Fenretinide inhibited de novo ceramide synthesis and proinflammatory cytokines induced by Aggregatibacter actinomycetemcomitans

Journal of Lipid Research

Volumn 54, Issue 1, 2013, Pages 189-201

  Yu, Hong ^a   Valerio, Michael ^a   Bielawski, Jacek ^b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Cytokine; Dihydroceramide; Inflammation; Macrophage; Protein kinase

Indexed keywords

CERAMIDE; CYCLOOXYGENASE 2; CYTOKINE; FENRETINIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; JANUS KINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN E2; PROTEIN KINASE B; PROTEIN KINASE C; STAT PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; LIPOGENESIS; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL LINE; CERAMIDES; CYTOKINES; FENRETINIDE; GENE EXPRESSION REGULATION; MACROPHAGES; MICE; NF-KAPPA B; PASTEURELLACEAE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84871250985     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M031427     Document Type: Article

References (69)

1. van Blitterswijk, W. J., A. H. van der Luit, R. J. Veldman, M. Verheij, and J. Borst. 2003. Ceramide: second messenger or modulator of membrane structure and dynamics? Biochem. J. 369: 199-211. (Pubitemid 36174190)
2. Hannun, Y. A., and L. M. Obeid. 2008. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9: 139-150. (Pubitemid 351158911)
3. Grassme, H., J. Riethmuller, and E. Gulbins. 2007. Biological aspects of ceramide-enriched membrane domains. Prog. Lipid Res. 46: 161-170. (Pubitemid 46962121)
4. Schenck, M., A. Carpinteiro, H. Grassme, F. Lang, and E. Gulbins. 2007. Ceramide: physiological and pathophysiological aspects. Arch. Biochem. Biophys. 462: 171-175. (Pubitemid 46856326)
5. Zanardi, S., D. Serrano, A. Argusti, M. Barile, M. Puntoni, and A. Decensi. 2006. Clinical trials with retinoids for breast cancer chemoprevention. Endocr. Relat. Cancer. 13: 51-68.
6. Villablanca, J. G., M. D. Krailo, M. M. Ames, J. M. Reid, G. H. Reaman, and C. P. Reynolds. 2006. Phase I trial of oral fenretinide in children with high-risk solid tumors: a report from the Children's Oncology Group (CCG 09709). J. Clin. Oncol. 24: 3423-3430. (Pubitemid 46638899)
7. O'Donnell, P. H., W. X. Guo, C. P. Reynolds, and B. J. Maurer. 2002. N-(4-hydroxyphenyl)retinamide increases ceramide and is cytotoxic to acute lymphoblastic leukemia cell lines, but not to non-malignant lymphocytes. Leukemia. 16: 902-910. (Pubitemid 34537564)
8. Puduvalli, V. K., Y. Saito, R. Xu, G. P. Kouraklis, V. A. Levin, and A. P. Kyritsis. 1999. Fenretinide activates caspases and induces apoptosis in gliomas. Clin. Cancer Res. 5: 2230-2235. (Pubitemid 29399282)
9. Lovat, P. E., S. Oliverio, M. Ranalli, M. Corazzari, C. Rodolfo, F. Bernassola, K. Aughton, M. Maccarrone, Q. D. Hewson, A. D. Pearson, et al. 2002. GADD153 and 12-lipoxygenase mediate fenretinide-induced apoptosis of neuroblastoma. Cancer Res. 62: 5158-5167. (Pubitemid 35024586)
10. Kalemkerian, G. P., R. Slusher, S. Ramalingam, S. Gadgeel, and M. Mabry. 1995. Growth inhibition and induction of apoptosis by fenretinide in small-cell lung cancer cell lines. J. Natl. Cancer Inst. 87: 1674-1680.
11. Kabbout, M., A. Hatoum, G. Abou-Lteif, I. Chakroun, F. R. Homaidan, and N. Darwiche. 2004. Stage-specific effect of N-(4- hydroxyphenyl)retinamide on cell growth in squamous cell carcinogenesis. Mol. Carcinog. 40: 12-23. (Pubitemid 38581659)
12. Li, X., W. Ling, A. Pennisi, S. Khan, and S. Yaccoby. 2009. Fenretinide inhibits myeloma cell growth, osteoclastogenesis and osteoclast viability. Cancer Lett. 284: 175-181.
13. Maurer, B. J., L. S. Metelitsa, R. C. Seeger, M. C. Cabot, and C. P. Reynolds. 1999. Increase of ceramide and induction of mixed apoptosis/necrosis by N-(4-hydroxyphenyl)- retinamide in neuroblastoma cell lines. J. Natl. Cancer Inst. 91: 1138-1146. (Pubitemid 29330552)
14. Wang, H., B. J. Maurer, C. P. Reynolds, and M. C. Cabot. 2001. N-(4-hydroxyphenyl)retinamide elevates ceramide in neuroblastoma cell lines by coordinate activation of serine palmitoyltransferase and ceramide synthase. Cancer Res. 61: 5102-5105. (Pubitemid 32681541)
15. Wang, H., A. G. Charles, A. J. Frankel, and M. C. Cabot. 2003. Increasing intracellular ceramide: an approach that enhances the cytotoxic response in prostate cancer cells. Urology. 61: 1047-1052. (Pubitemid 36547768)
16. Kraveka, J. M., L. Li, Z. M. Szulc, J. Bielawski, B. Ogretmen, Y. A. Hannun, L. M. Obeid, and A. Bielawska. 2007. Involvement of dihydroceramide desaturase in cell cycle progression in human neuroblastoma cells. J. Biol. Chem. 282: 16718-16728. (Pubitemid 47093220)
17. Bikman, B. T., Y. Guan, G. Shui, M. M. Siddique, W. L. Holland, J. Y. Kim, G. Fabrias, M. R. Wenk, and S. A. Summers. 2012. Fenretinide prevents lipid-induced insulin resistance by blocking ceramide biosynthesis. J. Biol. Chem. 287:17426-17437.
18. Vilela, R. M., L. C. Lands, B. Meehan, and S. Kubow. 2006. Inhibition of IL-8 release from CFTR-deficient lung epithelial cells following pre-treatment with fenretinide. Int. Immunopharmacol. 6: 1651-1664. (Pubitemid 44376605)
19. Villablanca, E. J., D. Zhou, B. Valentinis, A. Negro, L. Raccosta, L. Mauri, A. Prinetti, S. Sonnino, C. Bordignon, C. Traversari, and V. Russo. 2008. Selected natural and synthetic retinoids impair CCR7- and CXCR4-dependent cell migration in vitro and in vivo. J. Leukoc. Biol. 84:871-879.
20. Haraoui, B., R. L. Wilder, J. B. Allen, M. B. Sporn, R. K. Helfgott, and C. E. Brinckerhoff. 1985. Dose-dependent suppression by the synthetic retinoid, 4-hydroxyphenyl retinamide, of streptococcal cell wall-induced arthritis in rats. Int. J. Immunopharmacol. 7: 903-916. (Pubitemid 16213259)
21. Lopez-Vales, R., A. Redensek, T. A. Skinner, K. I. Rathore, N. Ghasemlou, G. Wojewodka, J. DeSanctis, D. Radzioch, and S. David. 2010. Fenretinide promotes functional recovery and tissue protection after spinal cord contusion injury in mice. J. Neurosci. 30: 3220-3226.
22. Bielawski, J., Z. M. Szulc, Y. A. Hannun, and A. Bielawska. 2006. Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods. 39: 82-91. (Pubitemid 44107706)
23. Grassme, H., V. Jendrossek, A. Riehle, G. von Kurthy, J. Berger, H. Schwarz, M. Weller, R. Kolesnick, and E. Gulbins. 2003. Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat. Med. 9: 322-330. (Pubitemid 36362788)
24. Yu, H., Y. H. Zeidan, B. X. Wu, R. W. Jenkins, T. R. Flotte, Y. A. Hannun, and I. Virella-Lowell. 2009. Defective acid sphingomyelinase pathway with Pseudomonas aeruginosa infection in cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 41: 367-375.
25. Grassme, H., E. Gulbins, B. Brenner, K. Ferlinz, K. Sandhoff, K. Harzer, F. Lang, and T. F. Meyer. 1997. Acidic sphingomyelinase mediates entry of N. gonorrhoeae into nonphagocytic cells. Cell. 91: 605-615. (Pubitemid 27513652)
26. Harrison, D. A. 2012. The Jak/STAT pathway. Cold Spring Harbor Perspect. Biol. 4: pii.
27. Stark, G. R., and J. E. Darnell, Jr. 2012. The JAK-STAT pathway at twenty. Immunity. 36: 503-514.
28. Hazeki, K., K. Nigorikawa, and O. Hazeki. 2007. Role of phosphoinositide 3-kinase in innate immunity. Biol. Pharm. Bull. 30: 1617-1623. (Pubitemid 47403233)
29. Weichhart, T., and M. D. Saemann. 2008. The PI3K/Akt/mTOR pathway in innate immune cells: emerging therapeutic applications. Ann. Rheum. Dis. 67 (Suppl 3) : iii70-iii74.
30. Narayana, Y., K. Bansal, A. Y. Sinha, N. Kapoor, G. Puzo, M. Gilleron, and K. N. Balaji. 2009. SOCS3 expression induced by PIM2 requires PKC and PI3K signaling. Mol. Immunol. 46: 2947-2954.
31. Shimizu, T., T. Kayamori, C. Murayama, and A. Miyamoto. 2012. Bone morphogenetic protein (BMP)-4 and BMP-7 suppress granulosa cell apoptosis via different pathways: BMP-4 via PI3K/PDK-1/Akt and BMP-7 via PI3K/PDK-1/PKC. Biochem. Biophys. Res. Commun. 417: 869-873.
32. Huang, G., L. Z. Shi, and H. Chi. 2009. Regulation of JNK and p38 MAPK in the immune system: signal integration, propagation and termination. Cytokine. 48: 161-169.
33. Kim, E. K., and E. J. Choi. 2010. Pathological roles of MAPK signaling pathways in human diseases. Biochim. Biophys. Acta. 1802: 396-405.
34. Sizemore, N., S. Leung, and G. R. Stark. 1999. Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-kappaB p65/RelA subunit. Mol. Cell. Biol. 19: 4798-4805. (Pubitemid 29289518)
35. Aksamitiene, E., A. Kiyatkin, and B. N. Kholodenko. 2012. Crosstalk between mitogenic Ras/MAPK and survival PI3K/Akt pathways: a fine balance. Biochem. Soc. Trans. 40: 139-146.
36. Gunzl, P., and G. Schabbauer. 2008. Recent advances in the genetic analysis of PTEN and PI3K innate immune properties. Immunobiology. 213: 759-765.
37. Bose, R., M. Verheij, A. Haimovitz-Friedman, K. Scotto, Z. Fuks, and R. Kolesnick. 1995. Ceramide synthase mediates daunorubicin-induced apoptosis: an alternative mechanism for generating death signals. Cell. 82: 405-414.
38. Chalfant, C. E., K. Rathman, R. L. Pinkerman, R. E. Wood, L. M. Obeid, B. Ogretmen, and Y. A. Hannun. 2002. De novo ceramide regulates the alternative splicing of caspase 9 and Bcl-x in A549 lung adenocarcinoma cells. Dependence on protein phosphatase-1. J. Biol. Chem. 277: 12587-12595. (Pubitemid 34952617)
39. Kroesen, B. J., S. Jacobs, B. J. Pettus, H. Sietsma, J. W. Kok, Y. A. Hannun, and L. F. de Leij. 2003. BcR-induced apoptosis involves differential regulation of C16 and C24-ceramide formation and sphingolipid-dependent activation of the proteasome. J. Biol. Chem. 278: 14723-14731. (Pubitemid 36799795)
40. Perry, D. K., J. Carton, A. K. Shah, F. Meredith, D. J. Uhlinger, and Y. A. Hannun. 2000. Serine palmitoyltransferase regulates de novo ceramide generation during etoposide-induced apoptosis. J. Biol. Chem. 275: 9078-9084. (Pubitemid 30180269)
41. Cowart, L. A., and Y. A. Hannun. 2007. Selective substrate supply in the regulation of yeast de novo sphingolipid synthesis. J. Biol. Chem. 282: 12330-12340. (Pubitemid 47100697)
42. Hanada, K. 2003. Serine palmitoyltransferase, a key enzyme of sphingolipid metabolism. Biochim. Biophys. Acta. 1632: 16-30. (Pubitemid 36628112)
43. Sims, K., C. A. Haynes, S. Kelly, J. C. Allegood, E. Wang, A. Momin, M. Leipelt, D. Reichart, C. K. Glass, M. C. Sullards, et al. 2010. Kdo2-lipid A, a TLR4-specific agonist, induces de novo sphingolipid biosynthesis in RAW264.7 macrophages, which is essential for induction of autophagy. J. Biol. Chem. 285: 38568-38579.
44. Petrache, I., V. Natarajan, L. Zhen, T. R. Medler, A. T. Richter, C. Cho, W. C. Hubbard, E. V. Berdyshev, and R. M. Tuder. 2005. Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat. Med. 11: 491-498. (Pubitemid 40685971)
45. Ndengele, M. M., S. Cuzzocrea, E. Masini, M. C. Vinci, E. Esposito, C. Muscoli, D. N. Petrusca, V. Mollace, E. Mazzon, D. Li, et al. 2009. Spinal ceramide modulates the development of morphine antinociceptive tolerance via peroxynitrite-mediated nitroxidative stress and neuroimmune activation. J. Pharmacol. Exp. Ther. 329: 64-75.
46. Gorshkova, I., T. Zhou, B. Mathew, J. R. Jacobson, D. Takekoshi, P. Bhattacharya, B. Smith, B. Aydogan, R. R. Weichselbaum, V. Natarajan, et al. 2012. Inhibition of serine palmitoyltransferase delays the onset of radiation-induced pulmonary fibrosis through the negative regulation of sphingosine kinase-1 expression. J. Lipid Res. 53: 1553-1568.
47. Ibarguren, M., P. H. Bomans, P. M. Frederik, M. Stonehouse, A. I. Vasil, M. L. Vasil, A. Alonso, and F. M. Goni. 2010. End-products diacylglycerol and ceramide modulate membrane fusion induced by a phospholipase C/sphingomyelinase from Pseudomonas aeruginosa. Biochim. Biophys. Acta. 1798: 59-64.
48. Milhas, D., C. J. Clarke, and Y. A. Hannun. 2010. Sphingomyelin metabolism at the plasma membrane: implications for bioactive sphingolipids. FEBS Lett. 584: 1887-1894.
49. Kitatani, K., J. Idkowiak-Baldys, and Y. A. Hannun. 2008. The sphingolipid salvage pathway in ceramide metabolism and signaling. Cell Signal 20: 1010-1018.
50. Okajima, F. 2002. Plasma lipoproteins behave as carriers of extracellular sphingosine 1-phosphate: is this an atherogenic mediator or an anti-atherogenic mediator? Biochim. Biophys. Acta. 1582: 132-137. (Pubitemid 34634121)
51. Bartke, N., and Y. A. Hannun. 2009. Bioactive sphingolipids: metabolism and function. J. Lipid Res. 50 (Suppl) : S91-S96.
52. Lopez-Montero, I., N. Rodriguez, S. Cribier, A. Pohl, M. Velez, and P. F. Devaux. 2005. Rapid transbilayer movement of ceramides in phospholipid vesicles and in human erythrocytes. J. Biol. Chem. 280: 25811-25819. (Pubitemid 40962291)
53. Cuzzocrea, S., H. P. Deigner, T. Genovese, E. Mazzon, E. Esposito, C. Crisafulli, R. Di Paola, P. Bramanti, G. Matuschak, and D. Salvemini. 2009. Inhibition of ceramide biosynthesis ameliorates pathological consequences of spinal cord injury. Shock. 31: 634-644.
54. Fabrias, G., J. Munoz-Olaya, F. Cingolani, P. Signorelli, J. Casas, V. Gagliostro, and R. Ghidoni. 2012. Dihydroceramide desaturase and dihydrosphingolipids: debutant players in the sphingolipid arena. Prog. Lipid Res. 51: 82-94.
55. Osone, S., H. Hosoi, Y. Kuwahara, Y. Matsumoto, T. Iehara, and T. Sugimoto. 2004. Fenretinide induces sustained-activation of JNK/ p38 MAPK and apoptosis in a reactive oxygen species-dependent manner in neuroblastoma cells. Int. J. Cancer. 112: 219-224. (Pubitemid 39244361)
56. Samuel, W., R. K. Kutty, S. Sekhar, C. Vijayasarathy, B. Wiggert, and T. M. Redmond. 2008. Mitogen-activated protein kinase pathway mediates N-(4-hydroxyphenyl)retinamide-induced neuronal differentiation in the ARPE-19 human retinal pigment epithelial cell line. J. Neurochem. 106: 591-602.
57. Lasserre, R., X. J. Guo, F. Conchonaud, Y. Hamon, O. Hawchar, A. M. Bernard, S. M. Soudja, P. F. Lenne, H. Rigneault, D. Olive, G. Bismuth, J. A. Nunes, B. Payrastre, D. Marguet, and H. T. He. 2008. Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat. Chem. Biol. 4: 538-547.
58. Gao, X., P. R. Lowry, X. Zhou, C. Depry, Z. Wei, G. W. Wong, and J. Zhang. 2011. PI3K/Akt signaling requires spatial compartmentalization in plasma membrane microdomains. Proc. Natl. Acad. Sci. USA. 108: 14509-14514.
59. Monick, M. M., R. K. Mallampalli, A. B. Carter, D. M. Flaherty, D. McCoy, P. K. Robeff, M. W. Peterson, and G. W. Hunninghake. 2001. Ceramide regulates lipopolysaccharide-induced phosphatidylinositol 3-kinase and Akt activity in human alveolar macrophages. J. Immunol. 167: 5977-5985. (Pubitemid 33062795)
60. Barsacchi, R., C. Perrotta, S. Bulotta, S. Moncada, N. Borgese, and E. Clementi. 2003. Activation of endothelial nitric-oxide synthase by tumor necrosis factor-alpha: a novel pathway involving sequential activation of neutral sphingomyelinase, phosphatidylinositol-3′ kinase, and Akt. Mol. Pharmacol. 63: 886-895. (Pubitemid 36368996)
61. Lee, J. Y., Y. A. Hannun, and L. M. Obeid. 1996. Ceramide inactivates cellular protein kinase Calpha. J. Biol. Chem. 271: 13169-13174. (Pubitemid 26175896)
62. Fox, T. E., K. L. Houck, S. M. O'Neill, M. Nagarajan, T. C. Stover, P. T. Pomianowski, O. Unal, J. K. Yun, S. J. Naides, and M. Kester. 2007. Ceramide recruits and activates protein kinase C zeta (PKC zeta) within structured membrane microdomains. J. Biol. Chem. 282: 12450-12457. (Pubitemid 47100622)
63. Schubert, K. M., M. P. Scheid, and V. Duronio. 2000. Ceramide inhibits protein kinase B/Akt by promoting dephosphorylation of serine 473. J. Biol. Chem. 275: 13330-13335. (Pubitemid 30257390)
64. Zhou, H., S. A. Summers, M. J. Birnbaum, and R. N. Pittman. 1998. Inhibition of Akt kinase by cell-permeable ceramide and its implications for ceramide-induced apoptosis. J. Biol. Chem. 273: 16568-16575. (Pubitemid 28311444)
65. Arboleda, G., Y. Cardenas, Y. Rodriguez, L. C. Morales, L. Matheus, and H. Arboleda. 2010. Differential regulation of AKT, MAPK and GSK3beta during C2-ceramide-induced neuronal death. Neurotoxicology. 31: 687-693.
66. Stratford, S., K. L. Hoehn, F. Liu, and S. A. Summers. 2004. Regulation of insulin action by ceramide: dual mechanisms linking ceramide accumulation to the inhibition of Akt/protein kinase B. J. Biol. Chem. 279: 36608-36615. (Pubitemid 39129005)
67. Koide, N., T. Sugiyama, I. Mori, M. M. Mu, T. Yoshida, and T. Yokochi. 2003. C2-ceramide inhibits LPS-induced nitric oxide production in RAW 264.7 macrophage cells through down-regulating the activation of Akt. J. Endotoxin Res. 9: 85-90. (Pubitemid 36603681)
68. Zundel, W., and A. Giaccia. 1998. Inhibition of the anti-apoptotic PI(3)K/Akt/Bad pathway by stress. Genes Dev. 12: 1941-1946. (Pubitemid 28323868)
69. Fukao, T., and S. Koyasu. 2003. PI3K and negative regulation of TLR signaling. Trends Immunol. 24: 358-363. (Pubitemid 36830961)