Transgelin promotes migration and invasion of cancer stem cells

Journal of Proteome Research

Volumn 9, Issue 10, 2010, Pages 5108-5117

  Lee, Eun Kyung ^a   Han, Gi Yeon ^a   Park, Hye Won ^b   Song, Yeo Ju ^a   Kim, Chan Wha ^a  

^a Korea University   (South Korea)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

2 dimensional electrophoresis; cancer stem cell; invasion; migration; transgelin

Indexed keywords

CD133 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; TRANSGELIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CANCER STEM CELL; CELL MIGRATION; COLORECTAL CARCINOMA; DOWN REGULATION; LIVER CELL CARCINOMA; METASTASIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; SIGNAL TRANSDUCTION; TWO DIMENSIONAL ELECTROPHORESIS;

ANIMALS; ANTIGENS, CD; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL MOVEMENT; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; HUMANS; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICE, INBRED BALB C; MICROFILAMENT PROTEINS; MUSCLE PROTEINS; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; PEPTIDES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TRANSPLANTATION, HETEROLOGOUS;

EID: 77957327502     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100378z     Document Type: Article

References (54)

1. Sawyers, C. Targeted cancer therapy Nature 2004, 432 (7015) 294-7
2. Parkin, D. M.; Bray, F.; Ferlay, J.; Pisani, P. Global cancer statistics, 2002 CA Cancer J. Clin. 2005, 55 (2) 74-108
3. Visvader, J. E.; Lindeman, G. J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions Nat. Rev. Cancer 2008, 8 (10) 755-68
4. Al-Hajj, M.; Wicha, M. S.; Benito-Hernandez, A.; Morrison, S. J.; Clarke, M. F. Prospective identification of tumorigenic breast cancer cells Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (7) 3983-8 (Pubitemid 36418143)
5. Singh, S. K.; Hawkins, C.; Clarke, I. D.; Squire, J. A.; Bayani, J.; Hide, T.; Henkelman, R. M.; Cusimano, M. D.; Dirks, P. B. Identification of human brain tumour initiating cells Nature 2004, 432 (7015) 396-401
6. Collins, A. T.; Berry, P. A.; Hyde, C.; Stower, M. J.; Maitland, N. J. Prospective identification of tumorigenic prostate cancer stem cells Cancer Res. 2005, 65 (23) 10946-51
7. Li, C.; Heidt, D. G.; Dalerba, P.; Burant, C. F.; Zhang, L.; Adsay, V.; Wicha, M.; Clarke, M. F.; Simeone, D. M. Identification of pancreatic cancer stem cells Cancer Res. 2007, 67 (3) 1030-7
8. OBrien, C. A.; Pollett, A.; Gallinger, S.; Dick, J. E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice Nature 2007, 445 (7123) 106-10
9. Ma, S.; Lee, T. K.; Zheng, B. J.; Chan, K. W.; Guan, X. Y. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway Oncogene 2008, 27 (12) 1749-58
10. Hong, S. P.; Wen, J.; Bang, S.; Park, S.; Song, S. Y. CD44-positive cells are responsible for gemcitabine resistance in pancreatic cancer cells Int. J. Cancer 2009, 125 (10) 2323-31
11. Hermann, P. C.; Huber, S. L.; Herrler, T.; Aicher, A.; Ellwart, J. W.; Guba, M.; Bruns, C. J.; Heeschen, C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer Cell Stem Cell 2007, 1 (3) 313-23
12. Yu, S. C.; Bian, X. W. Enrichment of cancer stem cells based on heterogeneity of invasiveness Stem Cell Rev. 2009, 5 (1) 66-71
13. Dean, M.; Fojo, T.; Bates, S. Tumour stem cells and drug resistance Nat. Rev. Cancer 2005, 5 (4) 275-84
14. Miraglia, S.; Godfrey, W.; Yin, A. H.; Atkins, K.; Warnke, R.; Holden, J. T.; Bray, R. A.; Waller, E. K.; Buck, D. W. A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning Blood 1997, 90 (12) 5013-21
15. Kasper, S. Identification, characterization, and biological relevance of prostate cancer stem cells from clinical specimens Urol. Oncol. 2009, 27 (3) 301-3
16. Ma, S.; Chan, K. W.; Hu, L.; Lee, T. K.; Wo, J. Y.; Ng, I. O.; Zheng, B. J.; Guan, X. Y. Identification and characterization of tumorigenic liver cancer stem/progenitor cells Gastroenterology 2007, 132 (7) 2542-56
17. Yin, S.; Li, J.; Hu, C.; Chen, X.; Yao, M.; Yan, M.; Jiang, G.; Ge, C.; Xie, H.; Wan, D.; Yang, S.; Zheng, S.; Gu, J. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity Int. J. Cancer 2007, 120 (7) 1444-50
18. Yu, H.; Konigshoff, M.; Jayachandran, A.; Handley, D.; Seeger, W.; Kaminski, N.; Eickelberg, O. Transgelin is a direct target of TGF-beta/Smad3-dependent epithelial cell migration in lung fibrosis FASEB J. 2008, 22 (6) 1778-89
19. Kim, H. J.; Cho, E. H.; Yoo, J. H.; Kim, P. K.; Shin, J. S.; Kim, M. R.; Kim, C. W. Proteome analysis of serum from type 2 diabetics with nephropathy J. Proteome Res. 2007, 6 (2) 735-43
20. Mayoral, R.; Fernandez-Martinez, A.; Bosca, L.; Martin-Sanz, P. Prostaglandin E2 promotes migration and adhesion in hepatocellular carcinoma cells Carcinogenesis 2005, 26 (4) 753-61
21. Patrawala, L.; Calhoun, T.; Schneider-Broussard, R.; Li, H.; Bhatia, B.; Tang, S.; Reilly, J. G.; Chandra, D.; Zhou, J.; Claypool, K.; Coghlan, L.; Tang, D. G. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells Oncogene 2006, 25 (12) 1696-708
22. Klarmann, G. J.; Hurt, E. M.; Mathews, L. A.; Zhang, X.; Duhagon, M. A.; Mistree, T.; Thomas, S. B.; Farrar, W. L. Invasive prostate cancer cells are tumor initiating cells that have a stem cell-like genomic signature Clin. Exp. Metastasis 2009, 26 (5) 433-46
23. Christiansen, J. J.; Rajasekaran, A. K. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis Cancer Res. 2006, 66 (17) 8319-26
24. Saur, D.; Seidler, B.; Schneider, G.; Algul, H.; Beck, R.; Senekowitsch-Schmidtke, R.; Schwaiger, M.; Schmid, R. M. CXCR4 expression increases liver and lung metastasis in a mouse model of pancreatic cancer Gastroenterology 2005, 129 (4) 1237-50
25. Sheridan, C.; Kishimoto, H.; Fuchs, R. K.; Mehrotra, S.; Bhat-Nakshatri, P.; Turner, C. H.; Goulet, R., Jr.; Badve, S.; Nakshatri, H. CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis Breast Cancer Res. 2006, 8 (5) R59
26. Miller, R. J.; Banisadr, G.; Bhattacharyya, B. J. CXCR4 signaling in the regulation of stem cell migration and development J. Neuroimmunol. 2008, 198 (1-2) 31-8
27. Krohn, A.; Song, Y. H.; Muehlberg, F.; Droll, L.; Beckmann, C.; Alt, E. CXCR4 receptor positive spheroid forming cells are responsible for tumor invasion in vitro Cancer Lett. 2009, 280 (1) 65-71
28. Mani, S. A.; Guo, W.; Liao, M. J.; Eaton, E. N.; Ayyanan, A.; Zhou, A. Y.; Brooks, M.; Reinhard, F.; Zhang, C. C.; Shipitsin, M.; Campbell, L. L.; Polyak, K.; Brisken, C.; Yang, J.; Weinberg, R. A. The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 2008, 133 (4) 704-15
29. Mani, S. A.; Yang, J.; Brooks, M.; Schwaninger, G.; Zhou, A.; Miura, N.; Kutok, J. L.; Hartwell, K.; Richardson, A. L.; Weinberg, R. A. Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (24) 10069-74
30. Lin, Y.; Buckhaults, P. J.; Lee, J. R.; Xiong, H.; Farrell, C.; Podolsky, R. H.; Schade, R. R.; Dynan, W. S. Association of the actin-binding protein transgelin with lymph node metastasis in human colorectal cancer Neoplasia 2009, 11 (9) 864-73
31. Yang, J.; Mani, S. A.; Donaher, J. L.; Ramaswamy, S.; Itzykson, R. A.; Come, C.; Savagner, P.; Gitelman, I.; Richardson, A.; Weinberg, R. A. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis Cell 2004, 117 (7) 927-39
32. Pozharskaya, V.; Torres-Gonzalez, E.; Rojas, M.; Gal, A.; Amin, M.; Dollard, S.; Roman, J.; Stecenko, A. A.; Mora, A. L. Twist: a regulator of epithelial-mesenchymal transition in lung fibrosis PLoS One 2009, 4 (10 e7559
33. Matsuo, N.; Shiraha, H.; Fujikawa, T.; Takaoka, N.; Ueda, N.; Tanaka, S.; Nishina, S.; Nakanishi, Y.; Uemura, M.; Takaki, A.; Nakamura, S.; Kobayashi, Y.; Nouso, K.; Yagi, T.; Yamamoto, K. Twist expression promotes migration and invasion in hepatocellular carcinoma BMC Cancer 2009, 9, 240
34. Lawson, D.; Harrison, M.; Shapland, C. Fibroblast transgelin and smooth muscle SM22alpha are the same protein, the expression of which is down-regulated in many cell lines Cell Motil. Cytoskeleton 1997, 38 (3) 250-7
35. Shapland, C.; Hsuan, J. J.; Totty, N. F.; Lawson, D. Purification and properties of transgelin: a transformation and shape change sensitive actin-gelling protein J. Cell Biol. 1993, 121 (5) 1065-73
36. Harkness, L.; Christiansen, H.; Nehlin, J.; Barington, T.; Andersen, J. S.; Kassem, M. Identification of a membrane proteomic signature for human embryonic stem cells independent of culture conditions Stem Cell Res. 2008, 1 (3) 219-27
37. Vartiainen, M. K.; Guettler, S.; Larijani, B.; Treisman, R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL Science 2007, 316 (5832) 1749-52
38. Hofmann, W. A.; Stojiljkovic, L.; Fuchsova, B.; Vargas, G. M.; Mavrommatis, E.; Philimonenko, V.; Kysela, K.; Goodrich, J. A.; Lessard, J. L.; Hope, T. J.; Hozak, P.; de Lanerolle, P. Actin is part of pre-initiation complexes and is necessary for transcription by RNA polymerase II Nat. Cell Biol. 2004, 6 (11) 1094-101 (Pubitemid 39468010)
39. Qi, Y.; Chiu, J. F.; Wang, L.; Kwong, D. L.; He, Q. Y. Comparative proteomic analysis of esophageal squamous cell carcinoma Proteomics 2005, 5 (11) 2960-71
40. Shi, Y. Y.; Wang, H. C.; Yin, Y. H.; Sun, W. S.; Li, Y.; Zhang, C. Q.; Wang, Y.; Wang, S.; Chen, W. F. Identification and analysis of tumour-associated antigens in hepatocellular carcinoma Br. J. Cancer 2005, 92 (5) 929-34
41. Li, N.; Zhang, J.; Liang, Y.; Shao, J.; Peng, F.; Sun, M.; Xu, N.; Li, X.; Wang, R.; Liu, S.; Lu, Y. A controversial tumor marker: is SM22 a proper biomarker for gastric cancer cells J. Proteome Res. 2007, 6 (8) 3304-12
42. Huang, Q.; Chen, W.; Wang, L.; Lin, W.; Lin, J.; Lin, X. Identification of transgelin as a potential novel biomarker for gastric adenocarcinoma based on proteomics technology J. Cancer Res. Clin. Oncol. 2008, 134 (11) 1219-27
43. Mikuriya, K.; Kuramitsu, Y.; Ryozawa, S.; Fujimoto, M.; Mori, S.; Oka, M.; Hamano, K.; Okita, K.; Sakaida, I.; Nakamura, K. Expression of glycolytic enzymes is increased in pancreatic cancerous tissues as evidenced by proteomic profiling by two-dimensional electrophoresis and liquid chromatography-mass spectrometry/mass spectrometry Int. J. Oncol. 2007, 30 (4) 849-55
44. Shields, J. M.; Rogers-Graham, K.; Der, C. J. Loss of transgelin in breast and colon tumors and in RIE-1 cells by Ras deregulation of gene expression through Raf-independent pathways J. Biol. Chem. 2002, 277 (12) 9790-9
45. Yang, Z.; Chang, Y. J.; Miyamoto, H.; Ni, J.; Niu, Y.; Chen, Z.; Chen, Y. L.; Yao, J. L.; di SantAgnese, P. A.; Chang, C. Transgelin functions as a suppressor via inhibition of ARA54-enhanced androgen receptor transactivation and prostate cancer cell growth Mol. Endocrinol. 2007, 21 (2) 343-58
46. Nair, R. R.; Solway, J.; Boyd, D. D. Expression cloning identifies transgelin (SM22) as a novel repressor of 92-kDa type IV collagenase (MMP-9) expression J. Biol. Chem. 2006, 281 (36) 26424-36
47. Zhang, Y.; Ye, Y.; Shen, D.; Jiang, K.; Zhang, H.; Sun, W.; Zhang, J.; Xu, F.; Cui, Z.; Wang, S. Identification of transgelin-2 as a biomarker of colorectal cancer by laser capture microdissection and quantitative proteome analysis Cancer Sci. 2010, 101 (2) 523-9
48. Becker, C.; Fantini, M. C.; Schramm, C.; Lehr, H. A.; Wirtz, S.; Nikolaev, A.; Burg, J.; Strand, S.; Kiesslich, R.; Huber, S.; Ito, H.; Nishimoto, N.; Yoshizaki, K.; Kishimoto, T.; Galle, P. R.; Blessing, M.; Rose-John, S.; Neurath, M. F. TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling Immunity 2004, 21 (4) 491-501
49. Qiu, P.; Ritchie, R. P.; Gong, X. Q.; Hamamori, Y.; Li, L. Dynamic changes in chromatin acetylation and the expression of histone acetyltransferases and histone deacetylases regulate the SM22alpha transcription in response to Smad3-mediated TGFbeta1 signaling Biochem. Biophys. Res. Commun. 2006, 348 (2) 351-8
50. Qiu, P.; Feng, X. H.; Li, L. Interaction of Smad3 and SRF-associated complex mediates TGF-beta1 signals to regulate SM22 transcription during myofibroblast differentiation J. Mol. Cell. Cardiol. 2003, 35 (12) 1407-20
51. Ullah, Z.; Buckley, M. S.; Arnosti, D. N.; Henry, R. W. Retinoblastoma protein regulation by the COP9 signalosome Mol. Biol. Cell 2007, 18 (4) 1179-86
52. Richardson, K. S.; Zundel, W. The emerging role of the COP9 signalosome in cancer Mol. Cancer Res. 2005, 3 (12) 645-53
53. Hwang-Verslues, W. W.; Chang, K. J.; Lee, E. Y.; Lee, W. H. Breast cancer stem cells and tumor suppressor genes J. Formosan Med. Assoc. 2008, 107 (10) 751-66
54. Bosco, E. E.; Wang, Y.; Xu, H.; Zilfou, J. T.; Knudsen, K. E.; Aronow, B. J.; Lowe, S. W.; Knudsen, E. S. The retinoblastoma tumor suppressor modifies the therapeutic response of breast cancer J. Clin. Invest. 2007, 117 (1) 218-28