Crystal structure of apo-cellular retinoic acid-binding protein type II (R111M) suggests a mechanism of ligand entry

Journal of Molecular Biology

Volumn 278, Issue 3, 1998, Pages 641-653

  Chen, Xin ^a   Tordova, Maria ^b   Gilliland, Gary L ^b   Wang, Lincong ^c   Li, Yue ^c   Yan, Honggao ^c   Ji, Xinhua ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^c Michigan State University   (United States)

Author keywords

Cellular retinoic acid binding protein type II; Crystal structure; Intracellular lipid binding proteins; Ligand entry; Retinoic acid

Indexed keywords

ARGININE; GUANIDINE DERIVATIVE; LIGAND; MUTANT PROTEIN; RETINOIC ACID; RETINOIC ACID BINDING PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 0032496377     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.1734     Document Type: Article

References (58)

1. Bacon D. J., Anderson W. F. A fast algorithm for rendering space-filling molecule pictures. J. Mol. Graph. 6:1988;219-220.
2. Bailey J. S., Siu C. H. Purification and partial characterization of a novel binding protein for retinoic acid from neonatal rat. J. Biol. Chem. 263:1988;9326-9332.
3. Banaszak L., Winter N., Xu Z., Bernlohr D. A., Cowan S., Jones T. A. Lipid-binding proteins: a family of fatty acid and retinoid transport proteins. Advan. Prot. Chem. 45:1994;89-151.
4. Bhat T. N. Calculation of an OMIT map. J. Appl. Crystallog. 21:1988;279-281.
5. Boylan J. F., Gudas L. J. The level of CRABP-I expression influences the amounts and types of all- trans -retinoic acid metabolites in F9 teratocarcinoma stem cells. J. Biol. Chem. 267:1992;21486-21491.
6. Brünger A. T. In X-PLOR (Version 3. 1) Manual. 1992;Yale University Press, New Haven. p. 187-218.
7. Brünger A. T. Assessment of phase accuracy by cross validation: the free R value. Method and applications. Acta Crystallog. sect. D. 49:1993;24-36.
8. Bucco R. A., Zheng W. L., Davis J. T., Sierra-Rivera E., Osteen K. G., Chaudhary A. K., Ong D. E. Cellular retinoic acid-binding protein(II) presence in rat uterine epithelial cells correlates with their synthesis of retinoic acid. Biochemistry. 36:1997;4009-4014.
9. Carson M. Ribbon models of macromolecules. J. Mol. Graph. 5:1987;103-106.
10. Elias P. M., Williams M. L. Retinoids, cancer, and the skin. Arch. Dermatol. 117:1981;160-168.
11. Engh R. A., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A. 47:1991;392-400.
12. Fiorella P. D., Napoli J. L. Expression of cellular retinoic acid binding protein (CRABP) in Escherichia coli. Characterization and evidence that holo-CRABP is a substrate in retinoic acid metabolism. J. Biol. Chem. 266:1991;16572-16579.
13. Fiorella P. D., Napoli J. L. Microsomal retinoic acid metabolism. Effects of cellular retinoic acid-binding protein (type I) and C18-hydroxylation as an initial step. J. Biol. Chem. 269:1994;10538-10544.
14. Furey W., Wang B., Sax M. Crystallographic computing on an array processor. J. Appl. Crystallog. 15:1982;160-166.
15. Giguere V., Ong E. S., Segui P., Evans R. M. Identification of a receptor for the morphogen retinoic acid. Nature. 330:1987;624-629.
16. Gorry P., Lufkin T., Dierich A., Rochette-Egly C., Decimo D., Dolle P., Mark M., Durand B., Chambon P. The cellular retinoic acid binding protein I is dispensable. Proc. Natl Acad. Sci. USA. 91:1994;9032-9036.
17. Gudas L. J., Sporn J., Roberts A. B. Cellular biology and biochemistry of retinoids. Sporn M. B., Roberts A. B., Goodman D. S. THE RETINOIDS: Biology, Chemistry, and Medicine. 1994;443-520 Raven Press, New York.
18. Haunerland N. H., Jacobson B. L., Wesenberg G., Rayment I., Holden H. M. Three-dimensional structure of the muscle fatty-acid-binding protein isolated from the desert locust Schistocerca gregaria. Biochemistry. 33:1994;12378-12385.
19. Hendrickson W. A. Stereochemically restrained refinement of macromolecular structures. Methods Enzymol. 115:1985;252-270.
20. Hodsdon M. E., Cistola D. P. Discrete backbone disorder in the nuclear magnetic resonance structure of apo intestinal fatty acid-binding protein: Implications for the mechanism of ligand entry. Biochemistry. 36:1997a;1450-1460.
21. 1H exchange. Biochemistry. 36:1997b;2278-2290.
22. Hong W. K., Itri L. M. Retinoids and human cancer. Sporn M. B., Roberts A. B., Goodman D. S. THE RETINOIDS: Biology, Chemistry, and Medicine. 1994;597-630 Raven Press, New York.
23. Howard A. J., Gilliland G. L., Finzel B. Z., Poulos T. L., Ohlendorf D. H., Salemme F. R. The use of an imaging proportional counter in macromolecular crystallography. J. Appl. Crystallog. 20:1987;383-387.
24. Hu X., Ji X., Srivastava S. K., Xia H., Awasthi S., Nanduri B., Awasthi Y. C., Zimniak P., Singh S. V. Mechanism of differential catalytic efficiency of two polymorphic forms of human glutathione S-transferase P1-1 in the glutathione conjugation of carcinogenic diol epoxide of chrysene. Arch. Biochem. Biophys. 345:1997a;32-38.
25. Hu X., O'Donnell R., Srivastava S. K., Xia H., Zimniak P., Nanduri B., Bleicher R. J., Awasthi S., Awasthi Y. C., Ji X., Singh S. V. Active site architecture of polymorphic forms of human glutathione S-transferase P1-1 accounts for their enantioselectivity and disparate activity in the glutathione conjugation of 7β,8α-dihydroxy-9α,10α-oxy-7,8,9,10-tetrahydrobenzo(a)pyr ene. Biochem. Biophys. Res. Commun. 235:1997b;424-428.
26. Jamison R. S., Newcomer M. E., Ong D. E. Cellular retinoid-binding proteins: limited proteolysis reveals a conformational change upon ligand binding. Biochemistry. 33:1994;2873-2879.
27. Jing Y., Waxman S., Mira-y-Lopez R. The cellular retinoic acid binding protein II is a positive regulator of retinoic acid signaling in breast cancer cells. Cancer Res. 57:1997;1668-1672.
28. Jones T. A., Zou J.-Y., Cowan S. W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these methods. Acta Crystallog. sect. A. 47:1991;110-119.
29. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:1983;2577-2637.
30. Kleywegt G. J., Bergfors T., Senn H., Le Motte P., Gsell B., Shudo K., Jones T. A. Crystal structures of cellular retinoic acid binding proteins I and II in complex with all- trans -retinoic acid and a synthetic retinoid. Structure. 2:1994;1241-1258.
31. Konnert J. M. A restrained-parameter structure factor least-squares refinement procedure for large asymmetric units. Acta Crystallog. sect. A. 32:1976;614-617.
32. Kraulis P. J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
33. Kunkel T. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl Acad. Sci. USA. 82:1985;488-492.
34. Lampron C., Rochette-Egly C., Gorry P., Dolle P., Mark M., Lufkin T., LeMeur M., Chambon P. Mice deficient in cellular retinoic acid binding protein II (CRABPII) or in both CRABPI and CRABPII are essentially normal. Development. 121:1995;539-548.
35. Laskowski R. A. PROCHECK: a program to check stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
36. Lotan R. Effects of vitamin A and its analogs (retinoids) on normal and neoplastic cells. Biochim. Biophys. Acta. 605:1980;33-91.
37. Mangelsdorf D. J., Ong E. S., Dyck J. A., Evans R. M. Nuclear receptor that identifies a novel retinoic acid response pathway. Nature. 345:1990;224-229.
38. Napoli J. L., Boerman M. H., Chai X., Zhai Y., Fiorella P. D. Enzymes and binding proteins affecting retinoic acid concentrations. J. Steroid Biochem. Mol. Biol. 53:1995;497-502.
39. Navaza J. An automated package for molecular replacement. Acta Crystallog. sect. A. 50:1994;157-163.
40. Newcomer M. E. Retinoid-binding proteins: structural determinants important for function. FASEB J. 9:1995;229-239.
41. Nicholls A., Sharp K. A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
42. Ong D. E., Chytil F. Retinoic acid-binding protein in rat tissue. Partial purification and comparison to rat tissue retinol-binding protein. J. Biol. Chem. 250:1975;6113-6117.
43. Ong D. E., Newcomer M. E., Chytil F. Cellular retinoid-binding proteins. Sporn M. B., Roberts A. B., Goodman D. S. THE RETINOIDS: Biology, Chemistry, and Medicine. 1994;283-317 Raven Press, New York.
44. Petkovich M., Brand N. J., Krust A., Chambon P. A human retinoic acid receptor which belongs to the family of nuclear receptors. Nature. 330:1987;444-450.
45. Powell M. J. D. Restart procedures for the conjugate gradient method. Math. Prog. 12:1977;241-254.
46. 15N resonance assignments and secondary structure of cellular retinoic acid-binding protein with and without bound ligand. J. Biomol. NMR. 4:1994;741-760.
47. Sacchettini J. C., Gordon J. I., Banaszak L. J. Crystal structure of rat intestinal fatty-acid-binding protein. Refinement and analysis of the Escherichia coli -derived protein with bound palmitate. J. Mol. Biol. 208:1989a;327-339.
48. Sacchettini J. C., Gordon J. I., Banaszak L. J. Refined apoprotein structure of rat intestinal fatty acid binding protein produced in Escherichia coli. Proc. Natl Acad. Sci. USA. 86:1989b;7736-7740.
49. Sack J. S. CHAIN: a crystallographic modeling program. J. Mol. Graph. 6:1988;224-225.
50. Sani B. P., Hill D. L. Retinoic acid: a binding protein in chick embryo metatarsal skin. Biochem. Biophys. Res. Commun. 61:1974;1276-1282.
51. Scapin G., Gordon J. I., Sacchettini J. C. Refinement of the structure of recombinant rat intestinal fatty acid-binding apoprotein at 1. 2-Å resolution. J. Biol. Chem. 267:1992;4253-4269.
52. Tallman M. S. Differentiating therapy in acute myeloid leukemia. Leukemia. 10:1996;s33-38.
53. Thompson J. R., Bratt J. M., Banaszak L. J. Crystal structure of cellular retinoic acid binding protein I shows increased access to the binding cavity due to formation of an intermolecular β-sheet. J. Mol. Biol. 252:1995;433-446.
54. Wang L., Li Y., Yan H. Structure-function relationships of cellular retinoic acid-binding proteins. Quantitative analysis of the ligand binding properties of the wild-type proteins and site-directed mutants. J. Biol. Chem. 272:1997;1541-1547.
55. Winter N., Bratt J. M., Banaszak L. J. Crystal structures of holo and apo-cellular retinol-binding protein II. J. Mol. Biol. 230:1993;1247-1259.
56. Xu Z., Bernlohr D. A., Banaszak L. J. Crystal structure of recombinant murine adipocyte lipid-binding protein. Biochemistry. 31:1992;3484-3492.
57. Xu Z., Bernlohr D. A., Banaszak L. J. The adipocyte lipid-binding protein at 1. 6-Å resolution. Crystal structures of the apoprotein and with bound saturated and unsaturated fatty acids. J. Biol. Chem. 268:1993;7874-7884.
58. Zhang J., Liu Z.-P., Jones T. A., Gierasch L. M., Sambrook J. F. Mutating the charged residues in the binding pocket of cellular retinoic acid-binding protein simultaneously reduced its binding affinity to retinoic acid and increases its thermostability. Proteins: Struct. Funct. Genet. 13:1992;87-99.