Fibril core of transforming growth factor beta-induced protein (TGFBIp) facilitates aggregation of corneal TGFBIp

Biochemistry

Volumn 54, Issue 19, 2015, Pages 2943-2956

  Sørensen, Charlotte S ^a,b   Runager, Kasper ^a,b   Scavenius, Carsten ^b   Jensen, Morten M ^b   Nielsen, Nadia S ^b   Christiansen, Gunna ^b   Petersen, Steen V ^b   Karring, Henrik ^c   Sanggaard, Kristian W ^a,b   Enghild, Jan J ^a,b  

^a AARHUS UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATES; AMINO ACIDS; PEPTIDES; PROTEINS;

AMINO ACID SUBSTITUTION; AMYLOID DEPOSITS; AMYLOID FORMATION; CORNEAL STROMA; INDUCED PROTEINS; PATHOPHYSIOLOGY; PROTEIN AGGREGATES; TRANSFORMING GROWTH FACTOR BETA;

GLYCOPROTEINS;

MUTANT PROTEIN; SYNTHETIC PEPTIDE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA INDUCED PROTEIN; UNCLASSIFIED DRUG; BETAIG-H3 PROTEIN; SCLEROPROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CORNEA DYSTROPHY; DEUTERIUM HYDROGEN EXCHANGE; HUMAN; LATTICE CORNEA DYSTROPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR CLONING; PATHOPHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; TRANSMISSION ELECTRON MICROSCOPY; CHEMISTRY; CONGENITAL CORNEA DYSTROPHY; CORNEA STROMA; MASS SPECTROMETRY; METABOLISM;

CORNEAL DYSTROPHIES, HEREDITARY; CORNEAL STROMA; EXTRACELLULAR MATRIX PROTEINS; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84929587128     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00292     Document Type: Article

References (51)

1. LeBaron, R. G., Bezverkov, K. I., Zimber, M. P., Pavelec, R., Skonier, J., and Purchio, A. F. (1995) Beta IG-H3, a novel secretory protein inducible by transforming growth factor-beta, is present in normal skin and promotes the adhesion and spreading of dermal fibroblasts in vitro J. Investig. Dermatol. 104, 844-849
2. Kitahama, S., Gibson, M. A., Hatzinikolas, G., Hay, S., Kuliwaba, J. L., Evdokiou, A., Atkins, G. J., and Findlay, D. M. (2000) Expression of fibrillins and other microfibril-associated proteins in human bone and osteoblast-like cells Bone 27, 61-67
3. Lee, S. H., Bae, J. S., Park, S. H., Lee, B. H., Park, R. W., Choi, J. Y., Park, J. Y., Ha, S. W., Kim, Y. L., Kwon, T. H., and Kim, I. S. (2003) Expression of TGF-beta-induced matrix protein betaig-h3 is up-regulated in the diabetic rat kidney and human proximal tubular epithelial cells treated with high glucose Kidney Int. 64, 1012-1021
4. Escribano, J., Hernando, N., Ghosh, S., Crabb, J., and Coca-Prados, M. (1994) cDNA from human ocular ciliary epithelium homologous to beta ig-h3 is preferentially expressed as an extracellular protein in the corneal epithelium J. Cell. Physiol. 160, 511-521
5. Kannabiran, C. and Klintworth, G. K. (2006) TGFBI gene mutations in corneal dystrophies Hum. Mutat. 27, 615-625
6. Price, F. W. and Price, M. O. (2008) Adult keratoplasty: has the prognosis improved in the last 25 years? Int. Ophthalmol. 28, 141-146
7. Unal, M., Arslan, O. S., Atalay, E., Mangan, M. S., and Bilgin, A. B. (2013) Deep anterior lamellar keratoplasty for the treatment of stromal corneal dystrophies Cornea 32, 301-305
8. Vajpayee, R. B., Tyagi, J., Sharma, N., Kumar, N., Jhanji, V., and Titiyal, J. S. (2007) Deep anterior lamellar keratoplasty by big-bubble technique for treatment corneal stromal opacities Am. J. Ophthalmol. 143, 954-957
9. Fagerholm, P. (2003) Phototherapeutic keratectomy: 12 years of experience Acta Ophthalmol. Scand. 81, 19-32
10. Yao, Y. F., Jin, Y. Q., Zhang, B., Zhou, P., Zhang, Y. M., Qiu, W. Y., Mou, S. L., and Wu, L. Q. (2006) Recurrence of lattice corneal dystrophy caused by incomplete removal of stroma after deep lamellar keratoplasty Cornea 25, S41-S46
11. Kim, T. I., Roh, M. I., Grossniklaus, H. E., Kang, S. J., Hamilton, S. M., Schorderet, D. F., Lee, W. B., and Kim, E. K. (2008) Deposits of transforming growth factor-beta-induced protein in granular corneal dystrophy type II after LASIK Cornea 27, 28-32
12. Aldave, A. J., Sonmez, B., Forstot, S. L., Rayner, S. A., Yellore, V. S., and Glasgow, B. J. (2007) A clinical and histopathologic examination of accelerated TGFBIp deposition after LASIK in combined granular-lattice corneal dystrophy Am. J. Ophthalmol. 143, 416-419
13. Chiti, F. and Dobson, C. M. (2009) Amyloid formation by globular proteins under native conditions Nat. Chem. Biol. 5, 15-22
14. Jahn, T. R., Makin, O. S., Morris, K. L., Marshall, K. E., Tian, P., Sikorski, P., and Serpell, L. C. (2010) The common architecture of cross-beta amyloid J. Mol. Biol. 395, 717-727
15. Yuan, C., Berscheit, H. L., and Huang, A. J. (2007) Identification of an amyloidogenic region on keratoepithelin via synthetic peptides FEBS Lett. 581, 241-247
16. Lakshminarayanan, R., Vithana, E. N., Chai, S. M., Chaurasia, S. S., Saraswathi, P., Venkatraman, A., Rojare, C., Venkataraman, D., Tan, D., Aung, T., Beuerman, R. W., and Mehta, J. S. (2011) A novel mutation in transforming growth factor-beta induced protein (TGFbetaIp) reveals secondary structure perturbation in lattice corneal dystrophy Br. J. Ophthalmol. 95, 1457-1462
17. Dighiero, P., Drunat, S., Ellies, P., DHermies, F., Savoldelli, M., Legeais, J. M., Renard, G., Delpech, M., Grateau, G., and Valleix, S. (2000) A new mutation (A546T) of the betaig-h3 gene responsible for a French lattice corneal dystrophy type IIIA Am. J. Ophthalmol. 129, 248-251
18. Stock, E. L., Feder, R. S., OGrady, R. B., Sugar, J., and Roth, S. I. (1991) Lattice corneal dystrophy type IIIA. Clinical and histopathologic correlations Arch. Ophthalmol. 109, 354-358
19. Runager, K., Basaiawmoit, R. V., Deva, T., Andreasen, M., Valnickova, Z., Sorensen, C. S., Karring, H., Thogersen, I. B., Christiansen, G., Underhaug, J., Kristensen, T., Nielsen, N. C., Klintworth, G. K., Otzen, D. E., and Enghild, J. J. (2011) Human phenotypically distinct TGFBI corneal dystrophies are linked to the stability of the fourth FAS1 domain of TGFBIp J. Biol. Chem. 286, 4951-4958
20. Karring, H., Runager, K., Thogersen, I. B., Klintworth, G. K., Hojrup, P., and Enghild, J. J. (2012) Composition and proteolytic processing of corneal deposits associated with mutations in the TGFBI gene Exp. Eye Res. 96, 163-170
21. Poulsen, E. T., Runager, K., Risor, M. W., Dyrlund, T. F., Scavenius, C., Karring, H., Praetorius, J., Vorum, H., Otzen, D. E., Klintworth, G. K., and Enghild, J. J. (2014) Comparison of two phenotypically distinct lattice corneal dystrophies caused by mutations in the transforming growth factor beta induced (TGFBI) gene Proteomics Clin. Appl. 8, 168-177
22. Karring, H., Poulsen, E. T., Runager, K., Thogersen, I. B., Klintworth, G. K., Hojrup, P., and Enghild, J. J. (2013) Serine protease HtrA1 accumulates in corneal transforming growth factor beta induced protein (TGFBIp) amyloid deposits Mol. Vis. 19, 861-876
23. Runager, K., Garcia-Castellanos, R., Valnickova, Z., Kristensen, T., Nielsen, N. C., Klintworth, G. K., Gomis-Ruth, F. X., and Enghild, J. J. (2009) Purification, crystallization and preliminary X-ray diffraction of wild-type and mutant recombinant human transforming growth factor beta-induced protein (TGFBIp) Acta Crystallogr. Sect. F 65, 299-303
24. Reed, S. E., Staley, E. M., Mayginnes, J. P., Pintel, D. J., and Tullis, G. E. (2006) Transfection of mammalian cells using linear polyethylenimine is a simple and effective means of producing recombinant adeno-associated virus vectors J. Virol. Methods 138, 85-98
25. Bury, A. F. (1981) Analysis of Protein and Peptide Mixtures-Evaluation of 3 Sodium Dodecyl Sulfate-Polyacrylamide Gel-Electrophoresis Buffer Systems J. Chromatogr. 213, 491-500
26. Matsudaira, P. (1987) Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes J. Biol. Chem. 262, 10035-10038
27. Wales, T. E. and Engen, J. R. (2006) Hydrogen exchange mass spectrometry for the analysis of protein dynamics Mass Spectrom. Rev. 25, 158-170
28. Kussmann, M., Nordhoff, E., Rahbek-Nielsen, H., Haebel, S., Rossel-Larsen, M., Jakobsen, L., Gobom, J., Mirgorodskaya, E., KrollKristensen, A., Palm, L., and Roepstorff, P. (1997) Matrix-assisted laser desorption/ionization mass spectrometry sample preparation techniques designed for various peptide and protein analytes J. Mass Spectrom. 32, 593-601
29. Runager, K., Klintworth, G. K., Karring, H., and Enghild, J. J. (2013) The insoluble TGFBIp fraction of the cornea is covalently linked via a disulfide bond to type XII collagen Biochemistry 52, 2821-2827
30. Karring, H., Runager, K., Valnickova, Z., Thogersen, I. B., Moller-Pedersen, T., Klintworth, G. K., and Enghild, J. J. (2010) Differential expression and processing of transforming growth factor beta induced protein (TGFBIp) in the normal human cornea during postnatal development and aging Exp. Eye Res. 90, 57-62
31. Andreasen, M., Nielsen, S. B., Runager, K., Christiansen, G., Nielsen, N. C., Enghild, J. J., and Otzen, D. E. (2012) Polymorphic fibrillation of the destabilized fourth fasciclin-1 domain mutant A546T of the Transforming growth factor-beta-induced protein (TGFBIp) occurs through multiple pathways with different oligomeric intermediates J. Biol. Chem. 287, 34730-34742
32. Yang, J., Han, X., Huang, D., Yu, L., Zhu, Y., Tong, Y., Zhu, B., Li, C., Weng, M., and Ma, X. (2010) Analysis of TGFBI gene mutations in Chinese patients with corneal dystrophies and review of the literature Molecular Vis. 16, 1186-1193
33. Takacs, L., Boross, P., Tozser, J., Modis, L., Jr., Toth, G., and Berta, A. (1998) Transforming growth factor-beta induced protein, betaIG-H3, is present in degraded form and altered localization in lattice corneal dystrophy type I Exp. Eye Res. 66, 739-745
34. Klintworth, G. K., Valnickova, Z., and Enghild, J. J. (1998) Accumulation of beta ig-h3 gene product in corneas with granular dystrophy Am. J. Pathol. 152, 743-748
35. Korvatska, E., Henry, H., Mashima, Y., Yamada, M., Bachmann, C., Munier, F. L., and Schorderet, D. F. (2000) Amyloid and non-amyloid forms of 5q31-linked corneal dystrophy resulting from kerato-epithelin mutations at Arg-124 are associated with abnormal turnover of the protein J. Biol. Chem. 275, 11465-11469
36. Stix, B., Leber, M., Bingemer, P., Gross, C., Ruschoff, J., Fandrich, M., Schorderet, D. F., Vorwerk, C. K., Zacharias, M., Roessner, A., and Rocken, C. (2005) Hereditary lattice corneal dystrophy is associated with corneal amyloid deposits enclosing C-terminal fragments of keratoepithelin Investig. Ophthalmol. Vis. Sci. 46, 1133-1139
37. Hedegaard, C. J., Thogersen, I. B., Enghild, J. J., Klintworth, G. K., and M?ller-Pedersen, T. (2003) Transforming growth factor beta induced protein accumulation in granular corneal dystrophy type III (Reis-Bucklers dystrophy). Identification by mass spectrometry in 15 year old two-dimensional protein gels Mol. Vis. 9, 355-359
38. Grothe, H. L., Little, M. R., Sjogren, P. P., Chang, A. A., Nelson, E. F., and Yuan, C. (2013) Altered protein conformation and lower stability of the dystrophic transforming growth factor beta-induced protein mutants Mol. Vis. 19, 593-603
39. Underhaug, J., Koldso, H., Runager, K., Nielsen, J. T., Sorensen, C. S., Kristensen, T., Otzen, D. E., Karring, H., Malmendal, A., Schiott, B., Enghild, J. J., and Nielsen, N. C. (2013) Mutation in transforming growth factor beta induced protein associated with granular corneal dystrophy type 1 reduces the proteolytic susceptibility through local structural stabilization Biochim. Biophys. Acta 1834, 2812-2822
40. Nazabal, A., Hornemann, S., Aguzzi, A., and Zenobi, R. (2009) Hydrogen/deuterium exchange mass spectrometry identifies two highly protected regions in recombinant full-length prion protein amyloid fibrils J. Mass Spectrom. 44, 965-977
41. French, K. C. and Makhatadze, G. I. (2012) Core sequence of PAPf39 amyloid fibrils and mechanism of pH-dependent fibril formation: the role of monomer conformation Biochemistry 51, 10127-10136
42. Yamaguchi, K., Katou, H., Hoshino, M., Hasegawa, K., Naiki, H., and Goto, Y. (2004) Core and heterogeneity of beta2-microglobulin amyloid fibrils as revealed by H/D exchange J. Mol. Biol. 338, 559-571
43. Carulla, N., Caddy, G. L., Hall, D. R., Zurdo, J., Gairi, M., Feliz, M., Giralt, E., Robinson, C. V., and Dobson, C. M. (2005) Molecular recycling within amyloid fibrils Nature 436, 554-558
44. Sanchez, L., Madurga, S., Pukala, T., Vilaseca, M., Lopez-Iglesias, C., Robinson, C. V., Giralt, E., and Carulla, N. (2011) Abeta40 and Abeta42 amyloid fibrils exhibit distinct molecular recycling properties J. Am. Chem. Soc. 133, 6505-6508
45. Tjernberg, L. O., Lilliehook, C., Callaway, D. J., Naslund, J., Hahne, S., Thyberg, J., Terenius, L., and Nordstedt, C. (1997) Controlling amyloid beta-peptide fibril formation with protease-stable ligands J. Biol. Chem. 272, 12601-12605
46. Tjernberg, L. O., Naslund, J., Lindqvist, F., Johansson, J., Karlstrom, A. R., Thyberg, J., Terenius, L., and Nordstedt, C. (1996) Arrest of beta-amyloid fibril formation by a pentapeptide ligand J. Biol. Chem. 271, 8545-8548
47. Gordon, D. J., Sciarretta, K. L., and Meredith, S. C. (2001) Inhibition of beta-amyloid(40) fibrillogenesis and disassembly of beta-amyloid(40) fibrils by short beta-amyloid congeners containing N-methyl amino acids at alternate residues Biochemistry 40, 8237-8245
48. Findeis, M. A., Musso, G. M., Arico-Muendel, C. C., Benjamin, H. W., Hundal, A. M., Lee, J. J., Chin, J., Kelley, M., Wakefield, J., Hayward, N. J., and Molineaux, S. M. (1999) Modified-peptide inhibitors of amyloid beta-peptide polymerization Biochemistry 38, 6791-6800
49. Bett, C. K., Serem, W. K., Fontenot, K. R., Hammer, R. P., and Garno, J. C. (2010) Effects of peptides derived from terminal modifications of the abeta central hydrophobic core on abeta fibrillization ACS Chem. Neurosci. 1, 661-678
50. Wei, C. W., Peng, Y., Zhang, L., Huang, Q., Cheng, M., Liu, Y. N., and Li, J. (2011) Synthesis and evaluation of ferrocenoyl pentapeptide (Fc-KLVFF) as an inhibitor of Alzheimers Abeta(1)-(4)(2) fibril formation in vitro Bioorg. Med. Chem. Lett. 21, 5818-5821
51. Ladiwala, A. R., Bhattacharya, M., Perchiacca, J. M., Cao, P., Raleigh, D. P., Abedini, A., Schmidt, A. M., Varkey, J., Langen, R., and Tessier, P. M. (2012) Rational design of potent domain antibody inhibitors of amyloid fibril assembly Proc. Natl. Acad. Sci. U.S.A. 109, 19965-19970