Matrix metalloproteinase-10 is required for lung cancer stem cell maintenance, tumor initiation and metastatic potential

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Justilien, Verline ^a   Regala, Roderick P ^a   Tseng, I Chu ^a   Walsh, Michael P ^a   Batra, Jyotica ^a   Radisky, Evette S ^a   Murray, Nicole R ^a   Fields, Alan P ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

STROMELYSIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CARCINOGENICITY; CELL CULTURE; CELL GROWTH; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE SILENCING; IN VITRO STUDY; LUNG CANCER; LUNG CARCINOGENESIS; METASTASIS POTENTIAL; MMP10 GENE; MOUSE; NONHUMAN; ONCOSPHERE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; STEM CELL EXPANSION; TUMOR GROWTH; ANIMAL; C57BL MOUSE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LUNG; LUNG TUMOR; METABOLISM; METASTASIS; PATHOLOGY; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

ANIMALS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 10; MICE; MICE, INBRED C57BL; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; TUMOR MICROENVIRONMENT;

EID: 84860116336     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035040     Document Type: Article

References (44)

1. Jemal A, Siegel R, Xu J, Ward E, (2010) Cancer statistics, 2010. CA Cancer J Clin 60: 277-300.
2. Reya T, Morrison SJ, Clarke MF, Weissman IL, (2001) Stem cells, cancer, and cancer stem cells. Nature 414: 105-111.
3. Al-Hajj M, Clarke MF, (2004) Self-renewal and solid tumor stem cells. Oncogene 23: 7274-7282.
4. Jordan CT, Guzman ML, Noble M, (2006) Cancer Stem Cells. N Engl J Med 355: 1253-1261.
5. Wang JCY, Dick JE, (2005) Cancer stem cells: lessons from leukemia. Trends in Cell Biology 15: 494-501.
6. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CHM, et al. (2006) Cancer Stem Cells-Perspectives on Current Status and Future Directions: AACR Workshop on Cancer Stem Cells. Cancer Research 66: 9339-9344.
7. 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.
8. Katoh Y, Katoh M, (2007) Comparative genomics on PROM1 gene encoding stem cell marker CD133. Int J Mol Med 19: 967-970.
9. Tirino V, Camerlingo R, Franco R, Malanga D, La Rocca A, et al. (2009) The role of CD133 in the identification and characterisation of tumour-initiating cells in non-small-cell lung cancer. European Journal of Cardio-Thoracic Surgery 36: 446-453.
10. Chiou SH, Wang ML, Chou YT, Chen CJ, Hong CF, et al. (2010) Coexpression of Oct4 and Nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell-like properties and epithelial-mesenchymal transdifferentiation. Cancer Res 70: 10433-10444.
11. Yuan P, Kadara H, Behrens C, Tang X, Woods D, et al. (2010) Sex determining region Y-Box 2 (SOX2) is a potential cell-lineage gene highly expressed in the pathogenesis of squamous cell carcinomas of the lung. PLoS One 5: e9112.
12. Katoh M, (2007) Integrative genomic analyses on HES/HEY family: Notch-independent HES1, HES3 transcription in undifferentiated ES cells, and Notch-dependent HES1, HES5, HEY1, HEY2, HEYL transcription in fetal tissues, adult tissues, or cancer. Int J Oncol 31: 461-466.
13. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, et al. (2008) Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 15: 504-514.
14. Egeblad M, Werb Z, (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2: 161-174.
15. Bodey B, Bodey B Jr, Groger AM, Siegel SE, Kaiser HE, (2001) Invasion and metastasis: the expression and significance of matrix metalloproteinases in carcinomas of the lung. In Vivo 15: 175-180.
16. Delebecq TJ, Porte H, Zerimech F, Copin MC, Gouyer V, et al. (2000) Overexpression level of stromelysin 3 is related to the lymph node involvement in non-small cell lung cancer. Clin Cancer Res 6: 1086-1092.
17. Gill JH, Kirwan IG, Seargent JM, Martin SW, Tijani S, et al. (2004) MMP-10 is overexpressed, proteolytically active, and a potential target for therapeutic intervention in human lung carcinomas. Neoplasia 6: 777-785.
18. Kren L, Goncharuk VN, Krenova Z, Stratil D, Hermanova M, et al. (2006) Expression of matrix metalloproteinases 3, 10 and 11 (stromelysins 1, 2 and 3) and matrix metalloproteinase 7 (matrilysin) by cancer cells in non-small cell lung neoplasms. Clinicopathologic studies. Cesk Patol 42: 16-19.
19. Frederick LA, Matthews JA, Jamieson L, Justilien V, Thompson EA, et al. (2008) Matrix metalloproteinase-10 is a critical effector of protein kinase Cι-Par6α-mediated lung cancer. Oncogene 27: 4841-4853.
20. Regala RP, Davis RK, Kunz A, Khoor A, Leitges M, et al. (2009) Atypical protein kinase Cι is required for bronchioalveolar stem cell expansion and lung tumorigenesis. Cancer Research 69: 7603-7611.
21. Regala R, Justilien V, Walsh MP, Weems C, Khoor A, et al. (2011) Matrix Metalloproteinase-10 Promotes Kras-Mediated Bronchio-Alveolar Stem Cell Expansion and Lung Cancer Formation. PLoS ONE 6: e26439.
22. Franks LM, Carbonell AW, Hemmings VJ, Riddle PN, (1976) Metastasizing tumors from serum-supplemented and serum-free cell lines from a C57BL mouse lung tumor. Cancer Res 36: 1049-1055.
23. Layton MG, Franks LM, (1984) Heterogeneity in a spontaneous mouse lung carcinoma: selection and characterisation of stable metastatic variants. Br J Cancer 49: 415-421.
24. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, et al. (2008) An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 40: 499-507.
25. 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.
26. Ho MM, Ng AV, Lam S, Hung JY, (2007) Side Population in Human Lung Cancer Cell Lines and Tumors Is Enriched with Stem-like Cancer Cells. Cancer Research 67: 4827-4833.
27. Jiang T, Collins BJ, Jin N, Watkins DN, Brock MV, et al. (2009) Achaete-scute complex homologue 1 regulates tumor-initiating capacity in human small cell lung cancer. Cancer Res 69: 845-854.
28. Bradfute SB, Graubert TA, Goodell MA, (2005) Roles of Sca-1 in hematopoietic stem/progenitor cell function. Exp Hematol 33: 836-843.
29. Fan X, Khaki L, Zhu TS, Soules ME, Talsma CE, et al. (2010) NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 28: 5-16.
30. Baty F, Facompre M, Kaiser S, Schumacher M, Pless M, et al. (2010) Gene profiling of clinical routine biopsies and prediction of survival in non-small cell lung cancer. Am J Respir Crit Care Med 181: 181-188.
31. Solar P, Sytkowski AJ, (2011) Differentially expressed genes associated with cisplatin resistance in human ovarian adenocarcinoma cell line A2780. Cancer Lett 309: 11-18.
32. Weiser-Evans MC, Wang XQ, Amin J, Van Putten V, Choudhary R, et al. (2009) Depletion of cytosolic phospholipase A2 in bone marrow-derived macrophages protects against lung cancer progression and metastasis. Cancer Res 69: 1733-1738.
33. Suzuki K, Kan CC, Hung W, Gehring MR, Brew K, et al. (1998) Expression of human pro-matrix metalloproteinase 3 that lacks the N-terminal 34 residues in Escherichia coli: autoactivation and interaction with tissue inhibitor of metalloproteinase 1 (TIMP-1). Biol Chem 379: 185-191.
34. Batra J, Robinson J, Soares AS, Fields AP, Radisky DC, et al. (2012) Matrix metalloproteinase-10 (MMP-10) interaction with tissue inhibitors of metalloproteinases TIMP-1 and TIMP-2: binding studies and crystal structure. Journal of Biological Chemistry Submitted.
35. Regala RP, Weems C, Jamieson L, Copland JA, Thompson EA, et al. (2005) Atypical protein kinase Ciota plays a critical role in human lung cancer cell growth and tumorigenicity. J Biol Chem 280: 31109-31115.
36. Regala RP, Weems C, Jamieson L, Khoor A, Edell ES, et al. (2005) Atypical protein kinase C iota is an oncogene in human non-small cell lung cancer. Cancer Res 65: 8905-8911.
37. Rice WR, Conkright JJ, Na CL, Ikegami M, Shannon JM, et al. (2002) Maintenance of the mouse type II cell phenotype in vitro. Am J Physiol Lung Cell Mol Physiol 283: L256-264.
38. Kupershmidt I, Su QJ, Grewal A, Sundaresh S, Halperin I, et al. (2010) Ontology-based meta-analysis of global collections of high-throughput public data. PLoS One 5.
39. Matsuyama T, Ishikawa T, Mogushi K, Yoshida T, Iida S, et al. (2010) MUC12 mRNA expression is an independent marker of prognosis in stage II and stage III colorectal cancer. International Journal of Cancer 127: 2292-2299.
40. Jonsson G, Busch C, Knappskog S, Geisler J, Miletic H, et al. (2010) Gene expression profiling-based identification of molecular subtypes in stage IV melanomas with different clinical outcome. Clinical Cancer Research 16: 3356-3367.
41. Bos PD, Zhang XH, Nadal C, Shu W, Gomis RR, et al. (2009) Genes that mediate breast cancer metastasis to the brain. Nature 459: 1005-1009.
42. Tan X, Zhai Y, Chang W, Hou J, He S, et al. (2008) Global analysis of metastasis-associated gene expression in primary cultures from clinical specimens of clear-cell renal-cell carcinoma. International Journal of Cancer 123: 1080-1088.
43. Lin AY, Chua MS, Choi YL, Yeh W, Kim YH, et al. (2011) Comparative profiling of primary colorectal carcinomas and liver metastases identifies LEF1 as a prognostic biomarker. PLoS One 6: e16636.
44. Chandran UR, Ma C, Dhir R, Bisceglia M, Lyons-Weiler M, et al. (2007) Gene expression profiles of prostate cancer reveal involvement of multiple molecular pathways in the metastatic process. BMC Cancer 7: 64.