Quantitative proteomics reveals altered expression of extracellular matrix related proteins of human primary dermal fibroblasts in response to sulfated hyaluronan and collagen applied as artificial extracellular matrix

Journal of Materials Science: Materials in Medicine

Volumn 23, Issue 12, 2012, Pages 3053-3065

  Müller, Stephan A ^a,b   Van Der Smissen, Anja ^b,c   Von Feilitzsch, Margarete ^b,c   Anderegg, Ulf ^c   Kalkhof, Stefan ^a   Von Bergen, Martin ^a  

^a HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^b Matrixengineering ^*  (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTIFICIAL EXTRACELLULAR MATRIXES; COLLAGEN TYPE VI; DECORIN; DEGRADING ENZYMES; DERMAL FIBROBLASTS; EXTRACELLULAR MATRICES; EXTRACELLULAR MATRIX REMODELING; GROWTH SUBSTRATES; HYALURONAN; MATERIAL OPTIMIZATION; MATRIX METALLOPROTEINASES; MOLECULAR EFFECT; PROTEIN EXPRESSIONS; PROTEOMICS; QUANTITATIVE PROTEOMICS; SULFATED HYALURONAN; WOUND HEALING PROCESS;

CELL CULTURE; ENZYME INHIBITION; FIBROBLASTS; GLYCOPROTEINS; MOLECULAR BIOLOGY;

COLLAGEN;

CATHEPSIN K; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 12; COLLAGEN TYPE 6; DECORIN; GELATINASE A; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOPROTEIN; HYALURONIC ACID; MATRIX METALLOPROTEINASE 14; SCLEROPROTEIN; THROMBOSPONDIN 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

ARTICLE; ARTIFICIAL EXTRACELLULAR MATRIX; CONTROLLED STUDY; DERMIS; DOWN REGULATION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; SKIN FIBROBLAST; SULFATION; TROPHOBLAST; WOUND HEALING;

CATHEPSIN K; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; CLUSTER ANALYSIS; COLLAGEN; DERMIS; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 2; PROTEOMICS; SKIN; TANDEM MASS SPECTROMETRY; WOUND HEALING;

EID: 84871440401     PISSN: 09574530     EISSN: 15734838     Source Type: Journal    
DOI: 10.1007/s10856-012-4760-x     Document Type: Article

References (70)

1. Dieckmann C, Renner R, Milkova L, Simon JC. Regenerative medicine in dermatology: Biomaterials, tissue engineering, stem cells, gene transfer and beyond. Exp Dermatol. 2010;19(8):697-706. doi:10.1111/j.1600-0625.2010.01087.x.
2. Eisenbud D, Huang NF, Luke S, Silberklang M. Skin substitutes and wound healing: Current status and challenges. Wounds Compend Clin Res Pract. 2004;16(1):2-17. (Pubitemid 38253195)
3. Damanhuri M, Boyle J, Enoch S. Advances in tissue-engineered skin substitutes. Wounds Int. 2011;2(1):27-34.
4. Metcalfe AD, Ferguson MWJ. Bioengineering skin using mechanisms of regeneration and repair. Biomaterials. 2007;28(34): 5100-13. doi:10.1016/j.biomaterials.2007.07.031. (Pubitemid 47488488)
5. Gravante G, Delogu D, Giordan N, Morano G, Montone A, Esposito G. The use of hyalomatrix PA in the treatment of deep partial-thickness burns. J Burn Care Res. 2007;28(2):269-74. doi: 10.1097/bcr.0b013e318031a236. (Pubitemid 46411564)
6. Wainwright DJ. Use of an acellular allograft dermal matrix (alloderm) in the management of full-thickness burns. Burns. 1995; 21(4):243-8. doi:10.1016/0305-4179(95)93866-i.
7. Kumbar SG, Nukavarapu SP, James R, Nair LS, Laurencin CT. Electrospun poly(lactic acid-co-glycolic acid) scaffolds for skin tissue engineering. Biomaterials. 2008;29(30):4100-7. doi:10. 1016/j.biomaterials.2008.06.028.
8. Brown-Etris M, Cutshall WD, Hiles MC. A new biomaterial derived from small intestine submucosa and developed into a wound matrix device. Wounds Compend Clin Res Pract. 2002; 14(4):150-66. (Pubitemid 41505207)
9. Hintze V, Miron A, Moeller S, Schnabelrauch M, Wiesmann HP, Worch H, et al. Sulfated hyaluronan and chondroitin sulfate derivatives interact differently with human transforming growth factor-b1 (TGF-b1). Acta Biomater. 2012;8(6):2144-52. doi: 10.1016/j.actbio.2012.03.021.
10. Pichert A, Samsonov SA, Theisgen S, Thomas L, Baumann L, Schiller J, et al. Characterization of the interaction of interleukin-8 with hyaluronan, chondroitin sulfate, dermatan sulfate and their sulfated derivatives by spectroscopy and molecular modeling. Glycobiology. 2012;22(1):134-45. doi:10.1093/glycob/cwr120.
11. Barbucci R, Benvenuti M, Casolaro M, Lamponi S, Magnani A. Sulfated hyaluronic-acid as heparin-like material: Physicochemical and biological characterization. J Mater Sci Mater Med. 1994;5(11):830-3. doi:10.1007/ bf00213143.
12. Ye S, Luo Y, Lu W, Jones RB, Linhardt RJ, Capila I, et al. Structural basis for interaction of FGF-1, FGF-2, and FGF-7 with different heparan sulfate motifs. Biochemistry. 2001;40(48): 14429-39. (Pubitemid 33111725)
13. Capila I, Linhardt RJ. Heparin-protein interactions. Angew Chem Int Ed Engl. 2002;41(3):391-412.
14. Ramdin L, Perks B, Sheron N, Shute JK. Regulation of interleukin-8 binding and function by heparin and alpha 2-macroglobulin. Clin Exp Allergy. 1998;28(5):616-24. (Pubitemid 28238277)
15. Fernandez-Botran R, Romanovskis P, Sun X, Spatola AF. Linear basic peptides for targeting interferon-c-glycosaminoglycan interactions: Synthesis and inhibitory properties. J Pept Res. 2004; 63(2):56-62. doi:10.1111/j.1399- 3011.2003.00107.x. (Pubitemid 38333834)
16. Simonis D, Christ K, Alban S, Bendas G. Affinity and kinetics of different heparins binding to P-and L-selectin. Semin Thromb Hemost. 2007;33(5):534-9. doi:10.1055/s-2007-982085. (Pubitemid 47105744)
17. Calaycay J, Pande H, Lee T, Borsi L, Siri A, Shively JE, et al. Primary structure of a DNA-and heparin-binding domain (Domain III) in human plasma fibronectin. J Biol Chem. 1985; 260(22):12136-41. (Pubitemid 16228377)
18. LuoY, LuW,MohamedaliKA, Jang JH, JonesRB,Gabriel JL, et al. The glycine box: A determinant of specificity for fibroblast growth factor. Biochemistry. 1998;37(47):16506-15. doi:10.1021/ bi9816599. (Pubitemid 28543909)
19. Nolte SV, Xu W, Rennekampff HO, Rodemann HP. Diversity of fibroblasts-a review on implications for skin tissue engineering. Cells Tissues Organs. 2008;187(3):165-76. (Pubitemid 351398230)
20. van der Smissen A, Hintze V, Scharnweber D, Moeller S, Schnabelrauch M, Majok A, et al. Growth promoting substrates for human dermal fibroblasts provided by artificial extracellular matrices composed of collagen I and sulfated glycosaminoglycans. Biomaterials. 2011;32(34):8938-46.
21. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics. 2002;1(5):376-86.
22. Ong SE, Mann M. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat Protoc. 2006;1(6): 2650-60. doi:10.1038/nprot.2006.427.
23. Greco TM, Seeholzer SH, Mak A, Spruce L, Ischiropoulos H. Quantitative mass spectrometry-based proteomics reveals the dynamic range of primary mouse astrocyte protein secretion. J Proteome Res. 2010;9(5):2764-74. doi:10.1021/pr100134n.
24. Thomas PD, Kejariwal A, Campbell MJ, Mi H, Diemer K, Guo N, et al. PANTHER: A browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res. 2003;31(1):334-41. (Pubitemid 36150398)
25. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44-57. doi:10.1038/nprot.2008. 211.
26. Saalbach A, Klein C, Schirmer C, Briest W, Anderegg U, Simon JC. Dermal fibroblasts promote the migration of dendritic cells. J Investig Dermatol. 2010;130(2):444-54. doi:10.1038/jid. 2009.253.
27. Muller SA, Kohajda T, Findeiss S, Stadler PF, Washietl S, Kellis M, et al. Optimization of parameters for coverage of low molecular weight proteins. Anal Bioanal Chem. 2010;398(7-8): 2867-81. doi:10.1007/s00216-010-4093-x.
28. Morbt N, Mogel I, Kalkhof S, Feltens R, Roder-Stolinski C, Zheng J, et al. Proteome changes in human bronchoalveolar cells following styrene exposure indicate involvement of oxidative stress in the molecular-response mechanism. Proteomics. 2009; 9(21):4920-33. doi:10.1002/pmic.200800836.
29. Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, Olsen JV, et al. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat Protoc. 2009;4(5): 698-705. doi:10.1038/nprot.2009. 36.
30. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. Andromeda: A peptide search engine integrated into the MaxQuant environment. J Proteome Res. 2011;10(4):1794-805. doi:10.1021/pr101065j.
31. Bhatia VN, Perlman DH, Costello CE, McComb ME. Software tool for researching annotations of proteins: Open-source protein annotation software with data visualization. Anal Chem. 2009; 81(23):9819-23. doi:10.1021/ac901335x.
32. Quintanilla-Dieck MJ, Codriansky K, Keady M, Bhawan J, Runger TM. Expression and regulation of cathepsin K in skin fibroblasts. Exp Dermatol. 2009;18(7):596-602. doi:10.1111/j. 1600-0625.2009.00855.x.
33. Pan CP, Kumar C, Bohl S, Klingmueller U, Mann M. Comparative proteomic phenotyping of cell lines and primary cells to assess preservation of cell type-specific functions. Mol Cell Proteomics. 2009;8(3):443-50. doi:10.1074/mcp.M800258-MCP200.
34. Abatangelo G, Barbucci R, Brun P, Lamponi S. Biocompatibility and enzymatic degradation studies on sulphated hyaluronic acid derivatives. Biomaterials. 1997;18(21):1411-5. (Pubitemid 27480603)
35. Maiolica A, Junger MA, Ezkurdia I, Aebersold R. Targeted proteome investigation via selected reaction monitoring mass spectrometry. J Proteomics. 2012;. doi:10.1016/j.jprot.2012.04.048.
36. Clark MF, Lister RM, Bar-Joseph M. ELISA techniques. In: Arthur Weissbach HW, editor. Methods in enzymology. London: Academic Press; 1986. p. 742-66. (Pubitemid 16155149)
37. Schultz GS, Ladwig G, Wysocki A. Extracellular matrix: Review of its roles in acute and chronic wounds. World Wide Wounds. 2005. http://www. worldwidewounds.com/2005/august/Schultz/Extrace-Matric-Acute-Chronic-Wounds. html.
38. Buehler MJ. Nature designs tough collagen: Explaining the nanostructure of collagen fibrils. Proc Natl Acad Sci USA. 2006; 103(33):12285-90. doi:10.1073/pnas.0603216103. (Pubitemid 44267251)
39. Vedrenne N, Coulomb B, Danigo A, Bonté F, Desmouliere A. The complex dialogue between (myo)fibroblasts and the extracellular matrix during skin repair processes and ageing. Pathol Biol (Paris). 2012;60(1):20-7. doi:10.1016/j.patbio.2011.10.002.
40. Akutsu N, Milbury CM, Burgeson RE, Nishiyama T. Effect of type XII or XIV collagen NC-3 domain on the human dermal fibroblast migration into reconstituted collagen gel. Exp Dermatol. 1999;8(1):17-21. doi:10.1111/j.1600- 0625.1999.tb00343.x. (Pubitemid 29038038)
41. Nishiyama T, McDonough AM, Bruns RR, Burgeson RE. Type XII and XIV collagens mediate interactions between banded collagen fibers in vitro and may modulate extracellular matrix deformability. J Biol Chem. 1994;269(45):28193-9. (Pubitemid 24354556)
42. Fluck M, Giraud MN, Tunc V, Chiquet M. Tensile stressdependent collagen XII and fibronectin production by fibroblasts requires separate pathways. Biochim Biophys Acta Mol Cell Res. 2003;1593(2-3):239-48. doi:10.1016/s0167- 4889(02)00394-4. (Pubitemid 36173492)
43. Hatamochi A, Aumailley M, Mauch C, Chu ML, Timpl R, Krieg T. Regulation of collagen VI expression in fibroblasts. Effects of cell density, cell-matrix interactions, and chemical transformation. J Biol Chem. 1989;264(6):3494-9. (Pubitemid 19063408)
44. Dameron KM, Volpert OV, Tainsky MA, Bouck N. Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science. 1994;265(5178):1582- 4. (Pubitemid 24308973)
45. Chen H, Herndon ME, Lawler J. The cell biology of thrombospondin-1. Matrix Biol. 2000;19(7):597-614. doi:10.1016/s0945-053x(00)00107-4.
46. McKeown-Longo PJ, Hanning R, Mosher DF. Binding and degradation of platelet thrombospondin by cultured fibroblasts. J Cell Biol. 1984;98(1):22-8. (Pubitemid 14220463)
47. Adams JC. Thrombospondin-1. Int J Biochem Cell Biol. 1997; 29(6):861-5. (Pubitemid 27364157)
48. Lawler J. The functions of thrombospondin-1 and-2. Curr Opin Cell Biol. 2000;12(5):634-40. doi:10.1016/s0955-0674(00)00 143-5.
49. Wang XQ, Lindberg FP, Frazier WA. Integrin-associated protein stimulates alpha2beta1-dependent chemotaxis via Gi-mediated inhibition of adenylate cyclase and extracellular-regulated kinases. J Cell Biol. 1999;147(2):389-400.
50. Peyssonnaux C, Eychene A. The Raf/MEK/ERK pathway: New concepts of activation. Biol Cell. 2001;93(1-2):53-62. doi: 10.1016/S0248-4900(01)01125-X. (Pubitemid 33040860)
51. Wong KK. Recent developments in anti-cancer agents targeting the Ras/Raf/MEK/ERK pathway. Recent Pat Anti-Cancer Drug Discov. 2009;4(1):28-35.
52. Hempel U, Hintze V, Moller S, Schnabelrauch M, Scharnweber D, Dieter P. Artificial extracellular matrices composed of collagen I and sulfated hyaluronan with adsorbed transforming growth factor b1 promote collagen synthesis of human mesenchymal stromal cells. Acta Biomater. 2012;8(2):659-66. doi:10.1016/j. actbio.2011.10.026.
53. Nareyeck G, Seidler DG, Troyer D, Rauterberg J, Kresse H, Schonherr E. Differential interactions of decorin and decorin mutants with type I and type VI collagens. Eur J Biochem/FEBS. 2004;271(16):3389-98. doi:10.1111/j.1432-1033. 2004.04273.x. (Pubitemid 39120338)
54. Font B, Eichenberger D, Rosenberg LM, van der Rest M. Characterization of the interactions of type XII collagen with two small proteoglycans from fetal bovine tendon, decorin and fibromodulin. Matrix Biol J Int Soc Matrix Biol. 1996;15(5):341-8. (Pubitemid 26419879)
55. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol. 1997; 136(3):729-43. (Pubitemid 27083772)
56. Merle B, Malaval L, Lawler J, Delmas P, Clezardin P. Decorin inhibits cell attachment to thrombospondin-1 by binding to aKKTRdependent cell adhesive site present within theN-terminal domain of thrombospondin-1. J Cell Biochem. 1997;67(1):75-83. doi:10. 1002/(sici)1097-4644(19971001)67:1\75:aid-jcb8[3.0. co;2-t. (Pubitemid 27430325)
57. Seidler DG, Dreier R. Decorin and its galactosaminoglycan chain: Extracellular regulator of cellular function? IUBMB Life. 2008;60(11):729-33. doi:10.1002/iub.115.
58. Sato H, Takino T, Miyamori H. Roles of membrane-type matrix metalloproteinase-1 in tumor invasion and metastasis. Cancer Sci. 2005;96(4):212-7. doi:10.1111/j.1349-7006.2005.00039.x. (Pubitemid 40767057)
59. Lee H, Overall CM, McCulloch CA, Sodek J. A critical role for the membrane-type 1 matrix metalloproteinase in collagen phagocytosis. Mol Biol Cell. 2006;17(11):4812-26. doi:10.1091/ mbc.E06-06-0486. (Pubitemid 44665750)
60. Nagase H. Matrix metalloproteinases. A mini-review. Contrib Nephrol. 1994;107:85-93.
61. Nagase H. Cell surface activation of progelatinase A (proMMP-2) and cell migration. Cell Res. 1998;8(3):179-86. doi:10.1038/cr. 1998.18. (Pubitemid 128544278)
62. Seltzer JL, Eisen AZ. Native Type I collagen is not a substrate for MMP2 (gelatinase a). J Investig Dermatol. 1999;112(6):993.
63. Strongin AY, Collier I, Bannikov G, Marmer BL, Grant GA, Goldberg GI. Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem. 1995;270(10):5331-8.
64. Yoshizaki T, Sato H, Furukawa M. Recent advances in the regulation of matrix metalloproteinase 2 activation: From basic research to clinical implication (review). Oncol Rep. 2002;9(3): 607-11.
65. Isnard N, Robert L, Renard G. Effect of sulfated GAGs on the expression and activation of MMP-2 and MMP-9 in corneal and dermal explant cultures. Cell Biol Int. 2003;27(9):779-84. doi: 10.1016/s1065-6995(03)00167-7. (Pubitemid 37101361)
66. Hou WS, Li ZQ, Gordon RE, Chan K, Klein MJ, Levy R, et al. Cathepsin K is a critical protease in synovial fibroblast-mediated collagen degradation. Am J Pathol. 2001;159(6):2167-77. doi: 10.1016/s0002-9440(10)63068-4. (Pubitemid 33104271)
67. Cullen B, Smith R, McCulloch E, Silcock D, Morrison L. Mechanism of action of PROMOGRAN, a protease modulating matrix, for the treatment of diabetic foot ulcers. Wound Repair Regen. 2002;10(1):16-25. doi:10.1046/j.1524-475X. 2002.10703.x. (Pubitemid 34496478)
68. Shi L, Ermis R, Kiedaisch B, Carson D. The effect of various wound dressings on the activity of debriding enzymes. Adv Skin Wound Care. 2010;23(10):456-62. doi:10.1097/01.ASW.000038 3224.64524.ae.
69. van den Berg AJ, Halkes SB, van Ufford HC, Hoekstra MJ, Beukelman CJ. A novel formulation of metal ions and citric acid reduces reactive oxygen species in vitro. J Wound Care. 2003; 12(10):413-8.
70. Karim RB, Brito BLR, Dutrieux RP, Lassance FP, Hage JJ. MMP-2 assessment as an indicator of wound healing: A feasibility study. Adv Skin Wound Care. 2006;19(6):324-7.