Are we missing the target? - Cancer stem cells and drug resistance in non-small cell lung cancer

Cancer Genomics and Proteomics

Volumn 9, Issue 5, 2012, Pages 275-286

  Gottschling, Sandra ^a   Schnabel, Philipp A ^b   Herth, Felix J F ^a   Herpel, Esther ^b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Cancer stem cells; Drug resistance; Non small cell lung cancer; Review; Targeted therapy

Indexed keywords

8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; ANTINEOPLASTIC AGENT; AXITINIB; BMS 833923; BUPARLISIB; CARBOPLATIN; CRIZOTINIB; EVEROLIMUS; GEFITINIB; IMETELSTAT; INIPARIB; LEQ 506; LY 2228820; LY 2606368; LY 3007113; MSC 1936369B; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; N (6,7 DIHYDRO 6 OXO 5H DIBENZ[B,D]AZEPIN 7 YL) 2,2 DIMETHYL N' (2,2,3,3,3 PENTAFLUOROPROPYL)PROPANEDIAMIDE; NAVELBINE; PACLITAXEL; PELITINIB; PF 04449913; PRI 724; SARIDEGIB; SELUMETINIB; TARIQUIDAR; TERTOMOTIDE; TRAMETINIB; UNCLASSIFIED DRUG; UNINDEXED DRUG; VANDETANIB; VISMODEGIB;

CANCER PROGNOSIS; CANCER RESISTANCE; CANCER STEM CELL; CANCER SURVIVAL; DRUG MECHANISM; GENE MUTATION; GENETIC ANALYSIS; HUMAN; LUNG ADENOCARCINOMA; LUNG ALVEOLUS EPITHELIUM; LUNG NON SMALL CELL CANCER; NONHUMAN; ONCOGENE K RAS; REVIEW; TREATMENT RESPONSE;

EID: 84867385274     PISSN: 11096535     EISSN: 17906245     Source Type: Journal    
DOI: None     Document Type: Review

References (86)

1. American Cancer Society: Cancer Statistics 2008. http://www.cancer.org/ docroot/STT/stt-0.asp.
2. Goeckenjan G, Sitter H, Thomas M, Branscheid D, Flentje M, Griesinger F, Niederle N, Stuschke M, Blum T, Deppermann KM, Ficker JH, Freitag L, Lübbe AS, Reinhold T, Späth-Schwalbe E, Ukena D, Wickert M, Wolf M, Andreas S, Auberger T, Baum RP, Baysal B, Beuth J, Bickeböller H, Böcking A, Bohle RM, Brüske I, Burghuber O, Dickgreber N, Diederich S, Dienemann H, Eberhardt W, Eggeling S, Fink T, Fischer B, Franke M, Friedel G, Gauler T, Gütz S, Hautmann H, Hellmann A, Hellwig D, Herth F, Heussel CP, Hilbe W, Hoffmeyer F, Horneber M, Huber RM, Hübner J, Kauczor HU, Kirchbacher K, Kirsten D, Kraus T, Lang SM, Martens U, Mohn-Staudner A, Müller KM, Müller-Nordhorn J, Nowak D, Ochmann U, Passlick B, Petersen I, Pirker R, Pokrajac B, Reck M, Riha S, Rübe C, Schmittel A, Schönfeld N, Schütte W, Serke M, Stamatis G, Steingräber M, Steins M, Stoelben E, Swoboda L, Teschler H, Tessen HW, Weber M, Werner A, Wichmann HE, Irlinger Wimmer E, Witt C, Worth H; German Respiratory Society; German Cancer Society: Prevention, diagnosis, therapy, and follow-up of lung cancer: interdisciplinary guideline of the German Respiratory Society and the German Cancer Society. Pneumologie 65: 39-59, 2011.
3. Fraire AE, Roggli VL, Vollmer RT, Greenberg SD, McGavran MH, Spjut HJ and Yesner R: Lung cancer heterogeneity. Prognostic implications. Cancer 60: 3701-375, 1987.
4. Reya T, Morrison SJ, Clarke MF, Weissman IL: Stem cells, cancer, and cancer stem cells. Nature 414: 105-111, 2001. (Pubitemid 33041634)
5. Sullivan JP, Minna JD and Shay JW: Evidence for self-renewing lung cancer stem cells and their implications in tumour initiation, progression, and targeted therapy. Cancer Metastasis Rev 29: 61-72, 2010.
6. Otto WR: Lung epithelial stem cells. J Pathol 197: 527-535, 2002.
7. Rawlins EL and Hogan BLM: Epithelial stem cells of the lung: privileged few or opportunities for many? Development 133: 2455-2465, 2006. (Pubitemid 44123396)
8. Maenhaut C, Dumont JE, Roger PP and van Staveren WCG: Cancer stem cells: a reality, a myth, a fuzzy concept or a misnomer? An analysis. Carcinogenesis 31: 149-158, 2010.
9. Adams JM and Strasser A: Is tumor growth sustained by rare cancer stem cells or dominant clones? Cancer Res 68: 4018-4021, 2008.
10. Hong KU, Reynolds SD, Watikins S, Fuchs E and Stripp BR: Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am J Pathol 164: 577-588, 2004. (Pubitemid 38364673)
11. Reynolds SD, Giangreco A, Power JHT and Stripp BR: Neuroepithelial bodies of pulmonary airways serve as a reservoir of progenitor cells capable of epithelial regeneration. Am J Pathol 156: 269-278, 2000. (Pubitemid 30644460)
12. Bender Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, Crowley D, Bronson RT and Jacks T: Identification of bronchioloalveolar stem cells in normal lung and lung cancer. Cell 121: 823-835, 2005. (Pubitemid 40806415)
13. McQualter JL, Yuen K, Williams B and Bertoncello I: Evidence of an epithelial stem/progenitor cell hierarchy in the adult mouse lung. Proc Natl Acad Sci USA 107: 1414-1419, 2010.
14. Chen H, Matsumoto K, Brockway BL, Rackley CR, Liang J, Lee JH, Jiang D, Noble PW, Randell SH, Kim CF and Stripp BR: Airway epithelial progenitors are region-specific and show differential response to bleomycin-induced lung injury. Stem Cells 2012 Jun 13. doi: 10.1002/stem.1150. [Epub ahead of print]
15. Xu X, Rock JR, lu Y, Futtner C, Schwab B, Guinney J, Hogan BLM and Onaitis MW: Evidence for type II cells as cells of origin of K-Ras-induced distal lung adenocarcinoma. Proc Natl Acad Sci USA 109: 4910-4915, 2012.
16. Ho MM, Ng AV, Lam S and Hung JY: Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 67: 4827-4833, 2007. (Pubitemid 46910191)
17. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, Conticello C, Ruco L, Peschle C and De Maria R: Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 15: 504-514, 2008. (Pubitemid 351267301)
18. Chen Y-C, Hsu H-S, Chen Y-W, Tsai T-H, How C-K, Wang C-Y, Hung S-C, Chang Y-L, Tsai M-L, Lee y-Y, Ku H-H and Chiou SH: Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS One 3: e2637, 2008.
19. Levina V, Marrangoni AM, DeMarco R, Gorelik E and Lokshin AE: Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PLoS One 3: e3077, 2008.
20. Bertolini G, Roz L, Perego P, Tortoreto M, Fontanella E, Gatti L, Pratesi G, Fabbri A, Andriani F, Tinelli S, Roz E, Caserini U, Lo Vullo S, Camerini T, Mariani L, Delia D, Calabro E, Pastorino U and Sozzi G: Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA 106: 16281-16286, 2009.
21. Curtis SJ, Sinkevicius KW, Li D, Lau AN, Roach RR, Zamponi R, Woolfenden AE, Kirsch DG, Wong K-K and Kim CF: Primary tumor genotype is an important determinant in identification of lung cancer propagating cells. Cell Stem Cell 7: 127-133, 2010.
22. Kris MG, Johnson BE, Kwiatkowski DJ, Iafrate AJ, Wistuba II, Aronson SL, Engelman JA, Shyr Y, Khuri FR, Rudin CM, Garon EB, Pao W, Schiller JH, Haura EB, Shirai K, Giaccone G, Berry LD, Kugler K, Minna JD and Bunn PA: Identification of driver mutations in tumor specimens from 1,000 patients with lung adenocarcinoma: The NCI's Lung Cancer Mutation Consortium (LCMC). J Clin Oncol 29 Suppl. (May 20 Supplement): CRA7506, 2011.
23. Ding L, Getz G, Wheeler DA, Mardis ER, McLellan MD, Cibulskis K, Sougnez C, Greulich H, Muzny DM, Morgan MB, Fulton L, Fulton RS, Zhang Q, Wendl MC, Lawrence MS, Larson DE, Chen K, Dooling DJ, Sabo A, Hawes AC, Shen H, Jhangiani SN, Lewis LR, Hall O, Zhu Y, Mathew T, Ren Y, Yao J, Scherer SE, Clerc K, Metcalf GA, Ng B, Milosavljevic A, Gonzalez-Garay ML, Osborne JR, Meyer R, Shi X, Tang Y, Koboldt DC, Lin L, Abbott R, Miner TL, Pohl C, Fewell G, Haipek C, Schmidt H, Dunford-Shore BH, Kraja A, Crosby SD, Sawyer CS, Vickery T, Sander S, Robinson J, Winckler W, Baldwin J, Chirieac LR, Dutt A, Fennell T, Hanna M, Johnson BE, Onofrio RC, Thomas RK, Tonon G, Weir BA, Zhao X, Ziaugra L, Zody MC, Giordano T, Orringer MB, Roth JA, Spitz MR, Wistuba II, Ozenberger B, Good PJ, Chang AC, Beer DG, Watson MA, Ladanyi M, Broderick S, Yoshizawa A, Travis WD, Pao W, Province MA, Weinstock GM, Varmus HE, Gabriel SB, Lander ES, Gibbs RA, Meyerson M and Wilson RK: Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455: 1069-1075, 2008.
24. Moreira AL, Gonen M, Rekhtman N, Downey RJ: Progenitor stem cell marker expression by pulmonary carcinomas. Mod Pathol 23: 889-895, 2010.
25. Herpel E, Jensen K, Muley T, Warth A, Schnabel PA, Meister M, Herth FJF, Dienemann H, Thomas M and Gottschling S: The cancer stem cell antigens CD133, BCRP1/ABCG2 and CD117/c-KIT are not associated with prognosis in resected early-stage non-small cell lung cancer. Anticancer Res 31: 4491-4500, 2011.
26. Yoh K, Ishii G, Yokose T, Minegishi Y, Tsuta K, Goto K, Nishiwaki Y, Kodama T, Suga M and Ochiai A: Breast cancer resistance protein impacts clinical outcome in platinum-based chemotherapy for advanced non-small cell lung cancer. Clin Cancer Res 10: 1691-1697, 2004. (Pubitemid 38435560)
27. Ota S, Ishii G, Goto K, Kubota K, Kim YH, Kojika M, Murata Y, Yamazaki M, Nishiwaki Y, Eguchi K and Ochiai A: Immunohistochemical expression of BCRP1 and ERCC1 in biopsy specimen predicts survival in advanced non-small-cell lung cancer treated with cisplatin-based chemotherapy. Lung Cancer 64: 98-104, 2009.
28. Li F, Zeng H and Ying K: The combination of stem cell markers CD133 and ABCG2 predicts relapse in stage I non-small cell lung carcinomas. Med Oncol 28: 1458-1462, 2011.
29. Salnikov AV, Gladkich J, Moldenhauer G, Volm M, Mattern J and Herr I: CD133 is indicative for a resistance phenotype but does not represent a prognostic marker for survival of non-small cell lung cancer patients. Int J Cancer 126: 950-958, 2010.
30. Woo T, Okudela K, Mitsui H, Yazawa T, Ogawa N, Tajiri M, Yamamoto T, Rino Y, Kitamura H and Masuda M: Prognostic value of CD133 expression in stage I lung adenocarcinomas. Int J Clin Exp Pathol 4: 32-42, 2010.
31. Shien K, Toyooka S, Ichimura K, Soh J, Furukawa M, Maki Y, Muraoka T, Tanaka N, Ueno T, Asano H, Tsukuda K, Yamane M, Oto T, Kiura K and Miyoshi S: Prognostic impact of cancer stem cell-related markers in non-small cell lung cancer patients treated with induction chemoradiotherapy. Lung Cancer 77: 162-167, 2012.
32. Ooi AT, Mah V, Nickerson DW, Gilbert JL, Ha VL, Hegab AE, Horvath S, Alavi M, Maresh EL, Chia D, Gower AC, Lenburg ME, Spira A, Solis LM, Wistuba II, Walser TC, Wallace WD, Dubinett SM, Goodglick L and Gomperts BN: Presence of a putative tumor-initiating progenitor cell population predicts poor prognosis in smokers with non-small cell lung cancer. Cancer Res 70: 6639-6648, 2010.
33. Zhang X, Han B, Huang J, Zheng B, Geng Q, Aziz F and Dong Q: Prognostic significance of OCT4 expression in adenocarcinoma of the lung. Jpn J Clin Oncol 40: 961-966, 2010.
34. Onaitis M, D'Amico TA, Clark CP, Guinney J, Harpole DH and Rawlins EL: A 10-gene progenitor cell signature predicts poor prognosis in lung adenocarcinoma. Ann Thorac Surg 91: 1046-1050, 2011.
35. Eismann U, Oberschmidt O, Ehnert M, Fleeth J, Lüdtke FE, Struck S, Schulz L, Blatter J, Lahn MM, Ma D, Niyikiza C, Paoletti P and Hanauske AR: Pemetrexed: mRNA expression of the target genes TS, GARFT and DHFR correlates with the in vitro chemosensitivity of human solid tumors. Int J Clin Pharmacol Ther 43: 567-569, 2005. (Pubitemid 43009351)
36. Reiman T, Lai R, Veillard AS, Paris E, Soria JC, Rosell R, Taron M, Graziano S, Kratzke R, Seymour L, Shepherd FA, Pignon JP, Sève P; LACE-Bio Group: Cross-validation study of class III beta-tubulin as a predictive marker for benefit from adjuvant chemotherapy in resected non-small-cell lung cancer: analysis of four randomized trials. Ann Oncol 23: 86-93, 2012.
37. Kaira K, Takahashi T, Murakami H, Shukuya T, Kenmotsu H, Ono A, Naito T, Tsuya A, Nakamura Y, Endo M, Kondo H, Nakajima T and Yamamoto N: The role of βIII-tubulin in nonsmall cell lung cancer patients treated by taxane-based chemotherapy. Int J Clin Oncol 2012 Feb 23. doi: 10.1007/s10147-012-0386-8. [Epub ahead of print]
38. Rosell R, Moran T, Queralt C, Porta R, Cardenal F, Camps C, Majem M, Lopez-Vivanco G, Isla D, Provencio M, Insa A, Massuti B, Gonzalez-Larriba JL, Paz-Ares L, Bover I, Garcia-Campelo R, Moreno MA, Catot S, Rolfo C, Reguart N, Palmero R, Sánchez JM, Bastus R, Mayo C, Bertran-Alamillo J, Molina MA, Sanchez JJ, Taron M; Spanish Lung Cancer Group: Screening for epidermal growth factor receptor mutations in lung cancer. N Engl J Med 361: 958-967, 2009.
39. Kwak EL, Bang YJ, Camidge DR, Shaw AT, Solomon B, Maki RG, Ou SH, Dezube BJ, Jänne PA, Costa DB, Varella-Garcia M, Kim WH, Lynch TJ, Fidias P, Stubbs H, Engelman JA, Sequist LV, Tan W, Gandhi L, Mino-Kenudson M, Wei GC, Shreeve SM, Ratain MJ, Settleman J, Christensen JG, Haber DA, Wilner K, Salgia R, Shapiro GI, Clark JW and Iafrate AJ: Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med 363: 1693-1703, 2010
40. Olaussen KA, Dunant A, Fouret P, Brambilla E, André F, Haddad V, Taranchon E, Filipits M, Pirker R, Popper HH, Stahel R, Sabatier L, Pignon JP, Tursz T, Le Chevalier T, Soria JC; IALT Bio Investigators: DNA repair by ERCC1 in non-smallcell lung cancer and cisplatin-based adjuvant chemotherapy. N Engl J Med 355: 983-991, 2006.
41. Ceppi P, Volante M, Novello S, Rapa I, Danenberg KD, Danenberg PV, Cambieri A, Selvaggi G, Saviozzi S, Calogero R, Papotti M and Scagliotti GV: ERCC1 and RRM1 gene expressions but not EGFR are predictive of shorter survival in advanced non-small-cell lung cancer treated with cisplatin and gemcitabine. Ann Oncol 17: 1818-1825, 2006. (Pubitemid 44884058)
42. Lord RV, Brabender J, Gandara D, Alberola V, Camps C, Domine M, Cardenal F, Sánchez JM, Gumerlock PH, Tarón M, Sánchez JJ, Danenberg PV and Rosell R: Low ERCC1 expression correlates with prolonged survival after cisplatin plus gemcitabine chemotherapy in non-small cell lung cancer. Clin Cancer Res 8: 2286-2291, 2002. (Pubitemid 34753602)
43. Papadaki C, Sfakianaki M, Ioannidis G, Lagoudaki E, Trypaki M, Tryfonidis K, Mavroudis D, Stathopoulos E, Georgoulias V and Souglakos J: ERCC1 and BRCA1 mRNA expression levels in the primary tumor could predict the effectiveness of the second-line cisplatin-based chemotherapy in pretreated patients with metastatic non-small cell lung cancer. J Thorac Oncol 7: 663-671, 2012.
44. Bepler G, Kusmartseva I, Sharma S, Gautam A, Cantor A, Sharma A and Simon G: RRM1 modulated in vitro and in vivo efficacy of gemcitabine and platinum in non-small-cell lung cancer. J Clin Oncol 24: 4731-4737, 2006. (Pubitemid 46646245)
45. Simon GR, Schell MJ, Begum M, Kim J, Chiappori A, Haura E, Antonia S and Bepler G: Preliminary indication of survival benefit from ERCC1 and RRM1-tailored chemotherapy in patients with advanced nonsmall cell lung cancer: Evidence from an individual patient analysis. Cancer 118: 2525-2531, 2012.
46. Tomasetti C and Levy D: Role of symmetric and asymmetric division of stem cells in developing drug resistance. Proc Natl Acad Sci USA 107: 16766-16771, 2010.
47. Lord CJ and Ashworth A: The DNA damage response and cancer therapy. Nature 481: 287-294, 2012.
48. Saini V and Shoemaker RH: Potential for therapeutic targeting of tumor stem cells. Cancer Sci 101: 16-21, 2010.
49. Pine SR, Ryan BM, Vartikovsky L, Robles AI and Harris CC: Microenvironmental modulation of asymmetric cell division in human lung cancer cells. Proc Natl Acad Sci USA 107: 2195-2200, 2010.
50. Dey-Guha I, Wolfer A, Yeh AC, Albeck JG, Darp R, Leon E, Wulfkuhle J, Petricoin III EF, Wittner BS and Ramaswamy S: Asymmetric cancer cell division regulated by AKT. Proc Natl Acad Sci USA 108: 12845-1250, 2011.
51. Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, McDermott U, Azizia N, Zou L, Fischbach MA, Wong KK, Brandstetter K, Wittner B, Ramaswamy S, Classon M and Settleman J: A chromatin-mediated reversible drug tolerant state in cancer cell subpopulations. Cell 141: 69-80, 2010.
52. Knoblich JA: Asymmetric cell division: recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 11: 849-860, 2010.
53. Sherley JL: Asymmetric cell kinetics genes: the key to expansion of adult stem cells in culture. Stem Cells 20: 561-572, 2002.
54. Saywers CL: Will kinase inhibitors have a dark side? New Engl J Med 355: 313-315, 2006.
55. Bai J, Sata N and Nagai H: Gene expression analysis for predicting gemcitabine sensitivity in pancreatic cancer patients. HPB 9: 150-155, 2007. (Pubitemid 46672391)
56. Gréen H, Söderkvist P, Rosenberg P, Horvath G and Peterson C: Mdr-1 single nucleotide polymorphisms in ovarian cancer tissue: G2677T/A correlates with response to paclitaxel chemotherapy. Clin Cancer Res 12: 854-859, 2006.
57. Hegedüs C, Truta-Feles K, Antalffy G, Várady G, Német K, Ozvegy-Laczka C, Kéri G, Orfi L, Szakács G, Settleman J, Váradi A and Sarkadi B: Interaction of the EGFR inhibitors gefitinib, vandetanib, pelitinib and neratinib with the ABCG2 multidrug transporter: Implications for the emergence and reversal of cancer drug resistance. Biochem Pharmacol 84: 260-267, 2012.
58. García Campelo MR, Alonso Curbera G, Aparicio Gallego G, Grande Pulido E and Antón Aparicio LM: Stem cell and lung cancer development: blaming the Wnt, Hh and Notch signalling pathway. Clin Transl Oncol 13: 77-83, 2011 Review.
59. Tsao PN, Chen F, Izvolsky KI, Walker J, Kukuruzinska MA, Lu J and Cardoso WV: Gamma-secretase activation of notch signaling regulates the balance of proximal and distal fates in progenitor cells of the developing lung. J Biol Chem 283: 29532-29544, 2008.
60. Sullivan JP, Spinola M, Dodge M, Raso MG, Behrens C, Gao B, Schuster K, Shao C, Larsen JE, Sullivan LA, Honorio S, Xie Y, Scaglioni PP, DiMaio JM, Gazdar AF, Shay JW, Wistuba II and Minna JD: Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling. Cancer Res 70: 9937-9948, 2010.
61. Westhoff B, Colaluca IN, D'Ario G, Donzelli M, Tosoni D, Volorio S, Pelosi G, Spaggiari L, Mazzarol G, Viale G, Pece S and Di Fiore PP: Alterations of the Notch pathway in lung cancer. Proc Natl Acad Sci USA 106: 22293-22298, 2009.
62. He B, Barg RN, You L, Xu Z, Reguart N, Mikami I, Batra S, Rosell R and Jablons DM: Wnt signaling in stem cells and non-small-cell lung cancer. Clin Lung Cancer 7: 54-60, 2005. (Pubitemid 41150474)
63. Teng Y, Wang X, Wang Y and Ma D: Wnt/beta-catenin signaling regulates cancer stem cells in lung cancer A549 cells. Biochem Biophys Res Comm 392: 373-379, 2010.
64. Zhang Y, Goss AM, Cohen ED, Kadzik R, Lepore JJ, Muthukumaraswamy K, Yang J, DeMayo FJ, Whitsett JA, Parmacek MS, Morrisey EE: A Gata6-Wnt pathway required for epithelial stem cell development and airway regeneration. Nat Genet 40: 862-870, 2008. (Pubitemid 351913647)
65. Shi Y, Fu X, Hua Y, Han Y, Lu Y and Wang J: The side population in human lung cancer cell line NCI-H460 is enriched in stem-like cancer cells. PLoS One 7: e33358, 2012.
66. Tian F, Schrödl K, Kiefl R, Huber RM and Bergner A: The hedgehog pathway inhibitor alters intracellular Ca2+ homeostasis and inhibits cell growth in cisplatin-resistant lung cancer cells. Anticancer Res 32: 89-94, 2012.
67. Tiozzo C, De Langhe S, Yu M, Londhe VA, Carraro G, Li M, Li C, Xing Y, Anderson S, Borok Z, Bellusci S and Minoo P: Deletion of Pten expands lung epithelial progenitor pools and confers resistance to airway injury. Am J Respir Crit Care Med 180: 701-712, 2009.
68. Yanagi S, Kishimoto H, Kawahara K, Sasaki T, Sasaki M, Nishio M, Yajima N, Hamada K, Horie Y, Kubo H, Whitsett JA, Mak TW, Nakano T, Nakazato M and Suzuki A: Pten controls lung morphogenesis, bronchioalveolar stem cells, and onset of lung adenocarcinoma in mice. J Clin Invest 117: 2929-2940, 2007. (Pubitemid 47529623)
69. Matsumoto K, Arao T, Tanaka K, Kaneda H, Kudo K, Fujita Y, Tamura D, Aomatsu K, Tamura T, Yamada Y, Saijo N and Nishio K: mTOR signal and hypoxia-inducible factor-1 alpha regulate CD133 expression in cancer cells. Cancer Res 69: 7160-7164, 2009.
70. Agrawal M, Abraham J, Balis FM, Edgerly M, Stein WD, Bates S, Fojo T and Chen CC: Increased 99mTc-sestamibi accumulation in normal liver and drug-resistant tumors after the administration of the glycoprotein inhibitor, XR9576 Clin Cancer Res 9: 650-656, 2003. (Pubitemid 36182597)
71. Kelly RJ, Draper D, Chen CC, Robey RW, Figg WD, Piekarz RL, Chen X, Gardner ER, Balis FM, Venkatesan AM, Steinberg SM, Fojo T and Bates SE: A pharmacodynamic study of docetaxel in combination with the P-glycoprotein antagonist tariquidar (XR9576) in patients with lung, ovarian, and cervical cancer. Clin Cancer Res 17: 569-580, 2011.
72. Kelly RJ, Robey RW, Chen CC, Draper D, Luchenko V, Barnett D, Oldham RK, Caluag Z, Frye AR, Steinberg SM, Fojo T and Bates SE: A pharmacodynamic study of the p-glycoprotein antagonist CBT-1(R) in combination with paclitaxel in solid tumors. Oncologist 17: 512, 2012.
73. Wang F, Mi YJ, Chen XG, Wu XP, Liu Z, Chen SP, Liang YJ, Cheng C and Fu LW: Axitinib targeted cancer stem-like cells to enhance efficacy of chemotherapeutic drug via inhibiting the drug transport function of ABCG2. Mol Med 2012 Apr 25. doi: 10.2119/molmed.2011.00444. [Epub ahead of print]
74. Zhou WJ, Zhang X, Cheng C, Wang F, Wang XK, Liang YJ, Kin Wah To K, Zhou W, Huang HB and Fu LW: Crizotinib (PF- 02341066) reverses multidrug resistance in cancer cells by inhibiting the function of p-glycoprotein. Br J Pharmacol. 2012 Jan 10. doi: 10.1111/j.1476-5381.2012.01849.x. [Epub ahead of print]
75. Bartucci M, Sevensson S, Romania P, Dattilo R, Patrizi M, Signore M, Navarra S, Lotti F, Biffoni M, Pilozzi E, Duranti E, Martinelli S, Rinaldo C, Zeuner A, Maugeri-Saccià M, Eramo A and De Maria R: Therapeutic targeting of Chk1 in NSCLC stem cells during chemotherapy. Cell Death Diff 19: 768-778, 2012.
76. Pierceall WE, Olaussen KA, Rousseau V, Brambilla E, Sprott KM, Andre F, Pignon JP, Le Chevalier T, Pirker R, Jiang C, Filipits M, Chen Y, Kutok JL, Weaver DT, Ward BE and Soria JC: Cisplatin benefit is predicted by immunohistochemical analysis of DNA repair proteins in squamous cell carcinoma but not adenocarcinoma: theranostic modeling by NSCLC constituent histological subclasses. Ann Oncol 2012 Jan 23. doi: 10.1093/annonc/mdr624. [Epub ahead of print].
77. Lai YS, Chang CW, Pawlik KM, Zhou D, Renfrow MB and Townes TM: SRY (sex determining region Y)-box2 (Sox2)/poly ADP-ribose polymerase 1 (Parp1) complexes regulate pluripotency. Proc Natl Acad Sci USA 109: 3772-3777, 2012.
78. Shay JW and Wright WE: Telomeres and telomerase in normal and cancer stem cells. FEBS Lett 584: 3819-3825, 2010.
79. Serrano D, Bleau AM, Fernandez-Garcia I, Fernandez-Marcelo T, Iniesta P, Ortiz-de-Solorzano C and Calvo A: Inhibition of telomerase activity preferentially targets aldehyde dehydrogenase-positive cancer stem-like cells in lung cancer. Mol Cancer 10: 96, 2011.
80. Kim CB: MAPK-ing out the pathways in lung stem cell regulation. Cell Stem Cell 1: 11-13, 2007.
81. Ventura JJ, Tenbaum S, Perdiguero E, Huth M, Guerra C, Barbacid M, Pasparakis M and Nebreda AR: p38alpha MAP kinase is essential in lung stem and progenitor cell proliferation and differentiation. Nature Genet 39: 750-758, 2007. (Pubitemid 46848588)
82. Reeves ME, Baldwin ML, Aragon R, Baldwin S, Chen ST, Li X, Mohan S and Amaar YG: RASSF1C modulates the expression of a stem cell renewal gene, PIWIL1. BMC Res Notes 5: 239, 2012.
83. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA and Lander ES: Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659, 2009.
84. Dizdarevic S and Peters AM: Imaging of multidrug resistance in cancer. Cancer Imaging 11: 1-8, 2011.
85. Wang C, Cheng L, Xu H and Liu Z: Towards whole-body imaging at the single cell level using ultra-sensitive stem cell labeling with oligo-arginine modified upconversion nanoparticles. Biomaterials 33: 4872-4881, 2012.
86. Krasznai ZT, Tóth A, Mikecz P, Fodor Z, Szabó G, Galuska L, Hernádi Z and Goda K: Pgp inhibition by UIC2 antibody can be followed in vitro by using tumor-diagnostic radiotracers, 99mTc-MIBI and 18FDG. Eur J Pharm Sci 41: 665-669, 2010.