Effect of Procysteine on aging-associated changes in hepatic GSH and SMase: Evidence for transcriptional regulation of smpd3

Journal of Lipid Research

Volumn 55, Issue 10, 2014, Pages 2041-2052

  Deevska, Gergana ^a   Sunkara, Manjula ^b   Karakashian, Claudia ^a   Peppers, Benjamin ^a   Morris, Andrew J ^b   Nikolova Karakashian, Mariana N ^a  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

^b LEXINGTON VA MEDICAL CENTER   (United States)

Author keywords

Aging; Ceramide; Diet; Oxidative stress; Reduced glutathione supplementation; Sphingomyelinase

Indexed keywords

2 OXO 4 THIAZOLIDINECARBOXYLIC ACID; CERAMIDE; GLUTATHIONE; GLUTATHIONE DISULFIDE; MESSENGER RNA; SPHINGOMYELIN PHOSPHODIESTERASE; 2-OXOTHIAZOLIDINE-4-CARBOXYLIC ACID; PYROGLUTAMIC ACID; SMPD3 PROTEIN, HUMAN; SMPD3 PROTEIN, MOUSE; THIAZOLIDINE DERIVATIVE;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVITY; FATTY LIVER; GENE; GENE EXPRESSION REGULATION; JUVENILE ANIMAL; LIPID LIVER LEVEL; LIPOGENESIS; LIVER WEIGHT; MALE; MOUSE; NONHUMAN; NUTRITIONAL STATUS; OUTCOME ASSESSMENT; PROTEIN EXPRESSION; SMPD3 GENE; TRANSCRIPTION REGULATION; UPREGULATION; WEIGHT CHANGE; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; HEPG2 CELL LINE; HUMAN; LIVER; METABOLISM;

AGING; ANIMALS; CERAMIDES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTATHIONE; HEP G2 CELLS; HUMANS; LIVER; MALE; MICE; PYRROLIDONECARBOXYLIC ACID; RNA, MESSENGER; SPHINGOMYELIN PHOSPHODIESTERASE; THIAZOLIDINES;

EID: 84907509674     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M048223     Document Type: Article

References (70)

1. Samiec, P. S., C. Drews-Botsch, E. W. Flagg, J. C. Kurtz, P. Sternberg, Jr., R. L. Reed, and D. P. Jones. 1998. Glutathione in human plasma: decline in association with aging, age-related macular degeneration, and diabetes. Free Radic. Biol. Med. 24: 699-704.
2. Erden-̄nal, M., E. Sunal, and G. Kanbak. 2002. Age-related changes in the glutathione redox system. Cell Biochem. Funct. 20: 61-66.
3. Lang, C. A., S. Naryshkin, D. L. Schneider, B. J. Mills, and R. D. Lindeman. 1992. Low blood glutathione levels in healthy aging adults. J. Lab. Clin. Med. 120: 720-725.
4. Zhu, Y., P. M. Carvey, and Z. Ling. 2006. Age-related changes in glutathione and glutathione-related enzymes in rat brain. Brain Res. 1090: 35-44.
5. Sasaki, T., M. Senda, S. N. Kim, S. Kojima, and A. Kubodera. 2001. Age-related changes of glutathione content, glucose transport and metabolism, and mitochondrial electron transfer function in mouse brain. Nucl. Med. Biol. 28: 25-31.
6. Paasche, G., D. Huster, and A. Reichenbach. 1998. The glutathione content of retinal Müller (glial) cells: the effects of aging and of application of free-radical scavengers. Ophthalmic Res. 30: 351-360.
7. Nakata, K., M. Kawase, S. Ogino, C. Kinoshita, H. Murata, T. Sakaue, K. Ogata, and S. Ohmori. 1996. Effects of age on levels of cysteine, glutathione and related enzyme activities in livers of mice and rats and an attempt to replenish hepatic glutathione level of mouse with cysteine derivatives. Mech. Ageing Dev. 90: 195-207.
8. Takahashi, S., and M. Zeydel. 1982. gamma-Glutamyl transpeptidase and glutathione in aging IMR-90 fibroblasts and in differentiating 3T3 L1 preadipocytes. Arch. Biochem. Biophys. 214: 260-267.
9. Chung, H. Y., E. K. Lee, Y. J. Choi, J. M. Kim, D. H. Kim, Y. Zou, C. H. Kim, J. Lee, H. S. Kim, N. D. Kim, et al. 2011. Molecular inflammation as an underlying mechanism of the aging process and agerelated diseases. J. Dent. Res. 90: 830-840.
10. Ballatori, N., S. M. Krance, S. Notenboom, S. Shi, K. Tieu, and C. L. Hammond. 2009. Glutathione dysregulation and the etiology and progression of human diseases. Biol. Chem. 390: 191-214.
11. Kondo, T., M. Hirose, and K. Kageyama. 2009. Roles of oxidative stress and redox regulation in atherosclerosis. J. Atheroscler. Thromb. 16: 532-538.
12. Lu, S. C. 1999. Regulation of hepatic glutathione synthesis: current concepts and controversies. FASEB J. 13: 1169-1183.
13. Cacciatore, I., C. Cornacchia, F. Pinnen, A. Mollica, and A. Di Stefano. 2010. Prodrug approach for increasing cellular glutathione levels. Molecules. 15: 1242-1264.
14. Nishina, H., J. Ohta, and T. Ubuka. 1987. Effect of L-2-oxothiazolidine-4-carboxylate administration on glutathione and cysteine concentrations in guinea pig liver and kidney. Physiol. Chem. Phys. Med. NMR. 19: 9-13.
15. Williamson, J. M., B. Boettcher, and A. Meister. 1982. Intracellular cysteine delivery system that protects against toxicity by promoting glutathione synthesis. Proc. Natl. Acad. Sci. USA. 79: 6246-6249.
16. Iimuro, Y., B. U. Bradford, S. Yamashina, I. Rusyn, M. Nakagami, N. Enomoto, H. Kono, W. Frey, D. Forman, D. Brenner, et al. 2000. The glutathione precursor L-2-oxothiazolidine-4-carboxylic acid protects against liver injury due to chronic enteral ethanol exposure in the rat. Hepatology. 31: 391-398.
17. Gwilt, P. R., L. E. Radick, X. Y. Li, J. J. Whalen, and C. D. Leaf. 1998. Pharmacokinetics of 2-oxothiazolidine-4-carboxylate, a cysteine prodrug, and cysteine. J. Clin. Pharmacol. 38: 945-950.
18. Porta, P., S. Aebi, K. Summer, and B. H. Lauterburg. 1991. L-2-oxothiazolidine-4-carboxylic acid, a cysteine prodrug: pharmacokinetics and effects on thiols in plasma and lymphocytes in human. J. Pharmacol. Exp. Ther. 257: 331-334.
19. Moberly, J. B., J. Logan, P. R. Borum, K. O. Story, L. E. Webb, S. V. Jassal, L. Mupas, H. Rodela, G. A. Alghamdi, J. E. Moran, et al. 1998. Elevation of whole-blood glutathione in peritoneal dialysis patients by L-2-oxothiazolidine-4-carboxylate, a cysteine prodrug (Procysteine). J. Am. Soc. Nephrol. 9: 1093-1099.
20. Kalayjian, R. C., G. Skowron, R. T. Emgushov, M. Chance, S. A. Spell, P. R. Borum, L. S. Webb, K. H. Mayer, J. B. Jackson, and B. Yen-Lieberman. 1994. A phase I/II trial of intravenous L-2-oxothiazolidine-4-carboxylic acid (procysteine) in asymptomatic HIV-infected subjects. J. Acquir. Immune Defic. Syndr. 7: 369-374.
21. Barditch-Crovo, P., D. Noe, G. Skowron, M. Lederman, R. Kalayjian, P. Borum, R. Buier, W. Rowe, D. Goldberg, and P. Lietman. 1998. A phase I/II evaluation of oral L-2-oxothiazolidine-4-carboxylic acid in asymptomatic patients infected with human immunodeficiency virus. J. Clin. Pharmacol. 38: 357-363.
22. Choi, J., K. H. Park, S. Z. Kim, J. H. Shin, and S. I. Jang. 2013. The ameliorative effects of L-2-oxothiazolidine-4-carboxylate on acetaminophen-induced hepatotoxicity in mice. Molecules. 18: 3467-3478.
23. Kim, I. H., D. G. Kim, P. Hao, Y. Wang, S. H. Kim, S. W. Kim, S. O. Lee, and S. T. Lee. 2012. Anti-fibrotic effects of L-2-oxothiazolidine-4-carboxylic acid via modulation of nuclear factor erythroid 2-related factor 2 in rats. BMB Rep. 45: 348-353.
24. Adamy, C., P. Mulder, L. Khouzami, N. Andrieu-abadie, N. Defer, G. Candiani, C. Pavoine, P. Caramelle, R. Souktani, P. Le Corvoisier, et al. 2007. Neutral sphingomyelinase inhibition participates to the benefits of N-acetylcysteine treatment in post-myocardial infarction failing heart rats. J. Mol. Cell. Cardiol. 43: 344-353.
25. Levy, M., S. S. Castillo, and T. Goldkorn. 2006. nSMase2 activation and trafficking are modulated by oxidative stress to induce apoptosis. Biochem. Biophys. Res. Commun. 344: 900-905.
26. Liu, B., N. Andrieu-Abadie, T. Levade, P. Zhang, L. M. Obeid, and Y. A. Hannun. 1998. Glutathione regulation of neutral sphingomyelinase in tumor necrosis factor-alpha-induced cell death. J. Biol. Chem. 273: 11313-11320.
27. Liu, B., and Y. A. Hannun. 1997. Inhibition of the neutral magnesium-dependent sphingomyelinase by glutathione. J. Biol. Chem. 272: 16281-16287.
28. Rutkute, K., R. H. Asmis, and M. N. Nikolova-Karakashian. 2007. Regulation of neutral sphingomyelinase-2 by GSH: a new insight to the role of oxidative stress in aging-associated inflammation. J. Lipid Res. 48: 2443-2452.
29. Chatterjee, S. 1994. Neutral sphingomyelinase action stimulates signal transduction of tumor necrosis factor-alpha in the synthesis of cholesteryl esters in human fibroblasts. J. Biol. Chem. 269: 879-882.
30. Nikolova-Karakashian, M., E. T. Morgan, C. Alexander, D. C. Liotta, and A. H. Merrill, Jr. 1997. Bimodal regulation of ceramidase by interleukin-1beta. Implications for the regulation of cytochrome p450 2C11. J. Biol. Chem. 272: 18718-18724.
31. Verheij, M., R. Bose, X. H. Lin, B. Yao, W. D. Jarvis, S. Grant, M. J. Birrer, E. Szabo, L. I. Zon, J. M. Kyriakis, et al. 1996. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature. 380: 75-79.
32. Yan, F., and D. B. Polk. 2001. Kinase suppressor of ras is necessary for tumor necrosis factor alpha activation of extracellular signal-regulated kinase/mitogen-activated protein kinase in intestinal epithelial cells. Cancer Res. 61: 963-969.
33. Chalfant, C. E., K. Kishikawa, M. C. Mumby, C. Kamibayashi, A. Bielawska, and Y. A. Hannun. 1999. Long chain ceramides activate protein phosphatase-1 and protein phosphatase-2A. Activation is stereospecific and regulated by phosphatidic acid. J. Biol. Chem. 274: 20313-20317.
34. Dobrowsky, R. T., and Y. A. Hannun. 1992. Ceramide stimulates a cytosolic protein phosphatase. J. Biol. Chem. 267: 5048-5051.
35. Scheid, M. P., I. N. Foltz, P. R. Young, J. W. Schrader, and V. Duronio. 1999. Ceramide and cyclic adenosine monophosphate (cAMP) induce cAMP response element binding protein phosphorylation via distinct signaling pathways while having opposite effects on myeloid cell survival. Blood. 93: 217-225.
36. Ruvolo, P. P., F. Gao, W. L. Blalock, X. Deng, and W. S. May. 2001. Ceramide regulates protein synthesis by a novel mechanism involving the cellular PKR activator RAX. J. Biol. Chem. 276: 11754-11758.
37. Palomero, J., A. I. Galan, M. E. Munoz, M. J. Tunon, J. Gonzalez-Gallego, and R. Jimenez. 2001. Effects of aging on the susceptibility to the toxic effects of cyclosporin A in rats. Changes in liver glutathione and antioxidant enzymes. Free Radic. Biol. Med. 30: 836-845.
38. Jung, K., and W. Henke. 1996. Developmental changes of antioxidant enzymes in kidney and liver from rats. Free Radic. Biol. Med. 20: 613-617.
39. Farooqui, M. Y., W. W. Day, and D. M. Zamorano. 1987. Glutathione and lipid peroxidation in the aging rat. Comp. Biochem. Physiol. B. 88: 177-180.
40. Hagen, T. M., V. Vinarsky, C. M. Wehr, and B. N. Ames. 2000. (R)-alpha-lipoic acid reverses the age-associated increase in susceptibility of hepatocytes to tert-butylhydroperoxide both in vitro and in vivo. Antioxid. Redox Signal. 2: 473-483.
41. Véricel, E., M. Narce, L. Ulmann, J. P. Poisson, and M. Lagarde. 1994. Age-related changes in antioxidant defence mechanisms and peroxidation in isolated hepatocytes from spontaneously hypertensive and normotensive rats. Mol. Cell. Biochem. 132: 25-29.
42. Stio, M., T. Iantomasi, F. Favilli, P. Marraccini, B. Lunghi, M. T. Vincenzini, and C. Treves. 1994. Glutathione metabolism in heart and liver of the aging rat. Biochem. Cell Biol. 72: 58-61.
43. Rebrin, I., S. Kamzalov, and R. S. Sohal. 2003. Effects of age and caloric restriction on glutathione redox state in mice. Free Radic. Biol. Med. 35: 626-635.
44. Rikans, L. E., and S. D. Kosanke. 1984. Effect of aging on liver glutathione levels and hepatocellular injury from carbon tetrachloride, allyl alcohol or galactosamine. Drug Chem. Toxicol. 7: 595-604.
45. Marchesini, N., W. Osta, J. Bielawski, C. Luberto, L. M. Obeid, and Y. A. Hannun. 2004. Role for mammalian neutral sphingomyelinase 2 in confluence-induced growth arrest of MCF7 cells. J. Biol. Chem. 279: 25101-25111.
46. Deevska, G. M., K. A. Rozenova, N. V. Giltiay, M. A. Chambers, J. White, B. B. Boyanovsky, J. Wei, A. Daugherty, E. J. Smart, M. B. Reid, et al. 2009. Acid sphingomyelinase deficiency prevents dietinduced hepatic triacylglycerol accumulation and hyperglycemia in mice. J. Biol. Chem. 284: 8359-8368.
47. Deaciuc, I. V., M. Nikolova-Karakashian, F. Fortunato, E. Y. Lee, D. B. Hill, and C. J. McClain. 2000. Apoptosis and dysregulated ceramide metabolism in a murine model of alcohol-enhanced lipopolysaccharide hepatotoxicity. Alcohol. Clin. Exp. Res. 24: 1557-1565.
48. Pagadala, M., T. Kasumov, A. J. McCullough, N. N. Zein, and J. P. Kirwan. 2012. Role of ceramides in nonalcoholic fatty liver disease. Trends Endocrinol. Metab. 23: 365-371.
49. Wang, H., H. Liu, and R. M. Liu. 2003. Gender difference in glutathione metabolism during aging in mice. Exp. Gerontol. 38: 507-517.
50. Hannun, Y. A., and L. M. Obeid. 2011. Many ceramides. J. Biol. Chem. 286: 27855-27862.
51. Molano, A., Z. Huang, M. G. Marko, A. Azzi, D. Wu, E. Wang, S. L. Kelly, A. H. Merrill, Jr., S. C. Bunnell, and S. N. Meydani. 2012. Age-dependent changes in the sphingolipid composition of mouse CD4+ T cell membranes and immune synapses implicate glucosylceramides in age-related T cell dysfunction. PLoS ONE. 7: e47650.
52. Monette, J. S., L. A. Gomez, R. F. Moreau, K. C. Dunn, J. A. Butler, L. A. Finlay, A. J. Michels, K. P. Shay, E. J. Smith, and T. M. Hagen. 2011. (R)-alpha-lipoic acid treatment restores ceramide balance in aging rat cardiac mitochondria. Pharmacol. Res. 63: 23-29.
53. Rivas, D. A., E. P. Morris, P. H. Haran, E. P. Pasha, S. Morais Mda, G. G. Dolnikowski, E. M. Phillips, and R. A. Fielding. 2012. Increased ceramide content and NFκB signaling may contribute to the attenuation of anabolic signaling after resistance exercise in aged males. J. Appl. Physiol. (1985). 113: 1727-1736.
54. Rutkute, K., A. A. Karakashian, N. V. Giltiay, A. Dobierzewska, and M. N. Nikolova-Karakashian. 2007. Aging in rat causes hepatic hyperresposiveness to interleukin-1beta which is mediated by neutral sphingomyelinase-2. Hepatology. 46: 1166-1176.
55. Nikolova-Karakashian, M., A. Karakashian, and K. Rutkute. 2008. Role of neutral sphingomyelinases in aging and inflammation. Subcell. Biochem. 49: 469-486.
56. Clarke, C. J., J. M. Guthrie, and Y. A. Hannun. 2008. Regulation of neutral sphingomyelinase-2 (nSMase2) by tumor necrosis factor-α involves protein kinase C-δ in lung epithelial cells. Mol. Pharmacol. 74: 1022-1032.
57. Filosto, S., M. Ashfaq, S. Chung, W. Fry, and T. Goldkorn. 2012. Neutral sphingomyelinase 2 activity and protein stability are modulated by phosphorylation of five conserved serines. J. Biol. Chem. 287: 514-522.
58. Ito, H., K. Tanaka, K. Hagiwara, M. Kobayashi, A. Hoshikawa, N. Mizutani, A. Takagi, T. Kojima, S. Sobue, M. Ichihara, et al. 2012. Transcriptional regulation of neutral sphingomyelinase 2 in alltrans retinoic acid-treated human breast cancer cell line, MCF-7. J. Biochem. 151: 599-610.
59. Meyers-Needham, M., J. A. Lewis, S. Gencer, R. D. Sentelle, S. A. Saddoughi, C. J. Clarke, Y. A. Hannun, H. Norell, T. M. da Palma, M. Nishimura, et al. 2012. Off-target function of the sonic hedgehog inhibitor cyclopamine in mediating apoptosis via nitric oxide-dependent neutral sphingomyelinase 2/ceramide induction. Mol. Cancer Ther. 11: 1092-1102.
60. Banks, M. F., and M. H. Stipanuk. 1994. The utilization of N-acetylcysteine and 2-oxothiazolidine-4-carboxylate by rat hepatocytes is limited by their rate of uptake and conversion to cysteine. J. Nutr. 124: 378-387.
61. Yamada, S., T. Abe, J. Ohta, N. Masuoka, and T. Ubuka. 1995. Increase in tissue cysteine level and excretion of sulfate and taurine after intragastric administration ofL-2-oxothiazolidine-4-carboxylate in rats. Amino Acids. 8: 37-45.
62. Hoang, M. H., Y. Jia, H. J. Jun, J. H. Lee, K. Y. Hwang, D. W. Choi, S. J. Um, B. Y. Lee, S. G. You, and S. J. Lee. 2012. Taurine is a liver X receptor-alpha ligand and activates transcription of key genes in the reverse cholesterol transport without inducing hepatic lipogenesis. Mol. Nutr. Food Res. 56: 900-911.
63. Jain, A., D. C. Madsen, P. A. M. Auld, W. W. Frayer, M. K. Schwartz, A. Meister, and J. Ma˚rtensson. 1995. L-2-oxothiazolidine-4-carboxylate, a cysteine precursor, stimulates growth and normalizes tissue glutathione concentrations in rats fed a sulfur amino acid-deficient diet. J. Nutr. 125: 851-856.
64. Bernard, G. R., A. P. Wheeler, M. M. Arons, P. E. Morris, H. L. Paz, J. A. Russell, and P. E. Wright. 1997. A trial of antioxidants N-acetylcysteine and procysteine in ARDS. The Antioxidant in ARDS Study Group. Chest. 112: 164-172.
65. Jurima-Romet, M., and H. S. Huang. 1992. Enalapril hepatotoxicity in the rat. Effects of modulators of cytochrome P450 and glutathione. Biochem. Pharmacol. 44: 1803-1810.
66. Crankshaw, D. L., L. I. Berkeley, J. F. Cohen, F. N. Shirota, and H. T. Nagasawa. 2002. Double-prodrugs of L-cysteine: differential protection against acetaminophen-induced hepatotoxicity in mice. J. Biochem. Mol. Toxicol. 16: 235-244.
67. Gerard-Monnier, D., S. Fougeat, J. F. Gourvest, and J. Chaudiere. 1993. Partial prevention of glutathione depletion in rats following acute intoxication with diethylmaleate. Clin. Physiol. Biochem. 10: 36-42.
68. Brodeur, J., and R. Goyal. 1987. Effect of a cysteine prodrug, L-2-oxothiazolidine-4-carboxylic acid, on the metabolism and toxicity of bromobenzene: an acute study. Can. J. Physiol. Pharmacol. 65: 816-822.
69. Maher, P. 2005. The effects of stress and aging on glutathione metabolism. Ageing Res. Rev. 4: 288-314.
70. Robciuc, A., T. Hyotylainen, M. Jauhiainen, and J. M. Holopainen. 2012. Hyperosmolarity-induced lipid droplet formation depends on ceramide production by neutral sphingomyelinase 2. J. Lipid Res. 53: 2286-2295.