Analysis of tumour- and stroma-supplied proteolytic networks reveals a brain-metastasis-promoting role for cathepsin S

Nature Cell Biology

Volumn 16, Issue 9, 2014, Pages 876-888

  Sevenich, Lisa ^a   Bowman, Robert L ^a   Mason, Steven D ^a   Quail, Daniela F ^a   Rapaport, Franck ^a   Elie, Benelita T ^a   Brogi, Edi ^a   Brastianos, Priscilla K ^b,c   Hahn, William C ^b   Holsinger, Leslie J ^d   Massagué, Joan ^a   Leslie, Christina S ^a   Joyce, Johanna A ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d Virobay Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN S; CD68 ANTIGEN; CYTOKERATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BONE METASTASIS; BRAIN METASTASIS; CANCER CELL; CELL INTERACTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; GENE EXPRESSION; HUMAN; HUMAN CELL; LUNG METASTASIS; MACROPHAGE; METASTASIS FREE SURVIVAL; METASTASIS POTENTIAL; METASTATIC BREAST CANCER; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; STROMA CELL; TROPISM; TUMOR MICROENVIRONMENT;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOOD-BRAIN BARRIER; BONE NEOPLASMS; BRAIN NEOPLASMS; BREAST NEOPLASMS; CATHEPSINS; CELL LINE, TUMOR; CELL MOVEMENT; CYSTATINS; DISEASE-FREE SURVIVAL; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, NUDE; MICE, SCID; ORGAN SPECIFICITY; PROTEASE INHIBITORS; PROTEOLYSIS; SERPINS; TIGHT JUNCTION PROTEINS; TUMOR MARKERS, BIOLOGICAL; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84908118492     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3011     Document Type: Article

References (49)

1. Quail, D. F. & Joyce, J. A. Microenvironmental regulation of tumor progression and metastasis. Nat. Med. 19, 1423-1437 (2013).
2. Nguyen, D. X., Bos, P. D. & Massague, J. Metastasis: from dissemination to organspecific colonization. Nat. Rev. Cancer 9, 274-284 (2009).
3. Goss, P. E. & Chambers, A. F. Does tumour dormancy offer a therapeutic target? Nat. Rev. Cancer 10, 871-877 (2010).
4. Affara, N. I., Andreu, P. & Coussens, L. M. Delineating protease functions during cancer development. Methods Mol. Biol. 539, 1-32 (2009).
5. Mason, S. D. & Joyce, J. A. Proteolytic networks in cancer. Trends Cell Biol. 21, 228-237 (2011).
6. Gocheva, V. et al. Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes Dev. 20, 543-556 (2006).
7. Murphy, G. The ADAMs: signalling scissors in the tumour microenvironment. Nat. Rev. Cancer 8, 929-941 (2008).
8. Butler, G. S. & Overall, C. M. Proteomic identification of multitasking proteins in unexpected locations complicates drug targeting. Nat. Rev. Drug Discov. 8, 935-948 (2009).
9. Lopez-Otin, C. & Hunter, T. The regulatory crosstalk between kinases and proteases in cancer. Nat. Rev. Cancer 10, 278-292 (2010).
10. Kessenbrock, K., Plaks, V. & Werb, Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141, 52-67 (2010).
11. Allinen, M. et al. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 6, 17-32 (2004).
12. Finak, G. et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat. Med. 14, 518-527 (2008).
13. Erez, N., Truitt, M., Olson, P., Arron, S. T. & Hanahan, D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-κB-dependent manner. Cancer Cell 17, 135-147 (2010).
14. Katz, A. M. et al. Astrocyte-specific expression patterns associated with the PDGF-induced glioma microenvironment. PLoS ONE 7, e32453 (2012).
15. Seaman, S. et al. Genes that distinguish physiological and pathological angiogenesis. Cancer Cell 11, 539-554 (2007).
16. Ojalvo, L. S., and Whittaker., C. A., Condeelis, J. S. & Pollard, J. W. Gene expression analysis of macrophages that facilitate tumor invasion supports a role for Wntsignaling in mediating their activity in primary mammary tumors. J. Immunol. 184, 702-712 (2010).
17. Paget, S. The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev. 8, 98-101 (1989).
18. Disibio, G. & French, S. W. Metastatic patterns of cancers: results from a large autopsy study. Arch. Pathol. Lab. Med. 132, 931-939 (2008).
19. Lee, Y. T. Breast carcinoma: pattern of metastasis at autopsy. J. Surg. Oncol. 23, 175-180 (1983).
20. Bos, P. D. et al. Genes that mediate breast cancer metastasis to the brain. Nature 459, 1005-1009 (2009).
21. Kang, Y. et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537-549 (2003).
22. Minn, A. J. et al. Genes that mediate breast cancer metastasis to lung. Nature 436, 518-524 (2005).
23. Schwartz, D. R. et al. Hu/Mu ProtIn oligonucleotide microarray: dual-species array for profiling protease and protease inhibitor gene expression in tumors and their microenvironment. Mol. Cancer Res. 5, 443-454 (2007).
24. Ponomarev, V. et al. A novel triple-modality reporter gene for whole-body fluorescent, bioluminescent, and nuclear noninvasive imaging. Eur. J. Nucl. Med. Mol. Imaging 31, 740-751 (2004).
25. Shi, G. P. et al. Cathepsin S required for normal MHC class II peptide loading and germinal center development. Immunity 10, 197-206 (1999).
26. Lorger, M. & Felding-Habermann, B. Capturing changes in the brain microenvironment during initial steps of breast cancer brain metastasis. Am. J. Pathol. 176, 2958-2971 (2010).
27. Small, D. M. et al. Cathepsin S from both tumor and tumor-associated cells promote cancer growth and neovascularization. Int. J. Cancer 133, 2102-2112 (2013).
28. Abbott, N. J., Ronnback, L. & Hansson, E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41-53 (2006).
29. Eugenin, E. A. & Berman, J. W. Chemokine-dependent mechanisms of leukocyte trafficking across a model of the blood-brain barrier. Methods 29, 351-361 (2003).
30. Jia, W., and Martin., T. A., Zhang, G. & Jiang, W. G. Junctional adhesion molecules in cerebral endothelial tight junction and brain metastasis. Anticancer Res. 33, 2353-2359 (2013).
31. Liu, W. Y., and Wang., Z. B., Zhang, L. C., Wei, X. & Li, L. Tight junction in blood-brain barrier: an overview of structure, regulation, and regulator substances. CNS Neurosci. Ther. 18, 609-615 (2012).
32. Gallagher, F. A. et al. Magnetic resonance imaging of pH in vivo using hyperpolarized 13C-labelled bicarbonate. Nature 453, 940-943 (2008).
33. Kirschke, H., Wiederanders, B., Bromme, D. & Rinne, A. Cathepsin S from bovine spleen. Purification, distribution, intracellular localization and action on proteins. Biochem. J. 264, 467-473 (1989).
34. Nolan, D. J. et al. Molecular signatures of tissue-specific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev. Cell 26, 204-219 (2013).
35. Choe, Y. et al. Substrate profiling of cysteine proteases using a combinatorial peptide library identifies functionally unique specificities. J. Biol. Chem. 281, 12824-12832 (2006).
36. Oliveira, M. et al. Improvement of cathepsin S detection using a designed FRET peptide based on putative natural substrates. Peptides 31, 562-567 (2010).
37. Biniossek, M. L., and Nagler., D. K., Becker-Pauly, C. & Schilling, O. Proteomic identification of protease cleavage sites characterizes prime and non-prime specificity of cysteine cathepsins B, L, and S. J. Proteome Res. 10, 5363-5373 (2011).
38. Oskarsson, T. et al. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat. Med. 17, 867-874 (2011).
39. Chapman, H. A. Endosomal proteases in antigen presentation. Curr. Opin. Immunol. 18, 78-84 (2006).
40. Gupta, S., and Singh., R. K., Dastidar, S. & Ray, A. Cysteine cathepsin S as an immunomodulatory target: present and future trends. Expert Opin. Ther. Targets 12, 291-299 (2008).
41. Madsen, C. D. & Sahai, E. Cancer dissemination-lessons from leukocytes. Dev. Cell 19, 13-26 (2010).
42. Steeg, P. S., Camphausen, K. A. & Smith, Q. R. Brain metastases as preventive and therapeutic targets. Nat. Rev. Cancer 11, 352-363 (2011).
43. Eichler, A. F. et al. The biology of brain metastases-translation to new therapies. Nat. Rev. Clin. Oncol. 8, 344-356 (2011).
44. Park, E. S. et al. Cross-species hybridization of microarrays for studying tumor transcriptome of brain metastasis. Proc. Natl Acad. Sci. USA 108, 17456-17461 (2011).
45. Turk, B. Targeting proteases: successes, failures and future prospects. Nat. Rev. Drug Discov. 5, 785-799 (2006).
46. Palermo, C. & Joyce, J. A. Cysteine cathepsin proteases as pharmacological targets in cancer. Trends Pharmacol. Sci. 29, 22-28 (2008).
47. Drag, M. & Salvesen, G. S. Emerging principles in protease-based drug discovery. Nat. Rev. Drug Discov. 9, 690-701 (2010).
48. Fingleton, B. Matrix metalloproteinases as valid clinical targets. Curr. Pharm. Des. 13, 333-346 (2007).
49. Seidah, N. G. & Prat, A. The biology and therapeutic targeting of the proprotein convertases. Nat. Rev. Drug Discov. 11, 367-383 (2012).