Down-modulation of SEL1L, an unfolded protein response and endoplasmic reticulum-associated degradation protein, sensitizes glioma stem cells to the cytotoxic effect of valproic acid

Journal of Biological Chemistry

Volumn 289, Issue 5, 2014, Pages 2826-2838

  Cattaneo, Monica ^a,i   Baronchelli, Simona ^a,i   Schiffer, Davide ^b   Mellai, Marta ^b   Caldera, Valentina ^b   Saccani, Gloria Jotti ^c   Dalpra, Leda ^d,e   Daga, Antonio ^f   Orlandi, Rosaria ^g   Deblasio, Pasquale ^h   Biunno, Ida ^a,i  

^a IRCCS MULTIMEDICA   (Italy)

^b Neuro bio oncology Center   (Italy)

^c UNIVERSITY OF PARMA   (Italy)

^d UNIVERSITY OF MILANO BICOCCA   (Italy)

^e SAN GERARDO HOSPITAL   (Italy)

^f UNIVERSITY OF GENOA   (Italy)

^g NATIONAL CANCER INSTITUTE   (Italy)

^h ISENET   (Italy)

ⁱ Milan Unit   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL-CYCLE PROGRESSION; CELLULAR ADAPTATION; ENDOPLASMIC RETICULUM STRESS; HISTONE DEACETYLASE INHIBITOR; IMMUNOHISTOCHEMISTRY; PROGRAMMED CELL DEATHS; PROLIFERATION RATE; UNFOLDED PROTEIN RESPONSE;

CELL DEATH; CELL MEMBRANES; CYTOTOXICITY; GENE EXPRESSION; GENE THERAPY; MODULATION; STEM CELLS; TUMORS;

PROTEINS;

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; SEL1L PROTEIN; UNCLASSIFIED DRUG; VALPROIC ACID;

ANCHORAGE INDEPENDENT GROWTH; ARTICLE; CANCER STEM CELL; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL RENEWAL; CELL VIABILITY; CELLULAR PARAMETERS; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG SENSITIZATION; ENDOPLASMIC RETICULUM STRESS; GLIOMA CELL; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MTT ASSAY; NEUROSPHERE FORMATION; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; TUMOR GROWTH; UNFOLDED PROTEIN RESPONSE;

BRAIN TUMORS; CANCER STEM CELLS; CELL PROLIFERATION; DRUG RESISTANCE; HISTONE DEACETYLASE;

BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; ENDOPLASMIC RETICULUM; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; NEOPLASTIC STEM CELLS; PROTEINS; UNFOLDED PROTEIN RESPONSE; VALPROIC ACID;

EID: 84893493393     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.527754     Document Type: Article

References (52)

1. Baylin, S. B., and Ohm, J. E. (2006) Epigenetic gene silencing in cancer. A mechanism for early oncogenic pathway addiction? Nat. Rev. Cancer 6, 107-116
2. Walkinshaw, D. R., and Yang, X. J. (2008) Histone deacetylase inhibitors as novel anticancer therapeutics. Curr. Oncol. 15, 237-243
3. Sun, P., Xia, S., Lal, B., and Eberhart, C. G., Quinones-Hinojosa, A., Maciaczyk, J., Matsui, W., Dimeco, F., Piccirillo, S. M., Vescovi, A. L., and Laterra, J. (2009) DNER, an epigenetically modulated gene, regulates glioblastoma. Derived neurosphere cell differentiation and tumor propagation. Stem Cells 27, 1473-1486
4. Das, C. M., Aguilera, D., Vasquez H, Prasad P, Zhang M, Wolff JE, and Gopalakrishnan V. (2007) Valproic acid induces p21 and topoisomerase-II (α/β) expression and synergistically enhances etoposide cytotoxicity in human glioblastoma cell lines. J. Neurooncol. 85, 159-170
5. Mottet, D., and Castronovo, V. (2008) Histone deacetylases. Target enzymes for cancer therapy. Clin. Exp. Metastasis 25, 183-189
6. Shankar, S., and Srivastava, R. K. (2008) Histone deacetylase inhibitors. Mechanisms and clinical significance in cancer. HDAC inhibitor-induced apoptosis. Adv. Exp. Med. Biol. 615, 261-298
7. Masoudi, A., Elopre, M., Amini, E., Nagel, M. E., Ater, J. L., Gopalakrishnan, V., and Wolff, J. E. (2008) Influence of valproic acid on outcome of high-grade gliomas in children. Anticancer Res. 28, 2437-2442
8. Su, J. M., Li, X. N., Thompson, P., Ou, C. N., Ingle, A. M., Russell, H, Lau, C. C., Adamson, P. C., and Blaney, S. M. (2011) Phase 1 study of valproic acid in pediatric patients with refractory solid or CNS tumors. A children's oncology group report. Clin. Cancer Res. 17, 589-597
9. Shabason, J. E., Tofilon, P. J., and Camphausen, K. (2011) Grand Rounds at the National Institutes of Health. HDAC inhibitors as radiation modifiers, from bench to clinic. J. Cell Mol. Med. 15, 2735-2744
10. Lu, Y., and Yang, S. (2009) Angiotensin II induces cardiomyocyte hypertrophy probably through histone deacetylases. Tohoku J. Exp. Med. 219, 17-23
11. Kahali, S., Sarcar, B., Fang, B., Williams, E. S., Koomen, J. M., Tofilon, P. J., and Chinnaiyan, P. (2010) Activation of the unfolded protein response contributes toward the antitumor activity of vorinostat. Neoplasia 12, 80-86
12. Malhotra, J. D., and Kaufman, R. J. (2007) The endoplasmic reticulum and the unfolded protein response. Semin. Cell Dev. Biol. 18, 716-731
13. Schönthal, A. H. (2013) Pharmacological targeting of endoplasmic reticulum stress signaling in cancer. Biochem. Pharmacol. 85, 653-666
14. Olzmann, J. A., Kopito, R. R., and Christianson, J. C. (2013) The mammalian endoplasmic reticulum-associated degradation system. Cold Spring Harb. Perspect. Biol. 5, a013185
15. Cattaneo, M., Otsu, M., Fagioli, C., Martino, S., Lotti, L. V., Sitia, R., and Biunno, I. (2008) SEL1L and HRD1 are involved in the degradation of unassembled secretory Ig-μ chains. J. Cell Physiol. 215, 794-802
16. Christianson, J. C, Shaler, T. A., Tyler, R. E., and Kopito, R. R. (2008) OS-9 and GRP94 deliver mutant α1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat. Cell Biol. 10, 272-282
17. Francisco, A. B., Singh, R., Li, S., Vani, A. K., Yang, L., Munroe, R. J., Diaferia, G., Cardano, M., Biunno, I., Qi, L., Schimenti, J. C, and Long, Q. (2010) Deficiency of suppressor enhancer Lin12 1 like (SEL1L) in mice leads to systemic endoplasmic reticulum stress and embryonic lethality. J. Biol. Chem. 285, 13694-13703
18. Cardano, M., Diaferia, G. R., Cattaneo, M., Dessì, S. S., Long, Q., Conti, L., Deblasio, P., Cattaneo, E., and Biunno, I. (2011) mSEL-1L(suppressor/enhancer Lin12-like) protein levels influence murine neural stem cell self-renewal and lineage commitment. J. Biol. Chem. 286, 18708-18719
19. Cattaneo, M., Orlandini, S., Beghelli, S., Moore, P. S., Sorio, C, Bonora, A., Bassi, C, Talamini, G., Zamboni, G., Orlandi, R., Ménard, S., Bernardi, L. R., Biunno, I., and Scarpa, A. (2003) SEL1L expression in pancreatic adenocarcinoma parallels SMAD4 expression and delays tumor growth in vitro and in vivo. Oncogene 22, 6359-6368
20. Liu, Q., Chen, J., Wang, J., Amos, C, Killary, A. M., Sen, S., Wei, C, and Frazier, M. L. P (2013) Putative tumor suppressor gene SEL1L was down-regulated by aberrantly up-regulated hsa-mir-155 in human pancreatic ductal adenocarcinoma. Mol. Carcinog. doi:10.1002/mc.22023
21. Orlandi, R., Cattaneo, M., Troglio, F., Casalini, P., Ronchini, C, Ménard, S., and Biunno, I. (2002) SEL1L expression decreases breast tumor cell aggressiveness in vivo and in vitro. Cancer Res. 62, 567-574
22. Barberis, M. C, Roz, E., and Biunno, I. (2006) SEL1L expression in prostatic intraepithelial neoplasia and adenocarcinoma. An immunohistochemical study. Histopathology 48, 614-616
23. Liu, P., Ramachandran, S., Ali Seyed, M., Scharer, C. D., Laycock, N., Dalton, W. B., Williams, H., Karanam, S., Datta, M. W., Jaye, D. L., and Moreno, C. S. (2006) Sex-determining region Y box 4 is a transforming oncogene in human prostate cancer cells. Cancer Res. 66, 4011-4019
24. Chandran, U. R., Ma, C, Dhir, R., Bisceglia, M., Lyons-Weiler, M., Liang, W., Michalopoulos, G., Becich, M., and Monzon, F. A. (2007) Gene expression profiles of prostate cancer reveal involvement of multiple molecular pathways in the metastatic process. BMC Cancer 7, 64
25. Granelli, P., Cattaneo, M., Ferrero, S., Bottiglieri, L., Bosari, S., Fichera, G., and Biunno, I. (2004) SEL1L and squamous cell carcinoma of the esophagus. Clin. Cancer Res. 10, 5857-5861
26. Ashktorab, H., Green, W., Finzi, G., Sessa, F., Nouraie, M., Lee, E. L., Morgano, A., Moschetta, A., Cattaneo, M., Mariani-Costantini, R., Brim, H., and Biunno, I. (2012) SEL1L, an UPR response protein, a potential marker of colonic cell transformation. Dig. Dis. Sci. 57, 905-912
27. Ferrero, S., Falleni, M., Cattaneo, M., Malferrari, G., Canton, C, Biagiotti, L., Maggioni, M., Nosotti, M., Coggi, G., Bosari, S., and Biunno, I. (2006) SEL1L expression in non-small cell lung cancer. Hum. Pathol. 37, 505-512
28. Pollard, S. M., Yoshikawa, K., Clarke, I. D., Danovi, D., Stricker, S., Russell, R., Bayani, J., Head, R., Lee, M., Bernstein, M., Squire, J. A., Smith, A., and Dirks, P. (2009) Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 4, 568-580
29. Griffero, F., Daga, A., Marubbi, D., Capra, M. C, Melotti, A., Pattarozzi, A., Gatti, M., Bajetto, A., Porcile, C, Barbieri, F., Favoni, R. E., Lo Casto, M., Zona, G., Spaziante, R., Florio, T., and Corte, G. (2009) Different response of human glioma tumor-initiating cells to epidermal growth factor receptor kinase inhibitors. J. Biol. Chem. 284, 7138-7148
30. Baronchelli, S., Bentivegna, A., Redaelli, S., Riva, G., Butta, V., Paoletta, L., Isimbaldi, G., Miozzo, M., Tabano, S., Daga, A., Marubbi, D., Cattaneo, M., Biunno, I., and Dalprà, L. (2013) Delineating the cytogenomic and epigenomic landscapes of glioma stem cell lines. PLoS ONE 8, e57462
31. Louis, D. N., Ohgaki, H., Wiestler, O. D., and Cavenee, W. K. (2007) WHO Classification of Tumors of the Central Nervous Systems, 4th Ed., International Agency for Research on Cancer (IARC), Lyon, France
32. Orlandi, R., Cattaneo, M., Troglio, F., Campiglio, M., Biunno, I., and Ménard, S. (2002) Production of a monoclonal antibody directed against the recombinant SEL1L protein. Int. J. Biol. Markers 17, 104-111
33. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., and Mesirov, J. P. (2005) Gene set enrichment analysis. A knowledgebased approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A. 102, 15545-15550
34. Grant, B., and Greenwald, I. (1996) The Caenorhabditis elegansSel-1 gene, a negative regulatorof Lin-12 and Glp-1, encodesa predicted extracellular protein. Genetics 143, 237-247
35. Li, S., Francisco, A. B., Munroe, R. J., Schimenti, J. C., and Long, Q. (2010) SEL1L deficiency impairs growth and differentiation of pancreatic epithelial cells. BMC Dev. Biol. 10, 19
36. Galanis, E., Jaeckle, K. A., Maurer, M. J., Reid, J. M., Ames, M. M., Hardwick, J. S., Reilly, J. F., Loboda, A., Nebozhyn, M., Fantin, V. R., Richon, V. M., Scheithauer, B., Giannini, C., Flynn, P. J., Moore, D. F. Jr., Zwiebel, J., and Buckner, J. C. (2009) Phase II trial of vorinostat in recurrent glioblastoma multiforme. A north central cancer treatment group study. J. Clin. Oncol. 27, 2052-2058
37. Bowden, C. L., Brugger, A. M., Swann, A. C., Calabrese, J. R., Janicak, P. G., Petty, F., Dilsaver, S. C., Davis, J. M., Rush, A. J., and Small, J. G. (1994) Efficacy of divalproex vs. lithium and placebo in the treatment of mania. The Depakote Mania Study Group. JAMA 271, 918-924
38. Thomas, R. P., Recht, L., and Nagpal, S. (2013) Advances in the managementofglioblastoma. The role of temozolomide and MGMT testing. Clin. Pharmacol. 5, 1-9
39. Chen, Y., Tsai, Y. H., and Tseng, S. H. (2012) Valproic acid affected the survival and invasiveness of human glioma cells through diverse mechanisms. J. Neurooncol. 109, 23-33
40. Shao, C. J., Wu, M. W., Chen, F. R., Li, C., Xia, Y. F., and Chen, Z. P. (2012) Histone deacetylase inhibitor, 2-propylpentanoic acid, increases the chemosensitivity and radiosensitivity ofhuman glioma cell linesin vitro. Chin. Med. J. 125, 4338-4343
41. Ryu, C. H., Yoon, W. S., Park, K. Y., Kim, S. M., Lim, J. Y., Woo, J. S., Jeong, C. H., Hou, Y., and Jeun, S. S. (2012) Valproic acid down-regulates the expression of MGMT and sensitizes temozolomide-resistant Glioma Cells. J. Biomed Biotechnol. 2012, 987495
42. Osuka, S., Takano, S., Watanabe, S., Ishikawa, E., Yamamoto, T., and Matsumura, A. (2012) Valproic acid inhibits angiogenesis in vitro and glioma angiogenesis in vivo in the brain. Neurol. Med. Chir. (Tokyo) 52, 186-193
43. Biunno, I., Cattaneo, M., Orlandi, R., Canton, C., Biagiotti, L., Ferrero, S., Barberis, M., Pupa, S. M., Scarpa, A., and Ménard, S. (2006) SEL1L a multifaceted protein playing a role in tumor progression. J. Cell Physiol. 208, 23-38
44. Fan, X., Khaki, L., Zhu, T. S., Soules, M. E., Talsma, C. E., Gul, N., Koh, C., Zhang, J., Li, Y. M., Maciaczyk, J., Nikkhah, G., Dimeco, F., Piccirillo, S., Vescovi, A. L., and Eberhart, C. G. (2010) NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 28, 5-16
45. Choi, M. S., Yoo, A. S., and Greenwald, I. (2010) sel-11 and cdc-42, two negative modulators of LIN-12/Notch activity in C. elegans. PloS ONE 5, e11885
46. Adler, J. T., Hottinger, D. G., Kunnimalaiyaan, M., and Chen, H. (2008) Histone deacetylase inhibitors up-regulate Notch-1 and inhibit growth in pheochromocytoma cells. Surgery. 144, 956-961; discussion 961-2
47. Obeng, E. A., Carlson, L. M., Gutman, D. M., Harrington, W. J. Jr., Lee, K. P., and Boise, L. H. (2006) Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 107, 4907-4916
48. Siegelin, M. D., Dohi, T., Raskett, C. M., Orlowski, G. M., Powers, C. M., Gilbert, C. A., Ross, A. H., Plescia, J., and Altieri, D. C. (2011) Exploiting the mitochondrial unfolded protein response for cancer therapy in mice and human cells. J. Clin. Invest. 121, 1349-1360
49. Natsume, A., Kinjo, S., Yuki, K., Kato, T., Ohno, M., Motomura, K., Iwami, K., and Wakabayashi, T. (2011) Glioma-initiating cells and molecular pathology. Implications for therapy. Brain Tumor Pathol. 28, 1-12
50. Takezaki, T., Hide, T., Takanaga, H., Nakamura, H., Kuratsu, J., and Kondo, T. (2011) Essential role of the Hedgehog signaling pathway in human glioma-initiating cells. Cancer Sci. 102, 1306-1312
51. Machado, M. C., Bellodi-Privato, M., Kubrusly, M. S., Molan, N. A., Tharcisio, T. Jr., De Oliveira, E. R., and D'Albuquerque, L. A. (2011) Valproic acid inhibits human hepatocellular cancer cells growth in vitroand in vivo. J. Exp. Ther. Oncol. 9, 85-92
52. Stockhausen, M. T., Sjölund, J., Manetopoulos, C., and Axelson, H. (2005) Effects of the histone deacetylase inhibitor valproic acid on Notch signalling in human neuroblastoma cells. Br. J. Cancer 92, 751-759