The neuro-steroid, 5-androstene 3β,17α diol; induces endoplasmic reticulum stress and autophagy through PERK/eIF2α signaling in malignant glioma cells and transformed fibroblasts

International Journal of Biochemistry and Cell Biology

Volumn 42, Issue 12, 2010, Pages 2019-2029

  Jia, Wentao ^a   Loria, Roger M ^b   Park, Margaret A ^c   Yacoub, Adly ^c   Dent, Paul ^c   Graf, Martin R ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Androstenediol; Autophagy; Eukaryotic translational initiation factor 2 ; Malignant glioma; Protein kinase like endoplasmic reticulum kinase

Indexed keywords

5 ANDROSTEN 3BETA,17ALPHA DIOL; ACTIVATING TRANSCRIPTION FACTOR 6; CCAAT BINDING FACTOR; CCAAT ENHANCER BINDING PROTEIN; GLUCOSE REGULATED PROTEIN 78; INITIATION FACTOR 2ALPHA; MESSENGER RNA; NEUROSTEROID; PROTEIN KINASE LIKE ENDOPLASMIC RETICULUM KINASE; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ARTICLE; AUTOPHAGY; CANCER CELL CULTURE; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOTOXICITY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; FIBROBLAST; GENE CONSTRUCT; GENETIC TRANSFECTION; GLIOBLASTOMA; HUMAN; HUMAN TISSUE; LIGHT CHAIN; MALIGNANT TRANSFORMATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANDROSTENEDIOLS; ANIMALS; AUTOPHAGY; CELL LINE, TRANSFORMED; EIF-2 KINASE; ENDOPLASMIC RETICULUM; FIBROBLASTS; GLIOMA; HUMANS; IMMUNOBLOTTING; MICE; MICE, NUDE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSFECTION;

EUKARYOTA; MURINAE;

EID: 78149282077     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2010.09.003     Document Type: Article

References (45)

1. Brewer J.W., Diehl J.A. PERK mediates cell-cycle exit during the mammalian unfolded protein response. Proc Natl Acad Sci USA 2000, 97:12625-12630.
2. Chen J.J. Regulation of protein synthesis by the heme-regulated eIF2alpha kinase: relevance to anemias. Blood 2007, 109:2693-2699.
3. Fels D.R., Koumenis C. The PERK/eIF2alpha/ATF4 module of the UPR in hypoxia resistance and tumor growth. Cancer Biol Ther 2006, 5:723-728.
4. Graf M.R., Jia W., Johnson R.S., Dent P., Mitchell C., Loria R.M. Autophagy and the functional roles of Atg5 and beclin-1 in the anti-tumor effects of 3β-androstene 17α-diol neuro-steroid on malignant glioma cells. J Steroid Biochem Mol Biol 2009, 115:137-145.
5. Graf M.R., Jia W., Loria R.M. The neuro-steroid, 3beta androstene 17alpha diol exhibits potent anti-tumour effects on human malignant glioma and lymphoma cells through different programmed cell death pathways. Br J Cancer 2007, 97:619-627.
6. Hamanaka R.B., Bennett B.S., Cullinan S.B., Diehl J.A. PERK CN2 contribute to eIF2alpha phosphorylation and cell cycle arrest after activation of the unfolded protein response pathway. Mol Biol Cell 2005, 16:5493-5501.
7. Han A.P., Yu C., Lu L., Fujiwara Y., Browne C., Chin G., et al. Heme-regulated eIF2alpha kinase (HRI) is required for translational regulation and survival of erythroid precursors in iron deficiency. EMBO J 2001, 20:6909-6918.
8. 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.
9. Harding H.P., Zhang Y., Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999, 397:271-274.
10. He B. Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ 2006, 13:393-403.
11. Huynh P.N., Loria R.M. Contrasting effects of alpha- and beta-androstenediol on oncogenic myeloid cell lines in vitro. J Leukoc Biol 1997, 62:258-267.
12. Kim J., Klionsky D.J. Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annu Rev Biochem 2000, 69:303-342.
13. Kondo Y., Kanzawa T., Sawaya R., Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005, 5:726-734.
14. 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.
15. Kouroku Y., Fujita E., Tanida I., Ueno T., Isoai A., Kumagai H., et al. ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 2007, 14:230-239.
16. Lathe R. Steroid and sterol 7-hydroxylation: ancient pathways. Steroids 2002, 67:967-977.
17. 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.
18. Lefranc F., Kiss R. Autophagy, the Trojan horse to combat glioblastomas. Neurosurg Focus 2006, 20:E7.
19. Levine B., Yuan J. Autophagy in cell death: an innocent convict?. J Clin Invest 2005, 115:2679-2688.
20. Loria R.M. Immune up-regulation and tumor apoptosis by androstene steroids. Steroids 2002, 67:953-966.
21. McCullough K.D., Martindale J.L., Klotz L.O., Aw T.Y., Holbrook N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001, 21:1249-1259.
22. Mizushima N. Methods for monitoring autophagy. Int J Biochem Cell Biol 2004, 36:2491-2502.
23. Moretti L., Cha Y.I., Niermann K.J., Lu B. Switch between apoptosis and autophagy: radiation-induced endoplasmic reticulum stress?. Cell Cycle 2007, 6:793-798.
24. Ogier-Denis E., Codogno P. Autophagy: a barrier or an adaptive response to cancer. Biochim Biophys Acta 2003, 1603:113-128.
25. Ohgaki H., Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am J Pathol 2007, 170:1445-1453.
26. Oyadomari S., Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004, 11:381-389.
27. Park M., Yacoub A., Rahmani M., Zhang G., Hart L., Hagan M., et al. OSU-03012 stimulates PERK-dependent increases in HSP70 expression, attenuating its lethal actions in transformed cells. Mol Pharmacol 2008, 73:1168-1184.
28. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939.
29. Petiot A., Ogier-Denis E., Blommaart E.F., Meijer A.J., Codogno P. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 2000, 275:992-998.
30. Rahmani M., Davis E.M., Crabtree T.R., Habibi J.R., Nguyen T.K., Dent P., et al. The kinase inhibitor sorafenib induces cell death through a process involving induction of endoplasmic reticulum stress. Mol Cell Biol 2007, 27:5499-5513.
31. Sarkaria J.N., Carlson B.L., Schroeder M.A., Grogan P., Brown P.D., Giannini C., et al. Use of an orthotopic xenograft model for assessing the effect of epidermal growth factor receptor amplification on glioblastoma radiation response. Clin Cancer Res 2006, 12:2264-2271.
32. Schroder M. Endoplasmic reticulum stress responses. Cell Mol Life Sci 2007, 65:862-894.
33. Schroder M., Kaufman R.J. The mammalian unfolded protein response. Annu Rev Biochem 2005, 74:739-789.
34. Stupp R., Hegi M.E., Mason W.P., van den Bent M.J., Taphoorn M.J., Janzer R.C., et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009, 10:459-466.
35. Surawicz T.S., Davis F., Freels S., Laws E.R., Menck H.R. Brain tumor survival: results from the National Cancer Data Base. J Neurooncol 1998, 40:151-160.
36. Szegezdi E., Logue S.E., Gorman A.M., Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 2006, 7:880-885.
37. Thomas K.C., Sabnis A.S., Johansen M.E., Lanza D.L., Moos P.J., Yost G.S., et al. Transient receptor potential vanilloid 1 agonists cause endoplasmic reticulum stress and cell death in human lung cells. J Pharmacol Exp Ther 2007, 321:830-838.
38. Traganos F., Darzynkiewicz Z. Lysosomal proton pump activity: supravital cell staining with acridine orange differentiates leukocyte subpopulations. Methods Cell Biol 1994, 41:185-194.
39. Wek R.C., Jiang H.Y., Anthony T.G. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 2006, 34:7-11.
40. Wu J., Rutkowski D.T., Dubois M., Swathirajan J., Saunders T., Wang J., et al. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell 2007, 13:351-364.
41. Yamamoto K., Yoshida H., Kokame K., Kaufman R.J., Mori K. Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J Biochem 2004, 136:343-350.
42. Yang Y.P., Liang Z.Q., Gu Z.L., Qin Z.H. Molecular mechanism and regulation of autophagy. Acta Pharmacol Sin 2005, 26:1421-1434.
43. Yokouchi M., Hiramatsu N., Hayakawa K., Kasai A., Takanp Y., Yao J., et al. Atypical, bidirectional regulation of cadmium-induced apoptosis via distinct signaling of unfolded protein response. Cell Death Differ 2007, 14:1467-1474.
44. 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.
45. Zwain I.H., Yen S.S. Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 1999, 140:3843-3852.