Crystal structure of η-crystallin: Adaptation of a class 1 aldehyde dehydrogenase for a new role in the eye lens

Biochemistry

Volumn 42, Issue 15, 2003, Pages 4349-4356

  Bateman, O A ^a   Purkiss, A G ^a   Van Montfort, R ^a,d   Slingsby, C ^a   Graham, C ^b,c   Wistow, G ^b  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b NATIONAL EYE INSTITUTE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d ASTEX PHARMACEUTICALS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTAL STRUCTURE; DIMERS; ENZYMES; OXIDATION; PROTEINS;

EYE LENSES;

BIOCHEMISTRY;

ALDEHYDE DEHYDROGENASE; CRYSTALLIN; DIMER; ETA CRYSTALLIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; RETINAL; RETINOIC ACID; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; BIOFILTER; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELEPHANT; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; HUMAN; LENS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RETINA; VISUAL ACUITY;

ALDEHYDE DEHYDROGENASE; ANIMALS; BINDING SITES; CATALYTIC DOMAIN; CRYSTALLINS; CRYSTALLOGRAPHY, X-RAY; LENS, CRYSTALLINE; PROTEIN STRUCTURE, TERTIARY; SHREWS;

ELEPHANT; MAMMALIA; SORICIDAE;

EID: 0037461267     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi027367w     Document Type: Article

References (48)

1. Sheikh, S., Ni, L., Hurley, T. D., and Weiner, H. (1997) The potential roles of the conserved amino acids in human liver mitochondrial aldehyde dehydrogenase. J. Biol. Chem. 272, 18817-18822.
2. Vasiliou, V., Pappa, A., and Petersen, D. R. (2000) Role of aldehyde dehydrogenases in endogenous and xenobiotic metabolism. Chem.-Biol. Interact. 129, 1-19.
3. Hempel, J., Nicholas, H., and Lindahl, R. (1993) Aldehyde dehydrogenases: widespread structural and functional diversity within a shared framework. Protein Sci. 2, 1890-1900.
4. Liu, Z.-J., Sun, Y.-J., Rose, J., Chung, Y.-J., Hsiao, C.-D., Chang, W.-R., Kuo, I., Perozich, J., Lindahl, R., Hempel, J., and Wang, B-C. (1997) The first structure of an aldehyde dehydrogenase reveals novel interactions between NAD and the Rossmann fold. Nat. Struct. Biol. 4, 317-326.
5. Steinmetz, C. G., Xie. P., Weiner, H., and Hurley, T. D. (1997) Structure of mitochondrial aldehyde dehydrogenase: the genetic component of ethanol aversion. Structure 5, 701-711.
6. Hammen, P. K., Allali-Hassani, A., Hallenga, K., Hurley, T. D., and Weiner, H. (2002) Multiple conformations of NAD and NADH when bound to human cytosolic and mitochondrial aldehyde dehydrogenase. Biochemistry 41, 7156-7168.
7. Moore, S. A., Baker, H. M., Blythe, T. J., Kitson, K. E., Kitson, T. M., and Baker, E. N. (1998) Sheep liver cytosolic aldehyde dehydrogenase: the structure reveals the basis for the retinal specificity of class 1 aldehyde dehydrogenases. Structure 6, 1541-1551.
8. Ni, L., Zhou, J., Hurley, T. D., and Weiner, H. (1999) Human liver mitochondrial aldehyde dehydrogenase: Three-dimensional structure and the restoration of solubility and activity of chimeric forms. Protein Sci. 8, 2784-2791.
9. Wei, B. X., Ni, L., Hurley, T. D., and Weiner, H. (2000) Cooperativity in niotinamide adenine dinucleotide binding induced by mutations of arginine 475 located at the interface in the human mitochondrial class 2 aldehyde dehydrogenase. Biochemistry 39, 5295-5302.
10. Hurley, T. D., Perez-Miller, S., and Breen, H. (2001) Order and disorder in mitochondrial aldehyde dehydrogenase. Chem.-Biol. Interact. 130-132, 3-14.
11. McBee, J. K., Palczewski, K., Baehr, W., and Pepperberg, D. R. (2001) Confronting complexity: the interlink of phototransduction and retinoid metabolism in the vertebrate retina. Prog. Retinal Eye Res. 20, 469-529.
12. Lin, M., and Napoli, J. L. (2000) cDNA cloning and expression of a human aldehyde dehydrogenase (ALDH) active with 9-cis-retinal and identification of a rat ortholog, ALDH12. J. Biol. Chem. 275, 40106-40112.
13. Lindahl, R. (1992) Aldehyde dehydrogenases and their role in carcinogenesis. Crit. Rev. Biochem. Mol. Biol. 27, 283-335.
14. Niederreither, K., Subbarayan, V., Dolle, P., and Chambon, P. (1999) Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet. 21, 444-448.
15. Bitzer, M., Feldkaemeper, M., and Schaeffel, F. (2002) Visually induced changes in components of the retinoic acid system in fundal layers of the chick. Exp. Eye Res. 70, 97-106.
16. Haselbeck, R. J., Hoffmann, I., and Duester, G. (1999) Distinct functions for Aldh1 and Raldh2 in the control of ligand production for embryonic retinoid signaling pathways. Dev. Genet. 25, 353-364.
17. Grün, F., Hirose, Y., Kawauch, S., Ogura, T., and Umesono, K. (2000) Aldehyde dehydrogenase 6, a cytosolic retinaldehyde dehydrogenase prominently expressed in sensory neuroepithelia during development. J. Biol. Chem. 275, 41210-41218.
18. Wistow, G., and Kim, H. (1991) Lens protein expression in mammals - taxon-specificity and the recruitment of crystallins. J. Mol. Evol. 32, 262-269.
19. Graham, C., Hodin, J., and Wistow, G. (1996) A retinaldehyde dehydrogenase as a structural protein in a mammalian eye lens. J. Biol. Chem. 271, 15623-15628.
20. van Dijk, M. A., Madsen, O., Catzeflis, F., Stanhope, M. J., de Jong, W. W., and Pagel, M. (2001) Protein sequence signatures support the African clade of mammals. Proc. Natl. Acad. Sci. U.S.A. 98, 188-93.
21. Wistow G. J. (1995) in Molecular Biology and Evolution of Crystallins: Gene Recruitment and Multifunctional Proteins in the Eye Lens, R. G. Landes, Austin, TX.
22. Piatigorsky, J., and Wistow, G. (1991) The recruitment of crystallins: new functions precede gene duplication. Science 252, 1078-1079.
23. Wistow, G. (1993) Lens crystallins: gene recruitment and evolutionary dynamism. Trends Biochem. Sci. 18, 301-6.
24. Roll B., Amons R., and de Jong, W. W. (1996) Vitamin A2 bound to cellular retinol-binding protein as ultraviolet filter in the eye lens of the gecko Lygodactylus picturatus. J. Biol. Chem. 271, 10437-10440.
25. Werten, P. J. L., Roll, B., van Aalten, D. M. F., and de Jong, W. W. (2000) Gecko iota-crystallin: how cellular retinol-binding protein became an eye lens ultraviolet filter. Proc. Natl. Acad. Sci. U.S.A. 97, 3282-3287.
26. Zinovieva, R. D., Tomarev, S. I., and Piatigorsky, J. (1993) Aldehyde dehydrogenase-derived omega-crystallins of squid and octopus - specialization for lens expression. J. Biol. Chem. 268, 11449-11455.
27. Piatigorsky, J., Kozmik, Z., Horwitz, J., Ding, L., Carosa, E., Robison, W. G. Jr., Steinbach, P. J., and Tamm, E. R. (2000) Ω-Crystallin of the scallop lens: a dimeric aldehyde dehydrogenase class 1/2 enzyme-crystallin. J. Biol. Chem. 275, 41064-41073.
28. Cooper, D. L., Isola, N. R., Stevenson, K., and Baptist, E. W. (1993) Members of the ALDH gene family are lens and corneal crystallins. Adv. Exp. Med. Biol. 328, 169-179.
29. Piatigorsky, J. (1998) Gene sharing in lens and cornea: facts and implications. Prog. Retinal Eye Res. 17, 145-174.
30. Karaolis, D. K. R., Johnson, J. A., Bailey, C. C., Boedeker, E. C., Kaper, J. B., and Reeves, P. R. (1998) A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc. Natl. Acad. Sci. U.S.A. 95, 3134-3139.
31. Clout, N. J., Kretschmar, M., Jaenicke, R., and Slingsby, C. (2001) Crystal structure of the calcium-loaded spherulin 3a dimer sheds light on the evolution of the eye lens βγ-crystallin domain fold. Structure 9, 115-124.
32. Simpson, A., Bateman, O., Driessen, H., Lindley, P., Moss, D., Mylvaganam, S., Narebor, E., and Slingsby, C. (1994) The structure of avian eye lens delta-crystallin reveals a new fold for a superfamily of oligomeric enzymes. Nat. Struct. Biol. 1, 724-734.
33. Sampaleanu, L. M., Vallee, F., Slingsby, C., and Howell, P. L. (2001) Structural studies of duck delta 1 and delta 2 Crystallin suggest conformational changes occur during catalysis. Biochemistry 40, 2732-2742.
34. Bollag, D. M., and Edelstein, S. J. (1991) Protein Methods, Wiley-Liss, New York.
35. Leslie, A. G. W. (1992) in Joint CCP4 + ESF-EAMCB Newsletter on Protein Corstallography, No. 26.
36. Number 4 Collaborative Computational Project (1994) The CCP4 suite: Programs for the protein crystallography. Acta Crystallogr. D50, 760-763.
37. Navaza, J. (1994) AMoRe: An automated package for molecular replacement. Acta Crystallogr. A50, 157-163.
38. Brunger, A. T., Adams, P. D., Clore, G. M., Delano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software system for macromolecular structure determination. Acta Crystallogr. D54, 905-921.
39. Kleywegt, G. J., and Jones, T. A. (1998) Databases in protein crystallography. Acta Crystallogr. D54, 1119-1131.
40. McRee, D. E. (1999) XtalView/Xfit - A Versatile Program for Manipulating Atomic Coordinates and Electron Density. J. Struct. Biol. 125, 156-165.
41. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of Macromolecular Structures by the Maximum-Likelihood Method. Acta Crystallogr. D53, 240-255.
42. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Boume, P. E. (2000) The Protein Data Bank, Nucleic Acids Res. 28, 235-242.
43. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55.
44. Purkiss (2000) URL: http://people.cryst.bbk.ac.uk/~bpurk01/contax/index.html.
45. Hutchinson, E. G., and Thomton, J. M. (1996) PROMOTIF - A program to identify and analyze structural motifs in proteins. Protein Sci. 5, 212-220.
46. Kleywegt, G. J., and Jones, T. A (1994) Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallogr. D50, 178-185.
47. Lamb, A. L., and Newcomer, M. E. (1999) The structure of retinal dehydrogenase type II at 2.7 Å resolution: implications for retinal specificity. Biochemistry 38, 6003-6011.
48. Cobessi, D., Favier-Tete, F., Marchal, S., Branlant, G., and Aubry, A. (2000) Structural and biochemical investigations of the catalytic mechanism of an NADP-dependent aldehyde dehydrogenase from Streptococcus mutans J. Mol. Biol. 300, 141-152.