Dependence of brown adipose tissue function on CD36-mediated coenzyme Q uptake

Cell Reports

Volumn 10, Issue 4, 2015, Pages 505-515

  Anderson, Courtney M ^a   Kazantzis, Melissa ^a   Wang, Jinshan ^a   Venkatraman, Subramaniam ^a   Goncalves, Renata L S ^b   Quinlan, Casey L ^b   Ng, Ryan ^b   Jastroch, Martin ^b   Benjamin, Daniel I ^a   Nie, Biao ^a   Herber, Candice ^a   Van, An Angela Ngoc ^a   Park, Michael J ^a   Yun, Dawee ^a   Chan, Karen ^a   Yu, Angela ^a   Vuong, Peter ^a   Febbraio, Maria ^c   Nomura, Daniel K ^a   Napoli, Joseph L ^a   Brand, Martin D ^b   Stahl, Andreas ^a   more..

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; SCAVENGER RECEPTOR; UBIQUINONE; MITOCHONDRIAL PROTEIN; PALMITIC ACID;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; FATTY ACID TRANSPORT; HOMEOSTASIS; HUMAN; HYDROPHOBICITY; LIPID METABOLISM; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; THERMOGENESIS; UPREGULATION; ANIMAL; ATAXIA; C57BL MOUSE; DEFICIENCY; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MITOCHONDRION; MUSCLE WEAKNESS; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

MUS;

ADIPOSE TISSUE, BROWN; ANIMALS; ANTIGENS, CD36; ATAXIA; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MITOCHONDRIAL PROTEINS; MUSCLE WEAKNESS; OXIDATION-REDUCTION; PALMITIC ACID; THERMOGENESIS; UBIQUINONE;

EID: 84922805752     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.12.048     Document Type: Article

References (53)

1. Abumrad N.A., el-Maghrabi M.R., Amri E.Z., Lopez E., Grimaldi P.A. Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J.Biol. Chem. 1993, 268:17665-17668.
2. Acton S., Rigotti A., Landschulz K.T., Xu S., Hobbs H.H., Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 1996, 271:518-520.
3. Aherne W., Hull D. Brown adipose tissue and heat production in the newborn infant. J.Pathol. Bacteriol. 1966, 91:223-234.
4. Ahmadian M., Duncan R.E., Varady K.A., Frasson D., Hellerstein M.K., Birkenfeld A.L., Samuel V.T., Shulman G.I., Wang Y., Kang C., Sul H.S. Adipose overexpression of desnutrin promotes fatty acid use and attenuates diet-induced obesity. Diabetes 2009, 58:855-866.
5. Anderson C.M., Stahl A. SLC27 fatty acid transport proteins. Mol. Aspects Med. 2013, 34:516-528.
6. Argyropoulos G., Harper M.E. Uncoupling proteins and thermoregulation. J.Appl. Physiol. 2002, 92:2187-2198.
7. 10 deficiencies in neuromuscular diseases. Adv. Exp. Med. Biol. 2009, 652:117-128.
8. Bartelt A., Bruns O.T., Reimer R., Hohenberg H., Ittrich H., Peldschus K., Kaul M.G., Tromsdorf U.I., Weller H., Waurisch C., et al. Brown adipose tissue activity controls triglyceride clearance. Nat. Med. 2011, 17:200-205.
9. Bastie C.C., Hajri T., Drover V.A., Grimaldi P.A., Abumrad N.A. CD36 in myocytes channels fatty acids to a lipase-accessible triglyceride pool that is related to cell lipid and insulin responsiveness. Diabetes 2004, 53:2209-2216.
10. Bentinger M., Tekle M., Dallner G. Coenzyme Q-biosynthesis and functions. Biochem. Biophys. Res. Commun. 2010, 396:74-79.
11. 10: absorption, tissue uptake, metabolism and pharmacokinetics. Free Radic. Res. 2006, 40:445-453.
12. Borel P., de Edelenyi F.S., Vincent-Baudry S., Malezet-Desmoulin C., Margotat A., Lyan B., Gorrand J.M., Meunier N., Drouault-Holowacz S., Bieuvelet S. Genetic variants in BCMO1 and CD36 are associated with plasma lutein concentrations and macular pigment optical density in humans. Ann. Med. 2011, 43:47-59.
13. Borel P., Lietz G., Goncalves A., Szabo de Edelenyi F., Lecompte S., Curtis P., Goumidi L., Caslake M.J., Miles E.A., Packard C., et al. CD36 and SR-BI are involved in cellular uptake of provitamin A carotenoids by Caco-2 and HEK cells, and some of their genetic variants are associated with plasma concentrations of these micronutrients in humans. J.Nutr. 2013, 143:448-456.
14. Calvo D., Dopazo J., Vega M.A. The CD36, CLA-1 (CD36L1), and LIMPII (CD36L2) gene family: cellular distribution, chromosomal location, and genetic evolution. Genomics 1995, 25:100-106.
15. Calvo D., Gómez-Coronado D., Suárez Y., Lasunción M.A., Vega M.A. Human CD36 is a high affinity receptor for the native lipoproteins HDL, LDL, and VLDL. J.Lipid Res. 1998, 39:777-788.
16. Coburn C.T., Knapp F.F., Febbraio M., Beets A.L., Silverstein R.L., Abumrad N.A. Defective uptake and utilization of long chain fatty acids in muscle and adipose tissues of CD36 knockout mice. J.Biol. Chem. 2000, 275:32523-32529.
17. Coburn C.T., Hajri T., Ibrahimi A., Abumrad N.A. Role of CD36 in membrane transport and utilization of long-chain fatty acids by different tissues. J.Mol. Neurosci. 2001, 16:117-121. discussion 151-117.
18. 10. J.Am. Coll. Nutr. 2001, 20:591-598.
19. Cypess A.M., Lehman S., Williams G., Tal I., Rodman D., Goldfine A.B., Kuo F.C., Palmer E.L., Tseng Y.H., Doria A., et al. Identification and importance of brown adipose tissue in adult humans. N.Engl. J. Med. 2009, 360:1509-1517.
20. Febbraio M., Abumrad N.A., Hajjar D.P., Sharma K., Cheng W., Pearce S.F., Silverstein R.L. A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J.Biol. Chem. 1999, 274:19055-19062.
21. Febbraio M., Podrez E.A., Smith J.D., Hajjar D.P., Hazen S.L., Hoff H.F., Sharma K., Silverstein R.L. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J.Clin. Invest. 2000, 105:1049-1056.
22. Greaves D.R., Gordon S. The macrophage scavenger receptor at 30 years of age: current knowledge and future challenges. J.Lipid Res. 2009, 50(Suppl):S282-S286.
23. Harmon C.M., Abumrad N.A. Binding of sulfosuccinimidyl fatty acids to adipocyte membrane proteins: isolation and amino-terminal sequence of an 88-kD protein implicated in transport of long-chain fatty acids. J.Membr. Biol. 1993, 133:43-49.
24. Heaton J.M. The distribution of brown adipose tissue in the human. J.Anat. 1972, 112:35-39.
25. Kiefer C., Sumser E., Wernet M.F., Von Lintig J. A class B scavenger receptor mediates the cellular uptake of carotenoids in Drosophila. Proc. Natl. Acad. Sci. USA 2002, 99:10581-10586.
26. Kuniyasu A., Hayashi S., Nakayama H. Adipocytes recognize and degrade oxidized low density lipoprotein through CD36. Biochem. Biophys. Res. Commun. 2002, 295:319-323.
27. Kuzuyama T., Seto H. Two distinct pathways for essential metabolic precursors for isoprenoid biosynthesis. Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci. 2012, 88:41-52.
28. Lass A., Agarwal S., Sohal R.S. Mitochondrial ubiquinone homologues, superoxide radical generation, and longevity in different mammalian species. J.Biol. Chem. 1997, 272:19199-19204.
29. Moussa M., Gouranton E., Gleize B., Yazidi C.E., Niot I., Besnard P., Borel P., Landrier J.F. CD36 is involved in lycopene and lutein uptake by adipocytes and adipose tissue cultures. Mol. Nutr. Food Res. 2011, 55:578-584.
30. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
31. Nergiz-Unal R., Rademakers T., Cosemans J.M., Heemskerk J.W. CD36 as a multiple-ligand signaling receptor in atherothrombosis. Cardiovasc. Hematol. Agents Med. Chem. 2011, 9:42-55.
32. Oelkrug R., Kutschke M., Meyer C.W., Heldmaier G., Jastroch M. Uncoupling protein 1 decreases superoxide production in brown adipose tissue mitochondria. J.Biol. Chem. 2010, 285:21961-21968.
33. Padilla-López S., Jiménez-Hidalgo M., Martín-Montalvo A., Clarke C.F., Navas P., Santos-Ocaña C. Genetic evidence for the requirement of the endocytic pathway in the uptake of coenzyme Q6 in Saccharomyces cerevisiae. Biochim. Biophys. Acta 2009, 1788:1238-1248.
34. Parker N., Crichton P.G., Vidal-Puig A.J., Brand M.D. Uncoupling protein-1 (UCP1) contributes to the basal proton conductance of brown adipose tissue mitochondria. J.Bioenerg. Biomembr. 2009, 41:335-342.
35. Plüddemann A., Neyen C., Gordon S. Macrophage scavenger receptors and host-derived ligands. Methods 2007, 43:207-217.
36. Podda M., Weber C., Traber M.G., Milbradt R., Packer L. Sensitive high-performance liquid chromatography techniques for simultaneous determination of tocopherols, tocotrienols, ubiquinols, and ubiquinones in biological samples. Methods Enzymol. 1999, 299:330-341.
37. 10 deficiencies. Biofactors 2008, 32:113-118.
38. Reboul E., Borel P. Proteins involved in uptake, intracellular transport and basolateral secretion of fat-soluble vitamins and carotenoids by mammalian enterocytes. Prog. Lipid Res. 2011, 50:388-402.
39. Schneider H., Lemasters J.J., Höchli M., Hackenbrock C.R. Fusion of liposomes with mitochondrial inner membranes. Proc. Natl. Acad. Sci. USA 1980, 77:442-446.
40. Sekhar B.S., Kurup C.K., Ramasarma T. Microsomal redox systems in brown adipose tissue: high lipid peroxidation, low cholesterol biosynthesis and no detectable cytochrome P-450. Mol. Cell. Biochem. 1990, 92:147-157.
41. Sell H., Deshaies Y., Richard D. The brown adipocyte: update on its metabolic role. Int. J. Biochem. Cell Biol. 2004, 36:2098-2104.
42. Sohet F.M., Delzenne N.M. Is there a place for coenzyme Q in the management of metabolic disorders associated with obesity?. Nutr. Rev. 2012, 70:631-641.
43. Su X., Abumrad N.A. Cellular fatty acid uptake: a pathway under construction. Trends Endocrinol. Metab. 2009, 20:72-77.
44. Taskinen M.R., Nikkilä E.A., Kuusi T., Tulikoura I. Changes of high density lipoprotein subfraction concentration and composition by intralipid invivo and by lipolysis of intralipid invitro. Arteriosclerosis 1983, 3:607-615.
45. Thelin A., Schedin S., Dallner G. Half-life of ubiquinone-9 in rat tissues. FEBS Lett. 1992, 313:118-120.
46. 10 ratio as a possible marker of increased risk for atherosclerosis. Biofactors 1999, 9:231-240.
47. van Marken Lichtenbelt W.D., Vanhommerig J.W., Smulders N.M., Drossaerts J.M., Kemerink G.J., Bouvy N.D., Schrauwen P., Teule G.J. Cold-activated brown adipose tissue in healthy men. N.Engl. J. Med. 2009, 360:1500-1508.
48. Van Nieuwenhoven F.A., Verstijnen C.P., Abumrad N.A., Willemsen P.H., Van Eys G.J., Van der Vusse G.J., Glatz J.F. Putative membrane fatty acid translocase and cytoplasmic fatty acid-binding protein are co-expressed in rat heart and skeletal muscles. Biochem. Biophys. Res. Commun. 1995, 207:747-752.
49. Virtanen K.A., Lidell M.E., Orava J., Heglind M., Westergren R., Niemi T., Taittonen M., Laine J., Savisto N.J., Enerbäck S., Nuutila P. Functional brown adipose tissue in healthy adults. N.Engl. J. Med. 2009, 360:1518-1525.
50. Williams J.N. A method for the simultaneous quantitative estimation of cytochromes a, b, c1, and c in mitochondria. Arch. Biochem. Biophys. 1964, 107:537-543.
51. Wu Q., Kazantzis M., Doege H., Ortegon A.M., Tsang B., Falcon A., Stahl A. Fatty acid transport protein 1 is required for nonshivering thermogenesis in brown adipose tissue. Diabetes 2006, 55:3229-3237.
52. Zeng Y., Tao N., Chung K.N., Heuser J.E., Lublin D.M. Endocytosis of oxidized low density lipoprotein through scavenger receptor CD36 utilizes a lipid raft pathway that does not require caveolin-1. J.Biol. Chem. 2003, 278:45931-45936.
53. Zimmet P., Alberti K.G., Shaw J. Global and societal implications of the diabetes epidemic. Nature 2001, 414:782-787.