Vimentin is a functional partner of hormone sensitive lipase and facilitates lipolysis

Journal of Proteome Research

Volumn 9, Issue 4, 2010, Pages 1786-1794

  Shen, Wen Jun ^a   Patel, Shailja ^a   Eriksson, John E ^b   Kraemer, Fredric B ^a  

^a STANFORD UNIVERSITY   (United States)

^b ÅBO AKADEMI UNIVERSITY   (Finland)

Author keywords

Adipose; Surface enhanced laser desorption ionization time of flight mass spectroscopy; Translocation

Indexed keywords

CELL PROTEIN; INSULIN; TRIACYLGLYCEROL LIPASE; VIMENTIN;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL LYSATE; HORMONE SENSITIVITY; IMMUNOPRECIPITATION; LIPOLYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MICROARRAY; SURFACE ENHANCED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; TIME OF FLIGHT MASS SPECTROMETRY;

ANALYSIS OF VARIANCE; ANIMALS; IMMUNOPRECIPITATION; LIPOLYSIS; MICE; PROTEIN ARRAY ANALYSIS; PROTEIN INTERACTION MAPPING; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STEROL ESTERASE; VIMENTIN;

EID: 77950632472     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr900909t     Document Type: Article

References (52)

1. Duncan, R. E.; Ahmadian, M.; Jaworski, K.; Sarkadi-Nagy, E.; Sul, H. S. Regulation of lipolysis in adipocytes Annu. Rev. Nutr. 2007, 27, 79 - 101
2. Greenberg, A. S.; Shen, W.-J.; Muliro, K.; Patel, S.; Souza, S. C.; Roth, R. A.; Kraemer, F. B. Stimulation of lipolysis and hormone-sensitive lipase via the extracellular signal-regulated kinase pathway J. Biol. Chem. 2001, 276 (48) 45456 - 45461
3. Robidoux, J.; Kumar, N.; Daniel, K. W.; Moukdar, F.; Cyr, M.; Medvedev, A. V.; Collins, S. Maximal beta3-adrenergic regulation of lipolysis involves Src and epidermal growth factor receptor-dependent ERK1/2 activation J. Biol. Chem. 2006, 281 (49) 37794 - 37802
4. Kraemer, F. B.; Shen, W.-J. Hormone-sensitive lipase: control of intracellular tri-(di-) acylglycerol and cholesteryl ester hydrolysis J. Lipid Res. 2002, 43 (10) 1585 - 1594
5. Greenberg, A. S.; Egan, J. J.; Wek, S. A.; Garty, N. B.; Blanchette-Mackie, E. J.; Londos, C. Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets J. Biol. Chem. 1991, 266 (17) 11341 - 11346
6. Brasaemle, D. L.; Dolios, G.; Shapiro, L.; Wang, R. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically-stimulated 3T3-L1 adipocytes J. Biol. Chem. 2004, 279, 46835 - 46842
7. Liu, P.; Ying, Y.; Zhao, Y.; Mundy, D. I.; Zhu, M.; Anderson, R. G. W. Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic J. Biol. Chem. 2004, 279 (5) 3787 - 3792
8. Osuga, J.-i.; Ishibashi, S.; Oka, T.; Yagyu, H.; Tozawa, R.; Fujimoto, A.; Shionoira, F.; Yahagi, N.; Kraemer, F. B.; Tsutsumi, O.; Yamada, N. Targeted disruption of hormone-sensitive lipase results in male sterility and adipocyte hypertrophy, but not in obesity Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 787 - 792
9. Villena, J. A.; Roy, S.; Sarkadi-Nagy, E.; Kim, K. H.; Sul, H. S. Desnutrin, an adipocyte gene encoding a novel patatin domain-containing protein, is induced by fasting and glucocorticoids: ectopic expression of desnutrin increases triglyceride hydrolysis J. Biol. Chem. 2004, 279 (45) 47066 - 47075
10. Jenkins, C. M.; Mancuso, D. J.; Yan, W.; Sims, H. F.; Gibson, B.; Gross, R. W. Identification, cloning, expression, and purification of three novel human calcium-independent phospholipase A2 family members possessing triacylglycerol lipase and acylglycerol transacylase activities J. Biol. Chem. 2004, 279, 48968 - 48975
11. Wilson, P. A.; Gardner, S. D.; Lambie, N. M.; Commans, S. A.; Crowther, D. J. Characterization of the human patatin-like phospholipase family J. Lipid Res. 2006, 47 (9) 1940 - 1949
12. Zimmermann, R.; Strauss, J. G.; Haemmerle, G.; Schoiswohl, G.; Birner-Gruenberger, R.; Riederer, M.; Lass, A.; Neuberger, G.; Eisenhaber, F.; Hermetter, A.; Zechner, R. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase Science 2004, 306 (5700) 1383 - 1386
13. Haemmerle, G.; Lass, A.; Zimmermann, R.; Gorkiewicz, G.; Meyer, C.; Rozman, J.; Heldmaier, G.; Maier, R.; Theussl, C.; Eder, S.; Kratky, D.; Wagner, E. F.; Klingenspor, M.; Hoefler, G.; Zechner, R. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase Science 2006, 312 (5774) 734 - 737
14. Kershaw, E. E.; Hamm, J. K.; Verhagen, L. A.; Peroni, O.; Katic, M.; Flier, J. S. Adipose triglyceride lipase: function, regulation by insulin, and comparison with adiponutrin Diabetes 2006, 55 (1) 148 - 157
15. Miyoshi, H.; Souza, S. C.; Zhang, H. H.; Strissel, K. J.; Christoffolete, M. A.; Kovsan, J.; Rudich, A.; Kraemer, F. B.; Bianco, A. C.; Obin, M. S.; Greenberg, A. S. Perilipin promotes hormone-sensitive lipase-mediated adipocyte lipolysis via phosphorylation-dependent and -independent mechanisms J. Biol. Chem. 2006, 281 (23) 15837 - 15844
16. Lass, A.; Zimmermann, R.; Haemmerle, G.; Riederer, M.; Schoiswohl, G.; Schweiger, M.; Kienesberger, P.; Strauss, J. G.; Gorkiewicz, G.; Zechner, R. Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman Syndrome Cell Metab. 2006, 3 (5) 309 - 319
17. Schweiger, M.; Schreiber, R.; Haemmerle, G.; Lass, A.; Fledelius, C.; Jacobsen, P.; Tornqvist, H.; Zechner, R.; Zimmermann, R. Adipose triglyceride lipase and hormone-sensitive lipase are the major enzymes in adipose tissue triacylglycerol catabolism J. Biol. Chem. 2006, 281 (52) 40236 - 40241
18. Egan, J. J.; Greenberg, A. S.; Chang, M.-K.; Wek, S. A.; Moos, Jr. M. C.; Londos, C. Mechanism of hormone-stimulated lipolysis in adipocytes: translocation of hormone-sensitive lipase to the lipid storage droplet Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 8537 - 8541
19. Clifford, G. M.; Londos, C.; Kraemer, F. B.; Vernon, R. G.; Yeaman, S. J. Translocation of hormone-sensitive lipase and perilipin upon lipolytic stimulation of rat adipocytes J. Biol. Chem. 2000, 275 (7) 5011 - 5015
20. Su, C.-L.; Sztalryd, C.; Contreras, J. A.; Holm, C.; Kimmel, A. R.; Londos, C. Mutational analysis of the hormone-sensitive lipase translocation reaction in adipocytes J. Biol. Chem. 2003, 278, 43615 - 43619
21. Granneman, J. G.; Moore, H. P.; Granneman, R. L.; Greenberg, A. S.; Obin, M. S.; Zhu, Z. Analysis of lipolytic protein trafficking and interactions in adipocytes J. Biol. Chem. 2007, 282 (8) 5726 - 5735
22. Sztalryd, C.; Xu, G.; Dorward, H.; Tansey, J. T.; Contreras, J. A.; Kimmel, A. R.; Londos, C. Perilipin A is essential for the translocation of hormone-sensitive lipase during lipolytic activation J. Cell Biol. 2003, 161 (6) 1093 - 1103
23. Wang, J.; Shen, W. J.; Patel, S.; Harada, K.; Kraemer, F. B. Mutational analysis of the "regulatory module" of hormone-sensitive lipase Biochemistry 2005, 44 (6) 1953 - 1959
24. Eliasson, C.; Sahlgren, C.; Berthold, C. H.; Stakeberg, J.; Celis, J. E.; Betsholtz, C.; Eriksson, J. E.; Pekny, M. Intermediate filament protein partnership in astrocytes J. Biol. Chem. 1999, 274 (34) 23996 - 24006
25. Sztalryd, C.; Hamilton, J.; Horwitz, B. A.; Johnson, P.; Kraemer, F. B. Alterations of lipolysis and lipoprotein lipase in chronically nicotine-treated rats Am. J. Physiol. 1996, 270 E215-E223
26. Shen, W. J.; Patel, S.; Yu, Z.; Jue, D.; Kraemer, F. B. Effects of rosiglitazone and high fat diet on lipase/esterase expression in adipose tissue Biochim. Biophys. Acta 2007, 1771 (2) 177 - 184
27. Sjostrom, L.; Bjorntorp, P.; Vrana, J. Microscopic fat cell size measurements on frozen-cut adipose tissue in comparison with automatic determinations of osmium-fixed fat cells J. Lipid Res. 1971, 12 (5) 521 - 530
28. Shen, W.-J.; Sridhar, K.; Bernlohr, D. A.; Kraemer, F. B. Interaction of rat hormone-sensitive lipase with adipocyte lipid-binding protein Proc. Natl. Acad. Sci. U.S.A. 1999, 96 (10) 5528 - 5532
29. Harada, K.; Shen, W.-J.; Patel, S.; Natu, V.; Wang, J.; Osuga, J.; Ishibashi, S.; Kraemer, F. Resistance to high fat diet-induced obesity associated with altered expression of adipose specific genes in hormone-sensitive lipase deficient mice Am. J. Physiol. Endocrinol. Metab. 2003, 285 E1182-1195
30. Shen, W.-J.; Liang, Y.; Hong, R.; Patel, S.; Natu, V.; Sridhar, K.; Jenkins, A.; Bernlohr, D. A.; Kraemer, F. B. Characterization of the functional interaction of adipocyte lipid-binding protein with hormone-sensitive lipase J. Biol. Chem. 2001, 276 (52) 49443 - 49448
31. Zhang, W.; Chait, B. T. ProFound: an expert system for protein identification using mass spectrometric peptide mapping information Anal. Chem. 2000, 72 (11) 2482 - 2489
32. Perkins, D. N.; Pappin, D. J.; Creasy, D. M.; Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data Electrophoresis 1999, 20 (18) 3551 - 3567
33. Franke, W. W.; Hergt, M.; Grund, C. Rearrangement of the vimentin cytoskeleton during adipose conversion: formation of an intermediate filament cage around lipid globules Cell 1987, 49 (1) 131 - 141
34. Brasaemle, D. L. Thematic review series: Adipocyte Biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis J. Lipid Res. 2007, 48 (12) 2547 - 2559
35. Souza, S. C.; Muliro, K. V.; Liscum, L.; Lien, P.; Yamamoto, M. T.; Schaffer, J. E.; Dallal, G. E.; Wang, X.; Kraemer, F. B.; Obin, M.; Greenberg, A. S. Modulation of hormone-sensitive lipase and protein kinase A-mediated lipolysis by perilipin A in an adenoviral reconstituted system J. Biol. Chem. 2002, 277 (10) 8267 - 8272
36. Miyoshi, H.; Perfield, J. W., 2nd; Souza, S. C.; Shen, W. J.; Zhang, H. H.; Stancheva, Z. S.; Kraemer, F. B.; Obin, M. S.; Greenberg, A. S. Control of adipose triglyceride lipase action by serine 517 of perilipin A globally regulates protein kinase A-stimulated lipolysis in adipocytes J. Biol. Chem. 2007, 282 (2) 996 - 1002
37. Subramanian, V.; Rothenberg, A.; Gomez, C.; Cohen, A. W.; Garcia, A.; Bhattacharyya, S.; Shapiro, L.; Dolios, G.; Wang, R.; Lisanti, M. P.; Brasaemle, D. L. Perilipin A mediates the reversible binding of CGI-58 to lipid droplets in 3T3-L1 adipocytes J. Biol. Chem. 2004, 279 (40) 42062 - 42071
38. Yamaguchi, T.; Omatsu, N.; Matsushita, S.; Osumi, T. CGI-58 interacts with perilipin and is localized to lipid droplets. Possible involvement of CGI-58 mislocalization in Chanarin-Dorfman syndrome J. Biol. Chem. 2004, 279 (29) 30490 - 30497
39. Moore, H. P.; Silver, R. B.; Mottillo, E. P.; Bernlohr, D. A.; Granneman, J. G. Perilipin targets a novel pool of lipid droplets for lipolytic attack by hormone-sensitive lipase J. Biol. Chem. 2005, 280 (52) 43109 - 43120
40. Jenkins-Kruchten, A. E.; Bennaars-Eiden, A.; Ross, J. R.; Shen, W. J.; Kraemer, F. B.; Bernlohr, D. A. Fatty acid-binding protein-hormone-sensitive lipase interaction: fatty acid dependence on binding J. Biol. Chem. 2003, 278 (48) 47636 - 47643
41. Smith, A. J.; Sanders, M. A.; Thompson, B. R.; Londos, C.; Kraemer, F. B.; Bernlohr, D. A. Physical association between the adipocyte fatty acid binding protein and hormone sensitive lipase: A fluorescence resonance energy transfer analysis J. Biol. Chem. 2004, 279, 52399 - 52405
42. Shen, W.-J.; Patel, S.; Kraemer, F. B. Hormone-sensitive lipase functions as an oligomer Biochemistry 2000, 39, 2392 - 2398
43. Fuchs, E.; Weber, K. Intermediate filaments: structure, dynamics, function, and disease Annu. Rev. Biochem. 1994, 63, 345 - 382
44. Chou, Y. H.; Flitney, F. W.; Chang, L.; Mendez, M.; Grin, B.; Goldman, R. D. The motility and dynamic properties of intermediate filaments and their constituent proteins Exp. Cell Res. 2007, 313 (10) 2236 - 2243
45. Colucci-Guyon, E.; Portier, M. M.; Dunia, I.; Paulin, D.; Pournin, S.; Babinet, C. Mice lacking vimentin develop and reproduce without an obvious phenotype Cell 1994, 79 (4) 679 - 694 (Pubitemid 24363811)
46. Runembert, I.; Queffeulou, G.; Federici, P.; Vrtovsnik, F.; Colucci-Guyon, E.; Babinet, C.; Briand, P.; Trugnan, G.; Friedlander, G.; Terzi, F. Vimentin affects localization and activity of sodium-glucose cotransporter SGLT1 in membrane rafts J. Cell Sci. 2002, 115 (Pt 4) 713 - 724
47. Hirabayashi, T.; Murayama, T.; Shimizu, T. Regulatory mechanism and physiological role of cytosolic phospholipase A2 Biol. Pharm. Bull. 2004, 27 (8) 1168 - 1173
48. Brasaemle, D. L.; Levin, D. M.; Adler-Wailes, D. C.; Londos, C. The lipolytic stimulation of 3T3-L1 adipocytes promotes the translocation of hormone-sensitive lipase to the surfaces of lipid storage droplets Biochim. Biophys. Acta 2000, 1483 (2) 251 - 262
49. Collot, M.; Louvard, D.; Singer, S. J. Lysosomes are associated with microtubules and not with intermediate filaments in cultured fibroblasts Proc. Natl. Acad. Sci. U.S.A. 1984, 81 (3) 788 - 792
50. Kumar, N.; Robidoux, J.; Daniel, K. W.; Guzman, G.; Floering, L. M.; Collins, S. Requirement of vimentin filament assembly for beta3-adrenergic receptor activation of ERK MAP kinase and lipolysis J. Biol. Chem. 2007, 282 (12) 9244 - 9250
51. Galarneau, L.; Loranger, A.; Gilbert, S.; Marceau, N. Keratins modulate hepatic cell adhesion, size and G1/S transition Exp. Cell Res. 2007, 313 (1) 179 - 194
52. Kim, S.; Wong, P.; Coulombe, P. A. A keratin cytoskeletal protein regulates protein synthesis and epithelial cell growth Nature 2006, 441 (7091) 362 - 365