Hydrolyzed eggshell membrane immobilized on phosphorylcholine polymer supplies extracellular matrix environment for human dermal fibroblasts

Cell and Tissue Research

Volumn 345, Issue 1, 2011, Pages 177-190

  Ohto Fujita, Eri ^a   Konno, Tomohiro ^a   Shimizu, Miho ^a   Ishihara, Kazuhiko ^a   Sugitate, Toshihiro ^a   Miyake, Jun ^a,c   Yoshimura, Kotaro ^b   Taniwaki, Kaori ^d   Sakurai, Takashi ^a   Hasebe, Yukio ^d   Atomi, Yoriko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d Almado Incorporation   (Japan)

Author keywords

Dermal fibroblasts; Eggshell membrane; Extracellular matrix; Human; Phospholipid polymer; Type III collagen

Indexed keywords

2 METHACRYLOYLOXYETHYL PHOSPHORYLCHOLINE POLYMER; COLLAGEN TYPE 3; DECORIN; EGG SHELL MEMBRANE PROTEIN; GELATINASE A; MEMBRANE PROTEIN; MESSENGER RNA; POLYMER; UNCLASSIFIED DRUG;

ARTICLE; ARTIFICIAL MEMBRANE; ATOMIC FORCE MICROSCOPY; CELL ADHESION; CONTROLLED STUDY; DERMAL FIBROBLAST; EGG SHELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYDROLYSIS; IN VITRO STUDY; INFANT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ANALYSIS; SKIN FIBROBLAST;

ALKALIES; ANIMALS; BIRDS; CELL ADHESION; COLLAGEN TYPE I; DERMIS; EGG SHELL; EXTRACELLULAR MATRIX; FIBROBLASTS; GENE EXPRESSION REGULATION; GLYCOSAMINOGLYCANS; HUMANS; HYDROLYSIS; MEMBRANES; METHACRYLATES; PHOSPHORYLCHOLINE; POLYMERS;

AVES;

EID: 79960211891     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-011-1172-z     Document Type: Article

References (69)

1. G Ahlborn BW Sheldon 2005 Enzymatic and microbiological inhibitory activity in eggshell membranes as influenced by layer (Pubitemid 44509953)
2. E Aiba-Kojima NH Tsuno K Inoue D Matsumoto T Shigeura T Sato H Suga H Kato T Nagase K Gonda I Koshima K Takahashi K Yoshimura 2007 Characterization of wound drainage fluids as a source of soluble factors associated with wound healing: comparison with platelet-rich plasma and potential use in cell culture Wound Repair Regen 15 511 520 17650095 10.1111/j.1524-475X.2007.00259.x (Pubitemid 47087644)
3. P Betz A Nerlich J Wilske J Tubel R Penning W Eisenmenger 1993 Analysis of the immunohistochemical localization of collagen type III and V for the time-estimation of human skin wounds Int J Leg Med 105 329 332 10.1007/BF01222117 1:STN:280:DyaK3s3pvVKlsw%3D%3D (Pubitemid 23156595)
4. F Boraldi MA Croce D Quaglino R Sammarco E Carnevali R Tiozzo I Pasquali-Ronchetti 2003 Cell-matrix interactions of in vitro human skin fibroblasts upon addition of hyaluronan Tissue Cell 35 37 45 12589728 10.1016/S0040-8166(02)00101-5 1:CAS:528:DC%2BD3sXhsFGgsLg%3D (Pubitemid 36329259)
5. P Bruckner 2010 Suprastructures of extracellular matrices: paradigms of functions controlled by aggregates rather than molecules Cell Tissue Res 339 7 18 19756756 10.1007/s00441-009-0864-0 1:CAS:528:DC%2BD1MXhsVymtrfP
6. Burley RW, Vadehra DV (1989) The avian egg, chemistry and biology. Wiley, New York
7. A Corsi T Xu XD Chen A Boyde J Liang M Mankani B Sommer RV Iozzo I Eichstetter PG Robey P Bianco MF Young 2002 Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues J Bone Miner Res 17 1180 1189 12102052 10.1359/jbmr.2002.17. 7.1180 1:CAS:528:DC%2BD38XlsF2nurc%3D (Pubitemid 34680494)
8. KG Danielson H Baribault DF Holmes H Graham KE Kadler RV Iozzo 1997 Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility J Cell Biol 136 729 743 9024701 10.1083/jcb.136.3.729 1:CAS:528:DyaK2sXhtFClt70%3D (Pubitemid 27083772)
9. L Debelle AM Tamburro 1999 Elastin: molecular description and function Int J Biochem Cell Biol 31 261 272 10216959 10.1016/S1357-2725(98)00098-3 1:CAS:528:DyaK1MXhvFehsbY%3D (Pubitemid 29094776)
10. RF Diegelmann MC Evans 2004 Wound healing: an overview of acute, fibrotic and delayed healing Front Biosci 9 283 289 14766366 10.2741/1184 1:CAS:528:DC%2BD2cXhtFCku78%3D (Pubitemid 38925460)
11. DE Discher P Janmey YL Wang 2005 Tissue cells feel and respond to the stiffness of their substrate Science 310 1139 1143 16293750 10.1126/science. 1116995 1:CAS:528:DC%2BD2MXht1WgtLbF (Pubitemid 41681732)
12. A El Sherif F Yano S Mittal CJ Filipi 2006 Collagen metabolism and recurrent hiatal hernia: cause and effect? Hernia 10 511 520 17021673 10.1007/s10029-006-0152-9 (Pubitemid 44834994)
13. SP Evanko JC Angello TN Wight 1999 Formation of hyaluronan- and versican-rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells Arterioscler Thromb Vasc Biol 19 1004 1013 10195929 10.1161/01.ATV.19.4.1004 1:CAS:528:DyaK1MXislaru7k%3D (Pubitemid 29177349)
14. JJ Grzesiak MD Pierschbacher MF Amodeo TI Malaney JR Glass 1997 Enhancement of cell interactions with collagen/glycosaminoglycan matrices by RGD derivatization Biomaterials 18 1625 1632 9613810 10.1016/S0142-9612(97)00103-8 1:CAS:528:DyaK1cXivFGisL8%3D (Pubitemid 28185062)
15. YW Ha MJ Son KS Yun YS Kim 2007 Relationship between eggshell strength and keratan sulfate of eggshell membranes Comp Biochem Physiol A Mol Integr Physiol 147 1109 1115 17466551 10.1016/j.cbpa.2007.03.022 (Pubitemid 46843633)
16. ED Harris JE Blount RM Leach Jr 1980 Localization of lysyl oxidase in hen oviduct: implications in egg shell membrane formation and composition Science 208 55 56 6102412 10.1126/science.6102412 1:CAS:528:DyaL3cXhvFCrt7k%3D (Pubitemid 10074624)
17. T Ino M Hattori T Yoshida S Hattori K Yoshimura K Takahashi 2006 Improved physical and biochemical features of a collagen membrane by conjugating with soluble egg shell membrane protein Biosci Biotechnol Biochem 70 865 873 16636453 10.1271/bbb.70.865 1:CAS:528:DC%2BD28Xks1Sgs70%3D
18. N Isnard L Robert G Renard 2003 Effect of sulfated GAGs on the expression and activation of MMP-2 and MMP-9 in corneal and dermal explant cultures Cell Biol Int 27 779 784 12972284 10.1016/S1065-6995(03)00167-7 1:CAS:528: DC%2BD3sXntVGmtbw%3D (Pubitemid 37101361)
19. N Itano T Sawai M Yoshida P Lenas Y Yamada M Imagawa T Shinomura M Hamaguchi Y Yoshida Y Ohnuki S Miyauchi AP Spicer JA McDonald K Kimata 1999 Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties J Biol Chem 274 25085 25092 10455188 10.1074/jbc.274.35.25085 1:CAS:528:DyaK1MXls1ymur8%3D (Pubitemid 29404720)
20. PL Jansen R Rosch M Jansen M Binnebosel K Junge A Alfonso-Jaume U Klinge DH Lovett PR Mertens 2007 Regulation of MMP-2 gene transcription in dermal wounds J Invest Dermatol 127 1762 1767 17344928 1:CAS:528:DC%2BD2sXms1Slt7Y%3D (Pubitemid 46933427)
21. H Jarvelainen P Puolakkainen S Pakkanen EL Brown M Hook RV Iozzo EH Sage TN Wight 2006 A role for decorin in cutaneous wound healing and angiogenesis Wound Repair Regen 14 443 452 16939572 10.1111/j.1743-6109.2006.00150.x (Pubitemid 44266601)
22. VM Kahari U Saarialho-Kere 1997 Matrix metalloproteinases in skin Exp Dermatol 6 199 213 9450622 10.1111/j.1600-0625.1997.tb00164.x 1:CAS:528:DyaK2sXmslCgtrs%3D (Pubitemid 27421661)
23. MH Kanzler DC Gorsulowsky NA Swanson 1986 Basic mechanisms in the healing cutaneous wound J Dermatol Surg Oncol 12 1156 1164 3490500 1:STN:280: DyaL2s%2FjsVGmsg%3D%3D (Pubitemid 17182079)
24. E Kerkela U Saarialho-Kere 2003 Matrix metalloproteinases in tumor progression: focus on basal and squamous cell skin cancer Exp Dermatol 12 109 125 12702139 10.1034/j.1600-0625.2003.120201.x 1:CAS:528:DC%2BD3sXksVWgtrs%3D (Pubitemid 36934696)
25. SG Kim T Akaike T Sasagaw Y Atomi H Kurosawa 2002 Gene expression of type I and type III collagen by mechanical stretch in anterior cruciate ligament cells Cell Struct Funct 27 139 144 12207044 10.1247/csf.27.139 1:CAS:528:DC%2BD38Xns1ahtrk%3D
26. T Konno J Watanabe K Ishihara 2004 Conjugation of enzymes on polymer nanoparticles covered with phosphorylcholine groups Biomacromolecules 5 342 347 15002993 10.1021/bm034356p 1:CAS:528:DC%2BD2cXhvVehs7k%3D (Pubitemid 38404469)
27. S Kontusaari G Tromp H Kuivaniemi AM Romanic DJ Prockop 1990 A mutation in the gene for type III procollagen (COL3A1) in a family with aortic aneurysms J Clin Invest 86 1465 1473 2243125 10.1172/JCI114863 1:STN:280: DyaK3M%2Fls1Wntw%3D%3D (Pubitemid 20372592)
28. H Kuivaniemi G Tromp WF Bergfeld M Kay TN Helm 1995 Ehlers-Danlos syndrome type IV: a single base substitution of the last nucleotide of exon 34 in COL3A1 leads to exon skipping J Invest Dermatol 105 352 356 7665911 10.1111/1523-1747.ep12320704 1:CAS:528:DyaK2MXptlamsbw%3D
29. TC Laurent JR Fraser 1992 Hyaluronan FASEB J 6 2397 2404 1563592 1:CAS:528:DyaK38XltVKgu7o%3D
30. S Lee T Sakurai M Ohsako R Saura H Hatta Y Atomi 2010 Tissue stiffness induced by prolonged immobilization of the rat knee joint and relevance of AGEs (pentosidine) Connect Tissue Res 51 467 477 20604714 10.3109/03008201003686941 1:CAS:528:DC%2BC3cXhtlCltbrO
31. F Li C Fan T Cheng C Jiang B Zeng 2009 Efficient inhibition of fibroblast proliferation and collagen expression by ERK2 siRNAs Biochem Biophys Res Commun 382 259 263 19285964 10.1016/j.bbrc.2009.02.165 1:CAS:528:DC%2BD1MXkt1Slurg%3D
32. SH Liu RS Yang R al-Shaikh JM Lane 1995 Collagen in tendon, ligament, and bone healing. A current revie Clin Orthop Relat Res 318 265 278 7671527
33. X Liu H Wu M Byrne S Krane R Jaenisch 1997 Type III collagen is crucial for collagen I fibrillogenesis and for normal cardiovascular development Proc Natl Acad Sci USA 94 1852 1856 9050868 10.1073/pnas.94.5.1852 1:CAS:528:DyaK2sXhslaru70%3D (Pubitemid 27113925)
34. KA Lygoe I Wall P Stephens MP Lewis 2007 Role of vitronectin and fibronectin receptors in oral mucosal and dermal myofibroblast differentiation Biol Cell 99 601 614 17516912 10.1042/BC20070008 1:CAS:528:DC%2BD2sXhtFygsbvK (Pubitemid 350120980)
35. J Meenakshi S Vidyameenakshi D Ananthram KM Ramakrishnan V Jayaraman M Babu 2009 Low decorin expression along with inherent activation of ERK1,2 in ear lobe keloids Burns 35 519 526 19268470 10.1016/j.burns.2008.07.012
36. RR Mohan R Gupta MK Mehan JW Cowden S Sinha 2010 Decorin transfection suppresses profibrogenic genes and myofibroblast formation in human corneal fibroblasts Exp Eye Res 91 238 245 20546727 10.1016/j.exer.2010.05.013 1:CAS:528:DC%2BC3cXovFymsrk%3D
37. T Moro Y Takatori K Ishihara T Konno Y Takigawa T Matsushita UI Chung K Nakamura H Kawaguchi 2004 Surface grafting of artificial joints with a biocompatible polymer for preventing periprosthetic osteolysis Nat Mater 3 829 836 15502835 10.1038/nmat1233 1:CAS:528:DC%2BD2cXptV2htLg%3D
38. A Mukhopadhyay MY Wong SY Chan DV Do A Khoo CT Ong HH Cheong IJ Lim TT Phan 2010 Syndecan-2 and decorin: proteoglycans with a difference-implications in keloid pathogenesis J Trauma 68 999 1008 20386290 10.1097/TA.0b013e3181c4070d 1:CAS:528:DC%2BC3cXks1Wksbc%3D
39. Y Nomura 2006 Structural change in decorin with skin aging Connect Tissue Res 47 249 255 17118746 10.1080/03008200600846606 1:CAS:528:DC%2BD28XhtlentrbP (Pubitemid 44803792)
40. BR Olsen 1995 The roles of collagen genes in skeletal development and morphogenesis Experientia 51 194 195 7698270 10.1007/BF01931087 1:STN:280:DyaK2M3ht1Cqsg%3D%3D
41. CI Osuoji 1971 Acid glycosaminoglycan of eggshell membranes Biochim Biophys Acta 244 481 483 4256641 1:CAS:528:DyaE3MXltlyjs7o%3D
42. L Pickart MM Thaler 1973 Tripeptide in human serum which prolongs survival of normal liver cells and stimulates growth in neoplastic liver Nat New Biol 243 85 87 4349963 1:CAS:528:DyaE3sXlt1aksb8%3D
43. DJ Prockop KI Kivirikko 1984 Heritable diseases of collagen N Engl J Med 311 376 386 6146097 10.1056/NEJM198408093110606 1:STN:280:DyaL2c3ksFOnug%3D%3D (Pubitemid 14096748)
44. D Quaglino Jr LB Nanney R Kennedy JM Davidson 1990 Transforming growth factor-beta stimulates wound healing and modulates extracellular matrix gene expression in pig skin. I. Excisional wound model Lab Invest 63 307 319 2395327 1:CAS:528:DyaK3MXhtFGlurc%3D (Pubitemid 20334762)
45. JL Rinn JK Wang H Liu K Montgomery M van de Rijn HY Chang 2008 A systems biology approach to anatomic diversity of skin J Invest Dermatol 128 776 782 18337710 10.1038/sj.jid.5700986 1:CAS:528:DC%2BD1cXjtFOit7o%3D (Pubitemid 351374284)
46. ML Rose MT Hincke 2009 Protein constituents of the eggshell: eggshell-specific matrix proteins Cell Mol Life Sci 66 2707 2719 19452125 10.1007/s00018-009-0046-y 1:CAS:528:DC%2BD1MXovFOlu70%3D
47. J Rosenbloom WR Abrams R Mecham 1993 Extracellular matrix 4: the elastic fiber FASEB J 7 1208 1218 8405806 1:CAS:528:DyaK3sXms1Oiu7w%3D (Pubitemid 23314355)
48. KJ Ruff DP DeVore MD Leu MA Robinson 2009 Eggshell membrane: a possible new natural therapeutic for joint and connective tissue disorders. Results from two open-label human clinical studies Clin Interv Aging 4 235 240 19554094 10.2147/CIA.S5797
49. KJ Ruff A Winkler RW Jackson DP DeVore BW Ritz 2009 Eggshell membrane in the treatment of pain and stiffness from osteoarthritis of the knee: a randomized, multicenter, double-blind, placebo-controlled clinical study Clin Rheumatol 28 907 914 19340512 10.1007/s10067-009-1173-4
50. UK Saarialho-Kere AP Pentland H Birkedal-Hansen WC Parks HG Welgus 1994 Distinct populations of basal keratinocytes express stromelysin-1 and stromelysin-2 in chronic wounds J Clin Invest 94 79 88 8040294 10.1172/JCI117351 1:CAS:528:DyaK2cXltlWltbo%3D (Pubitemid 24218079)
51. A Simeon Y Wegrowski Y Bontemps FX Maquart 2000 Expression of glycosaminoglycans and small proteoglycans in wounds: modulation by the tripeptide-copper complex glycyl-L-histidyl-L-lysine-Cu(2+) J Invest Dermatol 115 962 968 11121126 10.1046/j.1523-1747.2000.00166.x 1:CAS:528: DC%2BD3MXhtFamsw%3D%3D (Pubitemid 32037436)
52. RM Simpson S Meran D Thomas P Stephens T Bowen R Steadman A Phillips 2009 Age-related changes in pericellular hyaluronan organization leads to impaired dermal fibroblast to myofibroblast differentiation Am J Pathol 175 1915 1928 19808648 10.2353/ajpath.2009.090045 1:CAS:528:DC%2BC3cXhslSjtL4%3D
53. R Stern 2003 Devising a pathway for hyaluronan catabolism: are we there yet? Glycobiology 13 105R 115R 14514708 10.1093/glycob/cwg112 1:CAS:528:DC%2BD3sXptVeqtbo%3D (Pubitemid 37508893)
54. K Takahashi S Yamanaka 2006 Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 663 676 16904174 10.1016/j.cell.2006.07.024 1:CAS:528:DC%2BD28Xpt1aktbs%3D (Pubitemid 44233629)
55. EM Tan J Hoffren S Rouda S Greenbaum JWt Fox JH Moore Jr GR Dodge 1993 Decorin, versican, and biglycan gene expression by keloid and normal dermal fibroblasts: differential regulation by basic fibroblast growth factor Exp Cell Res 209 200 207 8262136 10.1006/excr.1993.1302 1:CAS:528:DyaK2cXks1ejug%3D%3D (Pubitemid 24005303)
56. FM Tholozan C Gribbon Z Li MW Goldberg AR Prescott N McKie RA Quinlan 2007 FGF-2 release from the lens capsule by MMP-2 maintains lens epithelial cell viability Mol Biol Cell 18 4222 4231 17699594 10.1091/mbc.E06-05-0416 1:CAS:528:DC%2BD2sXht12js7zN (Pubitemid 350060154)
57. KY Tsang MC Cheung D Chan KS Cheah 2010 The developmental roles of the extracellular matrix: beyond structure to regulation Cell Tissue Res 339 93 110 19885678 10.1007/s00441-009-0893-8 1:CAS:528:DC%2BD1MXhsVymtrbK
58. L Vitellaro-Zuccarello R Garbelli VD Rossi 1992 Immunocytochemical localization of collagen types I, III, IV, and fibronectin in the human dermis. Modifications with ageing Cell Tissue Res 268 505 511 1628306 10.1007/BF00319157 1:CAS:528:DyaK38XksVGhurw%3D
59. Volk SW, Wang Y, Mauldin EA, Liechty KW, Adams SL (2011) Diminished type III collagen promotes myofibroblast differentiation and increases scar deposition in cutaneous wound healing. Cells Tissues Organs (in press)
60. von der Mark K, Park J, Bauer S, Schmuki P (2010) Nanoscale engineering of biomimetic surfaces: cues from the extracellular matrix. Cell Tissue Res 339:131-153
61. JF Wang ME Olson CR Reno W Kulyk JB Wright DA Hart 2000 Molecular and cell biology of skin wound healing in a pig model Connect Tissue Res 41 195 211 11264869 10.3109/03008200009005290 1:CAS:528:DC%2BD3cXovF2qsb4%3D
62. Watanabe J, Ishihara K (2007) Multiple protein-immobilized phospholipid polymer nanoparticles: effect of spacer length on residual enzymatic activity and molecular diagnosis. Nanobiotechnol 3:76-82
63. HG Welgus EJ Campbell JD Cury AZ Eisen RM Senior SM Wilhelm GI Goldberg 1990 Neutral metalloproteinases produced by human mononuclear phagocytes. Enzyme profile, regulation, and expression during cellular development J Clin Invest 86 1496 1502 2173721 10.1172/JCI114867 1:CAS:528:DyaK3cXmt1ygurs%3D (Pubitemid 20372596)
64. SM Wilhelm IE Collier A Kronberger AZ Eisen BL Marmer GA Grant EA Bauer GI Goldberg 1987 Human skin fibroblast stromelysin: structure, glycosylation, substrate specificity, and differential expression in normal and tumorigenic cells Proc Natl Acad Sci USA 84 6725 6729 3477804 10.1073/pnas.84.19.6725 1:CAS:528:DyaL1MXntlWlsA%3D%3D (Pubitemid 18025491)
65. M Wong MJ Hendrix K von der Mark C Little R Stern 1984 Collagen in the egg shell membranes of the hen Dev Biol 104 28 36 6203793 10.1016/0012-1606(84) 90033-2 1:CAS:528:DyaL2cXksFajtb8%3D
66. JJ Wu MA Weis LS Kim DR Eyre 2010 Type III collagen, a fibril network modifier in articular cartilage J Biol Chem 285 18537 18544 20404341 10.1074/jbc.M110.112904 1:CAS:528:DC%2BC3cXmvFaqsL4%3D
67. T Xu P Bianco LW Fisher G Longenecker E Smith S Goldstein J Bonadio A Boskey AM Heegaard B Sommer K Satomura P Dominguez C Zhao AB Kulkarni PG Robey MF Young 1998 Targeted disruption of the biglycan gene leads to an osteoporosis-like phenotype in mice Nat Genet 20 78 82 9731537 10.1038/2477 1:CAS:528:DyaK1cXmtVOmur4%3D (Pubitemid 28455451)
68. L Zhang N Tran HQ Chen CJ Kahn S Marchal F Groubatch X Wang 2008 Time-related changes in expression of collagen types I and III and of tenascin-C in rat bone mesenchymal stem cells under co-culture with ligament fibroblasts or uniaxial stretching Cell Tissue Res 332 101 109 18196274 10.1007/s00441-007- 0564-6 1:CAS:528:DC%2BD1cXjsF2ms7w%3D
69. N Zoppi R Gardella A De Paepe S Barlati M Colombi 2004 Human fibroblasts with mutations in COL5A1 and COL3A1 genes do not organize collagens and fibronectin in the extracellular matrix, down-regulate alpha2beta1 integrin, and recruit alphavbeta3 instead of alpha5beta1 integrin J Biol Chem 279 18157 18168 14970208 10.1074/jbc.M312609200 1:CAS:528:DC%2BD2cXjsVKnt7o%3D (Pubitemid 38623228)