Post-translationally abnormal collagens of prolyl 3-hydroxylase-2 null mice offer a pathobiological mechanism for the high myopia linked to human LEPREL1 mutations

Journal of Biological Chemistry

Volumn 290, Issue 13, 2015, Pages 8613-8622

  Hudson, David M ^a   Joeng, Kyu Sang ^b   Werther, Rachel ^a   Rajagopal, Abbhirami ^b   Weis, Maryann ^a   Lee, Brendan H ^b   Eyre, David R ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; DIAGNOSIS; GENE ENCODING; HISTOLOGY; MAMMALS; TISSUE;

EARLY DIAGNOSIS; EYE TISSUES; MOLECULAR MECHANISM; VISION LOSS; WILD TYPES;

OPHTHALMOLOGY;

COLLAGEN TYPE 1; COLLAGEN TYPE 4; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROLYL 3 HYDROXYLASE 2; UNCLASSIFIED DRUG; LEPREL1 PROTEIN, HUMAN; LEPREL1 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; COLLAGEN DEFECT; CONTROLLED STUDY; CORNEA; ENZYME ACTIVITY; GENE; GENE MUTATION; HIGH MYOPIA; HYDROXYLATION; KNOCKOUT MOUSE; LENS CAPSULE; LEPREL1 GENE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROCESSING; SCLERA; SCREENING; TENDON; VITREOUS BODY; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; ENZYMOLOGY; GENETIC PREDISPOSITION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; MYOPIA; PATHOLOGY;

MUS;

AMINO ACID SEQUENCE; ANIMALS; COLLAGEN TYPE I; COLLAGEN TYPE IV; CORNEA; GENETIC PREDISPOSITION TO DISEASE; HUMANS; HYDROXYLATION; LENS CAPSULE, CRYSTALLINE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MUTATION; MYOPIA; ORGAN SPECIFICITY; PHENOTYPE; PROCOLLAGEN-PROLINE DIOXYGENASE; PROTEIN PROCESSING, POST-TRANSLATIONAL; SCLERA;

EID: 84925834990     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.634915     Document Type: Article

References (45)

1. Berg, R. A., and Prockop, D. J. (1973) The thermal transition of a nonhydroxylated form of collagen. Evidence for a role for hydroxyproline instabilizing the triple-helix of collagen. Biochem. Biophys. Res. Commun. 52, 115-120
2. Ogle, J. D., Arlinghaus, R. B., and Logan, M. A. (1962) 3-Hydroxyproline, a new amino acid of collagen. J. Biol. Chem. 237, 3667-3673
3. Hudson, D. M., and Eyre, D. R. (2013) Collagen prolyl 3-hydroxylation: a major role for a minor post-translational modification? Connect. Tissue Res. 54, 245-251
4. Hudson, D. M., Weis, M., and Eyre, D. R. (2011) Insights on the evolution of prolyl 3-hydroxylation sites from comparative analysis of chicken and Xenopus fibrillar collagens. PLoS One 6, e19336
5. Weis, M. A., Hudson, D. M., Kim, L., Scott, M., Wu, J. J., and Eyre, D. R. (2010) Location of 3-hydroxyproline residues in collagen types I, II, III, and V/XI implies a role in fibril supramolecular assembly. J. Biol. Chem. 285, 2580-2590
6. Dean, D. C., Barr, J. F., Freytag, J. W., and Hudson, B. G. (1983) Isolation of type IV procollagen-like polypeptides from glomerular basement membrane. Characterization of pro-α1(IV). J. Biol. Chem. 258, 590-596
7. Risteli, J., Bächinger, H. P., Engel, J., Furthmayr, H., and Timpl, R. (1980) 7-S collagen: characterization of an unusual basement membrane structure. Eur. J. Biochem. 108, 239-250
8. Morello, R., Bertin, T. K., Chen, Y., Hicks, J., Tonachini, L., Monticone, M., Castagnola, P., Rauch, F., Glorieux, F. H., Vranka, J., Bächinger, H. P., Pace, J. M., Schwarze, U., Byers, P. H., Weis, M., et al. (2006) CRTAP is required for prolyl 3-hydroxylation and mutations cause recessive osteogenesis imperfecta. Cell 127, 291-304
9. Barnes, A. M., Chang, W., Morello, R., Cabral, W. A., Weis, M., Eyre, D. R., Leikin, S., Makareeva, E., Kuznetsova, N., Uveges, T. E., Ashok, A., Flor, A. W., Mulvihill, J. J., Wilson, P. L., Sundaram, U. T., et al. (2006) Deficiency of cartilage-associated protein in recessive lethal osteogenesis imperfecta. N. Engl. J. Med. 355, 2757-2764
10. Cabral, W. A., Chang, W., Barnes, A. M., Weis, M., Scott, M. A., Leikin, S., Makareeva, E., Kuznetsova, N. V., Rosenbaum, K. N., Tifft, C. J., Bulas, D. I., Kozma, C., Smith, P. A., Eyre, D. R., and Marini, J. C. (2007) Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat. Genet. 39, 359-365
11. Baldridge, D., Schwarze, U., Morello, R., Lennington, J., Bertin, T. K., Pace, J. M., Pepin, M. G., Weis, M., Eyre, D. R., Walsh, J., Lambert, D., Green, A., Robinson, H., Michelson, M., Houge, G., et al. (2008) CRTAP and LEPRE1 mutations in recessive osteogenesis imperfecta. Hum. Mutat. 29, 1435-1442
12. van Dijk, F. S., Nesbitt, I. M., Zwikstra, E. H., Nikkels, P. G., Piersma, S. R., Fratantoni, S. A., Jimenez, C. R., Huizer, M., Morsman, A. C., Cobben, J. M., van Roij, M. H., Elting, M. W., Verbeke, J. I., Wijnaendts, L. C., Shaw, N. J., et al. (2009) PPIB mutations cause severe osteogenesis imperfecta. Am. J. Hum. Genet. 85, 521-527
13. Barnes, A. M., Carter, E. M., Cabral, W. A., Weis, M., Chang, W., Makareeva, E., Leikin, S., Rotimi, C. N., Eyre, D. R., Raggio, C. L., and Marini, J. C. (2010) Lack of cyclophilin B in osteogenesis imperfecta with normal collagen folding. N. Engl. J. Med. 362, 521-528
14. Marini, J. C., Cabral, W. A., and Barnes, A. M. (2010) Null mutations in LEPRE1 and CRTAP cause severe recessive osteogenesis imperfecta. Cell Tissue Res. 339, 59-70
15. Järnum, S., Kjellman, C., Darabi, A., Nilsson, I., Edvardsen, K., and Aman, P. (2004) LEPREL1, a novel ER and Golgi resident member of the Leprecan family. Biochem. Biophys. Res. Commun. 317, 342-351
16. Fernandes, R. J., Farnand, A. W., Traeger, G. R., Weis, M. A., and Eyre, D. R. (2011) A role for prolyl 3-hydroxylase 2 in post-translational modification of fibril-forming collagens. J. Biol. Chem. 286, 30662-30669
17. Guo, H., Tong, P., Peng, Y., Wang, T., Liu, Y., Chen, J., Li, Y., Tian, Q., Hu, Y., Zheng, Y., Xiao, L., Xiong, W., Pan, Q., Hu, Z., and Xia, K. (2014) Homozygous loss-of-function mutation of the LEPREL1 gene causes severe non-syndromic high myopia with early-onset cataract. Clin. Genet. 86, 575-579
18. Mordechai, S., Gradstein, L., Pasanen, A., Ofir, R., El Amour, K., Levy, J., Belfair, N., Lifshitz, T., Joshua, S., Narkis, G., Elbedour, K., Myllyharju, J., and Birk, O. S. (2011) High myopia caused by a mutation in LEPREL1, encoding prolyl 3-hydroxylase. Am. J. Hum. Genet. 89, 438-445
19. Hornbeak, D. M., and Young, T. L. (2009) Myopia genetics: a review of current research and emerging trends. Curr. Opin. Ophthalmol. 20, 356-362
20. Young, T. L., Ronan, S. M., Drahozal, L. A., Wildenberg, S. C., Alvear, A. B., Oetting, W. S., Atwood, L. D., Wilkin, D. J., and King, R. A. (1998) Evidence that a locus for familial high myopia maps to chromosome 18p. Am. J. Hum. Genet. 63, 109-119
21. Phillips, J. R., and McBrien, N. A. (1995) Form deprivation myopia: elastic properties of sclera. Ophthalmic Physiol. Opt. 15, 357-362
22. McBrien, N. A., Jobling, A. I., and Gentle, A. (2009) Biomechanics of the sclera in myopia: extracellular and cellular factors. Optom. Vis. Sci. 86, E23-E30
23. McBrien, N. A., Cornell, L. M., and Gentle, A. (2001) Structural and ultrastructural changes to the sclera in a mammalian model of high myopia. Invest. Ophthalmol. Vis. Sci. 42, 2179-2187
24. Guo, H., Jin, X., Zhu, T., Wang, T., Tong, P., Tian, L., Peng, Y., Sun, L., Wan, A., Chen, J., Liu, Y., Li, Y., Tian, Q., Xia, L., Zhang, L., et al. (2014) SLC39A5 mutations interfering with the BMP/TGF-beta pathway in nonsyndromic high myopia. J. Med. Genet. 51, 518-525
25. Tran-Viet, K. N., Powell, C., Barathi, V. A., Klemm, T., Maurer-Stroh, S., Limviphuvadh, V., Soler, V., Ho, C., Yanovitch, T., Schneider, G., Li, Y. J., Nading, E., Metlapally, R., Saw, S. M., Goh, L., et al. (2013) Mutations in SCO2 are associated with autosomal-dominant high-grade myopia. Am. J. Hum. Genet. 92, 820-826
26. Shi, Y., Li, Y., Zhang, D., Zhang, H., Li, Y., Lu, F., Liu, X., He, F., Gong, B., Cai, L., Li, R., Liao, S., Ma, S., Lin, H., Cheng, J., et, al. (2011) Exome sequencing identifies ZNF644 mutations in high myopia. PLoS Genet. 7, e1002084
27. Aldahmesh, M. A., Khan, A. O., Alkuraya, H., Adly, N., Anazi, S., Al-Saleh, A. A., Mohamed, J. Y., Hijazi, H., Prabakaran, S., Tacke, M., Al-Khrashi, A., Hashem, M., Reinheckel, T., Assiri, A., and Alkuraya, F. S. (2013) Mutations in LRPAP1 are associated with severe myopia in humans. Am. J. Hum. Genet. 93, 313-320
28. Pokidysheva, E., Boudko, S., Vranka, J., Zientek, K., Maddox, K., Moser, M., Fässler, R., Ware, J., and Bächinger, H. P. (2014) Biological role of prolyl 3-hydroxylation in type IV collagen. Proc. Natl. Acad. Sci. U.S.A. 111, 161-166
29. Hanson, D. A., and Eyre, D. R. (1996) Molecular site specificity of pyridinoline and pyrrole cross-links in type I collagen of human bone. J. Biol. Chem. 271, 26508-26516
30. Eyre, D. R., Weis, M., Hudson, D. M., Wu, J. J., and Kim, L. (2011) A novel 3-hydroxyproline (3Hyp)-rich motif marks the triple-helical C terminus of tendon type I collagen. J. Biol. Chem. 286, 7732-7736
31. Hudson, D. M., Werther, R., Weis, M., Wu, J. J., and Eyre, D. R. (2014) Evolutionary origins of C-terminal (GPP)n 3-hydroxyproline formation in vertebrate tendon collagen. PLoS One 9, e93467
32. Vranka, J., Stadler, H. S., and Bächinger, H. P. (2009) Expression of prolyl 3-hydroxylase genes in embryonic and adult mouse tissues. Cell Struct. Funct. 34, 97-104
33. Tiainen, P., Pasanen, A., Sormunen, R., and Myllyharju, J. (2008) Characterization of recombinant human prolyl 3-hydroxylase isoenzyme 2, an enzyme modifying the basement membrane collagen IV. J. Biol. Chem. 283, 19432-19439
34. Pokidysheva, E., Zientek, K. D., Ishikawa, Y., Mizuno, K., Vranka, J. A., Montgomery, N. T., Keene, D. R., Kawaguchi, T., Okuyama, K., and Bächinger, H. P. (2013) Posttranslational modifications in type I collagen from different tissues extracted from wild type and prolyl 3-hydroxylase 1 null mice. J. Biol. Chem. 288, 24742-24752
35. Vranka, J. A., Pokidysheva, E., Hayashi, L., Zientek, K., Mizuno, K., Ishikawa, Y., Maddox, K., Tufa, S., Keene, D. R., Klein, R., and Bächinger, H. P. (2010) Prolyl 3-hydroxylase 1 null mice display abnormalities in fibrillar collagen-rich tissues such as tendons, skin, and bones. J. Biol. Chem. 285, 17253-17262
36. Ishikawa, Y., Vranka, J. A., Boudko, S. P., Pokidysheva, E., Mizuno, K., Zientek, K., Keene, D. R., Rashmir-Raven, A. M., Nagata, K., Winand, N. J., and Bächinger, H. P. (2012) Mutation in cyclophilin B that causes hyperelastosis cutis in American Quarter Horse does not affect peptidylprolyl cis-trans isomerase activity but shows altered cyclophilin B-protein inter-actions and affects collagen folding. J. Biol. Chem. 287, 22253-22265
37. Eyre, D. (1987) Collagen cross-linking amino acids. Methods Enzymol. 144, 115-139
38. Henkel, W., Rauterberg, J., and Stirtz, T. (1976) Isolation of a crosslinked cyanogen-bromide peptide from insoluble rabbit collagen. Tissue differences in hydroxylation and glycosylation of the crosslink. Eur. J. Biochem. 69, 223-231
39. Olson, E. N., Arnold, H. H., Rigby, P. W., and Wold, B. J. (1996) Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell 85, 1-4
40. Ren, S. Y., Angrand, P. O., and Rijli, F. M. (2002) Targeted insertion results in a rhombomere 2-specific Hoxa2 knockdown and ectopic activation of Hoxa1 expression. Dev. Dyn. 225, 305-315
41. Kaufman, R. M., Lu, Z. H., Behl, R., Holt, J. M., Ackers, G. K., and Ley, T. J. (2001) Lack of neighborhood effects from a transcriptionally active phosphoglycerate kinase-neo cassette located between the murine β-major and β-minor globin genes. Blood 98, 65-73
42. Halfter, W., Winzen, U., Bishop, P. N., and Eller, A. (2006) Regulation of eye size by the retinal basement membrane and vitreous body. Invest. Ophthalmol. Vis. Sci. 47, 3586-3594
43. McBrien, N. A., Lawlor, P., and Gentle, A. (2000) Scleral remodeling during the development of and recovery from axial myopia in the tree shrew. Invest. Ophthalmol. Vis. Sci. 41, 3713-3719
44. Liu, H. H., Gentle, A., Jobling, A. I., and McBrien, N. A. (2010) Inhibition of matrix metalloproteinase activity in the chick sclera and its effect on myopia development. Invest. Ophthalmol. Vis. Sci. 51, 2865-2871
45. Gentle, A., Liu, Y., Martin, J. E., Conti, G. L., and McBrien, N. A. (2003) Collagen gene expression and the altered accumulation of scleral collagen during the development of high myopia. J. Biol. Chem. 278, 16587-16594