A Lys49 phospholipase A2, isolated from Bothrops asper snake venom, induces lipid droplet formation in macrophages which depends on distinct signaling pathways and the C-terminal region

BioMed Research International

Volumn 2013, Issue , 2013, Pages

  Cristina Giannotti, Karina ^a   Leiguez, Elbio ^a   Moreira, Vanessa ^a   Nascimento, Neide Galvão ^a   Lomonte, Bruno ^b   Gutiérrez, José Maria ^b   Lopes De Melo, Robson ^a   Teixeira, Catarina ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSIDAD DE COSTA RICA   (Costa Rica)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; BROMOENOL LACTONE; CALCIUM INDEPENDENT PHOSPHOLIPASE A2; CYTOSOLIC PHOSPHOLIPASE A2; FAT DROPLET; LYSINE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; MT II; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PHOSPHOLIPASE A2; PHOSPHOLIPASE A2 INHIBITOR; PROSTAGLANDIN E2; PROTEIN KINASE; PROTEIN KINASE C INHIBITOR; PYRROLIDINE 2; SECRETORY PHOSPHOLIPASE A2; SNAKE VENOM; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; LIPID; LYSINE; PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BOTHROPS; BOTHROPS ASPER; CARBOXY TERMINAL SEQUENCE; CELL ACTIVATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; MACROPHAGE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; ANIMAL; CATALYSIS; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ANIMALS; BOTHROPS; CATALYSIS; CELL SURVIVAL; LIPIDS; LYSINE; MACROPHAGES; MALE; MICE; PEPTIDES; PHOSPHOLIPASES A2; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; SNAKE VENOMS;

EID: 84874590814     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2013/807982     Document Type: Article

References (59)

1. Kaiser I. I., Gutiérrez J. M., Plummer D., Aird S. D., Odell G. V., The amino acid sequence of a myotoxic phospholipase from the venom of Bothrops asper. Archives of Biochemistry and Biophysics 1990 278 2 319 325 2-s2.0-0025218978 10.1016/0003-9861(90)90266-2 (Pubitemid 20126058)
2. 2 Enzymes: Structure, Function and Mechanisms 1997 Nova York, NY, USA Wiley
3. 2 homologues: dissociation between enzymatic and biological activities. European Journal of Pharmacology 1998 343 2-3 257 263 2-s2.0-0032545928 10.1016/S0014-2999(97)01546- X (Pubitemid 28138610)
4. 2 isolated from Bothrops asper snake venom: role of catalytic activity. Toxicon 2005 45 3 335 346 2-s2.0-15944429322 10.1016/j.toxicon.2004.11.004 (Pubitemid 40431278)
5. 2 Toxicon 2005 46 5 523 532 2-s2.0-24344440254 10.1016/j.toxicon.2005.06.017 (Pubitemid 41253370)
6. 2 and expression of cyclooxygenases. Toxicon 2008 52 3 428 439 2-s2.0-50549090862 10.1016/j.toxicon.2008.06.012
7. 2: insights into the mechanisms of local and systemic myotoxicity. Toxicon 2003 42 8 915 931 2-s2.0-1042287114 10.1016/j.toxicon.2003.11.005 (Pubitemid 38201492)
8. 2 proteins. Toxicon 1999 37 3 411 445 2-s2.0-0033027413 10.1016/S0041-0101(98)00188-3 (Pubitemid 29088240)
9. 2 myotoxins from crotalid snake venoms and their structural determinants of myotoxic action. Toxicon 2003 42 8 885 901 2-s2.0-1042264060 10.1016/j.toxicon.2003.11.008 (Pubitemid 38201490)
10. 2: biological and membrane-disrupting activities in the absence of catalysis. Biochemical Journal 2002 362 1 89 96 2-s2.0-0037084001 10.1042/0264-6021:3620089 (Pubitemid 34174465)
11. 2 by scanning alanine mutagenesis. Biochimica et Biophysica Acta-Biomembranes 2007 1768 5 1247 1257 2-s2.0-34047264804 10.1016/j.bbamem. 2007.01.023 (Pubitemid 46550359)
12. Lomonte B., Tarkowski A., Hanson L. Å., Host response to Bothrops asper snake venom. Analysis of edema formation, inflammatory cells, and cytokine release in a mouse model. Inflammation 1993 17 2 93 105 2-s2.0-0027534529 (Pubitemid 23105184)
13. Galli S. J., Borregaard N., Wynn T. A., Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nature Immunology 2011 12 11 1035 1044 10.1038/ni.2109
14. Kuerschner L., Moessinger C., Thiele C., Imaging of lipid biosynthesis: how a neutral lipid enters lipid droplets. Traffic 2008 9 3 338 352 2-s2.0-38849096602 10.1111/j.1600-0854.2007.00689.x (Pubitemid 351188994)
15. Walther T. C., Farese R. V. Jr., Lipid droplets and cellular lipid metabolism. Annual Review of Biochemistry 2012 81 687 714 10.1146/annurev- biochem-061009-102430
16. Pacheco P., Vieira-de-Abreu A., Gomes R. N., Barbosa-Lima G., Wermelinger L. B., Maya-Monteiro C. M., Silva A. R., Bozza M. T., Castro-Faria-Neto H. C., Bandeira-Melo C., Bozza P. T., Monocyte chemoattractant protein-1/CC chemokine ligand 2 controls microtubule-driven biogenesis and leukotriene B4-synthesizing function of macrophage lipid bodies elicited by innate immune response. Journal of Immunology 2007 179 12 8500 8508 2-s2.0-40049095755
17. 2 production in murine macrophages. PLoS Neglected Tropical Diseases 2010 4 11, article e873 2-s2.0-78649771192 10.1371/journal.pntd.0000873
18. Robenek H., Robenek M. J., Buers I., Lorkowski S., Hofnagel O., Troyer D., Severs N. J., Lipid droplets gain PAT family proteins by interaction with specialized plasma membrane domains. Journal of Biological Chemistry 2005 280 28 26330 26338 2-s2.0-22544445888 10.1074/jbc.M413312200 (Pubitemid 41022231)
19. Yuan, Y., Li P., Ye J., Lipid homeostasis and the formation of macrophage-derived foam cells in atherosclerosis. Protein Cell 2012 3 3 173 181
20. Schmitz G., Grandl M., Lipid homeostasis in macrophages-implications for atherosclerosis. Reviews of Physiology, Biochemistry and Pharmacology 2008 160 93 125 2-s2.0-48249108656 10.1007/112-2008-802
21. Mattos K. A., D'Avila H., Rodrigues L. S., Oliveira V. G. C., Sarno E. N., Atella G. C., Pereira G. M., Bozza P. T., Pessolani M. C. V., Lipid droplet formation in leprosy: toll-like receptor-regulated organelles involved in eicosanoid formation and mycobacterium leprae pathogenesis. Journal of Leukocyte Biology 2010 87 3 371 384 2-s2.0-77649106927 10.1189/jlb.0609433
22. 2 and distinct signaling pathways. Journal of Leukocyte Biology 2011 90 1 155 166 2-s2.0-79959814270 10.1189/jlb.0510263
23. Lomonte B., Gutiérrez J. M., A new muscle damaging toxin, myotoxin II, from the venom of the snake Bothrops asper (terciopelo). Toxicon 1989 27 7 725 733 2-s2.0-0024412266 (Pubitemid 19172025)
24. Takayama K., Mitchell D. H., Din Z. Z., Mukerjee P., Li C., Coleman D. L., Monomeric re lipopolysaccharide from escherichia coli is more active than the aggregated form in the limulus amebocyte lysate assay and in inducing Egr-1 mRNA in murine peritoneal macrophages. Journal of Biological Chemistry 1994 269 3 2241 2244 2-s2.0-0028157442 (Pubitemid 24035438)
25. Atherton E., Sheppard R. C., Solid Phase Peptide Synthesis-A Practical Approach 1989 Oxford, UK IRL Press
26. Maya-Monteiro C. M., Almeida P. E., D'Ávila H., Martins A. S., Rezende A. P., Castro-Faria-Neto H., Bozza P. T., Leptin induces macrophage lipid body formation by a phosphatidylinositol 3-kinase- and mammalian target of rapamycin-dependent mechanism. Journal of Biological Chemistry 2008 283 4 2203 2210 2-s2.0-38349174747 10.1074/jbc.M706706200
27. Silva A. R., Pacheco P., Vieira-de-Abreu A., Maya-Monteiro C. M., D'Alegria B., Magalhães K. G., de Assis E. F., Bandeira-Melo C., Castro-Faria-Neto H. C., Bozza P. T., Lipid bodies in oxidized LDL-induced foam cells are leukotriene-synthesizing organelles: a MCP-1/CCL2 regulated phenomenon. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids 2009 1791 11 1066 1075 2-s2.0-70349296790 10.1016/j.bbalip.2009.06.004
28. Bozza P. T., Magalhães K. G., Weller P. F., Leukocyte lipid bodies-biogenesis and functions in inflammation. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids 2009 1791 6 540 551 2-s2.0-67349265997 10.1016/j.bbalip.2009.01.005
29. Buhman K. K., Chen H. C., Farese R. V. Jr., The enzymes of neutral lipid synthesis. Journal of Biological Chemistry 2001 276 44 40369 40372 2-s2.0-0035798648 10.1074/jbc.R100050200
30. 2 myotoxins from Bothrops snake venoms. Toxicon 1995 33 11 1405 1424 2-s2.0-0028972997 10.1016/0041-0101(95)00085-Z (Pubitemid 3001583)
31. 2 homologues from viperidae snake venoms: biomimetic activities and potential applications. Current Pharmaceutical Design 2010 16 28 3224 3230 2-s2.0-78649867661 10.2174/138161210793292456
32. 2 from Bothrops asper snake venom. Archives of Biochemistry and Biophysics 1998 358 2 343 350 2-s2.0-0032532383 10.1006/abbi.1998.0853 (Pubitemid 28480954)
33. 2 by sequence analysis and site directed mutagenesis. Toxicon 2003 42 8 869 883 2-s2.0-1042287120 10.1016/j.toxicon.2003.11.027 (Pubitemid 38201489)
34. Heid H. W., Moll R., Schwetlick I., Rackwitz H. R., Keenan T. W., Adipophilin is a specific marker of lipid accumulation in diverse cell types and diseases. Cell and Tissue Research 1998 294 2 309 321 2-s2.0-0031733596 10.1007/s004410051181 (Pubitemid 28486407)
35. Londos C., Sztalryd C., Tansey J. T., Kimmel A. R., Role of PAT proteins in lipid metabolism. Biochimie 2005 87 1 45 49 2-s2.0-14544272347 10.1016/j.biochi.2004.12.010 (Pubitemid 40305232)
36. Paul A., Chang B. H. J., Li L., Yechoor V. K., Chan L., Deficiency of adipose differentiation-related protein impairs foam cell formation and protects against atherosclerosis. Circulation Research 2008 102 12 1492 1501 2-s2.0-48249100857 10.1161/CIRCRESAHA.107.168070
37. Gao J., Serrero G., Adipose differentiation related protein (ADRP) expressed in transfected COS-7 cells selectively stimulates long chain fatty acid uptake. Journal of Biological Chemistry 1999 274 24 16825 16830 2-s2.0-0033546310 10.1074/jbc.274.24.16825 (Pubitemid 29275132)
38. Bozza P. T., Melo R. C. N., Bandeira-Melo C., Leukocyte lipid bodies regulation and function: contribution to allergy and host defense. Pharmacology and Therapeutics 2007 113 1 30 49 2-s2.0-33845740182 10.1016/j.pharmthera.2006. 06.006 (Pubitemid 46001820)
39. Weller P. F., Ryeom S. W., Picard S. T., Ackerman S. J., Dvorak A. M., Cytoplasmic lipid bodies of neutrophils: formation induced by cis-unsaturated fatty acids and mediated by protein kinase C. Journal of Cell Biology 1991 113 1 137 146 2-s2.0-0025778642 (Pubitemid 21909680)
40. Bozza P. T., Yu W., Cassara J., Weller P. F., Pathways for eosinophil lipid body induction: differing signal transduction in cells from normal and hypereosinophilic subjects. Journal of Leukocyte Biology 1998 64 4 563 569 2-s2.0-0031715571 (Pubitemid 28455403)
41. Andersson L., Boström P., Ericson J., Rutberg M., Magnusson B., Marchesan D., Ruiz M., Asp L., Huang P., Frohman M. A., Borén J., Olofsson S. O., PLD1 and ERK2 regulate cytosolic lipid droplet formation. Journal of Cell Science 2006 119 11 2246 2257 2-s2.0-33745498250 10.1242/jcs.02941 (Pubitemid 43960314)
42. Bozza P. T., Payne J. L., Goulet J. L., Weller P. F., Mechanisms of platelet-activating factor-induced lipid body formation: requisite roles for 5-lipoxygenase and de novo protein synthesis in the compartmentalization of neutrophil lipids. Journal of Experimental Medicine 1996 183 4 1515 1525 2-s2.0-0029994949 10.1084/jem.183.4.1515 (Pubitemid 26134294)
43. Chen J. S., Greenberg A. S., Tseng Y. Z., Wang S. M., Possible involvement of protein kinase C in the induction of adipose differentiation- related protein by sterol ester in RAW 264.7 macrophages. Journal of Cellular Biochemistry 2001 83 2 187 199 2-s2.0-0034829990 10.1002/jcb.1225 (Pubitemid 32896589)
44. Fougerat A., Gayral S., Malet N., Briand-Mesange F., Breton-Douillon M., Laffargue M., Phosphoinositide 3-kinases and their role in inflammation: potential clinical targets in atherosclerosis? Clinical Science 2009 116 11-12 791 804 2-s2.0-67649243798 10.1042/CS20080549
45. Barberis L., Hirsch E., Targeting phosphoinositide 3-kinase γ to fight inflammation and more. Thrombosis and Haemostasis 2008 99 2 279 285 2-s2.0-38949089732 10.1160/TH07-10-0632 (Pubitemid 351230956)
46. 2 synthesis within unsaturated fatty acids-induced lipid bodies of epithelial cells. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids 2009 1791 3 156 165 2-s2.0-60849097223 10.1016/j.bbalip.2009.01.003
47. 2 synthesis in colon cancer cells. Cancer Research 2008 68 6 1732 1740 2-s2.0-40949096164 10.1158/0008-5472.CAN-07-1999 (Pubitemid 351416558)
48. 2 production by macrophages. Cellular Microbiology 2008 10 12 2589 2604 2-s2.0-55749099013 10.1111/j.1462-5822.2008.01233.x
49. 2 blocks inflammation, hyperalgesia, and interleukin 6 production in vivo. Journal of Experimental Medicine 1996 184 3 883 891 2-s2.0-0029787626
50. 2-induced mouse paw edema. Journal of Pharmacology and Experimental Therapeutics 2006 318 2 611 618 2-s2.0-33745943970 10.1124/jpet.106.102806 (Pubitemid 44061236)
51. D'Avila H., Melo R. C. N., Parreira G. G., Werneck-Barroso E., Castro-Faria-Neto H. C., Bozza P. T., Mycobacterium bovis bacillus calmette-guérin induces TLR2-mediated formation of lipid bodies: intracellular domains for eicosanoid synthesis in vivo. Journal of Immunology 2006 176 5 3087 3097 2-s2.0-33644534811
52. 2 modulates tumor necrosis factor- and interleukin-1 β -induced NF- B Activation. Journal of Biological Chemistry 2001 276 32 30527 30536 2-s2.0-0035839557 10.1074/jbc.M008481200
53. 2 isoforms: a perspective. Cellular Signalling 2003 15 7 637 665 2-s2.0-0038399752 10.1016/S0898-6568(02) 00144-4 (Pubitemid 36556070)
54. 2 enzymes. Prostaglandins and Other Lipid Mediators 2002 68-69 3 58 2-s2.0-0036669210 10.1016/S0090-6980(02)00020-5 (Pubitemid 35251864)
55. 2: structure and function. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids 2000 1488 1-2 28 39 2-s2.0-0034739445 10.1016/S1388-1981(00)00107-4
56. 2 Journal of Biological Chemistry 2009 284 47 32359 32369 2-s2.0-70450235103 10.1074/jbc.M109.061515
57. 2 Journal of Biological Chemistry 1996 271 44 27723 27729 2-s2.0-0029911368 10.1074/jbc.271.44.27723 (Pubitemid 26367343)
58. 2 lacking enzymatic activity. Biochemistry 2003 42 39 11494 11503 2-s2.0-0141483322 10.1021/bi0349930 (Pubitemid 37205744)
59. 2 GXIIB. Hepatology 2011 53 2 458 466 2-s2.0-79251523149 10.1002/hep.24066