Krüppel-like factor 5 is not required for K-RasG12D lung tumorigenesis, but represses ABCG2 expression and is associated with better disease-specific survival

American Journal of Pathology

Volumn 177, Issue 3, 2010, Pages 1503-1513

  Meyer, Sara E ^a   Hasenstein, Jason R ^a   Baktula, Avinash ^a   Velu, Chinavenmani S ^a   Xu, Yan ^a   Wan, Huajing ^a   Whitsett, Jeffrey A ^a   Gilks, C Blake ^b   Grimes, H Leighton ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b VANCOUVER GENERAL HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABCG2 PROTEIN, HUMAN; KLF5 PROTEIN, HUMAN; KRAS PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; ONCOPROTEIN; RAS PROTEIN; TUMOR PROTEIN;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CELL TRANSFORMATION; CHROMATIN IMMUNOPRECIPITATION; DISEASE FREE SURVIVAL; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; LUNG NON SMALL CELL CANCER; LUNG TUMOR; METABOLISM; MOUSE; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE MICROARRAY; TUMOR CELL LINE; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; DISEASE-FREE SURVIVAL; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LUNG NEOPLASMS; MICE; NEOPLASM PROTEINS; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE ARRAY ANALYSIS;

EID: 77956536155     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090651     Document Type: Article

References (46)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ: Cancer Statistics, 2008. CA Cancer J Clin 2008, 58:71-96
2. Pao W, Kris MG, Iafrate AJ, Ladanyi M, Janne PA, Wistuba II, Miake-Lye R, Herbst RS, Carbone DP, Johnson BE, Lynch TJ: Integration of molecular profiling into the lung cancer clinic. Clin Cancer Res 2009, 15:5317-5322
3. Rodenhuis S, Slebos RJ: Clinical significance of ras oncogene activation in human lung cancer. Cancer Res 1992, 52:2665s-2669s
4. Pao W, Wang TY, Riely GJ, Miller VA, Pan Q, Ladanyi M, Zakowski MF, Heelan RT, Kris MG, Varmus HE: KRAS mutations and primary resistance of lung adenocarcinomas to gefitinib or erlotinib. PLoS Med 2005, 2:e17
5. Sun S, Schiller JH, Spinola M, Minna JD: New molecularly targeted therapies for lung cancer. J Clin Invest 2007, 117:2740-2750
6. Salgia R, Skarin AT: Molecular abnormalities in lung cancer. J Clin Oncol 1998, 16:1207-1217
7. Meuwissen R, Berns A: Mouse models for human lung cancer. Genes Dev 2005, 19:643-664
8. Tuveson DA, Jacks T: Modeling human lung cancer in mice: similarities and shortcomings. Oncogene 1999, 18:5318-5324
9. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, Jacks T, Tuveson DA: Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001, 15:3243-3248
10. Johnson L, Mercer K, Greenbaum D, Bronson RT, Crowley D, Tuveson DA, Jacks T: Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 2001, 410:1111-1116 (Pubitemid 32391044)
11. Bieker JJ: Kruppel-like factors: three fingers in many pies. J Biol Chem 2001, 276:34355-34358 (Pubitemid 37384419)
12. Shi H, Zhang Z, Wang X, Liu S, Teng CT: Isolation and characterization of a gene encoding human Kruppel-like factor 5 (IKLF): binding to the CAAT/GT box of the mouse lactoferrin gene promoter. Nucleic Acids Res 1999, 27:4807-4815 (Pubitemid 30006672)
13. Sur I, Unden AB, Toftgard R: Human Kruppel-like factor5/KLF5: synergy with NF-kappaB/Rel factors and expression in human skin and hair follicles. Eur J Cell Biol 2002, 81:323-334 (Pubitemid 34692943)
14. Chen C, Bhalala HV, Qiao H, Dong JT: A possible tumor suppressor role of the KLF5 transcription factor in human breast cancer. Oncogene 2002, 21:6567-6572 (Pubitemid 35177035)
15. Nandan MO, Yoon HS, Zhao W, Ouko LA, Chanchevalap S, Yang VW: Kruppel-like factor 5 mediates the transforming activity of oncogenic H-Ras. Oncogene 2004, 23:3404-3413 (Pubitemid 38669830)
16. Taneyhill L, Pennica D: Identification of Wnt responsive genes using a murine mammary epithelial cell line model system. BMC Dev Biol 2004, 4:6
17. Beckers J, Herrmann F, Rieger S, Drobyshev AL, Horsch M, Hrabe de Angelis M, Seliger B: Identification and validation of novel ERBB2 (HER2. NEU) targets including genes involved in angiogenesis. Int J Cancer 2005, 114:590-597 (Pubitemid 40349618)
18. Nandan MO, McConnell BB, Ghaleb AM, Bialkowska AB, Sheng H, Shao J, Babbin BA, Robine S, Yang VW: Kruppel-like factor 5 mediates cellular transformation during oncogenic KRAS-induced intestinal tumorigenesis. Gastroenterology 2008, 134:120-130 (Pubitemid 350309321)
19. Chen C, Bhalala HV, Vessella RL, Dong JT: KLF5 is frequently deleted and down-regulated but rarely mutated in prostate cancer. Prostate 2003, 55:81-88 (Pubitemid 36443994)
20. Tong D, Czerwenka K, Heinze G, Ryffel M, Schuster E, Witt A, Leodolter S, Zeillinger R: Expression of KLF5 is a prognostic factor for disease-free survival and overall survival in patients with breast cancer. Clin Cancer Res 2006, 12:2442-2448
21. Bateman NW, Tan D, Pestell RG, Black JD, Black AR: Intestinal tumor progression is associated with altered function of KLF5. J Biol Chem 2004, 279:12093-12101 (Pubitemid 38445773)
22. Yang Y, Goldstein BG, Chao HH, Katz JP: KLF4 and KLF5 regulate proliferation, apoptosis and invasion in esophageal cancer cells. Cancer Biol Ther 2005, 4:1216-1221
23. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF: Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA: 2003, 100:3983-3988 (Pubitemid 36418143)
24. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB: Identification of human brain tumour initiating cells. Nature 2004, 432:396-401 (Pubitemid 39551674)
25. Ho MM, Ng AV, Lam S, Hung JY: Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 2007, 67:4827-4833 (Pubitemid 46910191)
26. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, Osawa M, Nakauchi H, Sorrentino BP: The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 2001, 7:1028-1034 (Pubitemid 32937383)
27. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC: Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 1996, 183:1797-1806 (Pubitemid 26134320)
28. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, Goodell MA, Brenner MK: A distinct "side population" of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA: 2004, 101:14228-14233
29. Kondo T, Setoguchi T, Taga T: Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci USA: 2004, 101:781-786 (Pubitemid 38121035)
30. Feuring-Buske M, Hogge DE: Hoechst 33342 efflux identifies a subpopulation of cytogenetically normal CD34(+)CD38(-) progenitor cells from patients with acute myeloid leukemia. Blood 2001, 97:3882-3889
31. Wulf GG, Wang RY, Kuehnle I, Weidner D, Marini F, Brenner MK, Andreeff M, Goodell MA: A leukemic stem cell with intrinsic drug efflux capacity in acute myeloid leukemia. Blood 2001, 98:1166-1173
32. Wan H, Luo F, Wert SE, Zhang L, Xu Y, Ikegami M, Maeda Y, Bell SM, Whitsett JA: Kruppel-like factor 5 is required for perinatal lung morphogenesis and function. Development 2008, 135:2563-2572
33. Akagi K, Sandig V, Vooijs M, Van der Valk M, Giovannini M, Strauss M, Berns A: Cre-mediated somatic site-specific recombination in mice. Nucleic Acids Res 1997, 25:1766-1773 (Pubitemid 27303358)
34. Nikitin AY, Alcaraz A, Anver MR, Bronson RT, Cardiff RD, Dixon D, Fraire AE, Gabrielson EW, Gunning WT, Haines DC, Kaufman MH, Linnoila RI, Maronpot RR, Rabson AS, Reddick RL, Rehm S, Rozengurt N, Schuller HM, Shmidt EN, Travis WD, Ward JM, Jacks T: Classification of proliferative pulmonary lesions of the mouse: recommendations of the mouse models of human cancers consortium. Cancer Res 2004, 64:2307-2316
35. Ionescu DN, Treaba D, Gilks CB, Leung S, Renouf D, Laskin J, Wood-Baker R, Gown AM: Nonsmall cell lung carcinoma with neuroendocrine differentiation-an entity of no clinical or prognostic significance. Am J Surg Pathol 2007, 31:26-32
36. Xu Y, Liu C, Clark JC, Whitsett JA: Functional genomic responses to cystic fibrosis transmembrane conductance regulator (CFTR) and CFTR(delta508) in the lung. J Biol Chem 2006, 281:11279-11291 (Pubitemid 43855553)
37. Xu Y, Ikegami M, Wang Y, Matsuzaki Y, Whitsett JA: Gene expression and biological processes influenced by deletion of Stat3 in pulmonary type II epithelial cells. BMC Genomics 2007, 8:455 (Pubitemid 351228656)
38. Wright GW, Simon RM: A random variance model for detection of differential gene expression in small microarray experiments. Bioinformatics 2003, 19:2448-2455
39. Shaw AT, Meissner A, Dowdle JA, Crowley D, Magendantz M, Ouyang C, Parisi T, Rajagopal J, Blank LJ, Bronson RT, Stone JR, Tuveson DA, Jaenisch R, Jacks T: Sprouty-2 regulates oncogenic K-ras in lung development and tumorigenesis. Genes Dev 2007, 21:694-707 (Pubitemid 46440291)
40. Chen C, Benjamin MS, Sun X, Otto KB, Guo P, Dong XY, Bao Y, Zhou Z, Cheng X, Simons JW, Dong JT: KLF5 promotes cell proliferation and tumorigenesis through gene regulation and the TSU-Pr1 human bladder cancer cell line. Int J Cancer 2006, 118:1346-1355 (Pubitemid 43306519)
41. Ghaleb AM, Nandan MO, Chanchevalap S, Dalton WB, Hisamuddin IM, Yang VW: Kruppel-like factors 4 and 5: the yin and yang regulators of cellular proliferation. Cell Res 2005, 15:92-96 (Pubitemid 41653948)
42. Black AR, Black JD, Azizkhan-Clifford J: Sp1 and kruppel-like factor family of transcription factors in cell growth regulation and cancer. J Cell Physiol 2001, 188:143-160
43. Donnenberg VS, Donnenberg AD: Multiple drug resistance in cancer revisited: the cancer stem cell hypothesis. J Clin Pharmacol 2005, 45:872-877 (Pubitemid 41060226)
44. Finlan LE, Hupp TR: p63: the phantom of the tumor suppressor. Cell Cycle 2007, 6:1062-1071
45. Nylander K, Vojtesek B, Nenutil R, Lindgren B, Roos G, Zhanxiang W, Sjostrom B, Dahlqvist A, Coates PJ: Differential expression of p63 isoforms in normal tissues and neoplastic cells. J Pathol 2002, 198:417-427
46. Ura H, Usuda M, Kinoshita K, Sun C, Mori K, Akagi T, Matsuda T, Koide H, Yokota T: STAT3 and Oct-3/4 control histone modification through induction of Eed in embryonic stem cells. J Biol Chem 2008, 283:9713-9723