Extracellular matrix signatures of human mammary carcinoma identify novel metastasis promoters

eLife

Volumn 2014, Issue 3, 2014, Pages

  Naba, Alexandra ^a   Clauser, Karl R ^b   Lamar, John M ^a   Carr, Steven A ^b   Hynes, Richard O ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BIOLOGICAL MARKER; COLLAGEN TYPE 1; CYSTEINE RICH PROTEIN 61; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; MESSENGER RNA; PROTEIN S 100; SCLEROPROTEIN; TENASCIN; TRANSFERRIN RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR PROMOTER; VASCULOTROPIN; PROTEOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOMA; CANCER GROWTH; CANCER PROGNOSIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; FLUORESCENCE MICROSCOPY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; LUNG METASTASIS; MASS SPECTROMETRY; METASTASIS POTENTIAL; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR SOLUBILIZATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR CELL; TUMOR XENOGRAFT; ANIMAL; BREAST TUMOR; CHEMISTRY; DISEASE MODEL; KNOCKOUT MOUSE; METASTASIS; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; SECONDARY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; BIOMARKERS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; HETEROGRAFTS; HUMANS; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; NEOPLASM METASTASIS; PROTEOME;

EID: 84898766031     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01308     Document Type: Article

References (59)

1. Anastassiades OT, Pryce DM. 1974. Fibrosis as in indication of time in infiltrating breast cancer and its importance in prognosis. British Journal of Cancer 29:232-239. doi: 10.1038/bjc.1974.62.
2. Barry-Hamilton V, Spangler R, Marshall D, McCauley S, Rodriguez HM, Oyasu M, Mikels A, Vaysberg M, Ghermazien H, Wai C, Garcia CA, Velayo AC, Jorgensen B, Biermann D, Tsai D, Green J, Zaffryar-Eilot S, Holzer A, Ogg S, Thai D, Neufeld G, Van Vlasselaer P, Smith V. 2010. Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nature Medicine 16:1009-1017. doi: 10.1038/nm.2208.
3. Bergamaschi A, Tagliabue E, Sørlie T, Naume B, Triulzi T, Orlandi R, Russnes HG, Nesland JM, Tammi R, Auvinen P, Kosma VM, Ménard S, Børresen-Dale AL. 2008. Extracellular matrix signature identifies breast cancer subgroups with different clinical outcome. Journal of Pathology 214:357-367. doi: 10.1002/path.2278.
4. Berra E, Benizri E, Ginouvès A, Volmat V, Roux D, Pouysségur J. 2003. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. The EMBO Journal 22:4082-4090. doi: 10.1093/emboj/cdg392.
5. Boudreau A, van't Veer LJ, Bissell MJ. 2012. An "elite hacker": breast tumors exploit the normal microenvironment program to instruct their progression and biological diversity. Cell Adhesion & Migration 6:236-248. doi: 10.4161/cam.20880.
6. Bulk E, Sargin B, Krug U, Hascher A, Jun Y, Knop M, Kerkhoff C, Gerke V, Liersch R, Mesters RM, Hotfilder M, Marra A, Koschmieder S, Dugas M, Berdel WE, Serve H, Müller-Tidow C. 2009. S100A2 induces metastasis in non-small cell lung cancer. Clinical Cancer Research 15:22-29. doi: 10.1158/1078-0432.CCR-08-0953.
7. Cailleau R, Olivé M, Cruciger QV. 1978. Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization. In Vitro 14:911-915. doi: 10.1007/BF02616120.
8. Chauhan VP, Stylianopoulos T, Boucher Y, Jain RK. 2011. Delivery of molecular and nanoscale medicine to tumors: transport barriers and strategies. Annual Review of Chemical and Biomolecular Engineering 2:281-298. doi: 10.1146/annurev-chembioeng-061010-114300.
9. Chen Y, Dabovic B, Annes JP, Rifkin DB. 2002. Latent TGF-beta binding protein-3 (LTBP-3) requires binding to TGF-beta for secretion. FEBS Letters 517:277-280. doi: 10.1016/S0014-5793(02)02648-0.
10. Comen EA. 2012. Tracking the seed and tending the soil: evolving concepts in metastatic breast cancer. Discovery Medicine 14:97-104.
11. Conklin MW, Keely PJ. 2012. Why the stroma matters in breast cancer. Cell Adhesion & Migration 6:249-260. doi: 10.4161/cam.20567.
12. Conklin MW, Eickhoff JC, Riching KM, Pehlke CA, Eliceiri KW, Provenzano PP, Friedl A, Keely PJ. 2011. Aligned collagen is a prognostic signature for survival in human breast carcinoma. American Journal of Pathology 178:1221-1232. doi: 10.1016/j.ajpath.2010.11.076.
13. Curran CS, Keely PJ. 2013. Breast tumor and stromal cell responses to TGF-β and hypoxia in matrix deposition. Matrix Biology 32:95-105. doi: 10.1016/j.matbio.2012.11.016.
14. Dvorak HF, Weaver VM, Tlsty TD, Bergers G. 2011. Tumor microenvironment and progression. Journal of Surgical Oncology 103:468-474. doi: 10.1002/jso.21709.
15. Egeblad M, Nakasone ES, Werb Z. 2010. Tumors as organs: complex tissues that interface with the entire organism. Developmental Cell 18:884-901. doi: 10.1016/j.devcel.2010.05.012.
16. Erler JT, Weaver VM. 2009. Three-dimensional context regulation of metastasis. Clinical & Experimental Metastasis 26:35-49. doi: 10.1007/s10585-008-9209-8.
17. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, Chen H, Omeroglu G, Meterissian S, Omeroglu A, Hallett M, Park M. 2008. Stromal gene expression predicts clinical outcome in breast cancer. Nature Medicine 14:518-527. doi: 10.1038/nm1764.
18. Fordyce CA, Patten KT, Fessenden TB, Defilippis R, Hwang ES, Zhao J, Tlsty TD. 2012. Cell-extrinsic consequences of epithelial stress: activation of protumorigenic tissue phenotypes. Breast Cancer Research 14:R155. doi: 10.1186/bcr3368.
19. Geiger B, Yamada KM. 2011. Molecular architecture and function of matrix adhesions. Cold Spring Harbor Perspectives in Biology 3:a005033. doi: 10.1101/cshperspect.a005033.
20. Gillette MA, Carr SA. 2013. Quantitative analysis of peptides and proteins in biomedicine by targeted mass spectrometry. Nature Methods 10:28-34. doi: 10.1038/nmeth.2309.
21. Goodman SL, Picard M. 2012. Integrins as therapeutic targets. Trends in Pharmacological Sciences 33:405-412. doi: 10.1016/j.tips.2012.04.002.
22. Gygi SP, Rochon Y, Franza BR, Aebersold R. 1999. Correlation between protein and mRNA abundance in yeast. Molecular and Cellular Biology 119:1720-1730.
23. Györffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, Szallasi Z. 2010. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Research and Treatment 123:725-731. doi: 10.1007/s10549-009-0674-9.
24. Hynes RO. 2002. Integrins: bidirectional, allosteric signaling machines. Cell 110:673-687. doi: 10.1016/S0092-8674(02)00971-6.
25. Hynes RO. 2009. The extracellular matrix: not just pretty fibrils. Science 326:1216-1219. doi: 10.1126/science.1176009.
26. Hynes RO, Naba A. 2012. Overview of the matrisome-an inventory of extracellular matrix constituents and functions. Cold Spring Harbor Perspectives in Biology 4:a004903. doi: 10.1101/cshperspect.a004903.
27. Jacobetz MA, Chan DS, Neesse A, Bapiro TE, Cook N, Frese KK, Feig C, Nakagawa T, Caldwell ME, Zecchini HI, Lolkema MP, Jiang P, Kultti A, Thompson CB, Maneval DC, Jodrell DI, Frost GI, Shepard HM, Skepper JN, Tuveson DA. 2013. Hyaluronan impairs vascular function and drug delivery in a mouse model of pancreatic cancer. Gut 62:112-120. doi: 10.1136/gutjnl-2012-302529.
28. Joyce JA, Pollard JW. 2009. Microenvironmental regulation of metastasis. Nature Reviews Cancer 9:239-252. doi: 10.1038/nrc2618.
29. Klotzsche-von Ameln A, Muschter A, Mamlouk S, Kalucka J, Prade I, Franke K, Rezaei M, Poitz DM, Breier G, Wielockx B. 2011. Inhibition of HIF prolyl hydroxylase-2 blocks tumor growth in mice through the antiproliferative activity of TGFβ. Cancer Research 71:3306-3316. doi: 10.1158/0008-5472.CAN-10-3838.
30. Korpal M, Ell BJ, Buffa FM, Ibrahim T, Blanco MA, Celià-Terrassa T, Mercatali L, Khan Z, Goodarzi H, Hua Y, Wei Y, Hu G, Garcia BA, Ragoussis J, Amadori D, Harris AL, Kang Y. 2011. Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization. Nature Medicine 17:1101-1108. doi: 10.1038/nm.2401.
31. Lamar JM, Stern P, Liu H, Schindler JW, Jiang Z-G, Hynes RO. 2012. The Hippo pathway target, YAP, promotes metastasis through its TEAD-interaction domain. Proceedings of the National Academy of Sciences of the United States of America 109:E2441-E2450. doi: 10.1073/pnas.1212021109.
32. Lamprecht MR, Sabatini DM, Carpenter AE. 2007. CellProfiler: free, versatile software for automated biological image analysis. Biotechniques 42:71-75. doi: 10.2144/000112257.
33. Leimeister C, Schumacher N, Diez H, Gessler M. 2004. Cloning and expression analysis of the mouse stroma marker Snep encoding a novel nidogen domain protein. Developmental Dynamics 230:371-377. doi: 10.1002/dvdy.20056.
34. Massague J. 2012. TGFβ signalling in context. Nature Reviews Molecular Cell Biology 13:616-630. doi: 10.1038/nrm3434.
35. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J. 2005. Genes that mediate breast cancer metastasis to lung. Nature 436:518-524. doi: 10.1038/nature03799.
36. Minn AJ, Gupta GP, Padua D, Bos P, Nguyen DX, Nuyten D, Kreike B, Zhang Y, Wang Y, Ishwaran H, Foekens JA, van de Vijver M, Massagué J. 2007. Lung metastasis genes couple breast tumor size and metastatic spread. Proceedings of the National Academy of Sciences of the United States of America 104:6740-6745. doi: 10.1073/pnas.0701138104.
37. Munger JS, Sheppard D. 2011. Cross talk among TGF-β signaling pathways, integrins, and the extracellular matrix. Cold Spring Harbor Perspectives Biology 3:a005017. doi: 10.1101/cshperspect.a005017.
38. Naba A, Clauser KR, Hoersch S, Liu H, Carr SA, Hynes RO. 2012. The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Molecular and Cellular Proteomics 11:M111.014647. doi: 10.1074/mcp.M111.014647.
39. Padua D, Massagué J. 2009. Roles of TGFbeta in metastasis. Cell Research 19:89-102. doi: 10.1038/cr.2008.316.
40. Padua D, Zhang XH-F, Wang Q, Nadal C, Gerald WL, Gomis RR, Massagué J. 2008. TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133:66-77. doi: 10.1016/j.cell.2008.01.046.
41. Paget S. 1889. The distribution of secondary growths in cancer of the breast. The Lancet 133:571-573. doi: 10.1016/S0140-6736(00)49915-0.
42. Pasche N, Neri D. 2012. Immunocytokines: a novel class of potent armed antibodies. Drug Discovery Today 17:583-590. doi: 10.1016/j.drudis.2012.01.007.
43. Polyak K, Haviv I, Campbell IG. 2009. Co-evolution of tumor cells and their microenvironment. Trends in Genetics 25:30-38. doi: 10.1016/j.tig.2008.10.012.
44. Ramirez F, Rifkin DB. 2009. Extracellular microfibrils: contextual platforms for TGFbeta and BMP signaling. Current Opinion In Cell Biology 21:616-622. doi: 10.1016/j.ceb.2009.05.005.
45. Rappsilber J, Ishihama Y, Mann M. 2003. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Analytical Chemistry 75:663-670. doi: 10.1021/ac026117i.
46. Ribatti D, Mangialardi G, Vacca A. 2006. Stephen Paget and the "seed and soil" theory of metastatic dissemination. Clinical and Experimental Medicine 6:145-149. doi: 10.1007/s10238-006-0117-4.
47. Ryan AJ, Napoletano S, Fitzpatrick PA, Currid CA, O'Sullivan NC, Harmey JH. 2009. Expression of a protease-resistant insulin-like growth factor-binding protein-4 inhibits tumour growth in a murine model of breast cancer. British Journal of Cancer 101:278-286. doi: 10.1038/sj.bjc.6605141.
48. Sevenich L, Schurigt U, Sachse K, Gajda M, Werner F, Müller S, Vasiljeva O, Schwinde A, Klemm N, Deussing J, Peters C, Reinheckel T. 2010. Synergistic antitumor effects of combined cathepsin B and cathepsin Z deficiencies on breast cancer progression and metastasis in mice. Proceedings of the National Academy of Sciences of the United States of America 107:2497-2502. doi: 10.1073/pnas.0907240107.
49. Sevenich L, Werner F, Gajda M, Schurigt U, Sieber C, Müller S, Follo M, Peters C, Reinheckel T. 2011. Transgenic expression of human cathepsin B promotes progression and metastasis of polyoma-middle-T-induced breast cancer in mice. Oncogene 30:54-64. doi: 10.1038/onc.2010.387.
50. Stern P, Astrof S, Erkeland SJ, Schustak J, Sharp PA, Hynes RO. 2008. A system for Cre-regulated RNA interference in vivo. Proceedings of the National Academy of Sciences of the United States of America 105:13895-13900. doi: 10.1073/pnas.0806907105.
51. Tchou J, Kossenkov AV, Chang L, Satija C, Herlyn M, Showe LC, Puré E. 2012. Human breast cancer associated fibroblasts exhibit subtype specific gene expression profiles. BMC Medical Genomics 5:39. doi: 10.1186/1755-8794-5-39.
52. Tlsty TD, Coussens LM. 2006. Tumor stroma and regulation of cancer development. Annual Review of Pathology 1:119-150. doi: 10.1146/annurev.pathol.1.110304.100224.
53. Todorovic V, Rifkin DB. 2012. LTBPs, more than just an escort service. Journal of Cellular Biochemistry 113:410-418. doi: 10.1002/jcb.23385.
54. Tsai MS, Hornby AE, Lakins J, Lupu R. 2000. Expression and function of CYR61, an angiogenic factor, in breast cancer cell lines and tumor biopsies. Cancer Research 60:5603-5607.
55. Tsai M-S, Bogart DF, Li P, Mehmi I, Lupu R. 2002. Expression and regulation of Cyr61 in human breast cancer cell lines. Oncogene 21:964-973. doi: 10.1038/sj.onc.1205131.
56. Vasiljeva O, Papazoglou A, Krüger A, Brodoefel H, Korovin M, Deussing J, Augustin N, Nielsen BS, Almholt K, Bogyo M, Peters C, Reinheckel T. 2006. Tumor cell-derived and macrophage-derived cathepsin B promotes progression and lung metastasis of mammary cancer. Cancer Research 66:5242-5250. doi: 10.1158/0008-5472.CAN-05-4463.
57. Whatcott CJ, Han H, Posner RG, Hostetter G, Von Hoff DD. 2011. Targeting the tumor microenvironment in cancer: why hyaluronidase deserves a second look. Cancer Discovery 1:291-296. doi: 10.1158/2159-8290.CD-11-0136.
58. Wilson R. 2010. The extracellular matrix: an underexplored but important proteome. Expert Review of Proteomics 7:803-806. doi: 10.1586/epr.10.93.
59. Yuan L, Siegel M, Choi K, Khosla C, Miller CR, Jackson EN, Piwnica-Worms D, Rich KM. 2007. Transglutaminase 2 inhibitor, KCC009, disrupts fibronectin assembly in the extracellular matrix and sensitizes orthotopic glioblastomas to chemotherapy. Oncogene 26:2563-2573. doi: 10.1038/sj.onc.1210048.