Variable Metastatic Potentials Correlate with Differential Plectin and Vimentin Expression in Syngeneic Androgen Independent Prostate Cancer Cells

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Burch, Tanya C ^a   Watson, Megan T ^a   Nyalwidhe, Julius O ^a  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 1; EPHRIN A2; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PLECTIN; SMALL INTERFERING RNA; VIMENTIN;

ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METASTASIS POTENTIAL; PROSTATE ADENOCARCINOMA; PROSTATE CANCER; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; SIGNAL TRANSDUCTION; UPREGULATION;

ANDROGENS; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMATOGRAPHY, LIQUID; GENE SILENCING; HUMANS; MALE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PLECTIN; PROSTATIC NEOPLASMS; PROTEOMICS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; VIMENTIN;

EID: 84878030464     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065005     Document Type: Article

References (89)

1. Siegel R, Naishadham D, Jemal A, (2012) Cancer Statistics. CA Cancer J Clin 62: 10-29.
2. LaSpina M, Haas GP, (2008) Update on the diagnosis and management of prostate cancer. Can J Urol 15: 3-13.
3. Zhu X, van Leeuwen PJ, Bul M, Bangma CH, Roobol MJ, et al. (2011) Identifying and characterizing "escapes"- men who develop metastases or die from prostate cancer despite screening (ERSPC, section Rotterdam). Int J Cancer 129: 2847-2854.
4. Bubendorf L, Schopfer A, Wagner U, Sauter G, Moch H, (2000) Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol 31: 578-583.
5. Stamey TA, Yang N, Hay AR, McNeal JE, Freiha FS, et al. (1987) Prostate specific antigen as a serum marker for adenocarcinoma of the prostate. N Engl J Med 317: 909-916.
6. Bunting PS, (2002) Screening for prostate cancer with prostate-specific antigen: beware the biases. Clin Chim Acta 315: 71-97.
7. Tricoli JV, Schoenfeldt M, Conley BA, (2004) Detection of prostate cancer and predicting progression: current and future diagnostic markers. Clin Cancer Res 10: 3943-3953.
8. van Gils MP, Stenman UH, Schalken JA, Schroder FH, Luider TM, et al. (2005) Innovations in serum and urine markers in prostate cancer current European research in the P-Mark project. Eur Urol 48: 1031-1041.
9. Thompson IM, Ankerst DP, Chi C, Goodman PJ, Tangen CM, et al. (2006) Assessing prostate cancer risk: results from the prostate cancer prevention trial. Cancer 78229: 529-534.
10. Lilja H, Ulmert D, Vickers AJ, (2008) Prostate-specific antigen and prostate cancer: prediction, detection and monitoring. Nat Rev Cancer 8: 268-278.
11. Moyer VA (2012) On behalf of the U.S. Preventive Services Task Force. Screening for Prostate Cancer: U.S. Preventive Services Task Force Recommendation Statement. Ann Intern Med May 21.
12. Srinivas PR, Verma M, Zhao Y, Srivastava S, (2002) Proteomics for cancer biomarker discovery. Clin Chem 48: 1160-9.
13. Beck F, Burkhart JM, Geiger J, Zahedi RP, Sickmann A, (2012) Robust workflow for iTRAQ-based peptide and protein quantification. Methods Mol Biol 893: 101-13.
14. Vaudel M, Burkhart JM, Zahedi RP, Martens L, Sickmann A, (2012) iTRAQ data interpretation. Methods Mol Biol 893: 501-9.
15. Wang M, Stearns ME, (1991) Isolation and characterization of PC-3 human prostatic tumor sublines which preferentially metastasize to select organs in S.C.I.D. mice. Differentiation 48: 115-125.
16. Dolloff NG, Shulby SS, Nelson AV, Stearns ME, Johannes GJ, (2005) Bone-metastatic potential of human prostate cancer cells correlates with Akt/PKB activation by alpha platelet-derived growth factor receptor. Oncogene 24: 6848-54.
17. Dolloff NG, Russell MR, Loizos N, Fatatis A, (2007) Human bone marrow activates the Akt pathway in metastatic prostate cells through transactivation of the alpha-platelet-derived growth factor receptor. Cancer Res. 67: 555-62.
18. Shilov IV, Seymour SL, Patel AA, Loboda A, Tang WH, (2007) The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteomics 6: 1638-55.
19. Tang WH, Shilov IV, Seymour SL, (2008) Nonlinear fitting method for determining local false discovery rates from decoy database searches. J Proteome Res. 7: 3661-7.
20. Pontén F, Jirström K, Uhlen M, (2008) The Human Protein Atlas-a tool for pathology. J Pathol. 16: 387-93.
21. Uhlén M, Björling E, Agaton C, Szigyarto CA, Amini B, et al. (2005) A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol Cell Proteomics. 4: 1920-32.
22. Karashima T, Tsuruta D, Hamada T, Ishii N, Ono F, et al. (2012) Interaction of plectin and intermediate filaments. J Dermatol Sci. 66: 44-50.
23. McInroy L, Määttä A, (2011) Plectin regulates invasiveness of SW480 colon carcinoma cells and is targeted to podosome-like adhesions in an isoform-specific manner. Exp Cell Res. 317: 2468-78.
24. Bausch D, Thomas S, Mino-Kenudson M, Fernández-del CC, Bauer TW, et al. (2011) Plectin-1 as a novel biomarker for pancreatic cancer. Clin Cancer Res. 17: 302-9.
25. Bausch D, Mino-Kenudson M, Fernández-Del C, Warshaw AL, Kelly KA, et al. (2009) J Gastrointest Surg. 13: 1948-54.
26. Katada K, Tomonaga T, Satoh M, Matsushita K, Tonoike Y, (2012) Plectin promotes migration and invasion of cancer cells and is a novel prognostic marker for head and neck squamous cell carcinoma. J Proteomics 75: 1803-15.
27. Eriksson JE, Dechat T, Grin B, Helfand B, Mendez M, et al. (2009) Introducing intermediate filaments: from discovery to disease. J Clin Invest. 119: 1763-71.
28. Guarino M, Rubino B, Ballabio G, (2007) The role of epithelial-mesenchymal transition in cancer pathology. Pathology 39: 305-318.
29. Wells A, Yates C, Shepard CR, (2008) E-cadherin as an indicator of mesenchymal to epithelial reverting transitions during the metastatic seeding of disseminated carcinomas. Clin Exp Metastasis 25: 621-628.
30. Janda E, Lehmann K, Killisch I, Jechlinger M, Herzig M, et al. (2002) Ras and TGF beta cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 156: 299-313.
31. Huang C, Jacobson K, Schaller MD, (2004) MAP kinases and cell migration. J Cell Sci 117: 4619-28.
32. Chakraborti S, Mandal M, Das S, Mandal A, Chakraborti T, (2003) Regulation of matrix metalloproteinases: an overview. Mol Cell Biochem 253: 269-85.
33. Osmanagic-Myers S, Gregor M, Walko G, Burgstaller G, Reipert S, et al. (2006) Plectin-controlled keratin cytoarchitecture affects MAP kinases involved in cellular stress response and migration. J Cell Biol. 174: 557-68.
34. Ding Y, Zhang L, Goodwin JS, Wang Z, Liu B, et al. (2008) Plectin regulates the signaling and trafficking of the HIV-1 co-receptor CXCR4 and plays a role in HIV-1 infection. Exp Cell Res 314: 590-602.
35. Malecz N, Foisner R, Stadler C, Wiche G, (1996) Identification of plectin as a substrate of p34cdc2 kinase and mapping of a single phosphorylation site. J Biol Chem 271: 8203-8.
36. Yang L, Nyalwidhe JO, Guo S, Drake RR, Semmes OJ, (2011) Targeted identification of metastasis-associated cell-surface sialoglycoproteins in prostate cancer. Mol Cell Proteomics. 10(6): M110.007294.
37. Rezniczek GA, de Pereda JM, Reipert S, Wiche G, (1998) Linking integrin alpha6beta4-based cell adhesion to the intermediate filament cytoskeleton: direct interaction between the beta4 subunit and plectin at multiple molecular sites. J Cell Biol 141: 209-225.
38. Humphries MJ, (2000) Integrin structure. Biochem Soc Trans 28: 311-339.
39. Chao C, Lotz MM, Clarke AC, Mercurio AM, (1996) A function for the integrin alpha6beta4 in the invasive properties of colorectal carcinoma cells. Cancer Res 56: 4811-4819.
40. Lu S, Simin K, Khan A, Mercurio AM, (2008) Analysis of integrin beta4 expression in human breast cancer: association with basal-like tumors and prognostic significance. Clin Cancer Res14: 1050-1058.
41. Franke WW, Grund C, Kuhn C, Jackson BW, Illmensee K, (1982) Formation of cytoskeletal elements during mouse embryogenesis. III. Primary mesenchymal cells and the first appearance of vimentin filaments. Differentiation 23: 43-59.
42. 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.
43. Vuoriluoto K, Haugen H, Kiviluoto S, Mpindi JP, Nevo J, et al. (2011) Vimentin regulates EMT induction by Slug and oncogenic H-Ras and migration by governing Axl expression in breast cancer. Oncogene 30: 1436-1448.
44. Mendez MG, Kojima S, Goldman RD, (2010) Vimentin induces changes in cell shape, motility, and adhesion during the epithelial to mesenchymal transition. FASEB J 24: 1838-1851.
45. Dutsch-Wicherek M, Lazar A, Tomaszewska R, (2010) The potential role of MT and vimentin immunoreactivity in the remodeling of the microenvironment of parotid adenocarcinoma. Cancer Microenviron 4: 105-113.
46. Glen A, Evans CA, Gan CS, Cross SS, Hamdy FC, (2010) Eight-plex iTRAQ analysis of variant metastatic human prostate cancer cells identifies candidate biomarkers of progression: An exploratory study. Prostate 70: 1313-1332.
47. Renz M, Betz B, Niederacher D, Bender HG, Langowski J, (2008) Invasive breast cancer cells exhibit increased mobility of the actin-binding protein CapG. Int J Cancer 122: 1476-1482.
48. Onoda K, Yu FX, Yin HL, (1993) gCap39 is a nuclear and cytoplasmic protein. Cell Motil Cytoskeleton 26: 227-238.
49. Pollard TD, Borisy GG, (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell. 112: 453-465.
50. Dahl E, Sadr-Nabavi A, Klopocki E, Betz B, et al. (2005) Systematic identification and molecular characterization of genes differentially expressed in breast and ovarian cancer. J Pathol 205: 21-28.
51. Thompson CC, Ashcroft FJ, Patel S, Saraga G, Vimalachandran D, (2007) Pancreatic cancer cells overexpress gelsolin family-capping proteins, which contribute to their cell motility. Gut 56: 95-106.
52. Lal A, Lash AE, Altschul SF, Velculescu V, Zhang L, et al. (1999) A public database for gene expression in human cancers. Cancer Res 59: 5403-5407.
53. Van Ginkel PR, Gee RL, Walker TM, Hu DN, Heizmann CW, et al. (1998) The identification and differential expression of calcium-binding proteins associated with ocular melanoma. Biochim Biophys Acta 1448: 290-297.
54. Li M, Li S, Lou Z, Liao X, Zhao X, et al. (2008) Crystal structure of human transgelin. J Struct Biol 162: 229-236.
55. Yang Z, Chang YJ, Miyamoto H, Ni J, Niu Y, et al. (2007) Transgelin functions as a suppressor via inhibition of ARA54-enhanced androgen receptor transactivation and prostate cancer cell growth. Mol Endocrinol 21: 343-358.
56. Nair RR, Solway J, Boyd DD, (2006) Expression cloning identifies transgelin (SM22) as a novel repressor of 92-kDa type IV collagenase (MMP-9) expression. J Biol Chem 281: 26424-26436.
57. Nishio S, Ushijima K, Tsuda N, Takemoto S, Kawano K, et al. (2008) Cap43/NDRG1/Drg-1 is a molecular target for angiogenesis and a prognostic indicator in cervical adenocarcinoma. Cancer Lett 264: 36-43.
58. Lachat P, Shaw P, Gebhard S, van Belzen N, Chaubert P, et al. (2002) Expression of NDRG1, a differentiation-related gene, in human tissues. Histochem Cell Biol 118: 399-408.
59. Ellen TP, Ke Q, Zhang P, Costa M, (2008) NDRG1, a growth and cancer related gene: regulation of gene expression and function in normal and disease states. Carcinogenesis 29: 2-8.
60. Cangul H, (2004) Hypoxia upregulates the expression of the NDRG1 gene leading to its overexpression in various human cancers. BMC Genet 5: 27.
61. Cangul H, Salnikow K, Yee H, Zagzag D, Commes T, et al. (2002) Enhanced overexpression of an HIF-1/hypoxia-related protein in cancer cells. Environ Health Perspect 110: 783-788.
62. Hengstschläger M, Pfeilstöcker M, Wawra E, (1998) Thymidine kinase expression-a marker for malignant cells. Adv Exp Med Biol 431: 455-460.
63. Mikulits W, Hengstschläger M, Sauer TE, Wintersberger E, Müllner EW, (1996) Overexpression of thymidine kinase mRNA eliminates cell cycle regulation of thymidine kinase enzyme activity. J Biol Chem 271: 853-860.
64. Loilome W, Wechagama P, Namwat N, Jusakul A, Sripa B, et al. (2012) Expression of oxysterol binding protein isoforms in opisthorchiasis-associated cholangiocarcinoma: a potential molecular marker for tumor metastasis. Parasitol Int 61: 136-139.
65. Wehder L, Arndt S, Murzik U, Bosserhoff AK, Kob R, et al. (2009) Annexin A5 is involved in migration and invasion of oral carcinoma. Cell Cycle 8: 1552-1558.
66. Lee EK, Cho H, Kim CW, (2011) Proteomic analysis of cancer stem cells in human prostate cancer cells. Biochem Biophys Res Commun 412: 279-285.
67. Santarius T, Bignell GR, Greenman CD, Widaa S, Chen L, et al. (2010) GLO1-A novel amplified gene in human cancer. Genes Chromosomes Cancer 49: 711-725.
68. Sakamoto H, Mashima T, Sato S, Hashimoto Y, Yamori T, et al. (2001) Selective activation of apoptosis program by S-p-bromobenzylglutathione cyclopentyl diester in glyoxalase I-overexpressing human lung cancer cells. Clin Cancer Res 7: 2513-2518.
69. Chen B, Chen J, House MG, Cullen KJ, Nephew KP, et al. (2012) Role of neurofilament light polypeptide in head and neck cancer chemoresistance. Mol Cancer Res 10: 305-315.
70. Koochekpour S, Hu S, Vellasco-Gonzalez C, Bernardo R, Azabdaftari G, et al. (2012) Serum prosaposin levels are increased in patients with advanced prostate cancer. Prostate 72: 253-269.
71. Hu S, Delorme N, Liu Z, Liu T, Velasco-Gonzalez C, et al. (2010) Prosaposin down-modulation decreases metastatic prostate cancer cell adhesion, migration, and invasion. Mol Cancer 9: 30.
72. Kang SY, Halvorsen OJ, Gravdal K, Bhattacharya N, Lee JM, et al. (2009) Prosaposin inhibits tumor metastasis via paracrine and endocrine stimulation of stromal p53 and Tsp-1. Proc Natl Acad Sci USA. 106: 12115-12120.
73. Meng MV, Grossfeld GD, Williams GH, Dilworth S, Stoeber K, et al. (2001) Minichromosome maintenance protein 2 expression in prostate: characterization and association with outcome after therapy for cancer. Clin Cancer Res 7: 2712-2718.
74. Dudderidge TJ, Kelly JD, Wollenschlaeger A, Okoturo O, Prevost T, et al. (2010) Diagnosis of prostate cancer by detection of minichromosome maintenance 5 protein in urine sediments. Br J Cancer 103: 701-7.
75. Almgren MA, Henriksson KC, Fujimoto J, Chang CL, (2004) Nucleoside diphosphate kinase A/nm23-H1 promotes metastasis of NB69-derived human neuroblastoma. Mol Cancer Res 2: 387-94.
76. Bartholow TL, Chandran UR, Becich MJ, Parwani AV, (2011) Immunohistochemical staining of radixin and moesin in prostatic adenocarcinoma. BMC Clin Pathol. 11: 1.
77. Carpenter B, Hill KJ, Charalambous M, Wagner KJ, Lahiri D, et al. (2004) BASP1 is a transcriptional cosuppressor for the Wilms' tumor suppressor protein WT1. Mol Cell Biol 24: 537-49.
78. Lee JW, Choi HS, Gyuris J, Brent R, Moore DD, (1995) Two classes of proteins dependent on either the presence or absence of thyroid hormone for interaction with the thyroid hormone receptor. Mol Endocrinol 9: 243.
79. Kang JU, Koo SH, Kwon KC, Park JW, Kim JM, (2008) Gain at chromosomal region 5p15. 33, containing TERT, is the most frequent genetic event in early stages of non-small cell lung cancer. Cancer Genet Cytogenet 182: 1-11.
80. Shaughnessy JD, Zhan F, Burington BE, Huang Y, Colla S, et al. (2007) A validated gene expression model of high-risk multiple myeloma is defined by deregulated expression of genes mapping to chromosome 1. Blood 109: 2276.
81. Lokman NA, Ween MP, Oehler MK, Ricciardelli C, (2011) The role of annexin A2 in tumorigenesis and cancer progression. Cancer Microenviron 4: 199-208.
82. Fang WB, Brantley-Sieders DM, Parker MA, Reith AD, Chen J, (2005) A kinase-dependent role for EphA2 receptor in promoting tumor growth and metastasis. Oncogene 24: 7859-7868.
83. Zelinski DP, Zantek ND, Stewart JC, Irizarry AR, Kinch MS, (2001) EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res 61: 2301-2306.
84. Miao H, Burnett E, Kinch M, Simon E, Wang B, (2000) Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nat. Cell Biol 2: 62-69.
85. Miao H, Wei BR, Peehl DM, Li Q, Alexandrou T, Schelling JR, et al. (2001) Activation of EphA receptor tyrosine kinase inhibits the Ras/MAPK pathway. Nat. Cell Biol 3: 527-530.
86. Miao H, Nickel CH, Cantley LG, Bruggeman LA, Bennardo LN, Wang B, (2003) EphA kinase activation regulates HGF-induced epithelial branching morphogenesis. J. Cell Biol 162: 1281-1292.
87. Dohn M, Jiang J, Chen X, (2001) Receptor tyrosine kinase EphA2 is regulated by p53-family proteins and induces apoptosis. Oncogene 20: 6503-6515.
88. Zhang G, Njauw CN, Park JM, Naruse C, Asano M, et al. (2008) EphA2 is an essential mediator of UV radiation-induced apoptosis. Cancer Res. 68: 1691-1696.
89. Guo H, Miao H, Gerber L, Singh J, Denning MF, et al. (2006) Disruption of EphA2 receptor tyrosine kinase leads to increased susceptibility to carcinogenesis in mouse skin. Cancer Res 66: 7050-7058.