Differential Phosphorylation of Perilipin 1A at the Initiation of Lipolysis Revealed by Novel Monoclonal Antibodies and High Content Analysis

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  McDonough, Patrick M ^a   Maciejewski Lenoir, Dominique ^a   Hartig, Sean M ^b   Hanna, Rita A ^a   Whittaker, Ross ^a   Heisel, Andrew ^a   Nicoll, James B ^c   Buehrer, Benjamin M ^c   Christensen, Kurt ^b   Mancini, Maureen G ^b   Mancini, Michael A ^b   Edwards, Dean P ^b   Price, Jeffrey H ^a,d  

^a VALA SCIENCES INC   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c Zen Bio Inc   (United States)

^d BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; HORMONE SENSITIVE LIPASE; INTERMEDIN; ISOPRENALINE; MONOCLONAL ANTIBODY; PERILIPIN; PERILIPIN 1A; SERINE; UNCLASSIFIED DRUG;

ADIPOCYTE; ADULT; ANTIBODY SPECIFICITY; ARTICLE; BINDING AFFINITY; CELL ASSAY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; LIPOLYSIS; MOLECULAR CLONING; MOLECULAR RECOGNITION; PROTEIN CONTENT; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; WESTERN BLOTTING;

3T3-L1 CELLS; ADIPOCYTES; ADULT; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; ARGININE; BLOTTING, WESTERN; CARRIER PROTEINS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; LIPID METABOLISM; LIPOLYSIS; MICE; PHOSPHOPROTEINS; PHOSPHORYLATION; RNA, SMALL INTERFERING; SERINE;

EID: 84873563783     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055511     Document Type: Article

References (41)

1. Greenberg AS, Coleman RA, Kraemer FB, McManaman JL, Obin MS, et al. (2011) The role of lipid droplets in metabolic disease in rodents and humans. J Clin Invest 121: 2102-2110.
2. Brasaemle DL, (2010) Lipolysis control: the plot thickens. Cell Metab 11: 173-174.
3. Kimmel AR, Brasaemle DL, McAndrews-Hill M, Sztalryd C, Londos C, (2010) Adoption of PERILIPIN as a unifying nomenclature for the mammalian PAT-family of intracellular lipid storage droplet proteins. J Lipid Res 51: 468-471.
4. Greenberg AS, Egan JJ, Wek SA, Garty NB, Blanchette-Mackie EJ, et al. (1991) Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets. J Biol Chem 266: 11341-11346.
5. Brasaemle DL, (2007) Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J Lipid Res 48: 2547-2559.
6. Tansey JT, Sztalryd C, Hlavin EM, Kimmel AR, Londos C, (2004) The central role of perilipin a in lipid metabolism and adipocyte lipolysis. IUBMB Life 56: 379-385.
7. Granneman JG, Moore HP, Krishnamoorthy R, Rathod M, (2009) Perilipin controls lipolysis by regulating the interactions of AB-hydrolase containing 5 (Abhd5) and adipose triglyceride lipase (Atgl). J Biol Chem 284: 34538-34544.
8. Brasaemle DL, Levin DM, Adler-Wailes DC, Londos C, (2000) The lipolytic stimulation of 3T3-L1 adipocytes promotes the translocation of hormone-sensitive lipase to the surfaces of lipid storage droplets. Biochim Biophys Acta 1483: 251-262.
9. Sztalryd C, Xu G, Dorward H, Tansey JT, Contreras JA, et al. (2003) Perilipin A is essential for the translocation of hormone-sensitive lipase during lipolytic activation. J Cell Biol 161: 1093-1103.
10. Greenberg AS, Egan JJ, Wek SA, Moos MC Jr, Londos C, et al. (1993) Isolation of cDNAs for perilipins A and B: sequence and expression of lipid droplet-associated proteins of adipocytes. Proc Natl Acad Sci U S A 90: 12035-12039.
11. Zhang HH, Souza SC, Muliro KV, Kraemer FB, Obin MS, et al. (2003) Lipase-selective functional domains of perilipin A differentially regulate constitutive and protein kinase A-stimulated lipolysis. J Biol Chem 278: 51535-51542.
12. Marcinkiewicz A, Gauthier D, Garcia A, Brasaemle DL, (2006) The phosphorylation of serine 492 of perilipin a directs lipid droplet fragmentation and dispersion. J Biol Chem 281: 11901-11909.
13. Miyoshi H, Perfield JW, 2nd, Souza SC, Shen WJ, Zhang HH, et al (2007) Control of adipose triglyceride lipase action by serine 517 of perilipin A globally regulates protein kinase A-stimulated lipolysis in adipocytes. J Biol Chem 282: 996-1002.
14. Holm C, (2003) Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Biochem Soc Trans 31: 1120-1124.
15. Greenberg AS, Shen WJ, Muliro K, Patel S, Souza SC, et al. (2001) Stimulation of lipolysis and hormone-sensitive lipase via the extracellular signal-regulated kinase pathway. J Biol Chem 276: 45456-45461.
16. Martin S, Okano S, Kistler C, Fernandez-Rojo MA, Hill MM, et al. (2009) Spatiotemporal regulation of early lipolytic signaling in adipocytes. J Biol Chem 284: 32097-32107.
17. Wong W, Scott JD, (2004) AKAP signalling complexes: focal points in space and time. Nat Rev Mol Cell Biol 5: 959-970.
18. Bicknell KA, Harmer SC, Yiangson S, Lockwood W, Bicknell AB, (2009) Lys-gamma3-MSH: a global regulator of hormone sensitive lipase activity? Mol Cell Endocrinol 300: 71-76.
19. Harmer SC, Pepper DJ, Cooke K, Bennett HP, Bicknell AB, (2008) Evidence of a possible role for Lys-gamma3-MSH in the regulation of adipocyte function. J Endocrinol 196: 149-158.
20. McDonough PM, Agustin RM, Ingermanson RS, Loy PA, Buehrer BM, et al. (2009) Quantification of lipid droplets and associated proteins in cellular models of obesity via high-content/high-throughput microscopy and automated image analysis. Assay Drug Dev Technol 7: 440-460.
21. Clemm DL, Sherman L, Boonyaratanakornkit V, Schrader WT, Weigel NL, et al. (2000) Differential hormone-dependent phosphorylation of progesterone receptor A and B forms revealed by a phosphoserine site-specific monoclonal antibody. Mol Endocrinol 14: 52-65.
22. Press M, Spaulding B, Groshen S, Kaminsky D, Hagerty M, et al. (2002) Comparison of different antibodies for detection of progesterone receptor in breast cancer. Steroids 67: 799-813.
23. Sasano H, Anderson TJ, Silverberg SG, Santen RJ, Conway M, et al. (2005) The validation of new aromatase monoclonal antibodies for immunohistochemistry-a correlation with biochemical activities in 46 cases of breast cancer. J Steroid Biochem Mol Biol 95: 35-39.
24. Whittaker R, Loy PA, Sisman E, Suyama E, Aza-Blanc P, et al. (2010) Identification of MicroRNAs That Control Lipid Droplet Formation and Growth in Hepatocytes via High-Content Screening. J Biomol Screen.
25. McDonough PM, Ingermanson RS, Loy PA, Koon ED, Whittaker R, et al. (2011) Quantification of hormone sensitive lipase phosphorylation and colocalization with lipid droplets in murine 3T3L1 and human subcutaneous adipocytes via automated digital microscopy and high-content analysis. Assay Drug Dev Technol 9: 262-280.
26. Yamaguchi T, Omatsu N, Omukae A, Osumi T, (2006) Analysis of interaction partners for perilipin and ADRP on lipid droplets. Mol Cell Biochem 284: 167-173.
27. Martinez-Botas J, Anderson JB, Tessier D, Lapillonne A, Chang BH, et al. (2000) Absence of perilipin results in leanness and reverses obesity in Lepr(db/db) mice. Nat Genet 26: 474-479.
28. Tansey JT, Sztalryd C, Gruia-Gray J, Roush DL, Zee JV, et al. (2001) Perilipin ablation results in a lean mouse with aberrant adipocyte lipolysis, enhanced leptin production, and resistance to diet-induced obesity. Proc Natl Acad Sci U S A 98: 6494-6499.
29. Nishino N, Tamori Y, Tateya S, Kawaguchi T, Shibakusa T, et al. (2008) FSP27 contributes to efficient energy storage in murine white adipocytes by promoting the formation of unilocular lipid droplets. J Clin Invest 118: 2808-2821.
30. Nguyen KD, Qiu Y, Cui X, Goh YP, Mwangi J, et al. (2011) Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature 480: 104-108.
31. Chen W, Chang B, Saha P, Hartig SM, Li L, et al. (2012) Berardinelli-seip congenital lipodystrophy 2/seipin is a cell-autonomous regulator of lipolysis essential for adipocyte differentiation. Mol Cell Biol 32: 1099-1111.
32. Zhou D, Samovski D, Okunade AL, Stahl PD, Abumrad NA, et al. (2012) CD36 level and trafficking are determinants of lipolysis in adipocytes. FASEB J 26: 4733-4742.
33. Rapold RA, Wueest S, Knoepfel A, Schoenle EJ, Konrad D (2012) Fas activates lipolysis in a Ca2+-CaMKII-dependent manner in 3T3-L1 adipocytes. J Lipid Res.
34. Pidoux G, Witczak O, Jarnaess E, Myrvold L, Urlaub H, et al. (2011) Optic atrophy 1 is an A-kinase anchoring protein on lipid droplets that mediates adrenergic control of lipolysis. EMBO J 30: 4371-4386.
35. Galello F, Portela P, Moreno S, Rossi S, (2010) Characterization of substrates that have a differential effect on Saccharomyces cerevisiae protein kinase A holoenzyme activation. J Biol Chem 285: 29770-29779.
36. Kemp BE, Graves DJ, Benjamini E, Krebs EG, (1977) Role of multiple basic residues in determining the substrate specificity of cyclic AMP-dependent protein kinase. J Biol Chem 252: 4888-4894.
37. Hilhorst R, Houkes L, van den Berg A, Ruijtenbeek R, (2009) Peptide microarrays for detailed, high-throughput substrate identification, kinetic characterization, and inhibition studies on protein kinase A. Anal Biochem. 387: 150-161.
38. Ben-Shimon A, Niv MY, (2011) Deciphering the Arginine-binding preferences at the substrate-binding groove of Ser/Thr kinases by computational surface mapping. PLoS Comput Biol 7: e1002288.
39. Shabb JB, (2001) Physiological substrates of cAMP-dependent protein kinase. Chem Rev 101: 2381-2411.
40. Ruppelt A, Oberprieler NG, Magklaras G, Tasken K (2009) Physiological substrates of PKA and PKG. In: Bradshaw RA, Dennis EA, editors. Handbook of Cell Signalling: Academic Press. 1497-1514.
41. Zhang X, Ji J, Yan G, Wu J, Sun X, et al. (2010) Sildenafil promotes adipogenesis through a PKG pathway. Biochem Biophys Res Commun 396: 1054-1059.