Increase in secretory sphingomyelinase activity and specific ceramides in the aorta of apolipoprotein e knockout mice during aging

Biological and Pharmaceutical Bulletin

Volumn 36, Issue 7, 2013, Pages 1192-1196

  Kobayashi, Keiko ^a   Nagata, Eri ^a   Sasaki, Kazuki ^a   Harada Shiba, Mariko ^b   Kojo, Shosuke ^c   Kikuzaki, Hiroe ^a  

^a NARA WOMEN'S UNIVERSITY   (Japan)

^b NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^c OPEN UNIVERSITY OF JAPAN   (Japan)

Author keywords

Aging; Apolipoprotein E; Atherosclerosis; Ceramide; Sphingomyelinase

Indexed keywords

APOLIPOPROTEIN E; CERAMIDE; LOW DENSITY LIPOPROTEIN; SPHINGOMYELIN PHOSPHODIESTERASE;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; BLOOD ANALYSIS; CONTROLLED STUDY; DIABETES MELLITUS; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; KNOCKOUT MOUSE; LIPID METABOLISM; LIPOPROTEIN BLOOD LEVEL; MOUSE; NONHUMAN; OXIDATIVE STRESS; UPREGULATION; WILD TYPE;

AGING; ANIMALS; AORTA; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CERAMIDES; DISEASE MODELS, ANIMAL; FEMALE; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 84880410237     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b13-00180     Document Type: Article

References (36)

1. Hannun YA, Obeid LM. The ceramide-centric universe of lipidmediated cell regulation: stress encounters of the lipid kind. J. Biol. Chem., 277, 25847-25850 (2002).
2. Kolesnick R. Ceramide: a novel second messenger. Trends Cell Biol., 2, 232-236 (1992).
3. Farrell AM, Uchida Y, Nagiec MM, Harris IR, Dickson RC, Elias PM, Holleran WM. UVB irradiation up-regulates serine palmitoyltransferase in cultured human keratinocytes. J. Lipid Res., 39, 2031-2038 (1998).
4. Santana P, Peña LA, Haimovitz-Friedman A, Martin S, Green D, McLoughlin M, Cordon-Cardo C, Schuchman EH, Fuks Z, Kolesnick R. Acid sphingomyelinase-deficient human lymphoblasts and mice are defective in radiation-induced apoptosis. Cell, 86, 189-199 (1996).
5. Merrill AH Jr, Jones DD. An update of the enzymology and regulation of sphingomyelin metabolism. Biochim. Biophys. Acta, 1044, 1-12 (1990).
6. Yamada Y, Kajiwara K, Yano M, Kishida E, Masuzawa Y, Kojo S. Increase of ceramides and its inhibition by catalase during chemically induced apoptosis of HL-60 cells determined by electrospray ionization tandem mass spectrometry. Biochim. Biophys. Acta, 1532, 115-120 (2001).
7. Goñi FM, Alonso A. Sphingomyelinases: enzymology and membrane activity. FEBS Lett., 531, 38-46 (2002).
8. Schuchman EH. Acid sphingomyelinase, cell membranes and human disease: lessons from Niemann-Pick disease. FEBS Lett., 584, 1895-1900 (2010).
9. Schissel SL, Keesler GA, Schuchman EH, Williams KJ, Tabas I. The cellular trafficking and zinc dependence of secretory and lysosomal sphingomyelinase, two products of the acid sphingomyelinase gene. J. Biol. Chem., 273, 18250-18259 (1998).
10. Jenkins RW, Canals D, Idkowiak-Baldys J, Simbari F, Roddy P, Perry DM, Kitatani K, Luberto C, Hannun YA. Regulated secretion of acid sphingomyelinase: implications for selectivity of ceramide formation. J. Biol. Chem., 285, 35706-35718 (2010).
11. Tabas I. Secretory sphingomyelinase. Chem. Phys. Lipids, 102, 123-130 (1999).
12. Walters MJ, Wrenn SP. Effect of sphingomyelinase-mediated generation of ceramide on aggregation of low-density lipoprotein. Langmuir, 24, 9642-9647 (2008).
13. Morita SY, Kawabe M, Sakurai A, Okuhira K, Vertut-Doï A, Nakano M, Handa T. Ceramide in lipid particles enhances heparan sulfate proteoglycan and low density lipoprotein receptor-related protein-mediated uptake by macrophages. J. Biol. Chem., 279, 24355-24361 (2004).
14. Ichi I, Nakahara K, Miyashita Y, Hidaka A, Kutsukake S, Inoue K, Maruyama T, Miwa Y, Harada-Shiba M, Tsushima M, Kojo S, Kisei Cohort Study Grooup. Association of ceramides in human plasma with risk factors of atherosclerosis. Lipids, 41, 859-863 (2006).
15. Deevska GM, Sunkara M, Morris AJ, Nikolova-Karakashian MN. Characterization of secretory sphingomyelinase activity, lipoprotein sphingolipid content and LDL aggregation in ldlr-/-mice fed on a high-fat diet. Biosci. Rep., 32, 479-490 (2012).
16. Ichi I, Takashima Y, Adachi N, Nakahara K, Kamikawa C, Harada-Shiba M, Kojo S. Effects of dietary cholesterol on tissue ceramides and oxidation products of apolipoprotein B-100 in ApoE-deficient mice. Lipids, 42, 893-900 (2007).
17. Kobayashi K, Ichi I, Nakagawa T, Kamikawa C, Kitamura Y, Koga E, Washino Y, Hoshinaga Y, Kojo S. Increase in plasma ceramide levels via secretory sphingomyelinase activity in streptozotocininduced diabetic rats. Med. Chem. Commun., 2, 536-541 (2011).
18. Doehner W, Bunck AC, Rauchhaus M, von Haehling S, Brunkhorst FM, Cicoira M, Tschope C, Ponikowski P, Claus RA, Anker SD. Secretory sphingomyelinase is upregulated in chronic heart failure: a second messenger system of immune activation relates to body composition, muscular functional capacity, and peripheral blood flow. Eur. Heart J., 28, 821-828 (2007).
19. Górska M, Baranczuk E, Dobrzyn A. Secretory Zn2+-dependent sphingomyelinase activity in the serum of patients with type 2 diabetes is elevated. Horm. Metab. Res., 35, 506-507 (2003).
20. Filosto S, Fry W, Knowlton AA, Goldkorn T. Neutral sphingomyelinase 2 (nSMase2) is a phosphoprotein regulated by calcineurin (PP2B). J. Biol. Chem., 285, 10213-10222 (2010).
21. Ichi I, Kamikawa C, Nakagawa T, Kobayashi K, Kataoka R, Nagata E, Kitamura Y, Nakazaki C, Matsura T, Kojo S. Neutral sphingomyelinase-induced ceramide accumulation by oxidative stress during carbon tetrachloride intoxication. Toxicology, 261, 33-40 (2009).
22. Lightle SA, Oakley JI, Nikolova-Karakashian MN. Activation of sphingolipid turnover and chronic generation of ceramide and sphingosine in liver during aging. Mech. Ageing Dev., 120, 111-125 (2000).
23. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193, 265-275 (1951).
24. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol., 37, 911-917 (1959).
25. Folch J, Ascoli I, Lees M, Meath JA, LeBaron N. Preparation of lipid extracts from brain tissue. J. Biol. Chem., 191, 833-841 (1951).
26. Yano M, Kishida E, Muneyuki Y, Masuzawa Y. Quantitative analysis of ceramide molecular species by high performance liquid chromatography. J. Lipid Res., 39, 2091-2098 (1998).
27. Wiesner P, Leidl K, Boettcher A, Schmitz G, Liebisch G. Lipid profiling of FPLC-separated lipoprotein fractions by electrospray ionization tandem mass spectrometry. J. Lipid Res., 50, 574-585 (2009).
28. Hammad SM, Pierce JS, Soodavar F, Smith KJ, Al Gadban MM, Rembiesa B, Klein RL, Hannun YA, Bielawski J, Bielawska A. Blood sphingolipidomics in healthy humans: impact of sample collection methodology. J. Lipid Res., 51, 3074-3087 (2010).
29. Kato R, Mori C, Kitazato K, Arata S, Obama T, Mori M, Takahashi K, Aiuchi T, Takano T, Itabe H. Transient increase in plasma oxidized LDL during the progression of atherosclerosis in apolipoprotein E knockout mice. Arterioscler. Thromb. Vasc. Biol., 29, 33-39 (2009).
30. Schissel SL, Tweedie-Hardman J, Rapp JH, Graham G, Williams KJ, Tabas I. Rabbit aorta and human atherosclerotic lesions hydrolyze the sphingomyelin of retained low-density lipoprotein. Proposed role for arterial-wall sphingomyelinase in subendothelial retention and aggregation of atherogenic lipoproteins. J. Clin. Invest., 98, 1455-1464 (1996).
31. Plump AS, Smith JD, Hayek T, Aalto-Setälä K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell, 71, 343-353 (1992).
32. Zhang SH, Reddick RL, Piedrahita JA, Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science, 258, 468-471 (1992).
33. Grösch S, Schiffmann S, Geisslinger G. Chain length-specific properties of ceramides. Prog. Lipid Res., 51, 50-62 (2012).
34. ten Grotenhuis E, Demel RA, Ponec M, Boer DR, van Miltenburg JC, Bouwstra JA. Phase behavior of stratum corneum lipids in mixed Langmuir-Blodgett monolayers. Biophys. J., 71, 1389-1399 (1996).
35. Mesicek J, Lee H, Feldman T, Jiang X, Skobeleva A, Berdyshev EV, Haimovitz-Fridman A, Fuks Z, Kolesnick R. Ceramide synthases 2, 5, and 6 confer distinct roles in radiation-induced apoptosis in HeLa cells. Cell. Signal., 22, 1300-1307 (2010).
36. Zigdon H, Kogot-Levin A, Park JW, Goldschmidt R, Kelly S, Merrill AH Jr, Scherz A, Pewzner-Jung Y, Saada A, Futerman AH. Ablation of ceramide synthase 2 causes chronic oxidative stress due to disruption of the mitochondrial respiratory chain. J. Biol. Chem., 288, 4947-4956 (2013).