Methylation and carbamylation of human γ-crystallins

Protein Science

Volumn 12, Issue 8, 2003, Pages 1762-1774

  Lapko, Veniamin N ^a   Smith, David L ^a   Smith, Jean B ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Cataract; Cysteine S methylation; Human lens crystallins; N terminal acetylation; N terminal carbamylation

Indexed keywords

CYSTEINE; GAMMA B CRYSTALLIN; GAMMA C CRYSTALLIN; GAMMA CRYSTALLIN; GAMMA D CRYSTALLIN; THIOL DERIVATIVE; TRYPSIN; UNCLASSIFIED DRUG;

ACETYLATION; ADOLESCENT; ADULT; AGED; AGING; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBAMOYLATION; CATARACT; CHEMISTRY; CHILD; CONTROLLED STUDY; CROSS LINKING; DISULFIDE BOND; ELECTROSPRAY MASS SPECTROMETRY; HUMAN; HUMAN TISSUE; INFANT; LENS; METABOLISM; METHYLATION; MOLECULAR GENETICS; MOLECULAR WEIGHT; NEWBORN; PHYSIOLOGY; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN PROCESSING; SEQUENCE HOMOLOGY;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; AMINO ACID SEQUENCE; CHILD; CHILD, PRESCHOOL; GAMMA-CRYSTALLINS; HUMANS; INFANT; INFANT, NEWBORN; LENS, CRYSTALLINE; METHYLATION; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TRYPSIN;

EID: 0042343671     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.0305403     Document Type: Article

References (69)

1. Abbasi, A., Smith, D.L., and Smith, J.B. 1998. Characterization of low molecular mass γ-crystallin fragments from human lenses. Exp. Eye Res. 67: 485-488.
2. Armitage, J.P. 1999. Bacterial tactic responses. Adv. Microb. Physiol. 41: 229-289.
3. Bailey, E., Connors, T.A., Farmer, P.B., Gorf, S.M., and Rickard, J. 1981. Methylation of cysteine in hemoglobin following exposure to methylating agents. Cancer Res. 41: 2514-2517.
4. Beswick, H.T. and Harding, J.J. 1984. Conformational changes induced in bovine lens α-crystallin by carbamylation. Biochem. J. 223: 221-227.
5. -. 1987. High-molecular-weight crystallin aggregate formation resulting from non-enzymic carbamylation of lens crystallins: Relevance to cataract formation. Exp. Eye Res. 45: 569-578.
6. Brakenhoff, R.H., Aarts, H.J., Rcek, F.H., Lubsen, N.H., and Schoenmakers, J.G. 1990. Human γ-crystallin genes. A gene family on its way to extinction. J. Mol. Biol. 216: 519-532.
7. Brown, J.L. 1970. The N-terminal region of soluble proteins from procaryotes and eucaryotes. Biochim. Biophys. Acta 221: 480-488.
8. Chadwick, L.H., McCandless, S.E., Silverman, G.L., Schwartz, S., Westaway, D., and Nadeau, J.H. 2000. Betaine-homocysteine methyltransferase-2: cDNA cloning, gene sequence, physical mapping, and expression of the human and mouse genes. Genomics 70: 66-73.
9. Chirgadze, Y.N., Driessen, H.P.C., Wright, G., Slingsby, C., Hay, R.E., and Lindley, P.F. 1996. Structure of the bovine eye lens gD (gIIIb)-crystallin at 1.95 Å. Acta Cryst. D52: 712-721.
10. Cornish, K.M., Williamson, G., and Sanderson, J. 2002. Quercetin metabolism in the lens: Role in inhibition of hydrogen peroxide induced cataract. Free Radic. Biol. Med. 33: 63-70.
11. Crompton, M., Rixon, K.C., and Harding, J.J. 1985. Aspirin prevents carbamylation of soluble lens proteins and prevents cyanate-induced phase separation opacities in vitro: A possible mechanism by which aspirin could prevent cataract. Exp. Eye Res. 40: 297-311.
12. Datiles, M.B., Schumer, D.J., Zigler, J.S., Russell, P., Anderson, L., and Garland, D. 1992. Two-dimensional gel electrophoretic analysis of human lens proteins. Curr. Eye Res. 11: 669-677.
13. Davie, J.K. and Dent, S.Y. 2002, Transcriptional control: An activating role for arginine methylation. Curr. Biol, 12: R59-R61.
14. den Dunnen, J.T., Moormann, R.J.M., Cremers, F.P.M., and Schoenmakers, J.G.G. 1985. Two human γ-crystallin genes are linked and riddled with Alu-repeats. Gene 38: 197-204.
15. Derham, B.K. and Harding, J.J. 1999. α-Crystallin as a molecular chaperone. Prog. Ret. Eye Res. 18: 463-509.
16. Dores, R.M., McDonald, L.K., Steveson, T.C., and Sei, C.A. 1990. The molecular evolution of neuropeptides: Prospects for the '90s. Brain Behav. Evol. 36: 80-99.
17. Driessen, H.P., de Jong, W.W., Tesser, G.I., and Bloemendal, H. 1985. The mechanism of N-terminal acetylation of proteins. CRC Crit. Rev. Biochem. 18: 281-325.
18. Ferranti, P., Sannolo, N., Mamone, G., Fiume, I., Carbone, V., Tornqvist, M., Bergman, A., and Malorni, A. 1996. Structural characterization by mass spectrometry of hemoglobin adducts formed after in vivo exposure to methyl bromide. Carcinogenesis 17: 2661-2671.
19. Friedman, M. 2001. Application of the S-pyridylethylation reaction to the elucidation of the structures and functions of proteins. J. Protein Chem. 20: 431-453.
20. Garner, B., Shaw, D.C., Lindner, R.A., Carver, J.A., and Truscott, R.J. 2000. Non-oxidative modification of lens crystallins by kynurenine: A novel post-translational protein modification with possible relevance to ageing and cataract. Biochim. Biophys. Acta 1476: 265-278.
21. Garrow, T.A. 1996. Purification, kinetic properties, and cDNA cloning of mammalian betaine-homocysteine methyltransferase. J. Biol. Chem. 271: 22831-22838.
22. Geller, A.M., Kotb, M.Y., Jernigan Jr., H.M., and Kredich, N.M. 1986. Purification and properties of rat lens methionine adenosyltransferase. Exp. Eye Res. 43: 997-1008.
23. Golemi, D., Maveyraud, L., Vakulenko, S., Samama, J.P., and Mobashery, S. 2001. Critical involvement of a carbamylated lysine in catalytic function of class D β-lactamases. Proc. Natl. Acad. Sci. 98: 14280-14285.
24. Graw, J. 1997. The crystallins: Genes, proteins and diseases. Biol. Chem. 378: 1331-1348.
25. Hanson, S.R.A., Smith, D.L., and Smith, J.B. 1998. Deamidation and disulfide bonding in the human lens g-crystallins. Exp. Eye Res. 67: 301-312.
26. Hanson, S.R.A., Hasan, A., Smith, D.L., and Smith, J.B. 2000. The major in vivo modifications of the human water-insoluble lens crystallins are disulfide bonds, deamidation, methionine oxidation, and backbone cleavage. Exp. Eye Res. 71: 195-207.
27. Harding, J.J. and Crabbe, M.J.C. 1984. The lens: Development, proteins, metabolism and cataract. In The eye (ed. H. Davson), pp. 207-492. Academic Press, Orlando, FL.
28. Hejtmancik, J.F. 1998. The genetics of cataract: Our vision becomes clearer. Am. J. Hum. Genet. 62: 520-525.
29. Heon, E., Priston, M., Schorderet, D.F., Billingsley, G.D., Girard, P.O., Lubsen, N., and Munier, F.L. 1999. The γ-crystallins and human cataracts: A puzzle made clearer. Am. J. Hum. Genet. 65: 1261-1267.
30. Kelley, M.J., David, L.L., Iwasaki, N., Wright, J., and Shearer, T.R. 1993. α-Crystallin chaperone activity is reduced by calpain II in vitro and in selenite cataract. J. Biol. Chem. 268: 18844-18849.
31. Kendall, R.L., Yamada, R., and Bradshaw, R.A. 1990. Cotranslational amino-terminal processing. Methods Enzymol. 185: 398-407.
32. Kmoch, S., Brynda, J., Asfaw, B., Bezouska, K., Novak, P., Rezacova, P., Ondrova, L., Filipec, M., Sedlacek, J., and Elleder, M. 2000. Link between a novel human γD-crystallin allele and a unique cataract phenotype explained by protein crystallography. Hum. Mol. Genet. 9: 1779-1786.
33. Kodama, T. and Takemoto, L. 1988. Characterization of disulfide-linked crystallins associated with human cataractous lens membranes. Invest. Ophthalmol. Vis. Sci. 29: 145-149.
34. Kouzarides, T. 2002. Histone methylation in transcriptional control. Curr. Opin. Genet. Dev. 12: 198-209.
35. Lampi, K.J., Ma, Z., Hanson, S.R.A., Azuma, M., Shih, M., Shearer, T.R., Smith, D.L., Smith, J.B., and David, L.L. 1998. Age-related changes in human lens crystallins identified by two dimensional gel electrophoresis. Exp. Eye Res. 67: 31-43.
36. Lapko, V.N., Smith, D.L., and Smith, J.B. 2001. In vivo carbamylation and acetylation of water-soluble human lens αB-crystallin lysine 92. Protein Sci. 10: 1130-1136.
37. -. 2002b. S-Methylated cysteines in human lens γ-S crystallins. Biochemistry 41: 14645-14651.
38. Lapko, V.N., Purkiss, A.G., Smith, D.L., and Smith, J.B. 2002a. Deamidation in human γ S-crystallin from cataractous lenses is influenced by surface exposure. Biochemistry 41: 8638-8648.
39. Lorimer, G.H. and Miziorko, H.M. 1980. Carbamate formation on the ε-amino group of a lysyl residue as the basis for the activation of ribulosebisphosphate carboxylase by CO2 and Mg2+. Biochemistry 19: 5321-5328.
40. Ma, Z., Hanson, S.R., Lampi, K., David, L., Smith, D.L., and Smith, J.B. 1998. Age-related changes in human lens crystallins identified by HPLC and mass spectrometry. Exp. Eye Res. 67: 21-30.
41. MacCoss, M.J., McDonald, W.H., Saraf, A., Sadygov, R., Clark, J.M., Tasto, J.J., Gould, K.L., Wolters, D., Washburn, M., Weiss, A., et al. 2002. Shotgun identification of protein modifications from protein complexes and lens tissue, Proc. Natl. Acad. Sci. 99: 7900-7905.
42. Magnaghi-Jaulin, L., Ait-Si-Ali, S., and Harel-Bellan, A. 2000. Histone acetylation and the control of the cell cycle. Prog. Cell Cycle Res. 4: 41-47.
43. Martin, S. and Harding, J.J. 1989. Site of carbamylation of bovine γ-II-crystallin by potassium [14C]cyanate. Biochem. J. 262: 909-915.
44. Meakin, S.O., Breitman, M.L., and Tsui, L.-C. 1985. Structural and evolutionary relationships among five members of the human γ-crystallin gene family. Mol. Cell. Biol. 5: 1408-1414.
45. Miesbauer, L.R., Zhou, X., Yang, Z., Yang, Z., Sun, Y., Smith, D.L., and Smith, J.B. 1994. Post-translational modifications of the water soluble human lens crystallins from young adults. J. Biol. Chem. 269: 12494-12502.
46. Olsson, M. and Lindahl, T. 1980. Repair of alkylated DNA in Escherichia coli. Methyl group transfer from O6-methylguanine to a protein cysteine residue. J. Biol. Chem. 255: 10569-10571.
47. Pace, C.N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. 1995. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4: 2411-2423.
48. Pande, A., Pande, J., Asherie, N., Lomakin, A., Ogun, O., King, J.A., Lubsen, N.H., Walton, D., and Benedek, G.B. 2000. Molecular basis of a progressive juvenile-onset hereditary cataract. Proc. Natl. Acad. Sci. 97: 1993-1998.
49. Park, I.K. and Paik, W.K. 1990. The occurance and analysis of methylated amino acids. In Protein methylation (eds. I.K. Park and W.K. Paik), pp. 1-22. CRC Press, Boca Raton, FL.
50. Potevoda, B., Norbeck, J., Takakura, H., Blomberg, A., and Sherman, F. 1999. Identification and specificities of N-terminal acetyltransferases from Saccharomyces cerevisiae. EMBO J. 18: 6155-6168.
51. Qin, W., Smith, J.B., and Smith, D.L. 1992. Rates of carbamylation of specific lysyl residues in bovine α-crystallins. J. Biol. Chem. 267: 26128-26133.
52. Rao, P.V., Garrow, T.A., John, F., Garland, D., Millian, N.S., and Zigler Jr., J.S. 1998. Betaine-homocysteine methyltransferase is a developmentally regulated enzyme crystallin in rhesus monkey lens. J. Biol. Chem. 273: 30669-30674.
53. Ren, Z., Li, A., Shastry, B.S., Padma, T., Ayyagari, R., Scott, M.H., Parks, M.M., Kaiser-Kupfer, M.I., and Hejtmancik, J.F. 2000. A 5-base insertion in the γC-crystallin gene is associated with autosomal dominant variable zonular pulverulent cataract. Hum. Genet. 106: 531-537.
54. Santhiya, S.T., Shyam Manohar, M., Rawlley, D., Vijayalakshmi, P., Namperumalsamy, P., Gopinath, P.M., Loster, J., and Graw, J. 2002. Novel mutations in the γ-crystallin genes cause autosomal dominant congenital cataracts. J. Med. Genet. 39: 352-358.
55. Smith, J.B., Shun-Shin, G.A., Sun, Y., Miesbauer, L.R., Yang, Z., Yang, Z., Zhou, X., Schwedler, J., and Smith, D.L. 1995. Glutathione adducts, not carbamylated lysines are the major modification of lens α-crystallins from renal failure patients. J. Protein. Chem. 14: 179-188.
56. Smyth, D.G. and Zakarian, S. 1980. Selective processing of β-endorphin in regions of porcine pituitary. Nature 288: 613-615.
57. Stephan, D.A., Gillanders, E., Vanderveen, D., Freas-Lutz, D., Wistow, G., Baxevanis, A.D., Robbins, C.M., VanAuken, A., Quesenberry, M.I., Bailey-Wilson, J., et al. 1999. Progressive juvenile-onset punctate cataracts caused by mutation of the γD-crystallin gene. Proc. Natl. Acad. Sci. 96: 1008-1012.
58. Sterner, D.E. and Berger, S.L. 2000. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64: 435-459.
59. Szilak, L., Finta, C., Patthy, A., Venetianer, P., and Kiss, A. 1994. Self-methylation of BspRI DNA-methyltransferase. Nucleic Acids Res. 22: 2876-2881.
60. Takemoto, L. 1999. Increased cleavage of the C-terminal serine from α-A crystallin present in the high molecular weight aggregate fraction from human and bovine lenses. Curr. Eye Res. 19: 450-455.
61. Takemoto, L. and Gopalarishnan, S. 1994. α-A crystallin: Quantitation of C-terminal modification during lens aging. Curr. Eye Res. 13: 879-883.
62. Takemoto, L.J. and Azari, P. 1977. Isolation and characterization of covalently linked, high molecular weight proteins from human cataractous lens. Exp. Eye Res. 24: 63-70.
63. Tercero, J.C., Dinman, J.D., and Wickner, R.B. 1993. Yeast MAK3 N-acetyl-transferase recognizes the N-terminal four amino acids of the major coat protein (gag) of the L-A double-stranded RNA virus. J. Bacteriol. 175: 3192-3194.
64. Thampi, P., Hassan, A., Smith, J.B., and Abraham, E.C. 2002. Enhanced C-terminal truncation of αA- and αB-crystallins in diabetic lenses, Invest. Ophthalmol. Vis. Sci. 229: 113-118.
65. Tornqvist, M., Osterman-Golkar, S., Kautiainen, A., Naslund, M., Calleman, C.J., and Ehrenberg, L. 1988. Methylations in human hemoglobin. Mutat. Res. 204: 521-529.
66. Tsunasawa, S. and Sakiyama, F. 1984. Amino-terminal acetylation of proteins: An overview. Methods Enzymol. 106: 165-170.
67. Van Driessche, G., Vandenberghe, I., Jacquemotte, F., Devreese, B., and Van Becumen, J.J. 2002. Mass spectrometric identification of in vivo carbamylation of the amino terminus of Ectothiorhodospira mobilis high-potential iron-sulfur protein, isozyme 1. J. Mass Spectrom. 37: 858-866.
68. van Heyningen, R. and Harding, J.J. 1988. A case-control study of cataract in Oxfordshire: Some risk factors. Br. J. Ophthalmol. 72: 804-808.
69. Wistow, G.J. and Piatigorsky, J. 1988. Lens crystallins: The evolution and expression of proteins for a highly specialized tissue. Annu. Rev. Biochem. 57: 479-504.