Tumor cell heterogeneity in Small Cell Lung Cancer (SCLC): Phenotypical and functional differences associated with Epithelial-Mesenchymal Transition (EMT) and DNA methylation changes

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Krohn, Alexander ^a   Ahrens, Theresa ^a,b   Yalcin, Arzu ^a   Plönes, Till ^c   Wehrle, Julius ^a   Taromi, Sanaz ^a   Wollner, Stefan ^a   Follo, Marie ^a   Brabletz, Thomas ^a   Mani, Sendurai A ^d   Claus, Rainer ^a   Hackanson, Björn ^a   Burger, Meike ^a,e  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e FURTWANGEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE 3; ETOPOSIDE; FIBRONECTIN; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; PROTEIN ZO1; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TISSUE INHIBITOR OF METALLOPROTEINASE 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAI1; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; BIOLOGICAL MARKER; CADHERIN;

ARTICLE; CANCER RECURRENCE; CELL FUNCTION; CELL HETEROGENEITY; CELL INVASION; CELL MIGRATION; CELL STRUCTURE; CELL SUBPOPULATION; CELL VIABILITY; CONTROLLED STUDY; DISEASE COURSE; DNA METHYLATION; DRUG MECHANISM; DRUG RESISTANCE; ENZYME RELEASE; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG CANCER CELL LINE; LUNG SMALL CELL CANCER; PHENOTYPIC VARIATION; PROTEIN EXPRESSION; BIOSYNTHESIS; CELL MOTION; EXTRACELLULAR SPACE; GENETIC ASSOCIATION; GENETICS; LUNG TUMOR; METABOLISM; PATHOLOGY; PROTEIN DEGRADATION; SMALL CELL LUNG CANCER; TUMOR CELL LINE;

BIOLOGICAL MARKERS; CADHERINS; CELL LINE, TUMOR; CELL MOVEMENT; DNA METHYLATION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; EXTRACELLULAR SPACE; GENE EXPRESSION; GENETIC ASSOCIATION STUDIES; HUMANS; LUNG NEOPLASMS; MATRIX METALLOPROTEINASES; PROTEOLYSIS; SMALL CELL LUNG CARCINOMA; VIMENTIN;

EID: 84903545021     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100249     Document Type: Article

References (48)

1. Govindan R, Page N, Morgensztern D, Read W, Tierney R, et al. (2006) Changing epidemiology of small-cell lung cancer in the United States over the last 30 years: analysis of the surveillance, epidemiologic, and end results database. J Clin Oncol 24: 4539-4544. doi:10.1200/JCO.2005.04.4859. (Pubitemid 46630948)
2. Riaz SP, Lüchtenborg M, Coupland VH, Spicer J, Peake MD, et al. (2011) Trends in incidence of small cell lung cancer and all lung cancer. Lung Cancer.
3. Van Meerbeeck JP, Fennell DA, De Ruysscher DKM (2011) Small-cell lung cancer. Lancet 378: 1741-1755. doi:10.1016/S0140-6736(11)60165-7.
4. Haberland J, Bertz J, Wolf U, Ziese T, Kurth BM (2010) German cancer statistics 2004. BMC cancer 10: 52.
5. Lovly CM, Carbone DP (2011) Lung cancer in 2010: One size does not fit all. Nat Rev Clin Oncol 8: 68-70. doi:10.1038/nrclinonc.2010.224.
6. Haddadin S, Perry MC (2011) History of small-cell lung cancer. Clin Lung Cancer 12: 87-93. doi:10.1016/j.cllc.2011.03.002.
7. Ploenes T, Osei-Agyemang T, Krohn A, Kayser G, Burger M, et al. (2012) Surgical treatment of early stage small cell lung cancer. Asian Cardiovasc Thorac Ann 20: 694-698. doi:10.1177/0218492312453348.
8. Rekhtman N (2010) Neuroendocrine Tumors of the Lung An Update. Arch Pathol Lab Med 134: 1628-1638.
9. Cancer TIA for Ron (2004) Pathology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart. 1st ed. Travis WD, Brambilla E, Muller-Hermelink HK, Harris CC, editors World Health Organization. 344 p.
10. Sehested M, Hirsch F, Osterlind K, Olsen J (1986) Morphological Variations of Small-Cell Lung-Cancer - a Histopathologic Study of Pretreatment and Posttreatment Specimens in 104 Patients. Cancer 57: 804-807. doi:10.1002/1097-0142(19860215)57:4〈804::AID-CNCR2820570420〉3.0. CO;2-E. (Pubitemid 16161060)
11. Brambilla E, Moro D, Gazzeri S, Brichon PY, Nagy-Mignotte H, et al. (1991) Cytotoxic chemotherapy induces cell differentiation in small-cell lung carcinoma. JCO 9: 50-61.
12. Scheel C, Weinberg RA (2012) Cancer stem cells and epithelial-mesenchymal transition: Concepts and molecular links. Seminars in Cancer Biology. Available: http://www.ncbi.nlm.nih.gov/pubmed/22554795. Accessed 2012 Jun 5.
13. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142. doi:10.1038/nrm1835. (Pubitemid 43278296)
14. Shibue T, Weinberg RA (2011) Metastatic colonization: settlement, adaptation and propagation of tumor cells in a foreign tissue environment. Semin Cancer Biol 21: 99-106. doi:10.1016/j.semcancer.2010.12.003.
15. Polyak K, Weinberg RA (2009) Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9: 265-273. doi:10.1038/nrc2620.
16. Calbo J, van Montfort E, Proost N, van Drunen E, Beverloo HB, et al. (2011) A functional role for tumor cell heterogeneity in a mouse model of small cell lung cancer. Cancer Cell 19: 244-256. doi:10.1016/j.ccr.2010.12.021.
17. Iwatsuki M, Mimori K, Yokobori T, Ishi H, Beppu T, et al. (2010) Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer Sci 101: 293-299. doi:10.1111/j.1349-7006.2009.01419.x.
18. Tiwari N, Gheldof A, Tatari M, Christofori G (2012) EMT as the ultimate survival mechanism of cancer cells. Semin Cancer Biol 22: 194-207. doi:10.1016/j.semcancer.2012.02.013.
19. Brabletz T (2012) To differentiate or not - routes towards metastasis. Nat Rev Cancer 12: 425-436. doi:10.1038/nrc3265.
20. Khan MZ, Freshney RI, Murray AM, Merry S, Plumb JA, et al. (1991) Identification and characterisation in vitro of cells with a non-SCLC cell-like phenotype derived from a continuous SCLC cell line. Anticancer Res 11: 1687-1695.
21. Hartmann TN, Burger JA, Glodek A, Fujii N, Burger M (2005) CXCR4 chemokine receptor and integrin signaling co-operate in mediating adhesion and chemoresistance in small cell lung cancer (SCLC) cells. Oncogene 24(27):4462-71. (Pubitemid 40961769)
22. Hara J, Miyata H, Yamasaki M, Sugimura K, Takahashi T, et al. (2014) Mesenchymal phenotype after chemotherapy is associated with chemoresistance and poor clinical outcome in esophageal cancer. Oncol Rep 31: 589-596. doi:10.3892/or.2013.2876.
23. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, et al. (2007) Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449: 557-563. doi:10.1038/nature06188. (Pubitemid 47525152)
24. Kalluri R, Weinberg RA (2009) The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428. doi:10.1172/JCI39104.
25. Liu L-K, Jiang X-Y, Zhou X-X, Wang D-M, Song X-L, et al. (2010) Upregulation of vimentin and aberrant expression of E-cadherin/beta-catenin complex in oral squamous cell carcinomas: correlation with the clinicopathological features and patient outcome. Mod Pathol 23: 213-224. doi:10.1038/modpathol.2009.160.
26. Satelli A, Li S (2011) Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell Mol Life Sci 68: 3033-3046. doi:10.1007/s00018-011-0735-1.
27. Gunasinghe NPAD, Wells A, Thompson EW, Hugo HJ (2012) Mesenchymalepithelial transition (MET) as a mechanism for metastatic colonisation in breast cancer. Cancer Metastasis Reviews. Available: http://www.ncbi.nlm.nih.gov/pubmed/22729277. Accessed 2012 Jul 2.
28. Carney DN, Gazdar AF, Bepler G, Guccion JG, Marangos PJ, et al. (1985) Establishment and identification of small cell lung cancer cell lines having classic and variant features. Cancer Res 45: 2913-2923. (Pubitemid 15232769)
29. Kraus AC, Ferber I, Bachmann S-O, Specht H, Wimmel A, et al. (2002) In vitro chemo- and radio-resistance in small cell lung cancer correlates with cell adhesion and constitutive activation of AKT and MAP kinase pathways. Oncogene 21: 8683-8695. doi:10.1038/sj.onc.1205939. (Pubitemid 36132389)
30. Kobayashi S, Okada S, Hasumi T, Sato N, Fujimura S (1999) The significance of NSE and CEA as a differentiation marker for the cellular heterogeneity of small cell lung cancer. Tohoku J Exp Med 189: 37-49.
31. Pirozzi G, Tirino V, Camerlingo R, Franco R, La Rocca A, et al. (2011) Epithelial to Mesenchymal Transition by TGFβ-1 Induction Increases Stemness Characteristics in Primary Non Small Cell Lung Cancer Cell Line. PLoS ONE 6: e21548. doi:10.1371/journal.pone.0021548.
32. Friedl P, Wolf K (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3: 362-374. doi:10.1038/nrc1075. (Pubitemid 37328856)
33. Islam S, Kim JB, Trendel J, Wheelock MJ, Johnson KR (2000) Vimentin expression in human squamous carcinoma cells: relationship with phenotypic changes and cadherin-based cell adhesion. J Cell Biochem 78: 141-150. (Pubitemid 30346390)
34. Radisky DC, LaBarge MA (2008) Epithelial-Mesenchymal Transition and the Stem Cell Phenotype. Cell Stem Cell 2: 511-512. doi:10.1016/j.stem.2008.05.007. (Pubitemid 351729219)
35. Mani SA, Guo W, Liao M-J, Eaton EN, Ayyanan A, et al. (2008) The Epithelial-Mesenchymal Transition Generates Cells with Properties of Stem Cells. Cell 133: 704-715. doi:10.1016/j.cell.2008.03.027. (Pubitemid 351636299)
36. Chhabra ES, Higgs HN (2007) The many faces of actin: matching assembly factors with cellular structures. Nat Cell Biol 9: 1110-1121. doi:10.1038/ncb1007-1110. (Pubitemid 47500485)
37. Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2: 161-174. doi:10.1038/nrc745. (Pubitemid 37328786)
38. Coussens LM, Fingleton B, Matrisian LM (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295: 2387-2392. doi:10.1126/science.1067100. (Pubitemid 34270240)
39. Annes JP, Munger JS, Rifkin DB (2003) Making sense of latent TGFbeta activation. J Cell Sci 116: 217-224. (Pubitemid 36163863)
40. Iniesta P, Moran A, De Juan C, Gomez A, Hernando F, et al. (2007) Biological and clinical significance of MMP-2, MMP-9, TIMP-1 and TIMP-2 in non-small cell lung cancer. Oncol Rep 17: 217-223.
41. Brooks PC, Strömblad S, Sanders LC, von Schalscha TL, Aimes RT, et al. (1996) Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 85: 683-693. (Pubitemid 26181048)
42. Jing J, Lien CF, Sharma S, Rice J, Brennan PA, et al. (2004) Aberrant expression, processing and degradation of dystroglycan in squamous cell carcinomas. Eur J Cancer 40: 2143-2151. doi:10.1016/j.ejca.2004.05.018. (Pubitemid 39165549)
43. Justilien V, Regala RP, Tseng I-C, Walsh MP, Batra J, et al. (2012) Matrix metalloproteinase-10 is required for lung cancer stem cell maintenance, tumor initiation and metastatic potential. PLoS ONE 7: e35040. doi:10.1371/journal.pone.0035040.
44. Mirski SE, Gerlach JH, Cole SP (1987) Multidrug resistance in a human small cell lung cancer cell line selected in adriamycin. Cancer Res 47: 2594-2598. (Pubitemid 17083146)
45. Kraus AC, Ferber I, Bachmann S-O, Specht H, Wimmel A, et al. (2002) In vitro chemo- and radio-resistance in small cell lung cancer correlates with cell adhesion and constitutive activation of AKT and MAP kinase pathways. Oncogene 21: 8683-8695. doi:10.1038/sj.onc.1205939. (Pubitemid 36132389)
46. Sánchez-Tilló E, Liu Y, de Barrios O, Siles L, Fanlo L, et al. (2012) EMT-activating transcription factors in cancer: beyond EMT and tumor invasiveness. Cell Mol Life Sci 69: 3429-3456. doi:10.1007/s00018-012-1122-2.
47. Grady WM, Willis J, Guilford PJ, Dunbier AK, Toro TT, et al. (2000) Methylation of the CDH1 promoter as the second genetic hit in hereditary diffuse gastric cancer. Nat Genet 26: 16-17. doi:10.1038/79120.
48. Graff JR, Herman JG, Lapidus RG, Chopra H, Xu R, et al. (1995) E-cadherin expression is silenced by DNA hypermethylation in human breast and prostate carcinomas. Cancer Res 55: 5195-5199.