The CD44high Tumorigenic Subsets in Lung Cancer Biospecimens Are Enriched for Low miR-34a Expression

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Basak, Saroj K ^a,b   Veena, Mysore S ^a   Oh, Scott ^a,b   Lai, Chi ^b   Vangala, Sitaram ^b   Elashoff, David ^b   Fishbein, Michael C ^b   Sharma, Sanjai ^a,b   Rao, Nagesh P ^b   Rao, Dinesh ^b   Phan, Ryan ^a,b   Srivatsan, Eri S ^a,b   Batra, Raj K ^a,b  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; HERMES ANTIGEN; MICRORNA 34A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER GRADING; CANCER STEM CELL; CARCINOGENICITY; CELL CYCLE G2 PHASE; CELL SUBPOPULATION; CELL TRANSPLANTATION; CHROMATIN; CHROMOSOME 1P; CHROMOSOME ABERRATION; CHROMOSOME DELETION; COLONY FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG ADENOCARCINOMA; LUNG CANCER; LUNG SQUAMOUS CELL CARCINOMA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

ADENOCARCINOMA; ANTIGENS, CD44; BASE SEQUENCE; CARCINOMA, SQUAMOUS CELL; CHROMOSOMES, HUMAN, PAIR 1; DNA PRIMERS; FLOW CYTOMETRY; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; KARYOTYPING; LUNG NEOPLASMS; MICRORNAS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR MARKERS, BIOLOGICAL;

EID: 84883353254     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073195     Document Type: Article

References (42)

1. Siegel R, Naishadham D, Jemal A, (2012) Cancer statistics, 2012. CA Cancer J Clin 62(1): 10-29.
2. Naruke T, Tsuchiya R, Kondo H, Asamura H, Nakayama H (1997) Implications of staging in lung cancer. Chest 112(4 Suppl): 242S-248S.
3. Sugiura S, Ando Y, Minami H, Ando M, Sakai S, et al. (1997) Prognostic value of pleural effusion in patients with non-small cell lung cancer. Clin Cancer Res 3: 47-50.
4. Mott FE, Sharma N, Ashley P, (2001) Malignant pleural effusion in non-small cell lung cancer-time for a stage revision? Chest 119: 317-328.
5. Basak SK, Veena MS, Oh S, Huang G, Srivatsan E, et al. (2009) The malignant pleural effusion as a model to investigate intratumoral heterogeneity in lung cancer. PLoS One 12: e5884.
6. Neumeister V, Agarwal S, Bordeaux J, Camp RL, Rimm DL, (2010) In situ identification of putative cancer stem cells by multiplexing ALDH1, CD44, and cytokeratin identifies breast cancer patients with poor prognosis. Am J Pathol 176: 2131-2138.
7. Joshua B, Kaplan MJ, Doweck I, Pai R, Weissman IL, et al. (2012) Frequency of cells expressing CD44, a head and neck cancer stem cell marker: correlation with tumor aggressiveness. Head Neck 34: 42-49.
8. Su J, Xu XH, Huang Q, Lu MQ, Li DJ, et al. (2011) Identification of cancer stem-like CD44+ cells in human nasopharyngeal carcinoma cell line. Arch Med Res 42: 15-21.
9. Shi C, Tian R, Wang M, Wang X, Jiang J,et al. (20110) CD44+ CD133+ population exhibits cancer stem cell-like characteristics in human gallbladder carcinoma. Cancer Biol Ther 10: 1182-1190.
10. Wei HJ, Yin T, Zhu Z, Shi PF, Tian Y, et al. (2011) Expression of CD44, CD24 and ESA in pancreatic adenocarcinoma cell lines varies with local microenvironment. Hepatobiliary Pancreat Dis Int 10: 428-434.
11. Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, et al. (2006) Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 25: 1696-1708.
12. Patrawala L, Calhoun-Davis T, Schneider-Broussard R, Tang DG, (2007) Hierarchical organization of prostate cancer cells in xenograft tumors: the CD44+alpha2beta1+ cell population is enriched in tumor-initiating cells. Cancer Res 67: 6796-6805. Erratum in: Cancer Res 2007 67: 8973.
13. Hurt EM, Kawasaki BT, Klarmann GJ, Thomas SB, Farrar WL, (2008) CD44+ CD24(-) prostate cells are early cancer progenitor/stem cells that provide a model for patients with poor prognosis. Br J Cancer 98: 756-765.
14. Eaton CL, Colombel M, van der Pluijm G, Cecchini M, Wetterwald A, et al. (2010) Evaluation of the frequency of putative prostate cancer stem cells in primary and metastatic prostate cancer. Prostate. 70: 875-882.
15. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, et al. (2011) The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 17: 211-215.
16. Leung EL, Fiscus RR, Tung JW, Tin VP, Cheng LC, et al. (2010) Non-small cell lung cancer cells expressing CD44 are enriched for stem cell-like properties. PLoS One 5: e14062.
17. Takanami I, Takeuchi K, Naruke M, (2000) Expression and prognostic value of the standard CD44 protein in pulmonary adenocarcinoma. Oncol Rep 7: 1065-1067.
18. Travis WD, Brambilla E, Riely GJ, (2013) New pathologic classification of lung cancer: relevance for clinical practice and clinical trials. J Clin Oncol 31: 992-1001.
19. Gallardo E, Navarro A, Viñolas N, Marrades RM, Diaz T, et al. (2009) miR-34a as a prognostic marker of relapse in surgically resected non-small-cell lung cancer. Carcinogenesis 30: 1903-1909.
20. Srivatsan ES, Chakrabarti R, Zainabadi K, Pack SD, Benyamini P, et al. (2002) Localization of deletion to a 300 Kb interval of chromosome 11q13 in cervical cancer. Oncogene 21: 5631-5642.
21. Phelps RM, Johnson BE, Ihde DC, Gazdar AF, Carbone DP, et al. (1996) NCI-Navy Medical Oncology Branch cell line data base. J Cell Biochem Suppl. 24: 32-91.
22. Qin M, Chen S, Yu T, Escuadro B, Sharma S, et al. (2003) Coxsackievirus adenovirus receptor expression predicts the efficiency of adenoviral gene transfer into non-small cell lung cancer xenografts. Clin Cancer Res 9: 4992-4999.
23. Veena MS, Qin M, Andersson A, Sharma S, Batra RK, (2009) CAR mediates efficient tumor engraftment of mesenchymal type lung cancer cells. Lab Invest 89: 875-886.
24. Basak SK, Harui A, Stolina M, Sharma S, Mitani K, et al. (2002) Increased dendritic cell number and function following continuous in vivo infusion of granulocyte macrophage-colony-stimulating factor and interleukin-4. Blood 99: 2869-2879.
25. Srivatsan ES, Bengtsson U, Manickam P, Benyamini P, Chandrasekharappa SC, et al. (2000) Interstitial deletion of 11q13 sequences in HeLa cells. Genes Chromosomes Cancer 29: 157-165.
26. Winokur ST, Bengtsson U, Vargas JC, Wasmuth JJ, Altherr MR, et al. (1996) The evolutionary distribution and structural organization of the homeobox-containing repeat D4Z4 indicates a functional role for the ancestral copy in the FSHD region. Hum Mol Genet 5: 1567-75. Erratum in: Hum Mol Genet (1997) 6: 502.
27. Miki J, Rhim JS, (2008) Prostate cell cultures as in vitro models for the study of normal stem cells and cancer stem cells. Prostate Cancer Prostatic Dis 11: 32-9.
28. Simpson-Abelson MR, Sonnenberg GF, Takita H, Yokota SJ, Conway TF Jr, et al. (2008) Long-term engraftment and expansion of tumor-derived memory T cells following the implantation of non-disrupted pieces of human lung tumor into NOD-scid IL2Rgamma(null) mice. J Immunol 180: 7009-7018.
29. Gee HE, Buffa FM, Camps C, Ramachandran A, Leek R, et al. (2011) The small-nucleolar RNAs commonly used for microRNA normalisation correlate with tumour pathology and prognosis. Br J Cancer 104: 1168-1177.
30. Harper LJ, Costea DE, Gammon L, Fazil B, Biddle A, et al. (2010) Normal and malignant epithelial cells with stem-like properties have an extended G2 cell cycle phase that is associated with apoptotic resistance. BMC Cancer 10: 166.
31. Zhang Y, Wei J, Wang H, Xue X, An Y, et al. (2012) Epithelial mesenchymal transition correlates with CD24+CD44+ and CD133+ cells in pancreatic cancer. Oncol Rep 27: 1599-1605.
32. Sullivan JP, Spinola M, Dodge M, Raso MG, Behrens C, et al. (2010) Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling. Cancer Res 70: 9937-9948.
33. Moreb JS, Baker HV, Chang LJ, Amaya M, Lopez MC, et al. (2008) ALDH isozymes downregulation affects cell growth, cell motility and gene expression in lung cancer cells. Mol Cancer 7: 87.
34. Wang YC, Yo YT, Lee HY, Liao YP, Chao TK, et al. (2012) ALDH1-bright epithelial ovarian cancer cells are associated with CD44 expression, drug resistance, and poor clinical outcome. Am J Pathol 180: 1159-1169.
35. Mitsuuchi Y, Testa JR, (2002) Cytogenetics and molecular genetics of lung cancer. Am J Med Genet 115: 183-188.
36. Cole KA, Attiyeh EF, Mosse YP, Laquaglia MJ, Diskin SJ, et al. (2008) A functional screen identifies miR-34a as a candidate neuroblastoma tumor suppressor gene. Mol Cancer 6: 735-742.
37. Nalls D, Tang SN, Rodova M, Srivastava RK, Shankar S, (2011) Targeting epigenetic regulation of miR-34a for treatment of pancreatic cancer by inhibition of pancreatic cancer stem cells. PLoS ONE 6: e24099.
38. de Antonellis P, Medaglia C, Cusanelli E, Andolfo I, Liguori L, et al. (2011) MiR-34a targeting of Notch ligand delta like 1 impairs CD15+/CD133+ tumor-propagating cells and supports neural differentiation in medulloblastoma. PLoS ONE 6: e24584.
39. Guessous F, Zhang Y, Kofman A, Catania A, Li Y, et al. (2010) microRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle 9: 1031-1036.
40. Wiggins JF, Ruffino L, Kelnar K, Omotola M, Patrawala L, et al. (2010) Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res 70: 5923-5930.
41. Trang P, Wiggins JF, Daige CL, Cho C, Omotola M, et al. (2011) Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol Ther 19: 1116-1122.
42. Batra RK, Warburton D, (2010) On the derivation and clinical implications of "driver" mutations in lung cancer. Am J Respir Crit Care Med 182: 4-5.