Chronic voluntary ethanol consumption induces favorable ceramide profiles in selectively bred alcohol-preferring (P) rats

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Godfrey, Jessica ^a   Jeanguenin, Lisa ^a   Castro, Norma ^a   Olney, Jeffrey J ^a   Dudley, Jason ^a   Pipkin, Joseph ^a   Walls, Stanley M ^a   Wang, Wei ^b   Herr, Deron R ^a,b   Harris, Greg L ^a   Brasser, Susan M ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; CHOLESTEROL; OXYGENASE; SPHINGOLIPID DELTA DESATURASE; UNCLASSIFIED DRUG; ACYL COENZYME A DESATURASE;

ADULT; ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL DAMAGE; CHROMATOGRAPHY; CONTROLLED STUDY; DRINKING BEHAVIOR; FOOD PREFERENCE; GENE EXPRESSION REGULATION; HEART PROTECTION; LIPID ANALYSIS; LIPID COMPOSITION; LIPOGENESIS; LONG TERM EXPOSURE; MALE; NEUROPROTECTION; NONHUMAN; RAT; REAL TIME POLYMERASE CHAIN REACTION; ALCOHOLISM; ANIMAL; BRAIN; CARDIAC MUSCLE; GENETIC SELECTION; GENETICS; INBREEDING; LIPID METABOLISM; LIVER; METABOLISM; WISTAR RAT;

ALCOHOLISM; ANIMALS; BRAIN; CERAMIDES; FATTY ACID DESATURASES; INBREEDING; LIPID METABOLISM; LIVER; MYOCARDIUM; RATS; RATS, WISTAR; SELECTION, GENETIC;

EID: 84947275515     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0139012     Document Type: Article

References (70)

1. Cargiulo T. Understanding the health impact of alcohol dependence. Am J Health Syst Pharm. 2007; 64: S5-11.
2. Room R, Babor T, Rehm J. Alcohol and public health. Lancet. 2005; 365: 519-530. PMID: 15705462
3. Collins MA, Neafsey EJ, Mukamal KJ, Gray MO, Parks DA, Das DK, et al. Alcohol in moderation, cardioprotection, and neuroprotection: epidemiological considerations and mechanistic studies. Alcohol Clin Exp Res. 2009; 33: 206-219. doi: 10.1111/j.1530-0277.2008.00828.x PMID: 19032583
4. Standridge JB, Zylstra RG, Adams SM. Alcohol consumption: an overview of benefits and risks. South Med J. 2004; 97: 664-672. PMID: 15301124
5. Barnes DE, Walker DW. Prenatal ethanol exposure permanently reduces the number of pyramidal neurons in rat hippocampus. Brain Res. 1981; 227: 333-340. PMID: 7260643
6. Bonthius DJ, West JR. Alcohol-induced neuronal loss in developing rats: increased brain damage with binge exposure. Alcohol Clin Exp Res. 1990; 14: 107-118. PMID: 1689970
7. Chen WA, Maier SE, West JR. Toxic effects of ethanol on the fetal brain. In: Deitrich RA, Erwin VG, editors. Pharmacological effects of ethanol on the nervous system. Boca Raton: CRC Press; 1996. pp. 343-361.
8. Harper C. The neuropathology of alcohol-specific brain damage, or does alcohol damage the brain? J Neuropathol Exp Neurol. 1998; 57: 101-110. PMID: 9600202
9. Harper C, Dixon G, Sheedy D, Garrick T. Neuropathological alterations in alcoholic brains. Studies arising from the New South Wales Tissue Resource Centre. Prog Neuropsychopharmacol Biol Psychiatry. 2003; 27: 951-961. PMID: 14499312
10. Ikonomidou C, Bittigau P, Ishimaru MJ, Wozniak DF, Koch C, Genz K, et al. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science. 2000; 287: 1056-1060. PMID: 10669420
11. de la Monte SM. Disproportionate atrophy of cerebral white matter in chronic alcoholics. Arch Neurol. 1988; 45: 990-992. PMID: 3415529
12. Hannun YA. The sphingomyelin cycle and the second messenger function of ceramide. J Biol Chem. 1994; 269: 3125-3128. PMID: 8106344
13. Hannun YA, Bell RM. Functions of sphingolipids and sphingolipid breakdown products in cellular regulation. Science. 1989; 243: 500-507. PMID: 2643164
14. Goswami R, Dawson G. Does ceramide play a role in neural cell apoptosis? J Neurosci Res. 2000; 60: 141-149. PMID: 10740218
15. Jana A, Hogan EL, Pahan K. Ceramide and neurodegeneration: susceptibility of neurons and oligodendrocytes to cell damage and death. J Neurol Sci. 2009; 278: 5-15. doi: 10.1016/j.jns.2008.12.010 PMID: 19147160
16. Pettus BJ, Chalfant CE, Hannun YA. Ceramide in apoptosis: an overview and current perspectives. Biochim Biophys Acta. 2002; 1585: 114-125. PMID: 12531544
17. Spiegel S, Olivera A, Carlson RO. The role of sphingosine in cell growth regulation and transmembrane signaling. Adv Lipid Res. 1993; 25: 105-129. PMID: 8368147
18. Fyrst H, Saba JD. An update on sphingosine-1-phosphate and other sphingolipid mediators. Nat Chem Biol. 2010; 6: 489-497. doi: 10.1038/nchembio.392 PMID: 20559316
19. Chakraborty G, Saito M, Shah R, Mao RF, Vadasz C, Saito M. Ethanol triggers sphingosine 1-phosphate elevation along with neuroapoptosis in the developing mouse brain. J Neurochem. 2012; 121: 806-817. doi: 10.1111/j.1471-4159.2012.07723.x PMID: 22393932
20. de la Monte SM, Longato L, Tong M, DeNucci S, Wands JR. The liver-brain axis of alcohol-mediated neurodegeneration: role of toxic lipids. Int J Environ Res Public Health. 2009; 6: 2055-2075. doi: 10.3390/ijerph6072055 PMID: 19742171
21. Saito M, Chakraborty G, Hegde M, Ohsie J, Paik SM, Vadasz C, et al. Involvement of ceramide in ethanol-induced apoptotic neurodegeneration in the neonatal mouse brain. J Neurochem. 2010; 115: 168-177. doi: 10.1111/j.1471-4159.2010.06913.x PMID: 20663015
22. Dasgupta S, Adams JA, Hogan EL. Maternal alcohol consumption increases sphingosine levels in the brains of progeny mice. Neurochem Res. 2007; 32: 2217-2224. PMID: 17701351
23. Saito M, Saito M, Cooper TB, Vadasz C. Ethanol-induced changes in the content of triglycerides, ceramides, and glucosylceramides in cultured neurons. Alcohol Clin Exp Res. 2005; 29: 1374-1383. PMID: 16131844
24. Cohen AC, Tong M, Wands JR, de la Monte SM. Insulin and insulin-like growth factor resistance with neurodegeneration in an adult chronic ethanol exposure model. Alcohol Clin Exp Res. 2007; 31: 1558-1573. PMID: 17645580
25. de la Monte SM, Yeon JE, Tong M, Longato L, Chaudhry R, Pang MY, et al. Insulin resistance in experimental alcohol-induced liver disease. J Gastroenterol Hepatol. 2008; 23: e477-486. doi: 10.1111/j. 1440-1746.2008.05339.x PMID: 18505416
26. Pang M, de la Monte SM, Longato L, Tong M, He J, Chaudhry R, et al. PPARdelta agonist attenuates alcohol-induced hepatic insulin resistance and improves liver injury and repair. J Hepatol. 2009; 50: 1192-1201. doi: 10.1016/j.jhep.2009.01.021 PMID: 19398227
27. Simms JA, Steensland P, Medina B, Abernathy KE, Chandler LJ, Wise R, et al. Intermittent access to 20% ethanol induces high ethanol consumption in Long-Evans and Wistar rats. Alcohol Clin Exp Res. 2008; 32: 1816-1823. doi: 10.1111/j.1530-0277.2008.00753.x PMID: 18671810
28. Carnicella S, Ron D, Barak S. Intermittent ethanol access schedule in rats as a preclinical model of alcohol abuse. Alcohol. 2014; 48: 243-252. doi: 10.1016/j.alcohol.2014.01.006 PMID: 24721195
29. Wise RA. Voluntary ethanol intake in rats following exposure to ethanol on various schedules. Psychopharmacologia. 1973; 29: 203-210. PMID: 4702273
30. Lumeng L, Hawkins TD, Li TK. New strains of rats with alcohol preference and non-preference. In: Thurman RG, Williamson JR, Drott H, Chance B, editors. Alcohol and aldehyde metabolizing systems, vol III. New York: Academic Press; 1977. pp. 537-544.
31. Herr DR, Fyrst H, Creason MB, Phan VH, Saba JD, Harris GL. Characterization of the Drosophila sphingosine kinases and requirement for Sk2 in normal reproductive function. J Biol Chem. 2004; 279: 12685-12694. PMID: 14722126
32. Chiva-Blanch G, Arranz S, Lamuela-Raventos RM, Estruch R. Effects of wine, alcohol and polyphenols on cardiovascular disease risk factors: evidences from human studies. Alcohol Alcohol. 2013; 48: 270-277. doi: 10.1093/alcalc/agt007 PMID: 23408240
33. Gunzerath L, Faden V, Zakhari S, Warren K. National Institute on Alcohol Abuse and Alcoholism report on moderate drinking. Alcohol Clin Exp Res. 2004; 28: 829-847. PMID: 15201626
34. Krenz M, Korthuis RJ. Moderate ethanol ingestion and cardiovascular protection: from epidemiologic associations to cellular mechanisms. J Mol Cell Cardiol. 2012; 52: 93-104. doi: 10.1016/j.yjmcc.2011. 10.011 PMID: 22041278
35. Miyamae M, Kaneda K, Domae N, Figueredo VM. Cardioprotection by regular ethanol consumption: potential mechanisms and clinical application. Curr Drug Abuse Rev. 2010; 3: 39-48. PMID: 20230376
36. O'Keefe JH, Bhatti SK, Bajwa A, DiNicolantonio JJ, Lavie CJ. Alcohol and cardiovascular health: the dose makes the poison⋯ or the remedy. Mayo Clin Proc. 2014; 89: 382-393. doi: 10.1016/j.mayocp. 2013.11.005 PMID: 24582196
37. Poli A, Marangoni F, Avogaro A, Barba G, Bellentani S, Bucci M, et al. Moderate alcohol use and health: a consensus document. Nutr Metab Cardiovasc Dis. 2013; 23: 487-504. doi: 10.1016/j.numecd.2013. 02.007 PMID: 23642930
38. Thompson PL. J-curve revisited: cardiovascular benefits of moderate alcohol use cannot be dismissed. Med J Aust. 2013; 198: 419-422. PMID: 23641990
39. Brasser SM, McCaul ME, Houtsmuller EJ. Alcohol effects during acamprosate treatment: a doseresponse study in humans. Alcohol Clin Exp Res. 2004; 28: 1074-1083. PMID: 15252294
40. Walls SM Jr, Attle SJ, Brulte GB, Walls ML, Finley KD, Chatfield DA, et al. Identification of sphingolipid metabolites that induce obesity via misregulation of appetite, caloric intake and fat storage in Drosophila. PLoS Genet. 2013; 9: e1003970. doi: 10.1371/journal.pgen.1003970 PMID: 24339790
41. Chen CH, Gray MO, Mochly-Rosen D. Cardioprotection from ischemia by a brief exposure to physiological levels of ethanol: role of epsilon protein kinase C. Proc Natl Acad Sci U S A. 1999; 96: 12784-12789. PMID: 10536000
42. Wang Q, Sun AY, Simonyi A, Kalogeris TJ, Miller DK, Sun GY, et al. Ethanol preconditioning protects against ischemia/reperfusion-induced brain damage: role of NADPH oxidase-derived ROS. Free Radic Biol Med. 2007; 43: 1048-1060. PMID: 17761301
43. Zhou HZ, Karliner JS, Gray MO. Moderate alcohol consumption induces sustained cardiac protection by activating PKC-epsilon and Akt. Am J Physiol Heart Circ Physiol. 2002; 283: H165-174. PMID: 12063287
44. Collins MA, Neafsey EJ, Wang K, Achille NJ, Mitchell RM, Sivaswamy S. Moderate ethanol preconditioning of rat brain cultures engenders neuroprotection against dementia-inducing neuroinflammatory proteins: possible signaling mechanisms. Mol Neurobiol. 2010; 41: 420-425. doi: 10.1007/s12035-010-8138-0 PMID: 20422315
45. Mitchell RM, Neafsey EJ, Collins MA. Essential involvement of the NMDA receptor in ethanol preconditioning-dependent neuroprotection from amyloid-betain vitro. J Neurochem. 2009; 111: 580-588. doi: 10.1111/j.1471-4159.2009.06351.x PMID: 19694907
46. Singh AK, Jiang Y, Gupta S, Benlhabib E. Effects of chronic ethanol drinking on the blood brain barrier and ensuing neuronal toxicity in alcohol-preferring rats subjected to intraperitoneal LPS injection. Alcohol Alcohol. 2007; 42: 385-399. PMID: 17341516
47. Sivaswamy S, Neafsey EJ, Collins MA. Neuroprotective preconditioning of rat brain cultures with ethanol: potential transduction by PKC isoforms and focal adhesion kinase upstream of increases in effector heat shock proteins. Eur J Neurosci. 2010; 32: 1800-1812. doi: 10.1111/j.1460-9568.2010.07451.x PMID: 21050276
48. Davies MJ, Baer DJ, Judd JT, Brown ED, Campbell WS, Taylor PR. Effects of moderate alcohol intake on fasting insulin and glucose concentrations and insulin sensitivity in postmenopausal women: a randomized controlled trial. JAMA. 2002; 287: 2559-2562. PMID: 12020337
49. Lucas DL, Brown RA, Wassef M, Giles TD. Alcohol and the cardiovascular system: research challenges and opportunities. J Am Coll Cardiol. 2005; 45: 1916-1924. PMID: 15963387
50. Ping P, Zhang J, PierceWMJr., Bolli R. Functional proteomic analysis of protein kinase C epsilon signaling complexes in the normal heart and during cardioprotection. Circ Res. 2001; 88: 59-62. PMID: 11139474
51. Abou-Agag LH, Khoo NK, Binsack R, White CR, Darley-Usmar V, Grenett HE, et al. Evidence of cardiovascular protection by moderate alcohol: role of nitric oxide. Free Radic Biol Med. 2005; 39: 540-548. PMID: 16043025
52. Getz GS. The two Cs: ceramide and cardiomyopathy. J Lipid Res. 2008; 49: 2077-2078. doi: 10.1194/jlr.E800015-JLR200 PMID: 18650556
53. Park TS, Hu Y, Noh HL, Drosatos K, Okajima K, Buchanan J, et al. Ceramide is a cardiotoxin in lipotoxic cardiomyopathy. J Lipid Res. 2008; 49: 2101-2112. doi: 10.1194/jlr.M800147-JLR200 PMID: 18515784
54. Beresewicz A, Dobrzyn A, Gorski J. Accumulation of specific ceramides in ischemic/reperfused rat heart; effect of ischemic preconditioning. J Physiol Pharmacol. 2002; 53: 371-382. PMID: 12369735
55. de Mello VD, Lankinen M, Schwab U, Kolehmainen M, Lehto S, Seppänen-Laakso T, et al. Link between plasma ceramides, inflammation and insulin resistance: association with serum IL-6 concentration in patients with coronary heart disease. Diabetologia. 2009; 52: 2612-2615. doi: 10.1007/s00125-009-1482-9 PMID: 19669729
56. Ichi I, Nakahara K, Miyashita Y, Hidaka A, Kutsukake S, Inoue K, et al. Association of ceramides in human plasma with risk factors of atherosclerosis. Lipids. 2006; 41: 859-863. PMID: 17152923
57. Holland WL, Brozinick JT, Wang LP, Hawkins ED, Sargent KM, Liu Y, et al. Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab. 2007; 5: 167-179. PMID: 17339025
58. Ussher JR, Koves TR, Cadete VJ, Zhang L, Jaswal JS, Swyrd SJ, et al. Inhibition of de novo ceramide synthesis reverses diet-induced insulin resistance and enhances whole-body oxygen consumption. Diabetes. 2010; 59: 2453-2464. doi: 10.2337/db09-1293 PMID: 20522596
59. Ussher JR, Folmes CD, Keung W, Fillmore N, Jaswal JS, Cadete VJ, et al. Inhibition of serine palmitoyl transferase I reduces cardiac ceramide levels and increases glycolysis rates following diet-induced insulin resistance. PLoS One. 2012; 7: e37703. doi: 10.1371/journal.pone.0037703 PMID: 22629445
60. Chen Y, Davis-Gorman G, Watson RR, McDonagh PF. Chronic ethanol consumption modulates myocardial ischaemia-reperfusion injury in murine AIDS. Alcohol Alcohol. 2003; 38: 18-24. PMID: 12554602
61. Kamada K, Dayton CB, Yamaguchi T, Korthuis RJ. Antecedent ethanol ingestion prevents postischemic microvascular dysfunction. Pathophysiology. 2004; 10: 131-137. PMID: 15006419
62. Korthius RJ. Antecedent ethanol ingestion prevents postischemic microvascular dysfunction. In: Shepro D, editor. Microvascular research: biology and pathology. Boston: Elsevier Academic Press; 2006. pp. 777-782.
63. Yamaguchi T, Dayton C, Shigematsu T, Carter P, Yoshikawa T, Gute DC, et al. Preconditioning with ethanol prevents postischemic leukocyte-endothelial cell adhesive interactions. Am J Physiol Heart Circ Physiol. 2002; 283: H1019-1030. PMID: 12181132
64. Yamaguchi T, Kamada K, Dayton C, Gaskin FS, Yusof M, Yoshikawa T, et al. Role of eNOS-derived NO in the postischemic anti-inflammatory effects of antecedent ethanol ingestion in murine small intestine. Am J Physiol Heart Circ Physiol. 2007; 292: H1435-1442. PMID: 17098834
65. Roux A, Muller L, Jackson SN, Baldwin K, Womack V, Pagiazitis JG, et al. Chronic ethanol consumption profoundly alters regional brain ceramide and sphingomyelin content in rodents. ACS Chem Neurosci. 2015; 6: 247-259. doi: 10.1021/cn500174c PMID: 25387107
66. Thiele TE, Navarro M. "Drinking in the dark" (DID) procedures: a model of binge-like ethanol drinking in non-dependent mice. Alcohol. 2014; 48: 235-241. doi: 10.1016/j.alcohol.2013.08.005 PMID: 24275142
67. Sprow GM, Thiele TE. The neurobiology of binge-like ethanol drinking: evidence from rodent models. Physiol Behav. 2012; 106: 325-331. doi: 10.1016/j.physbeh.2011.12.026 PMID: 22245775
68. Rhodes JS, Best K, Belknap JK, Finn DA, Crabbe JC. Evaluation of a simple model of ethanol drinking to intoxication in C57BL/6J mice. Physiol Behav. 2005; 84: 53-63. PMID: 15642607
69. Rhodes JS, Ford MM, Yu CH, Brown LL, Finn DA, Garland T Jr, et al. Mouse inbred strain differences in ethanol drinking to intoxication. Genes Brain Behav. 2007; 6: 1-18. PMID: 17233637
70. Bae M, Bandaru VV, Patel N, Haughey NJ. Ceramide metabolism analysis in a model of binge drinking reveals both neuroprotective and toxic effects of ethanol. J Neurochem. 2014; 131: 645-654. doi: 10.1111/jnc.12834 PMID: 25060779