Pazopanib inhibits the activation of PDGFRβ-expressing astrocytes in the brain metastatic microenvironment of breast cancer cells

American Journal of Pathology

Volumn 182, Issue 6, 2013, Pages 2368-2379

  Gril, Brunilde ^a   Palmieri, Diane ^a   Qian, Yongzhen ^a   Anwar, Talha ^a   Liewehr, David J ^a   Steinberg, Seth M ^a   Andreu, Zoraida ^b   Masana, Daniel ^b   Fernández, Paloma ^b   Steeg, Patricia S ^a   Vidal Vanaclocha, Fernando ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSIDAD SAN PABLO CEU   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PAZOPANIB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN METASTASIS; BREAST CANCER; CANCER CELL CULTURE; CELL ACTIVATION; CELL SUBPOPULATION; CONTROLLED STUDY; CRANIOTOMY; DRUG EFFECT; GLIA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROMETASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; ANTINEOPLASTIC AGENTS; ASTROCYTES; BRAIN NEOPLASMS; BREAST NEOPLASMS; DRUG EVALUATION, PRECLINICAL; FEMALE; HUMANS; MICE; NEOPLASM MICROMETASTASIS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NEUROGLIA; PHOSPHORYLATION; PYRIMIDINES; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; SULFONAMIDES; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

EID: 84878217484     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.02.043     Document Type: Article

References (67)

1. J.S. Barnholtz-Sloan, A.E. Sloan, F.G. Davis, F.D. Vigneau, P. Lai, and R.E. Sawaya Incidence proportions of brain metastases in patients diagnosed (1973 to 2001) in the Metropolitan Detroit Cancer Surveillance System J Clin Oncol 22 2004 2865 2872
2. H.J. Stemmler, and V. Heinemann Central nervous system metastases in HER-2-overexpressing metastatic breast cancer: a treatment challenge Oncologist 13 2008 739 750
3. B. Gril, L. Evans, D. Palmieri, and P.S. Steeg Translational research in brain metastasis is identifying molecular pathways that may lead to the development of new therapeutic strategies Eur J Cancer 46 2010 1204 1210
4. N.U. Lin, and E.P. Winer Brain metastases: the HER2 paradigm Clin Cancer Res 13 2007 1648 1655
5. P.S. Steeg, K.A. Camphausen, and Q.R. Smith Brain metastases as preventive and therapeutic targets Nat Rev Cancer 11 2011 352 363
6. A.F. Eichler, E. Chung, D.P. Kodack, J.S. Loeffler, D. Fukumura, and R.K. Jain The biology of brain metastases-translation to new therapies Nat Rev Clin Oncol 8 2011 344 356
7. P.S. Steeg Perspective: the right trials Nature 485 2012 S58 S59
8. D. Palmieri, D. Fitzgerald, S.M. Shreeve, E. Hua, J.L. Bronder, R.J. Weil, S. Davis, A.M. Stark, M.J. Merino, R. Kurek, H.M. Mehdorn, G. Davis, S.M. Steinberg, P.S. Meltzer, K. Aldape, and P.S. Steeg Analyses of resected human brain metastases of breast cancer reveal the association between up-regulation of hexokinase 2 and poor prognosis Mol Cancer Res 7 2009 1438 1445
9. D. Palmieri, P.R. Lockman, F.C. Thomas, E. Hua, J. Herring, E. Hargrave, M. Johnson, N. Flores, Y. Qian, E. Vega-Valle, K.S. Taskar, V. Rudraraju, R.K. Mittapalli, J.A. Gaasch, K.A. Bohn, H.R. Thorsheim, D.J. Liewehr, S. Davis, J.F. Reilly, R. Walker, J.L. Bronder, L. Feigenbaum, S.M. Steinberg, K. Camphausen, P.S. Meltzer, V.M. Richon, Q.R. Smith, and P.S. Steeg Vorinostat inhibits brain metastatic colonization in a model of triple-negative breast cancer and induces DNA double-strand breaks Clin Cancer Res 15 2009 6148 6157
10. B. Gril, D. Palmieri, J.L. Bronder, J.M. Herring, E. Vega-Valle, L. Feigenbaum, D.J. Liewehr, S.M. Steinberg, M.J. Merino, S.D. Rubin, and P.S. Steeg Effect of lapatinib on the outgrowth of metastatic breast cancer cells to the brain J Natl Cancer Inst 100 2008 1092 1103
11. H. Zhao, K. Cui, F. Nie, L. Wang, M.B. Brandl, G. Jin, F. Li, Y. Mao, Z. Xue, A. Rodriguez, J. Chang, and S.T. Wong The effect of mTOR inhibition alone or combined with MEK inhibitors on brain metastasis: an in vivo analysis in triple-negative breast cancer models Breast Cancer Res Treat 131 2012 425 436
12. S. Paget The distribution of secondary growths in cancer of the breast Lancet 1 1889 99 101
13. J. Condeelis, and J.W. Pollard Macrophages: obligate partners for tumor cell migration, invasion, and metastasis Cell 124 2006 263 266
14. R. Kalluri, and M. Zeisberg Fibroblasts in cancer Nat Rev Cancer 6 2006 392 401
15. I. Fidler The pathogenesis of cancer metastasis: the "seed and soil" hypothesis revisited Nat Rev Cancer 3 2003 453 458
16. F. Vidal-Vanaclocha The liver prometastatic reaction of cancer patients: implications for microenvironment-dependent colon cancer gene regulation Cancer Microenviron 4 2011 163 180
17. D. Palmieri, J.L. Bronder, J.M. Herring, T. Yoneda, R.J. Weil, A.M. Stark, R. Kurek, E. Vega-Valle, L. Feigenbaum, D. Halverson, A.O. Vortmeyer, S.M. Steinberg, K. Aldape, and P.S. Steeg Her-2 overexpression increases the metastatic outgrowth of breast cancer cells in the brain Cancer Res 67 2007 4190 4198
18. D.P. Fitzgerald, P. Subramanian, M. Deshpande, C. Graves, I. Gordon, Y. Qian, Y. Snitkovsky, D.J. Liewehr, S.M. Steinberg, J.D. Paltan-Ortiz, M.M. Herman, K. Camphausen, D. Palmieri, S.P. Becerra, and P.S. Steeg Opposing effects of pigment epithelium-derived factor on breast cancer cell versus neuronal survival: implication for brain metastasis and metastasis-induced brain damage Cancer Res 72 2012 144 153
19. B. Gril, D. Palmieri, Y. Qian, D. Smart, L. Ileva, D.J. Liewehr, S.M. Steinberg, and P.S. Steeg Pazopanib reveals a role for tumor cell B-Raf in the prevention of HER2+ breast cancer brain metastasis Clin Cancer Res 17 2011 142 153
20. T. Oskarsson, S. Acharyya, X.H. Zhang, S. Vanharanta, S.F. Tavazoie, P.G. Morris, R.J. Downey, K. Manova-Todorova, E. Brogi, and J. Massague Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs Nat Med 17 2011 867 874
21. W.S. Carbonell, O. Ansorge, N. Sibson, and R. Muschel The vascular basement membrane as "soil" in brain metastasis PLoS One 4 2009 e5857
22. D. Fitzgerald, D. Palmieri, E. Hua, E. Hargrave, J. Herring, Y. Qian, E. Vega-Valle, R. Weil, A. Stark, A. Vortmeyer, and P. Steeg Reactive glia are recruited by highly proliferative brain metastases of breast cancer and promote tumor cell colonization Clin Exp Metast 25 2008 799 810
23. M. Lorger, and B. Felding-Habermann Capturing changes in the brain microenvironment during initial steps of breast cancer brain metastasis Am J Pathol 176 2010 2958 2971
24. T. Seike, K. Fujita, Y. Yamakawa, M.A. Kido, S. Takiguchi, N. Teramoto, H. Iguchi, and M. Noda Interaction between lung cancer cells and astrocytes via specific inflammatory cytokines in the microenvironment of brain metastasis Clin Exp Metastasis 28 2011 13 25
25. S.J. Kim, J.S. Kim, E.S. Park, J.S. Lee, Q. Lin, R.R. Langley, M. Maya, J. He, S.W. Kim, Z. Weihua, K. Balasubramanian, D. Fan, G.B. Mills, M.C. Hung, and I.J. Fidler Astrocytes upregulate survival genes in tumor cells and induce protection from chemotherapy Neoplasia 13 2011 286 298
26. A. Norazit, M.N. Nguyen, C.G. Dickson, G. Tuxworth, B. Goss, A. Mackay-Sim, and A.C. Meedeniya Vascular endothelial growth factor and platelet derived growth factor modulates the glial response to a cortical stab injury Neuroscience 192 2011 652 660
27. M. Fisher Pericyte signaling in the neurovascular unit Stroke 40 2009 S13 S15
28. C.F. Valenzuela, A. Kazlauskas, and J.L. Weiner Roles of platelet-derived growth factor in the developing and mature nervous systems Brain Res Brain Res Rev 24 1997 77 89
29. E.A. Winkler, R.D. Bell, and B.V. Zlokovic Pericyte-specific expression of PDGF beta receptor in mouse models with normal and deficient PDGF beta receptor signaling Mol Neurodegener 5 2010 32
30. A. Ostman, and C.H. Heldin PDGF receptors as targets in tumor treatment Adv Cancer Res 97 2007 247 274
31. R. Kumar, V.B. Knick, S.K. Rudolph, J.H. Johnson, R.M. Crosby, M.C. Crouthamel, T.M. Hopper, C.G. Miller, L.E. Harrington, J.A. Onori, R.J. Mullin, T.M. Gilmer, A.T. Truesdale, A.H. Epperly, A. Boloor, J.A. Stafford, D.K. Luttrell, and M. Cheung Pharmacokinetic-pharmacodynamic correlation from mouse to human with pazopanib, a multikinase angiogenesis inhibitor with potent antitumor and antiangiogenic activity Mol Cancer Ther 6 2007 2012 2021
32. B. Gril, D. Palmieri, Y. Qian, T. Anwar, L. Ileva, M. Bernardo, P. Choyke, D.J. Liewehr, S.M. Steinberg, and P.S. Steeg The B-Raf status of tumor cells may be a significant determinant of both antitumor and anti-angiogenic effects of pazopanib in xenograft tumor models PLoS One 6 2011 e256k25
33. Y. Sonoda, T. Ozawa, Y. Hirose, K.D. Aldape, M. McMahon, M.S. Berger, and R.O. Pieper Formation of intracranial tumors by genetically modified human astrocytes defines four pathways critical in the development of human anaplastic astrocytoma Cancer Res 61 2001 4956 4960
34. L. Diaz-Flores, R. Gutierrez, J.F. Madrid, H. Varela, F. Valladares, E. Acosta, P. Martin-Vasallo, and L. Diaz-Flores Jr. Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche Histol Histopathol 24 2009 909 969
35. S.H. Kang, M. Fukaya, J.K. Yang, J.D. Rothstein, and D.E. Bergles NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration Neuron 68 2010 668 681
36. E. Park, S. Kim, S. Kim, S.L. Yoon, S.H. Leem, S.B. Kim, S. Kim, Y.Y. Park, J.H. Cheong, H. Woo, G. Mills, I. Fidler, and J.S. Lee Cross-species hybridization of microarrays for studying tumor transcriptome of brain metastasis Proc Natl Acad Sci U S A 108 2011 17456 17461
37. M. Zhang, and Y. Olsson Reactions of astrocytes and microglial cells around hematogenous metastases of the human brain. Expression of endothelin-like immunoreactivity in reactive astrocytes and activation of microglial cells J Neurol Sci 134 1995 26 32
38. E. Gerstner, and R. Fine Increased permeability of the blood-brain barrier to chemotherapy in metastatic brain tumors: establishing a treatment paradigm J Clin Oncol 25 2007 2306 2312
39. P. Lockman, R. Mittapalli, K. Taskar, V. Rudraruju, B. Gril, K. Bohn, C. Adkins, F. Thomas, H. Thorsheim, J. Gaasch, S. Huang, D. Palmieri, P. Steeg, and Q. Smith Heterogeneous blood-brain barrier permeability determines drug efficacy in mouse brain metastases of breast cancer Clin Cancer Res 16 2010 5662 5678
40. D.B. Percy, E.J. Ribot, Y. Chen, C. McFadden, C. Simedrea, P.S. Steeg, A.F. Chambers, and P.J. Foster In vivo characterization of changing blood-tumor barrier permeability in a mouse model of breast cancer metastasis: a complementary magnetic resonance imaging approach Invest Radiol 46 2011 718 725
41. J.F. Deeken, and W. Loscher The blood-brain barrier and cancer: transporters, treatment, and Trojan horses Clin Cancer Res 13 2007 1663 1674
42. V. Castronovo, M. Bracke, M. Mareel, M. Reznik, and J. Foidart Absence of laminin deposition in breast-cancer and metastases except to the brain Pathol Res Pract 187 1991 201 208
43. J. McArdle, H. Muller, B. Roff, and W. Murphy Basal lamina redevelopment in tumours metastatic to the brain: an immunoperoxidase study using an antibody to type-IV collagen Int J Cancer 34 1984 633 638
44. K. Arimura, T. Ago, M. Kamouchi, K. Nakamura, K. Ishitsuka, J. Kuroda, H. Sugimori, H. Ooboshi, T. Sasaki, and T. Kitazono PDGF receptor beta signaling in pericytes following ischemic brain injury Curr Neurovasc Res 9 2012 1 9
45. N. Song, Y. Huang, H. Shi, S. Yuan, Y. Ding, X. Song, Y. Fu, and Y. Luo Overexpression of platelet-derived growth factor-BB increases tumor pericyte content via stromal-derived factor-1alpha/CXCR4 axis Cancer Res 69 2009 6057 6064
46. C. Dai, J.C. Celestino, Y. Okada, D.N. Louis, G.N. Fuller, and E.C. Holland PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo Genes Dev 15 2001 1913 1925
47. H.C. Wilson, N.J. Scolding, and C.S. Raine Co-expression of PDGF alpha receptor and NG2 by oligodendrocyte precursors in human CNS and multiple sclerosis lesions J Neuroimmunol 176 2006 162 173
48. Y. Maeda, M. Solanky, J. Menonna, J. Chapin, W. Li, and P. Dowling Platelet-derived growth factor-alpha receptor-positive oligodendroglia are frequent in multiple sclerosis lesions Ann Neurol 49 2001 776 785
49. J.B. Grinspan, U.R. Reddy, J.L. Stern, M. Hardy, M. Williams, L. Baird, and D. Pleasure Oligodendroglia express PDGF beta-receptor protein and are stimulated to proliferate by PDGF Ann N Y Acad Sci 605 1990 71 80
50. J. Krupinski, R. Issa, T. Bujny, M. Slevin, P. Kumar, S. Kumar, and J. Kaluza A putative role for platelet-derived growth factor in angiogenesis and neuroprotection after ischemic stroke in humans Stroke 28 1997 564 573
51. A. Nakamura-Ishizu, T. Kurihara, Y. Okuno, Y. Ozawa, K. Kishi, N. Goda, K. Tsubota, H. Okano, T. Suda, and Y. Kubota The formation of an angiogenic astrocyte template is regulated by the neuroretina in a HIF-1-dependent manner Dev Biol 363 2012 106 114
52. H.H. Wang, H.L. Hsieh, and C.M. Yang Calmodulin kinase II-dependent transactivation of PDGF receptors mediates astrocytic MMP-9 expression and cell motility induced by lipoteichoic acid J Neuroinflammation 7 2010 84
53. I. Nazarenko, A. Hedren, H. Sjodin, A. Orrego, J. Andrae, G.B. Afink, M. Nister, and M.S. Lindstrom Brain abnormalities and glioma-like lesions in mice overexpressing the long isoform of PDGF-A in astrocytic cells PLoS One 6 2011 e18303
54. X. Zhang, and A. Neufeld Activation of the epidermal growth factor receptor in optic nerve astrocytes leads to early and transient induction of cyclooxygenase-2 Invest Opthamol Vis Sci 46 2005 2035 2041
55. B. Liu, H. Chen, T. Johns, and A. Neufeld Epidermal growth factor receptor activation: an upstream signal for transition of quiescent astrocytes into reactive astrocytes after injury J Neurosc 26 2006 7532 7540
56. G. Mundy Metastasis to the bone: causes, consequences and therapeutic opportunities Nat Cancer Rev 2 2002 584 593
57. K.A. Olaussen, F. Commo, M. Tailler, L. Lacroix, I. Vitale, S.Q. Raza, C. Richon, P. Dessen, V. Lazar, J.C. Soria, and G. Kroemer Synergistic proapoptotic effects of the two tyrosine kinase inhibitors pazopanib and lapatinib on multiple carcinoma cell lines Oncogene 28 2009 4249 4260
58. D. Marchetti, J. Li, and R. Shen Astrocytes contribute to the brain-metastatic specificity of melanoma cells by producing heparanase Cancer Res 60 2000 4767 4770
59. A.F. Samdani, E.B. Kuchner, L. Rhines, D.C. Adamson, C. Lawson, B. Tyler, H. Brem, V.L. Dawson, and T.M. Dawson Astroglia induce cytotoxic effects on brain tumors via a nitric oxide-dependent pathway both in vitro and in vivo Neurosurgery 54 2004 1231 1237 discussion 1237-1238
60. A. Sierra, J. Price, M. Garcia-Ramirez, O. Mendez, L. Lopez, and A. Fabra Astrocyte derived cytokines contribute to the metastatic brain specificity of breast cancer cells Lab Invest 77 1997 357 368
61. M. Zhang, and Y. Olsson Reactions of astrocytes and microglial cells around hematogenous metastases of the human brain. Expression of endothelin-like immunoreactivity in reactive astrocytes and action of microglial cells J Neurol Sci 134 1995 26 32
62. P.A. Prieto, J.C. Yang, R.M. Sherry, M.S. Hughes, U.S. Kammula, D.E. White, C.L. Levy, S.A. Rosenberg, and G.Q. Phan CTLA-4 blockade with ipilimumab: long-term follow-up of 177 patients with metastatic melanoma Clin Cancer Res 18 2012 2039 2047
63. A. Kruger, O.H. Sanchez-Sweatman, D.C. Martin, J.E. Fata, A.T. Ho, F.W. Orr, U. Ruther, and R. Khokha Host TIMP-1 overexpression confers resistance to experimental brain metastasis of a fibrosarcoma cell line Oncogene 16 1998 2419 2423
64. C. Maillard, C. Bouquet, M. Petitjean, M. Mesdagt, E. Frau, M. Jost, A. Masset, P. Opolon, F. Beermann, M. Abitbol, J. Foidart, M. Perricaudet, and A. Noel Reduction of brain metastases in plasminogen activator inhibitor-1 deficient mice with transgenic ocular tumors Carcinogenesis 29 2008 2236 2242
65. D. Marchetti, and G. Nicolson Human haparanase: a molecular determinant of brain metastasis Advan Enzyme Regul 41 2001 343 359
66. D.P. Fitzgerald, D.L. Emerson, Y. Qian, T. Anwar, D.J. Liewehr, S.M. Steinberg, S. Silberman, D. Palmieri, and P.S. Steeg TPI-287, a new taxane family member, reduces the brain metastatic colonization of breast cancer cells Mol Cancer Ther 11 2012 1959 1967
67. Y. Qian, E. Hua, K. Bisht, S. Woditschka, K.W. Skordos, D.J. Liewehr, S.M. Steinberg, E. Brogi, M.M. Akram, J.K. Killian, D.C. Edelman, M. Pineda, S. Scurci, Y.Y. Degenhardt, S. Laquerre, T.A. Lampkin, P.S. Meltzer, K. Camphausen, P.S. Steeg, and D. Palmieri Inhibition of Polo-like kinase 1 prevents the growth of metastatic breast cancer cells in the brain Clin Experimental Metastasis 28 2011 899 908