Acid sphingomyelinase promotes endothelial stress response in systemic inflammation and sepsis

Molecular Medicine

Volumn 22, Issue , 2016, Pages 412-423

  Chung, Ha Yeun ^a   Hupe, Daniel C ^a   Otto, Gordon P ^a   Sprenger, Marcel ^a   Bunck, Alexander C ^b   Dorer, Michael J ^a   Bockmeyer, Clemens L ^c   Deigner, Hans Peter ^d,e   Gräler, Markus H ^a   Claus, Ralf A ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^d FURTWANGEN UNIVERSITY   (Germany)

^e FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; DESIPRAMINE; FAS LIGAND; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; VON WILLEBRAND FACTOR CLEAVING PROTEINASE;

ADULT; AGED; ARTICLE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DISEASE SEVERITY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; HYDROLYSIS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LIPID RAFT; MAJOR CLINICAL STUDY; MALE; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; SEPSIS; SIGNAL TRANSDUCTION; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

EID: 84987629345     PISSN: 10761551     EISSN: 15283658     Source Type: Journal    
DOI: 10.2119/molmed.2016.00140     Document Type: Article

References (60)

1. Angus, DC, Pereira, CA and Silva, E (2006) Epidemiology of severe sepsis around the world. Endocr Metab Immune Disord Drug Targets 6(2): 207–12.
2. Deutschman, CS Tracey KJ (2014) Sepsis: current dogma and new perspectives. Immunity 40(4): 463–75.
3. Opal, SM et al. (2014) The next generation of sepsis clinical trial designs: what is next after the demise of recombinant human activated protein C?*. Crit. Care Med. 42(7): 1714–21.
4. Henneke P, Golenbock, DT (2002) Innate immune recognition of lipopolysaccharide by endothelial cells. Crit. Care Med. 30(5 Suppl): S207–13.
5. Schouten, M., et al. (2008) Inflammation, endothelium, and coagulation in sepsis. J. Leukoc. Biol. 83(3): 536–45.
6. Aird, WC (2007) Endothelium as a therapeutic target in sepsis. Curr Drug Targets 8(4): 501–7.
7. Kinasewitz, GT et al. (2005) Prognostic value of a simple evolving disseminated intravascular coagulation score in patients with severe sepsis. Crit. Care Med. 33(10): 2214–21.
8. Bockmeyer, CL et al. (2008) Inflammation-associated ADAMTS13 deficiency promotes formation of ultra-large von Willebrand factor. Haematologica 93(1): 137–140.
9. Gulbins, E et al. (2004) Ceramide, membrane rafts and infections. J Mol. Med. 82(6): 357–63.
10. Claus, RA et al. (2010) Approaching clinical reality: markers for monitoring systemic inflammation and sepsis. Curr Mol. Med. 10(2): 227–35.
11. Marchesini, N and Hannun, YA (2004) Acid and neutral sphingomyelinases: roles and mechanisms of regulation. Biochem Cell Biol 82(1): 27–44.
12. Gulbins, E. and Li, PL (2006) Physiological and pathophysiological aspects of ceramide. Am. J. Physiol. 290(1): R11–26.
13. Jenkins, RW et al. (2010) Regulated secretion of acid sphingomyelinase: implications for selectivity of ceramide formation. J Biol. Chem. 285(46) 35706–18.
14. Miller, ME et al. (2012) Ebolavirus requires acid sphingomyelinase activity and plasma membrane sphingomyelin for infection. J Virol 86(14): 7473–83.
15. Grassme, H, Schwarz H and Gulbins E (2001) Molecular mechanisms of ceramide-mediated CD95 clustering. Biochem. Biophys. Res. Commun. 284(4): 1016–30.
16. Cuschieri, J et al. (2007) Acid sphingomyelinase is required for lipid Raft TLR4 complex formation. Surg Infect. (Larchmt) 8(1): 91–106.
17. Brameshuber, M et al. (2016) Oxidized Phospholipids Inhibit the Formation of Cholesterol-Dependent Plasma Membrane Nanoplatforms. Biophys J 110(1): 205–13.
18. van Blitterswijk, WJ et al. (2003) Ceramide: second messenger or modulator of membrane structure and dynamics? Biochem. J. 369(Pt 2): p. 199–211.
19. Delogu, G et al., (1999) Ceramide concentrations in septic patients: a possible marker of multiple organ dysfunction syndrome. Crit. Care Med. 27(11): 2413–7.
20. Claus, RA, et al. (2005) Plasma platelet-activating factor acetylhydrolase activity in critically ill patients. Crit. Care Med. 33(6): 1416–9.
21. Kott, M et al. (2014) Acid sphingomyelinase serum activity predicts mortality in intensive care unit patients after systemic inflammation: a prospective cohort study. PLoS One 9(11): e112323.
22. Roumestan, C et al. (2007) Anti-inflammatory properties of desipramine and fluoxetine. Respir. Res. 8: 35.
23. Kornhuber, J et al. (2010) Functional Inhibitors of Acid Sphingomyelinase (FIASMAs): a novel pharmacological group of drugs with broad clinical applications. Cell Physiol Biochem 26(1): 9–20.
24. Peng, H et al. (2015) Acid sphingomyelinase inhibition protects mice from lung edema and lethal Staphylococcus aureus sepsis. J Mol. Med. 93(6): 675–89.
25. Arenz, C (2010) Small molecule inhibitors of acid sphingomyelinase. Cell Physiol Biochem 26(1): 1–8.
26. Ekaney, ML et al. (2015) Preserved Expression of mRNA Coding von Willebrand Factor-Cleaving Protease ADAMTS13 by Selenite and Activated Protein C. Mol. Med. 21: 355–63.
27. Loidl, A et al. (2002) High-precision fluorescence assay for sphingomyelinase activity of isolated enzymes and cell lysates. J Lipid Res 43(5): 815–23.
28. Loidl, A et al. (2004) Role of ceramide in activation of stress-associated MAP kinases by minimally modified LDL in vascular smooth muscle cells. Biochim Biophys Acta 1690(2): 150–8.
29. Osawa, Y et al. (2011) Acid sphingomyelinase regulates glucose and lipid metabolism in hepatocytes through AKT activation and AMP-activated protein kinase suppression. FASEB J. 25(4): 1133–44.
30. Ceppi, ED, Smith, FS and itheradge MA (1996) Effect of multiple cytokines plus bacterial endotoxin on glucose and nitric oxide production by cultured hepatocytes. Biochem. J. 317 (Pt 2): 503–7.
31. Deigner, HP et al. (2001) Ceramide induces aSMase expression: implications for oxLDL-induced apoptosis. Faseb J 15(3): 807–14.
32. Martin, OC and Pagano, RE (1994) Internalization and sorting of a fluorescent analogue of glucosylceramide to the Golgi apparatus of human skin fibroblasts: utilization of endocytic and nonendocytic transport mechanisms. J. Cell Biol. 125(4): 769–81.
33. Bligh, EG and Dyer, WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8): 911–7.
34. Ames, BN and Dubin, DT The role of polyamines in the neutralization of bacteriophage deoxyribonucleic acid. J Biol. Chem. 235: 769–75.
35. Blaess, M, Claus, RA and Deigner, HP (2015) HPLC separation and ultrasensitive optical quantification of ceramide species applying 7-(diethylamino)coumarin-3-carbonyl azide derivatisation. J Chromatogr B Analyt Technol Biomed Life Sci. 986–987: 123–8.
36. Sieber, MW et al. (2010) Substantial performance discrepancies among commercially available kits for reverse transcription quantitative polymerase chain reaction: a systematic comparative investigator-driven approach. Anal. Biochem. 401(2): 303–11.
37. Gassert, E et al. (2009) Induction of membrane ceramides: a novel strategy to interfere with T lymphocyte cytoskeletal reorganisation in viral immunosuppression. PLoS Pathog. 5(10): e1000623.
38. American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference: definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit. Care Med., 1992. 20(6): 864–74.
39. Koval, M and Pagano RE, (1991) Intracellular transport and metabolism of sphingomyelin. Biochim Biophys Acta. 1082(2): 113–25.
40. Nikolaeva, S et al. (2014) GM1 and GD1a gangliosides modulate toxic and inflammatory effects of E. coli lipopolysaccharide by preventing TLR4 translocation into lipid rafts. Biochim Biophys Acta.
41. Opal, SM and van der Poll, T (2015) Endothelial barrier dysfunction in septic shock. J. Intern. Med. 277(3): 277–93.
42. Abraham, E and Singer, M (2007) Mechanisms of sepsis-induced organ dysfunction. Crit. Care Med. 35(10): 2408–16.
43. Fernandez, A et al. (2013) ASMase is required for chronic alcohol induced hepatic endoplasmic reticulum stress and mitochondrial cholesterol loading. J Hepatol 59(4): 805–13.
44. Garcia-Ruiz, C et al. (2015) Acid sphingomyelinaseceramide system in steatohepatitis: a novel target regulating multiple pathways. J Hepatol. 62(1): 219–33.
45. Bouis, D et al. (2001) Endothelium in vitro: a review of human vascular endothelial cell lines for blood vessel-related research. Angiogenesis 4(2): 91–102.
46. Vinals, F and Pouyssegur, J (1999) Confluence of vascular endothelial cells induces cell cycle exit by inhibiting p42/p44 mitogen-activated protein kinase activity. Mol. Cell. Biol. 19(4): 2763–72.
47. Regan, ER and Aird, WC (2012) Dynamical systems approach to endothelial heterogeneity. Circ. Res. 111(1): 110–30.
48. Smith, EL and Schuchman, EH (2008) The unexpected role of acid sphingomyelinase in cell death and the pathophysiology of common diseases. FASEB J. 22(10): 3419–31.
49. Moles, A et al. (2010) Acidic sphingomyelinase controls hepatic stellate cell activation and in vivo liver fibrogenesis. Am. J. Pathol. 177(3): 1214–24.
50. Hannun, YA and Obeid, LM (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol. Cell. Biol. 9(2): 139–50.
51. Kok, JW et al. (1995) Fluorescent, short-chain C6-NBD-sphingomyelin, but not C6-NBD-glucosylceramide, is subject to extensive degradation in the plasma membrane: implications for signal transduction related to cell differentiation. Biochem. J. 309 (Pt 3): 905–12.
52. Kolesnick, RN, Goni, FM and Alonso, A (2000) Compartmentalization of ceramide signaling: physical foundations and biological effects. J Cell Physiol. 184(3): 285–300.
53. Olsson, S and Sundler, R (2006) The role of lipid rafts in LPS-induced signaling in a macrophage cell line. Mol. Immunol. 43(6): 607–12.
54. Rotolo, J et al. (2012) Anti-ceramide antibody prevents the radiation gastrointestinal syndrome in mice. J. Clin. Invest. 122(5): 1786–90.
55. Petersen, NH et al. (2013) Transformation-associated changes in sphingolipid metabolism sensitize cells to lysosomal cell death induced by inhibitors of acid sphingomyelinase. Cancer Cell 24(3): 379–93.
56. Chiantia, S et al. (2008) Role of ceramide in membrane protein organization investigated by combined AFM and FCS. Biochim Biophys Acta 1778(5): 1356–64.
57. Zhao, J et al. (2009) Phosphotyrosine protein dynamics in cell membrane rafts of sphingosine-1-phosphate-stimulated human endothelium: Role in barrier enhancement. Cell Signal.
58. Castro-Gomes, T et al. (2016) Plasma Membrane Repair Is Regulated Extracellularly by Proteases Released from Lysosomes. PLoS One 11(3): e0152583.
59. Elojeimy, S et al. (2006) New insights on the use of desipramine as an inhibitor for acid ceramidase. FEBS Lett. 580(19): 4751–6.
60. Der, P, Cui, J and Das, DK (2006) Role of lipid rafts in ceramide and nitric oxide signaling in the ischemic and preconditioned hearts. J Mol Cell Cardiol. 40(2): 313–20.