Transforming Growth Factor Beta 3 Modifies Mechanics and Composition of Extracellular Matrix Deposited by Human Trabecular Meshwork Cells

ACS Biomaterials Science and Engineering

Volumn 1, Issue 2, 2015, Pages 110-118

  Raghunathan, Vijay Krishna ^a   Morgan, Joshua T ^a   Chang, Yow Ren ^a   Weber, Darren ^a   Phinney, Brett ^a   Murphy, Christopher J ^a,b   Russell, Paul ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

atomic force microscopy; biomechanics; extracellular matrix; glaucoma; pseudoexfoliation syndrome; trabecular meshwork

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; ANGIOPOIETIN LIKE 4 PROTEIN; BONE MORPHOGENETIC PROTEIN; F ACTIN; FIBROBLAST GROWTH FACTOR 5; GREMLIN 1 PROTEIN; GREMLIN 4 PROTEIN; INTERALPHA TRYPSIN INHIBITOR HEAVY CHAIN 3; MELANOTRANSFERRIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN; SECRETED FRIZZLED RELATED PROTEIN 1; SECRETED FRIZZLED RELATED PROTEIN 4; TRANSCRIPTION FACTOR RUNX2; TRANSFERRIN; TRANSFORMING GROWTH FACTOR BETA3; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; BIOCHEMICAL COMPOSITION; BIOMECHANICS; CELL CULTURE; CELL ISOLATION; CONTROLLED STUDY; DECELLULARIZATION; DONOR; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; QUANTITATIVE ANALYSIS; TANDEM MASS SPECTROMETRY; TRABECULAR MESHWORK; WNT SIGNALING PATHWAY;

EID: 84969190216     PISSN: None     EISSN: 23739878     Source Type: Journal    
DOI: 10.1021/ab500060r     Document Type: Article

References (72)

1. Ritch, R.; Schlötzer-Schrehardt, U. Exfoliation Syndrome Surv. Ophthalmol. 2001, 45, 265-315 10.1016/S0039-6257(00)00196-X
2. Schlötzer-Schrehardt, U.; von der Mark, K.; Sakai, L. Y.; Naumann, G. O. Increased extracellular deposition of fibrillin-containing fibrils in pseudoexfoliation syndrome Invest. Ophthalmol. Vis. Sci. 1997, 38, 970-984
3. Last, J. A.; Pan, T.; Ding, Y.; Reilly, C. M.; Keller, K.; Acott, T. S.; Fautsch, M. P.; Murphy, C. J.; Russell, P. Elastic modulus determination of normal and glaucomatous human trabecular meshwork Invest. Ophthalmol. Vis. Sci. 2011, 52, 2147-2152 10.1167/iovs.10-6342
4. Camras, L. J.; Stamer, W. D.; Epstein, D.; Gonzalez, P.; Yuan, F. Circumferential Tensile Stiffness of Glaucomatous Trabecular Meshwork Invest. Ophthalmol. Vis. Sci. 2014, 55, 814-823 10.1167/iovs.13-13091
5. Camras, L. J.; Stamer, W. D.; Epstein, D.; Gonzalez, P.; Yuan, F. Differential Effects of Trabecular Meshwork Stiffness on Outflow Facility in Normal Human and Porcine Eyes Invest. Ophthalmol. Vis. Sci. 2012, 53, 5242-5250 10.1167/iovs.12-9825
6. Koliakos, G. G.; Konstas, A. G.; Dimitrakoulias, N.; Triantos, A.; Kardasopoulos, A.; Dimitriadou, A.; Trakatellis, A. C. Possible role of transferrin in exfoliation syndrome Acta Ophthalmol. Scand. 1996, 74, 155-159 10.1111/j.1600-0420.1996.tb00061.x
7. Küchle, M.; Ho, T. S.; Nguyen, N. X.; Hannappel, E.; Naumann, G. O. Protein quantification and electrophoresis in aqueous humor of pseudoexfoliation eyes Invest. Ophthalmol. Vis. Sci. 1994, 35, 748-752
8. Küchle, M.; Nguyen, N. X.; Hannappel, E.; Naumann, G. O. The blood-aqueous barrier in eyes with pseudoexfoliation syndrome Ophthalmic Res. 1995, 27 (Suppl 1) 136-142 10.1159/000267859
9. Küchle, M.; Nguyen, N. X.; Horn, F.; Naumann, G. O. Quantitative assessment of aqueous flare and aqueous cells in pseudoexfoliation syndrome Acta Ophthalmol. (Copenh.) 1992, 70, 201-208 10.1111/j.1755-3768.1992.tb04124.x
10. Koliakos, G. G.; Schlotzer-Schrehardt, U.; Konstas, A. G.; Bufidis, T.; Georgiadis, N.; Dimitriadou, A. Transforming and insulin-like growth factors in the aqueous humour of patients with exfoliation syndrome Graefes Arch. Clin. Exp. Ophthalmol. 2001, 239, 482-487 10.1007/s004170100287
11. Tripathi, R. C.; Li, J.; Chan, W. A.; Tripathi, B. J. Aqueous humor in glaucomatous eyes contains an increased level of TGF-β2 Exp. Eye Res. 1994, 59, 723-728 10.1006/exer.1994.1158
12. Picht, G.; Welge-Luessen, U.; Grehn, F.; Lutjen-Drecoll, E. Transforming growth factor beta 2 levels in the aqueous humor in different types of glaucoma and the relation to filtering bleb development Graefes Arch. Clin. Exp. Ophthalmol. 2001, 239, 199-207 10.1007/s004170000252
13. Prendes, M. A.; Harris, A.; Wirostko, B. M.; Gerber, A. L.; Siesky, B. The role of transforming growth factor β in glaucoma and the therapeutic implications Br. J. Ophthalmol. 2013, 97, 680-686 10.1136/bjophthalmol-2011-301132
14. Yoneda, K.; Nakano, M.; Mori, K.; Kinoshita, S.; Tashiro, K. Disease-related quantitation of TGF-beta3 in human aqueous humor Growth Factors 2007, 25, 160-167 10.1080/08977190701723505
15. Fitzgerald, A. M.; Benz, C.; Clark, A. F.; Wordinger, R. J. The effects of transforming growth factor-β2 on the expression of follistatin and activin A in normal and glaucomatous human trabecular meshwork cells and tissues Invest. Ophthalmol. Vis. Sci. 2012, 53, 7358-7369 10.1167/iovs.12-10292
16. Sethi, A.; Jain, A.; Zode, G. S.; Wordinger, R. J.; Clark, A. F. Role of TGFβ/Smad Signaling in Gremlin Induction of Human Trabecular Meshwork Extracellular Matrix Proteins Invest. Ophthalmol. Vis. Sci. 2011, 52, 5251-5259 10.1167/iovs.11-7587
17. Sethi, A.; Mao, W.; Wordinger, R. J.; Clark, A. F. Transforming Growth Factorβ Induces Extracellular Matrix Protein Cross-Linking Lysyl Oxidase (LOX) Genes in Human Trabecular Meshwork Cells Invest. Ophthalmol. Vis. Sci. 2011, 52, 5240-5250 10.1167/iovs.11-7287
18. Zhao, X.; Ramsey, K. E.; Stephan, D. A.; Russell, P. Gene and Protein Expression Changes in Human Trabecular Meshwork Cells Treated with Transforming Growth Factor-β Invest. Ophthalmol. Vis. Sci. 2004, 45, 4023-4034 10.1167/iovs.04-0535
19. Morgan, J. T.; Wood, J. A.; Walker, N. J.; Raghunathan, V. K.; Borjesson, D. L.; Murphy, C. J.; Russell, P. Human trabecular meshwork cells exhibit several characteristics of, but are distinct from, adipose-derived mesenchymal stem cells J. Ocul. Pharmacol. Ther. 2014, 30, 254-266 10.1089/jop.2013.0175
20. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75, 4646-4658 10.1021/ac0341261
21. Thomasy, S. M.; Raghunathan, V. K.; Winkler, M.; Reilly, C. M.; Sadeli, A. R.; Russell, P.; Jester, J. V.; Murphy, C. J. Elastic modulus and collagen organization of the rabbit cornea: epithelium to endothelium Acta Biomater. 2014, 10, 785-791 10.1016/j.actbio.2013.09.025
22. McKee, C. T.; Raghunathan, V. K.; Nealey, P. F.; Russell, P.; Murphy, C. J. Topographic modulation of the orientation and shape of cell nuclei and their influence on the measured elastic modulus of epithelial cells Biophys. J. 2011, 101, 2139-2146 10.1016/j.bpj.2011.09.042
23. McKee, C. T.; Wood, J. A.; Shah, N. M.; Fischer, M. E.; Reilly, C. M.; Murphy, C. J.; Russell, P. The effect of biophysical attributes of the ocular trabecular meshwork associated with glaucoma on the cell response to therapeutic agents Biomaterials 2011, 32, 2417-2423 10.1016/j.biomaterials.2010.11.071
24. Anseth, K. S.; Bowman, C. N.; Brannon-Peppas, L. Mechanical properties of hydrogels and their experimental determination Biomaterials 1996, 17, 1647-1657 10.1016/0142-9612(96)87644-7
25. Dimitriadis, E. K.; Horkay, F.; Maresca, J.; Kachar, B.; Chadwick, R. S. Determination of Elastic Moduli of Thin Layers of Soft Material Using the Atomic Force Microscope Biophys. J. 2002, 82, 2798-2810 10.1016/S0006-3495(02)75620-8
26. Ahearne, M.; Yang, Y.; El Haj, A. J.; Then, K. Y.; Liu, K. K. Characterizing the viscoelastic properties of thin hydrogel-based constructs for tissue engineering applications J. R.Soc. 2005, 2, 455-463 10.1098/rsif.2005.0065
27. Vinckier, A.; Semenza, G. Measuring elasticity of biological materials by atomic force microscopy FEBS Lett. 1998, 430, 12-16 10.1016/S0014-5793(98)00592-4
28. Hermann, L. R. Elasticity equations for incompressible and nearly incompressible materials by a variational theorem AIAA J. 1965, 3, 1896-1900 10.2514/3.3277
29. Mahaffy, R. E.; Shih, C. K.; MacKintosh, F. C.; Kas, J. Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells Phys. Rev. Lett. 2000, 85, 880-883 10.1103/PhysRevLett.85.880
30. Zhang, B.; VerBerkmoes, N. C.; Langston, M. A.; Uberbacher, E.; Hettich, R. L.; Samatova, N. F. Detecting differential and correlated protein expression in label-free shotgun proteomics J. Proteome Res. 2006, 5, 2909-2918 10.1021/pr0600273
31. Jacobi, P. C.; Krieglstein, G. K. Trabecular aspiration. A new mode to treat pseudoexfoliation glaucoma Invest. Ophthalmol. Vis. Sci. 1995, 36, 2270-2276
32. Jelodari-Mamaghani, S.; Haji-Seyed-Javadi, R.; Suri, F.; Nilforushan, N.; Yazdani, S.; Kamyab, K.; Elahi, E. Contribution of the latent transforming growth factor-β binding protein 2 gene to etiology of primary open angle glaucoma and pseudoexfoliation syndrome Mol. Vis. 2013, 19, 333-347
33. Djordjevic-Jocic, J.; Zlatanovic, G.; Veselinovic, D.; Jovanovic, P.; Djordjevic, V.; Zvezdanovic, L.; Stankovic-Babic, G.; Vujanovic, M.; Cekic, S.; Zenkel, M.; Schlotzer-Schrehardt, U. Transforming growth factor beta1, matrix-metalloproteinase-2 and its tissue inhibitor in patients with pseudoexfoliation glaucoma/syndrome Vojnosanit. Pregl. 2012, 69, 231-236 10.2298/VSP1203231D
34. Kara, S.; Yildirim, N.; Ozer, A.; Colak, O.; Sahin, A. Matrix metalloproteinase-2, tissue inhibitor of matrix metalloproteinase-2, and transforming growth factor beta 1 in the aqueous humor and serum of patients with pseudoexfoliation syndrome Clin. Ophthalmol. 2014, 8, 305-309 10.2147/OPTH.S55914
35. Kottler, U. B.; Junemann, A. G.; Aigner, T.; Zenkel, M.; Rummelt, C.; Schlotzer-Schrehardt, U. Comparative effects of TGF-beta 1 and TGF-beta 2 on extracellular matrix production, proliferation, migration, and collagen contraction of human Tenons capsule fibroblasts in pseudoexfoliation and primary open-angle glaucoma Exp. Eye Res. 2005, 80, 121-134 10.1016/j.exer.2004.08.018
36. Schlötzer-Schrehardt, U.; Küchle, M.; Hofmann-Rummelt, C.; Kaiser, A.; Kirchner, T. [Latent TGF-beta 1 binding protein (LTBP-1); a new marker for intra-and extraocular PEX deposits] Klin Monbl Augenheilkd 2000, 216, 412-419 10.1055/s-2000-10588
37. Schlotzer-Schrehardt, U.; Zenkel, M.; Kuchle, M.; Sakai, L. Y.; Naumann, G. O. Role of transforming growth factor-beta1 and its latent form binding protein in pseudoexfoliation syndrome Exp. Eye Res. 2001, 73, 765-780 10.1006/exer.2001.1084
38. Karamichos, D.; Rich, C. B.; Zareian, R.; Hutcheon, A. E.; Ruberti, J. W.; Trinkaus-Randall, V.; Zieske, J. D. TGF-beta3 Stimulates Stromal Matrix Assembly by Human Corneal Keratocyte-Like Cells Invest. Ophthalmol. Vis. Sci. 2013, 54, 6612-6619 10.1167/iovs.13-12861
39. Raghunathan, V. K.; Morgan, J. T.; Dreier, B.; Reilly, C. M.; Thomasy, S. M.; Wood, J. A.; Ly, I.; Tuyen, B. C.; Hughbanks, M.; Murphy, C. J.; Russell, P. Role of substratum stiffness in modulating genes associated with extracellular matrix and mechanotransducers YAP and TAZ Invest. Ophthalmol. Vis. Sci. 2013, 54, 378-386 10.1167/iovs.12-11007
40. Thomasy, S. M.; Morgan, J. T.; Wood, J. A.; Murphy, C. J.; Russell, P. Substratum stiffness and latrunculin B modulate the gene expression of the mechanotransducers YAP and TAZ in human trabecular meshwork cells Exp. Eye Res. 2013, 113, 66-73 10.1016/j.exer.2013.05.014
41. Thomasy, S. M.; Wood, J. A.; Kass, P. H.; Murphy, C. J.; Russell, P. Substratum stiffness and latrunculin B regulate matrix gene and protein expression in human trabecular meshwork cells Invest. Ophthalmol. Vis. Sci. 2012, 53, 952-958 10.1167/iovs.11-8526
42. Han, H.; Wecker, T.; Grehn, F.; Schlunck, G. Elasticity-dependent modulation of TGF-beta responses in human trabecular meshwork cells Invest. Ophthalmol. Vis. Sci. 2011, 52, 2889-2896 10.1167/iovs.10-6640
43. Schlunck, G.; Han, H.; Wecker, T.; Kampik, D.; Meyer-ter-Vehn, T.; Grehn, F. Substrate Rigidity Modulates Cell-Matrix Interactions and Protein Expression in Human Trabecular Meshwork Cells Invest. Ophthalmol. Vis. Sci. 2008, 49, 262-269 10.1167/iovs.07-0956
44. Wecker, T.; Han, H.; Kneitz, S.; Grehn, F.; Schlunck, G. Influence of Extracellular Matrix Stiffness on Micro-RNA Expression in Human Trabecular Meshwork Cells Biophys. J. 2014, 106, 595a 10.1016/j.bpj.2013.11.3293
45. Koli, K.; Myllarniemi, M.; Vuorinen, K.; Salmenkivi, K.; Ryynanen, M. J.; Kinnula, V. L.; Keski-Oja, J. Bone morphogenetic protein-4 inhibitor gremlin is overexpressed in idiopathic pulmonary fibrosis Am. J. Pathol. 2006, 169, 61-71 10.2353/ajpath.2006.051263
46. Myllarniemi, M.; Lindholm, P.; Ryynanen, M. J.; Kliment, C. R.; Salmenkivi, K.; Keski-Oja, J.; Kinnula, V. L.; Oury, T. D.; Koli, K. Gremlin-mediated decrease in bone morphogenetic protein signaling promotes pulmonary fibrosis Am. J. Respir. Crit. Care Med. 2008, 177, 321-329
47. Carvajal, G.; Droguett, A.; Burgos, M.; Aros, C.; Ardiles, L.; Flores, C.; Carpio, D.; Ruiz-Ortega, M.; Egido, J.; Mezzano, S. Gremlin: a novel mediator of epithelial mesenchymal transition and fibrosis in chronic allograft nephropathy Transplant. Proc. 2008, 40, 734-739 10.1016/j.transproceed.2008.02.064
48. Lee, H.; OMeara, S. J.; OBrien, C.; Kane, R. The role of gremlin, a BMP antagonist, and epithelial-to-mesenchymal transition in proliferative vitreoretinopathy Invest. Ophthalmol. Vis. Sci. 2007, 48, 4291-4299 10.1167/iovs.07-0086
49. Wordinger, R. J.; Fleenor, D. L.; Hellberg, P. E.; Pang, I. H.; Tovar, T. O.; Zode, G. S.; Fuller, J. A.; Clark, A. F. Effects of TGF-beta2, BMP-4, and gremlin in the trabecular meshwork: implications for glaucoma Invest. Ophthalmol. Vis. Sci. 2007, 48, 1191-1200 10.1167/iovs.06-0296
50. Kuchtey, J.; Kallberg, M. E.; Gelatt, K. N.; Rinkoski, T.; Komaromy, A. M.; Kuchtey, R. W. Angiopoietin-like 7 secretion is induced by glaucoma stimuli and its concentration is elevated in glaucomatous aqueous humor Invest. Ophthalmol. Vis. Sci. 2008, 49, 3438-3448 10.1167/iovs.07-1347
51. Gonzalez, P.; Epstein, D. L.; Borrás, T. Characterization of Gene Expression in Human Trabecular Meshwork Using Single-Pass Sequencing of 1060 Clones Invest. Ophthalmol. Vis. Sci. 2000, 41, 3678-3693
52. Tomarev, S. I.; Wistow, G.; Raymond, V.; Dubois, S.; Malyukova, I. Gene Expression Profile of the Human Trabecular Meshwork: NEIBank Sequence Tag Analysis Invest. Ophthalmol. Vis. Sci. 2003, 44, 2588-2596 10.1167/iovs.02-1099
53. Rozsa, F. W.; Reed, D. M.; Scott, K. M.; Pawar, H.; Moroi, S. E.; Kijek, T. G.; Krafchak, C. M.; Othman, M. I.; Vollrath, D.; Elner, V. M.; Richards, J. E. Gene expression profile of human trabecular meshwork cells in response to long-term dexamethasone exposure Mol. Vis. 2006, 12, 125-141
54. Mathieu, M.; Iampietro, M.; Chuchana, P.; Guérit, D.; Djouad, F.; Noël, D.; Jorgensen, C. Involvement of angiopoietin-like 4 in matrix remodeling during chondrogenic differentiation of mesenchymal stem cells J. Biol. Chem. 2014, 289, 8402-8412 10.1074/jbc.M113.539825
55. Goh, Y. Y.; Pal, M.; Chong, H. C.; Zhu, P.; Tan, M. J.; Punugu, L.; Tan, C. K.; Huang, R.-L.; Sze, S. K.; Tang, M. B. Y.; Ding, J. L.; Kersten, S.; Tan, N. S. Angiopoietin-like 4 interacts with matrix proteins to modulate wound healing J. Biol. Chem. 2010, 285, 32999-33009 10.1074/jbc.M110.108175
56. Chomel, C.; Cazes, A.; Faye, C.; Bignon, M.; Gomez, E.; Ardidie-Robouant, C.; Barret, A.; Ricard-Blum, S.; Muller, L.; Germain, S.; Monnot, C. Interaction of the coiled-coil domain with glycosaminoglycans protects angiopoietin-like 4 from proteolysis and regulates its antiangiogenic activity FASEB J. 2009, 23, 940-949 10.1096/fj.08-115170
57. Goh, Y. Y.; Pal, M.; Chong, H. C.; Zhu, P.; Tan, M. J.; Punugu, L.; Lam, C. R. I.; Yau, Y. H.; Tan, C. K.; Huang, R.-L.; Tan, S. M.; Tang, M. B. Y.; Ding, J. L.; Kersten, S.; Tan, N. S. Angiopoietin-like 4 interacts with integrins beta1 and beta5 to modulate keratinocyte migration Am. J. Pathol. 2010, 177, 2791-2803 10.2353/ajpath.2010.100129
58. Choquet, D.; Felsenfeld, D. P.; Sheetz, M. P. Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages Cell 1997, 88, 39-48 10.1016/S0092-8674(00)81856-5
59. Oka, T.; Xu, J.; Kaiser, R. A.; Melendez, J.; Hambleton, M.; Sargent, M. A.; Lorts, A.; Brunskill, E. W.; Dorn, G. W.; Conway, S. J.; Aronow, B. J.; Robbins, J.; Molkentin, J. D. Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling Circ. Res. 2007, 101, 313-321 10.1161/CIRCRESAHA.107.149047
60. Norris, R. A.; Damon, B.; Mironov, V.; Kasyanov, V.; Ramamurthi, A.; Moreno-Rodriguez, R.; Trusk, T.; Potts, J. D.; Goodwin, R. L.; Davis, J.; Hoffman, S.; Wen, X.; Sugi, Y.; Kern, C. B.; Mjaatvedt, C. H.; Turner, D. K.; Oka, T.; Conway, S. J.; Molkentin, J. D.; Forgacs, G.; Markwald, R. R. Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues J. Cell. Biochem. 2007, 101, 695-711 10.1002/jcb.21224
61. Borrás, T.; Comes, N. Evidence for a calcification process in the trabecular meshwork Exp. Eye Res. 2009, 88, 738-746 10.1016/j.exer.2008.11.027
62. Pohjolainen, V.; Rysa, J.; Napankangas, J.; Koobi, P.; Eraranta, A.; Ilves, M.; Serpi, R.; Porsti, I.; Ruskoaho, H. Left ventricular periostin gene expression is associated with fibrogenesis in experimental renal insufficiency Nephrol. Dial. Transplant. 2012, 27, 115-122 10.1093/ndt/gfr279
63. Vittal, V.; Rose, A.; Gregory, K. E.; Kelley, M. J.; Acott, T. S. Changes in gene expression by trabecular meshwork cells in response to mechanical stretching Invest. Ophthalmol. Vis. Sci. 2005, 46, 2857-2868 10.1167/iovs.05-0075
64. Johnson, E. C.; Jia, L.; Cepurna, W. O.; Doser, T. A.; Morrison, J. C. Global Changes in Optic Nerve Head Gene Expression after Exposure to Elevated Intraocular Pressure in a Rat Glaucoma Model Invest. Ophthalmol. Vis. Sci. 2007, 48, 3161-3177 10.1167/iovs.06-1282
65. Didangelos, A.; Yin, X.; Mandal, K.; Baumert, M.; Jahangiri, M.; Mayr, M. Proteomics Characterization of Extracellular Space Components in the Human Aorta Mol. Cell. Proteomics 2010, 9, 2048-2062 10.1074/mcp.M110.001693
66. Lyons, P. J.; Mattatall, N. R.; Ro, H. S. Modeling and functional analysis of AEBP1, a transcriptional repressor Proteins 2006, 63, 1069-1083 10.1002/prot.20946
67. Layne, M. D.; Endege, W. O.; Jain, M. K.; Yet, S.-F.; Hsieh, C.-M.; Chin, M. T.; Perrella, M. A.; Blanar, M. A.; Haber, E.; Lee, M.-E. Aortic Carboxypeptidase-like Protein, a Novel Protein with Discoidin and Carboxypeptidase-like Domains, Is Up-regulated during Vascular Smooth Muscle Cell Differentiation J. Biol. Chem. 1998, 273, 15654-15660 10.1074/jbc.273.25.15654
68. Wang, W. H.; McNatt, L. G.; Pang, I. H.; Millar, J. C.; Hellberg, P. E.; Hellberg, M. H.; Steely, H. T.; Rubin, J. S.; Fingert, J. H.; Sheffield, V. C.; Stone, E. M.; Clark, A. F. Increased expression of the WNT antagonist sFRP-1 in glaucoma elevates intraocular pressure J. Clin. Invest. 2008, 118, 1056-1064 10.1172/JCI3387
69. Zhuo, L.; Hascall, V. C.; Kimata, K. Inter-alpha-trypsin inhibitor, a covalent protein-glycosaminoglycan-protein complex J. Biol. Chem. 2004, 279, 38079-38082 10.1074/jbc.R300039200
70. Zhuo, L.; Kimata, K. Structure and Function of Inter-α-Trypsin Inhibitor Heavy Chains Connect. Tissue Res. 2008, 49, 311-320 10.1080/03008200802325458
71. Michaud-Levesque, J.; Rolland, Y.; Demeule, M.; Bertrand, Y.; Béliveau, R. Inhibition of endothelial cell movement and tubulogenesis by human recombinant soluble melanotransferrin: involvement of the u-PAR/LRP plasminolytic system Biochim. Biophys. Acta 2005, 1743, 243-253 10.1016/j.bbamcr.2004.10.010
72. Rolland, Y.; Demeule, M.; Béliveau, R. Melanotransferrin stimulates t-PA-dependent activation of plasminogen in endothelial cells leading to cell detachment Biochim. Biophys. Acta 2006, 1763, 393-401 10.1016/j.bbamcr.2006.03.006