The Structure of Apo-wild-type Cellular Retinoic Acid Binding Protein II at 1.4 Å and its Relationship to Ligand Binding and Nuclear Translocation

Journal of Molecular Biology

Volumn 363, Issue 3, 2006, Pages 687-701

  Vaezeslami, Soheila ^a   Mathes, Erika ^b   Vasileiou, Chrysoula ^a   Borhan, Babak ^a   Geiger, James H ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cellular retinoic acid binding protein type II; crystal structure; intracellular lipid binding proteins; retinoic acid; retinoic acid binding proteins

Indexed keywords

CELLULAR RETINOIC ACID BINDING PROTEIN II; RETINOIC ACID; RETINOIC ACID BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CRYSTAL STRUCTURE; CRYSTALLIZATION; GENE MUTATION; LIGAND BINDING; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; WILD TYPE;

EID: 33749258949     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.08.059     Document Type: Article

References (65)

1. Giguere V. Retinoic acid receptors and cellular retinoid-binding proteins-complex interplay in retinoid signaling. Endocr. Rev. 15 (1994) 61-79
2. DeLuca L.M. Retinoids and their receptors in differentiation, embryogenesis, and neoplasia. FASEB J. 5 (1991) 2924-2933
3. Gudas L.J., Sporn M.B., and A. B. R. Cellular biology and biochemistry of the retinoids. In: Sporn M.B., Roberts A.B., and Goodman D.S. (Eds). The Retinoids: Biology, Chemistry, and Medicine. 2nd edit. (1994), Raven Press, New York 443-520
4. Lotan R. Effects of vitamin A and its analogs (retinoids) on normal and neoplastic cells. Biochim. Biophys. Acta 605 (1980) 33-91
5. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J. 10 (1996) 940-954
6. Chomienne C., Fenaux P., and Degos L. Retinoid differentiation therapy in promyelocytic leukemia. FASEB J. 10 (1996) 1025-1030
7. Delva L., Bastie J.N., Rochette-Egly C., Kraiba R., Balitrand N., Despouy G., et al. Physical and functional interactions between cellular retinoic acid binding protein II and the retinoic acid-dependent nuclear complex. Mol. Cell. Biol. 19 (1999) 7158-7167
8. Tallman M.S. Differentiating therapy in acute myeloid leukemia. Leukemia 10 (1996) 1262-1268
9. Fisher G.J., and Voorhees J.J. Molecular mechanisms of retinoid actions in skin. FASEB J. 10 (1996) 1002-1013
10. Hong W.K., and Itri L.M. Retinoids and human cancer. In: Sporn M.B., Roberts A.B., and Goodman D.S. (Eds). The Retinoids: Biology, Chemistry, and Medicine. 2nd edit. (1994), Raven Press, New York 597-630
11. Morrisskay G. Retinoic acid and craniofacial development - molecules and morphogenesis. Bioessays 15 (1993) 9-15
12. Mangelsdorf D.J., Thummel C., Beato M., Herrlich P., Schutz G., Umesono K., et al. The nuclear receptor superfamily-The 2nd decade. Cell 83 (1995) 835-839
13. Leroy P., Krust A., Kastner P., Mendelsohn C., Zelent A., and Chambon P. Retinoic Acid Receptors. In: Morriss-Kay G. (Ed). Retinoids in Normal Development and Teratogenesis (1992), Oxford University Press, Oxford 7-25
14. Leid M., Kastner P., Lyons R., Nakshatri H., Saunders M., Zacharewski T., et al. Purification, cloning, and Rxr identity of the Hela-Cell factor with which Rar or Tr Heterodimerizes to bind target sequences efficiently. Cell 68 (1992) 377-395
15. Kreutz M., Fritsche J., Andreesen R., and Krause S.W. Regulation of cellular retinoic acid binding protein (CRABP II) during human monocyte differentiation in vitro. Biochem. Biophys. Res. Commun. 248 (1998) 830-834
16. Kliewer S.A., Umesono K., Mangelsdorf D.J., and Evans R.M. Retinoid X-receptor interacts with nuclear receptors in retinoic acid, thyroid-hormone and vitamin-D3 signaling. Nature 355 (1992) 446-449
17. Sani B.P., and Hill D.L. Retinoic acid-binding-protein in chick-embryo metatarsal skin. Biochem. Biophys. Res. Commun. 61 (1974) 1276-1282
18. Ong D.E., and 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
19. Bailey J.S., and 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
20. Ong D.E., Newcomer M.E., and Chytil F. Cellular retinoid-binding proteins. In: Sporn M.B., Roberts A., and Goodman D.S. (Eds). The Retinoids: Biology, Chemistry, and Medicine. 2nd edit. (1994), Raven Press, New York 283-318
21. Gaub M.P., Lutz Y., Ghyselinck N.B., Scheuer I., Pfister V., Chambon P., and Rochette-Egly C. Nuclear detection of cellular retinoic acid binding proteins I and II with new antibodies. J. Histochem. Cytochem. 46 (1998) 1103-1111
22. Napoli J.L. Retinoic acid homeostasis. Prespective roles of B-carotene, retinol, CRBP and CRABP. In: Blomhoff R. (Ed). Vitamin A in Health and Disease (1994), Marcel Dekker, New York 135-188
23. Napoli J.L. Retinoic acid biosynthesis and metabolism. FASEB J. 10 (1996) 993-1001
24. Napoli J.L. Interactions of retinoid binding proteins and enzymes in retinoid metabolism. Biochim. Biophys. Acta 1440 (1999) 139-162
25. Boylan J.F., and Gudas L.J. Overexpression of the cellular retinoic acid binding protein-I (Crabp-I) results in a reduction in differentiation-specific gene-expression in F9 teratocarcinoma cells. J. Cell. Biol. 112 (1991) 965-979
26. Boylan J.F., and 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
27. Dolle P., Ruberte E., Leroy P., Morrisskay G., and Chambon P. Retinoic acid receptors and cellular retinoid binding-proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development 110 (1990) 1133-1151
28. Maden M. Roles of retinoids in embryonic development. In: Blomhoff R. (Ed). Vitamin A in Health and Disease (1994), Marcel Dekker, New York 289-322
29. Zheng W.L., Bucco R.A., Schmitt M.C., Wardlaw S.A., and Ong D.E. Localization of cellular retinoic acid-binding protein (CRABP) II and CRABP in developing rat testis. Endocrinology 137 (1996) 5028-5035
30. Ong D.E., and Chytil F. Cellular retinoic acid-binding protein from rat testis-purification and characterization. J. Biol. Chem. 253 (1978) 4551-4554
31. Wardlaw S.A., Bucco R.A., Zheng W.L., and Ong D.E. Variable expression of cellular retinol- and cellular retinoic acid-binding proteins in the rat uterus and ovary during the estrous cycle. Biol. Reprod. 56 (1997) 125-132
32. Zheng W.L., and Ong D.E. Spatial and temporal patterns of expression of cellular retinol-binding protein and cellular retinoic acid-binding proteins in rat uterus during early pregnancy. Biol. Reprod. 58 (1998) 963-970
33. Yamamoto M., Drager U.C., Ong D.E., and McCaffery P. Retinoid-binding proteins in the cerebellum and choroid plexus and their relationship to regionalized retinoic acid synthesis and degradation. Eur. J. Biochem. 257 (1998) 344-350
34. Banaszak L., Winter N., Xu Z.H., Bernlohr D.A., Cowan S., and Jones T.A. Lipid-binding proteins-a family of fatty-acid and retinoid transport proteins. Adv. Protein Chem. 45 (1994) 89-151
35. Budhu A., Gillilan R., and Noy N. Localization of the RAR interaction domain of cellular retinoic acid binding protein-II. J. Mol. Biol. 305 (2001) 939-949
36. Budhu A.S., and Noy N. Direct channeling of retinoic acid between cellular retinoic acid-binding protein II and retinoic acid receptor sensitizes mammary carcinoma cells to retinoic acid-induced growth arrest. Mol. Cell. Biol. 22 (2002) 2632-2641
37. Jing Y.K., Waxman S., and Miray 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
38. Takase S., Ong D.E., and Chytil F. Transfer of retinoic acid from its complex with cellular retinoic acid-binding protein to the nucleus. Arch. Biochem. Biophys. 247 (1986) 328-334
39. Dong D., Ruuska S.E., Levinthal D.J., and Noy N. Distinct roles for cellular retinoic acid-binding proteins I and II in regulating signaling by retinoic acid. J. Biol. Chem. 274 (1999) 23695-23698
40. Sessler R.J., and Noy N. A ligand-activated nuclear localization signal in cellular retinoic acid binding protein-II. Mol. Cell. 18 (2005) 343-353
41. Stryer L. Biochemistry. 3rd edit., (1988), W.H. Freeman and Company, New York
42. Cokol M., Nair R., and Rost B. Finding nuclear localization signals. EMBO Rep. 1 (2000) 411-415
43. Chen X., Tordova M., Gilliland G.L., Wang L.C., Li Y., Yan H.G., and Ji X.H. Crystal structure of apo-cellular retinoic acid-binding protein type II (R111M) suggests a mechanism of ligand entry. J. Mol. Biol. 278 (1998) 641-653
44. Kleywegt G.J., Bergfors T., Senn H., Lemotte P., Gsell B., Shudo K., and Jones T.A. Crystal-structures of cellular retinoic acid-binding protein-I and protein-Ii in complex with all-trans-retinoic acid and a synthetic retinoid. Structure 2 (1994) 1241-1258
45. Gunasekaran K., Hagler A.T., and Gierasch L.M. Sequence and structural analysis of cellular retinoic acid-binding proteins reveals a network of conserved hydrophobic interactions. Proteins: Struct. Funct. Genet. 54 (2004) 179-194
46. Wang L.C., and Yan H.G. NMR study suggests a major role for Arg111 in maintaining the structure and dynamical properties of type II human cellular retinoic acid binding protein. Biochemistry 37 (1998) 13021-13032
47. Wang L.C., Li Y., and Yan H.G. 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
48. Winter N.S., Bratt J.M., and Banaszak L.J. Crystal-structures of holo and apo-cellular retinol-binding protein-Ii. J. Mol. Biol. 230 (1993) 1247-1259
49. Xu Z.H., Bernlohr D.A., and Banaszak L.J. Crystal-structure of recombinant murine adipocyte lipid-binding protein. Biochemistry 31 (1992) 3484-3492
50. Kabsch W., and Sander C. Dictionary of protein secondary structure-pattern-recognition of hydrogen-bonded and geometrical features. Biopolymers 22 (1983) 2577-2637
51. Bailey S. The Ccp4 suite - programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
52. Crist R.M., Vasileiou C., Rabago-Smith M., Geiger J.H., and Borhan B. Engineering a Rhodopsin protein surrogate. J. Am. Chem. Soc. 128 (2006) 4522-4523
53. Wang L.C., Li Y., Abildgaard F., Markley J.L., and Yan H.G. NMR solution structure of type II human cellular retinoic acid binding protein: Implications for ligand binding. Biochemistry 37 (1998) 12727-12736
54. Thompson J.R., Bratt J.M., and 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 beta-sheet. J. Mol. Biol. 252 (1995) 433-446
55. Haunerland N.H., Jacobson B.L., Wesenberg G., Rayment I., and Holden H.M. 3-dimensional structure of the muscle fatty-acid-binding protein isolated from the desert locust Schistocerca-Gregaria. Biochemistry 33 (1994) 12378-12385
56. Sacchettini J.C., Gordon J.I., and Banaszak L.J. Refined apoprotein structure of rat intestinal fatty-acid binding-protein produced in Escherichia-Coli-(protein-structure x-ray crystallography fatty acid-protein interactions). Proc. Natl Acad. Sci. USA 86 (1989) 7736-7740
57. Scapin G., Gordon J.I., and 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
58. Xu Z.H., Bernlohr D.A., and 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
59. Bergfors T., Kleywegt G.J., and Jones T.A. Crystallization and preliminary-x-ray analysis of recombinant bovine cellular retinoic acid-binding protein. Acta Crystallog. sect. D 50 (1994) 370-374
60. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. In: Carter Jr. C.W., and Sweet R.M. (Eds). Methods in Enzymology vol. 276 (1997), Academic Press, New York 307-326
61. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
62. Roussel A., and Cambillau C. Turbo-Frodo. Silicon Graphics Geometry Partners Directory (1989), Silicon Graphics, Mountain View
63. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
64. Brunger A.T. Assessment of phase accuracy by cross validation-The Free R-Value-Methods and Applications. Acta Crystallog. sect. D 49 (1993) 24-36
65. Laskowski R.A., Macarthur M.W., Moss D.S., and Thornton J.M. Procheck-A program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-291