Enzymatic activity of Lecithin:retinol acyltransferase: A thermostable and highly active enzyme with a likely mode of interfacial activation

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1844, Issue 6, 2014, Pages 1128-1136

  Horchani, Habib ^b   Bussières, Sylvain ^b   Cantin, Line ^b   Lhor, Mustapha ^b   Laliberté Gemme, Jean Sébastien ^b   Breton, Rock ^b   Salesse, Christian ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Enzymatic activity; Lecithin:retinol acyltransferase; Retinol; Thermostability; Truncated LRAT; Visual cycle

Indexed keywords

LECITHIN RETINOL ACYLTRANSFERASE; PHOSPHOLIPASE; PHOSPHOLIPID;

ALKALINITY; ARTICLE; CIRCULAR DICHROISM; ENZYMATIC ASSAY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME KINETICS; ENZYME MODIFICATION; ENZYME STABILITY; ENZYME STRUCTURE; EXTRACTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; INFRARED SPECTROSCOPY; LIPID HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; SOLUBILIZATION; STORAGE TEMPERATURE; TEMPERATURE DEPENDENCE;

ENZYMATIC ACTIVITY; LECITHIN:RETINOL ACYLTRANSFERASE; RETINOL; THERMOSTABILITY; TRUNCATED LRAT; VISUAL CYCLE;

ACYLTRANSFERASES; CIRCULAR DICHROISM; ESCHERICHIA COLI; HOT TEMPERATURE; HUMANS; KINETICS; LECITHINS; MICELLES; PHOSPHOLIPID ETHERS; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SPECTROPHOTOMETRY, INFRARED; SUBSTRATE SPECIFICITY; VITAMIN A;

EID: 84898619141     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2014.02.022     Document Type: Article

References (56)

1. P.N. MacDonald, and D.E. Ong Evidence for a lecithin-retinol acyltransferase activity in the rat small intestine J. Biol. Chem. 263 1988 12478 12482 (Pubitemid 19000429)
2. J.C. Saari, and D.L. Bredberg Lecithin:retinol acyltransferase in retinal pigment epithelial microsomes J. Biol. Chem. 264 1989 8636 8640 (Pubitemid 19151579)
3. M.C. Schmitt, and D.E. Ong Expression of cellular retinol-binding protein and lecithin-retinol acyltransferase in developing rat testis Biol. Reprod. 49 1993 972 979 (Pubitemid 23313821)
4. P.N. MacDonald, and D.E. Ong A lecithin:retinol acyltransferase activity in human and rat liver Biochem. Biophys. Res. Commun. 156 1988 157 163
5. O.L. Francone, and C.J. Fielding Structure-function relationships in human lecithin:cholesterol acyltransferase. Site-directed mutagenesis at serine residues 181 and 216 Biochemistry 30 1991 10074 10077
6. O.L. Francone, and C.J. Fielding Effects of site-directed mutagenesis at residues cysteine-31 and cysteine-184 on lecithin-cholesterol acyltransferase activity Proc. Natl. Acad. Sci. U. S. A. 88 1991 1716 1720 (Pubitemid 21916296)
7. R.R. Rando The biochemistry of the visual cycle Chem. Rev. 101 2001 1881 1896 (Pubitemid 35377790)
8. A. Ruiz, A. Winston, Y.-H. Lim, B.A. Gilbert, R.R. Rando, and D. Bok Molecular and biochemical characterization of lecithin retinol acyltransferase J. Biol. Chem. 274 1999 3834 3841 (Pubitemid 29077233)
9. W.J. Jahng, L. Xue, and R.R. Rando Lecithin retinol acyltransferase is a founder member of a novel family of enzymes Biochemistry 42 2003 12805 12812 (Pubitemid 37385811)
10. P.J. Hughes, and G. Stanway The 2A proteins of three diverse picornaviruses are related to each other and to the H-rev107 family of proteins involved in the control of cell proliferation J. Gen. Virol. 81 2000 201 207 (Pubitemid 30047923)
11. A. Hajnal, R. Klemenz, and R. Schafer Subtraction cloning of H-rev107, a gene specifically expressed in H-ras resistant fibroblasts Oncogene 9 1994 479 490 (Pubitemid 24041527)
12. W. Hanna-Rose, and M. Han The Caenorhabditis elegans EGL-26 protein mediates vulval cell morphogenesis Dev. Biol. 241 2002 247 258 (Pubitemid 34098690)
13. C. Sers, U. Emmenegger, K. Husmann, K. Bucher, A.C. Andres, and R. Schafer Growth-inhibitory activity and downregulation of the class II tumor-suppressor gene H-rev107 in tumor cell lines and experimental tumors J. Cell Biol. 136 1997 935 944 (Pubitemid 27098748)
14. M. Golczak, and K. Palczewski An acyl-covalent enzyme intermediate of lecithin:retinol acyltransferase J. Biol. Chem. 285 2010 29217 29222
15. M.S. Mondal, A. Ruiz, D. Bok, and R.R. Rando Lecithin retinol acyltransferase contains cysteine residues essential for catalysis Biochemistry 39 2000 5215 5220 (Pubitemid 30241644)
16. M. Jin, S. Li, W.N. Moghrabi, H. Sun, and G.H. Travis Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium Cell 122 2005 449 459 (Pubitemid 41127145)
17. G. Moiseyev, Y. Chen, Y. Takahashi, B.X. Wu, and J.X. Ma RPE65 is the isomerohydrolase in the retinoid visual cycle Proc. Natl. Acad. Sci. U. S. A. 102 2005 12413 12418 (Pubitemid 41266373)
18. P.D. Kiser, M. Golczak, A. Maeda, and K. Palczewski Key enzymes of the retinoid (visual) cycle in vertebrate retina Biochim. Biophys. Acta 1821 2012 137 151
19. J.C. Saari Vitamin A metabolism in rod and cone visual cycles Annu. Rev. Nutr. 32 2012 125 145
20. T.D. Lamb, and E.N. Pugh Jr. Dark adaptation and the retinoid cycle of vision Prog. Retin. Eye Res. 23 2004 307 380 (Pubitemid 38737131)
21. J. von Lintig, P.D. Kiser, M. Golczak, and K. Palczewski The biochemical and structural basis for trans-to-cis isomerization of retinoids in the chemistry of vision Trends Biochem. Sci. 35 2010 400 410
22. R.O. Parker, and R.K. Crouch Retinol dehydrogenases (RDHs) in the visual cycle Exp. Eye Res. 91 2010 788 792
23. A.R. Moise, M. Golczak, Y. Imanishi, and K. Palczewski Topology and membrane association of lecithin: retinol acyltransferase J. Biol. Chem. 282 2007 2081 2090 (Pubitemid 47076711)
24. S. Bussières, L. Cantin, B. Desbat, and C. Salesse Binding of a truncated form of lecithin:retinol acyltransferase and its N- and C-terminal peptides to lipid monolayers Langmuir 28 2012 3516 3523
25. D. Bok, A. Ruiz, O. Yaron, W.J. Jahng, A. Ray, L. Xue, and R.R. Rando Purification and characterization of a transmembrane domain-deleted form of lecithin retinol acyltransferase Biochemistry 42 2003 6090 6098 (Pubitemid 36608916)
26. R.R. Rando Membrane-bound lecithin-retinol acyltransferase Biochem. Biophys. Res. Commun. 292 2002 1243 1250 (Pubitemid 34681093)
27. L. Xue, and R.R. Rando Roles of cysteine 161 and tyrosine 154 in the lecithin retinol acyltransferase mechanism Biochemistry 43 2004 6120 6126 (Pubitemid 38669480)
28. J.W. Chisholm, A.K. Gebre, and J.S. Parks Characterization of C-terminal histidine-tagged human recombinant lecithin:cholesterol acyltransferase J. Lipid Res. 40 1999 1512 1519 (Pubitemid 29379993)
29. I. Bustos-Jaimes, R. Mora-Lugo, M.L. Calcagno, and A. Farrés Kinetic studies of Gly28:Ser mutant form of Bacillus pumilus lipase: Changes in kcat and thermal dependence Biochim. Biophys. Acta 1804 2010 2222 2227
30. N.C. Benson, and V. Daggett Dynameomics: large-scale assessment of native protein flexibility Protein Sci. 17 2008 2038 2050
31. S. Bussières, T. Buffeteau, B. Desbat, R. Breton, and C. Salesse Secondary structure of a truncated form of lecithin retinol acyltransferase in solution and evidence for its binding and hydrolytic action in monolayers Biochim. Biophys. Acta 1778 2008 1324 1334
32. J. Boldnigh, H.R. Camma, F.D. Collins, R.A. Morton, N.T. Gridgeman, O. Isler, M. Kofler, R.J. Taylor, A.S. Welland, and T. Bradbury Pure all-trans vitamin A acetate and the assessment of vitamin A potency by spectrophotometry Nature (London) 168 1951 598
33. A.C. Ross Separation and quantitation of retinyl esters and retinol by high-performance liquid chromatography Methods Enzymol. 123 1986 68 74 (Pubitemid 16045240)
34. E. Trudel, S. Beaufils, A. Renault, R. Breton, and C. Salesse Binding of RPE65 fragments to lipid monolayers and identification of its partners by glutathione S-transferase pull-down assays Biochemistry 45 2006 3337 3347 (Pubitemid 43376352)
35. R. Verger, and G.H. De Haas Interfacial enzyme kinetics of lipolysis Annu. Rev. Biophys. Bioeng. 5 1976 77 117
36. E.R. Berman, J. Horowitz, N. Segal, S. Fisher, and L. Feeney-Burns Enzymatic esterification of vitamin A in the pigment epithelium of bovine retina Biochim. Biophys. Acta 630 1980 36 46 (Pubitemid 10019434)
37. Y. Gargouri, G. Pieroni, P.A. Lowe, L. Sarda, and R. Verger Human gastric lipase Eur. J. Biochem. 156 1986 305 310
38. Y. Ben Ali, H. Chahinian, S. Petry, G. Muller, F. Carrière, R. Verger, and A. Abousalham Might the kinetic behavior of hormone-sensitive lipase reflect the absence of the lid domain? Biochemistry 43 2004 9298 9306 (Pubitemid 38955463)
39. S. Adimoolam, L. Jin, E. Grabbe, J.J. Shieh, and A. Jonas Structural and functional properties of two mutants of lecithin-cholesterol acyltransferase (T123I and N228K) J. Biol. Chem. 273 1998 32561 32567 (Pubitemid 28557634)
40. S. Furuyoshi, Y.Q. Shi, and R.R. Rando Acyl group transfer from the sn-1 position of phospholipids in the biosynthesis of n-dodecyl palmitate Biochemistry 32 1993 5425 5430 (Pubitemid 23167984)
41. K. Potvin-Fournier, T. Lefèvre, A. Picard-Lafond, G. Valois-Paillard, L. Cantin, C. Salesse, and M. Auger The thermal stability of recoverin depends on calcium binding and its myristoyl moiety as revealed by infrared spectroscopy Biochemistry 53 2013 48 56
42. V. Voet, and J.G. Voet Biochemistry 1997 John Wiley & Sons
43. L. Xue, W.J. Jahng, D. Gollapalli, and R.R. Rando Palmitoyl transferase activity of lecithin retinol acyl transferase Biochemistry 45 2006 10710 10718 (Pubitemid 44320486)
44. J.L. Kaar Lipase activation and stabilization in room-temperature ionic liquids Methods Mol. Biol. 679 2011 25 35
45. A. Clark, D. Saunderson, and A. Suggett Infrared and laser-Raman spectroscopic studies of thermally-induced globular protein gels Int. J. Pept. Protein Res. 17 1981 353 364
46. A. Dong, S. Prestrelski, S. Allison, and J. Carpenter Infrared spectroscopic studies of lyophilization- and temperature-induced protein aggregation J. Pharm. Sci. 84 1995 415 424
47. W.K. Surewicz, A.G. Szabo, and H.H. Mantsch Conformational properties of azurin in solution as determined from resolution-enhanced Fourier-transform infrared spectra Eur. J. Biochem. 167 1987 519 523
48. W. Surewicz, J. Leddy, and H. Mantsch Structure, stability, and receptor interaction of cholera toxin as studied by Fourier-transform infrared spectroscopy Biochemistry 29 1990 8106 8111 (Pubitemid 20283296)
49. E. Labruyere, M. Mock, W.K. Surewicz, H.H. Mantsch, T. Rose, H. Munier, R.S. Sarfati, and O. Barzu Structural and ligand-binding properties of a truncated form of Bacillus anthracis adenylate cyclase and of a catalytically inactive variant in which glutamine substitutes for lysine-346 Biochemistry 30 1991 2619 2624
50. A. Muga, H.H. Mantsch, and W.K. Surewicz Membrane binding induces destabilization of cytochrome c structure Biochemistry 30 1991 7219 7224
51. A.A. Ismail, H.H. Mantsch, and P.T.T. Wong Aggregation of chymotrypsinogen: portrait by infrared spectroscopy Biochim. Biophys. Acta 1121 1992 183 188
52. M. Jackson, and H.H. Mantsch The use and misuse of FTIR spectroscopy in the determination of protein structure Crit. Rev. Biochem. Mol. Biol. 30 1995 95 120
53. T. Theophanides, J. Anastassopoulou, N. Fotopoulos, U. Görne-Tschelnokow, D. Naumann, W. Mäntele, C. Schultz, and F. Hucho FTIR studies of the acetylcholine receptor; secondary structure, temperature behaviour, agonist induced changes and linear dichroitic measurements Fifth International Conference on the Spectroscopy of Biological Molecules 1993 403 404
54. M. Urbanova, P. Pancoska, and T.A. Keiderling Spectroscopic study of the temperature-dependent conformation of glucoamylase Biochim. Biophys. Acta 1203 1993 290 294 (Pubitemid 24027135)
55. U. Görne-Tschelnokow, D. Naumann, C. Weise, and F. Hucho Secondary structure and temperature behaviour of acetylcholinesterase Eur. J. Biochem. 213 1993 1235 1242
56. F. Tanfani, E. Bertoli, M. Signorini, and C.M. Bergamini Structural investigation of transglutaminase by Fourier transform infrared spectroscopy Eur. J. Biochem. 218 1993 499 505 (Pubitemid 24003766)