Ceramide kinase contributes to proliferation but not to prostaglandin E 2 formation in renal mesangial cells and fibroblasts

Cellular Physiology and Biochemistry

Volumn 34, Issue 1, 2014, Pages 119-133

  Pastukhov, Oleksandr ^a   Schwalm, Stephanie ^b   Römer, Isolde ^b   Zangemeister Wittke, Uwe ^a   Pfeilschifter, Josef ^b   Huwiler, Andrea ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Apoptosis; Ceramide kinase; Fibroblasts; M phase arrest; Mesangial cells; NVP 231; Proliferation

Indexed keywords

ARACHIDONIC ACID; CERAMIDE KINASE; CYCLIN DEPENDENT KINASE 2; HISTONE H3; POLO LIKE KINASE 1; PROSTAGLANDIN E2; CYCLIN DEPENDENT KINASE 1; DNA; INTERLEUKIN 1BETA; NVP 231; PHOSPHOTRANSFERASE INHIBITOR; THYMIDINE; UNCLASSIFIED DRUG; BENZOTHIAZOLE DERIVATIVE; BRIDGED COMPOUND; CELL CYCLE PROTEIN; HISTONE; ONCOPROTEIN; PHOSPHOTRANSFERASE; POLO-LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL FUNCTION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME INHIBITION; FIBROBLAST; GLOMERULUS; IC 50; INFLAMMATION; M PHASE CELL CYCLE CHECKPOINT; MESANGIUM CELL; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; ANTIPROLIFERATIVE ACTIVITY; G2 PHASE CELL CYCLE CHECKPOINT; IC50; IN VITRO STUDY; MEMBRANOPROLIFERATIVE GLOMERULONEPHRITIS; PROSTAGLANDIN SYNTHESIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; GENE INACTIVATION; GENETICS; KIDNEY; METABOLISM;

RATTUS;

ANIMALS; APOPTOSIS; ARACHIDONIC ACID; BENZOTHIAZOLES; BRIDGED COMPOUNDS; CDC2 PROTEIN KINASE; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; DINOPROSTONE; FIBROBLASTS; GENE KNOCKOUT TECHNIQUES; HISTONES; KIDNEY; M PHASE CELL CYCLE CHECKPOINTS; MESANGIAL CELLS; MICE; MICE, INBRED BALB C; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RATS;

EID: 84903936727     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000362989     Document Type: Article

References (61)

1. Pfeilschifter J: Mesangial cells orchestrate inflammation in the renal glomerulus. News Physiol Sci 1994;9:271-276.
2. Gómez-Guerrero C, Hernández-Vargas P, López-Franco O, Ortiz-Muñoz G, Egido J: Mesangial cells and glomerular inflammation: from the pathogenesis to novel therapeutic approaches. Curr Drug Targets Inflamm Allergy 2005;4:341-351. (Pubitemid 40873122)
3. Migliorini A, Ebid R, Scherbaum CR, Anders HJ: The danger control concept in kidney disease: mesangial cells. J Nephrol 2013;26:437-449.
4. Murakami M, Kudo I: Secretory phospholipase A2. Biol Pharm Bull 2004;27:1158-1164.
5. Masuda S, Murakami M, Komiyama K, Ishihara M, Ishikawa Y, Ishii T, Kudo I : Various secretory phospholipase A2 enzymes are expressed in rheumatoid arthritis and augment prostaglandin production in cultured synovial cells. FEBS J 2005;272:655-672. (Pubitemid 40208870)
6. Murakami M, Lambeau G: Emerging roles of secreted phospholipase A(2) enzymes: an update. Biochimie 2013;95:43-50.
7. Magrioti V, Kokotos G: Phospholipase A2 inhibitors as potential therapeutic agents for the treatment of inflammatory diseases. Expert Opin Ther Pat 2010;20:1-18.
8. Magrioti V, Kokotos G: Phospholipase A2 inhibitors for the treatment of inflammatory diseases: a patent review (2010-present). Expert Opin Ther Pat 2013;23:333-344.
9. Huwiler A, Kolter T, Pfeilschifter J, Sandhoff K: Physiology and pathophysiology of sphingolipid metabolism and signaling. Biochim Biophys Acta 2000;1485:63-99. (Pubitemid 30314727)
10. Maceyka M, Harikumar KB, Milstien S, Spiegel S: Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol 2012;22:50-60.
11. Bornancin, F: Ceramide kinase: the first decade. Cell Signal 2011;23:999-1008.
12. Stahelin RV, Subramanian P, Vora M, Cho W, Chalfant CE: Ceramide-1-phosphate binds group IVA cytosolic phospholipase a2 via a novel site in the C2 domain. J Biol Chem 2007;282;20467-20474. (Pubitemid 47100015)
13. Sugiura M, Kono K, Liu H, Shimizugawa T, Minekura H, Spiegel S, Kohama T: Ceramide kinase, a novel lipid kinase. Molecular cloning and functional charcterization. J Biol Chem 2002;277:23294-23300. (Pubitemid 34952158)
14. Carré A, Graf C, Stora S, Mechtcheriakova D, Csonga R, Urtz N, Billich A, Baumruker T, Bornancin F: Ceramide kinase targeting and activity determined by its N-terminal pleckstrin homology domain. Biochem Biophys Res Commun 2004;324:1215-1219. (Pubitemid 40292152)
15. Rovina P, Schanzer A, Graf C, Mechtcheriakova D, Jaritz M, Bornancin F: Subcellular localization of ceramide kinase and ceramide kinase-like protein requires interplay of their Pleckstrin Homology domain-containing N-terminal regions together with C-terminal domains. Biochim Biophys Acta 2009;1791:1023-1030.
16. Huwiler A, Fabbro D, Pfeilschifter J: Possible regulatory functions of protein kinase C-alpha and-epsilon isoenzymes in rat renal mesangial cells. Stimulation of prostaglandin synthesis and feedback inhibition of angiotensin II-stimulated phosphoinositide hydrolysis. Biochem J 1991;279:441-445.
17. Graf C, Zemann B, Rovina P, Urtz N, Schanzer A, Reuschel R, Mechtcheriakova D, Müller M, Fischer E, Reichel C, Huber S, Dawson J, Meingassner JG, Billich A, Niwa S, Badegruber R, Van Veldhoven PP, Kinzel B, Baumruker T, Bornancin F: Neutropenia with impaired immune response to Streptococcus pneumoniae in ceramide kinase-deficient mice. J Immunol 2008;180:3457-3466.
18. Nakagawa N, Yuhki K, Kawabe J, Fujino T, Takahata O, Kabara M, Abe K, Kojima F, Kashiwagi H, Hasebe N, Kikuchi K, Sugimoto Y, Narumiya S, Ushikubi F: The intrinsic prostaglandin E2-EP4 system of the renal tubular epithelium limits the development of tubulointerstitial fibrosis in mice. Kidney Int 2012;82:158-171.
19. Huwiler A, Fabbro D, Pfeilschifter J: Comparison of different tumour promoters and bryostatin 1 on protein kinase C activation and down-regulation in rat renal mesangial cells. Biochem Pharmacol 1994;48:689-700. (Pubitemid 24283838)
20. Hofmann LP, Ren S, Schwalm S, Pfeilschifter J, Huwiler A: Sphingosine kinase 1 and 2 regulate the capacity of mesangial cells to resist apoptotic stimuli in an opposing manner. Biol Chem 2008;389:1399-1407.
21. Graf C, Klumpp M, Habig M, Rovina P, Billich A, Baumruker T, Oberhauser B, Bornancin F: Targeting ceramide metabolism with a potent and specific ceramide kinase inhibitor. Mol Pharmacol 2008;74:925-932.
22. Kramer RM, Roberts EF, Manetta JV, Hyslop PA, Jakubowski JA: Thrombin-induced phosphorylation and activation of Ca2+-sensitive cytosolic phospholipase A2 in human platelets. J Biol Chem 1993;268;26796-26804. (Pubitemid 23361770)
23. Qiu ZH, Gijón MA, de Carvalho MS, Spencer DM, Leslie CC: The role of calcium and phosphorylation of cytosolic phospholipase A2 in regulating arachidonic acid release in macrophages. J Biol Chem 1998;273;8203-8211. (Pubitemid 28168876)
24. Pfeilschifter J, Leighton J, Pignat W, Märki F, Vosbeck K: Cyclic AMP mimics, but does not mediate, interleukin-1-and tumour-necrosis-factor- stimulated phospholipase A2 secretion from rat renal mesangial cells. Biochem J 1991;273:199-204.
25. Pfeilschifter J, Schalkwijk C, Briner VA, van den Bosch H: Cytokine-stimulated secretion of group II phospholipase A2 by rat mesangial cells. Its contribution to arachidonic acid release and prostaglandin synthesis by cultured rat glomerular cells. J Clin Invest 1993;92:2516-2523. (Pubitemid 23333562)
26. Vassilev LT, Tovar C, Chen S, Knezevic D, Zhao X, Sun H, Heimbrook DC, Chen L: Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc Natl Acad Sci USA 2006;103:10660-10665. (Pubitemid 44078033)
27. Enserink JM, Kolodner RD. An overview of Cdk1-controlled targets and processes. Cell Div 2010;5:11.
28. Petronczki M, Lénárt P, Peters JM: Polo on the Rise-from Mitotic Entry to Cytokinesis with Plk1. Dev Cell 2008;14:646-659. (Pubitemid 351622626)
29. Kaufmann SH, Desnoyers S, Ottaviano Y, Davidson NE, Poirier GG: Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res 1993;53:3976-3985. (Pubitemid 23267698)
30. Lamour NF, Chalfant CE : Ceramide kinase and the ceramide-1-phosphate/ cPLA2alpha interaction as a therapeutic target. Curr Drug Targets 2008;9:674-682.
31. Saxena S, Banerjee M, Shirumalla RK, Ray A: Ceramide kinase: a potential anti-inflammatory target? Curr Opin Investig Drugs 2008;9:455-462. (Pubitemid 351677898)
32. Mietla JA, Wijesinghe DS, Hoeferlin LA, Shultz MD, Natarajan R, Fowler AA 3rd, Chalfant CE: Characterization of eicosanoid synthesis in a genetic ablation model of ceramide kinase. J Lipid Res 2013;54:1834-1847.
33. Niwa S, Urtz N, Baumruker T, Billich A, Bornancin F: Ovalbumin-induced plasma interleukin-4 levels are reduced in ceramide kinase-deficient DO11.10 RAG1-/-mice. Lipids Health Dis 2010;9:1.
34. Balsinde J, Balboa MA, Dennis EA: Inflammatory activation of arachidonic acid signaling in murine P388D1 macrophages via sphingomyelin synthesis. J Biol Chem 1997;272:20373-20377. (Pubitemid 27355586)
35. Klapisz E, Masliah J, Béréziat G, Wolf C, Koumanov KS: Sphingolipids and cholesterol modulate membrane susceptibility to cytosolic phospholipase A(2). J Lipid Res 2000;41:1680-1688.
36. Huwiler A, Johansen B, Skarstad A, Pfeilschifter J: Ceramide binds to the CaLB domain of cytosolic phospholipase A2 and facilitates its membrane docking and arachidonic acid release. FASEB J 2001;15:7-9.
37. Kitatani K, Akiba S, Sato T: Ceramide-induced enhancement of secretory phospholipase A2 expression via generation of reactive oxygen species in tumor necrosis factor-alpha-stimulated mesangial cells. Cell Signal 2004;16:967-974. (Pubitemid 38638786)
38. Ballou LR, Chao CP, Holness MA, Barker SC, Raghow R: Interleukin-1- mediated PGE2 production and sphingomyelin metabolism. Evidence for the regulation of cyclooxygenase gene expression by sphingosine and ceramide. J Biol Chem 1992;267:20044-20050.
39. Hayakawa M, Jayadev S, Tsujimoto M, Hannun YA, Ito F: Role of ceramide in stimulation of the transcription of cytosolic phospholipase A2 and cyclooxygenase 2. Biochem Biophys Res Commun 1996;220:681-686. (Pubitemid 26198571)
40. Subbaramaiah K, Chung WJ, Dannenberg AJ: Ceramide regulates the transcription of cyclooxygenase-2. Evidence for involvement of extracellular signal-regulated kinase/c-Jun N-terminal kinase and p38 mitogen-activated protein kinase pathways. J Biol Chem 1998;273:32943-32949. (Pubitemid 28557687)
41. Teichgräber V, Ulrich M, Endlich N, Riethmüller J, Wilker B, De Oliveira-Munding CC, van Heeckeren AM, Barr ML, von Kürthy G, Schmid KW, Weller M, Tümmler B, Lang F, Grassme H, Döring G, Gulbins E: Ceramide accumulation mediates inflammation, cell death and infection susceptibility in cystic fibrosis. Nat Med 2008;14:382-391. (Pubitemid 351499396)
42. Tibboel J, Reiss I, de Jongste JC, Post M : Ceramides: a potential therapeutic target in pulmonary emphysema. Respir Res 2013;14:96.
43. Petrache I, Kamocki K, Poirier C, Pewzner-Jung Y, Laviad EL, Schweitzer KS, Van Demark M, Justice MJ, Hubbard WC, Futerman AH: Ceramide synthases expression and role of ceramide synthase-2 in the lung: insight from human lung cells and mouse models. PLoS One 2013;8:e62968.
44. Liang H, Yao N, Song JT, Luo S, Lu H, Greenberg JT: Ceramides modulate programmed cell death in plants. Genes Dev 2003;17:2636-26341.
45. Townley HE, McDonald K, Jenkins GI, Knight MR, Leaver CJ: Ceramides induce programmed cell death in Arabidopsis cells in a calcium-dependent manner. Biol Chem 2005;386:161-166. (Pubitemid 40361442)
46. Mitra P, Maceyka M, Payne SG, Lamour N, Milstien S, Chalfant CE, Spiegel S: Ceramide kinase regulates growth and survival of A549 human lung adenocarcinoma cells. FEBS Lett 2007;581:735-740. (Pubitemid 46217927)
47. Ruckhäberle E, Karn T, Rody A, Hanker L, Gätje R, Metzler D, Holtrich U, Kaufmann M: Gene expression of ceramide kinase, galactosyl ceramide synthase and ganglioside GD3 synthase is associated with prognosis in breast cancer. J Cancer Res Clin Oncol. 2009;135:1005-1013.
48. Hsieh SY, Hsu CY, He JR, Liu CL, Lo SJ, Chen YC, Huang HY: Identifying apoptosis-evasion proteins/ pathways in human hepatoma cells via induction of cellular hormesis by UV irradiation. J Proteome Res 2009;8:3977-3986.
49. Bini F, Frati A, Garcia-Gil M, Battistini C, Granado M, Martinesi M, Mainardi M, Vannini E, Luzzati F, Caleo M, Peretto P, Gomez-Muñoz A, Meacci E: New signalling pathway involved in the anti-proliferative action of vitamin D3 and its analogues in human neuroblastoma cells. A role for ceramide kinase. Neuropharmacology 2012;63:524-537.
50. Murakami M, Ito H, Hagiwara K, Yoshida K, Sobue S, Ichihara M, Takagi A, Kojima T, Tanaka K, Tamiya-Koizumi K, Kyogashima M, Suzuki M, Banno Y, Nozawa Y, Murate T: ATRA inhibits ceramide kinase transcription in a human neuroblastoma cell line, SH-SY5Y cells: the role of COUP-TFI. J Neurochem 2010;112:511-520.
51. Tsuji K, Mitsutake S, Yokose U, Sugiura M, Kohama T, Igarashi Y: Role of ceramide kinase in peroxisome proliferator-activated receptor beta-induced cell survival of mouse keratinocytes. FEBS J 2008;275:3815-3826. (Pubitemid 351990946)
52. Dbaibo GS, Pushkareva MY, Jayadev S, Schwarz JK, Horowitz JM, Obeid LM, Hannun YA : Retinoblastoma gene product as a downstream target for a ceramide-dependent pathway of growth arrest. Proc Natl Acad Sci USA 1995;92:1347-1351.
53. Alesse E, Zazzeroni F, Angelucci A, Giannini G, Di Marcotullio L, Gulino A: The growth arrest and downregulation of c-myc transcription induced by ceramide are related events dependent on p21 induction, Rb underphosphorylation and E2F sequestering. Cell Death Differ 1998;5:381-389. (Pubitemid 28356814)
54. Oh WJ, Kim WH, Kang KH, Kim TY, Kim MY, Choi KH: Induction of p21 during ceramide-mediated apoptosis in human hepatocarcinoma cells. Cancer Lett 1998;129:215-222. (Pubitemid 28386604)
55. Rani CS, Abe A, Chang Y, Rosenzweig N, Saltiel AR, Radin NS, Shayman JA: Cell cycle arrest induced by an inhibitor of glucosylceramide synthase. Correlation with cyclin-dependent kinases. J Biol Chem 1995;270:2859-2867.
56. Drobnik W, Liebisch G, Biederer C, Tr mbach B, Rogler G, Müller P, Schmitz G: Growth and cell cycle abnormalities of fibroblasts from Tangier disease patients. Arterioscler Thromb Vasc Biol 1999;19:28-38. (Pubitemid 29031909)
57. Takai N, Ueda T, Kawano Y, Nishida M, Nasu K, Narahara H: C2-ceramide exhibits antiproliferative activity and potently induces apoptosis in endometrial carcinoma. Oncol Rep 2005;14:1287-1291.
58. Huwiler, A., Pfeilschifter, J: Altering the sphingosine-1-phosphate/ ceramide balance: a promising approach for tumor therapy. Curr Pharm Des 2006;12:4625-4635. (Pubitemid 44835150)
59. Huwiler A, Zangemeister-Wittke U: Targeting the conversion of ceramide to sphingosine 1-phosphate as a novel strategy for cancer therapy. Crit Rev Oncol Hematol 2007;63:150-159. (Pubitemid 46990918)
60. Holthuis JC, Luberto C: Tales and mysteries of the enigmatic sphingomyelin synthase family. Adv Exp Med Biol 2010;688:72-85.
61. Kartal Yandim M, Apohan E, Baran Y: Therapeutic potential of targeting ceramide/glucosylceramide pathway in cancer. Cancer Chemother Pharmacol 2013;71:13-20.