Distinct receptor-mediated activities in macrophages for natural ceramide-1-phosphate (C1P) and for phospho-ceramide analogue-1 (PCERA-1)

Molecular and Cellular Endocrinology

Volumn 314, Issue 2, 2010, Pages 248-255

  Levi, Maya ^a   Meijler, Michael M ^b   Gómez Muñoz, Antonio ^c   Zor, Tsaffrir ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

C1P; Cell migration; Inflammation; Macrophages; PCERA 1; Phospholipid binding receptors

Indexed keywords

1 METHYL 2 (3 METHOXYPHENYL) 2 (OCTANOYLAMINO)ETHYLDISODIUM PHOSPHATE; ARACHIDONIC ACID; CASPASE 3; CASPASE 9; CERAMIDE 1 PHOSPHATE; CERAMIDE DERIVATIVE; CYCLIN D1; CYCLOOXYGENASE 2; CYTOCHROME C; GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE A2; PROSTAGLANDIN E2; PROTEIN KINASE B; SERINE PALMITOYLTRANSFERASE; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARACHIDONIC ACID METABOLISM; CELL DEATH; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CYTOKINE PRODUCTION; DRUG POTENCY; DRUG SENSITIVITY; DRUG SYNTHESIS; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; INFLAMMATION; MACROPHAGE; NONHUMAN; PHOSPHOLIPID METABOLISM; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; REVIEW; SEPSIS; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

ANIMALS; CELL MOVEMENT; CERAMIDES; HUMANS; INFLAMMATION; MACROPHAGES; SIGNAL TRANSDUCTION;

EID: 71849107705     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.05.007     Document Type: Review

References (74)

1. Adachi H., and Tsujimoto M. Endothelial scavenger receptors. Prog. Lipid Res. 45 (2006) 379-404
2. Alvarez S.E., Milstien S., and Spiegel S. Autocrine and paracrine roles of sphingosine-1-phosphate. Trends Endocrinol. Metab. 18 (2007) 300-307
3. Anliker B., and Chun J. Lysophospholipid G protein-coupled receptors. J. Biol. Chem. 279 (2004) 20555-20558
4. Avni D., Goldsmith M., Ernst O., Mashiach R., Tuntland T., Meijler M.M., Gray N.S., Rosen H., and Zor T. Modulation of TNFα, IL-10 and IL-12p40 levels by a ceramide-1-phosphate analog, PCERA-1, in-vivo and ex-vivo in primary macrophages. Immunol. Lett. 123 (2009) 1-8
5. Avni, D., Philosoph, A., Meijler, M.M., Zor, T., 2009b. The ceramide-1-phosphate analog PCERA-1 modulates TNFα and IL-10 production in macrophages via the cAMP-PKA-CREB pathway in a GTP-dependent manner. Immunology, in press.
6. Azzi M., Charest P.G., Angers S., Rousseau G., Kohout T., Bouvier M., and Pineyro G. Beta-arrestin-mediated activation of MAPK by inverse agonists reveals distinct active conformations for G protein-coupled receptors. Proc. Natl. Acad. Sci. USA. 100 (2003) 11406-11411
7. Bajjalieh S.M., Martin T.F., and Floor E. Synaptic vesicle ceramide kinase. A calcium-stimulated lipid kinase that co-purifies with brain synaptic vesicles. J. Biol. Chem. 264 (1989) 14354-14360
8. Boath A., Graf C., Lidome E., Ullrich T., Nussbaumer P., and Bornancin F. Regulation and traffic of ceramide 1-phosphate produced by ceramide kinase: comparative analysis to glucosylceramide and sphingomyelin. J. Biol. Chem. 283 (2008) 8517-8526
9. Boudker O., and Futerman A.H. Detection and characterization of ceramide-1-phosphate phosphatase activity in rat liver plasma membrane. J. Biol. Chem. 268 (1993) 22150-22155
10. Chalfant C.E., and Spiegel S. Sphingosine 1-phosphate and ceramide 1-phosphate: expanding roles in cell signaling. J. Cell. Sci. 118 (2005) 4605-4612
11. Cole A.L., Subbanagounder G., Mukhopadhyay S., Berliner J.A., and Vora D.K. Oxidized phospholipid-induced endothelial cell/monocyte interaction is mediated by a cAMP-dependent R-Ras/PI3-kinase pathway. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 1384-1390
12. Condeelis J., and Pollard J.W. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124 (2006) 263-266
13. Cremesti A.E., Goni F.M., and Kolesnick R. Role of sphingomyelinase and ceramide in modulating rafts: do biophysical properties determine biologic outcome?. FEBS Lett. 531 (2002) 47-53
14. Gangoiti P., Granado M.H., Arana L., Ouro A., and Gomez-Munoz A. Involvement of nitric oxide in the promotion of cell survival by ceramide 1-phosphate. FEBS Lett. 582 (2008) 2263-2269
15. Gangoiti P., Granado M.H., Wang S.W., Kong J.Y., Steinbrecher U.P., and Gomez-Munoz A. Ceramide 1-phosphate stimulates macrophage proliferation through activation of the PI3-kinase/PKB, JNK and ERK1/2 pathways. Cell. Signal. 20 (2008) 726-736
16. Goldsmith M., Avni D., Levy-Rimler G., Mashiach R., Ernst O., Levi M., Webb B., Meijler M.M., Gray N.S., Rosen H., and Zor T. A ceramide-1-phosphate analogue, PCERA-1, simultaneously suppresses tumour necrosis factor-alpha and induces interleukin-10 production in activated macrophages. Immunology 127 (2008) 103-115
17. Goldsmith M., Avni D., Ernst O., Glucksam Y., Levy-Rimler G., Meijler M.M., and Zor T. Synergistic IL-10 induction by LPS and the ceramide-1-phosphate analog PCERA-1 is mediated by the cAMP and p38 MAP kinase pathways. Mol. Immunol. 46 (2009) 1979-1987
18. Gomez-Munoz A., Duffy P.A., Martin A., O'Brien L., Byun H.S., Bittman R., and Brindley D.N. Short-chain ceramide-1-phosphates are novel stimulators of DNA synthesis and cell division: antagonism by cell-permeable ceramides. Mol. Pharmacol. 47 (1995) 833-839
19. Gomez-Munoz A., Frago L.M., Alvarez L., and Varela-Nieto I. Stimulation of DNA synthesis by natural ceramide 1-phosphate. Biochem. J. 325 Pt 2 (1997) 435-440
20. Gomez-Munoz A. Modulation of cell signalling by ceramides. Biochim Biophys Acta 1391 (1998) 92-109
21. Gomez-Munoz A., Kong J., Salh B., and Steinbrecher U.P. Sphingosine-1-phosphate inhibits acid sphingomyelinase and blocks apoptosis in macrophages. FEBS Lett. 539 (2003) 56-60
22. Gomez-Munoz A. Ceramide-1-phosphate: a novel regulator of cell activation. FEBS Lett. 562 (2004) 5-10
23. Gomez-Munoz A., Kong J.Y., Salh B., and Steinbrecher U.P. Ceramide-1-phosphate blocks apoptosis through inhibition of acid sphingomyelinase in macrophages. J. Lipid Res. 45 (2004) 99-105
24. Gomez-Munoz A., Kong J.Y., Parhar K., Wang S.W., Gangoiti P., Gonzalez M., Eivemark S., Salh B., Duronio V., and Steinbrecher U.P. Ceramide-1-phosphate promotes cell survival through activation of the phosphatidylinositol 3-kinase/protein kinase B pathway. FEBS Lett. 579 (2005) 3744-3750
25. Gomez-Munoz A. Ceramide 1-phosphate/ceramide, a switch between life and death. Biochim. Biophys. Acta 1758 (2006) 2049-2056
26. Gómez-Muñoz A., Gangoiti P., Granado M.H., Arana L., Ouro A., 2009. Ceramide 1-phosphate in cell survival and inflammatory signaling. In: Chalfant C. and Del Poeta M. (Ed.), Sphingolipids as signal and regulatory molecules. Landes Bioscience, Austin, in press.
27. Goni F.M., and Alonso A. Sphingomyelinases: enzymology and membrane activity. FEBS Lett. 531 (2002) 38-46
28. Graf C., Rovina P., Tauzin L., Schanzer A., and Bornancin F. Enhanced ceramide-induced apoptosis in ceramide kinase overexpressing cells. Biochem. Biophys. Res. Commun. 354 (2007) 309-314
29. Granado M.H., Gangoiti P., Ouro A., Arana L., and Gomez-Muñoz A. Ceramide 1-phosphate inhibits serine palmitoyltransferase and blocks apoptosis in alveolar macrophages. Biochem. Biophys. Acta 1791 (2009) 263-272
30. Granado M.H., Gangoiti P., Ouro A., Arana L., Gonzalez M., Trueba M., and Gomez-Munoz A. Ceramide 1-phosphate (C1P) promotes cell migration Involvement of a specific C1P receptor. Cell. Signal 21 (2009) 405-412
31. Hannun Y.A., Loomis C.R., Merrill Jr. A.H., and Bell R.M. Sphingosine inhibition of protein kinase C activity and of phorbol dibutyrate binding in vitro and in human platelets. J. Biol. Chem. 261 (1986) 12604-12609
32. Hannun Y.A. The sphingomyelin cycle and the second messenger function of ceramide. J. Biol. Chem. 269 (1994) 3125-3128
33. Hannun Y.A., and Obeid L.M. Ceramide: an intracellular signal for apoptosis. Trends Biochem. Sci. 20 (1995) 73-77
34. Hannun Y.A. Functions of ceramide in coordinating cellular responses to stress. Science 274 (1996) 1855-1859
35. Hannun Y.A., and Obeid L.M. The Ceramide-centric universe of lipid-mediated cell regulation: stress encounters of the lipid kind. J. Biol. Chem. 277 (2002) 25847-25850
36. Hinkovska-Galcheva V., Boxer L.A., Kindzelskii A., Hiraoka M., Abe A., Goparju S., Spiegel S., Petty H.R., and Shayman J.A. Ceramide 1-phosphate, a mediator of phagocytosis. J. Biol. Chem. 280 (2005) 26612-26621
37. Hinkovska-Galcheva V.T., Boxer L.A., Mansfield P.J., Harsh D., Blackwood A., and Shayman J.A. The formation of ceramide-1-phosphate during neutrophil phagocytosis and its role in liposome fusion. J. Biol. Chem 273 (1998) 33203-33209
38. Kolesnick R. Signal transduction through the sphingomyelin pathway. Mol. Chem. Neuropathol. 21 (1994) 287-297
39. Kolesnick R.N. 1,2-Diacylglycerols but not phorbol esters stimulate sphingomyelin hydrolysis in GH3 pituitary cells. J. Biol. Chem. 262 (1987) 16759-16762
40. Kolesnick R.N., and Hemer M.R. Characterization of a ceramide kinase activity from human leukemia (HL-60) cells. Separation from diacylglycerol kinase activity. J. Biol. Chem. 265 (1990) 18803-18808
41. Kolesnick R.N., Goni F.M., and Alonso A. Compartmentalization of ceramide signaling: physical foundations and biological effects. J. Cell. Physiol. 184 (2000) 285-300
42. Lamour N.F., and Chalfant C.E. Ceramide-1-phosphate: the "missing" link in eicosanoid biosynthesis and inflammation. Mol. Interv. 5 (2005) 358-367
43. Lamour N.F., Stahelin R.V., Wijesinghe D.S., Maceyka M., Wang E., Allegood J.C., Merrill Jr. A.H., Cho W., and Chalfant C.E. Ceramide kinase uses ceramide provided by ceramide transport protein: localization to organelles of eicosanoid synthesis. J. Lipid Res. 48 (2007) 1293-1304
44. Lamour N.F., and Chalfant C.E. Ceramide kinase and the ceramide-1-phosphate/cPLA2alpha interaction as a therapeutic target. Curr. Drug Targets 9 (2008) 674-682
45. Li R., Mouillesseaux K.P., Montoya D., Cruz D., Gharavi N., Dun M., Koroniak L., and Berliner J.A. Identification of prostaglandin E2 receptor subtype 2 as a receptor activated by OxPAPC. Circulation Res. 98 (2006) 642-650
46. Matsui T., Kondo T., Nishita Y., Itadani S., Nakatani S., Omawari N., Sakai M., Nakazawa S., Ogata A., Mori H., Terai K., Kamoshima W., Ohno H., Obata T., Nakai H., and Toda M. Highly potent inhibitors of TNF-α production. Part I. Discovery of new chemical leads and their structure-activity relationships. Bioorg. Med. Chem. 10 (2002) 3757-3786
47. Matsui T., Kondo T., Nishita Y., Itadani S., Nakatani S., Omawari N., Sakai M., Nakazawa S., Ogata A., Ohno H., Obata T., Nakai H., and Toda M. Highly potent inhibitors of TNF-α production. Part 1. Discovery of chemical leads. Bioorg. Med. Chem. Lett. 12 (2002) 903-905
48. Matsui T., Kondo T., Nishita Y., Itadani S., Tsuruta H., Fujita S., Omawari N., Sakai M., Nakazawa S., Ogata A., Mori H., Kamoshima W., Terai K., Ohno H., Obata T., Nakai H., and Toda M. Highly potent inhibitors of TNF-α production. Part II: metabolic stabilization of a newly found chemical lead and conformational analysis of an active diastereoisomer. Bioorg. Med. Chem. 10 (2002) 3787-3805
49. Matsui T., Kondo T., Nishita Y., Itadani S., Tsuruta H., Fujita S., Omawari N., Sakai M., Nakazawa S., Ogata A., Mori H., Ohno H., Obata T., Nakai H., and Toda M. Highly potent inhibitors of TNF-α production. Part 2: identification of drug candidates. Bioorg. Med. Chem. Lett. 12 (2002) 907-910
50. Matsui T., Takahashi S., Matsunaga N., Nakamura K., Omawari N., Sakai M., Kamoshima W., Terai K., Ohno H., Obata T., Nakai H., and Toda M. Discovery of novel phosphonic acid derivatives as new chemical leads for inhibitors of TNF-α production. Bioorg. Med. Chem. 10 (2002) 3807-3815
51. Matsui T., Kondo T., Nakatani S., Omawari N., Sakai M., Mori H., Ogata A., Kato J., Ohno H., Obata T., Nakai H., and Toda M. Synthesis, further biological evaluation and pharmacodynamics of newly discovered inhibitors of TNF-α production. Bioorg. Med. Chem. 11 (2003) 3937-3943
52. Merrill Jr. A.H., and Jones D.D. An update of the enzymology and regulation of sphingomyelin metabolism. Biochim. Biophys. Acta 1044 (1990) 1-12
53. Merrill Jr. A.H., Schmelz E.M., Dillehay D.L., Spiegel S., Shayman J.A., Schroeder J.J., Riley R.T., Voss K.A., and Wang E. Sphingolipids--the enigmatic lipid class: biochemistry, physiology, and pathophysiology. Toxicol. Appl. Pharmacol. 142 (1997) 208-225
54. Merrill Jr. A.H. De novo sphingolipid biosynthesis: a necessary, but dangerous, pathway. J. Biol. Chem. 277 (2002) 25843-25846
55. Mitra P., Maceyka M., Payne S.G., Lamour N., Milstien S., Chalfant C.E., and Spiegel S. Ceramide kinase regulates growth and survival of A549 human lung adenocarcinoma cells. FEBS Lett. 581 (2007) 735-740
56. Mitsutake S., Kim T.J., Inagaki Y., Kato M., Yamashita T., and Igarashi Y. Ceramide kinase is a mediator of calcium-dependent degranulation in mast cells. J. Biol. Chem. 279 (2004) 17570-17577
57. Pettus B.J., Bielawska A., Spiegel S., Roddy P., Hannun Y.A., and Chalfant C.E. Ceramide kinase mediates cytokine- and calcium ionophore-induced arachidonic acid release. J. Biol. Chem. 278 (2003) 38206-38213
58. Pettus B.J., Bielawska A., Subramanian P., Wijesinghe D.S., Maceyka M., Leslie C.C., Evans J.H., Freiberg J., Roddy P., Hannun Y.A., and Chalfant C.E. Ceramide 1-phosphate is a direct activator of cytosolic phospholipase A2. J. Biol. Chem. 279 (2004) 11320-11326
59. Pettus B.J., Kitatani K., Chalfant C.E., Taha T.A., Kawamori T., Bielawski J., Obeid L.M., and Hannun Y.A. The coordination of prostaglandin E2 production by sphingosine-1-phosphate and ceramide-1-phosphate. Mol. Pharmacol. 68 (2005) 330-335
60. Prather P.L. Inverse agonists: tools to reveal ligand-specific conformations of G protein-coupled receptors. Sci. STKE 2004 (2004) pe1
61. Rader D.J., and Daugherty A. Translating molecular discoveries into new therapies for atherosclerosis. Nature 451 (2008) 904-913
62. Rosen H., and Goetzl E.J. Sphingosine 1-phosphate and its receptors: an autocrine and paracrine network. Nat. Rev. Immunol. 5 (2005) 560-570
63. Saxena S., Banerjee M., Shirumalla R.K., and Ray A. Ceramide kinase: a potential anti-inflammatory target?. Curr. Opin. Investig. Drugs 9 (2008) 455-462
64. Spiegel S., Olivera A., and Carlson R.O. The role of sphingosine in cell growth regulation and transmembrane signaling. Adv. Lipid Res. 25 (1993) 105-129
65. Spiegel S., Foster D., and Kolesnick R. Signal transduction through lipid second messengers. Curr. Opin. Cell. Biol. 8 (1996) 159-167
66. Spiegel S., and Merrill Jr. A.H. Sphingolipid metabolism and cell growth regulation. Faseb J. 10 (1996) 1388-1397
67. Spiegel S., and Milstien S. Sphingosine 1-phosphate, a key cell signaling molecule. J. Biol. Chem. 277 (2002) 25851-25854
68. Spiegel S., and Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell. Biol. 4 (2003) 397-407
69. Subramanian P., Stahelin R.V., Szulc Z., Bielawska A., Cho W., and Chalfant C.E. Ceramide 1-phosphate acts as a positive allosteric activator of group IVA cytosolic phospholipase A2 alpha and enhances the interaction of the enzyme with phosphatidylcholine. J. Biol. Chem. 280 (2005) 17601-17607
70. Truett III A.P., and King Jr. L.E. Sphingomyelinase D: a pathogenic agent produced by bacteria and arthropods. Adv. Lipid Res. 26 (1993) 275-291
71. Wijesinghe D.S., Massiello A., Subramanian P., Szulc Z., Bielawska A., and Chalfant C.E. Substrate specificity of human ceramide kinase. J. Lipid Res. 46 (2005) 2706-2716
72. Wijesinghe D.S., Lamour N.F., Gomez-Munoz A., and Chalfant C.E. Ceramide kinase and ceramide-1-phosphate. Methods Enzymol. 434 (2007) 265-292
73. Wijesinghe D.S., Subramanian P., Lamour N.F., Gentile L.B., Granado M.H., Szulc Z., Bielawska A., Gomez-Munoz A., Chalfant C.E., 2008. The chain length specificity for the activation of group IV cytosolic phospholipase A2 by ceramide-1-phosphate. Use of the dodecane delivery system for determining lipid-specific effects. J. Lipid Res., in press.
74. Worgall T.S. Sphingolipids: major regulators of lipid metabolism. Curr. Opin. Clin. Nutr. Metab. Care 10 (2007) 149-155