Tumor endothelial cells acquire drug resistance by MDR1 up-regulation via VEGF signaling in tumor microenvironment

American Journal of Pathology

Volumn 180, Issue 3, 2012, Pages 1283-1293

  Akiyama, Kosuke ^a   Ohga, Noritaka ^a   Hida, Yasuhiro ^b   Kawamoto, Taisuke ^a   Sadamoto, Yoshihiro ^a   Ishikawa, Shuhei ^a   Maishi, Nako ^a   Akino, Tomoshige ^a,b   Kondoh, Miyako ^a   Matsuda, Aya ^a   Inoue, Nobuo ^a   Shindoh, Masanobu ^a   Hida, Kyoko ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; GLYCOPROTEIN P; KI 8751; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; PACLITAXEL; PROTEIN KINASE B; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR 2; Y BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ISOLATION; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR CELL; TUMOR ENDOTHELIAL CELL; TUMOR MICROENVIRONMENT; TUMOR RESISTANCE; UPREGULATION;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; ENDOTHELIAL CELLS; HUMANS; NEOPLASMS; P-GLYCOPROTEIN; PACLITAXEL; PHENYLUREA COMPOUNDS; QUINOLINES; SIGNAL TRANSDUCTION; TRANSPLANTATION, HETEROLOGOUS; TUBULIN MODULATORS; TUMOR MICROENVIRONMENT; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; Y-BOX-BINDING PROTEIN 1;

EID: 84857197449     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.11.029     Document Type: Article

References (56)

1. J. Folkman Angiogenesis in cancer, vascular, rheumatoid and other disease Nat Med 1 1995 27 31
2. J. Folkman Role of angiogenesis in tumor growth and metastasis Semin Oncol 29 2002 15 18
3. R. Auerbach, N. Akhtar, R.L. Lewis, B.L. Shinners Angiogenesis assays: problems and pitfalls Cancer Metastasis Rev 19 2000 167 172
4. R.S. Kerbel, J. Yu, J. Tran, S. Man, A. Viloria-Petit, G. Klement, B.L. Coomber, J. Rak Possible mechanisms of acquired resistance to anti-angiogenic drugs: implications for the use of combination therapy approaches Cancer Metastasis Rev 20 2001 79 86
5. T. Browder, C.E. Butterfield, B.M. Kraling, B. Shi, B. Marshall, M.S. O'Reilly, J. Folkman Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer Cancer Res 60 2000 1878 1886
6. S. Man, G. Bocci, G. Francia, S.K. Green, S. Jothy, D. Hanahan, P. Bohlen, D.J. Hicklin, G. Bergers, R.S. Kerbel Antitumor effects in mice of low-dose (metronomic) cyclophosphamide administered continuously through the drinking water Cancer Res 62 2002 2731 2735
7. H. Kato, Y. Ichinose, M. Ohta, E. Hata, N. Tsubota, H. Tada, Y. Watanabe, H. Wada, M. Tsuboi, N. Hamajima A randomized trial of adjuvant chemotherapy with uracil-tegafur for adenocarcinoma of the lung N Engl J Med 350 2004 1713 1721
8. R.S. Mehta, D. Jackson, T. Schubbert Metronomic schedule of paclitaxel is effective in hormone receptor-positive and hormone receptor-negative breast cancer J Clin Oncol 27 2009 3067 3068 author reply 30683069
9. R.K. Jain Molecular regulation of vessel maturation Nat Med 9 2003 685 693
10. D.M. McDonald, P. Baluk Significance of blood vessel leakiness in cancer Cancer Res 62 2002 5381 5385
11. S. Morikawa, P. Baluk, T. Kaidoh, A. Haskell, R.K. Jain, D.M. McDonald Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors Am J Pathol 160 2002 985 1000
12. B. St Croix, C. Rago, V. Velculescu, G. Traverso, K.E. Romans, E. Montgomery, A. Lal, G.J. Riggins, C. Lengauer, B. Vogelstein, K.W. Kinzler Genes expressed in human tumor endothelium Science 289 2000 1197 1202
13. C. Lu, T. Bonome, Y. Li, A.A. Kamat, L.Y. Han, R. Schmandt, R.L. Coleman, D.M. Gershenson, R.B. Jaffe, M.J. Birrer, A.K. Sood Gene alterations identified by expression profiling in tumor-associated endothelial cells from invasive ovarian carcinoma Cancer Res 67 2007 1757 1768
14. S. Seaman, J. Stevens, M.Y. Yang, D. Logsdon, C. Graff-Cherry, B. St Croix Genes that distinguish physiological and pathological angiogenesis Cancer Cell 11 2007 539 554
15. K. Hida, Y. Hida, D.N. Amin, A.F. Flint, D. Panigrahy, C.C. Morton, M. Klagsbrun Tumor-associated endothelial cells with cytogenetic abnormalities Cancer Res 64 2004 8249 8255
16. K. Hida, M. Klagsbrun A new perspective on tumor endothelial cells: unexpected chromosome and centrosome abnormalities Cancer Res 65 2005 2507 2510
17. D.N. Amin, K. Hida, D.R. Bielenberg, M. Klagsbrun Tumor endothelial cells express epidermal growth factor receptor (EGFR) but not ErbB3 and are responsive to EGF and to EGFR kinase inhibitors Cancer Res 66 2006 2173 2180
18. K. Tsuchiya, K. Hida, Y. Hida, C. Muraki, N. Ohga, T. Akino, T. Kondo, T. Miseki, K. Nakagawa, M. Shindoh, T. Harabayashi, N. Shinohara, K. Nonomura, M. Kobayashi Adrenomedullin antagonist suppresses tumor formation in renal cell carcinoma through inhibitory effects on tumor endothelial cells and endothelial progenitor mobilization Int J Oncol 36 2010 1379 1386
19. K. Matsuda, N. Ohga, Y. Hida, C. Muraki, K. Tsuchiya, T. Kurosu, T. Akino, S.C. Shih, Y. Totsuka, M. Klagsbrun, M. Shindoh, K. Hida Isolated tumor endothelial cells maintain specific character during long-term culture Biochem Biophys Res Commun 394 2010 947 954
20. N. Ohga, K. Hida, Y. Hida, C. Muraki, K. Tsuchiya, K. Matsuda, Y. Ohiro, Y. Totsuka, M. Shindoh Inhibitory effects of epigallocatechin-3 gallate, a polyphenol in green tea, on tumor-associated endothelial cells and endothelial progenitor cells Cancer Sci 100 2009 1963 1970
21. T. Akino, K. Hida, Y. Hida, K. Tsuchiya, D. Freedman, C. Muraki, N. Ohga, K. Matsuda, K. Akiyama, T. Harabayashi, N. Shinohara, K. Nonomura, M. Klagsbrun, M. Shindoh Cytogenetic abnormalities of tumor-associated endothelial cells in human malignant tumors Am J Pathol 175 2009 2657 2667
22. B. Streubel, A. Chott, D. Huber, M. Exner, U. Jager, O. Wagner, I. Schwarzinger Lymphoma-specific genetic aberrations in microvascular endothelial cells in B-cell lymphomas N Engl J Med 351 2004 250 259
23. B. Bussolati, I. Deambrosis, S. Russo, M.C. Deregibus, G. Camussi Altered angiogenesis and survival in human tumor-derived endothelial cells FASEB J 17 2003 1159 1161
24. C. Grange, B. Bussolati, S. Bruno, V. Fonsato, A. Sapino, G. Camussi Isolation and characterization of human breast tumor-derived endothelial cells Oncol Rep 15 2006 381 386
25. Y.Q. Xiong, H.C. Sun, W. Zhang, X.D. Zhu, P.Y. Zhuang, J.B. Zhang, L. Wang, W.Z. Wu, L.X. Qin, Z.Y. Tang Human hepatocellular carcinoma tumor-derived endothelial cells manifest increased angiogenesis capability and drug resistance compared with normal endothelial cells Clin Cancer Res 15 2009 4838 4846
26. J.M. Kozlowski, I.R. Hart, I.J. Fidler, N. Hanna A human melanoma line heterogeneous with respect to metastatic capacity in athymic nude mice J Natl Cancer Inst 72 1984 913 917
27. K. Hida, Y. Hida, M. Shindoh Understanding tumor endothelial cell abnormalities to develop ideal anti-angiogenic therapies Cancer Sci 99 2008 459 466
28. J.L. Arbiser, H. Larsson, L. Claesson-Welsh, X. Bai, K. LaMontagne, S.W. Weiss, S. Soker, E. Flynn, L.F. Brown Overexpression of VEGF 121 in immortalized endothelial cells causes conversion to slowly growing angiosarcoma and high level expression of the VEGF receptors VEGFR-1 and VEGFR-2 in vivo Am J Pathol 156 2000 1469 1476
29. T. Kurosu, N. Ohga, Y. Hida, N. Maishi, K. Akiyama, W. Kakuguchi, T. Kuroshima, M. Kondo, T. Akino, Y. Totsuka, M. Shindoh, F. Higashino, K. Hida HuR keeps an angiogenic switch on by stabilising mRNA of VEGF and COX-2 in tumour endothelium Br J Cancer 104 2011 819 829
30. M. Janz, N. Harbeck, P. Dettmar, U. Berger, A. Schmidt, K. Jurchott, M. Schmitt, H.D. Royer Y-box factor YB-1 predicts drug resistance and patient outcome in breast cancer independent of clinically relevant tumor biologic factors HER2, uPA and PAI-1 Int J Cancer 97 2002 278 282
31. P. Gimenez-Bonafe, M.N. Fedoruk, T.G. Whitmore, M. Akbari, J.L. Ralph, S. Ettinger, M.E. Gleave, C.C. Nelson YB-1 is upregulated during prostate cancer tumor progression and increases P-glycoprotein activity Prostate 59 2004 337 349
32. X. Huang, K. Ushijima, K. Komai, Y. Takemoto, S. Motoshima, T. Kamura, K. Kohno Co-expression of Y box-binding protein-1 and P-glycoprotein as a prognostic marker for survival in epithelial ovarian cancer Gynecol Oncol 93 2004 287 291
33. M. Kuwano, T. Uchiumi, H. Hayakawa, M. Ono, M. Wada, H. Izumi, K. Kohno The basic and clinical implications of ABC transporters: Y-box-binding protein-1 (YB-1) and angiogenesis-related factors in human malignancies Cancer Sci 94 2003 9 14
34. H. Zhu, H. Wu, X. Liu, B.R. Evans, D.J. Medina, C.G. Liu, J.M. Yang Role of MicroRNA miR-27a and miR-451 in the regulation of MDR1/P-glycoprotein expression in human cancer cells Biochem Pharmacol 76 2008 582 588
35. N. Patel, S.K. Chatterjee, V. Vrbanac, I. Chung, C.J. Mu, R.R. Olsen, C. Waghorne, B.R. Zetter Rescue of paclitaxel sensitivity by repression of Prohibitin1 in drug-resistant cancer cells Proc Natl Acad Sci U S A 107 2010 2503 2508
36. Y.J. Mi, Y.J. Liang, H.B. Huang, H.Y. Zhao, C.P. Wu, F. Wang, L.Y. Tao, C.Z. Zhang, C.L. Dai, A.K. Tiwari, X.X. Ma, K.K. To, S.V. Ambudkar, Z.S. Chen, L.W. Fu Apatinib (YN968D1) reverses multidrug resistance by inhibiting the efflux function of multiple ATP-binding cassette transporters Cancer Res 70 2010 7981 7991
37. S. Kesari, D. Schiff, L. Doherty, D.C. Gigas, T.T. Batchelor, A. Muzikansky, A. O'Neill, J. Drappatz, A.S. Chen-Plotkin, N. Ramakrishna, S.E. Weiss, B. Levy, J. Bradshaw, J. Kracher, A. Laforme, P.M. Black, J. Folkman, M. Kieran, P.Y. Wen Phase II study of metronomic chemotherapy for recurrent malignant gliomas in adults Neuro Oncol 9 2007 354 363
38. M.K. Krzyzanowska, I.F. Tannock, G. Lockwood, J. Knox, M. Moore, G.A. Bjarnason A phase II trial of continuous low-dose oral cyclophosphamide and celecoxib in patients with renal cell carcinoma Cancer Chemother Pharmacol 60 2007 135 141
39. R.S. Bhatt, J. Merchan, R. Parker, H.K. Wu, L. Zhang, V. Seery, J.V. Heymach, M.B. Atkins, D. McDermott, V.P. Sukhatme A phase 2 pilot trial of low-dose, continuous infusion, or "metronomic" paclitaxel and oral celecoxib in patients with metastatic melanoma Cancer 116 2010 1751 1756
40. E. Pasquier, M. Kavallaris, N. Andre Metronomic chemotherapy: new rationale for new directions Nat Rev Clin Oncol 7 2010 455 465
41. B. Sarkadi, L. Homolya, G. Szakacs, A. Varadi Human multidrug resistance ABCB and ABCG transporters: participation in a chemoimmunity defense system Physiol Rev 86 2006 1179 1236
42. N. Lasagna, O. Fantappie, M. Solazzo, L. Morbidelli, S. Marchetti, G. Cipriani, M. Ziche, R. Mazzanti Hepatocyte growth factor and inducible nitric oxide synthase are involved in multidrug resistance-induced angiogenesis in hepatocellular carcinoma cell lines Cancer Res 66 2006 2673 2682
43. I.J. Fidler, S.J. Kim, R.R. Langley The role of the organ microenvironment in the biology and therapy of cancer metastasis J Cell Biochem 101 2007 927 936
44. M. Perez-Sayans, J.M. Somoza-Martin, F. Barros-Angueira, P.G. Diz, J.M. Rey, A. Garcia-Garcia Multidrug resistance in oral squamous cell carcinoma: the role of vacuolar ATPases Cancer Lett 295 2010 135 143
45. A. Sandler, R. Gray, M.C. Perry, J. Brahmer, J.H. Schiller, A. Dowlati, R. Lilenbaum, D.H. Johnson Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer N Engl J Med 355 2006 2542 2550
46. K. Miller, M. Wang, J. Gralow, M. Dickler, M. Cobleigh, E.A. Perez, T. Shenkier, D. Cella, N.E. Davidson Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer N Engl J Med 357 2007 2666 2676
47. S.K. Swamynathan, A. Nambiar, R.V. Guntaka Role of single-stranded DNA regions and Y-box proteins in transcriptional regulation of viral and cellular genes FASEB J 12 1998 515 522
48. K. Mantwill, N. Kohler-Vargas, A. Bernshausen, A. Bieler, H. Lage, A. Kaszubiak, P. Surowiak, T. Dravits, U. Treiber, R. Hartung, B. Gansbacher, P.S. Holm Inhibition of the multidrug-resistant phenotype by targeting YB-1 with a conditionally oncolytic adenovirus: implications for combinatorial treatment regimen with chemotherapeutic agents Cancer Res 66 2006 7195 7202
49. M. Takahashi, S. Shimajiri, H. Izumi, G. Hirano, E. Kashiwagi, Y. Yasuniwa, Y. Wu, B. Han, M. Akiyama, S. Nishizawa, Y. Sasaguri, K. Kohno Y-box binding protein-1 is a novel molecular target for tumor vessels Cancer Sci 101 2010 1367 1373
50. A.E. Karnoub, A.B. Dash, A.P. Vo, A. Sullivan, M.W. Brooks, G.W. Bell, A.L. Richardson, K. Polyak, R. Tubo, R.A. Weinberg Mesenchymal stem cells within tumour stroma promote breast cancer metastasis Nature 449 2007 557 563
51. B. Vogelstein, K.W. Kinzler Cancer genes and the pathways they control Nat Med 10 2004 789 799
52. A.S. Alavi, L. Acevedo, W. Min, D.A. Cheresh Chemoresistance of endothelial cells induced by basic fibroblast growth factor depends on Raf-1-mediated inhibition of the proapoptotic kinase, ASK1 Cancer Res 67 2007 2766 2772
53. M. Barancik, V. Bohacova, J. Sedlak, Z. Sulova, A. Breier LY294,002, a specific inhibitor of PI3K/Akt kinase pathway, antagonizes P-glycoprotein- mediated multidrug resistance Eur J Pharm Sci 29 2006 426 434
54. B.H. Choi, C.G. Kim, Y. Lim, S.Y. Shin, Y.H. Lee Curcumin down-regulates the multidrug-resistance mdr1b gene by inhibiting the PI3K/Akt/NF kappa B pathway Cancer Lett 259 2008 111 118
55. Y. Zhang, X. Qu, X. Hu, X. Yang, K. Hou, Y. Teng, J. Zhang, K. Sada, Y. Liu Reversal of P-glycoprotein-mediated multi-drug resistance by the E3 ubiquitin ligase Cbl-b in human gastric adenocarcinoma cells J Pathol 218 2009 248 255
56. B.W. Sutherland, J. Kucab, J. Wu, C. Lee, M.C. Cheang, E. Yorida, D. Turbin, S. Dedhar, C. Nelson, M. Pollak, H. Leighton Grimes, K. Miller, S. Badve, D. Huntsman, C. Blake-Gilks, M. Chen, C.J. Pallen, S.E. Dunn Akt phosphorylates the Y-box binding protein 1 at Ser102 located in the cold shock domain and affects the anchorage-independent growth of breast cancer cells Oncogene 24 2005 4281 4292