Lipid droplets and steroidogenic cells

Experimental Cell Research

Volumn 340, Issue 2, 2016, Pages 209-214

  Shen, Wen Jun ^a,b   Azhar, Salman ^a,b   Kraemer, Fredric B ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

Adrenal gland; Cholesteryl esters; Gonads; Lipid droplet proteins; PLIN; Steroid synthesizing enzymes; Steroidogenesis

Indexed keywords

CELL DEATH INDUCING DFFA LIKE EFFECTOR; CHOLESTEROL ESTER; FAT DROPLET; PEPTIDES AND PROTEINS; PERILIPIN; UNCLASSIFIED DRUG; CHOLESTEROL; STEROID;

CELLS BY BODY ANATOMY; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; FLUORESCENCE IMAGING; HUMAN; LIPID METABOLISM; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; REVIEW; STEROIDOGENESIS; STEROIDOGENIC CELL; ANIMAL; METABOLISM; PHYSIOLOGY; PROCEDURES; PROTEOMICS;

ANIMALS; CHOLESTEROL; HUMANS; LIPID DROPLETS; LIPID METABOLISM; MITOCHONDRIA; PROTEOMICS; STEROIDS;

EID: 84957957230     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.11.024     Document Type: Review

References (70)

1. Farese R.V., Walther T.C. Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 2009, 139(5):855-860.
2. Murphy D.J. The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog. Lipid Res. 2001, 40(5):325-438.
3. Sato S., et al. Proteomic profiling of lipid droplet proteins in hepatoma cell lines expressing hepatitis C virus core protein. J. Biochem. 2006, 139(5):921-930.
4. TK Nestler J.E., Strauss J.F. Lipoprotein and cholesterol metabolism in cells that synthesize steroid hormones. Advances in Cholesterol Research 1990, 133-170. The Telford Press, Caldwell, New Jersey. M. Esfahani, J. Swaney (Eds.).
5. Plump A.S., et al. Apolipoprotein A-is required for cholesteryl ester accumulation in steroidogenic cells and for normal adrenal steroid production. J. Clin. Investig. 1996, 97(11):2660-2671.
6. Londos C., et al. On the control of lipolysis in adipocytes. Ann. NY Acad. Sci. 1999, 892:155-168.
7. 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(45):46835-46842.
8. Liu P., et al. Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J. Biol. Chem. 2004, 279(5):3787-3792.
9. Krahmer N., et al. Protein correlation profiles identify lipid droplet proteins with high confidence. Mol. Cell. Proteom. 2013, 12(5):1115-1126.
10. Khor V.K., et al. The proteome of cholesteryl-ester-enriched versus triacylglycerol-enriched lipid droplets. PLoS One 2014, 9(8):e105047.
11. Garren L.D., Ney R.L., Davis W.W. Studies on the role of protein synthesis in the regulation of corticosterone production by adrenocorticotropic hormone in vivo. Proc. Natl. Acad. Sci. USA 1965, 53(6):1443-1450.
12. Davis W., Garren L. On the mechanism of action of adrenocorticotropic hormone: the inhibitory site of cycloheximide in the pathway of steroid biosynthesis. J. Biol. Chem. 1968, 243:5153-5157.
13. Yamaguchi T., et al. Characterization of lipid droplets in steroidogenic MLTC-Leydig cells: Protein profiles and the morphological change induced by hormone stimulation. Biochim. Biophys. Acta 2015, 1851(10):1285-1295.
14. Hsieh K., et al. Perilipin family members preferentially sequester to either triacylglycerol-specific or cholesteryl-ester-specific intracellular lipid storage droplets. J. Cell Sci. 2012, 125(Pt 17):4067-4076.
15. Greenberg A.S., et al. Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets. J. Biol. Chem. 1991, 266(17):11341-11346.
16. Jiang H.P., Serrero G. Isolation and characterization of a full-length cDNA coding for an adipose differentiation-related protein. Proc. Natl. Acad. Sci. USA 1992, 89(17):7856-7860.
17. Diaz E., Pfeffer S.R. TIP47: a cargo selection device for mannose 6-phosphate receptor trafficking. Cell 1998, 93(3):433-443.
18. Scherer P.E., Bickel P.E., Kotler M., Lodish H.F. Cloning of cell-specific secreted and surface proteins by subtractive antibody screening. Nat. Biotechnol. 1998, 16(6):581-586.
19. Dalen K.T., et al. LSDP5 is a PAT protein specifically expressed in fatty acid oxidizing tissues. Biochim. Biophys. Acta 2007, 1771(2):210-227.
20. Lu X., et al. The murine perilipin gene: the lipid droplet-associated perilipins derive from tissue-specific, mRNA splice variants and define a gene family of ancient origin. Mamm. Genome 2001, 12(9):741-749.
21. Greenberg A.S., et al. Stimulation of lipolysis and hormone-sensitive lipase via the extracellular signal-regulated kinase pathway. J. Biol. Chem. 2001, 276(48):45456-45461.
22. Grahn T.H., et al. FSP27 and PLIN1 interaction promotes the formation of large lipid droplets in human adipocytes. Biochem. Biophys. Res. Commun. 2013, 432(2):296-301.
23. Hayashi F., et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 2001, 410(6832):1099-1103.
24. Bronner M., Hertz R., Bar-Tana J. Kinase-independent transcriptional co-activation of peroxisome proliferator-activated receptor alpha by AMP-activated protein kinase. Biochem. J. 2004, 384(Pt 2):295-305.
25. Lee W.J., et al. AMPK activation increases fatty acid oxidation in skeletal muscle by activating PPARalpha and PGC-1. Biochem. Biophys. Res. Commun. 2006, 340(1):291-295.
26. Bose M., Whittal R.M., Miller W.L., Bose H.S. Steroidogenic activity of StAR requires contact with mitochondrial VDAC1 and phosphate carrier protein. J. Biol. Chem. 2008, 283(14):8837-8845.
27. Stocco D.M. StAR protein and the regulation of steroid hormone biosynthesis. Annu. Rev. Physiol. 2001, 63:193-213.
28. Kraemer F.B. Adrenal cholesterol utilization. Mol. Cell. Endocrinol. 2007, 265-266:42-45.
29. Jagerstrom S., et al. Lipid droplets interact with mitochondria using SNAP23. Cell. Biol. Intern. 2009, 33(9):934-940.
30. Magne J., et al. The minor allele of the missense polymorphism Ser251Pro in perilipin 2 (PLIN2) disrupts an alpha-helix, affects lipolysis, and is associated with reduced plasma triglyceride concentration in humans. FASEB J. 2013, 27(8):3090-3099.
31. Hulce J.J., Cognetta A.B., Niphakis M.J., Tully S.E., Cravatt B.F. Proteome-wide mapping of cholesterol-interacting proteins in mammalian cells. Nat. Methods 2013, 10(3):259-264.
32. Picotti P., Bodenmiller B., Mueller L.N., Domon B., Aebersold R. Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 2009, 138(4):795-806.
33. Seachord C.L., VandeVoort C.A., Duffy D.M. Adipose differentiation-related protein: a gonadotropin- and prostaglandin-regulated protein in primate periovulatory follicles. Biol. Reprod. 2005, 72(6):1305-1314.
34. Zhou Z., et al. Cidea-deficient mice have lean phenotype and are resistant to obesity. Nat. Genet. 2003, 35(1):49-56.
35. Li J.Z., et al. Cideb regulates diet-induced obesity, liver steatosis, and insulin sensitivity by controlling lipogenesis and fatty acid oxidation. Diabetes 2007, 56(10):2523-2532.
36. Ueno M., et al. Fat-specific protein 27 modulates nuclear factor of activated T cells 5 and the cellular response to stress. J. Lipid Res. 2013, 54(3):734-743.
37. Yang X., et al. Identification of perilipin-as a lipid droplet protein regulated in oocytes during maturation. Reprod. Fertil. Dev. 2010, 22(8):1262-1271.
38. Wang W., et al. Proteomic analysis of murine testes lipid droplets. Sci. Rep. 2015, 5:12070.
39. Zimmermann R., et al. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 2004, 306(5700):1383-1386.
40. Kraemer F., Shen W. Hormone-sensitive lipase: control of intracellular tri-(di)acylglycerol and cholesteryl ester hydrolysis. J. Lipid Res. 2002, 43:1585-1594.
41. Eichmann T.O., et al. ATGL and CGI-58 are lipid droplet proteins of the hepatic stellate cell line HSC-T6. J. Lipid Res. 2015, 56(10):1972-1984.
42. Taschler U., et al. Adipose triglyceride lipase is involved in the mobilization of triglyceride and retinoid stores of hepatic stellate cells. Biochim. Biophys. Acta 2015, 1851(7):937-945.
43. Scalvini L., Piomelli D., Mor M. Monoglyceride lipase: structure and inhibitors. Chem. Phys. Lipids 2015, pii: S0009-3084(15)30016-5. 10.1016/j.chemphyslip.2015.07.011.
44. Wei E., et al. Loss of TGH/Ces3 in mice decreases blood lipids, improves glucose tolerance, and increases energy expenditure. Cell Metab. 2010, 11(3):183-193.
45. Bostrom P., et al. SNARE proteins mediate fusion between cytosolic lipid droplets and are implicated in insulin sensitivity. Nat. Cell Biol. 2007, 9(11):1286-1293.
46. Rostovtseva T.K., Bezrukov S.M. VDAC regulation: role of cytosolic proteins and mitochondrial lipids. J. Bioenerg. Biomembr. 2008, 40(3):163-170.
47. Shoshan-Barmatz V., et al. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol. Asp. Med. 2010, 31(3):227-285.
48. Wu C.C., Howell K.E., Neville M.C., Yates J.R., McManaman J.L. Proteomics reveal a link between the endoplasmic reticulum and lipid secretory mechanisms in mammary epithelial cells. Electrophoresis 2000, 21(16):3470-3482.
49. Bartz R., et al. Dynamic activity of lipid droplets: protein phosphorylation and GTP-mediated protein translocation. J. Proteome Res. 2007, 6(8):3256-3265.
50. Almahbobi G., Hall P.F. The role of intermediate filaments in adrenal steroidogenesis. J. Cell Sci. 1990, 97:679-687.
51. Shen W.J., et al. Ablation of vimentin results in defective steroidogenesis. Endocrinology 2012, 153(7):3249-3257.
52. Xu N., et al. The FATP1-DGAT2 complex facilitates lipid droplet expansion at the ER-lipid droplet interface. J. Cell Biol. 2012, 198(5):895-911.
53. Wang C., Liu Z., Huang X. Rab32 is important for autophagy and lipid storage in Drosophila. PLoS One 2012, 7(2):e32086.
54. Jo Y., Hartman I.Z., DeBose-Boyd R.A. Ancient ubiquitous protein-mediates sterol-induced ubiquitination of 3-hydroxy-3-methylglutaryl CoA reductase in lipid droplet-associated endoplasmic reticulum membranes. Mol. Biol. Cell. 2013, 24(3):169-183.
55. Bosma M., et al. The lipid droplet coat protein perilipin 5 also localizes to muscle mitochondria. Histochem. Cell. Biol. 2012, 137(2):205-216.
56. Guo Y., et al. Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 2008, 453(7195):657-661.
57. Stevanovic A., Thiele C. Monotopic topology is required for lipid droplet targeting of ancient ubiquitous protein 1. J. Lipid Res. 2013, 54(2):503-513.
58. Wang C.W., Lee S.C. The ubiquitin-like (UBX)-domain-containing protein Ubx2/Ubxd8 regulates lipid droplet homeostasis. J. Cell. Sci. 2012, 125(Pt 12):2930-2939.
59. Olzmann J.A., Richter C.M., Kopito R.R. Spatial regulation of UBXD8 and p97/VCP controls ATGL-mediated lipid droplet turnover. Proc. Natl. Acad. Sci. USA 2013, 110(4):1345-1350.
60. Koves T.R., et al. PPARgamma coactivator-1alpha contributes to exercise-induced regulation of intramuscular lipid droplet programming in mice and humans. J. Lipid Res. 2013, 54(2):522-534.
61. Li H., et al. LSDP5 enhances triglyceride storage in hepatocytes by influencing lipolysis and fatty acid beta-oxidation of lipid droplets. PLoS One 2012, 7(6):e36712.
62. Jiang W., Napoli J.L. The retinol dehydrogenase Rdh10 localizes to lipid droplets during acyl ester biosynthesis. J. Biol. Chem. 2013, 288(1):589-597.
63. Testerink N., et al. Replacement of retinyl esters by polyunsaturated triacylglycerol species in lipid droplets of hepatic stellate cells during activation. PLoS One 2012, 7(4):e34945.
64. Kraemer F.B., et al. Adrenal neutral cholesteryl hydrolase: identification, subcellular distribution and sex differences. Endocrinology 2002, 143:801-806.
65. Kraemer F.B., et al. Hormone-sensitive lipase is required for high-density lipoprotein cholesteryl ester-supported adrenal steroidogenesis. Mol. Endocrinol. 2004, 18(3):549-557.
66. Shen W.J., Patel S., Eriksson J.E., Kraemer F.B. Vimentin is a functional partner of hormone sensitive lipase and facilitates lipolysis. J. Proteome Res. 2010, 9(4):1786-1794.
67. Shen W.J., et al. Interaction of hormone-sensitive lipase with steroidogenic acute regulatory protein: facilitation of cholesterol transfer in adrenal. J. Biol. Chem. 2003, 278(44):43870-43876.
68. Wilfling F., et al. Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets. Dev. Cell. 2013, 24(4):384-399.
69. Velikkakath A.K., Nishimura T., Oita E., Ishihara N., Mizushima N. Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol. Biol. Cell. 2012, 23(5):896-909.
70. Millership S., et al. Increased lipolysis and altered lipid homeostasis protect gamma-synuclein-null mutant mice from diet-induced obesity. Proc. Natl. Acad. Sci. USA 2012, 109(51):20943-20948.