The extracellular matrix: Tools and insights for the "omics" era

Matrix Biology

Volumn 49, Issue , 2016, Pages 10-24

  Naba, Alexandra ^a   Clauser, Karl R ^b   Ding, Huiming ^a   Whittaker, Charles A ^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

Bioinformatics; ECM atlas; Extracellular matrix; Matrisome; MatrisomeDB; Proteomics

Indexed keywords

BIOLOGICAL MARKER; CELL PROTEIN; SCLEROPROTEIN;

BIOINFORMATICS; COMPUTER MODEL; DATA BASE; EXTRACELLULAR MATRIX; HUMAN; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; NORMAL HUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEOMICS; REGENERATIVE MEDICINE; REVIEW; SOLUBILIZATION; ANIMAL; ANTIBODY SPECIFICITY; BIOLOGY; INTERNET; METABOLISM; NEOPLASM; PROCEDURES; PROTEIN DATABASE;

ANIMALS; COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; HUMANS; INTERNET; NEOPLASMS; ORGAN SPECIFICITY; PROTEOMICS;

EID: 84957860866     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2015.06.003     Document Type: Review

References (97)

1. Humphrey J.D., Dufresne E.R., Schwartz M.A. Mechanotransduction and extracellular matrix homeostasis. Nat. Rev. Mol. Cell Biol. 2014, 15:802-812. 10.1038/nrm3896.
2. Hynes R.O. The extracellular matrix: not just pretty fibrils. Science 2009, 326:1216-1219. 10.1126/science.1176009.
3. Huttenlocher A., Horwitz A.R. Integrins in cell migration. Cold Spring Harb. Perspect. Biol. 2011, 3:a005074. 10.1101/cshperspect.a005074.
4. Charras G., Sahai E. Physical influences of the extracellular environment on cell migration. Nat. Rev. Mol. Cell Biol. 2014, 10.1038/nrm3897.
5. Ingber D.E. Extracellular matrix: a solid-state regulator of cell form, function, and tissue development. Comprehensive Physiology 2011, 541-556.
6. Campbell I.D., Humphries M.J. Integrin structure, activation, and interactions. Cold Spring Harb. Perspect. Biol. 2011, 10.1101/cshperspect.a004994.
7. Rozario T., DeSimone D.W. The extracellular matrix in development and morphogenesis: a dynamic view. Dev. Biol. 2010, 341:126-140. 10.1016/j.ydbio.2009.10.026.
8. Wickström S.A., Radovanac K., Fässler R. Genetic analyses of integrin signaling. Cold Spring Harb. Perspect. Biol. 2011, 10.1101/cshperspect.a005116.
9. Hynes R.O. The evolution of metazoan extracellular matrix. J. Cell Biol. 2012, 196:671-679. 10.1083/jcb.201109041.
10. Evolution of Extracellular Matrix 2013, Springer, Berlin, Heidelberg. F.W. Keeley, R.P. Mecham (Eds.).
11. Bateman J.F., Boot-Handford R.P., Lamandé S.R. Genetic diseases of connective tissues: cellular and extracellular effects of ECM mutations. Nat. Rev. Genet. 2009, 10:173-183. 10.1038/nrg2520.
12. Bonnans C., Chou J., Werb Z. Remodelling the extracellular matrix in development and disease. Nat. Rev. Mol. Cell Biol. 2014, 15:786-801. 10.1038/nrm3904.
13. Naba A., Clauser K.R., Lamar J.M., et al. Extracellular matrix signatures of human mammary carcinoma identify novel metastasis promoters. eLife 2014, 10.7554/eLife.01308.
14. Pickup M.W., Mouw J.K., Weaver V.M. The extracellular matrix modulates the hallmarks of cancer. EMBO Rep. 2014, 15:1243-1253. 10.15252/embr.201439246.
15. Martin G.R., Kleinman H.K., Terranova V.P., et al. The regulation of basement membrane formation and cell-matrix interactions by defined supramolecular complexes. Ciba Found. Symp. 1984, 108:197-212.
16. Naba A., Clauser K.R., Hoersch S., et al. The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Mol. Cell. Proteomics 2012, 11. (M111.014647). 10.1074/mcp.M111.014647.
17. Naba A., Hoersch S., Hynes R.O. Towards definition of an ECM parts list: an advance on GO categories. Matrix Biol. 2012, 31:371-372. 10.1016/j.matbio.2012.11.008.
18. Hynes R.O., Naba A. Overview of the matrisome-an inventory of extracellular matrix constituents and functions. Cold Spring Harb. Perspect. Biol. 2012, 10.1101/cshperspect.a004903.
19. Hohenester E., Engel J. Domain structure and organisation in extracellular matrix proteins. Matrix Biol. 2002, 21:115-128. 10.1016/S0945-053X(01)00191-3.
20. Extracellular Matrix Biology., Cold Spring Harbor Perspectives in Biology 2012, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. R.O. Hynes, K.M. Yamada (Eds.).
21. Iozzo R.V., Schaefer L. Proteoglycan form and function: a comprehensive nomenclature of proteoglycans. Matrix Biol. 2015, 42:11-55. 10.1016/j.matbio.2015.02.003.
22. Mecham R. The Extracellular Matrix: an Overview 2011, Springer Science & Business Media.
23. Consortium TU UniProt: a hub for protein information. Nucleic Acids Res. 2015, 43:D204-D212. 10.1093/nar/gku989.
24. Mitchell A., Chang H.-Y., Daugherty L., et al. The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res. 2015, 43:D213-D221. 10.1093/nar/gku1243.
25. Schultz J., Milpetz F., Bork P., Ponting C.P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. 1998, 95:5857-5864.
26. Letunic I., Doerks T., Bork P. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 2015, 43:D257-D260. 10.1093/nar/gku949.
27. Maglott D., Ostell J., Pruitt K.D., Tatusova T. Entrez Gene: gene-centered information at NCBI. Nucleic Acids Res. 2011, 39:D52-D57. 10.1093/nar/gkq1237.
28. Tagliabracci V.S., Engel J.L., Wen J., et al. Secreted kinase phosphorylates extracellular proteins that regulate biomineralization. Science 2012, 336:1150-1153. 10.1126/science.1217817.
29. Naba A., Ding H., Whittaker C.A., Hynes R.O. http://matrisomeproject.mit.edu.
30. Gray K.A., Daugherty L.C., Gordon S.M., et al. Genenames.org: the HGNC resources in 2013. Nucleic Acids Res. 2013, 41:D545-D552. 10.1093/nar/gks1066.
31. Jackson Laboratories Mouse Genome Informatics website. http://www.informatics.jax.org/.
32. Liberzon A. A description of the Molecular Signatures Database (MSigDB) web site. Methods Mol. Biol. Clifton, NJ 2014, 1150:153-160. 10.1007/978-1-4939-0512-6_9.
33. Subramanian A., Tamayo P., Mootha V.K., et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. 2005, 102:15545-15550. 10.1073/pnas.0506580102.
34. Langlois B., Saupe F., Rupp T., et al. AngioMatrix, a signature of the tumor angiogenic switch-specific matrisome, correlates with poor prognosis for glioma and colorectal cancer patients. Oncotarget 2014, 5:10529-10545.
35. Chautard E., Ballut L., Thierry-Mieg N., Ricard-Blum S. MatrixDB, a database focused on extracellular protein-protein and protein-carbohydrate interactions. Bioinformatics 2009, 25:690-691. 10.1093/bioinformatics/btp025.
36. Launay G., Salza R., Multedo D., et al. MatrixDB, the extracellular matrix interaction database: updated content, a new navigator and expanded functionalities. Nucleic Acids Res. 2015, 43:D321-D327. 10.1093/nar/gku1091.
37. Naba A., Clauser K.R., Whittaker C.A., et al. Extracellular matrix signatures of human primary metastatic colon cancers and their metastases to liver. BMC Cancer 2014, 14:518. 10.1186/1471-2407-14-518.
38. Kapushesky M., Adamusiak T., Burdett T., et al. Gene Expression Atlas update-a value-added database of microarray and sequencing-based functional genomics experiments. Nucleic Acids Res. 2012, 40:D1077-D1081. 10.1093/nar/gkr913.
39. Petryszak R., Burdett T., Fiorelli B., et al. Expression Atlas update-a database of gene and transcript expression from microarray- and sequencing-based functional genomics experiments. Nucleic Acids Res. 2014, 42:D926-D932. 10.1093/nar/gkt1270.
40. Kim M.-S., Pinto S.M., Getnet D., et al. A draft map of the human proteome. Nature 2014, 509:575-581. 10.1038/nature13302.
41. Wilhelm M., Schlegl J., Hahne H., et al. Mass-spectrometry-based draft of the human proteome. Nature 2014, 509:582-587. 10.1038/nature13319.
42. Uhlén M., Fagerberg L., Hallström B.M., et al. Tissue-based map of the human proteome. Science 2015, 347:1260419. 10.1126/science.1260419.
43. Naba A., Clauser K.R., Hynes R.O. Enrichment of extracellular matrix proteins from tissues and digestion into peptides for mass spectrometry analysis. J. Vis. Exp. 2015, 10.3791/53057.
44. Barallobre-Barreiro J., Didangelos A., Yin X., et al. A sequential extraction methodology for cardiac extracellular matrix prior to proteomics analysis. Heart Proteomics 2013, 215-223. Humana Press, Totowa, NJ. F. Vivanco (Ed.).
45. Wilson R., Belluoccio D., Bateman J.F. Proteomic analysis of cartilage proteins. Methods 2008, 45:22-31. 10.1016/j.ymeth.2008.01.008.
46. Hansen K.C., Kiemele L., Maller O., et al. An in-solution ultrasonication-assisted digestion method for improved extracellular matrix proteome coverage. Mol. Cell. Proteomics 2009, 8:1648-1657. 10.1074/mcp.M900039-MCP200.
47. Myllyharju J. Intracellular post-translational modifications of collagens. Collagen 2005, 115-147. Springer Berlin Heidelberg. J. Brinckmann, H. Notbohm, P.K. Müller (Eds.).
48. Yamauchi M., Sricholpech M. Lysine post-translational modifications of collagen. Essays Biochem. 2012, 52:113-133. 10.1042/bse0520113.
49. Belluoccio D., Wilson R., Thornton D.J., et al. Proteomic analysis of mouse growth plate cartilage. Proteomics 2006, 6:6549-6553. 10.1002/pmic.200600191.
50. Schreiweis M.A., Butler J.P., Kulkarni N.H., et al. A proteomic analysis of adult rat bone reveals the presence of cartilage/chondrocyte markers. J. Cell. Biochem. 2007, 101:466-476. 10.1002/jcb.21196.
51. Balasubramani M., Schreiber E.M., Candiello J., et al. Molecular interactions in the retinal basement membrane system: a proteomic approach. Matrix Biol. 2010, 29:471-483. 10.1016/j.matbio.2010.04.002.
52. Didangelos A., Yin X., Mandal K., et al. Proteomics characterization of extracellular space components in the human aorta. Mol. Cell. Proteomics 2010, 9:2048-2062. 10.1074/mcp.M110.001693.
53. O'Brien J., Fornetti J., Schedin P. Isolation of mammary-specific extracellular matrix to assess acute cell-ECM interactions in 3D culture. J. Mammary Gland Biol. Neoplasia 2010, 15:353-364. 10.1007/s10911-010-9185-x.
54. Wilson R., Diseberg A.F., Gordon L., et al. Comprehensive profiling of cartilage extracellular matrix formation and maturation using sequential extraction and label-free quantitative proteomics. Mol. Cell. Proteomics 2010, 9:1296-1313. 10.1074/mcp.M000014-MCP201.
55. Didangelos A., Yin X., Mandal K., et al. Extracellular matrix composition and remodeling in human abdominal aortic aneurysms: a proteomics approach. Mol. Cell. Proteomics 2011, 10. (M111.008128). 10.1074/mcp.M111.008128.
56. Barallobre-Barreiro J., Didangelos A., Schoendube F.A., et al. Proteomics analysis of cardiac extracellular matrix remodeling in a porcine model of ischemia/reperfusion injury. Circulation 2012, 125:789-802. 10.1161/CIRCULATIONAHA.111.056952.
57. Booth A.J., Hadley R., Cornett A.M., et al. Acellular normal and fibrotic human lung matrices as a culture system for in vitro investigation. Am. J. Respir. Crit. Care Med. 2012, 186:866-876. 10.1164/rccm.201204-0754OC.
58. Önnerfjord P., Khabut A., Reinholt F.P., et al. Quantitative proteomic analysis of eight cartilaginous tissues reveals characteristic differences as well as similarities between subgroups. J. Biol. Chem. 2012, 287:18913-18924. 10.1074/jbc.M111.298968.
59. Decaris M.L., Gatmaitan M., FlorCruz S., et al. Proteomic analysis of altered extracellular matrix turnover in bleomycin-induced pulmonary fibrosis. Mol. Cell. Proteomics 2014, 13:1741-1752. 10.1074/mcp.M113.037267.
60. Lennon R., Byron A., Humphries J.D., et al. Global analysis reveals the complexity of the human glomerular extracellular matrix. J. Am. Soc. Nephrol. 2014, 25:939-951. 10.1681/ASN.2013030233.
61. Müller C., Khabut A., Dudhia J., et al. Quantitative proteomics at different depths in human articular cartilage reveals unique patterns of protein distribution. Matrix Biol. 2014, 40:34-45. 10.1016/j.matbio.2014.08.013.
62. Uechi G., Sun Z., Schreiber E.M., et al. Proteomic view of basement membranes from human retinal blood vessels, inner limiting membranes, and lens capsules. J. Proteome Res. 2014, 10.1021/pr5002065.
63. Hill R.C., Calle E.A., Dzieciatkowska M., et al. Quantification of extracellular matrix proteins from a rat lung scaffold to provide a molecular readout for tissue engineering. Mol. Cell. Proteomics MCP 2015, 14:961-973. 10.1074/mcp.M114.045260.
64. Hu J.C.-C., Yamakoshi Y., Yamakoshi F., et al. Proteomics and genetics of dental enamel. Cells Tissues Organs 2005, 181:219-231. 10.1159/000091383.
65. Zimmermann D.R., Dours-Zimmermann M.T. Extracellular matrix of the central nervous system: from neglect to challenge. Histochem. Cell Biol. 2008, 130:635-653. 10.1007/s00418-008-0485-9.
66. Barros C.S., Franco S.J., Müller U. Extracellular matrix: functions in the nervous system. Cold Spring Harb. Perspect. Biol. 2011, 10.1101/cshperspect.a005108.
67. Schwarzbauer J.E., DeSimone D.W. Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harb. Perspect. Biol. 2011, 10.1101/cshperspect.a005041.
68. Chiquet-Ehrismann R., Tucker R.P. Tenascins and the importance of adhesion modulation. Cold Spring Harb. Perspect. Biol. 2011, 10.1101/cshperspect.a004960.
69. Boja E.S., Rodriguez H. Mass spectrometry-based targeted quantitative proteomics: achieving sensitive and reproducible detection of proteins. Proteomics 2012, 12:1093-1110. 10.1002/pmic.201100387.
70. Carr S.A., Abbatiello S.E., Ackermann B.L., et al. Targeted peptide measurements in biology and medicine: best practices for mass spectrometry-based asay development using a fit-for-purpose approach. Mol. Cell. Proteomics 2014, 13:907-917. 10.1074/mcp.M113.036095.
71. Pontén F., Jirström K., Uhlen M. The Human Protein Atlas-a tool for pathology. J. Pathol. 2008, 216:387-393. 10.1002/path.2440.
72. Gillette M.A., Carr S.A. Quantitative analysis of peptides and proteins in biomedicine by targeted mass spectrometry. Nat. Methods 2013, 10:28-34. 10.1038/nmeth.2309.
73. Yalak G., Olsen B.R. Proteomic database mining opens up avenues utilizing extracellular protein phosphorylation for novel therapeutic applications. J. Transl. Med. 2015, 13:125. 10.1186/s12967-015-0482-4.
74. Sasisekharan R., Raman R., Prabhakar V. Glycomics approach to structure-function relationships of glycosaminoglycans. Annu. Rev. Biomed. Eng. 2006, 8:181-231. 10.1146/annurev.bioeng.8.061505.095745.
75. Lech M., Capila I., Kaundinya G.V. Mass spectrometric methods for the analysis of heparin and heparan sulfate. Methods Mol. Biol. Clifton NJ 2015, 1229:119-128. 10.1007/978-1-4939-1714-3_12.
76. Chiu Y., Huang R., Orlando R., Sharp J.S. GAG-ID: Heparan Sulfate and Heparin Glycosaminoglycan High-Throughput Identification Software. Mol. Cell. Proteomics MCP 2015, 10.1074/mcp.M114.045856.
77. Ricard-Blum S., Salza R. Matricryptins and matrikines: biologically active fragments of the extracellular matrix. Exp. Dermatol. 2014, 23:457-463. 10.1111/exd.12435.
78. Rogers L.D., Overall C.M. Proteolytic post-translational modification of proteins: proteomic tools and methodology. Mol. Cell. Proteomics 2013, 12:3532-3542. 10.1074/mcp.M113.031310.
79. Schlage P., Auf dem Keller U. Proteomic approaches to uncover MMP function. Matrix Biol. 2015, 44--46:232-238.
80. Santimaria M., Moscatelli G., Viale G.L., et al. Immunoscintigraphic detection of the ED-B domain of fibronectin, a marker of angiogenesis, in patients with cancer. Clin. Cancer Res. 2003, 9:571-579.
81. Pasche N., Neri D. Immunocytokines: a novel class of potent armed antibodies. Drug Discov. Today 2012, 17:583-590. 10.1016/j.drudis.2012.01.007.
82. Yao L., Lao W., Zhang Y., et al. Identification of EFEMP2 as a serum biomarker for the early detection of colorectal cancer with lectin affinity capture assisted secretome analysis of cultured fresh tissues. J. Proteome Res. 2012, 11:3281-3294. 10.1021/pr300020p.
83. Schierwagen R., Leeming D.J., Klein S., et al. Serum markers of the extracellular matrix remodeling reflect antifibrotic therapy in bile-duct ligated rats. Front. Physiol. 2013, 4:195. 10.3389/fphys.2013.00195.
84. Bunatova K., Pesta M., Kulda V., et al. Plasma TIMP1 level is a prognostic factor in patients with liver metastases. Anticancer Res. 2012, 32:4601-4606.
85. Goodman S.L., Picard M. Integrins as therapeutic targets. Trends Pharmacol. Sci. 2012, 33:405-412. 10.1016/j.tips.2012.04.002.
86. Estevez B., Shen B., Du X. Targeting integrin and integrin signaling in treating thrombosis. Arterioscler. Thromb. Vasc. Biol. 2015, 35:24-29. 10.1161/ATVBAHA.114.303411.
87. Vandenbroucke R.E., Libert C. Is there new hope for therapeutic matrix metalloproteinase inhibition?. Nat. Rev. Drug Discov. 2014, 13:904-927. 10.1038/nrd4390.
88. Järveläinen H., Sainio A., Koulu M., et al. Extracellular matrix molecules: potential targets in pharmacotherapy. Pharmacol. Rev. 2009, 61:198-223. 10.1124/pr.109.001289.
89. Dvir T., Timko B.P., Kohane D.S., Langer R. Nanotechnological strategies for engineering complex tissues. Nat. Nanotechnol. 2011, 6:13-22. 10.1038/nnano.2010.246.
90. Watt F.M., Huck W.T.S. Role of the extracellular matrix in regulating stem cell fate. Nat. Rev. Mol. Cell Biol. 2013, 14:467-473. 10.1038/nrm3620.
91. Gattazzo F., Urciuolo A., Bonaldo P. Extracellular matrix: a dynamic microenvironment for stem cell niche. Biochim. Biophys. Acta 2014, 1840:2506-2519. 10.1016/j.bbagen.2014.01.010.
92. Badylak S.F., Weiss D.J., Caplan A., Macchiarini P. Engineered whole organs and complex tissues. Lancet 2012, 379:943-952. 10.1016/S0140-6736(12)60073-7.
93. Faulk D.M., Johnson S.A., Zhang L., Badylak S.F. Role of the extracellular matrix in whole organ engineering. J. Cell. Physiol. 2014, 229:984-989. 10.1002/jcp.24532.
94. Bonvillain R.W., Danchuk S., Sullivan D.E., et al. A nonhuman primate model of lung regeneration: detergent-mediated decellularization and initial In vitro recellularization with mesenchymal stem cells. Tissue Eng. Part A 2012, 18:2437-2452. 10.1089/ten.tea.2011.0594.
95. Petersen T.H., Calle E.A., Zhao L., et al. Tissue-engineered lungs for in vivo implantation. Science 2010, 329:538-541. 10.1126/science.1189345.
96. Kyburz K.A., Anseth K.S. Synthetic mimics of the extracellular matrix: how simple is complex enough?. Ann. Biomed. Eng. 2015, 1-12. 10.1007/s10439-015-1297-4.
97. Hynes R.O. Stretching the boundaries of extracellular matrix research. Nat. Rev. Mol. Cell Biol. 2014, 15:761-763. 10.1038/nrm3908.