Targeting Neuroblastoma Stem Cells with Retinoic Acid and Proteasome Inhibitor

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Hämmerle, Barbara ^a   Yañez, Yania ^b   Palanca, Sarai ^b   Cañete, Adela ^b   Burks, Deborah J ^a,c   Castel, Victoria ^b   Font de Mora, Jaime ^b,d  

^a CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^b HOSPITAL UNIVERSITARIO LA FE   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d UNIVERSIDAD CATÓLICA DE VALENCIA SAN VICENTE MÁRTIR   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BORTEZOMIB; ISOTRETINOIN; NESTIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SOX2;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRAIN; CELL STRAIN SH SY5Y; CELL STRAIN SK N BE; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; ENZYME INHIBITION; GROWTH INHIBITION; HUMAN; HUMAN CELL; NEURAL STEM CELL; NEUROBLASTOMA; NEUROBLASTOMA CELL; PROTEIN DEGRADATION; TARGET CELL; TUMOR RECURRENCE;

APOPTOSIS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; FLOW CYTOMETRY; G2 PHASE CELL CYCLE CHECKPOINTS; HUMANS; LEUPEPTINS; MICROSCOPY, CONFOCAL; NEOPLASTIC STEM CELLS; NESTIN; NEUROBLASTOMA; OCTAMER TRANSCRIPTION FACTOR-3; PROTEASOME INHIBITORS; SIDE-POPULATION CELLS; SOXB1 TRANSCRIPTION FACTORS; TIME FACTORS; TRETINOIN;

EID: 84885052613     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076761     Document Type: Article

References (51)

1. Canete A, Gerrard M, Rubie H, Castel V, Di Cataldo A, et al. (2009) Poor survival for infants with MYCN-amplified metastatic neuroblastoma despite intensified treatment: the International Society of Paediatric Oncology European Neuroblastoma Experience. J Clin Oncol 27: 1014-1019. doi:10.1200/JCO.2007.14.5839. PubMed: 19171715.
2. London WB, Castel V, Monclair T, Ambros PF, Pearson AD, et al. (2011) Clinical and biologic features predictive of survival after relapse of neuroblastoma: a report from the International Neuroblastoma Risk Group project. J Clin Oncol 29: 3286-3292. doi:10.1200/JCO.2010.34.3392. PubMed: 21768459.
3. Maris JM, Hogarty MD, Bagatell R, Cohn SL, (2007) Neuroblastoma. Lancet 369: 2106-2120. doi:10.1016/S0140-6736(07)60983-0. PubMed: 17586306.
4. Matthay KK, Villablanca JG, Seeger RC, Stram DO, Harris RE, et al. (1999) Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children's Cancer Group. N Engl J Med 341: 1165-1173.
5. Fang Y, Zhou X, Lin M, Ying M, Luo P, et al. (2011) Inhibition of all-trans-retinoic acid-induced proteasome activation potentiates the differentiating effect of retinoid in acute myeloid leukemia cells. Mol Carcinog 50: 24-35. doi:10.1002/mc.20687. PubMed: 20945414.
6. Luo P, Lin M, Li L, Yang B, He Q, (2011) The proteasome inhibitor bortezomib enhances ATRA-induced differentiation of neuroblastoma cells via the JNK mitogen-activated protein kinase pathway. PLOS ONE 6: e27298. doi:10.1371/journal.pone.0027298. PubMed: 22087283.
7. Horton TM, Pati D, Plon SE, Thompson PA, Bomgaars LR, et al. (2007) A phase 1 study of the proteasome inhibitor bortezomib in pediatric patients with refractory leukemia: a Children's Oncology Group study. Clin Cancer Res 13: 1516-1522. doi:10.1158/1078-0432.CCR-06-2173. PubMed: 17332297.
8. Orlowski RZ, Kuhn DJ, (2008) Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin Cancer Res 14: 1649-1657. doi:10.1158/1078-0432.CCR-07-2218. PubMed: 18347166.
9. Brignole C, Marimpietri D, Pastorino F, Nico B, Di Paolo D, et al. (2006) Effect of bortezomib on human neuroblastoma cell growth, apoptosis, and angiogenesis. J Natl Cancer Inst 98: 1142-1157. doi:10.1093/jnci/djj309. PubMed: 16912267.
10. Combaret V, Boyault S, Iacono I, Brejon S, Rousseau R, et al. (2008) Effect of bortezomib on human neuroblastoma: analysis of molecular mechanisms involved in cytotoxicity. Mol Cancer 7: 50. doi:10.1186/1476-4598-7-50. PubMed: 18534018.
11. Suzuki E, Demo S, Deu E, Keats J, Arastu-Kapur S, et al. (2011) Molecular mechanisms of bortezomib resistant adenocarcinoma cells. PLOS ONE 6: e27996. doi:10.1371/journal.pone.0027996. PubMed: 22216088.
12. Tanturli M, Giuntoli S, Barbetti V, Rovida E, Dello Sbarba P, (2011) Hypoxia selects bortezomib-resistant stem cells of chronic myeloid leukemia. PLOS ONE 6: e17008. doi:10.1371/journal.pone.0017008. PubMed: 21347297.
13. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, et al. (2004) A distinct "side population" of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci U S A 101: 14228-14233. doi:10.1073/pnas.0400067101. PubMed: 15381773.
14. Mahller YY, Williams JP, Baird WH, Mitton B, Grossheim J, et al. (2009) Neuroblastoma cell lines contain pluripotent tumor initiating cells that are susceptible to a targeted oncolytic virus. PLOS ONE 4: e4235. doi:10.1371/journal.pone.0004235. PubMed: 19156211.
15. Hagenbuchner J, Ausserlechner MJ, Porto V, David R, Meister B, et al. (2010) The anti-apoptotic protein BCL2L1/Bcl-xL is neutralized by pro-apoptotic PMAIP1/Noxa in neuroblastoma, thereby determining bortezomib sensitivity independent of prosurvival MCL1 expression. J Biol Chem 285: 6904-6912. doi:10.1074/jbc.M109.038331. PubMed: 20051518.
16. Nakaso K, Yoshimoto Y, Yano H, Takeshima T, Nakashima K, (2004) p53-mediated mitochondrial dysfunction by proteasome inhibition in dopaminergic SH-SY5Y cells. Neurosci Lett 354: 213-216. doi:10.1016/j.neulet.2003.10.048. PubMed: 14700734.
17. Bavi P, Uddin S, Ahmed M, Jehan Z, Bu R, et al. (2011) Bortezomib stabilizes mitotic cyclins and prevents cell cycle progression via inhibition of UBE2C in colorectal carcinoma. Am J Pathol 178: 2109-2120. doi:10.1016/j.ajpath.2011.01.034. PubMed: 21514426.
18. Hutter G, Rieken M, Pastore A, Weigert O, Zimmermann Y, et al. (2012) The proteasome inhibitor bortezomib targets cell cycle and apoptosis and acts synergistically in a sequence-dependent way with chemotherapeutic agents in mantle cell lymphoma. Ann Hematol 91: 847-856. doi:10.1007/s00277-011-1377-y. PubMed: 22231280.
19. Kim OH, Lim JH, Woo KJ, Kim YH, Jin IN, et al. (2004) Influence of p53 and p21Waf1 expression on G2/M phase arrest of colorectal carcinoma HCT116 cells to proteasome inhibitors. Int J Oncol 24: 935-941. PubMed: 15010833.
20. Ling YH, Liebes L, Jiang JD, Holland JF, Elliott PJ, et al. (2003) Mechanisms of proteasome inhibitor PS-341-induced G(2)-M-phase arrest and apoptosis in human non-small cell lung cancer cell lines. Clin Cancer Res 9: 1145-1154. PubMed: 12631620.
21. Pagnan G, Di Paolo D, Carosio R, Pastorino F, Marimpietri D, et al. (2009) The combined therapeutic effects of bortezomib and fenretinide on neuroblastoma cells involve endoplasmic reticulum stress response. Clin Cancer Res 15: 1199-1209. doi:10.1158/1078-0432.CCR-08-2477. PubMed: 19228726.
22. Yin D, Zhou H, Kumagai T, Liu G, Ong JM, et al. (2005) Proteasome inhibitor PS-341 causes cell growth arrest and apoptosis in human glioblastoma multiforme (GBM). Oncogene 24: 344-354. doi:10.1038/sj.onc.1208225. PubMed: 15531918.
23. Williams SA, McConkey DJ, (2003) The proteasome inhibitor bortezomib stabilizes a novel active form of p53 in human LNCaP-Pro5 prostate cancer cells. Cancer Res 63: 7338-7344. PubMed: 14612532.
24. Tweddle DA, Malcolm AJ, Bown N, Pearson AD, Lunec J, (2001) Evidence for the development of p53 mutations after cytotoxic therapy in a neuroblastoma cell line. Cancer Res 61: 8-13. PubMed: 11196202.
25. Barkett M, Gilmore TD, (1999) Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 18: 6910-6924. doi:10.1038/sj.onc.1203238. PubMed: 10602466.
26. Pickering BM, de Mel S, Lee M, Howell M, Habens F, et al. (2007) Pharmacological inhibitors of NF-kappaB accelerate apoptosis in chronic lymphocytic leukaemia cells. Oncogene 26: 1166-1177. doi:10.1038/sj.onc.1209897. PubMed: 16924235.
27. Dong QG, Sclabas GM, Fujioka S, Schmidt C, Peng B, et al. (2002) The function of multiple IkappaB: NF-kappaB complexes in the resistance of cancer cells to Taxol-induced apoptosis. Oncogene 21: 6510-6519. doi:10.1038/sj.onc.1205848. PubMed: 12226754.
28. Loercher A, Lee TL, Ricker JL, Howard A, Geoghegen J, et al. (2004) Nuclear factor-kappaB is an important modulator of the altered gene expression profile and malignant phenotype in squamous cell carcinoma. Cancer Res 64: 6511-6523. doi:10.1158/0008-5472.CAN-04-0852. PubMed: 15374962.
29. Hideshima T, Chauhan D, Richardson P, Mitsiades C, Mitsiades N, et al. (2002) NF-kappa B as a therapeutic target in multiple myeloma. J Biol Chem 277: 16639-16647. doi:10.1074/jbc.M200360200. PubMed: 11872748.
30. Hideshima T, Richardson P, Chauhan D, Palombella VJ, Elliott PJ, et al. (2001) The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res 61: 3071-3076. PubMed: 11306489.
31. Sunwoo JB, Chen Z, Dong G, Yeh N, Crowl Bancroft C, et al. (2001) Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor-kappa B, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma. Clin Cancer Res 7: 1419-1428. PubMed: 11350913.
32. Reynolds CP, Wang Y, Melton LJ, Einhorn PA, Slamon DJ, et al. (2000) Retinoic-acid-resistant neuroblastoma cell lines show altered MYC regulation and high sensitivity to fenretinide. Med Pediatr Oncol 35: 597-602. doi:10.1002/1096-911X(20001201)35:6. PubMed: 11107126.
33. Richardson PG, Hideshima T, Anderson KC, (2003) Bortezomib (PS-341): a novel, first-in-class proteasome inhibitor for the treatment of multiple myeloma and other cancers. Cancer Contr 10: 361-369. PubMed: 14581890.
34. Lavelin I, Beer A, Kam Z, Rotter V, Oren M, et al. (2009) Discovery of novel proteasome inhibitors using a high-content cell-based screening system. PLOS ONE 4: e8503. doi:10.1371/journal.pone.0008503. PubMed: 20041034.
35. Adams J, Palombella VJ, Sausville EA, Johnson J, Destree A, et al. (1999) Proteasome inhibitors: a novel class of potent and effective antitumor agents. Cancer Res 59: 2615-2622. PubMed: 10363983.
36. Cusack JC Jr., Liu R, Houston M, Abendroth K, Elliott PJ, et al. (2001) Enhanced chemosensitivity to CPT-11 with proteasome inhibitor PS-341: implications for systemic nuclear factor-kappaB inhibition. Cancer Res 61: 3535-3540. PubMed: 11325813.
37. MacLaren AP, Chapman RS, Wyllie AH, Watson CJ, (2001) p53-dependent apoptosis induced by proteasome inhibition in mammary epithelial cells. Cell Death Differ 8: 210-218. doi:10.1038/sj.cdd.4400801. PubMed: 11319603.
38. Moon KY, (2007) The chemopreventive effect of retinoids on cellular NF-kappaB activity induced by NMU and NEU in human malignant keratinocytes. Cancer Res Treat 39: 82-87. doi:10.4143/crt.2007.39.2.82. PubMed: 19746216.
39. Brown RE, Tan D, Taylor JS, Miller M, Prichard JW, et al. (2007) Morphoproteomic confirmation of constitutively activated mTOR, ERK, and NF-kappaB pathways in high risk neuro-blastoma, with cell cycle and protein analyte correlates. Ann Clin Lab Sci 37: 141-147. PubMed: 17522369.
40. Lorenzi S, Forloni M, Cifaldi L, Antonucci C, Citti A, et al. (2012) IRF1 and NF-kB restore MHC class I-restricted tumor antigen processing and presentation to cytotoxic T cells in aggressive neuroblastoma. PLOS ONE 7: e46928. doi:10.1371/journal.pone.0046928. PubMed: 23071666.
41. Schwitalla S, Fingerle AA, Cammareri P, Nebelsiek T, Göktuna SI, et al. (2013) Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 152: 25-38. doi:10.1016/j.cell.2012.12.012. PubMed: 23273993.
42. Polyak K, Hahn WC, (2006) Roots and stems: stem cells in cancer. Nat Med 12: 296-300. doi:10.1038/nm1379. PubMed: 16520777.
43. Chambers I, Tomlinson SR, (2009) The transcriptional foundation of pluripotency. Development 136: 2311-2322. doi:10.1242/dev.024398. PubMed: 19542351.
44. Newton TC, Wolcott K, Roberts SS, (2010) Comparison of the side populations in pretreatment and postrelapse neuroblastoma cell lines. Transl Oncol 3: 246-251. PubMed: 20689766.
45. Wang X, Wang J, Huang V, Place RF, Li LC, (2012) Induction of NANOG expression by targeting promoter sequence with small activating RNA antagonizes retinoic acid-induced differentiation. Biochem J 443: 821-828. doi:10.1042/BJ20111491. PubMed: 22339500.
46. Kumar SM, Liu S, Lu H, Zhang H, Zhang PJ, et al. (2012) Acquired cancer stem cell phenotypes through Oct4-mediated dedifferentiation. Oncogene 31: 4898-4911. doi:10.1038/onc.2011.656. PubMed: 22286766.
47. Thomas SK, Messam CA, Spengler BA, Biedler JL, Ross RA, (2004) Nestin is a potential mediator of malignancy in human neuroblastoma cells. J Biol Chem 279: 27994-27999. doi:10.1074/jbc.M312663200. PubMed: 15117961.
48. Ying M, Zhou X, Zhong L, Lin N, Jing H, et al. (2013) Bortezomib sensitizes human acute myeloid leukemia cells to all-trans-retinoic acid-induced differentiation by modifying the RARalpha/STAT1 axis. Mol Cancer Ther 12: 195-206. doi:10.1158/1535-7163.MCT-12-0433. PubMed: 23243061.
49. Uttenweiler-Joseph S, Bouyssié D, Calligaris D, Lutz PG, Monsarrat B, et al. (2013) Quantitative proteomic analysis to decipher the differential apoptotic response of bortezomib-treated APL cells before and after retinoic acid differentiation reveals involvement of protein toxicity mechanisms. Proteomics 13: 37-47. doi:10.1002/pmic.201200233. PubMed: 23135970.
50. Reynolds CP, Matthay KK, Villablanca JG, Maurer BJ, (2003) Retinoid therapy of high-risk neuroblastoma. Cancer Lett 197: 185-192. doi:10.1016/S0304-3835(03)00108-3. PubMed: 12880980.
51. Veal GJ, Cole M, Errington J, Pearson AD, Foot AB, et al. (2007) Pharmacokinetics and metabolism of 13-cis-retinoic acid (isotretinoin) in children with high-risk neuroblastoma- a study of the United Kingdom Children's Cancer Study Group. Br J Cancer 96: 424-431. doi:10.1038/sj.bjc.6603554. PubMed: 17224928.