Lipopolysaccharide induces disseminated endothelial apoptosis requiring ceramide generation

Journal of Experimental Medicine

Volumn 186, Issue 11, 1997, Pages 1831-1841

  Haimovitz Friedman, Adriana ^a   Cordon Cardo, Carlos ^a   Bayoumy, Shariff ^a   Garzotto, Mark ^a   McLoughlin, Maureen ^a   Gallily, Ruth ^a   Edwards III, Carl K ^b   Schuchman, Edward H ^c   Fuks, Zvi ^a   Kolesnick, Richard ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b AMGEN INC   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; CERAMIDE; LIPOPOLYSACCHARIDE; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; SPHINGOMYELIN PHOSPHODIESTERASE; TUMOR NECROSIS FACTOR BINDING PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARBOHYDRATE ANALYSIS; CELL SURVIVAL; CONTROLLED STUDY; ENDOTHELIUM CELL; IMMUNOPATHOLOGY; INTRAVENOUS DRUG ADMINISTRATION; MOUSE; MULTIPLE ORGAN FAILURE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SEPTIC SHOCK;

ADIPOSE TISSUE; ANIMALS; APOPTOSIS; CAPILLARIES; CARRIER PROTEINS; CERAMIDES; ENDOTHELIUM, VASCULAR; FIBROBLAST GROWTH FACTOR 2; INTESTINAL MUCOSA; LIPOPOLYSACCHARIDES; LUNG; MICE; MICE, INBRED C57BL; RECEPTORS, TUMOR NECROSIS FACTOR; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SHOCK, SEPTIC; SIGNAL TRANSDUCTION; SPECIFIC PATHOGEN-FREE ORGANISMS; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELINS; THYMUS GLAND; TUMOR NECROSIS FACTOR DECOY RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0030784482     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.186.11.1831     Document Type: Article

References (62)

1. Morrison, D.C., and J.L. Ryan. 1987. Endotoxins and disease mechanisms. Ann. Rev. Med. 38:417-432.
2. Bone, R.C. 1991. Sepsis, the sepsis syndrome, multi-organ failure: a plea for comparable definitions. Ann. Int. Med. 114: 332-333.
3. Tracey, K.J., and S.F. Lowry. 1990. The role of cytokine mediators in septic shock. Adv. Snrg. 23:21-56.
4. Beutler, B., I.W. Milsark, and A.C. Cerami. 1985. Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science (Wash. DC). 229:869-871.
5. Tracey, K.J., B. Beutler, S.F. Lowry, J. Merryweather, S. Wolpe, I.W. Milsark, R.J. Hariri, T.J. Fahey III, A. Zentella, J.D. Albert et al. 1986. Shock and tissue injury induced by recombinant human Cachectin. Science (Wash. DC). 234:470-474.
6. Mathison, J.C., E. Wolfson, and R.J. Ulevitch. 1988. Participation of tumor necrosis factor in the mediation of gram negative bacterial lipopolysaccharide-induced injury in rabbits. J. Clin. Invest. 81:1925-1937.
7. Lesslauer, W., H. Tabuchi, R. Gentz, M. Brockhaus, E.J. Schlaeger, G. Grau, P.F. Piguet, P. Pointaire, P. Vassalli, and H. Loetscher. 1991. Recombinant soluble tumor necrosis factor receptor proteins protect mice from lipopolysaccharide-induced lethality. Eur. J. Immunol. 21:2883-2886.
8. Hale, K.K., C.G. Smith, S.L. Baker, R.W. Vanderslice, C.H Squires, T.M. Gleason, K.K. Tucker, T. Kohno, and D.A. Russell. 1995. Multifunctional regulation of the biological effects of TNF-alpha by the soluble type I and type II TNF receptors. Cytokine. 7:26-38.
9. Russell, D.A., K.K. Tucker, N. Chinookoswong, R.C. Thompson, and T. Kohno. 1995. Combined inhibition of interleukin-1 and tumor necrosis factor in rodent endotoxemia: improved survival and organ function. J. Infect. Dis. 171:1528-1538.
10. Van Zee, K., L. Moldawer, H. Oldenburg, W. Thompson, S. Stackpole, W. Montegut, M. Rogy, C. Meschter, H. Gallati, C. Schiller et al. 1996. Protection against lethal Escherichia coli bacteremia in baboons (Papio anubis) by pretreatment with a 55-kD TNF receptor (CD120a)-Ig fusion protein, Ro 45-2081. J. Immunol. 156:2221-2230.
11. Espat, N.J., J.C. Cendan, E.A. Beierle, T.A. Auffenberg, J. Rosenberg, D. Russell, J.S. Kenney, E. Fischer, W. Montegut, S.F. Lowry et al. 1995. PEG-BP-30 monotherapy attenuates the cytokine-mediated inflammatory cascade in baboon Escherichia coli septic shock. J. Surg. Res. 59:153-158.
12. Rothe, J., W. Lesslauer, H. Lotscher, Y. Lang, P. Koebel, F. Kontgen, A. Althage, R. Zinkernagel, M. Steinmetz, and H. Bluethmann. 1993. Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly-susceptible to infection by Listeria monocytogenes. Nature (Lond.). 364:798-802.
13. Pfeffer, K., T. Matsuyama, T.M. Kundig, A. Wakeham, K. Kishihara, A. Shahinian, K. Wiegmann, P.S. Ohashi, M. Kronke, and T.W. Mak. 1993. Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell. 73: 457-467.
14. Merrill, J.-A.H., and D.D. Jones. 1990. An update of the enzymology and regulation of sphingomyelin metabolism. Biochim. Biophys. Acta. 1044:1-12.
15. Kolesnick, R.N. 1991. Sphingomyelin and derivatives as cellular signals. Prog. Lipid. Res. 30:1-38.
16. Horinouchi, K., S. Erlich, D.P. Perl, K. Ferlinz, C.L. Bisgaier, K. Sandhoff, R.J. Desnick, C.L. Stewart, and E.H. Schuchman. 1995. Acid sphingomyelinase deficient mice: a model of types A and B Niemann-Pick disease. Nat. Genet. 10:288-293.
17. Spiegel, S., D.A. Foster, and R.N. Kolesnick. 1996. Signal tranduction through lipid second messengers. Curr. Opin. Cell Biol. 8:159-167.
18. Ballon, L.R., S.J.F. Laulederkind, E.F. Rosloniec, and R. Raghow. 1996. Ceramide signalling and the immune response. Biochim. Biophys. Acta. 1301:273-287.
19. Hannun, Y.A. 1996. Function of ceramide in coordinating cellular responses to stress. Science (Wash. DC). 274:1855-1859.
20. Jarvis, W.D., R.N. Kolesnick, F.A. Fornari, R.S. Traylor, D.A. Gewirtz, and S. Grant. 1994. Induction of apoptotic DNA damage and cell death by activation of the sphingomyelin pathway. Proc. Natl. Acad. Sci. USA. 91:73-77.
21. Obeid, L.M., C.M. Linardic, L.A. Karolak, and Y.A. Hannun. 1993. Programmed cell death induced by ceramide. Science (Wash. DC). 259:1769-1771.
22. Cai, Z., M. Korner, N. Tarantino, and S. Chouaib. 1997. IkappaB alpha overexpression in human breast carcinoma MCF7 cells inhibits nuclear factor-kappaB activation but not tumor necrosis factor-alpha-induced apoptosis. J. Biol. Chem. 272:96-101.
23. Cifone, M.G., R. DeMaria, P. Roncaioli, M.R. Rippo, M. Azuma, L.L. Lanier, A. Santoni, and R. Testi. 1994. Apoptotic signaling through CD95 (Fas/Apo-1) activates an acidic sphingomyelinase. J. Exp. Med. 177:1547-1552.
24. Cifone, M.G., P. Roncaioli, R. De Maria, G. Camarda, A. Santoni, G. Ruberti, and R. Testi. 1995. Multiple pathways originate at the Fas/APO-1 (CD95) receptor: sequential involvement of phosphaddylcholine-specific phospholipase C and acidic sphingomyelinase in the propagation of the apoptotic signal. EMBO (Eur. Mol. Biol. Organ.) J. 14:5859-5868.
25. Gulbins, E., R. Bissonnette, A. Mahboubi, S. Martin, W. Nishioka, T. Brunner, G. Baier, G. Bitterlich-Baier, C. Byrd, F. Lang et al. 1995. Fas-induced apoptosis is mediated by a ceramide-initiated Ras signaling pathway. Immunity. 2:341-351.
26. Verheij, M., R. Bose, X.H. Lin, B. Yao, W.D. Jarvis, S. Grant, M.J. Birrer, E. Szabo, L.I. Zon, J.M. Kyriakis et al. 1996. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature (Lond.). 380:75-79.
27. Haimovitz-Friedman, A., C.C. Kan, D. Ehleiter, R.S. Persaud, M. McLoughlin, Z. Fuks, and R.N. Kolesnick. 1994. Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J. Exp. Med. 180:525-535.
28. Chmura, S.J., E. Nodzenski, M.A. Beckett, D.W. Kufe, J. Quintans, and R.R. Weichselbaum. 1997. Loss of ceramide production confers resistance to radiation-induced apoptosis. Cancer Res. 57:1270-1275.
29. Santana, P., L.A. Pena, A. Haimovitz-Friedman, S. Martin, D. Green, M. McLoughlin, C. Cordon-Cardo, E.H. Schuchman, Z. Fuks, and R. Kolesnick. 1996. Acid sphingomyelinase-deficient human lymphoblasts and mice are defective in radiation-induced apoptosis. Cell. 86:189-199.
30. Kaplan, E., and P. Meier. 1958. Nonparametric estimation from incomplete observations. J. Am. Statist. Assoc. 53:457-816.
31. Fuks, Z., R.S. Persaud, A. Alfieri, M. McLoughlin, D. Ehleiter, J.L. Schwartz, A.P. Seddon, C. Cordon-Cardo, and A. Haimovitz-Friedman. 1994. Basic fibroblast growth factor protects endothelial cells against radiation-induced programmed cell death in vitro and in vivo. Cancer Res. 54:2582-2590.
32. Mantel, N. 1966. Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemother. Rep. 50:163-170.
33. Vecchi, A., C. Garlanda, M. Lampugnani, M. Resnati, C. Matteucci, A. Stoppacciaro, H. Schnurch, W. Risau, L. Ruco, and A. Mantovani. 1994. Monoclonal antibodies specific for endothelial cells of mouse bloodvessels. Their application in the identification of adult and embryonic endothelium. Eur. J. Cell biol. 63:247-254.
34. Colagiovanni, D.B., R.J. Evans, J.M. McCabe, A.M. Bendele, and C.K. Edwards III. 1997. Protection of fas mutant MRL-lpr/lpr mice to LPS or Staphylococcal enterotoxin B-induced septic shock by tumor necrosis factor binding protein (TNF-bp). In press.
35. Solorzano, C.C., R. Ksontini, J.H. Pruitt, P.J. Hess, P.D. Edwards, A. Kaibara, A. Abouhamze, T. Auffenberg, R.E. Galardy, J.N. Vauthey et al. 1997. Involvement of 26-kD cell-associated TNF-alpha in experimental hepatitis and exacerbation of liver injury with a matrix metalloproteinase inhibitor. J. Immunol. 158:414-419.
36. Fuks, Z., A. Alfieri, A. Haimovitz-Friedman, A. Seddon, and C. Cordon-Cardo. 1995. Intravenous basic fibroblast growth factor protects the lung but not mediastinal organs against radiation-induced apoptosis in vivo. Cancer J. 1:62-72.
37. Takei, Y., S. Kawano, Y. Nishimura, M. Goto, H. Nagai, S.S. Chen, A. Omae, H. Fusamoto, T. Kamada, K. Ikeda et al. 1995. Apoptosis: a new mechanism of endothelial and Kupffer cell killing. J. Gastroenterol. Hepatol. 10:S65-S67.
38. Eissner, G., F. Kohlhuber, M. Grell, M. Ueffing, P. Scheurich, A. Hieke, G. Multhoff, G.W. Bornkamm, and E. Holler. 1995. Critical involvement of transmembrane tumor necrosis factor-alpha in endothelial programmed cell death mediated by ionizing radiation and bacterial endotoxin. Blood. 86:4184-4193.
39. Xu, D.Z., Q. Lu, G.M. Swank, and E.A. Deitch. 1996. Effect of heat shock and endotoxin stress on enterocyte viability apoptosis and function varies based on whether the cells are exposed to heat shock or endotoxin first. Arch. Surg. 131: 1222-1228.
40. Buchman, T.G., P.A. Abello, E.H. Smith, and G.B. Bulkley. 1993. Induction of heat shock response leads to apoptosis in endothelial cells previously exposed to endotoxin. Am. J. Physiol. 265:165-170.
41. Hoyt, D.G., R.J. Mannix, J.M. Rusnak, B.R. Pitt, and J.S. Lazo. 1995. Collagen is a survival factor against LPS-induced apoptosis in cultured sheep pulmonary artery endothelial cells. Am. J. Physiol. 269:171-177.
42. Hoyt, D.G., R.J. Mannix, M.E. Gerritsen, S.C. Watkins, J.S. Lazo, and D.R. Pitt. 1996. Integrins inhibit LPS-induced DNA strand breakage in cultured lung endothelial cells. Am. J. Physiol. 270:689-694.
43. Tartaglia, L., T. Ayres, G. Wong, and D. Goeddel. 1993. A novel domain within the 55 kd TNF receptor signals cell death. Cell. 74:845-853.
44. Hsu, H., J. Xiong, and D.V. Goeddel. 1995. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell. 81:495-504.
45. Hsu, H., H.B. Shu, M.G. Pan, and D.V. Goeddel. 1996. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell. 84:299-308.
46. Chinnaiyan, A.M., K. O'Rourke, M. Tewari, and V.M. Dixit. 1995. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell. 81:505-512.
47. Chinnaiyan, A.M., C.G. Tepper, M.F. Seldin, K. O'Rourke, F.C. Kischkel, S. Hellbardt, P.H. Krammer, M.E. Peter, and V.M. Dixit. 1996. FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem. 271:4961-4965.
48. Boldin, M.P., T.M. Goncharov, Y.V. Goltsev, and D. Wallach. 1996. Involvement of MACH, a novel MORT1/ FADD-interacting protease, in Fas/APO-1-and TNF receptor-induced cell death. Cell. 85:803-15.
49. Boldin, M.P., I.L. Mett, E.E. Varfolomeev, I. Chumakov, Y. Shemer-Avni, J.H. Camonis, and D. Wallach. 1995. Self-association of the "death domains" of the p55 tumor necrosis factor (TNF) receptor and Fas/APO1 prompts signaling for TNF and Fas/APO1 effects. J. Biol. Chem. 270:387-391.
50. Chinnaiyan, A.M., K. Orth, K. O'Rourke, H. Duan, G.G. Poirier, and V.M. Dixit. 1996. Molecular ordering of the cell death pathway. Bcl-2 and Bcl-xL function upstream of the CED-3-like apoptotic proteases. J. Biol. Chem, 271:4573-4576.
51. Muzio, M., A.M. Chinnaiyan, F.C. Kischkel, K. Orourke, A. Shevchenko, J. Ni, C. Scaffidi, J.D. Bretz, M. Zhang, R. Gentz et al. 1996. FLICE, a novel FADD-homologous ICE/ CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell. 85:817-827.
52. Kischkel, F.C., S. Hellbardt, I. Behrmann, M. Germer, M. Pawlita, P.H. Krammer, and M.E. Peter. 1995. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO (Eur. Mol. Biol. Organ.) J. 14:5579-5588.
53. Wiegmann, K., S. Schutze, T. Machleidt, D. Witte, and M. Kronke. 1994. Functional dichotomy of neutral and acidic sphingomyelinases in tumor necrosis factor signaling. Cell. 78:1005-1015.
54. Pronk, G.J., K. Ramer, P. Amiri, and L.T. Williams. 1996. Requirement of an ICE-like protease for induction of apoptosis and ceramide generation by REAPER. Science (Wash. DC). 271:808-810.
55. Susin, S.A., N. Zamzami, M. Castedo, T. Hirsch, P. Marchetti, A. Macho, E. Daugas, M. Geuskens, and G. Kroemer. 1996. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184:1331-1341.
56. Pastorino, J., G. Simbula, K. Yamamoto, P.J. Glascott, R. Rothman, and J. Farber. 1996. The cytotoxicity of tumor necrosis factor depends on induction of the mitochondrial permeability transition. J. Biol. Chem. 271:29792-29798.
57. Liu, X.S., C.N. Kim, J. Yang, R. Jemmerson, and X.D. Wang. 1996. Induction of apoptotic program in cell-free extracts - requirement for datp and cytochrome C. Cell. 86: 147-157.
58. Kluck, R.M., E. Bossywetzel, D.R. Green, and D.D. Newmeyer. 1997. The release of cytochrome C from mitochondria - a primary site for Bcl-2 regulation of apoptosis. Science (Wash. DC). 275:1132-1136.
59. Yang, J., X.S. Liu, K. Bhalla, C.N. Kim, A.M. Ibrado, J.Y. Cai, T.I. Peng, D.P. Jones, and X.D. Wang. 1997. Prevention of apoptosis by Bcl-2 - release of cytochrome C from mitochondria blocked. Science (Wash. DC). 275:1129-1132.
60. Castedo, M., T. Hirsch, S. Susin, N. Zamzami, P. Marchetti, A. Macho, and G. Kroemer. 1996. Sequential acquisition of mitochondrial and plasma membrane alterations during early lymphocyte apoptosis. J. Immunol. 157:512-521.
61. Zhang, K.Z., J.A. Westberg, E. Holtta, and L.C. Andersson. 1996. Bcl-2 regulates neural differentiation. Prof. Natl. Acad. Sci. USA. 93:4504-4508.
62. Martin, S.J., S. Takayama, A.J. McGahon, T. Miyashita, J. Corbeil, R.N. Kolesnick, J.C. Reed, and D.R. Green. 1995. Inhibition of ceramide-induced apoptosis by Bcl-2. Cell Death Differ. 2:253-257.