An off-target nucleostemin RNAi inhibits growth in human glioblastoma-derived cancer stem cells

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Gil Ranedo, Jon ^a   Mendiburu Eliçabe, Marina ^a   García Villanueva, Mercedes ^b   Medina, Diego ^b   del Álamo, Marta ^b   Izquierdo, Marta ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b HOSPITAL RAMÓN Y CAJAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; LENTIVIRUS VECTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEOSTEMIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; CD133 ANTIGEN; GLYCOPROTEIN; GNL3 PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; NUCLEAR PROTEIN; PEPTIDE; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER STEM CELL; CANCER TISSUE; CANCER TRANSPLANTATION; CARCINOGENESIS; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; ANIMAL; CELL AGGREGATION; CELL SURVIVAL; CELL TRANSFORMATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; KINETICS; METABOLISM; NUDE RAT; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD; APOPTOSIS; CELL AGGREGATION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; GLYCOPROTEINS; GTP-BINDING PROTEINS; HUMANS; KINETICS; NEOPLASTIC STEM CELLS; NUCLEAR PROTEINS; PEPTIDES; RATS; RATS, NUDE; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 83155176317     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028753     Document Type: Article

References (48)

1. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, et al. (2001) Malignant glioma: genetics and biology of a grave matter. Genes Dev 15: 1311-1333.
2. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, et al. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352: 987-996.
3. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, et al. (2006) Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 66: 9339-9344.
4. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, et al. (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367: 645-648.
5. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF, (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988.
6. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, et al. (2003) Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100: 15178-15183.
7. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ, (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65: 10946-10951.
8. Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, et al. (2005) A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 65: 9328-9337.
9. Szotek PP, Pieretti-Vanmarcke R, Masiakos PT, Dinulescu DM, Connolly D, et al. (2006) Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc Natl Acad Sci U S A 103: 11154-11159.
10. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, et al. (2007) Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci U S A 104: 973-978.
11. O'Brien CA, Pollett A, Gallinger S, Dick JE, (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110.
12. Li C, Heidt DG, (2007) Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037.
13. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, et al. (2008) Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 15: 504-514.
14. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, et al. (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760.
15. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, et al. (2006) Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5: 67.
16. Baumann M, Krause M, Hill R, (2008) Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer.
17. Irvin DK, Jouanneau E, Duvall G, Zhang XX, Zhai Y, et al. (2010) T cells enhance stem-like properties and conditional malignancy in gliomas. PLoS One 7: e10974 1-17.
18. Charles N, Holland EC, (2009) Brain tumor treatment increases the number of cancer stem-like cells. Expert Rev Neurother 9: 1447-1449.
19. Shu Q, Wong KK, Su JM, Adesina AM, Yu LT, et al. (2008) Direct orthotopic transplantation of fresh surgical specimen preserves CD133+ tumor cells in clinically relevant mouse models of medulloblastoma and glioma. Stem Cells 26: 1414-1424.
20. Wakimoto H, Kesari S, Farrel CJ, Curry WT, Zaupa C, et al. (2009) Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic Herpes simplex virus vectors. Cancer Res 69: 3472-3481.
21. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, et al. (2006) Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444: 761-765.
22. Tsai RY, McKay RD, (2002) A nucleolar mechanism controlling cell proliferation in stem cells and cancer cells. Genes Dev 16: 2991-3003.
23. Ma H, Pederson T, (2007) Depletion of the nucleolar protein nucleostemin causes G1 cell cycle arrest via the p53 pathway. Mol Biol Cell 18: 2630-2635.
24. Liu RL, Zhang ZH, Zhao WM, Wang M, Qi SY, et al. (2008) Expression of nucleostemin in prostate cancer and its effect on the proliferation of PC-3 cells. Chin Med J (Engl) 121: 299-304.
25. Zhu Q, Yasumoto H, Tsai RY, (2006) Nucleostemin delays cellular senescence and negatively regulates TRF1 protein stability. Mol Cell Biol 26: 9279-9290.
26. Dai MS, Sun XX, Lu H, (2008) Aberrant expression of nucleostemin activates p53 and induces cell cycle arrest via inhibition of MDM2. Mol Cell Biol 28: 4365-4376.
27. Kafienah W, Mistry S, Williams C, Hollander AP, (2006) Nucleostemin is a marker of proliferating stromal stem cells in adult human bone marrow. Stem Cells 24: 1113-1120.
28. Jafarnejad SM, Mowla SJ, Matin MM, (2008) Knocking-down the expression of nucleostemin significantly decreases rate of proliferation of rat bone marrow stromal stem cells in an apparently p53-independent manner. Cell Prolif 41: 28-35.
29. Beekman C, Nichane M, De Clercq S, Maetens M, Floss T, et al. (2006) Evolutionarily conserved role of nucleostemin: controlling proliferation of stem/progenitor cells during early vertebrate development. Mol Cell Biol 26: 9291-9301.
30. Nomura J, Maruyama M, Katano M, Kato H, Zhang J, et al. (2009) Differential requirement for nucleostemin in embryonic stem cell and neural stem cell viability. Stem Cells 27: 1066-1076.
31. Sijin L, Ziwei C, Yajun L, Meiyu D, Hongwei Z, et al. (2004) The effect of knocking-down nucleostemin gene expression on the in vitro proliferation and in vivo tumorigenesis of HeLa cells. J Exp Clin Cancer Res 23: 529-538.
32. Romanova L, Grand A, Zhang L, Rayner S, Katoku-Kikyo N, et al. (2009) Critical role of nucleostemin in pre-rRNA processing. J Biol Chem 284: 4968-4977.
33. Romanova L, Kellner S, Katoku-Kikyo N, Kikyo N, (2009) Novel role of nucleostemin in the maintenance of nucleolar architecture and integrity of small nucleolar ribonucleoproteins and the telomerase complex. J Biol Chem 284: 26685-26694.
34. Gross C, (2000) Neurogenesis in the adult brain: death of a dogma. Nature Reviews Neuroscience 1: 67-73.
35. Morrison SJ, Kimble J, (2006) Asymetric and symetric stem-cell divisions in development and cancer. Nature 441: 1068-1074.
36. Werbowetski-Ogilvie TE, Bossé M, Stewart M, Schnerch A, Ramos-Mejia V, et al. (2009) Characterization of human embryonic stem cells with features of neoplastic progression. Nature Biotechnol 27: 91-97.
37. Grupta PB, Chaffer CL, Weinberg RA, (2009) Cancer stem cells: mirage or reality? Nature Medicine 15: 1010-1012.
38. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, et al. (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828.
39. Nikpour P, Mowla SJ, Jafarnejad SM, Fischer U, Schulz WA, (2009) Differential effects of nucleostemin suppression on cell cycle arrest and apoptosis in the bladder cancer cell lines 5637 and SW1710. Cell Prolif 42: 762-769.
40. Lin T, Meng L, Li Y, Tsai RY, (2010) Tumor-initiating function of nucleostemin-enriched mammary tumor cells. Cancer Res 70: 9444-9452.
41. Malakootian M, Mowla SJ, Saberi H, Asadi MH, Atlasi Y, et al. (2010) Differential expression of nucleostemin, a stem cell marker, and its variants in different types of brain tumors. Mol Carcinog 49: 818-825.
42. Naito Y, Yamada T, Matsumiya T, Ui-Tei K, Saigo K, et al. (2005) dsCheck: highly sensitive off-target search software for double-stranded RNA-mediated RNA interference. Nucleic Acids Res 33: 589-591.
43. Jackson AL, Burchard J, Schelter J, Chau BN, Cleary M, et al. (2006) Widespread siRNA "off-target" transcript silencing mediated by seed region sequence complementarity. RNA 12: 1179-1187.
44. Echeverri CJ, Beachy PA, Baum B, Boutros M, Buchholz F, et al. (2006) Minimizing the risk of reporting false positives in large-scale RNAi screens. Nat Methods 3: 777-779.
45. Jackson AL, Linsley PS, (2010) Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nature Reviews Drug Discovery 9: 57-67.
46. Schultz N, Marenstein DR, De Angelis DA, Wang WQ, Nelander S, et al. (2011) Off-target effects dominate a large-scale RNAi screen for modulators of the TGF-β pathway and reveal microRNA regulation of TGFBR2. Silence 2 PMID: 21401928 [PubMed- in process]PMCID: PMC23068080Free PMC Article.
47. Lin X, Ruan X, Anderson MG, McDowell JA, Kroeger PE, et al. (2005) siRNA-mediated off-target gene silencing triggered by a 7 nt complementation. Nucleic Acids Res 33: 4527-4535.
48. Kim YW, Liu TJ, Koul D, Tiao N, Feroze AH, et al. (2011) Identification of novel synergistic targets for rational drug combinations with PI3 kinase inhibitors using siRNA synthetic lethality screening against GBM. Neuro Oncol 13: 367-375.