MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells

PLoS ONE

Volumn 4, Issue 8, 2009, Pages

  Ji, Qing ^a,c,e   Hao, Xinbao ^a,d   Zhang, Min ^a   Tang, Wenhua ^a   Meng, Yang ^a   Li, Ling ^a   Xiang, Debing ^a   DeSano, Jeffrey T ^a   Bommer, Guido T ^b   Fan, Daiming ^c   Fearon, Eric R ^a,b   Lawrence, Theodore S ^a   Xu, Liang ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d HAINAN UNIVERSITY   (China)

^e THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CD133 ANTIGEN; HERMES ANTIGEN; LENTIVIRUS VECTOR; MICRORNA; MIR 34; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; PROTEIN BCL 2; PROTEIN P53; UNCLASSIFIED DRUG; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; PEPTIDE; PRIMER DNA;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER RADIOTHERAPY; CANCER STEM CELL; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL FATE; CELL GROWTH; CELL INVASION; CELL RENEWAL; CHEMOSENSITIZATION; COLONY FORMATION; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVATION; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MUTANT; NONHUMAN; PANCREAS CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIOSENSITIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; CELL CYCLE; CELL DIVISION; IMMUNOLOGY; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PANCREAS TUMOR; PATHOLOGY; PHYSIOLOGY;

3' UNTRANSLATED REGIONS; ANIMALS; ANTIGENS, CD; ANTIGENS, CD44; APOPTOSIS; BASE SEQUENCE; CELL CYCLE; CELL DIVISION; DNA PRIMERS; FEMALE; GLYCOPROTEINS; HUMANS; MICE; MICE, NUDE; MICRORNAS; PANCREATIC NEOPLASMS; PEPTIDES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 69949087531     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006816     Document Type: Article

References (48)

1. Croce CM, Calin GA (2005) miRNAs, cancer, and stem cell division. Cell 122: 6-7.
2. Hatfield S, Ruohola-Baker H (2008) microRNA and stem cell function. Cell Tissue Res 331: 57-66.
3. Zhang W, Dahlberg JE, Tam W (2007) MicroRNAs in tumorigenesis: a primer. Am J Pathol 171: 728-738.
4. Papagiannakopoulos T, Kosik KS (2008) MicroRNAs: regulators of oncogenesis and stemness. BMC Med 6: 15.
5. Yu F, Yao H, Zhu P, Zhang X, Pan Q, et al. (2007) let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 131: 1109-1123.
6. Ji Q, Hao X, Meng Y, Zhang M, Desano J, et al. (2008) Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer 8: 266.
7. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, et al. (2007) Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 6: 1586-1593.
8. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, et al. (2007) Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 26: 745-752.
9. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, et al. (2007) Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 26: 731-743.
10. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, et al. (2007) p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 17: 1298-1307.
11. He L, He X, Lim LP, de Stanchina E, Xuan Z, et al. (2007) A microRNA component of the p53 tumour suppressor network. Nature 447: 1130-1134.
12. Yamakuchi M, Ferlito M, Lowenstein CJ (2008) miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci U S A 105: 13421-13426.
13. Zenz T, Mohr J, Eldering E, Kater AP, Buhler A, et al. (2008) MiR-34a as part of the chemotherapy resistance network in chronic lymphocytic leukemia. Blood.
14. Dontu G, Jackson KW, McNicholas E, Kawamura MJ, Abdallah WM, et al. (2004) Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res 6: R605-615.
15. Xu L, Yang D, Wang S, Tang W, Liu M, et al. (2005) (-)-Gossypol enhances response to radiation therapy and results in tumor regression of human prostate cancer. Mol Cancer Ther 4: 197-205.
16. Dai Y, Liu M, Tang W, Desano J, Burstein E, et al. (2008) Molecularly targeted radiosensitization of human prostate cancer by modulating inhibitor of apoptosis. Clin Cancer Res 14: 7701-7710.
17. Dai Y, DeSano JT, Meng Y, Ji Q, Ljungman M, et al. (2009) Celastrol potentiates radiotherapy by impairment of DNA damage processing in human prostate cancer. Int J Radiat Oncol Biol Phys 74: 1217-1225.
18. Meng Y, TangW, Dai Y, Wu X, LiuM, et al. (2008) Natural BH3 mimetic (-)-gossypol chemosensitizes human prostate cancer via Bcl-xL inhibition accompanied by increase of Puma and Noxa. Mol Cancer Ther 7: 2192-2202.
19. Immervoll H, Hoem D, Sakariassen PO, Steffensen OJ, Molven A (2008) Expression of the "stem cell marker" CD133 in pancreas and pancreatic ductal adenocarcinomas. BMC Cancer 8: 48.
20. Bloomston M, Frankel WL, Petrocca F, Volinia S, Alder H, et al. (2007) MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. Jama 297: 1901-1908.
21. Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, Nikitin AY (2007) MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res 67: 8433-8438.
22. Welch C, Chen Y, Stallings RL (2007) MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 26: 5017-5022.
23. Xu L, Huang CC, Huang W, Tang WH, Rait A, et al. (2002) Systemic tumor-targeted gene delivery by anti-transferrin receptor scFv-immunoliposomes. Mol Cancer Ther 1: 337-346.
24. Xu L, Frederik P, Pirollo KF, Tang WH, Rait A, et al. (2002) Self-assembly of a virus-mimicking nanostructure system for efficient tumor-targeted gene delivery. Hum Gene Ther 13: 469-481.
25. Dai Y, Lawrence TS, Xu L (2009) Overcoming cancer therapy resistance by targeting inhibitors of apoptosis proteins and nuclear factor-kappa B. Am J Transl Res 1: 4-18.
26. Tazawa H, Tsuchiya N, Izumiya M, Nakagama H (2007) Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci U S A 104: 15472-15477.
27. Xu L, Pirollo KF, Rait A, Murray AL, Chang EH (1999) Systemic p53 Gene Therapy In Combination with Radiation Results in Human Tumor Regression. Tumor Targeting 4: 92-104.
28. Xu L, Pirollo KF, Chang EH (1997) Transferrin-liposome-mediated p53 sensitization of squamous cell carcinoma of the head and neck to radiation in vitro. Hum Gene Ther 8: 467-475.
29. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, et al. (2007) Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037.
30. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, et al. (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323.
31. Han Z, Hong L, Han Y, Wu K, Han S, et al. (2007) Phospho Akt mediates multidrug resistance of gastric cancer cells through regulation of P-gp, Bcl-2 and Bax. J Exp Clin Cancer Res 26: 261-268.
32. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) From the Cover: Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences 100: 3983-3988.
33. Lee CJ, Dosch J, Simeone DM (2008) Pancreatic cancer stem cells. J Clin Oncol 26: 2806-2812.
34. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, et al. (2007) ALDH1 Is a Marker of Normal and Malignant Human Mammary Stem Cells and a Predictor of Poor Clinical Outcome. Cell Stem Cell 1: 555-567.
35. 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.
36. Simeone DM (2008) Pancreatic cancer stem cells: implications for the treatment of pancreatic cancer. Clin Cancer Res 14: 5646-5648.
37. Rich JN (2007) Cancer stem cells in radiation resistance. Cancer Res 67: 8980-8984.
38. Wicha MS (2006) Cancer stem cells and metastasis: lethal seeds. Clin Cancer Res 12: 5606-5607.
39. Phillips TM, McBride WH, Pajonk F (2006) The response of CD24(-/low)/ CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 98: 1777-1785.
40. Dontu G, Al-Hajj M, Abdallah WM, Clarke MF, Wicha MS (2003) Stem cells in normal breast development and breast cancer. Cell Prolif 36 Suppl 1: 59-72.
41. Bui M, Reiter RE (1999) Stem cell genes in androgen-independent prostate cancer. Cancer Metastasis Rev 17: 391-399.
42. Wong DJ, Liu H, Ridky TW, Cassarino D, Segal E, et al. (2008) Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2: 333-344.
43. Nicolis SK (2007) Cancer stem cells and "stemness" genes in neuro-oncology. Neurobiol Dis 25: 217-229.
44. Fan X, Matsui W, Khaki L, Stearns D, Chun J, et al. (2006) Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 66: 7445-7452.
45. Wang Z, Zhang Y, Li Y, Banerjee S, Liao J, et al. (2006) Down-regulation of Notch-1 contributes to cell growth inhibition and apoptosis in pancreatic cancer cells. Mol Cancer Ther 5: 483-493.
46. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, et al. (2006) Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442: 823-826.
47. Houbaviy HB, Murray MF, Sharp PA (2003) Embryonic stem cell-specific MicroRNAs. Dev Cell 5: 351-358.
48. Korkaya H, Wicha MS (2007) Selective targeting of cancer stem cells: a new concept in cancer therapeutics. BioDrugs 21: 299-310.