Roles of the cyclooxygenase 2 matrix metalloproteinase 1 pathway in brain metastasis of breast cancer

Journal of Biological Chemistry

Volumn 290, Issue 15, 2015, Pages 9842-9854

  Wu, Kerui ^a   Fukuda, Koji ^c   Xing, Fei ^a   Zhang, Yingyu ^b   Sharma, Sambad ^a   Liu, Yin ^a   Chan, Michael D ^a   Zhou, Xiaobo ^a   Qasem, Shadi A ^a   Pochampally, Radhika ^b   Mo, Yin Yuan ^b   Watabe, Kounosuke ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^c KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; BLOOD VESSELS; CELL CULTURE; CELLS; CYTOLOGY; DISEASES; PATHOLOGY; TUMORS;

BLOOD-BRAIN BARRIER; BRAIN METASTASIS; CENTRAL NERVOUS SYSTEMS; ECTOPIC EXPRESSIONS; MATRIX METALLOPROTEINASE-1; MATRIX METALLOPROTEINASES; SELECTIVE INTERFACES; THERAPEUTIC TARGETS;

ENZYME INHIBITION;

CLAUDIN; CYCLOOXYGENASE 2; INTERSTITIAL COLLAGENASE; MONOCYTE CHEMOTACTIC PROTEIN 3; OCCLUDIN; PROSTAGLANDIN; PROTEIN ZO1; CCR7 PROTEIN, HUMAN; CHEMOKINE RECEPTOR CCR7;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN CELL; BRAIN METASTASIS; BREAST CANCER; CANCER STEM CELL; CELL ACTIVATION; CELL RENEWAL; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG TARGETING; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO STUDY; METASTASIS FREE SURVIVAL; METASTASIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BRAIN TUMOR; BREAST TUMOR; CANCER TRANSPLANTATION; DNA MICROARRAY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECONDARY; SURVIVAL ANALYSIS; TUMOR CELL LINE; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN NEOPLASMS; BREAST NEOPLASMS; CELL LINE, TUMOR; CYCLOOXYGENASE 2; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MATRIX METALLOPROTEINASE 1; MICE, NUDE; NEOPLASM TRANSPLANTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, CCR7; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84927156917     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.602185     Document Type: Article

References (59)

1. Cheng, X., and Hung, M. C. (2007) Breast cancer brain metastases. Cancer Metastasis Rev. 26, 635-643
2. Abbott, N. J., Patabendige, A. A., Dolman, D. E., Yusof, S. R., and Begley, D. J. (2010) Structure and function of the blood-brain barrier. Neurobiol. Dis. 37, 13-25
3. Abbott, N. J., Rönnbäck, L., and Hansson, E. (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41-53
4. Dejana, E. (2004) Endothelial cell-cell junctions: happy together. Nat. Rev. Mol. Cell Biol. 5, 261-270
5. Liebner, S., Kniesel, U., Kalbacher, H., and Wolburg, H. (2000) Correlation of tight junction morphology with the expression of tight junction proteins in blood-brain barrier endothelial cells. Eur. J. Cell Biol. 79, 707-717
6. Fanning, A. S., Jameson, B. J., Jesaitis, L. A., and Anderson, J. M. (1998) The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J. Biol. Chem. 273, 29745-29753
7. Latorre, I. J., Roh, M. H., Frese, K. K., Weiss, R. S., Margolis, B., and Javier, R. T. (2005) Viral oncoprotein-induced mislocalization of select PDZ proteins disrupts tight junctions and causes polarity defects in epithelial cells. J. Cell Sci. 118, 4283-4293
8. Fedwick, J. P., Lapointe, T. K., Meddings, J. B., Sherman, P. M., and Buret, A. G. (2005) Helicobacter pylori activates myosin light-chain kinase to disrupt claudin-4 and claudin-5 and increase epithelial permeability. Infect. Immun. 73, 7844-7852
9. Feng, S., Huang, Y., and Chen, Z. (2011) Does VEGF secreted by leukemic cells increase the permeability of blood-brain barrier by disrupting tightjunction proteins in central nervous system leukemia? Med. Hypotheses 76, 618-621
10. Romero, I. A., Radewicz, K., Jubin, E., Michel, C. C., Greenwood, J., Couraud, P. O., and Adamson, P. (2003) Changes in cytoskeletal and tight junctional proteins correlate with decreased permeability induced by dexamethasone in cultured rat brain endothelial cells. Neurosci. Lett. 344, 112-116
11. Poola, I., DeWitty, R. L., Marshalleck, J. J., Bhatnagar, R., Abraham, J., and Leffall, L. D. (2005) Identification of MMP-1 as a putative breast cancer predictive marker by global gene expression analysis. Nat. Med. 11, 481-483
12. Minn, A. J., Gupta, G. P., Siegel, P. M., Bos, P. D., Shu, W., Giri, D. D., Viale, A., Olshen, A. B., Gerald, W. L., and Massagué, J. (2005) Genes that mediate breast cancer metastasis to lung. Nature 436, 518-524
13. Gupta, G. P., Nguyen, D. X., Chiang, A. C., Bos, P. D., Kim, J. Y., Nadal, C., Gomis, R. R., Manova-Todorova, K., and Massagué, J. (2007) Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 446, 765-770
14. Laningham, F. H., Kun, L. E., Reddick, W. E., Ogg, R. J., Morris, E. B., and Pui, C. H. (2007) Childhood central nervous system leukemia: historical perspectives, current therapy, and acute neurological sequelae. Neuroradiology 49, 873-888
15. Ii, M., Yamamoto, H., Adachi, Y., Maruyama, Y., and Shinomura, Y. (2006) Role of matrix metalloproteinase-7 (matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis. Exp. Biol. Med. (Maywood) 231, 20-27
16. Greenwald, R. A. (1999) Thirty-six years in the clinic without an MMP inhibitor. What hath collagenase wrought? Ann. N.Y. Acad. Sci. 878, 413-419
17. Asahi, M., Wang, X., Mori, T., Sumii, T., Jung, J. C., Moskowitz, M. A., Fini, M. E., and Lo, E. H. (2001) Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J. Neurosci. 21, 7724-7732
18. Cunnea, P., McMahon, J., O'Connell, E., Mashayekhi, K., Fitzgerald, U., and McQuaid, S. (2010) Gene expression analysis of the microvascular compartment in multiple sclerosis using laser microdissected blood vessels. Acta Neuropathol. 119, 601-615
19. Yang, Y., Estrada, E. Y., Thompson, J. F., Liu, W., and Rosenberg, G. A. (2007) Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J. Cereb. Blood Flow Metab. 27, 697-709
20. Bauer, A. T., Bürgers, H. F., Rabie, T., and Marti, H. H. (2010) Matrix metalloproteinase-9 mediates hypoxia-induced vascular leakage in the brain via tight junction rearrangement. J. Cereb. Blood Flow Metab. 30, 837-848
21. Hirase, T., Staddon, J. M., Saitou, M., Ando-Akatsuka, Y., Itoh, M., Furuse, M., Fujimoto, K., Tsukita, S., and Rubin, L. L. (1997) Occludin as a possible determinant of tight junction permeability in endothelial cells. J. Cell Sci. 110, 1603-1613
22. Gurney, K. J., Estrada, E. Y., and Rosenberg, G. A. (2006) Blood-brain barrier disruption by stromelysin-1 facilitates neutrophil infiltration in neuroinflammation. Neurobiol. Dis. 23, 87-96
23. Giebel, S. J., Menicucci, G., McGuire, P. G., and Das, A. (2005) Matrix metalloproteinases in early diabetic retinopathy and their role in alteration of the blood-retinal barrier. Lab. invest. 85, 597-607
24. Liu, J., Jin, X., Liu, K. J., and Liu, W. (2012) Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage. J. Neurosci. 32, 3044-3057
25. Zlokovic, B. V. (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57, 178-201
26. Mendes, O., Kim, H. T., Lungu, G., and Stoica, G. (2007) MMP2 role in breast cancer brain metastasis development and its regulation by TIMP2 and ERK1/2. Clin. Exp. Metastasis 24, 341-351
27. Liu, S., Clouthier, S. G., and Wicha, M. S. (2012) Role of microRNAs in the regulation of breast cancer stem cells. J. Mammary Gland Biol. Neoplasia 17, 15-21
28. Oskarsson, T., Batlle, E., and Massagué, J. (2014) Metastatic stem cells: sources, niches, and vital pathways. Cell Stem Cell 14, 306-321
29. Valiente, M., Obenauf, A. C., Jin, X., Chen, Q., Zhang, X. H., Lee, D. J., Chaft, J. E., Kris, M. G., Huse, J. T., Brogi, E., and Massagué, J. (2014) Serpins promote cancer cell survival and vascular co-option in brain metastasis. Cell 156, 1002-1016
30. Greenhough, A., Smartt, H. J., Moore, A. E., Roberts, H. R., Williams, A. C., Paraskeva, C., and Kaidi, A. (2009) The COX-2/PGE2 pathway: key roles in the hallmarks of cancer and adaptation to the tumour microenvironment. Carcinogenesis 30, 377-386
31. Li, H. J., Reinhardt, F., Herschman, H. R., and Weinberg, R. A. (2012) Cancer-stimulated mesenchymal stem cells create a carcinoma stem cell niche via prostaglandin E2 signaling. Cancer Discov. 2, 840-855
32. Honn, K. V., Bockman, R. S., and Marnett, L. J. (1981) Prostaglandins and cancer: a review of tumor initiation through tumor metastasis. Prostaglandins 21, 833-864
33. Xing, F., Kobayashi, A., Okuda, H., Watabe, M., Pai, S. K., Pandey, P. R., Hirota, S., Wilber, A., Mo, Y. Y., Moore, B. E., Liu, W., Fukuda, K., Iiizumi, M., Sharma, S., Liu, Y., Wu, K., Peralta, E., and Watabe, K. (2013) Reactive astrocytes promote the metastatic growth of breast cancer stem-like cells by activating Notch signalling in brain. EMBO Mol. Med. 5, 384-396
34. Rajaram, M., Li, J., Egeblad, M., and Powers, R. S. (2013) System-wide analysis reveals a complex network of tumor-fibroblast interactions involved in tumorigenicity. PLoS Genet. 9, e1003789
35. Louie, E., Chen, X. F., Coomes, A., Ji, K., Tsirka, S., and Chen, E. I. (2013) Neurotrophin-3 modulates breast cancer cells and the microenvironment to promote the growth of breast cancer brain metastasis. Oncogene 32, 4064-4077
36. Quail, D. F., and Joyce, J. A. (2013) Microenvironmental regulation of tumor progression and metastasis. Nat. Med. 19, 1423-1437
37. Ohtsuki, S., Sato, S., Yamaguchi, H., Kamoi, M., Asashima, T., and Terasaki, T. (2007) Exogenous expression of claudin-5 induces barrier properties in cultured rat brain capillary endothelial cells. J. Cell. Physiol. 210, 81-86
38. Nitta, T., Hata, M., Gotoh, S., Seo, Y., Sasaki, H., Hashimoto, N., Furuse, M., and Tsukita, S. (2003) Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J. Cell Biol. 161, 653-660
39. Furuse, M., Hirase, T., Itoh, M., Nagafuchi, A., Yonemura, S., Tsukita, S., and Tsukita, S. (1993) Occludin: a novel integral membrane protein localizing at tight junctions. J. Cell Biol. 123, 1777-1788
40. Ohtsuki, S., Yamaguchi, H., Katsukura, Y., Asashima, T., and Terasaki, T. (2008) mRNA expression levels of tight junction protein genes in mouse brain capillary endothelial cells highly purified by magnetic cell sorting. J. Neurochem. 104, 147-154
41. Wachtel, M., Frei, K., Ehler, E., Fontana, A., Winterhalter, K., and Gloor, S. M. (1999) Occludin proteolysis and increased permeability in endothelial cells through tyrosine phosphatase inhibition. J. Cell Sci. 112, 4347-4356
42. Benson, C. S., Babu, S. D., Radhakrishna, S., Selvamurugan, N., and Ravi Sankar, B. (2013) Expression of matrix metalloproteinases in human breast cancer tissues. Dis. Markers 34, 395-405
43. Sternlicht, M. D., Lochter, A., Sympson, C. J., Huey, B., Rougier, J. P., Gray, J. W., Pinkel, D., Bissell, M. J., and Werb, Z. (1999) The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 98, 137-146
44. Bertucci, F., Nasser, V., Granjeaud, S., Eisinger, F., Adelaïde, J., Tagett, R., Loriod, B., Giaconia, A., Benziane, A., Devilard, E., Jacquemier, J., Viens, P., Nguyen, C., Birnbaum, D., and Houlgatte, R. (2002) Gene expression profiles of poor-prognosis primary breast cancer correlate with survival. Hum. Mol. Genet. 11, 863-872
45. Lu, X., Wang, Q., Hu, G., Van Poznak, C., Fleisher, M., Reiss, M., Massagué, J., Kang, Y. (2009) ADAMTS1 and MMP1 proteolytically engage EGF-like ligands in an osteolytic signaling cascade for bone metastasis. Genes Dev. 23, 1882-1894
46. Bos, P. D., Zhang, X. H., Nadal, C., Shu, W., Gomis, R. R., Nguyen, D. X., Minn, A. J., van de Vijver, M. J., Gerald, W. L., Foekens, J. A., and Massagué, J. (2009) Genes that mediate breast cancer metastasis to the brain. Nature 459, 1005-1009
47. Liu, H., Kato, Y., Erzinger, S. A., Kiriakova, G. M., Qian, Y., Palmieri, D., Steeg, P. S., and Price, J. E. (2012) The role of MMP-1 in breast cancer growth and metastasis to the brain in a xenograft model. BMC Cancer 12, 583
48. Heinecke, J. L., Ridnour, L. A., Cheng, R. Y., Switzer, C. H., Lizardo, M. M., Khanna, C., Glynn, S. A., Hussain S. P., Young, H. A., Ambs, S., Wink, D. A. (2014) Tumor microenvironment-based feed-forward regulation of NOS2 in breast cancer progression. Proc. Natl. Acad. Sci. U.S.A. 111, 6323-6328
49. Reel, B., Sala-Newby, G. B., Huang, W. C., and Newby, A. C. (2011) Diverse patterns of cyclooxygenase-independent metalloproteinase gene regulation in human monocytes. Br. J. Pharmacol. 163, 1679-1690
50. Lee, K. Y., Kim, Y. J., Yoo, H., Lee, S. H., Park, J. B., and Kim, H. J. (2011) Human brain endothelial cell-derived COX-2 facilitates extravasation of breast cancer cells across the blood-brain barrier. Anticancer Res. 31, 4307-4313
51. Ichikawa, Y., Ishikawa, T., Momiyama, N., Kamiyama, M., Sakurada, H., Matsuyama, R., Hasegawa, S., Chishima, T., Hamaguchi, Y., Fujii, S., Saito, S., Kubota, K., Hasegawa, S., Ike, H., Oki, S., and Shimada, H. (2006) Matrilysin (MMP-7) degrades VE-cadherin and accelerates accumulation of β-catenin in the nucleus of human umbilical vein endothelial cells. Oncol. Rep. 15, 311-315
52. Shuman Moss, L. A., Jensen-Taubman, S., and Stetler-Stevenson, W. G. (2012) Matrix metalloproteinases: changing roles in tumor progression and metastasis. Am. J. Pathol. 181, 1895-1899
53. Nguyen, D. X., Bos, P. D., and Massagué, J. (2009) Metastasis: from dissemination to organ-specific colonization. Nat. Rev. Cancer 9, 274-284
54. Schenk, S., Mal, N., Finan, A., Zhang, M., Kiedrowski, M., Popovic, Z., McCarthy, P. M., and Penn, M. S. (2007) Monocyte chemotactic protein-3 is a myocardial mesenchymal stem cell homing factor. Stem Cells 25, 245-251
55. Vande Broek, I., Asosingh, K., Vanderkerken, K., Straetmans, N., Van Camp, B., and Van Riet, I. (2003) Chemokine receptor CCR2 is expressed by human multiple myeloma cells and mediates migration to bone mar-row stromal cell-produced monocyte chemotactic proteins MCP-1, -2, and -3. Br. J. Cancer 88, 855-862
56. Jung, D. W., Che, Z. M., Kim, J., Kim, K., Kim, K. Y., Williams, D., and Kim, J. (2010) Tumor-stromal crosstalk in invasion of oral squamous cell carcinoma: a pivotal role of CCL7. Int. J. Cancer 127, 332-344
57. Hwang, T. L., Lee, L. Y., Wang, C. C., Liang, Y., Huang, S. F., and Wu, C. M. (2012) CCL7 and CCL21 overexpression in gastric cancer is associated with lymph node metastasis and poor prognosis. World J. Gastroenterol. 18, 1249-1256
58. Ong, V. H., Carulli, M. T., Xu, S., Khan, K., Lindahl, G., Abraham, D. J., and Denton, C. P. (2009) Cross-talk between MCP-3 and TGFβ promotes fibroblast collagen biosynthesis. Exp. Cell Res. 315, 151-161
59. Armstrong, L., Hughes, O., Yung, S., Hyslop, L., Stewart, R., Wappler, I., Peters, H., Walter, T., Stojkovic, P., Evans, J., Stojkovic, M., and Lako, M. (2006) The role of PI3K/AKT, MAPK/ERK and NFκβ signalling in the maintenance of human embryonic stem cell pluripotency and viability highlighted by transcriptional profiling and functional analysis. Hum. Mol. Genet. 15, 1894-1913