The Dermatan Sulfate Proteoglycan Decorin Modulates α2β1 Integrin and the Vimentin Intermediate Filament System during Collagen Synthesis

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Jungmann, Oliver ^a   Nikolovska, Katerina ^a   Stock, Christian ^a   Schulz, Jan Niklas ^b   Eckes, Beate ^b   Riethmüller, Christoph ^c   Owens, Rick T ^d   Iozzo, Renato V ^e   Seidler, Daniela G ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c Serend ip GmbH   (Germany)

^d LIFECELL CORPORATION   (United States)

^e THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DECORIN; MESSENGER RNA; VERY LATE ACTIVATION ANTIGEN 2; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL STRUCTURE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; INTERMEDIATE FILAMENT; MASS SPECTROMETRY; MESSENGER RNA SYNTHESIS; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; SKIN FIBROBLAST; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

ANIMALS; CELL CULTURE TECHNIQUES; CELL NUCLEUS; CHONDROITIN SULFATE PROTEOGLYCANS; COLLAGEN; DECORIN; DERMATAN SULFATE; EXTRACELLULAR MATRIX; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; INTEGRIN ALPHA2BETA1; INTERMEDIATE FILAMENTS; MICE; PHOSPHORYLATION; PROTONS; RNA, MESSENGER; SKIN; VIMENTIN;

MUS;

EID: 84870690407     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050809     Document Type: Article

References (67)

1. Reed CC, Iozzo RV, (2002) The role of decorin in collagen fibrillogenesis and skin homeostasis. Glycoconj J 19: 249-255.
2. Kalamajski S, Oldberg A, (2010) The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Biol 29: 248-253.
3. Iozzo RV, (1999) The biology of the small leucine-rich proteoglycans. Functional network of interactive proteins. J Biol Chem 274: 18843-18846.
4. Ferdous Z, Peterson SB, Tseng H, Anderson DK, Iozzo RV, et al. (2010) A role for decorin in controlling proliferation, adhesion, and migration of murine embryonic fibroblasts. J Biomed Mater Res A 93: 419-428.
5. Iozzo RV, Moscatello DK, McQuillan DJ, Eichstette I, (1999) Decorin is a biological ligand for the epidermal growth factor receptor. J Biol Chem 274: 4489-4492.
6. Seidler DG, Goldoni S, Agnew C, Cardi C, Thakur ML, et al. (2006) Decorin protein core inhibits in vivo cancer growth and metabolism by hindering epidermal growth factor receptor function and triggering apoptosis via caspase-3 activation. J Biol Chem 281: 26408-26418.
7. Goldoni S, Seidler DG, Heath J, Fassan M, Baffa R, et al. (2008) An antimetastatic role for decorin in breast cancer. Am J Pathol 173: 844-855.
8. Schönherr E, Sunderkötter C, Iozzo RV, Schaefer L, (2005) Decorin, a novel player in the insulin-like growth factor system. J Biol Chem 280: 15767-15772.
9. Iozzo RV, Buraschi S, Genua M, Xu SQ, Solomides CC, et al. (2011) Decorin Antagonizes IGF Receptor I (IGF-IR) Function by Interfering with IGF-IR Activity and Attenuating Downstream Signaling J. Biol. Chem. 286: 34712-34721.
10. Goldoni S, Humphries A, Nystrom A, Sattar S, Owens RT, et al. (2009) Decorin is a novel antagonistic ligand of the Met receptor. J.Cell Biol. 185: 743-754.
11. Brandan E, Retamal C, Cabello-Verrugio C, Marzolo MP, (2006) The low density lipoprotein receptor-related protein functions as an endocytic receptor for decorin. J Biol Chem 281: 31562-31571.
12. Seidler DG, Mohamed NA, Bocian C, Stadtmann A, Hermann S, et al. (2011) The role for decorin in delayed-type hypersensitivity. J.Immunol. 187: 6108-6119.
13. Merline R, Moreth K, Beckmann J, Nastase MV, Zeng-Brouwers J, et al. (2011) Signaling by the matrix proteoglycan decorin controls inflammation and cancer through PDCD4 and MicroRNA-21. Sci.Signal. 4: ra75.
14. Yamaguchi Y, Mann DM, Ruoslahti E, (1990) Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature 346: 281-284.
15. Kresse H, Rosthoj S, Quentin E, Hollmann J, Glossl J, et al. (1987) Glycosaminoglycan-free small proteoglycan core protein is secreted by fibroblasts from a patient with a syndrome resembling progeroid. Am J Hum Genet 41: 436-453.
16. Seidler DG, Faiyaz-Ul-Haque M, Hansen U, Yip GW, Zaidi SH, et al. (2006) Defective glycosylation of decorin and biglycan, altered collagen structure, and abnormal phenotype of the skin fibroblasts of an Ehlers-Danlos syndrome patient carrying the novel Arg270Cys substitution in galactosyltransferase I (beta4GalT-7). J Mol Med 84: 583-594.
17. Miyake N, Kosho T, Mizumoto S, Furuichi T, Hatamochi A, et al. (2010) Loss-of-function mutations of CHST14 in a new type of Ehlers-Danlos syndrome. Hum Mutat 31: 966-974.
18. Seidler DG, (2012) The galactosaminoglycan-containing decorin and its impact on diseases. Curr Opin Struct Biol. 22: 578-82.
19. Maccarana M, Kalamajski S, Kongsgaard M, Magnusson SP, Oldberg A, et al. (2009) Dermatan sulfate epimerase 1-deficient mice have reduced content and changed distribution of iduronic acids in dermatan sulfate and an altered collagen structure in skin. Mol Cell Biol 29: 5517-5528.
20. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, et al. (1997) Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 136: 729-743.
21. Järveläinen H, Puolakkainen P, Pakkanen S, Brown EL, Hook M, et al. (2006) A role for decorin in cutaneous wound healing and angiogenesis. Wound Repair Regen 14: 443-452.
22. Seidler DG, Schaefer L, Robenek H, Iozzo RV, Kresse H, et al. (2005) A physiologic three-dimensional cell culture system to investigate the role of decorin in matrix organisation and cell survival. Biochem Biophys Res Commun 332: 1162-1170.
23. Rühland C, Schönherr E, Robenek H, Hansen U, Seidler DG, et al. (2007) The glycosaminoglycan chain of decorin plays an important role in collagen fibril formation at the early stages of fibrillogenesis. FEBS J 274: 4246-4255.
24. White DJ, Puranen S, Johnson MS, Heino J, (2004) The collagen receptor subfamily of the integrins. Int J Biochem Cell Biol 36: 1405-1410.
25. Cukierman E, Pankov R, Stevens DR, Yamada KM, (2001) Taking cell-matrix adhesions to the third dimension. Science 294: 1708-1712.
26. Merle B, Durussel L, Delmas PD, Clezardin P, (1999) Decorin inhibits cell migration through a process requiring its glycosaminoglycan side chain. J Cell Biochem 75: 538-546.
27. Fiedler LR, Schönherr E, Waddington R, Niland S, Seidler DG, et al. (2008) Decorin regulates endothelial cell motility on collagen I through activation of insulin-like growth factor I receptor and modulation of alpha2beta1 integrin activity. J Biol Chem 283: 17406-17415.
28. Kim S, Coulombe PA, (2007) Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm. Genes Dev. 21: 1581-1597.
29. Martys JL, Ho CL, Liem RK, Gundersen GG, (1999) Intermediate filaments in motion: observations of intermediate filaments in cells using green fluorescent protein-vimentin. Mol Biol Cell 10: 1289-1295.
30. Steinert PM, Steven AC, Roop DR, (1985) The molecular biology of intermediate filaments. Cell 42: 411-420.
31. Helfand BT, Chang L, Goldman RD, (2004) Intermediate filaments are dynamic and motile elements of cellular architecture. J Cell Sci 117: 133-141.
32. Tsuruta D, Jones JC, (2003) The vimentin cytoskeleton regulates focal contact size and adhesion of endothelial cells subjected to shear stress. J Cell Sci 116: 4977-4984.
33. Ivaska J, Pallari HM, Nevo J, Eriksson JE, (2007) Novel functions of vimentin in cell adhesion, migration, and signaling. Exp Cell Res 313: 2050-2062.
34. Kreis S, Schonfeld HJ, Melchior C, Steiner B, Kieffer N, (2005) The intermediate filament protein vimentin binds specifically to a recombinant integrin alpha2/beta1 cytoplasmic tail complex and co-localizes with native alpha2/beta1 in endothelial cell focal adhesions. Exp.Cell Res. 305: 110-121.
35. Coulombe PA, Wong P, (2004) Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nat.Cell Biol. 6: 699-706.
36. Toivola DM, Tao GZ, Habtezion A, Liao J, Omary MB, (2005) Cellular integrity plus: organelle-related and protein-targeting functions of intermediate filaments. Trends Cell Biol 15: 608-617.
37. Perlson E, Hanz S, Ben-Yaakov K, Segal-Ruder Y, Seger R, et al. (2005) Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45: 715-726.
38. Colucci-Guyon E, Portier MM, Dunia I, Paulin D, Pournin S, et al. (1994) Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79: 679-694.
39. Eckes B, Dogic D, Colucci-Guyon E, Wang N, Maniotis A, et al. (1998) Impaired mechanical stability, migration and contractile capacity in vimentin-deficient fibroblasts. J Cell Sci 111: 1897-1907.
40. Eckes B, Colucci-Guyon E, Smola H, Nodder S, Babinet C, et al. (2000) Impaired wound healing in embryonic and adult mice lacking vimentin. J Cell Sci 113: 2455-2462.
41. Holtkötter O, Nieswandt B, Smyth N, Müller W, Hafner M, et al. (2002) Integrin alpha 2-deficient mice develop normally, are fertile, but display partially defective platelet interaction with collagen. J. Biol. Chem. 277: 10789-10794.
42. Fisher LW, Stubbs JT, Young MF (1995) Antisera and cDNA probes to human and certain animal model bone matrix noncollagenous proteins. Acta Orthop Scand Suppl 266: 61-65.
43. O'Farrell PH, (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007-4021.
44. Neuhoff V, Arold N, Taube D, Ehrhardt W, (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9: 255-262.
45. Parsons-Wingerter P, Kasman IM, Norberg S, Magnussen A, Zanivan S, et al. (2005) Uniform overexpression and rapid accessibility of alpha5beta1 integrin on blood vessels in tumors. Am J Pathol 167: 193-211.
46. Zamfir AD, Flangea C, Sisu E, Serb AF, Seidler DG, et al. (2009) Analysis of novel over- and under-sulfated glycosaminoglycan sequences by enzyme cleavage and multiple stage MS. Proteomics 9: 3435-3444.
47. Goldoni S, Owens RT, McQuillan DJ, Shriver Z, Sasisekharan R, et al. (2004) Biologically active decorin is a monomer in solution. J Biol Chem 279: 6606-12.
48. Riethmüller C, Nasdala I, Vestweber D, (2008) Nano-surgery at the leukocyte-endothelial docking site. Pflugers Arch 456: 71-81.
49. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
50. Stock C, Jungmann O, Seidler DG, (2011) Decorin and chondroitin-6 sulfate inhibit B16V melanoma cell migration and invasion by cellular acidification. J Cell Physiol 226: 2641-2650.
51. Kovbasnjuk ON, Spring KR, (2000) The apical membrane glycocalyx of MDCK cells. J Membr Biol 176: 19-29.
52. Khatau SB, Hale CM, Stewart-Hutchinson PJ, Patel MS, Stewart CL, et al. (2009) A perinuclear actin cap regulates nuclear shape. Proc. Natl. Acad. Sci. U. S. A 106: 19017-19022.
53. Schaefer L, Iozzo RV, (2008) Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction. J Biol Chem 283: 21305-21309.
54. Barczyk M, Carracedo S, Gullberg D, (2010) Integrins. Cell Tissue Res. 339: 269-280.
55. Paradise RK, Lauffenburger DA, Van Vliet KJ, (2011) Acidic extracellular pH promotes activation of integrin alpha(v)beta(3) PLoS. One. 6: e15746.
56. Liu J, He X, Qi Y, Tian X, Monkley SJ, et al. (2011) Talin1 regulates integrin turnover to promote embryonic epithelial morphogenesis. Mol Cell Biol 31: 3366-3377.
57. Ridger VC, Wagner BE, Wallace WA, Hellewell PG, (2001) Differential effects of CD18, CD29, and CD49 integrin subunit inhibition on neutrophil migration in pulmonary inflammation. J.Immunol. 166: 3484-3490.
58. Inagaki M, Nishi Y, Nishizawa K, Matsuyama M, Sato C, (1987) Site-specific phosphorylation induces disassembly of vimentin filaments in vitro. Nature 328: 649-652.
59. Schaefer L, Gröne HJ, Raslik I, Robenek H, Ugorcakova J, et al. (2000) Small proteoglycans of normal adult human kidney: distinct expression patterns of decorin, biglycan, fibromodulin, and lumican. Kidney Int 58: 1557-1568.
60. Ranta V, Mikkola T, Ylikorkala O, Viinikka L, Orpana A, (1998) Reduced viability of human vascular endothelial cells cultured on Matrigel. J Cell Physiol 176: 92-8.
61. Wolf K, Alexander S, Schacht V, Coussens LM, von Andrian UH, et al. (2009) Collagen-based cell migration models in vitro and in vivo. Semin Cell Dev Biol 20: 931-941.
62. Jokinen J, Dadu E, Nykvist P, Kapyla J, White DJ, et al. (2004) Integrin-mediated cell adhesion to type I collagen fibrils. J Biol Chem 279: 31956-31963.
63. Bhide VM, Laschinger CA, Arora PD, Lee W, Hakkinen L, et al. (2005) Collagen phagocytosis by fibroblasts is regulated by decorin. J.Biol.Chem. 280, 23103-23113.
64. Heino J, Ignotz RA, Hemler ME, Crouse C, Massague J, (1989) Regulation of cell adhesion receptors by transforming growth factor-beta. Concomitant regulation of integrins that share a common beta 1 subunit. J.Biol.Chem. 264: 380-388.
65. Nieminen M, Henttinen T, Merinen M, Marttila-Ichihara F, Eriksson JE, et al. (2006) Vimentin function in lymphocyte adhesion and transcellular migration. Nat.Cell Biol. 8: 156-162.
66. Takagi J, Springer TA, (2002) Integrin activation and structural rearrangement. Immunol Rev 186: 141-163.
67. Stock C, Gassner B, Hauck CR, Arnold H, Mally S, et al. (2005) Migration of human melanoma cells depends on extracellular pH and Na+/H+ exchange. J Physiol 567: 225-238.