Quantitative extracellular matrix proteomics to study mammary and liver tissue microenvironments

International Journal of Biochemistry and Cell Biology

Volumn 81, Issue , 2016, Pages 223-232

  Goddard, Erica T ^a   Hill, Ryan C ^b   Barrett, Alexander ^b   Betts, Courtney ^a   Guo, Qiuchen ^a   Maller, Ori ^c   Borges, Virginia F ^b,d,e   Hansen, Kirk C ^b   Schedin, Pepper ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF COLORADO CANCER CENTER   (United States)

Author keywords

Breast cancer; Extracellular matrix; Liver; Liver metastasis; Mammary gland; Mass spectrometry proteomics

Indexed keywords

PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CHEMICAL COMPOSITION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; MASS SPECTROMETRY; METASTASIS; MOUSE; NONHUMAN; OVARY CYCLE; PROTEOMICS; QUANTITATIVE ANALYSIS; TUMOR MICROENVIRONMENT; ANIMAL; CYTOLOGY; LIVER; METABOLISM; RAT; REPRODUCTION; SPRAGUE DAWLEY RAT; UDDER;

ANIMALS; CELLULAR MICROENVIRONMENT; EXTRACELLULAR MATRIX; FEMALE; LIVER; MAMMARY GLANDS, ANIMAL; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCTION;

EID: 85002125744     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2016.10.014     Document Type: Article

References (78)

1. Aggeler, J., Park, C.S., Bissell, M.J., Regulation of milk protein and basement membrane gene expression: the influence of the extracellular matrix. J. Dairy Sci. 71 (1988), 2830–2842.
2. Baiocchini, A., et al. Extracellular matrix molecular remodeling in human liver fibrosis evolution. PLoS One, 11, 2016, e0151736.
3. Barcellos-Hoff, M.H., Aggeler, J., Ram, T.G., Bissell, M.J., Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Dev. (Cambridge, Engl.) 105 (1989), 223–235.
4. Barkan, D., et al. Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment. Cancer Res. 70 (2010), 5706–5716.
5. Bemis, L.T., Schedin, P., Reproductive state of rat mammary gland stroma modulates human breast cancer cell migration and invasion. Cancer Res. 60 (2000), 3414–3418.
6. Berman, A.T., Thukral, A.D., Hwang, W.T., Solin, L.J., Vapiwala, N., Incidence and patterns of distant metastases for patients with early-stage breast cancer after breast conservation treatment. Clin. Breast Cancer 13 (2013), 88–94.
7. Bissell, M.J., Barcellos-Hoff, M.H., The influence of extracellular matrix on gene expression: is structure the message?. J. Cell Sci. Suppl. 8 (1987), 327–343.
8. Boyd, N.F., et al. Mammographic densities and breast cancer risk. Breast Dis. 10 (1998), 113–126.
9. Burnier, J.V., et al. Type IV collagen-initiated signals provide survival and growth cues required for liver metastasis. Oncogene 30 (2011), 3766–3783.
10. Callihan, E.B., et al. Postpartum diagnosis demonstrates a high risk for metastasis and merits an expanded definition of pregnancy-associated breast cancer. Breast Cancer Res. Treat. 138 (2013), 549–559.
11. Chu, M.L., et al. The structure of type VI collagen. Ann. N. Y. Acad. Sci. 580 (1990), 55–63.
12. Costa-Silva, B., et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat. Cell Biol. 17 (2015), 816–826.
13. Cummings, M.C., et al. Metastatic progression of breast cancer: insights from 50 years of autopsies. J. Pathol. 232 (2014), 23–31.
14. Da Costa, G.G., et al. Comparative proteomics of tumor and paired normal Breast tissue highlights potential biomarkers in Breast cancer. Cancer Genom. Proteom. 12 (2015), 251–261.
15. Dennis, G. Jr., et al. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol., 4, 2003, P3.
16. Didangelos, A., et al. Proteomics characterization of extracellular space components in the human aorta. Mol. Cell. Proteom. 9 (2010), 2048–2062.
17. DuFort, C.C., Paszek, M.J., Weaver, V.M., Balancing forces: architectural control of mechanotransduction. Nat. Rev. Mol. Cell Biol. 12 (2011), 308–319.
18. Erler, J.T., et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15 (2009), 35–44.
19. Fata, J.E., Werb, Z., Bissell, M.J., Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast Cancer Res.: BCR 6 (2004), 1–11.
20. Fischbach, C., et al. Engineering tumors with 3D scaffolds. Nat. Methods 4 (2007), 855–860.
21. Geiger, T., et al. Initial quantitative proteomic map of 28 mouse tissues using the SILAC mouse. Mol. Cell. Proteom. 12 (2013), 9–1722.
22. Ghajar, C.M., et al. The perivascular niche regulates breast tumour dormancy. Nat. Cell Biol. 15 (2013), 807–817.
23. Goto, R., Nakamura, Y., Takami, T., Sanke, T., Tozuka, Z., Quantitative LC–MS/MS analysis of proteins involved in metastasis of Breast cancer. PLoS One, 10, 2015, e0130760.
24. Hancox, R.A., et al. Tumour-associated tenascin-C isoforms promote breast cancer cell invasion and growth by matrix metalloproteinase-dependent and independent mechanisms. Breast Cancer Res., 11, 2009, R24.
25. Hansen, K.C., et al. An in-solution ultrasonication-assisted digestion method for improved extracellular matrix proteome coverage. Mol. Cell. Proteom. 8 (2009), 1648–1657.
26. Harrell, J.C., et al. Genomic analysis identifies unique signatures predictive of brain, lung, and liver relapse. Breast Cancer Res. Treat. 132 (2012), 523–535.
27. Hattar, R., et al. Tamoxifen induces pleiotrophic changes in mammary stroma resulting in extracellular matrix that suppresses transformed phenotypes. Breast Cancer Res., 11, 2009, R5.
28. Hill, R.C., Calle, E.A., Dzieciatkowska, M., Niklason, L.E., Hansen, K.C., Quantification of extracellular matrix proteins from a rat lung scaffold to provide a molecular readout for tissue engineering. Mol. Cell. Proteom., 2015.
29. Howlett, A.R., Bissell, M.J., The influence of tissue microenvironment (stroma and extracellular matrix) on the development and function of mammary epithelium. Epithelial Cell Biol. 2 (1993), 79–89.
30. Ioachim, E., et al. Immunohistochemical expression of extracellular matrix components tenascin, fibronectin, collagen type IV and laminin in breast cancer: their prognostic value and role in tumour invasion and progression. Eur. J. Cancer 38 (2002), 2362–2370.
31. Iyengar, P., et al. Adipocyte-derived collagen VI affects early mammary tumor progression in vivo, demonstrating a critical interaction in the tumor/stroma microenvironment. J. Clin. Invest. 115 (2005), 1163–1176.
32. Johansson, A.L., Andersson, T.M., Hsieh, C.C., Cnattingius, S., Lambe, M., Increased mortality in women with breast cancer detected during pregnancy and different periods postpartum. Cancer Epidemiol. Biomark. Prev. 20 (2011), 1865–1872.
33. Johnson, T.D., et al. Quantification of decellularized human myocardial matrix: a comparison of six patients. Proteom. Clin. Appl. 10 (2016), 75–83.
34. Kaplan, R.N., et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438 (2005), 0820–827.
35. Karagiannis, G.S., et al. Proteomic signatures of the desmoplastic invasion front reveal collagen type XII as a marker of myofibroblastic differentiation during colorectal cancer metastasis. Oncotarget 3 (2012), 267–285.
36. Krause, S., Maffini, M.V., Soto, A.M., Sonnenschein, C., A novel 3D in vitro culture model to study stromal-epithelial interactions in the mammary gland. Tissue Eng. Part C Methods 14 (2008), 261–271.
37. Lai, K.K., Kolippakkam, D., Beretta, L., Comprehensive and quantitative proteome profiling of the mouse liver and plasma. Hepatology 47 (2008), 1043–1051.
38. Lai, K.K., et al. Extracellular matrix dynamics in hepatocarcinogenesis: a comparative proteomics study of PDGFC transgenic and Pten null mouse models. PLoS Genet., 7, 2011, e1002147.
39. Lee, G.Y., Kenny, P.A., Lee, E.H., Bissell, M.J., Three- dimensional culture models of normal and malignant breast epithelial cells. Nat. Methods 4 (2007), 359–365.
40. Levental, K.R., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139 (2009), 891–906.
41. Li, T., et al. The association of measured breast tissue characteristics with mammographic density and other risk factors for breast cancer. Cancer Epidemiol. Biomark. Prev. 14 (2005), 343–349.
42. Lund, L.R., et al. Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and -dependent pathways. Development 122 (1996), 181–193.
43. Luzzi, K.J., et al. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am. J. Pathol. 153 (1998), 865–873.
44. Lyons, T.R., et al. Postpartum mammary gland involution drives progression of ductal carcinoma in situ through collagen and COX-2. Nat. Med. 17 (2011), 1109–1115.
45. MacLean, B., et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26 (2010), 966–968.
46. Maity, G., et al. Culture of human breast cancer cell line (MDA-MB-231) on fibronectin-coated surface induces pro-matrix metalloproteinase-9 expression and activity. Tumour Biol. 32 (2011), 129–138.
47. Malanchi, I., et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481 (2012), 85–89.
48. Maller, O., et al. Collagen architecture in pregnancy-induced protection from breast cancer. J. Cell Sci. 126 (2013), 4108–4110.
49. Martinson, H.A., Jindal, S., Durand-Rougely, C., Borges, V.F., Schedin, P., Wound healing-like immune program facilitates postpartum mammary gland involution and tumor progression. Int. J. Cancer, 2014.
50. McDaniel, S.M., et al. Remodeling of the mammary microenvironment after lactation promotes breast tumor cell metastasis. Am. J. Pathol. 168 (2006), 608–620.
51. Moreira, J.M., et al. Tissue proteomics of the human mammary gland: towards an abridged definition of the molecular phenotypes underlying epithelial normalcy. Mol. Oncol. 4 (2010), 539–561.
52. Mouw, J.K., Ou, G., Weaver, V.M., Extracellular matrix assembly: a multiscale deconstruction. Nat. Rev. Mol. Cell Biol. 15 (2014), 771–785.
53. Naba, A., et al. Extracellular matrix signatures of human primary metastatic colon cancers and their metastases to liver. BMC Cancer, 14, 2014, 518.
54. Naba, A., Clauser, K.R., Lamar, J.M., Carr, S.A., Hynes, R.O., Extracellular matrix signatures of human mammary carcinoma identify novel metastasis promoters. Elife, 3, 2014, e01308.
55. Nelson, C.M., Vanduijn, M.M., Inman, J.L., Fletcher, D.A., Bissell, M.J., Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Sci. (New York, N.Y.) 314 (2006), 298–300.
56. Nguyen-Ngoc, K.V., et al. ECM microenvironment regulates collective migration and local dissemination in normal and malignant mammary epithelium. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), E2595–E2604.
57. O'Brien, J., et al. Alternatively activated macrophages and collagen remodeling characterize the postpartum involuting mammary gland across species. Am. J. Pathol. 176 (2010), 1241–1255.
58. O'Brien, J.H., Vanderlinden, L.A., Schedin, P.J., Hansen, K.C., Rat mammary extracellular matrix composition and response to ibuprofen treatment during postpartum involution by differential GeLC–MS/MS analysis. J. Proteome Res. 11 (2012), 4894–4905.
59. Oskarsson, T., et al. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat. Med. 17 (2011), 867–874.
60. Pratt, J.M., et al. Multiplexed absolute quantification for proteomics using concatenated signature peptides encoded by QconCAT genes. Nat. Protoc. 1 (2006), 1029–1043.
61. Provenzano, P.P., et al. Collagen density promotes mammary tumor initiation and progression. BMC Med., 6, 2008, 11.
62. Savci-Heijink, C.D., et al. Retrospective analysis of metastatic behaviour of breast cancer subtypes. Breast Cancer Res. Treat. 150 (2015), 547–557.
63. Schedin, P., Keely, P.J., Mammary gland ECM remodeling, stiffness, and mechanosignaling in normal development and tumor progression. Cold Spring Harb. Perspect. Biol., 3, 2011, a003228.
64. Schedin, P., Mitrenga, T., McDaniel, S., Kaeck, M., Mammary ECM composition and function are altered by reproductive state. Mol. Carcinog. 41 (2004), 207–220.
65. Schedin, P., Pregnancy- associated breast cancer and metastasis. Nat. Rev. Cancer 6 (2006), 281–291.
66. Schmeichel, K.L., Weaver, V.M., Bissell, M.J., Structural cues from the tissue microenvironment are essential determinants of the human mammary epithelial cell phenotype. J. Mammary Gland Biol. Neoplasia 3 (1998), 201–213.
67. Shaw, K.R., Wrobel, C.N., Brugge, J.S., Use of three-dimensional basement membrane cultures to model oncogene-induced changes in mammary epithelial morphogenesis. J. Mammary Gland Biol. Neoplasia 9 (2004), 297–310.
68. Stensheim, H., Moller, B., van Dijk, T., Fossa, S.D., Cause- specific survival for women diagnosed with cancer during pregnancy or lactation: a registry-based cohort study. J. Clin. Oncol. 27 (2009), 45–51.
69. Streuli, C.H., Bailey, N., Bissell, M.J., Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell–cell interaction and morphological polarity. J. Cell Biol. 115 (1991), 1383–1395.
70. Tarhan, M.O., et al. The clinicopathological evaluation of the breast cancer patients with brain metastases: predictors of survival. Clin. Exp. Metastasis 30 (2013), 201–213.
71. Tseng, L.M., et al. Distant metastasis in triple-negative breast cancer. Neoplasma 60 (2013), 290–294.
72. Weigelt, B., Ghajar, C.M., Bissell, M.J., The need for complex 3D culture models to unravel novel pathways and identify accurate biomarkers in breast cancer. Adv. Drug Deliv. Rev. 69–70 (2014), 42–51.
73. Werb, Z., et al. Extracellular matrix remodeling and the regulation of epithelial-stromal interactions during differentiation and involution. Kidney Int. 54 (1996), S68–74.
74. Wyld, L., et al. Prognostic factors for patients with hepatic metastases from breast cancer. Br. J. Cancer 89 (2003), 284–290.
75. Xia, J., Sinelnikov, B., Wishart, D.S., MetaboAnalyst 3. 0 – making metabolomics more meaningful. Nucleic Acids Res. 43 (2015), W251–W257.
76. Yee, K.O., et al. The effect of thrombospondin-1 on breast cancer metastasis. Breast Cancer Res. Treat. 114 (2009), 85–96.
77. Yen, T.Y., et al. Using a cell line breast cancer progression system to identify biomarker candidates. J. Proteom. 96 (2014), 173–183.
78. Zhang, H., et al. Galectin-3 as a marker and potential therapeutic target in breast cancer. PLoS One, 9, 2014, e103482.