The Journal of Nutritional Biochemistry
Volume 21, Issue 4 , Pages 338-344 , April 2010

Docosahexaenoic acid down-regulates phenobarbital-induced cytochrome P450 2B1 gene expression in rat primary hepatocytes via the sphingomyelinase/ceramide pathway

  • Chia-Yang Lu

      Affiliations

    • Department of Nutrition, Chung Shan Medical University, Taichung 40201, Taiwan
    • ,
  • Chien-Chun Li

      Affiliations

    • Department of Nutrition and Health Sciences, Chang Jung Christian University, Tainan 71101, Taiwan
    • ,
  • Kai-Li Liu

      Affiliations

    • Department of Nutrition, Chung Shan Medical University, Taichung 40201, Taiwan
    • ,
  • Chia-Wen Tsai

      Affiliations

    • Department of Nutrition, China Medical University, Taichung 40402, Taiwan
    • ,
  • Chong-Kuei Lii

      Affiliations

    • Department of Nutrition, China Medical University, Taichung 40402, Taiwan
    • Corresponding Author InformationCorresponding authors. Tel.: +886 4 22053366x7520; fax: +886 4 2206 2891.
    • ,
  • Haw-Wen Chen

      Affiliations

    • Department of Nutrition, China Medical University, Taichung 40402, Taiwan
    • Corresponding Author InformationCorresponding authors. Tel.: +886 4 22053366x7520; fax: +886 4 2206 2891.

Received 5 November 2008 ,Revised 8 January 2009 ,Accepted 9 January 2009.

References 

  1. Mathias S, Peña LA, Kolesnick RN. Signal transduction of stress via ceramide. Biochem J. 1998;335:465–480
  2. Merrill AH, Schmelz EM, Dillehay DL, Spiegel S, Shayman JA, Schroeder JJ, et al. Sphingolipids—the enigmatic lipid class: biochemistry, physiology, and pathophysiology. Toxicol Appl Pharmacol. 1997;142:208–225
  3. Kolesnick RN, Krönke M. Regulation of ceramide production and apoptosis. Annu Rev Physiol. 1998;60:643–665
  4. Sala G, Minutolo F, Macchia M, Sacchi N, Ghidoni R. Resveratrol structure and ceramide-associated growth inhibition in prostate cancer cells. Drugs Exp Clin Res. 2003;29:263–269
  5. Struckhoff AP, Bittman R, Burow ME, Clejan S, Elliott S, Hammond T, et al. Novel ceramide analogs as potential chemotherapeutic agents in breast cancer. J Pharmacol Exp Ther. 2004;309:523–532
  6. Fillet M, Bentires-Alj M, Deregowski V, Greimers R, Gielen J, Piette J, et al. Mechanisms involved in exogenous C2- and C6-ceramide-induced cancer cell toxicity. Biochem Pharmacol. 2003;65:1633–1642
  7. Zhu XF, Liu ZC, Xie BF, Feng GK, Zeng YX. Ceramide induces cell cycle arrest and upregulates p27kip in nasopharyngeal carcinoma cells. Cancer Lett. 2003;193:149–154
  8. Dillehay DL, Webb SK, Schmelz EM, Merrill AH. Dietary sphingomyelin inhibits 1,2-dimethylhydrazine-induced colon cancer in CF1 mice. J Nutr. 1994;124:615–620
  9. Hertervig E, Nilsson A, Nyberg L, Duan RD. Alkaline sphingomyelinase activity is decreased in human colorectal carcinoma. Cancer. 1997;79:448–453
  10. Hannun YA, Linardic CM. Sphingolipid breakdown products: anti-proliferative and tumor-suppressor lipids. Biochim Biophys Acta. 1993;1154:223–236
  11. von Schacky C. N-3 PUFA in CVD: influence of cytokine polymorphism. Proc Nutr Soc. 2007;66:166–170
  12. Mori TA, Beilin LJ. Omega-3 fatty acids and inflammation. Curr Atheroscler Rep. 2004;6:461–467
  13. Simopoulos AP. Omega-3 fatty acids in inflammation and autoimmune diseases. J Am Coll Nutr. 2002;21:495–505
  14. Cole GM, Lim GP, Yang F, Teter B, Begum A, Ma Q, et al. Prevention of Alzheimer's disease: omega-3 fatty acid and phenolic anti-oxidant interventions. Neurobiol Aging. 2005;26:133–136
  15. Schley PD, Jijon HB, Robinson LE, Field CJ. Mechanisms of omega-3 fatty acid-induced growth inhibition in MDA-MB-231 human breast cancer cells. Breast Cancer Res Treat. 2005;92:187–195
  16. Zhang W, Long Y, Zhang J, Wang C. Modulatory effects of EPA and DHA on proliferation and apoptosis of pancreatic cancer cells. J Huazhong Univ Sci Technolog Med Sci. 2007;27:547–550
  17. Danbara N, Yuri T, Tsujita-Kyutoku M, Sato M, Senzaki H, Takada H, et al. Conjugated docosahexaenoic acid is a potent inducer of cell cycle arrest and apoptosis and inhibits growth of colo 201 human colon cancer cells. Nutr Cancer. 2004;50:71–79
  18. Siddiqui RA, Jenski LJ, Harvey KA, Wiesehan JD, Stillwell W, Zaloga GP. Cell-cycle arrest in Jurkat leukaemic cells: a possible role for docosahexaenoic acid. Biochem J. 2003;371:621–629
  19. Xu C, Li CY, Kong AN. Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharm Res. 2005;28:249–268
  20. Sidhu JS, Omiecinski CJ. cAMP-Associated inhibition of phenobarbital-inducible cytochrome P450 gene expression in primary rat hepatocyte cultures. J Biol Chem. 1995;270:12762–12773
  21. Li CC, Lii CK, Liu KL, Yang JJ, Chen HW. DHA Down-regulates phenobarbital-induced cytochrome P450 2B1 gene expression in rat primary hepatocytes by attenuating CAR translocation. Toxicol Appl Pharmacol. 2007;225:329–336
  22. Mercadé M, Cascalló M, Carrió J, Calbó A, Gómez-Treviño C, Fillat AM, et al. Treatment based on a combination of the CYP2B1/cyclophosphamide system and p53 delivery enhances tumour regression in human pancreatic cancer. Ann Oncol. 2001;12:379–388
  23. Iida M, Kojima H, Miyazaki H, Manome Y. Enhancement of cyclophosphamide sensitivity in squamous cell carcinoma transfected with cytochrome P-450 2B1. Am J Otolaryngol. 2005;26:22–27
  24. Roy P, Yu LJ, Crespi CL, Waxman DJ. Development of a substrate-activity based approach to identify the major human liver P-450 catalysts of cyclophosphamide and ifosfamide activation based on cDNA-expressed activities and liver microsomal P-450 profiles. Drug Metab Dispos. 1999;27:655–666
  25. Tsai CF, Lii CK, Yang JJ, Liu KL, Lin WL, Chen HW. Prostaglandin E2 is involved in the increase of cytochrome P-450 2B1 expression by alpha-tocopheryl succinate in primary rat hepatocytes in the presence of phenobarbital. Nutr Cancer. 2001;41:188–195
  26. Sando T, Usui T, Tanaka I, Mori K, Sasaki Y, Fukuda Y. Molecular cloning and expression of rat prostaglandin E receptor EP2 subtype. Biochem Biophys Res Commun. 1994;200:1329–1333
  27. Takeuchi K, Abe T, Takahashi N, Abe K. Molecular cloning and intrarenal localization of rat prostaglandin E2 receptor EP3 subtype. Biochem Biophys Res Commun. 1993;194:885–891
  28. Li CC, Shen HL, Lii CK, Liu KL, Yang JJ, Chen HW. Prostaglandin E2 down-regulation of cytochrome P-450 2B1 expression induced by phenobarbital is through EP2 receptor in rat hepatocytes. Biochem Biophys Res Commun. 2005;327:424–430
  29. Reschly EJ, Krasowski MD. Evolution and function of the NR1I nuclear hormone receptor subfamily (VDR, PXR, and CAR) with respect to metabolism of xenobiotics and endogenous compounds. Curr Drug Metab. 2006;7:349–365
  30. Kawamoto T, Sueyoshi T, Zelko I, Moore R, Washburn K, Negishi M. Phenobarbital-responsive nuclear translocation of the receptor CAR in induction of the CYP2B gene. Mol Cell Biol. 1999;19:6318–6322
  31. Kim J, Min G, Kemper B. Chromatin assembly enhances binding to the CYP2B1 phenobarbital-responsive unit (PBRU) of nuclear factor-1, which binds simultaneously with constitutive androstane receptor (CAR)/retinoid X receptor (RXR) and enhances CAR/RXR-mediated activation of the PBRU. J Biol Chem. 2001;276:7559–7567
  32. Seglen PO. Preparation of isolated rat liver cells. Methods Cell Biol. 1976;13:29–83
  33. Moldéus P, Högberg J, Orrenius S. Isolation and use of liver cells. Methods Enzymol. 1978;52:60–71
  34. Yang JJ, Krauss RS. Extracellular ATP induces anchorage-independent expression of cyclin A and rescues the transformed phenotype of a ras-resistant mutant cell line. J Biol Chem. 1997;272:3103–3108
  35. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685
  36. Konno Y, Degawa M. Gene activations of CYP2B1 and CYP3A1 by dihydropyridine calcium channel antagonists in the rat liver: the structure–activity relationship. Biol Pharm Bull. 2004;27:903–905
  37. Beck NB, Omiecinski CJ. Lack of modulation by phenobarbital of cyclic AMP levels or protein kinase A activity in rat primary hepatocytes. Biochem Pharmacol. 1999;58:1109–1114
  38. Lee WK, Torchalski B, Thevenod F. Cadmium-induced ceramide formation triggers calpain-dependent apoptosis in cultured kidney proximal tubule cells. Am J Physiol Cell Physiol. 2007;293:C839–C847
  39. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:265–275
  40. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37:911–917
  41. Suomalainen L, Hakala JK, Pentikainen V, Otala M, Erkkilä K, Pentikäinen MO, et al. Sphingosine-1-phosphate in inhibition of male germ cell apoptosis in the human testis. J Clin Endocrinol Metab. 2003;88:5572–5579
  42. Wu M, Harvey KA, Ruzmetov N, Welch ZR, Sech L, Jackson K, et al. Omega-3 polyunsaturated fatty acids attenuate breast cancer growth through activation of a neutral sphingomyelinase-mediated pathway. Int J Cancer. 2005;117:340–348
  43. Yabu T, Imamura S, Yamashita M, Okazaki T. Identification of Mg2+-dependent neutral sphingomyelinase 1 as a mediator of heat stress-induced ceramide generation and apoptosis. J Biol Chem. 2008;283:29971–29982
  44. Gu X, Song X, Dong Y, Cai H, Sech L, Jackson K, et al. Vitamin E succinate induces ceramide-mediated apoptosis in head and neck squamous cell carcinoma in vitro and in vivo. Clin Cancer Res. 2008;14:1840–1848
  45. Robinson BS, Hii CS, Poulos A, Ferrante A. Activation of neutral sphingomyelinase in human neutrophils by polyunsaturated fatty acids. Immunology. 1997;91:274–280
  46. Sánchez AM, Malagarie-Cazenave S, Olea N, Vara D, Chiloeches A, Díaz-Laviada I. Apoptosis induced by capsaicin in prostate PC-3 cells involves ceramide accumulation, neutral sphingomyelinase, and JNK activation. Apoptosis. 2007;12:2013–2024
  47. Liu B, Obeid LM, Hannun YA. Sphingomyelinases in cell regulation. Semin Cell Dev Biol. 1997;8:311–322
  48. Li CC, Lii CK, Liu KL, Yang JJ, Chen HW. n-6 and n-3 polyunsaturated fatty acids down-regulate cytochrome P-450 2B1 gene expression induced by phenobarbital in primary rat hepatocytes. J Nutr Biochem. 2006;17:707–715
  49. Chen L, Waxman DJ, Chen D, Kufe DW. Sensitization of human breast cancer cells to cyclophosphamide and ifosfamide by transfer of a liver cytochrome P450 gene. Cancer Res. 1996;56:1331–1340
  50. Lu CY, Li CC, Liu KL, Lii CK, Chen HW. Docosahexaenoic acid downregulates phenobarbital-induced cytochrome P450 2B1 gene expression in rat primary hepatocytes via the c-Jun NH2-terminal kinase mitogen-activated protein kinase pathway. Mol Nutr Food Res. 2009;Epub ahead of press
  51. Chen J, Nikolova-Karakashian M, Merrill AH, Morgan ET. Regulation of cytochrome P450 2C11 (CYP2C11) gene expression by interleukin-1, sphingomyelin hydrolysis, and ceramides in rat hepatocytes. J Biol Chem. 1995;270:25233–25238
  52. Chun YJ, Lee S, Yang SA, Park S, Kim MY. Modulation of CYP3A4 expression by ceramide in human colon carcinoma HT-29 cells. Biochem Biophys Res Commun. 2002;298:687–692
  53. Luberto C, Hannun YA. Sphingomyelin synthase, a potential regulator of intracellular levels of ceramide and diacylglycerol during SV40 transformation. Does sphingomyelin synthase account for the putative phosphatidylcholine-specific phospholipase C?. J Biol Chem. 1998;273:14550–14559
  54. Kolmakova A, Kwiterovich P, Virgil D, Alaupovic P, Knight-Gibson C, Martin SF. Apolipoprotein C-I induces apoptosis in human aortic smooth muscle cells via recruiting neutral sphingomyelinase. Arterioscler Thromb Vasc Biol. 2004;24:264–269
  55. Barsacchi R, Perrotta C, Sestili P, Cantoni O, Moncada S, Clementi E. Cyclic GMP-dependent inhibition of acid sphingomyelinase by nitric oxide: an early step in protection against apoptosis. Cell Death Differ. 2002;9:1248–1255
  56. Jaffrézou JP, Maestre N, de Mas-Mansat V, Bezombes C, Levade T, Laurent G. Positive feedback control of neutral sphingomyelinase activity by ceramide. FASEB J. 1998;12:999–1006
  57. De Nadai C, Sestili P, Cantoni O, Lièvremont JP, Sciorati C, Barsacchi R, et al. Nitric oxide inhibits tumor necrosis factor-alpha-induced apoptosis by reducing the generation of ceramide. Proc Natl Acad Sci U S A. 2000;97:5480–5485
  58. Hannun YA. Functions of ceramide in coordinating cellular responses to stress. Science. 1996;274:1855–1859
  59. Sawai H, Hannun YA. Ceramide and sphingomyelinases in the regulation of stress responses. Chem Phys Lipids. 1999;102:141–147
  60. Hannun YA, Luberto C. Ceramide in the eukaryotic stress response. Trends Cell Biol. 2000;10:73–80
  61. Ramos B, Lahti JM, Claro E, Jackowski S. Prevalence of necrosis in C2-ceramide-induced cytotoxicity in NB16 neuroblastoma cells. Mol Pharmacol. 2003;64:502–511
  62. Mu YM, Yanase T, Nishi Y, Tanaka A, Saito M, Jin CH, et al. Saturated FFAs, palmitic acid and stearic acid, induce apoptosis in human granulosa cells. Endocrinology. 2001;142:3590–3597
  63. Cacicedo JM, Benjachareowong S, Chou E, Ruderman NB, Ido Y. Palmitate-induced apoptosis in cultured bovine retinal pericytes: roles of NAD(P)H oxidase, oxidant stress, and ceramide. Diabetes. 2005;54:1838–1845
  64. Jumpsen JA, Brown NE, Thomson AB, Paul Man SF, Goh YK, Ma D, et al. Fatty acids in blood and intestine following docosahexaenoic acid supplementation in adults with cystic fibrosis. J Cystic Fibrosis. 2006;5:77–84
  65. Bösel A, Pfeuffer T. Differential effects of ceramides upon adenylyl cyclase subtypes. FEBS Lett. 1998;422:209–212
  66. Dragusin M, Wehner S, Kelly S, Wang E, Merrill AH, Kalff JC, et al. Effects of sphingosine-1-phosphate and ceramide-1-phosphate on rat intestinal smooth muscle cells: implications for postoperative ileus. FASEB J. 2006;20:1351–1359
  67. Robinson BS, Hii CS, Ferrante A. Activation of phospholipase A2 in human neutrophils by polyunsaturated fatty acids and its role in stimulation of superoxide production. Biochem J. 1998;336:611–617
  68. Brash AR. Arachidonic acid as a bioactive molecule. J Clin Invest. 2001;107:1339–1345

☆ This work was supported by NSC-95-2320-B-040-029-MY2.

PII: S0955-2863(09)00016-3

doi: 10.1016/j.jnutbio.2009.01.007

The Journal of Nutritional Biochemistry
Volume 21, Issue 4 , Pages 338-344 , April 2010

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