The galactolipase activity of some microbial lipases and pancreatic enzymes

European Journal of Lipid Science and Technology

Volumn 115, Issue 4, 2013, Pages 442-451

  Amara, Sawsan ^a   Lafont, Dominique ^b   Parsiegla, Goetz ^a   Point, Vanessa ^a   Chabannes, Aurélie ^a   Rousset, Audric ^b   Carrière, Frédéric ^a  

^a Centre National de la Recherche Scientifique   (France)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

Carboxylester hydrolase; Fusarium solani cutinase; Galactolipid; Pancreatic lipase related protein 2; Thermomyces lanuginosus lipase

Indexed keywords

CAVIA; FUSARIUM SOLANI; THERMOMYCES LANUGINOSUS; TRITICUM AESTIVUM;

EID: 84876085326     PISSN: 14387697     EISSN: 14389312     Source Type: Journal    
DOI: 10.1002/ejlt.201300004     Document Type: Article

References (68)

1. Carter, H. E., McCluer, R. H., Slifer, E. D., Lipids of wheat flour. 1. Characterization of galactosylglycerol components. J. Am. Chem. Soc. 1956, 78, 3735-3738.
2. Benson, A. A., Wiser, R., Ferrari, R. A., Miller, J., Photosynthesis of galactolipids. J. Am. Chem. Soc. 1958, 80, 4740.
3. Jacob, J. S., Miller, K. R., The effects of galactolipid depletion on the structure of a photosynthetic membrane. J. Cell. Biol. 1986, 103, 1337-1347.
4. Kelly, A. A., Dormann, P., Green light for galactolipid trafficking. Curr. Opin. Plant Biol. 2004, 7, 262-269.
5. Schmid, R. D., Verger, R., Lipases: Interfacial enzymes with attractive applications. Angew. Chem. Int. Ed. 1998, 37, 1608-1633.
6. Jaeger, K.-E., Ransac, S., Dijkstra, B. W., Colson, C. et al., Bacterial lipases. FEMS Microbiol. Rev. 1994, 15, 29-63.
7. Andersson, L., Bratt, C., Arnoldsson, K. C., Herslof, B. et al., Hydrolysis of galactolipids by human pancreatic lipolytic enzymes and duodenal contents. J. Lipid Res. 1995, 36, 1392-1400.
8. Andersson, L., Carrière, F., Lowe, M., Nilsson, A., Verger, R., Pancreatic lipase-related protein 2 but not classical pancreatic lipase hydrolyzes galactolipids. Biochim. Biophys. Acta 1996, 1302, 236-240.
9. Roussel, A., Yang, Y., Ferrato, F., Verger, R. et al., Structure and activity of rat pancreatic lipase-related protein 2. J. Biol. Chem. 1998, 273, 32121-32128.
10. Amara, S., Lafont, D., Fiorentino, B., Boullanger, P. et al., Continuous measurement of galactolipid hydrolysis by pancreatic lipolytic enzymes using the pH-stat technique and a medium chain monogalactosyl diglyceride as substrate. Biochim. Biophys. Acta 2009, 1791, 983-990.
11. Amara, S., Barouh, N., Lecomte, J., Lafont, D. et al., Lipolysis of natural long chain and synthetic medium chain galactolipids by pancreatic lipase-related protein 2. Biochim. Biophys. Acta 2010, 1801, 508-516.
12. Sias, B., Ferrato, F., Grandval, P., Lafont, D. et al., Human pancreatic lipase-related protein 2 is a galactolipase. Biochemistry 2004, 43, 10138-10148.
13. Hasson, E. P., Laties, G. G., Separation and characterization of potato lipid acylhydrolases. Plant Physiol. 1976, 57, 142-147.
14. Sakaki, T., Kato, T., Saji, H., Lipid acyl-hydrolase in leaves of different kidney bean (Phaseolus vulgaris L.) cultivars: Purification and characterization of a kidney bean lipid acyl-hydrolase, and foliar lipid changes in the cultivars with ozone exposure. Plant Sci. 2007, 172, 462-472.
15. Matos, A. R., d'Arcy-Lameta, A., Franca, M., Zuily-Fodil, Y., Pham-Thi, A. T., A patatin-like protein with galactolipase activity is induced by drought stress in Vigna unguiculata leaves. Biochem. Soc. Trans. 2000, 28, 779-781.
16. Kim, M. J., Oh, J. M., Cheon, S. H., Cheong, T. K. et al., Thermal inactivation kinetics and application of phospho- and galactolipid-degrading enzymes for evaluation of quality changes in frozen vegetables. J. Agric. Food Chem. 2001, 49, 2241-2248.
17. Terasaki, M., Itabashi, Y., Glycerolipid acyl hydrolase activity in the brown alga Cladosiphon okamuranus TOKIDA. Biosci. Biotechnol. Biochem. 2003, 67, 1986-1989.
18. Li, X., Moellering, E. R., Liu, B., Johnny, C. et al., A Galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell. 2012, 24, 4670-4686.
19. De Caro, J., Sias, B., Grandval, P., Ferrato, F. et al., Characterization of pancreatic lipase-related protein 2 isolated from human pancreatic juice. Biochim. Biophys. Acta 2004, 1701, 89-99.
20. Eydoux, C., De Caro, J., Ferrato, F., Boullanger, P. et al., Further biochemical characterization of human pancreatic lipase-related protein 2 expressed in yeast cells. J. Lipid Res. 2007, 48, 1539-1549.
21. De Caro, J., Eydoux, C., Cherif, S., Lebrun, R. et al., Occurrence of pancreatic lipase-related protein-2 in various species and its relationship with herbivore diet. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2008, 150, 1-9.
22. Withers-Martinez, C., Carrière, F., Verger, R., Bourgeois, D., Cambillau, C., A pancreatic lipase with a phospholipase A1 activity: Crystal structure of a chimeric pancreatic lipase-related protein 2 from guinea pig. Structure 1996, 4, 1363-1374.
23. Eydoux, C., Spinelli, S., Davis, T. L., Walker, J. R. et al., Structure of human pancreatic lipase-related protein 2 with the lid in an open conformation. Biochemistry 2008, 47, 9553-9564.
24. Carrière, F., Withers-Martinez, C., van Tilbeurgh, H., Roussel, A. et al., Structural basis for the substrate selectivity of pancreatic lipases and some related proteins. Biochim. Biophys. Acta 1998, 1376, 417-432.
25. Hjorth, A., Carrière, F., Cudrey, C., Wöldike, H. et al., A structural domain (the lid) found in pancreatic lipases is absent in the guinea pig (phospho)lipase. Biochemistry 1993, 32, 4702-4707.
26. Dawson, R. M. C., Hemington, N., Hazlewood, G. P., On the role of higher plant and microbial lipases in the ruminal hydrolysis of grass lipids. Br. J. Nutr. 1977, 38, 225-232.
27. Fischer, W., Heinz, E., Zeus, M., The suitability of lipase from Rhizopus arrhizus delemar for analysis of fatty acid distribution in dihexosyl diglycerides, phospholipids and plant sulfolipids. Hoppe-Seyler's Z. Physiol. Chem. 1973, 354, 1115-1123.
28. Murakami, N., Morimoto, T., Imamura, H., Nagatsu, A., Sakakibara, J., Enzymatic transformation of glyceroglycolipids into sn-1 and sn-2 lysoglyceroglycolipids by use of Rhizopus arrhizus lipase. Tetrahedron 1994, 50, 1993-2002.
29. Morimoto, T., Nagatsu, A., Murakami, N., Sakakibara, J., Chemoenzymatic synthesis of 1-O-acyl-3-O-(6′-O-acyl-β-D-galactopyranosyl)-sn-glycerol. Tetrahedron Lett. 1995, 51, 6443-6450.
30. Persson, P., Svensson, I., Adlercreutz, P., Enzymatic fatty acid exchange in digalactosyldiacylglycerol. Chem. Phys. Lipids 2000, 104, 13-21.
31. Adlercreutz, P., Virto, C., Persson, M., Vaz, S. et al., Enzymatic conversions of polar lipids. Principles, problems and solutions. J. Mol. Catal. B: Enzym. 2001, 11, 173-178.
32. Prieto, J. A., Ebri, A., Collar, C., Composition and distribution of individual molecular species of major glycolipids in wheat flour. J. Am. Oil Chem. Soc. 1993, 69, 1019-1022.
33. Mas, E., Abouakil, N., Roudani, S., Miralles, F. et al., Human fetoacinar pancreatic protein: An oncofetal glycoform of the normally secreted pancreatic bile-salt-dependent lipase. Biochem. J. 1993, 289, 609-615.
34. Petersen, S. B., Jonson, P. H., Fojan, P., Petersen, E. I. et al., Protein engineering the surface of enzymes. J. Biotechnol. 1998, 66, 11-26.
35. Aloulou, A., Rodriguez, J. A., Puccinelli, D., Mouz, N. et al., Purification and biochemical characterization of the LIP2 lipase from Yarrowia lipolytica. Biochim. Biophys. Acta 2007, 1771, 228-237.
36. Laemmli, U. K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227, 680-685.
37. Amara, S., Delorme, V., Record, M., Carriere, F., Inhibition of phospholipase A1, lipase and galactolipase activities of pancreatic lipase-related protein 2 by methyl arachidonyl fluorophosphonate (MAFP). Biochim. Biophys. Acta 2012, 1821, 1379-1385.
38. Lafont, D., Carriere, F., Ferrato, F., Boullanger, P., Syntheses of an α-D-Gal-(1→6)-β-D-Gal diglyceride as lipase substrate. Carbohydr. Res. 2006, 341, 695-704.
39. Verger, R., de Haas, G. H., Enzyme reactions in a membrane model. 1: A new technique to study enzyme reactions in monolayers. Chem. Phys. Lipids 1973, 10, 127-136.
40. Yapoudjian, S., Ivanova, M. G., Brzozowski, A. M., Patkar, S. A. et al., Binding of Thermomyces (Humicola) lanuginosa lipase to the mixed micelles of cis-parinaric acid/NaTDC. Eur. J. Biochem. 2002, 269, 1613-1621.
41. Trott, O., Olson, A. J., AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 2010, 31, 455-461.
42. Seeliger, D., de Groot, B. L., Ligand docking and binding site analysis with PyMOL and Autodock/Vina. J. Comput. Aided Mol. Des. 2010, 24, 417-422.
43. Schué, M., Maurin, D., Dhouib, R., Bakala N'Goma, J. C. et al., Two secreted cutinase-like proteins from Mycobacterium tuberculosis display very different lipolytic activities related to their physiological function. FASEB J. 2010, 24, 1893-1903.
44. Verger, R., Mieras, M. C. E., de Haas, G. H., Action of phospholipase A at interfaces. J. Biol. Chem. 1973, 248, 4023-4034.
45. Brzozowski, A. M., Derewenda, U., Derewenda, Z. S., Dodson, G. G. et al., A model for interfacial activation in lipases from the structure of a fungal lipase-inhibitor complex. Nature 1991, 351, 491-494.
46. van Tilbeurgh, H., Egloff, M.-P., Martinez, C., Rugani, N. et al., Interfacial activation of the lipase-procolipase complex by mixed micelles revealed by X-ray crystallography. Nature 1993, 362, 814-820.
47. Brzozowski, A. M., Savage, H., Verma, C. S., Turkenburg, J. P. et al., Structural origins of the interfacial activation in Thermomyces (Humicola) lanuginosa lipase. Biochemistry 2000, 39, 15071-15082.
48. Grochulski, P., Li, Y., Schrag, J. D., Cygler, M., Two conformational states of Candida rugosa lipase. Protein Sci. 1994, 3, 82-91.
49. Belle, V., Fournel, A., Woudstra, M., Ranaldi, S. et al., Probing the opening of the pancreatic lipase lid using site-directed spin labeling and epr spectroscopy. Biochemistry 2007, 46, 2205-2214.
50. Carrière, F., Thirstrup, K., Hjorth, S., Ferrato, F. et al., Pancreatic lipase stucture-function relationships by domain exchange. Biochemistry 1997, 36, 239-248.
51. Carvalho, C. M., Aires-Barros, M. R., Cabral, J. M., Cutinase: From molecular level to bioprocess development. Biotechnol. Bioeng. 1999, 66, 17-34.
52. Egmond, M. R., de Vlieg, J., Fusarium solani pisi cutinase. Biochimie 2000, 82, 1015-1021.
53. Kolattukudy, P. E., in: Borgström, B., Brockman, H. (Eds.), Lipases, Elsevier, Amsterdam 1984, pp. 471-504.
54. Lauwereys, M., de Geus, P., de Meutter, J., Stanssens, P., Matthyssens, G., Cloning, expression and characterization of cutinase, a fungal lipolytic enzyme. GBF monogr. 1991, 16, 243-251.
55. Mannesse, M. L., Boots, J. W., Dijkman, R., Slotboom, A. J. et al., Phosphonate analogues of triacylglycerols are potent inhibitors of lipase. Biochim. Biophys. Acta 1995, 1259, 56-64.
56. Mannesse, M. L. M., Cox, R. C., Koops, B. C., Verheij, H. M. et al., Cutinase from Fusarium solani pisi hydrolyzing triglyceride analogues. effect of acyl chain length and position in the substrate molecule on activity and enantioselectivity. Biochemistry 1995, 34, 6400-6407.
57. Mannesse, M. L., de Haas, G. H., van der Hijden, H. T., Egmond, M. R., Verheij, H. M., Chiral preference of cutinase in the reaction with phosphonate inhibitors. Biochem. Soc. Trans. 1997, 25, 165-170.
58. Martinez, C., de Geus, P., Lauwereys, M., Matthyssens, G., Cambillau, C., Fusarium solani cutinase is a lipolytic enzyme with a catalytic serine accessible to solvent. Nature 1992, 356, 615-618.
59. Martinez, C., Degeus, P., Stanssens, P., Lauwereys, M., Cambillau, C., Engineering cysteine mutants to obtain crystallographic phases with a cutinase from Fusarium solani pisi. Protein Eng. 1993, 6, 157-165.
60. Martinez, C., Nicolas, A., van Tilbeurgh, H., Egloff, M. P. et al., Cutinase, a lipolytic enzyme with a preformed oxyanion hole. Biochemistry 1994, 33, 83-89.
61. Longhi, S., Czjzek, M., Lamzin, V., Nicolas, A., Cambillau, C., Atomic resolution (1.0 A) crystal structure of Fusarium solani cutinase: Stereochemical analysis. J. Mol. Biol. 1997, 268, 779-799.
62. Longhi, S., Mannesse, M., Verheij, H. M., De Haas, G. H. et al., Crystal structure of cutinase covalently inhibited by a triglyceride analogue. Protein Sci. 1997, 6, 275-286.
63. Longhi, S., Nicolas, A., Creveld, L., Egmond, M. et al., Dynamics of Fusarium solani cutinase investigated through structural comparison among different crystal forms of its variants. Prot. Struct. Funct. Genet. 1996, 26, 442-458.
64. Prompers, J. J., Groenewegen, A., Hilbers, C. W., Pepermans, H. A., Backbone dynamics of Fusarium solani pisi cutinase probed by nuclear magnetic resonance: The lack of interfacial activation revisited. Biochemistry 1999, 38, 5315-5327.
65. Prompers, J. J., van Noorloos, B., Mannesse, M. L., Groenewegen, A. et al., NMR studies of Fusarium solani pisi cutinase in complex with phosphonate inhibitors. Biochemistry 1999, 38, 5982-5994.
66. Thirstrup, K., Verger, R., Carrière, F., Evidence for a pancreatic lipase subfamily with new kinetic properties. Biochemistry 1994, 33, 2748-2756.
67. Derewenda, U., Swenson, L., Wei, Y. Y., Green, R. et al., Conformational lability of lipases observed in the absence of an oil-water interface. Crystallographic studies of enzymes from the fungi Humicola lanuginosa and Rhizopus delemar. J. Lipid Res. 1994, 35, 524-534.
68. Aloulou, A., Puccinelli, D., De Caro, A., Leblond, Y., Carriere, F., A comparative study on two fungal lipases from Thermomyces lanuginosus and Yarrowia lipolytica shows the combined effects of detergents and pH on lipase adsorption and activity. Biochim. Biophys. Acta 2007, 1771, 1446-1456.