Sequential Ordered Fatty Acid α Oxidation and Δ9 Desaturation Are Major Determinants of Lipid Storage and Utilization in Differentiating Adipocytes

Biochemistry

Volumn 43, Issue 17, 2004, Pages 5033-5044

  Su, Xiong ^a   Han, Xianlin ^a   Yang, Jingyue ^a   Mancuso, David J ^a   Chen, Jeannie ^a   Bickel, Perry E ^a   Gross, Richard W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPIDS; METABOLISM; OXIDATION; REACTION KINETICS;

GLOBAL LIPIDOMICS; METABOLIC FATE; PREOXISOMAL PROCESSING; UNSATURATIONS;

FATTY ACIDS;

ACYL COENZYME A DEHYDROGENASE; FATTY ACID; MESSENGER RNA; OXYGENASE; PHOSPHATIDYLCHOLINE; PHYTANOYL COENZYME A ALPHA HYDROXYLASE; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN 3T3; FATTY ACID DESATURATION; FATTY ACID OXIDATION; LIPID STORAGE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

3T3-L1 CELLS; ACYL-COA OXIDASE; ADIPOCYTES; ANIMALS; CARBON RADIOISOTOPES; CELL DIFFERENTIATION; ENZYME INHIBITORS; FATTY ACIDS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; IMMUNOHISTOCHEMISTRY; KINETICS; MICE; MIXED FUNCTION OXYGENASES; OXIDATION-REDUCTION; PALMITIC ACID; PEROXISOMES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; STEAROYL-COA DESATURASE; SUBSTRATE SPECIFICITY; TRITIUM;

ANIMALIA;

EID: 2142652105     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035867z     Document Type: Article

References (48)

1. Friedman, J. M. (2000) Obesity in the new millennium, Nature 404, 632-634.
2. Kopelman, P. G. (2000) Obesity as a medical problem, Nature 404, 635-643.
3. Gregoire, F. M., Smas, C. M., and Sul, H. S. (1998) Understanding adipocyte differentiation, Physiol. Rev. 78, 783-809.
4. Pi-Sunyer, X. (2003) A clinical view of the obesity problem, Science 299, 859-860.
5. Spiegelman, B. M., and Flier, J. S. (2001) Obesity and the regulation of energy balance, Cell 104, 531-543.
6. Lowell, B. B., and Spiegelman, B. M. (2000) Towards a molecular understanding of adaptive thermogenesis, Nature 404, 652-660.
7. Green, H., and Kehinde, O. (1975) An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion, Cell 5, 19-27.
8. Green, H., and Kehinde, O. (1976) Spontaneous heritable changes leading to increased adipose conversion in 3T3 cells, Cell 7, 105-113.
9. Reginato, M. J., Krakow, S. L., Bailey, S. T., and Lazar, M. A. (1998) Prostaglandins promote and block adipogenesis through opposing effects on peroxisome proliferator-activated receptor g, J. Biol. Chem. 273, 1855-1858.
10. Alexander, M., Curtis, G., Avruch, J., and Goodman, H. M. (1985) Insulin regulation of protein biosynthesis in differentiated 3T3 adipocytes. Regulation of glyceraldehyde-3-phosphate dehydrogenase, J. Biol. Chem. 260, 11978-11985.
11. Green, H., and Kehinde, O. (1979) Formation of normally differentiated subcutaneous fat pads by an established preadipose cell line, J. Cell. Physiol. 101, 169-171.
12. Wanders, R. J., Jansen, G. A., and Lloyd, M. D. (2003) Phytanic acid α-oxidation, new insights into an old problem: a review, Biochim. Biophys. Acta 1631, 119-135.
13. Wanders, R. J., Vreken, P., Ferdinandusse, S., Jansen, G. A., Waterham, H. R., van Roermund, C. W., and Van Grunsven, E. G. (2001) Peroxisomal fatty acid α- and β-oxidation in humans: enzymology, peroxisomal metabolite transporters and peroxisomal diseases, Biochem. Soc. Trans. 29, 250-267.
14. 2+ in addition to its known hydroxylation cofactors, J. Lipid Res. 41, 629-636.
15. Mukherji, M., Kershaw, N. J., Schofield, C. J., Wierzbicki, A. S., and Lloyd, M. D. (2002) Utilization of sterol carrier protein-2 by phytanoyl-CoA 2-hydroxylase in the peroxisomal α oxidation of phytanic acid, Chem. Biol. 9, 597-605.
16. Jansen, G. A., van den Brink, D. M., Ofman, R., Draghici, O., Dacremont, G., and Wanders, R. J. (2001) Identification of pristanal dehydrogenase activity in peroxisomes: conclusive evidence that the complete phytanic acid α-oxidation pathway is localized in peroxisomes, Biochem. Biophys. Res. Commun. 283, 674-679.
17. Jansen, G. A., Ofman, R., Denis, S., Ferdinandusse, S., Hogenhout, E. M., Jakobs, C., and Wanders, R. J. (1999) Phytanoyl-CoA hydroxylase from rat liver. Protein purification and cDNA cloning with implications for the subcellular localization of phytanic acid α-oxidation, J. Lipid Res. 40, 2244-2254.
18. Verhoeven, N. M., and Jakobs, C. (2001) Human metabolism of phytanic acid and pristanic acid, Prog. Lipid Res. 40, 453-466.
19. Mihalik, S. J., Morrell, J. C., Kim, D., Sacksteder, K. A., Watkins, P. A., and Gould, S. J. (1997) Identification of PAHX, a Refsum disease gene, Nat. Genet. 17, 185-189.
20. Frost, S. C., and Lane, M. D. (1985) Evidence for the involvement of vicinal sulfhydryl groups in insulin-activated hexose transport by 3T3-L1 adipocytes, J. Biol. Chem. 260, 2646-2652.
21. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipide extraction and purification, Can. J. Biochem. Physiol. 37, 911-917.
22. Han, X., and Gross, R. W. (1994) Electrospray ionization mass spectroscopic analysis of human erythrocyte plasma membrane phospholipids, Proc. Natl. Acad. Sci. U.S.A. 91, 10635-10639.
23. Han, X., Gubitosi-Klug, R. A., Collins, B. J., and Gross, R. W. (1996) Alterations in individual molecular species of human platelet phospholipids during thrombin stimulation: electrospray ionization mass spectrometry-facilitated identification of the boundary conditions for the magnitude and selectivity of thrombin-induced platelet phospholipid hydrolysis, Biochemistry 35, 5822-5832.
24. Han, X., Abendschein, D. R., Kelley, J. G., and Gross, R. W. (2000) Diabetes-induced changes in specific lipid molecular species in rat myocardium, Biochem. J. 352, 79-89.
25. Han, X., and Gross, R. W. (2001) Quantitative analysis and molecular species fingerprinting of triacylglyceride molecular species directly from lipid extracts of biological samples by electrospray ionization tandem mass spectrometry, Anal. Biochem. 295, 88-100.
26. Ford, D. A., Han, X., Homer, C. C., and Gross, R. W. (1996) Accumulation of Unsaturated Acylcamitine Molecular Species During Acute Myocardial Ischemia: Metabolic Compartmentalization of Products of Fatty Acyl Chain Elongation in the Acylcarnitine Pool, Biochemistry 35, 7903-7909.
27. Han, X., and Gross, R. W. (1995) Structural determination of picomole amounts of phospholipids via electrospray ionization tandem mass spectrometry, J. Am. Soc. Mass Spectrom. 6, 1202-1210.
28. Ford, D. A., Rosenbloom, K. B., and Gross, R. W. (1992) The primary determinant of rabbit myocardial ethanolamine phosphotransferase substrate selectivity is the covalent nature of the sn-1 aliphatic group of diradyl glycerol acceptors, J. Biol. Chem. 267, 11222-11228.
29. Gross, R. W. (1984) High plasmalogen and arachidonic acid content of canine myocardial sarcolemma: a fast atom bombardment mass spectroscopic and gas chromatography-mass spectroscopic characterization, Biochemistry 23, 158-165.
30. Buser, H. R., Am, H., Guerin, P., and Rauscher, S. (1983) Determination of double bond position in mono-unsaturated acetates by mass spectrometry of dimethyl disulfide adducts, Anal. Chem. 55, 818-822.
31. Ryhage, R., and Stenhagen, E. (1960) Mass spectrometry in lipid research, J. Lipid Res. 1, 361-390.
32. Gulick, T., Cresci, S., Caira, T., Moore, D. D., and Kelly, D. P. (1994) The peroxisome proliferator-activated receptor regulates mitochondrial fatty acid oxidative enzyme gene expression, Proc. Natl. Acad. Sci. U.S.A. 91, 11012-11016.
33. Cohen, P., Miyazaki, M., Socci, N. D., Hagge-Greenberg, A., Liedtke, W., Soukas, A. A., Sharma, R., Hudgins, L. C., Ntambi, J. M., and Friedman, J. M. (2002) Role for stearoyl-CoA desaturase-1 in leptin-mediated weight loss, Science 297, 240-243.
34. Ntambi, J. M., Miyazaki, M., Stoehr, J. P., Lan, H., Kendziorski, C. M., Yandell, B. S., Song, Y., Cohen, P., Friedman, J. M., and Attie, A. D. (2002) Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity, Proc. Natl. Acad. Sci. U.S.A. 99, 11482-11486.
35. Hajra, A. K., Larkins, L. K., Das, A. K., Hemati, N., Erickson, R. L., and MacDougald, O. A. (2000) Induction of the peroxisomal glycerolipid-synthesizing enzymes during differentiation of 3T3-L1 adipocytes. Role in triacylglycerol synthesis, J. Biol. Chem. 275, 9441-9446.
36. Ntambi, J. M., Buhrow, S. A., Kaestner, K. H., Christy, R. J., Sibley, E., Kelly, T. J., Jr., and Lane, M. D. (1988) Differentiation-induced gene expression in 3T3-L1 preadipocytes. Characterization of a differentially expressed gene encoding stearoyl-CoA desaturase, J. Biol. Chem. 263, 17291-17300.
37. Rachubinski, R. A., and Subramani, S. (1995) How proteins penetrate peroxisomes, Cell 83, 525-528.
38. Subramani, S. (1996) Protein translocation into peroxisomes, J. Biol. Chem. 271, 32483-32486.
39. Teasdale, R. D., and Jackson, M. R. (1996) Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the golgi apparatus, Annu. Rev. Cell Dev. Biol. 12, 27-54.
40. Blanchette-Mackie, E. J., Dwyer, N. K., Barber, T., Coxey, R. A., Takeda, T., Rondinone, C. M., Theodorakis, J. L., Greenberg, A. S., and Londos, C. (1995) Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes, J. Lipid Res. 36, 1211-1226.
41. Novikoff, A. B., Novikoff, P. M., Rosen, O. M., and Rubin, C. S. (1980) Organelle relationships in cultured 3T3-L 1 preadipocytes, J. Cell Biol. 87, 180-196.
42. Han, X., and Gross, R. W. (2003) Global analyses of cellular lipidomes directly from crude extracts of biological samples by ESI mass spectrometry: A bridge to lipidomics, J. Lipid Res. 44, 1071-1079.
43. Fowler, S., Remacle, J., Trouet, A., Beaufay, H., Berthet, J., Wibo, M., and Hauser, P. (1976) Analytical study of microsomes and isolated subcellular membranes from rat liver. V. Immunological localization of cytochrome b5 by electron microscopy: methodology and application to various subcellular fractions, J. Cell Biol. 71, 535-550.
44. Appelkvist, E. L., Brunk, U., and Dallner, G. (1981) Isolation of peroxisomes from rat liver using sucrose and Percoll gradients, J. Biochem. Biophys. Methods 5, 203-217.
45. Kikuchi, M., Hatano, N., Yokota, S., Shimozawa, N., Imanaka, T., and Taniguchi, H. (2004) Proteomic Analysis of Rat Liver Peroxisome: Presence of Peroxisome-Specific Isozyme of Lon Protease, J. Biol. Chem. 279, 421-428.
46. Belmouden, A., Le, K. H., Lederer, F., and Garchon, H. J. (1993) Molecular cloning and nucleotide sequence of cDNA encoding rat kidney long-chain L-2-hydroxy acid oxidase. Expression of the catalytically active recombinant protein as a chimaera, Eur. J. Biochem. 214, 17-25.
47. Diep Le, K. H., and Lederer, F. (1991) Amino acid sequence of long chain α-hydroxy acid oxidase from rat kidney, a member of the family of FMN-dependent α-hydroxy acid-oxidizing enzymes, J. Biol. Chem. 266, 20877-20881.
48. Jones, J. M., Morrell, J. C., and Gould, S. J. (2000) Identification and characterization of HAOX1, HAOX2, and HAOX3, three human peroxisomal 2-hydroxy acid oxidases, J. Biol. Chem. 275, 12590-12597.