P-glycoprotein associates with Anxa2 and promotes invasion in multidrug resistant breast cancer cells

Biochemical Pharmacology

Volumn 87, Issue 2, 2014, Pages 292-302

  Zhang, Fei ^a   Zhang, Haichang ^a,b   Wang, Zhiyong ^a   Yu, Man ^c   Tian, Ran ^a   Ji, Wei ^a   Yang, Yi ^a   Niu, Ruifang ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b TIANJIN FIRST CENTRAL HOSPITAL   (China)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Anxa2; Breast cancer; Invasion; MDR; P glycoprotein; Src

Indexed keywords

DOXORUBICIN; MULTIDRUG RESISTANCE PROTEIN 1; PHOSPHOLIPID BINDING PROTEIN; PROTEIN ANXA 2; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BREAST CANCER; BREAST CARCINOMA; CANCER CELL; CANCER GROWTH; CANCER PATIENT; CELL INVASION; CELL MIGRATION; CELL MOTILITY; COMPARATIVE STUDY; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRADUCTAL CARCINOMA; LYMPH NODE METASTASIS; MIDDLE AGED; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION; VERY ELDERLY;

ANXA2; BREAST CANCER; INVASION; MDR; P-GLYCOPROTEIN; SRC;

ANNEXIN A2; BREAST NEOPLASMS; DOXORUBICIN; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; MCF-7 CELLS; NEOPLASM INVASIVENESS; P-GLYCOPROTEIN; RNA, MESSENGER;

EID: 84892143460     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2013.11.003     Document Type: Article

References (71)

1. A. Jemal, F. Bray, M.M. Center, J. Ferlay, E. Ward, and D. Forman Global cancer statistics CA Cancer J Clin 61 2011 69 90
2. W.T. Beck, M.C. Cirtain, M.K. Danks, R.L. Felsted, A.R. Safa, and J.S. Wolverton et al. Pharmacological, molecular, and cytogenetic analysis of "atypical" multidrug-resistant human leukemic cells Cancer Res 47 1987 5455 5460 (Pubitemid 17152963)
3. I. Bosch, and J. Croop P-glycoprotein multidrug resistance and cancer Biochim Biophys Acta 1288 1996 F37 F54
4. J.I. Fletcher, M. Haber, M.J. Henderson, and M.D. Norris ABC transporters in cancer: more than just drug efflux pumps Nat Rev Cancer 10 2010 147 156
5. M.J. Smyth, E. Krasovskis, V.R. Sutton, and R.W. Johnstone The drug efflux protein, P-glycoprotein, additionally protects drug-resistant tumor cells from multiple forms of caspase-dependent apoptosis Proc Natl Acad Sci U S A 95 1998 7024 7029
6. A.A. Ruefli, K.M. Tainton, P.K. Darcy, M.J. Smyth, and R.W. Johnstone P-glycoprotein inhibits caspase-8 activation but not formation of the death inducing signal complex (disc) following Fas ligation Cell Death Differ 9 2002 1266 1272 (Pubitemid 35331774)
7. S.Y. Katoh, M. Ueno, and N. Takakura Involvement of MDR1 function in proliferation of tumour cells J Biochem 143 2008 517 524 (Pubitemid 351451765)
8. A. Rocco, D. Compare, E. Liguori, A. Cianflone, G. Pirozzi, and V. Tirino et al. MDR1-P-glycoprotein behaves as an oncofetal protein that promotes cell survival in gastric cancer cells Lab Invest 92 2012 1407 1418
9. M.L. Guenova, G.N. Balatzenko, V.R. Nikolova, B.V. Spassov, and S.M. Konstantinov An anti-apoptotic pattern correlates with multidrug resistance in acute myeloid leukemia patients: a comparative study of active caspase-3, cleaved PARPs, Bcl-2, Survivin and MDR1 gene Hematology 15 2010 135 143
10. J.P. Van Brussel, G. Jan Van Steenbrugge, C. Van Krimpen, J.F. Bogdanowicz, T.H. Van Der Kwast, and F.H. Schroder et al. Expression of multidrug resistance related proteins and proliferative activity is increased in advanced clinical prostate cancer J Urol 165 2001 130 135
11. J. Schneider, S. Gonzalez-Roces, M. Pollan, R. Lucas, A. Tejerina, and M. Martin et al. Expression of LRP and MDR1 in locally advanced breast cancer predicts axillary node invasion at the time of rescue mastectomy after induction chemotherapy Breast Cancer Res 3 2001 183 191 (Pubitemid 32390219)
12. S. Zochbauer-Muller, M. Filipits, M. Rudas, R. Brunner, G. Krajnik, and R. Suchomel et al. P-glycoprotein and MRP1 expression in axillary lymph node metastases of breast cancer patients Anticancer Res 21 2001 119 124 (Pubitemid 32267633)
13. F. Leonessa, and R. Clarke ATP binding cassette transporters and drug resistance in breast cancer Endocr Relat Cancer 10 2003 43 73 (Pubitemid 36457239)
14. S. Raguz, M. Tamburo De Bella, G. Tripuraneni, M.J. Slade, C.F. Higgins, and R.C. Coombes et al. Activation of the MDR1 upstream promoter in breast carcinoma as a surrogate for metastatic invasion Clin Cancer Res 10 2004 2776 2783 (Pubitemid 38509155)
15. C. Mignogna, S. Staibano, V. Altieri, G. De Rosa, G. Pannone, and A. Santoro et al. Prognostic significance of multidrug-resistance protein (MDR-1) in renal clear cell carcinomas: a five year follow-up analysis BMC Cancer 6 2006 293
16. S. Vander Borght, M. Komuta, L. Libbrecht, A. Katoonizadeh, R. Aerts, and S. Dymarkowski et al. Expression of multidrug resistance-associated protein 1 in hepatocellular carcinoma is associated with a more aggressive tumour phenotype and may reflect a progenitor cell origin Liver Int 28 2008 1370 1380
17. H. Chen, J. Hao, L. Wang, and Y. Li Coexpression of invasive markers (uPA, CD44) and multiple drug-resistance proteins (MDR1, MRP2) is correlated with epithelial ovarian cancer progression Br J Cancer 101 2009 432 440
18. A.C. Hoffmann, P. Wild, C. Leicht, S. Bertz, K.D. Danenberg, and P.V. Danenberg et al. MDR1 and ERCC1 expression predict outcome of patients with locally advanced bladder cancer receiving adjuvant chemotherapy Neoplasia 12 2010 628 636
19. M. Colone, A. Calcabrini, L. Toccacieli, G. Bozzuto, A. Stringaro, and M. Gentile et al. The multidrug transporter P-glycoprotein: a mediator of melanoma invasion? J Invest Dermatol 128 2008 957 971 (Pubitemid 351374289)
20. Q.Q. Li, W.J. Wang, J.D. Xu, X.X. Cao, Q. Chen, and J.M. Yang et al. Up-regulation of CD147 and matrix metalloproteinase-2, -9 induced by P-glycoprotein substrates in multidrug resistant breast cancer cells Cancer Sci 98 2007 1767 1774 (Pubitemid 47487914)
21. K.E. Miletti-Gonzalez, S. Chen, N. Muthukumaran, G.N. Saglimbeni, X. Wu, and J. Yang et al. The CD44 receptor interacts with P-glycoprotein to promote cell migration and invasion in cancer Cancer Res 65 2005 6660 6667 (Pubitemid 41060702)
22. E.W. Thompson, S. Paik, N. Brunner, C.L. Sommers, G. Zugmaier, and R. Clarke et al. Association of increased basement membrane invasiveness with absence of estrogen receptor and expression of vimentin in human breast cancer cell lines J Cell Physiol 150 1992 534 544
23. M.A. dit Faute, L. Laurent, D. Ploton, M.F. Poupon, J.C. Jardillier, and H. Bobichon Distinctive alterations of invasiveness, drug resistance and cell-cell organization in 3D-cultures of MCF-7, a human breast cancer cell line, and its multidrug resistant variant Clin Exp Metastasis 19 2002 161 168 (Pubitemid 34264086)
24. J.M. Yang, Z. Xu, H. Wu, H. Zhu, X. Wu, and W.N. Hait Overexpression of extracellular matrix metalloproteinase inducer in multidrug resistant cancer cells Mol Cancer Res 1 2003 420 427 (Pubitemid 36459252)
25. A.N. Staroselsky, T. Mahlin, N. Savion, O. Klein, J. Nordenberg, and N. Donin et al. Metastatic potential and multidrug resistance correlation in the B16 melanoma system J Exp Ther Oncol 1 1996 251 259
26. K. Bjornland, G. Lehne, H.T. Johansen, O. Fodstad, H.E. Rugstad, and A.O. Aasen et al. Human hepatoma cells rich in P-glycoprotein display enhanced in vitro invasive properties compared to P-glycoprotein-poor hepatoma cells Oncol Res 10 1998 255 262 (Pubitemid 128736321)
27. V. Gerke, C.E. Creutz, and S.E. Moss Annexins: linking Ca2+ signalling to membrane dynamics Nat Rev Mol Cell Biol 6 2005 449 461 (Pubitemid 40780557)
28. A. Bharadwaj, M. Bydoun, R. Holloway, and D. Waisman Annexin A2 heterotetramer: structure and function Int J Mol Sci 14 2013 6259 6305
29. X. Zhang, S. Liu, C. Guo, J. Zong, and M.Z. Sun The association of annexin A2 and cancers Clin Transl Oncol 14 2012 634 640
30. N.A. Lokman, M.P. Ween, M.K. Oehler, and C. Ricciardelli The role of annexin A2 in tumorigenesis and cancer progression Cancer Microenviron 4 2011 199 208
31. F. Zhang, L. Zhang, B. Zhang, X. Wei, Y. Yang, and R.Z. Qi et al. Anxa2 plays a critical role in enhanced invasiveness of the multidrug resistant human breast cancer cells J Proteome Res 8 2009 5041 5047
32. X. Peng, F. Gong, G. Xie, Y. Zhao, M. Tang, and L. Yu et al. A proteomic investigation into adriamycin chemo-resistance of human leukemia K562 cells Mol Cell Biochem 351 2011 233 241
33. S.P. Cole, M.J. Pinkoski, G. Bhardwaj, and R.G. Deeley Elevated expression of annexin II (lipocortin II, p36) in a multidrug resistant small cell lung cancer cell line Br J Cancer 65 1992 498 502
34. S. Chuthapisith, B.E. Bean, G. Cowley, J.M. Eremin, S. Samphao, and R. Layfield et al. Annexins in human breast cancer: possible predictors of pathological response to neoadjuvant chemotherapy Eur J Cancer 45 2009 1274 1281
35. S. Takano, A. Togawa, H. Yoshitomi, T. Shida, F. Kimura, and H. Shimizu et al. Annexin II overexpression predicts rapid recurrence after surgery in pancreatic cancer patients undergoing gemcitabine-adjuvant chemotherapy Ann Surg Oncol 15 2008 3157 3168
36. S. Kagawa, S. Takano, H. Yoshitomi, F. Kimura, M. Satoh, and H. Shimizu et al. Akt/mTOR signaling pathway is crucial for gemcitabine resistance induced by Annexin II in pancreatic cancer cells J Surg Res 178 2012 758 767
37. U. Rescher, C. Ludwig, V. Konietzko, A. Kharitonenkov, and V. Gerke Tyrosine phosphorylation of annexin A2 regulates Rho-mediated actin rearrangement and cell adhesion J Cell Sci 121 2008 2177 2185
38. M. de Graauw, I. Tijdens, M.B. Smeets, P.J. Hensbergen, A.M. Deelder, and B. van de Water Annexin A2 phosphorylation mediates cell scattering and branching morphogenesis via cofilin Activation Mol Cell Biol 28 2008 1029 1040 (Pubitemid 351160059)
39. L. Zheng, K. Foley, L. Huang, A. Leubner, G. Mo, and K. Olino et al. Tyrosine 23 phosphorylation-dependent cell-surface localization of annexin A2 is required for invasion and metastases of pancreatic cancer PLoS ONE 6 2011 e19390
40. P. Zhao, W. Zhang, J. Tang, X. Ma, J. Dai, and Y. Li et al. Annexin II promotes invasion and migration of human hepatocellular carcinoma cells in vitro via its interaction with HAb18G/CD147 Cancer Sci 101 2010 387 395
41. S. Das, P. Shetty, M. Valapala, S. Dasgupta, Z. Gryczynski, and J.K. Vishwanatha Signal transducer and activator of transcription 6 (STAT6) is a novel interactor of annexin A2 in prostate cancer cells Biochemistry 49 2010 2216 2226
42. H.C. Zhang, F. Zhang, B. Wu, J.H. Han, W. Ji, and Y. Zhou et al. Identification of the interaction between P-glycoprotein and Anxa2 in multidrug-resistant human breast cancer cells Cancer Biology & Medicine 9 2012 99 104
43. B. Wu, F. Zhang, M. Yu, P. Zhao, W. Ji, and H. Zhang et al. Up-regulation of Anxa2 gene promotes proliferation and invasion of breast cancer MCF-7 cells Cell Prolif 45 2012 189 198
44. Y. Liang, L. O'Driscoll, S. McDonnell, P. Doolan, I. Oglesby, and K. Duffy et al. Enhanced in vitro invasiveness and drug resistance with altered gene expression patterns in a human lung carcinoma cell line after pulse selection with anticancer drugs Int J Cancer 111 2004 484 493 (Pubitemid 39045313)
45. L.E. Schroder, B.A. Blumenstein, R.L. Flanigan, J.R. Borst, and E. David Crawford Phase II evaluation of doxorubicin/vinblastine combined with inhibitors trifluoperazine/verapamil of P-glycoprotein in patients with advanced renal carcinoma Urologic Oncology 3 1997 94 98 (Pubitemid 28135506)
46. J.R. Murren, H.J. Durivage, A.C. Buzaid, M. Reiss, S.D. Flynn, and D. Carter et al. Trifluoperazine as a modulator of multidrug resistance in refractory breast cancer Cancer Chemother Pharmacol 38 1996 65 70
47. M.R. Sharma, L. Koltowski, R.T. Ownbey, G.P. Tuszynski, and M.C. Sharma Angiogenesis-associated protein annexin II in breast cancer: selective expression in invasive breast cancer and contribution to tumor invasion and progression Exp Mol Pathol 81 2006 146 156 (Pubitemid 44715786)
48. J. Inokuchi, N. Narula, D.S. Yee, D.W. Skarecky, A. Lau, and D.K. Ornstein et al. Annexin A2 positively contributes to the malignant phenotype and secretion of IL-6 in DU145 prostate cancer cells Int J Cancer 124 2009 68 74
49. H.S. Mohammad, K. Kurokohchi, H. Yoneyama, M. Tokuda, A. Morishita, and G. Jian et al. Annexin A2 expression and phosphorylation are up-regulated in hepatocellular carcinoma Int J Oncol 33 2008 1157 1163
50. V. Gerke, and K. Weber Identity of p36K phosphorylated upon Rous sarcoma virus transformation with a protein purified from brush borders; calcium-dependent binding to non-erythroid spectrin and F-actin EMBO J 3 1984 227 233
51. K.L. Gould, J.R. Woodgett, C.M. Isacke, and T. Hunter The protein-tyrosine kinase substrate p36 is also a substrate for protein kinase C in vitro and in vivo Mol Cell Biol 6 1986 2738 2744
52. J.A. Spijkers-Hagelstein, S. Mimoso Pinhancos, P. Schneider, R. Pieters, and R.W. Stam Src kinase-induced phosphorylation of annexin A2 mediates glucocorticoid resistance in MLL-rearranged infant acute lymphoblastic leukemia Leukemia 27 2013 1063 1071
53. I. Mantovani, A. Cappellini, P.L. Tazzari, V. Papa, L. Cocco, and A.M. Martelli Caspase-dependent cleavage of 170-kDa P-glycoprotein during apoptosis of human T-lymphoblastoid CEM cells J Cell Physiol 207 2006 836 844 (Pubitemid 43668249)
54. K.M. Tainton, M.J. Smyth, J.T. Jackson, J.E. Tanner, L. Cerruti, and S.M. Jane et al. Mutational analysis of P-glycoprotein: suppression of caspase activation in the absence of ATP-dependent drug efflux Cell Death Differ 11 2004 1028 1037 (Pubitemid 39232362)
55. S. Barakat, S. Turcotte, M. Demeule, M.P. Lachambre, A. Regina, and L.G. Baggetto et al. Regulation of brain endothelial cells migration and angiogenesis by P-glycoprotein/caveolin-1 interaction Biochem Biophys Res Commun 372 2008 440 446
56. P. Surowiak, V. Materna, R. Matkowski, K. Szczuraszek, J. Kornafel, and A. Wojnar et al. Relationship between the expression of cyclooxygenase 2 and MDR1/P-glycoprotein in invasive breast cancers and their prognostic significance Breast Cancer Res 7 2005 R862 R870
57. Y. Liang, P. Meleady, I. Cleary, S. McDonnell, L. Connolly, and M. Clynes Selection with melphalan or paclitaxel (Taxol) yields variants with different patterns of multidrug resistance, integrin expression and in vitro invasiveness Eur J Cancer 37 2001 1041 1052 (Pubitemid 32397691)
58. E.C. Lopes, G. Ernst, P. Aulicino, S. Vanzulli, M. Garcia, and E. Alvarez et al. Dissimilar invasive and metastatic behavior of vincristine and doxorubicin-resistant cell lines derived from a murine T cell lymphoid leukemia Clin Exp Metastasis 19 2002 283 290 (Pubitemid 34606753)
59. R. Kotchetkov, J. Cinatl, R. Blaheta, J.U. Vogel, J. Karaskova, and J. Squire et al. Development of resistance to vincristine and doxorubicin in neuroblastoma alters malignant properties and induces additional karyotype changes: a preclinical model Int J Cancer 104 2003 36 43 (Pubitemid 36184144)
60. S. Hiscox, W.G. Jiang, K. Obermeier, K. Taylor, L. Morgan, and R. Burmi et al. Tamoxifen resistance in MCF7 cells promotes EMT-like behaviour and involves modulation of beta-catenin phosphorylation Int J Cancer 118 2006 290 301 (Pubitemid 41779067)
61. Q.Q. Li, W.J. Wang, J.D. Xu, X.X. Cao, Q. Chen, and J.M. Yang et al. Involvement of CD147 in regulation of multidrug resistance to P-gp substrate drugs and in vitro invasion in breast cancer cells Cancer Sci 98 2007 1064 1069 (Pubitemid 46865392)
62. L. Tatenhorst, U. Rescher, V. Gerke, and W. Paulus Knockdown of annexin 2 decreases migration of human glioma cells in vitro Neuropathol Appl Neurobiol 32 2006 271 277
63. S. Mussunoor, and G.I. Murray The role of annexins in tumour development and progression J Pathol 216 2008 131 140
64. Y. Shiozawa, A.M. Havens, Y. Jung, A.M. Ziegler, E.A. Pedersen, and J. Wang et al. Annexin II/annexin II receptor axis regulates adhesion, migration, homing, and growth of prostate cancer J Cell Biochem 105 2008 370 380
65. M. Sharma, R.T. Ownbey, and M.C. Sharma Breast cancer cell surface annexin II induces cell migration and neoangiogenesis via tPA dependent plasmin generation Exp Mol Pathol 88 2010 278 286
66. Y.Q. Wang, F. Zhang, R. Tian, W. Ji, Y. Zhou, and X.M. Sun et al. Tyrosine 23 phosphorylation of annexin A2 promotes proliferation, invasion, and Stat3 phosphorylation in the nucleus of human breast cancer SK-BR-3 cells Cancer Biology & Medicine 9 2012 248 253
67. C.R. Rankin, R.S. Hilgarth, G. Leoni, M. Kwon, K.A. Den Beste, and C.A. Parkos et al. Annexin A2 regulates beta1 integrin internalization and intestinal epithelial cell migration J Biol Chem 288 2013 15229 15239
68. P.J. Maxwell, D.B. Longley, T. Latif, J. Boyer, W. Allen, and M. Lynch et al. Identification of 5-fluorouracil-inducible target genes using cDNA microarray profiling Cancer Res 63 2003 4602 4606 (Pubitemid 36951036)
69. J. Boyer, P.J. Maxwell, D.B. Longley, and P.G. Johnston 5-Fluorouracil: identification of novel downstream mediators of tumour response Anticancer Res 24 2004 417 423 (Pubitemid 38623115)
70. P. Zhao, W. Zhang, S.J. Wang, X.L. Yu, J. Tang, and W. Huang et al. HAb18G/CD147 promotes cell motility by regulating annexin II-activated RhoA and Rac1 signaling pathways in hepatocellular carcinoma cells Hepatology 54 2011 2012 2024
71. J.M. Yang, A. Vassil, and W.N. Hait Involvement of phosphatidylinositol- 3-kinase in membrane ruffling induced by P-glycoprotein substrates in multidrug-resistant carcinoma cells Biochem Pharmacol 63 2002 959 966 (Pubitemid 34243009)