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ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2013; 59(4): 93-106

Endoplasmic reticulum stress and angiogenesis

Minchenko DO1, Kubaĭchuk KI1, Hubenia OV1, Kryvdiuk IV1, Khomenko IeV1, Herasymenko RM1, Sulik RV1, Murashko NK2, Minchenko OH3

  1. Palladin Institute of Biochemistry, National Academy ofSciences of Ukraine, Kyiv, Ukraine
  2. Bogomolets National Medical University, Kyiv, Ukraine
  3. Shupik National Medical Academy of Post-GraduateEducation, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz59.04.093


Abstract

The endoplasmic reticulum is a dynamic intracellular organelle with exquisite sensitivity to alterations in homeostasis, and provides stringent quality control systems to ensure that the only correctly folded proteins transit to the Golgi and unfolded or misfolded proteins are retained and ultimately degraded. The endoplasmic reticulum stress represents the unfolded protein response to cope with the accumulation of unfolded or misfolded proteins and is required to maintain the functional integrity of the endoplasmic reticulum. The endoplasmic reticulum stress is a fundamental phenomenon which provides a secure protection of the cells from different factors. This stress provides a wide spectrum of physiological roles in diverse developmental and metabolic processes, especially for professional secretory cells with high-level secretory protein synthesis, such as pancreatic beta cells, hepatocytes and osteoblasts and is required throughout the entire life. The endoplasmic reticulum stress and hypoxia are the obligate components of malignant tumor growth, are interconnected and activate angiogenesis via growth and metabolism control. The endoplasmic reticulum stress is mediated by three by three sensor and signaling pathways (PERK, ATF6 and ERN1), besides that blockade one (ERN1) leads to a decrease of tumor growth through suppression of angiogenesis and proliferation. The data concerning the interaction of signaling enzyme ERN1 and pro- and anti-angiogenic gene expressions is analyzed.

Keywords: endoplasmic reticulum stress, angiogenesis, hypoxia, gene expressions, ERN1, HIF, proliferation.

Full text: (PDF, in Ukrainian)

References

  1. Kubaichuk K., Minchenko D., Ratushna O., Minchenko O. Vpliv gipoksii ta ishemii na ekspresiyu proangiogennih geniv u klitinah gliomi U87 z prignichenoyu funktsiieyu gena ERN1 . Visn. KNU im. T. Shevchenka. 2012. 58. P. 46-50.
    2.  
  2. Acosta-Alvear D., Zhou Y., Blais A. et al. XBP1 controls diverse cell typeand condition-specific transcriptional regulatory networks . Mol. Cell. 2007. 27, N 1. P. 53-66. CrossRef PubMed
    3.  
  3. Agani F., Jiang B.H. Oxygen-independent regulation of HIF-1: novel involvement of PI3K/AKT/mTOR pathway in cancer . Curr. Cancer Drug Targets. 2013. 13, N 3. P. 245-251. CrossRef PubMed
    4.  
  4. Auf G., Jabouille A., Guerit S. et al. Inositol-requiring enzyme 1alpha is a key regulator of angiogenesis and invasion in malignant glioma . Proc. Natl. Acad. Sci. USA. 2010. 107, N 35. P. 15553-15558. CrossRef PubMed PubMedCentral
    5.  
  5. Backer M. V., Backer J. M., Chinnaiyan P. Targeting the unfolded protein response in cancer therapy . Methods Enzymol. 2011. 491. P. 37-56. CrossRef PubMed
    6.  
  6. Badiola N., Penas C., Minano-Molina A. et al. Induction of ER stress in response to oxygen-glucose deprivation of cortical cultures involves the activation of the PERK and IRE-1 pathways and of caspase-12 . Cell death & disease. 2011. 2. P. e149. CrossRef PubMed PubMedCentral
    7.  
  7. Bartrons R., Caro J. Hypoxia, glucose metabolism and the Warburg's effect . J. Bioenerg. Biomembr. 2007. 39, N 3. P. 223-229. CrossRef PubMed
    8.  
  8. Bertolotti A., Zhang Y., Hendershot L. M. et al. Dynamic interaction of BiP and ER stress transducers in the unfoldedprotein response . Nature Cell Biol. 2000. 2, N 6. P. 326-332. CrossRef PubMed
    9.  
  9. Bi M., Naczki C., Koritzinsky M. et al. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth . EMBO J. 2005. 24, N 19. P. 3470-3481.  CrossRef PubMed PubMedCentral
    10.  
  10. Blais J. D., Filipenko V., Bi M. et al. Activating transcription factor 4 is translationally regulated by hypoxic stress . Mol. Cell. Biol. 2004. 24, N 17. P. 7469-7482.  CrossRef PubMed PubMedCentral
    11.  
  11. Bobrovnikova-Marjon E., Grigoriadou C., Pytel D. et al. PERK promotes cancer cell proliferation and tumor growth by limiting oxidative DNA damage . Oncogene. 2010. 29, N 27. P. 3881-3895. CrossRef PubMed PubMedCentral
    12.  
  12. Bouchecareilh M., Higa A., Fribourg S., Moenner M. et al. Peptides derived from the bifunctional kinase/RNase enzyme IRE1alpha modulate IRE1alpha activity and protect cells from endoplasmic reticulum stress . FASEB J. 2011. 25, N 9. P. 3115-3129. CrossRef PubMed
    13.  
  13. Bravo R., Parra V., Gatica D. et al. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration . Int. Rev. Cell. Mol. Biol. 2013. 301. P. 215-290. CrossRef PubMed PubMedCentral
    14.  
  14. Cao J., Dai D.L., Yao L. et al. Saturated fatty acid induction of endoplasmic reticulum stress and apoptosis in human liver cells via the PERK/ATF4/CHOP signaling pathway . Mol. Cell. Biochem. 2012. 364, N 1-2. P. 115-129. CrossRef PubMed
    15.  
  15. Cao S.S., Kaufman R.J. Targeting endoplasmic reticulum stress in metabolic disease . Expert. Opin. Ther. Targets. 2013. 17, N 4. P. 437-448. CrossRef PubMed
    16.  
  16. Chakrabarti A., Chen A.W., Varner J.D. A review of the mammalian unfolded protein response . Biotechnol. Bioengineer. 2011. 108, N 12. P. 2777-2793. CrossRef PubMed PubMedCentral
    17.  
  17. Chesney J. 6-phosphofructo-2-kinase/fructose-2,6bisphosphatase and tumor cell glycolysis . Curr. Opin. Clin. Nutr. Metab. Care. 2006. 9, N 5. P. 535-539. CrossRef PubMed
    18.  
  18. Citri A., Yarden Y. EGF-ERBB signalling: towards the systems level . Nat. Rev. Mol. Cell. Biol. 2006. 7, N 7. P. 505-516. CrossRef PubMed
    19.  
  19. Denko N. C. Hypoxia, HIF1 and glucose metabolism in the solid tumour . Nat. Rev. Cancer. 2008. 8, N 9. P. 705-713.  CrossRef PubMed
    20.  
  20. Drogat B., Auguste P., Nguyen D.T. et al. IRE1 signaling is essential for ischemia-induced vascular endothelial growth factor-A expression and contributes to angiogenesisand tumor growth in vivo . Cancer Res. 2007. 67. P. 6700-6707.  CrossRef PubMed
    21.  
  21. Farias M., Puebla C., Westermeier F. et al. Nitric oxide reduces SLC29A1 promoter activity and adenosine transport involving transcription factor complex hCHOP-C/EBPalpha in human umbilical vein endothelial cells from gestational diabetes . Cardiovascular. Res. 2010. 86, N 1. P. 45-54. CrossRef PubMed
    22.  
  22. Feldman D. E., Chauhan V., Koong A. C. The unfolded D.O. Minchenko, K.I. Kubaichuk, O.V. Gubenya, I.V. Krivdyuk, Ie.V. Homenko, R.M. Gerasimenko, R.V. Sulik, N.K. Murashko, O.G. Minchenko The unfolded protein response: a novel component of the hypoxic stress response in tumors . Mol. Cancer Res. 2005. 3, N 11. P. 597-605. CrossRef PubMed
    23.  
  23. Fels D.R., Koumenis C. The PERK/eIF2a/ATF4 module of the UPR in hypoxia resistance and tumor growth . Cancer Biol. Therap. 2006. 5, N 7. P. 723-728. CrossRef PubMed
    24.  
  24. Gentz S.H., Bertollo C.M., Souza-Fagundes E.M., da Silva A.M. Implication of eIF2? kinase GCN2 in induction of apoptosis and endoplasmic reticulum stress-responsive genes by sodium salicylate . J. Pharm. Pharmacol. 2013. 65, N 3. P. 430-440. CrossRef PubMed
    25.  
  25. Giltaire S., Lambert S., Poumay Y. HB-EGF synthesis and release induced by cholesterol depletion of human epidermal keratinocytes is controlled by extracellular ATP and involves both p38 and ERK1/2 signaling pathways . J. Cell. Physiol. 2011. 226, N 6. P. 1651-1659. CrossRef PubMed
    26.  
  26. Han D., Lerner A.G., Vande Walle L.V. et al. IRE1a Kinase Activation Modes Control Alternate Endoribonuclease Outputs to Determine Divergent Cell Fates . Cell. 2009. 138, N 3. P. 562-575. CrossRef PubMed PubMedCentral
    27.  
  27. Han D., Upton J. P., Hagen A. et al. A kinase inhibitor activates the IRE1alpha RNase to confer cytoprotection against ER stress . Biochem. Biophys. Res. Commun. 2008. 365, N 4. P. 777-783. CrossRef PubMed
    28.  
  28. Hashimoto G., Inoki I., Fujii Y. et al. Matrix metalloproteinases cleave connective tissue growth factor and reactivate angiogenic activity of vascular endothelial growth factor 165 . J. Biol. Chem. 2002. 277, N 39. P. 36288-36295. CrossRef PubMed
    29.  
  29. Hollien J., Lin J. H., Li H. et al. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells . J. Cell Biol. 2009. 186, N 3. P. 323-331.  CrossRef PubMed PubMedCentral
    30.  
  30. Hose D., Moreaux J., Meissner T. et al. Induction of angiogenesis by normal and malignant plasma cells. . Blood. 2009. 114, N 1. P. 128-143.  CrossRef PubMed
    31.  
  31. Jabouille A., Auf G., Guerit S. Pineau R., Favereaux A., Maitre M., Gaiser T., von Deimling A., Minchenko O.H., Chevet E., Bikfalvi A., Moenner M. IRE1 in glioma angiogenesis and invasiveness . In: Angiogenesis. Helsinki, Finland. 2009. P. 24.
    32.  
  32. Karbovskyi L.L., Minchenko D.O., Danilovskyi S. et al. Endoplasmic reticulum-nuclei signaling enzyme-1 knockdown modulates effect of hypoxia and ischemia on the expression of circadian genes in glioma cells . Studia Biologica. 2011. 5, N 2. P. 37-50. CrossRef  
  33. Kaufman R. J. Orchestrating the unfolded protein response in health and disease . J. Clin. Invest. 2002. 110, N 10. P. 1389-1398. CrossRef PubMed PubMedCentral
    34.  
  34. Kaufman R. J., Back S. H., Song B. et al. The unfolded protein response is required to maintain the integrity of the endoplasmic reticulum, prevent oxidative stress and preserve differentiation in beta-cells . Diabetes, obesity & metabolism. 2010. 12, Suppl. 2. P. 99-107. CrossRef PubMed PubMedCentral
    35.  
  35. Kee H.J., Koh J.T., Kim M.Y. et al. Expression of brainspecific angiogenesis inhibitor 2 (BAI2) in normal and ischemic brain: involvement of BAI2 in the ischemiainduced brain angiogenesis . J. Cerebral Blood Flow Metab. 2002. 22, N 9. P. 1054-1067. CrossRef PubMed
    36.  
  36. Korennykh A.V., Egea P.F., Korostelev A.A. et al. The unfolded protein response signals through high-order assembly of Ire1 . Nature. 2009. 457, N 7230. P. 687-693. CrossRef PubMed PubMedCentral
    37.  
  37. Koshikawa N., Mizushima H., Minegishi T. et al. Proteolytic activation of heparin-binding EGF-like growth factor by membrane-type matrix metalloproteinase-1 in ovarian carcinoma cells . Cancer Sci. 2011. 10, N 1. P. 111-116. CrossRef PubMed
    38.  
  38. Koumenis C. ER stress, hypoxia tolerance and tumor progression . Curr. Mol. Med. 2006. 6, N 1. P. 55-69. CrossRef PubMed
    39.  
  39. Koumenis C., Naczki C., Koritzinsky M. 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, N 21. P. 7405-7416.  CrossRef PubMed PubMedCentral
    40.  
  40. Kubaichuk K.I., Minchenko D.O., Danilovskyi S.V. et al. Hypoxic regulation of the expression of anti-angiogenic genes in U87 glioma cells with ERN1 signaling enzyme loss of function . Studia Biologica. 2012. 6, N 3. P. 15-28.  CrossRef  
  41. Kubaichuk K.I., Minchenko D.O., Moenner M., Minchenko O.H. Blockade of ERN1 induces anti-angiogenic gene expressions and suppresses tumor growth. In: Molecular and Cellular Mechanisms in Angiogenesis. Capri, Italy. 2012. P. 75.
    42.  
  42. Kyriakakis E., Philippova M., Joshi M.B. et al. T-cadherin attenuates the PERK branch of the unfolded protein response and protects vascular endothelial cells from endoplasmic reticulum stress-induced apoptosis . Cell. Signall. 2010. 22. P. 1308-1316. CrossRef PubMed
    43.  
  43. Lee AS. GRP78 induction in cancer: therapeutic and prognostic implications . Cancer Res. 2007. 67, N 8. P. 3496-3499. CrossRef PubMed
    44.  
  44. Lee J., Sun C., Zhou Y. et al. p38 MAPK-mediated regulation of Xbp1s is crucial for glucose homeostasis . Nat Med. 2011. 17, N 10. P. 1251-1260. CrossRef PubMed PubMedCentral
    45.  
  45. Lee S.K., Kim Y.S. Phosphorylation of eIF2? attenuates statin-induced apoptosis by inhibiting the stabilization and translocation of p53 to the mitochondria . Int. J. Oncol. 2013. 42, N 3. P. 810-816. CrossRef PubMed PubMedCentral
    46.  
  46. Liu C.Y., Kaufman R.J. The unfolded protein response . J. Cell Sci. 2003. 116, Pt 10. P. 1861-1862. CrossRef PubMed
    47.  
  47. Magagnin M. G., Koritzinsky M., Wouters B. G. Patterns of tumor oxygenation and their influence on the cellular hypoxic response and hypoxia-directed therapies . Drug Resistance Updates : reviews and commentaries in antimicrobial and anticancer chemotherapy. 2006. 9, N 4-5. P. 185-197.
    48.  
  48. Mahadevan N. R., Rodvold J., Sepulveda H. et al. Transmission of endoplasmic reticulum stress and pro-inflammation from tumor cells to myeloid cells . Proc. Natl. Acad. Sci. USA. 2011. 108, N 16. P. 6561-6566. CrossRef PubMed PubMedCentral
    49.  
  49. 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 Stres endoplazmatichnogo retikuluma ta angiogenez tumor microenvironment . J. Immunol. 2011. 187, N 9. P. 4403-4409.  CrossRef PubMed
    50.  
  50. Marciniak S.J., Ron D. Endoplasmic Reticulum Stress Signaling in Disease . Physiol. Rev. 2006. 86. P. 1133-1149.  CrossRef PubMed
    51.  
  51. McIntyre E., Blackburn E., Brown P.J. et al. The complete family of epidermal growth factor receptors and their ligands are co-ordinately expressed in breast cancer . Breast Cancer Res. Treat. 2010. 122. P. 105-110. CrossRef PubMed
    52.  
  52. Minchenko A.G., Leshchinsky I., Opentanova I.L. et al. Hypoxia-inducible factor-1-mediated expression of the 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-3 (PFKFB3) gene . J. Biol. Chem. 2002. 277, N 8. P. 6183-6187. CrossRef PubMed PubMedCentral
    53.  
  53. Minchenko D., Hubenya O., Terletsky B. et al. Blockade of the endoplasmic reticulum stress sensor inositol requiring enzyme-1 changes the expression of cyclin and growth arrest-specific genes in glioma cells . Annales Universitatis Mariae Curie-Sklodowska. 2010. 23, N 3. P. 179-184.
    54.  
  54. Minchenko D.O., Hubenya O.V., Terletsky B.M. et al. Effect of hypoxia, glutamine and glucose deprivation on the expression of cyclin and cyclin-dependent kinase genes in glioma cell line U87 and its subline with suppressed activity of signaling enzyme endoplasmic reticulum-nuclei-1 . Ukr. Biokhim. Zh. 2011. 83, N 1.P. 18-29.
    55.  
  55. Minchenko D.O., Karbovskyi L.L., Danilovskyi S. V. et al. Effect of hypoxia and glutamine or glucose deprivation on the expression of retinoblastoma and retinoblastomarelated genes in ERN1 knockdown glioma U87 cell line . Amer. J. Mol. Biol. 2012. 2, N 1. P. 21-31. CrossRef  
  56. Minchenko D.O., Karbovskyi L.L., Danilovskyi S.V. Kharkova A.P., Minchenko O.H. Expression of casein kinase genes in glioma cell line U87: effect of hypoxia and glucose or glutamine deprivation . Nat. Sci. 2012. 4, N 1. P. 38-46. CrossRef  
  57. Minchenko D.O., Karbovskyi L.L., Danylovsky S.V. et al. Effect of hypoxia, glutamine and glucose deprivation on the expression of mRNA of the retinoblastoma binding proteins in glioma cells . Studia Biologica. 2011. 5, N 1. P. 57-68. CrossRef  
  58. Minchenko D.O., Kharkova A.P., Hubenia O.V., Minchenko O.H. Insulin receptor, IRS1, IRS2, INSIG1, INSIG2, RRA D, and BAIAP2 gene expressions in glioma U87 cells with ERN1 loss of function: effect of hypoxia and glutamine or glucose deprivation . Endocr. regulation. 2013. 47, N 1. P. 15-26. CrossRef PubMed
    59.  
  59. Minchenko D.O., Kubajchuk K.I., Ratushna O.O. et al. The effect of hypoxia and ischemic condition on the expression of VEGF genes in glioma U87 cells is dependent from ERN1 knockdown . Adv. Biol. Chem. 2011. 2, N 2, 198-206.  CrossRef  
  60. Minchenko O. H., Ochiai A., Opentanova I.L. Ogura T., Minchenko D.O., Caro J., Komisarenko S.V., Esumi H. Overexpression of 6-phosphofructo-2-kinase/fructose-2,6bisphosphatase-4 in the human breast and colon malignant tumors . Biochimie. 2005. 87, N 11. P. 1005 1010.  CrossRef PubMed
    61.  
  61. Minchenko O.H., Opentanova I.L., Minchenko D.O. et al. Hypoxia induces transcription of 6-phosphofructo-2-kinase/ fructose-2,6-bisphosphatase 4 gene via hypoxia-inducible factor-1alpha activation . FEBS Lett. 2004. 576, N 1. P. 14-20. CrossRef PubMed
    62.  
  62. Moenner M., Pluquet O., Bouchecareilh M., Chevet E. Integrated endoplasmic reticulum stress responses in cancer . Cancer Res. 2007. 67, N 22. P. 10631-10634. CrossRef PubMed
    63.  
  63. Mozos A., Roue G., Lopez-Guillermo A. The expression of the endoplasmic reticulum stress sensor BiP/GRP78 predicts response to chemotherapy and determines the efficacy of proteasome inhibitors in diffuse large b-cell lymphoma . Am. J. Pathol. 2011. 179, N 5. P. 2601-2610. CrossRef PubMed PubMedCentral
    64.  
  64. Muaddi H., Majumder M., Peidis P. et al. Phosphorylation of eIF2? at serine 51 is an important determinant of cell survival and adaptation to glucose deficiency . Mol. Biol. Cell. 2010. 21, N 18. P. 3220-3231. CrossRef PubMed PubMedCentral
    65.  
  65. Nagelkerke A., Bussink J., Mujcic H. 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, N 1. P. R2. CrossRef PubMed PubMedCentral
    66.  
  66. Neelam S., Brooks M.M., Cammarata P.R. Lenticular cytoprotection. Part 1: The role of hypoxia inducible factors-1? and 2? and vascular endothelial growth factor in lens epithelial cell survival in hypoxia . Mol. Vis. 2013. 19. P. 1-15. PubMed PubMedCentral
    67.  
  67. Neill T., Painter H., Buraschi S. et al. Decorin antagonizes the angiogenic network: concurrent inhibition of Met, hypoxia inducible factor 1alpha, vascular endothelial growth factor A, and induction of thrombospondin-1 and TIMP3 . J. Biol. Chem. 2012. 287, N 8. P. 5492-5506. CrossRef PubMed PubMedCentral
    68.  
  68. Ozawa K., Kuwabara K., Tamatani M. et al. 150-kDa oxygen-regulated protein (ORP150) suppresses hypoxiainduced apoptotic cell death . J. Biol. Chem. 1999. 274, N 10. P. 6397-6404. CrossRef PubMed
    69.  
  69. Park S.W., Zhou Y., Lee J. et al. The regulatory subunits of PI3K, p85alpha and p85beta, interact with XBP-1 and increase its nuclear translocation . Nat Med. 2010. 16, N 4. P. 429-437.  CrossRef PubMed PubMedCentral
    70.  
  70. Pereira E.R., Liao N., Neale G.A., Hendershot L.M. Transcriptional and post-transcriptional regulation of proangiogenic factors by the unfolded protein response . LoS One. 2010. 5, N 9. P. e12521. CrossRef PubMed PubMedCentral
    71.  
  71. Rivera L.B., Bradshaw A.D., Brekken R.A. The regulatory function of SPARC in vascular biology . Cell. Mol. Life Sci. 2011. 68, N 19. P. 3165-3173. CrossRef PubMed
    72.  
  72. Romero-Ramirez L., Cao H., Nelson D. et al. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth . Cancer Research. 2004. 64. P. 59435947. CrossRef PubMed
    73.  
  73. Romero-Ramirez L., Cao H., Regalado M.P. et al. X boxbinding protein 1 regulates angiogenesis in human pancreatic adenocarcinomas . Translat. Oncology. 2009. 2, N 1. P. 31-38. CrossRef PubMed PubMedCentral
    74.  
  74. Saito A., Ochiai K., Kondo S. et al. Endoplasmic reticulum stress response mediated by the PERK-eIF2(alpha)D.O. Minchenko, K.I. Kubaichuk, O.V. Gubenya, I.V. Krivdyuk, Ie.V. Homenko, R.M. Gerasimenko, R.V. Sulik, N.K. Murashko, O.G. Minchenko. ATF4 pathway is involved in osteoblast differentiation induced by BMP2 . J. Biol. Chem. 2011. 286, N 6. P. 4809-4818. CrossRef PubMed PubMedCentral
    75.  
  75. Schroder M. Endoplasmic reticulum stress responses . Cell. Mol. Life Sci. 2008. 65, N 6. P. 862-894. CrossRef PubMed
    76.  
  76. Schroder M., Kaufman R.J. The mammalian unfolded protein response . Annu. Rev. Biochem. 2005. 74. P. 739-789. CrossRef PubMed
    77.  
  77. Seo D.W., Saxinger W.C., Guedez L. et al. An integrinbinding N-terminal peptide region of TIMP-2 retains potent angio-inhibitory and anti-tumorigenic activity in vivo . Peptides. 2011. 32, N 9. P. 1840-1848. CrossRef PubMed PubMedCentral
    78.  
  78. Shen X., Zhang K., Kaufman R.J. The unfolded protein response a stress signaling pathway of the endoplasmic reticulum . J. Chem. Neuroanat. 2004. 28, N 1-2. P. 79-92. CrossRef PubMed
    79.  
  79. Svensson K.J., Kucharzewska P., Christianson H.C. et al. Hypoxia triggers a proangiogenic pathway involving cancer cell microvesicles and PAR-2-mediated heparinbinding EGF signaling in endothelial cells . Proc. Natl. Acad. Sci. USA. 2011. 108, N 32. P. 13147-13152.  CrossRef PubMed PubMedCentral
    80.  
  80. Thorpe J.A., Schwarze S.R. IRE1alpha controls cyclin A1 expression and promotes cell proliferation through XBP-1 . Cell Stress & Chaperones. 2010. 15, N 5. P. 497-508.  CrossRef PubMed PubMedCentral
    81.  
  81. Tolino M.A., Block E.R., Klarlund J.K. Brief treatment with heparin-binding EGF-like growth factor, but not with EGF, is sufficient to accelerate epithelial wound healing . Biochim. and Biophys. Acta. 2011. 1810, N 9. P. 875-878. CrossRef PubMed PubMedCentral
    82.  
  82. Wang M., Ye R., Barron E. et al. Essential role of the unfolded protein response regulator GRP78/BiP in protection from neuronal apoptosis . Cell Death Differ. 2010. 17, N 3. P. 488-498. CrossRef PubMed PubMedCentral
    83.  
  83. Wang S., Kaufman R.J. The impact of the unfolded protein response on human disease . J. Cell. Biol. 2012. 197, N 7. P. 857-867. CrossRef PubMed PubMedCentral
    84.  
  84. Wang S., Kaufman R.J. The impact of the unfolded protein response on human disease . J. Cell. Biol. 2012. 197, N 7. P. 857-867. CrossRef PubMed PubMedCentral
    85.  
  85. Woehlbier U., Hetz C. Modulating stress responses by the UPRosome: a matter of life and death . Trends Biochem. Sci. 2011. 36, N 6. P. 329-337. CrossRef PubMed
    86.  
  86. Wolf A., Agnihotri S., Micallef J. et al. Hexokinase 2 is a key mediator of aerobic glycolysis and promotes tumor growth in human glioblastoma multiforme . J. Exp. Med. 2011. 208, N 2. P. 313-326. CrossRef PubMed PubMedCentral
    87.  
  87. Woo C.W., Cui D., Arellano J. et al. Adaptive suppression of the ATF4-CHOP branch of the unfolded protein response by toll-like receptor signalling . Nat. Cell Biol. 2009. 11, N 12. P. 1473-1480. CrossRef PubMed PubMedCentral
    88.  
  88. Wu J., Kaufman R.J. From acute ER stress to physiological roles of the Unfolded Protein Response . Cell Death Differ. 2006. 13, N 3. P. 374-384. CrossRef PubMed
    89.  
  89. Yuzefovych L.V., Musiyenko S.I., Wilson G.L., Rachek L.I. Mitochondrial DNA damage and dysfunction, and oxidative stress are associated with endoplasmic reticulum stress, protein degradation and apoptosis in high fat diet-induced insulin resistance mice . PLoS One. 2013. 8, N 1. P. e54059.  CrossRef PubMed PubMedCentral
    90.  
  90. Zhang K., Kaufman R.J. The unfolded protein response: a stress signaling pathway critical for health and disease . Neurology. 2006. 66, N 2. Suppl 1. S102-S109.
    91.  
  91. Zhou J., Liu C.Y., Back S.H. The crystal structure of human IRE1 luminal domain reveals a conserved dimerization interface required for activation of the unfolded protein response . Proc. Natl. Acad. Sci. U.S.A. 2006. 103, N 39. P. 14343-14348. CrossRef PubMed PubMedCentral
  92. Zhou Y., Lee J., Reno C.M. et al. Regulation of glucose homeostasis through a XBP-1-FoxO1 interaction. . Nat. Med. 2011. 17, N 3. P. 356-365.  CrossRef PubMed PubMedCentral
    93.  
  93. Zou J., Li P., Lu F. et al. Notch1 is required for hypoxiainduced proliferation, invasion and chemoresistance of T-cell acute lymphoblastic leukemia cells . J. Hematol. Oncol. 2013. 6, N 1. P. 3. CrossRef PubMed PubMedCentral
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