Increased Oxidative Stress Impairs Adipose Tissue Function in Sphingomyelin Synthase 1 Null Mice

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Yano, Masato ^a   Yamamoto, Tadashi ^a,b   Nishimura, Naotaka ^a   Gotoh, Tomomi ^a   Watanabe, Ken ^c   Ikeda, Kazutaka ^d,f,i   Garan, Yohei ^a   Taguchi, Ryo ^d,g,i   Node, Koichi ^b   Okazaki, Toshiro ^e,h   Oike, Yuichi ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b SAGA UNIVERSITY   (Japan)

^c NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e TOTTORI UNIVERSITY   (Japan)

^f KEIO UNIVERSITY   (Japan)

^g CHUBU UNIVERSITY   (Japan)

^h KANAZAWA MEDICAL UNIVERSITY   (Japan)

ⁱ JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; LIPOPROTEIN LIPASE; MESSENGER RNA; SPHINGOMYELIN SYNTHASE 1; SYNTHETASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOGENESIS; CELL CULTURE; CELL STRESS; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME REPRESSION; FATTY ACID TRANSPORT; IN VITRO STUDY; IN VIVO STUDY; LIPODYSTROPHY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PROTEIN CONTENT; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; WHITE ADIPOSE TISSUE;

ACETYLCYSTEINE; ADIPOSE TISSUE, WHITE; ANIMALS; ANTIOXIDANTS; FATTY ACIDS; HYPERLIPIDEMIAS; LIPODYSTROPHY; LIPOPROTEIN LIPASE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL TURNOVER; OXIDATIVE STRESS; PHENOTYPE; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS);

MUS;

EID: 84876086377     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061380     Document Type: Article

References (55)

1. Futerman AH, Hannun YA, (2004) The complex life of simple sphingolipids. EMBO Rep 5: 777-782.
2. Zheng W, Kollmeyer J, Symolon H, Momin A, Munter E, et al. (2006) Ceramides and other bioactive sphingolipid backbones in health and disease: lipidomic analysis, metabolism and roles in membrane structure, dynamics, signaling and autophagy. Biochim Biophys Acta 1758: 1864-1884.
3. Simons K, Gerl MJ, (2010) Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 11: 688-699.
4. Lingwood D, Simons K, (2010) Lipid rafts as a membrane-organizing principle. Science 327: 46-50.
5. Milhas D, Clarke CJ, Hannun YA, (2010) Sphingomyelin metabolism at the plasma membrane: implications for bioactive sphingolipids. FEBS Lett 584: 1887-1894.
6. Hannun YA, Obeid LM, (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9: 139-150.
7. Zeidan YH, Hannun YA, (2007) Translational aspects of sphingolipid metabolism. Trends Mol Med 13: 327-336.
8. Alvarez SE, Milstien S, Spiegel S, (2007) Autocrine and paracrine roles of sphingosine-1-phosphate. Trends Endocrinol Metab 18: 300-307.
9. van Meer G, Voelker DR, Feigenson GW, (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9: 112-124.
10. Wymann MP, Schneiter R, (2008) Lipid signalling in disease. Nat Rev Mol Cell Biol 9: 162-176.
11. Fyrst H, Saba JD, (2010) An update on sphingosine-1-phosphate and other sphingolipid mediators. Nat Chem Biol 6: 489-497.
12. Hannun YA, Obeid LM, (2002) The Ceramide-centric universe of lipid-mediated cell regulation: stress encounters of the lipid kind. J Biol Chem 277: 25847-25850.
13. Mao C, Obeid LM, (2008) Ceramidases: regulators of cellular responses mediated by ceramide, sphingosine, and sphingosine-1-phosphate. Biochim Biophys Acta 1781: 424-434.
14. Haughey NJ, Bandaru VV, Bae M, Mattson MP, (2010) Roles for dysfunctional sphingolipid metabolism in Alzheimer's disease neuropathogenesis. Biochim Biophys Acta 1801: 878-886.
15. Park JH, Schuchman EH, (2006) Acid ceramidase and human disease. Biochim Biophys Acta 1758: 2133-2138.
16. Menaldino DS, Bushnev A, Sun A, Liotta DC, Symolon H, et al. (2003) Sphingoid bases and de novo ceramide synthesis: enzymes involved, pharmacology and mechanisms of action. Pharmacol Res 47: 373-381.
17. Tafesse FG, Ternes P, Holthuis JC, (2006) The multigenic sphingomyelin synthase family. J Biol Chem 281: 29421-29425.
18. Hanada K, Kumagai K, Yasuda S, Miura Y, Kawano M, et al. (2003) Molecular machinery for non-vesicular trafficking of ceramide. Nature 426: 803-809.
19. Hanada K, Kumagai K, Tomishige N, Yamaji T, (2009) CERT-mediated trafficking of ceramide. Biochim Biophys Acta 1791: 684-691.
20. Yamaoka S, Miyaji M, Kitano T, Umehara H, Okazaki T, (2004) Expression cloning of a human cDNA restoring sphingomyelin synthesis and cell growth in sphingomyelin synthase-defective lymphoid cells. J Biol Chem 279: 18688-18693.
21. Wang X, Rao RP, Kosakowska-Cholody T, Masood MA, Southon E, et al. (2009) Mitochondrial degeneration and not apoptosis is the primary cause of embryonic lethality in ceramide transfer protein mutant mice. J Cell Biol 184: 143-158.
22. Rao RP, Yuan C, Allegood JC, Rawat SS, Edwards MB, et al. (2007) Ceramide transfer protein function is essential for normal oxidative stress response and lifespan. Proc Natl Acad Sci USA 104: 11364-11369.
23. Hailemariam TK, Huan C, Liu J, Li Z, Roman C, et al. (2008) Sphingomyelin synthase 2 deficiency attenuates NFkappaB activation. Arterioscl Thromb Vasc Biol 28: 1519-1526.
24. Liu J, Huan C, Chakraborty M, Zhang H, Lu D, et al. (2009) Macrophage sphingomyelin synthase 2 deficiency decreases atherosclerosis in mice. Circ Res 105: 295-303.
25. Mitsutake S, Zama K, Yokota H, Yoshida T, Tanaka M, et al. (2011) Dynamic modification of sphingomyelin in lipid microdomains controls development of obesity, fatty liver, and type 2 diabetes. J Biol Chem 286: 28544-28555.
26. Miyaji M, Jin ZX, Yamaoka S, Amakawa R, Fukuhara S, et al. (2005) Role of membrane sphingomyelin and ceramide in platform formation for Fas-mediated apoptosis. J Exp Med 202: 249-259.
27. Separovic D, Semaan L, Tarca AL, Awad Maitah MY, Hanada K, et al. (2008) Suppression of sphingomyelin synthase 1 by small interference RNA is associated with enhanced ceramide production and apoptosis after photodamage. Exp Cell Res 314: 1860-1868.
28. Yano M, Watanabe K, Yamamoto T, Ikeda K, Senokuchi T, et al. (2011) Mitochondrial dysfunction and increased reactive oxygen species impair insulin secretion in sphingomyelin synthase 1-null mice. J Biol Chem 286: 3992-4002.
29. Oike Y, Akao M, Yasunaga K, Yamauchi T, Morisada T, et al. (2005) Angiopoietin-related growth factor antagonizes obesity and insulin resistance. Nat Med 11: 400-408.
30. Usui S, Hara Y, Hosaki S, Okazaki M, (2002) A new on-line dual enzymatic method for simultaneous quantification of cholesterol and triglycerides in lipoproteins by HPLC. J Lipid Res 43: 805-814.
31. Nunes AF, Saraiva MJ, Sousa MM, (2006) Transthyretin knockouts are a new mouse model for increased neuropeptide Y. FASEB J 20: 166-168.
32. Bligh EG, Dyer WJ, (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
33. Ikeda K, Oike Y, Shimizu T, Taguchi R, (2009) Global analysis of triacylglycerols including oxidized molecular species by reverse-phase high resolution LC/ESI-QTOF MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci 877: 2639-2647.
34. Yano M, Terada K, Gotoh T, Mori M, (2007) In vitro analysis of Bcl-2 proteins in mitochondria and endoplasmic reticulum: similarities in anti-apoptotic functions and differences in regulation. Exp Cell Res 313: 3767-3778.
35. Schägger H, Pfeiffer K, (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19: 1777-1783.
36. Dabbeni-Sala F, Di Santo S, Franceschini D, Skaper SD, Giusti P, (2001) Melatonin protects against 6-OHDA-induced neurotoxicity in rats: a role for mitochondrial complex I activity. FASEB J 15: 164-170.
37. Klemm DJ, Leitner JW, Watson P, Nesterova A, Reusch JE, et al. (2001) Insulin-induced adipocyte differentiation. Activation of CREB rescues adipogenesis from the arrest caused by inhibition of prenylation. J Biol Chem 276: 28430-28435.
38. Fajas L, Fruchart JC, Auwerx J, (1998) Transcriptional control of adipogenesis. Curr Opin Cell Biol 10: 165-173.
39. Lefterova MI, Lazar MA, (2009) New developments in adipogenesis. Trends Endocrinol Metab 20: 107-114.
40. White UA, Stephens JM, (2009) Transcriptional factors that promote formation of white adipose tissue. Mol Cell Endocrinol 318: 10-14.
41. Grimsrud PA, Xie H, Griffin TJ, Bernlohr DA, (2008) Oxidative stress and covalent modification of protein with bioactive aldehydes. J Biol Chem 283: 21837-21841.
42. Esterbauer H, Schaur RJ, Zollner H, (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11: 81-128.
43. Voshol PJ, Rensen PC, van Dijk KW, Romijn JA, Havekes LM, (2009) Effect of plasma triglyceride metabolism on lipid storage in adipose tissue: studies using genetically engineered mouse models. Biochim Biophys Acta 1791: 479-485.
44. Simha V, Garg A, (2009) Inherited lipodystrophies and hypertriglyceridemia. Curr Opin Lipidol 20: 300-308.
45. Garg A, Agarwal AK, (2009) Lipodystrophies: disorders of adipose tissue biology. Biochim Biophys Acta 1791: 507-513.
46. Hannun YA, (1996) Functions of ceramide in coordinating cellular responses to stress. Science 274: 1855-1859.
47. Pettus BJ, Chalfant CE, Hannun YA, (2002) Ceramide in apoptosis: an overview and current perspectives. Biochim Biophys Acta 1585: 114-125.
48. Richter C, Gogvadze V, Laffranchi R, Schlapbach R, Schweizer M, et al. (1995) Oxidants in mitochondria: from physiology to diseases. Biochim Biophys Acta 1271: 67-74.
49. Baker BM, Haynes CM, (2011) Mitochondrial protein quality control during biogenesis and aging. Trends Biochem Sci 36: 254-261.
50. Aldridge JE, Horibe T, Hoogenraad NJ, (2007) Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements. PLoS One 2: e874.
51. Choksi KB, Boylston WH, Rabek JP, Widger WR, Papaconstantinou J, (2004) Oxidatively damaged proteins of heart mitochondrial electron transport complexes. Biochim Biophys Acta 1688: 95-101.
52. Singh NR, Rondeau P, Hoareau L, Bourdon E, (2007) Identification of preferential protein targets for carbonylation in human mature adipocytes treated with native or glycated albumin. Free Radic Res 41: 1078-1088.
53. Wang T, Si Y, Shirihai OS, Si H, Schultz V, et al. (2010) Respiration in adipocytes is inhibited by reactive oxygen species. Obesity (Silver Spring) 18: 1493-1502.
54. Lu MH, Takemoto M, Watanabe K, Luo H, Nishimura M, et al. (2012) Deficiency of sphingomyelin synthase-1 but not sphingomyelin synthase-2 causes hearing impairments in mice. J Physiol 590: 4029-4044.
55. Dong L, Watanabe K, Itoh M, Huan CR, Tong XP, et al. (2012) CD4+ T-cell dysfunctions through the impaired lipid rafts ameliorate concanavalin A-induced hepatitis in sphingomyelin synthase 1-knockout mice. Int Immunol 24: 327-337.