 2009, 106:2200-2205.
103. Talmadge J.E., Fidler I.J. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res 2010, 70:5649-5669.
104. Mujcic H., Rzymski T., Rouschop K.M., Koritzinsky M., Milani M., Harris A.L., et al. Hypoxic activation of the unfolded protein response (UPR) induces expression of the metastasis-associated gene LAMP3. Radiother Oncol: J Eur Soc Ther Radiol Oncol 2009, 92:450-459.
105. Mujcic H., Nagelkerke A., Rouschop K.M., Chung S., Chaudary N., Span P.N., et al. Hypoxic activation of the PERK/eIF2alpha arm of the unfolded protein response promotes metastasis through induction of LAMP3. Clin Cancer Res: Off J Am Assoc Cancer Res 2013, 19:6126-6137.
106. Nagelkerke A., Bussink J., Mujcic H., Wouters B.G., Lehmann S., Sweep F.C., et al. Hypoxia stimulates migration of breast cancer cells via the PERK/ATF4/LAMP3-arm of the unfolded protein response. Breast Cancer Res: BCR 2013, 15:R2.
107. Nagelkerke A., Sweep F.C., Stegeman H., Grenman R., Kaanders J.H., Bussink J., et al. Hypoxic regulation of the PERK/ATF4/LAMP3-arm of the unfolded protein response in head and neck squamous cell carcinoma. Head & Neck 2014.
108. Zhu H., Chen X., Chen B., Song W., Sun D., Zhao Y. 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.
109. Feng Y.X., Sokol E.S., Del Vecchio C.A., Sanduja S., Claessen J.H., Proia T.A., et al. Epithelial-to-mesenchymal transition activates PERK-eIF2alpha and sensitizes cells to endoplasmic reticulum stress. Cancer Discov 2014, 4:702-715.
110. Simpson K.J., Selfors L.M., Bui J., Reynolds A., Leake D., Khvorova A., et al. Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat Cell Biol 2008, 10:1027-1038.
111. Dejeans N., Pluquet O., Lhomond S., Grise F., Bouchecareilh M., Juin A., et al. Autocrine control of glioma cells adhesion and migration through IRE1alpha-mediated cleavage of SPARC mRNA. J Cell Sci 2012, 125:4278-4287.
112. He Y., Beatty A., Han X., Ji Y., Ma X., Adelstein R.S., et al. Nonmuscle myosin IIB links cytoskeleton to IRE1alpha signaling during ER stress. Dev Cell 2012, 23:1141-1152.
113. Ishiwata-Kimata Y., Yamamoto Y.H., Takizawa K., Kohno K., Kimata Y. F-actin and a type-II myosin are required for efficient clustering of the ER stress sensor Ire1. Cell Struct Fun 2013, 38:135-143.
114. Alvarez C., Sztul E.S., Brefeldin A. (BFA) disrupts the organization of the microtubule and the actin cytoskeletons. Eur J Cell Biol 1999, 78:1-14.
115. Gipson I.K., Kiorpes T.C., Brennan S.J. Epithelial sheet movement: effects of tunicamycin on migration and glycoprotein synthesis. Dev Biol 1984, 101:212-220.
116. Linxweiler M., Schorr S., Schauble N., Jung M., Linxweiler J., Langer F., et al. Targeting cell migration and the endoplasmic reticulum stress response with calmodulin antagonists: a clinically tested small molecule phenocopy of SEC62 gene silencing in human tumor cells. BMC Cancer 2013, 13:574.
117. Yi N., Chen S.Y., Ma A., Chen P.S., Yao B., Liang T.M., et al. Tunicamycin inhibits PDGF-BB-induced proliferation and migration of vascular smooth muscle cells through induction of HO-1. Anat Rec (Hoboken) 2012, 295:1462-1472.
118. Zagris N., Panagopoulou M. N-glycosylated proteins interfere with the first cellular migrations in early chick embryo. Int J Dev Biol 1992, 36:439-443.
119. Nakamura S., Takizawa H., Shimazawa M., Hashimoto Y., Sugitani S., Tsuruma K., et al. Mild endoplasmic reticulum stress promotes retinal neovascularization via induction of BiP/GRP78. PLOS ONE 2013, 8:e60517.
120. Li Y., Liu H., Huang Y.Y., Pu L.J., Zhang X.D., Jiang C.C., 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, 31:1234-1242.
121. Mahadevan N.R., Rodvold J., Sepulveda H., Rossi S., Drew A.F., Zanetti M. Transmission of endoplasmic reticulum stress and pro-inflammation from tumor cells to myeloid cells. Proc Natl Acad Sci U S A 2011, 108:6561-6566.
122. Mahadevan N.R., Zanetti M. Tumor stress inside out: cell-extrinsic effects of the unfolded protein response in tumor cells modulate the immunological landscape of the tumor microenvironment. J Immunol 2011, 187:4403-4409.
123. Mahadevan N.R., Anufreichik V., Rodvold J.J., Chiu K.T., Sepulveda H., Zanetti M. Cell-extrinsic effects of tumor ER stress imprint myeloid dendritic cells and impair CD8(+) T cell priming. PloS ONE 2012, 7:e51845.
124. Martinon F., Chen X., Lee A.H., Glimcher L.H. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat Immunol 2010, 11:411-418.
125. Woo C.W., Kutzler L., Kimball S.R., Tabas I. Toll-like receptor activation suppresses ER stress factor CHOP and translation inhibition through activation of eIF2B. Nat Cell Biol 2012, 14:192-200.
126. Martinon F., Glimcher L.H. Regulation of innate immunity by signaling pathways emerging from the endoplasmic reticulum. Curr Opin Immunol 2011, 23:35-40.
127. Thevenot P.T., Sierra R.A., Raber P.L., Al-Khami A.A., Trillo-Tinoco J., Zarreii P., et al. The stress-response sensor chop regulates the function and accumulation of myeloid-derived suppressor cells in tumors. Immunity 2014, 41:389-401.
128. Kroemer G., Galluzzi L., Kepp O., Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013, 31:51-72.
129. Burikhanov R., Zhao Y., Goswami A., Qiu S., Schwarze S.R., Rangnekar V.M. The tumor suppressor Par-4 activates an extrinsic pathway for apoptosis. Cell 2009, 138:377-388.
130. Taylor R.C., Berendzen K.M., Dillin A. Systemic stress signalling: understanding the cell non-autonomous control of proteostasis. Nat Rev Mol Cell Biol 2014, 15:211-217.
131. Mardones P., Dillin A., Hetz C. Cell-nonautonomous control of the UPR: mastering energy homeostasis. Cell Metab 2014, 20:385-387.
132. Schonthal A.H. Endoplasmic reticulum stress: its role in disease and novel prospects for therapy. Scientifica 2012, 2012:857516.