Generation of reactive oxygen species (ROS) is a key factor for stimulation of macrophage proliferation by ceramide 1-phosphate

Experimental Cell Research

Volumn 318, Issue 4, 2012, Pages 350-360

  Arana, Lide ^a   Gangoiti, Patricia ^a   Ouro, Alberto ^a   Rivera, Io Guané ^a   Ordoñez, Marta ^a   Trueba, Miguel ^a   Lankalapalli, Ravi S ^b   Bittman, Robert ^b   Gomez Muñoz, Antonio ^a  

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

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Ceramide 1 phosphate; Ceramides; NADPH oxidase; Proliferation; ROS; Sphingolipids

Indexed keywords

CALCIUM; CERAMIDE 1 PHOSPHATE; PHOSPHOLIPASE A2; PROTEIN KINASE C ALPHA; PROTEIN P40; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ROTENONE; THENOYLTRIFLUOROACETONE;

ANIMAL CELL; ARTICLE; BONE MARROW; CELL GROWTH; CELL ISOLATION; CELL MEMBRANE; CELL PROLIFERATION; CELL STIMULATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; MACROPHAGE; MITOGENICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84856094739     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.11.013     Document Type: Article

References (65)

1. Gomez-Munoz A., Duffy P.A., Martin A., O'Brien L., Byun H.S., Bittman R., Brindley D.N. Short-chain ceramide-1-phosphates are novel stimulators of DNA synthesis and cell division: antagonism by cell-permeable ceramides. Mol. Pharmacol. 1995, 47:833-839.
2. Gangoiti P., Granado M.H., Wang S.W., Kong J.Y., Steinbrecher U.P., Gomez-Munoz A. Ceramide 1-phosphate stimulates macrophage proliferation through activation of the PI3-kinase/PKB, JNK and ERK1/2 pathways. Cell. Signal. 2008, 20:726-736.
3. Gangoiti P., Granado M.H., Arana L., Ouro A., Gomez-Munoz A. Involvement of nitric oxide in the promotion of cell survival by ceramide 1-phosphate. FEBS Lett. 2008, 582:2263-2269.
4. Gomez-Munoz A., Kong J.Y., Parhar K., Wang S.W., Gangoiti P., Gonzalez M., Eivemark S., Salh B., Duronio V., Steinbrecher U.P. Ceramide-1-phosphate promotes cell survival through activation of the phosphatidylinositol 3-kinase/protein kinase B pathway. FEBS Lett. 2005, 579:3744-3750.
5. Gomez-Munoz A., Kong J.Y., Salh B., Steinbrecher U.P. Ceramide-1-phosphate blocks apoptosis through inhibition of acid sphingomyelinase in macrophages. J. Lipid Res. 2004, 45:99-105.
6. Granado M.H., Gangoiti P., Ouro A., Arana L., Gomez-Munoz A. Ceramide 1-phosphate inhibits serine palmitoyltransferase and blocks apoptosis in alveolar macrophages. Biochim. Biophys. Acta 2009, 1791:263-272.
7. Chalfant C.E., Spiegel S. Sphingosine 1-phosphate and ceramide 1-phosphate: expanding roles in cell signaling. J. Cell Sci. 2005, 118:4605-4612.
8. Pettus B.J., Bielawska A., Spiegel S., Roddy P., Hannun Y.A., Chalfant C.E. Ceramide kinase mediates cytokine- and calcium ionophore-induced arachidonic acid release. J. Biol. Chem. 2003, 278:38206-38213.
9. 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., Chalfant C.E. Ceramide 1-phosphate is a direct activator of cytosolic phospholipase A2. J. Biol. Chem. 2004, 279:11320-11326.
10. Hinkovska-Galcheva V., Boxer L.A., Kindzelskii A., Hiraoka M., Abe A., Goparju S., Spiegel S., Petty H.R., Shayman J.A. Ceramide 1-phosphate, a mediator of phagocytosis. J. Biol. Chem. 2005, 280:26612-26621.
11. Hinkovska-Galcheva V.T., Boxer L.A., Mansfield P.J., Harsh D., Blackwood A., Shayman J.A. The formation of ceramide-1-phosphate during neutrophil phagocytosis and its role in liposome fusion. J. Biol. Chem. 1998, 273:33203-33209.
12. Mitsutake S., Kim T.J., Inagaki Y., Kato M., Yamashita T., Igarashi Y. Ceramide kinase is a mediator of calcium-dependent degranulation in mast cells. J. Biol. Chem. 2004, 279:17570-17577.
13. Granado M.H., Gangoiti P., Ouro A., Arana L., Gonzalez M., Trueba M., Gomez-Munoz A. Ceramide 1-phosphate (C1P) promotes cell migration Involvement of a specific C1P receptor. Cell. Signal. 2009, 21:405-412.
14. Lamour N.F., Chalfant C.E. Ceramide-1-phosphate: the "missing" link in eicosanoid biosynthesis and inflammation. Mol. Interv. 2005, 5:358-367.
15. Gomez-Munoz A., Gangoiti P., Granado M.H., Arana L., Ouro A. Ceramide-1-phosphate in Cell Survival and Inflammatory Signaling. Adv Exp Med Biol 2010, 118-130.
16. Gangoiti P., Arana L., Ouro A., Granado M.H., Trueba M., Gomez-Munoz A. Activation of mTOR and RhoA is a major mechanism by which Ceramide 1-phosphate stimulates macrophage proliferation. Cell. Signal. 2010, 23:27-34.
17. Bae Y.S., Kang S.W., Seo M.S., Baines I.C., Tekle E., Chock P.B., Rhee S.G. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J. Biol. Chem. 1997, 272:217-221.
18. 2 for platelet-derived growth factor signal transduction. Science 1995, 270:296-299.
19. Salmeen A., Park B.O., Meyer T. The NADPH oxidases NOX4 and DUOX2 regulate cell cycle entry via a p53-dependent pathway. Oncogene 2010, 29:4473-4484.
20. Hole P.S., Pearn L., Tonks A.J., James P.E., Burnett A.K., Darley R.L., Tonks A. Ras-induced reactive oxygen species promote growth factor-independent proliferation in human CD34+ hematopoietic progenitor cells. Blood 2010, 115:1238-1246.
21. Chowdhury R., Chatterjee R., Giri A.K., Mandal C., Chaudhuri K. Arsenic-induced cell proliferation is associated with enhanced ROS generation, Erk signaling and CyclinA expression. Toxicol. Lett. 2010, 198:263-271.
22. Giordano F.J. Oxygen, oxidative stress, hypoxia, and heart failure. J. Clin. Invest. 2005, 115:500-508.
23. Diehn M., Cho R.W., Lobo N.A., Kalisky T., Dorie M.J., Kulp A.N., Qian D., Lam J.S., Ailles L.E., Wong M., Joshua B., Kaplan M.J., Wapnir I., Dirbas F.M., Somlo G., Garberoglio C., Paz B., Shen J., Lau S.K., Quake S.R., Brown J.M., Weissman I.L., Clarke M.F. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458:780-783.
24. Shimada K., Fujii T., Anai S., Fujiimoto K., Konishi N. ROS generation via NOX4 and its utility in the cytological diagnosis of urothelial carcinoma of the urinary bladder. BMC Urol. 2010, 11:22.
25. Gangoiti P., Granado M.H., Arana L., Ouro A., Gomez-Munoz A. Activation of protein kinase C-alpha is essential for stimulation of cell proliferation by ceramide 1-phosphate. FEBS Lett. 2010, 584:517-524.
26. Lankalapalli R.S., Ouro A., Arana L., Gomez-Munoz A., Bittman R. Caged ceramide 1-phosphate analogues: synthesis and properties. J. Org. Chem. 2009, 74:8844-8847.
27. Hamilton J.A., Myers D., Jessup W., Cochrane F., Byrne R., Whitty G., Moss S. Oxidized LDL can induce macrophage survival, DNA synthesis, and enhanced proliferative response to CSF-1 and GM-CSF. Arterioscler. Thromb. Vasc. Biol. 1999, 19:98-105.
28. Hundal R.S., Salh B.S., Schrader J.W., Gomez-Munoz A., Duronio V., Steinbrecher U.P. Oxidized low density lipoprotein inhibits macrophage apoptosis through activation of the PI 3-kinase/PKB pathway. J. Lipid Res. 2001, 42:1483-1491.
29. Hundal R.S., Gomez-Munoz A., Kong J.Y., Salh B.S., Marotta A., Duronio V., Steinbrecher U.P. Oxidized low density lipoprotein inhibits macrophage apoptosis by blocking ceramide generation, thereby maintaining protein kinase B activation and Bcl-XL levels. J. Biol. Chem. 2003, 278:24399-24408.
30. Gomez-Munoz A., Frago L.M., Alvarez L., Varela-Nieto I. Stimulation of DNA synthesis by natural ceramide 1-phosphate. Biochem. J. 1997, 325(Pt 2):435-440.
31. Gangoiti P., Camacho L., Arana L., Ouro A., Granado M.H., Brizuela L., Casas J., Fabrias G., Abad J.L., Delgado A., Gomez-Munoz A. Control of metabolism and signaling of simple bioactive sphingolipids: implications in disease. Prog. Lipid Res. 2010, 49:316-334.
32. Blanchetot C., Boonstra J. The ROS-NOX connection in cancer and angiogenesis. Crit. Rev. Eukaryot. Gene Expr. 2008, 18:35-45.
33. Chiarugi P., Fiaschi T. Redox signalling in anchorage-dependent cell growth. Cell. Signal. 2007, 19:672-682.
34. Leslie N.R. The redox regulation of PI 3-kinase-dependent signaling. Antioxid. Redox Signal. 2006, 8:1765-1774.
35. Sablina A.A., Budanov A.V., Ilyinskaya G.V., Agapova L.S., Kravchenko J.E., Chumakov P.M. The antioxidant function of the p53 tumor suppressor. Nat. Med. 2005, 11:1306-1313.
36. Zangar R.C., Bollinger N., Weber T.J., Tan R.M., Markillie L.M., Karin N.J. Reactive oxygen species alter autocrine and paracrine signaling. Free Radic. Biol. Med. 2011, 51:2041-2047.
37. Finkel T., Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408:239-247.
38. Novo E., Parola M. Redox mechanisms in hepatic chronic wound healing and fibrogenesis. Fibrogenesis Tissue Repair 2008, 1:5.
39. Manea A. NADPH oxidase-derived reactive oxygen species: involvement in vascular physiology and pathology. Cell Tissue Res. 2010, 342:325-339.
40. Sharma A., Bernatchez P.N., de Haan J.B. Targeting endothelial dysfunction in vascular complications associated with diabetes. Int. J. Vasc. Med. 2011, 2012:750126.
41. Syed I., Kyathanahalli C.N., Jayaram B., Govind S., Rhodes C.J., Kowluru R.A., Kowluru A. Increased phagocyte-like NADPH oxidase and ROS generation in Type 2 diabetic ZDF rat and human islets: role of Rac1-JNK1/2 signaling pathway in mitochondrial dysregulation in the diabetic islet. Diabetes 2011, 60:2843-2852.
42. Lambert A.J., Brand M.D. Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase complex I. J. Biol. Chem. 2004, 279:39414-39420.
43. Schuh R.A., Matthews C.C., Fishman P.S. Interaction of mitochondrial respiratory inhibitors and excitotoxins potentiates cell death in hippocampal slice cultures. J. Neurosci. Res. 2008, 86:3306-3313.
44. Piconi L., Quagliaro L., Assaloni R., Da Ros R., Maier A., Zuodar G., Ceriello A. Constant and intermittent high glucose enhances endothelial cell apoptosis through mitochondrial superoxide overproduction. Diabetes Metab. Res. Rev. 2006, 22:198-203.
45. Orient A., Donko A., Szabo A., Leto T.L., Geiszt M. Novel sources of reactive oxygen species in the human body. Nephrol. Dial. Transplant. 2007, 22:1281-1288.
46. Dworakowski R., Anilkumar N., Zhang M., Shah A.M. Redox signalling involving NADPH oxidase-derived reactive oxygen species. Biochem. Soc. Trans. 2006, 34:960-964.
47. Wei Y., Sowers J., Nistala R., Gong H., Uptergrove G., Clark S., Morris E., Szary N., Manrique C., Stump C. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J. Biol. Chem. 2006, 281:35137-35146.
48. Nauseef W.M. Biological roles for the NOX family NADPH oxidases. J. Biol. Chem. 2008, 283:16961-16965.
49. Matthiesen S., Lindemann D., Warnken M., Juergens U.R., Racke K. Inhibition of NADPH oxidase by apocynin inhibits lipopolysaccharide (LPS) induced up-regulation of arginase in rat alveolar macrophages. Eur. J. Pharmacol. 2008, 579:403-410.
50. Higai K., Satake M., Nishioka H., Azuma Y., Matsumoto K. Glycated human serum albumin enhances macrophage inflammatory protein-1beta mRNA expression through protein kinase C-delta and NADPH oxidase in macrophage-like differentiated U937 cells. Biochim. Biophys. Acta 2008, 1780:307-314.
51. Comalada M., Xaus J., Sanchez E., Valledor A.F., Celada A. Macrophage colony-stimulating factor-, granulocyte-macrophage colony-stimulating factor-, or IL-3-dependent survival of macrophages, but not proliferation, requires the expression of p21(Waf1) through the phosphatidylinositol 3-kinase/Akt pathway. Eur. J. Immunol. 2004, 34:2257-2267.
52. Sancho P., Fabregat I. NADPH oxidase NOX1 controls autocrine growth of liver tumor cells through up-regulation of the epidermal growth factor receptor pathway. J. Biol. Chem. 2010, 285:24815-24824.
53. del Bello B., Paolicchi A., Comporti M., Pompella A., Maellaro E. Hydrogen peroxide produced during gamma-glutamyl transpeptidase activity is involved in prevention of apoptosis and maintenance of proliferation in U937 cells. FASEB J. 1999, 13:69-79.
54. Burdon R.H. Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic. Biol. Med. 1995, 18:775-794.
55. Suzuki Y.J., Forman H.J., Sevanian A. Oxidants as stimulators of signal transduction. Free Radic. Biol. Med. 1997, 22:269-285.
56. Wijesinghe D.S., Subramanian P., Lamour N.F., Gentile L.B., Granado M.H., Szulc Z., Bielawska A., Gomez-Munoz A., Chalfant C.E. 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. 2008, 50:1986-1995.
57. Herbert S.P., Odell A.F., Ponnambalam S., Walker J.H. Activation of cytosolic phospholipase A2-{alpha} as a novel mechanism regulating endothelial cell cycle progression and angiogenesis. J. Biol. Chem. 2009, 284:5784-5796.
58. Caiazza F., Harvey B.J., Thomas W. Cytosolic phospholipase A2 activation correlates with HER2 overexpression and mediates estrogen-dependent breast cancer cell growth. Mol. Endocrinol. 2010, 24:953-968.
59. Nishizuka Y. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 1988, 334:661-665.
60. Ase K., Berry N., Kikkawa U., Kishimoto A., Nishizuka Y. Differential down-regulation of protein kinase C subspecies in KM3 cells. FEBS Lett. 1988, 236:396-400.
61. Huang F.L., Yoshida Y., Cunha-Melo J.R., Beaven M.A., Huang K.P. Differential down-regulation of protein kinase C isozymes. J. Biol. Chem. 1989, 264:4238-4243.
62. Weiss S., Ellis J., Hendley D.D., Lenox R.H. Translocation and activation of protein kinase C in striatal neurons in primary culture: relationship to phorbol dibutyrate actions on the inositol phosphate generating system and neurotransmitter release. J. Neurochem. 1989, 52:530-536.
63. Xing M., Firestein B.L., Shen G.H., Insel P.A. Dual role of protein kinase C in the regulation of cPLA2-mediated arachidonic acid release by P2U receptors in MDCK-D1 cells: involvement of MAP kinase-dependent and -independent pathways. J. Clin. Invest. 1997, 99:805-814.
64. Chakraborti S., Michael J.R., Chakraborti T. Role of an aprotinin-sensitive protease in protein kinase Calpha-mediated activation of cytosolic phospholipase A2 by calcium ionophore (A23187) in pulmonary endothelium. Cell. Signal. 2004, 16:751-762.
65. Wang S.W., Parhar K., Chiu K.J., Tran A., Gangoiti P., Kong J., Gonzalez M., Salh B., Duronio V., Steinbrecher U.P., Gomez-Munoz A. Pertussis toxin promotes macrophage survival through inhibition of acid sphingomyelinase and activation of the phosphoinositide 3-kinase/protein kinase B pathway. Cell. Signal. 2007, 19:1772-1783.