Palmitoyl protein thioesterase 1 modulates tumor necrosis factor α-induced apoptosis

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1793, Issue 7, 2009, Pages 1250-1258

  Tardy, Claudine ^a   Sabourdy, Frédérique ^a,b,c   Garcia, Virginie ^a,b   Jalanko, Anu ^d   Therville, Nicole ^a,b   Levade, Thierry ^a,b,c   Andrieu Abadie, Nathalie ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c CHU PURPAN   (France)

^d NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

Apoptosis; Cell death; Lysosome; Neuronal ceroid lipofuscinosis; Palmitoylation

Indexed keywords

CASPASE 3; CASPASE 8; CELL PROTEIN; CYTOCHROME C; DEATH RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PALMITOYL PROTEIN THIOESTERASE; PALMITOYL PROTEIN THIOESTERASE 1; PROTEIN BID; PROTEIN CLN3; PROTEIN CLN5; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; STAUROSPORINE; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL TRANSFORMATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; EMBRYO; ENZYME ACTIVATION; FIBROBLAST; HUMAN; HUMAN CELL; MOUSE; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN SECRETION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL TRANSFORMATION, NEOPLASTIC; FIBROBLASTS; FLOW CYTOMETRY; HUMANS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MOLECULAR CHAPERONES; NEURONAL CEROID-LIPOFUSCINOSES; NF-KAPPA B; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SKIN; THIOLESTER HYDROLASES; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR NECROSIS FACTOR-ALPHA;

MUS;

EID: 67649390792     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2009.03.007     Document Type: Article

References (75)

1. Baud V., and Karin M. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol. 11 (2001) 372-377
2. Chen G., and Goeddel D.V. TNF-R1 signaling: a beautiful pathway. Science 296 (2002) 1634-1635
3. Wajant H., Pfizenmaier K., and Scheurich P. Tumor necrosis factor signaling. Cell Death Differ. 10 (2003) 45-65
4. Muppidi J.R., Tschopp J., and Siegel R.M. Life and death decisions: secondary complexes and lipid rafts in TNF receptor family signal transduction. Immunity 21 (2004) 461-465
5. Beyaert R., Van Loo G., Heyninck K., and Vandenabeele P. Signaling to gene activation and cell death by tumor necrosis factor receptors and Fas. Int. Rev. Cyt. 214 (2002) 225-272
6. Dempsey P.W., Doyle S.E., He J.Q., and Cheng G. The signaling adaptors and pathways activated by TNF superfamily. Cytokine Growth Factor Rev. 14 (2003) 193-209
7. Micheau O., and Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114 (2003) 181-190
8. Schneider-Brachert W., Tchikov V., Neumeyer J., Jakob M., Winoto-Morbach S., Held-Feindt J., Heinrich M., Merkel O., Ehrenschwender M., Adam D., Mentlein R., Kabelitz D., and Schutze S. Compartmentalization of TNF receptor 1 signaling: internalized TNF receptosomes as death signaling vesicles. Immunity 21 (2004) 415-428
9. Legler D.F., Micheau O., Doucey M.A., Tschopp J., and Bron C. Recruitment of TNF receptor 1 to lipid rafts is essential for TNFalpha-mediated NF-kappaB activation. Immunity 18 (2003) 655-664
10. Schutze S., Tchikov V., and Schneider-Brachert W. Regulation of TNFR1 and CD95 signalling by receptor compartmentalization. Nat. Rev., Mol. Cell Biol. 9 (2008) 655-662
11. Tardy C., Codogno P., Autefage H., Levade T., and Andrieu-Abadie N. Lysosomes and lysosomal proteins in cancer cell death (new players of an old struggle). Biochim. Biophys. Acta 1765 (2006) 101-125
12. Heinrich M., Wickel M., Schneider-Brachert W., Sandberg C., Gahr J., Schwandner R., Weber T., Saftig P., Peters C., Brunner J., Kronke M., and Schutze S. Cathepsin D targeted by acid sphingomyelinase-derived ceramide. EMBO J. 18 (1999) 5252-5263
13. Heinrich M., Neumeyer J., Jakob M., Hallas C., Tchikov V., Winoto-Morbach S., Wickel M., Schneider-Brachert W., Trauzold A., Hethke A., and Schutze S. Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and -3 activation. Cell Death Differ. 11 (2004) 550-563
14. Nilsson C., Johansson U., Johansson A.C., Kagedal K., and Ollinger K. Cytosolic acidification and lysosomal alkalinization during TNF-alpha induced apoptosis in U937 cells. Apoptosis 11 (2006) 1149-1159
15. Guicciardi M.E., Miyoshi H., Bronk S.F., and Gores G.J. Cathepsin B knockout mice are resistant to tumor necrosis factor-alpha-mediated hepatocyte apoptosis and liver injury: implications for therapeutic applications. Am. J. Pathol. 159 (2001) 2045-2054
16. Fehrenbacher N., Gyrd-Hansen M., Poulsen B., Felbor U., Kallunki T., Boes M., Weber E., Leist M., and Jaattela M. Sensitization to the lysosomal cell death pathway upon immortalization and transformation. Cancer Res. 64 (2004) 5301-5310
17. Foghsgaard L., Wissing D., Mauch D., Lademann U., Bastholm L., Boes M., Elling F., Leist M., and Jaattela M. Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J. Cell Biol. 153 (2001) 999-1010
18. Mathiasen I.S., Hansen C.M., Foghsgaard L., and Jaattela M. Sensitization to TNF-induced apoptosis by 1,25-dihydroxy vitamin D(3) involves up-regulation of the TNF receptor 1 and cathepsin B. Int. J. Cancer 93 (2001) 224-231
19. Taha T.A., Kitatani K., Bielawski J., Cho W., Hannun Y.A., and Obeid L.M. Tumor necrosis factor induces the loss of sphingosine kinase-1 by a cathepsin B-dependent mechanism. J. Biol. Chem. 280 (2005) 17196-17202
20. Liu J., Guo Q., Chen B., Yu Y., Lu H., and Li Y.Y. Cathepsin B and its interacting proteins, bikunin and TSRC1, correlate with TNF-induced apoptosis of ovarian cancer cells OV-90. FEBS Lett. 580 (2006) 245-250
21. Miao Q., Sun Y., Wei T., Zhao X., Zhao K., Yan L., Zhang X., Shu H., and Yang F. Chymotrypsin B cached in rat liver lysosomes and involved in apoptotic regulation through a mitochondrial pathway. J. Biol. Chem. 283 (2008) 8218-8228
22. Cho S., and Dawson G. Palmitoyl protein thioesterase 1 protects against apoptosis mediated by Ras-Akt-caspase pathway in neuroblastoma cells. J. Neurochem. 74 (2000) 1478-1488
23. Cho S., Dawson P.E., and Dawson G. Antisense palmitoyl protein thioesterase 1 (PPT1) treatment inhibits PPT1 activity and increases cell death in LA-N-5 neuroblastoma cells. J. Neurosci. Res. 62 (2000) 234-240
24. Zhang Z., Butler J.D., Levin S.W., Wisniewski K.E., Brooks S.S., and Mukherjee A.B. Lysosomal ceroid depletion by drugs: therapeutic implications for a hereditary neurodegenerative disease of childhood. Nat. Med. 7 (2001) 478-484
25. Hellsten E., Vesa J., Olkkonen V.M., Jalanko A., and Peltonen L. Human palmitoyl protein thioesterase: evidence for lysosomal targeting of the enzyme and disturbed cellular routing in infantile neuronal ceroid lipofuscinosis. EMBO J. 15 (1996) 5240-5245
26. Verkruyse L.A., and Hofmann S.L. Lysosomal targeting of palmitoyl-protein thioesterase. J. Biol. Chem. 271 (1996) 15831-15836
27. Camp L.A., Verkruyse L.A., Afendis S.J., Slaughter C.A., and Hofmann S.L. Molecular cloning and expression of palmitoyl-protein thioesterase. J. Biol. Chem. 269 (1994) 23212-23219
28. Vesa J., Hellsten E., Verkruyse L.A., Camp L.A., Rapola J., Santavuori P., Hofmann S.L., and Peltonen L. Mutations in the palmitoyl protein thioesterase gene causing infantile neuronal ceroid lipofuscinosis. Nature 376 (1995) 584-587
29. Riikonen R., Vanhanen S.L., Tyynela J., Santavuori P., and Turpeinen U. CSF insulin-like growth factor-1 in infantile neuronal ceroid lipofuscinosis. Neurology 54 (2000) 1828-1832
30. Haltia M. The neuronal ceroid-lipofuscinoses. J. Neuropathol. Exp. Neurol. 62 (2003) 1-13
31. Mitchison H.M., Lim M.J., and Cooper J.D. Selectivity and types of cell death in the neuronal ceroid lipofuscinoses. Brain Pathol. 14 (2004) 86-96
32. Gupta P., Soyombo A.A., Atashband A., Wisniewski K.E., Shelton J.M., Richardson J.A., Hammer R.E., and Hofmann S.L. Disruption of PPT1 or PPT2 causes neuronal ceroid lipofuscinosis in knockout mice. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 13566-13571
33. Jalanko A., Vesa J., Manninen T., von Schantz C., Minye H., Fabritius A.L., Salonen T., Rapola J., Gentile M., Kopra O., and Peltonen L. Mice with Ppt1Deltaex4 mutation replicate the INCL phenotype and show an inflammation-associated loss of interneurons. Neurobiol. Dis. 18 (2005) 226-241
34. Kielar C., Maddox L., Bible E., Pontikis C.C., Macauley S.L., Griffey M.A., Wong M., Sands M.S., and Cooper J.D. Successive neuron loss in the thalamus and cortex in a mouse model of infantile neuronal ceroid lipofuscinosis. Neurobiol. Dis. 25 (2007) 150-162
35. Chatelut M., Harzer K., Christomanou H., Feunteun J., Pieraggi M.T., Paton B.C., Kishimoto Y., O'Brien J.S., Basile J.P., Thiers J.C., Salvayre R., and Levade T. Model SV40-transformed fibroblast lines for metabolic studies of human prosaposin and acid ceramidase deficiencies. Clin. Chim. Acta 262 (1997) 61-76
36. Mitchison H.M., Bernard D.J., Greene N.D., Cooper J.D., Junaid M.A., Pullarkat R.K., de Vos N., Breuning M.H., Owens J.W., Mobley W.C., Gardiner R.M., Lake B.D., Taschner P.E., and Nussbaum R.L. Targeted disruption of the Cln3 gene provides a mouse model for Batten disease. The Batten Mouse Model Consortium [corrected]. Neurobiol. Dis. 6 (1999) 321-334
37. Kopra O., Vesa J., von Schantz C., Manninen T., Minye H., Fabritius A.L., Rapola J., van Diggelen O.P., Saarela J., Jalanko A., and Peltonen L. A mouse model for Finnish variant late infantile neuronal ceroid lipofuscinosis, CLN5, reveals neuropathology associated with early aging. Hum. Mol. Genet. 13 (2004) 2893-2906
38. Denizot F., and Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods 89 (1986) 271-277
39. van Diggelen O.P., Keulemans J.L., Winchester B., Hofman I.L., Vanhanen S.L., Santavuori P., and Voznyi Y.V. A rapid fluorogenic palmitoyl-protein thioesterase assay: pre- and postnatal diagnosis of INCL. Mol. Genet. Metab. 66 (1999) 240-244
40. Vandenabeele P., Declercq W., Beyaert R., and Fiers W. Two tumour necrosis factor receptors: structure and function. Trends Cell Biol. 5 (1995) 392-399
41. Haltia M. The neuronal ceroid-lipofuscinoses: from past to present. Biochim. Biophys. Acta 1762 (2006) 850-856
42. Lu J.Y., Verkruyse L.A., and Hofmann S.L. Lipid thioesters derived from acylated proteins accumulate in infantile neuronal ceroid lipofuscinosis: correction of the defect in lymphoblasts by recombinant palmitoyl-protein thioesterase. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 10046-10050
43. Camp L.A., and Hofmann S.L. Purification and properties of a palmitoyl-protein thioesterase that cleaves palmitate from H-Ras. J. Biol. Chem. 268 (1993) 22566-22574
44. Stoka V., Turk B., Schendel S.L., Kim T.H., Cirman T., Snipas S.J., Ellerby L.M., Bredesen D., Freeze H., Abrahamson M., Bromme D., Krajewski S., Reed J.C., Yin X.M., Turk V., and Salvesen G.S. Lysosomal protease pathways to apoptosis. Cleavage of bid, not pro-caspases, is the most likely route. J. Biol. Chem. 276 (2001) 3149-3157
45. Ahtiainen L., Van Diggelen O.P., Jalanko A., and Kopra O. Palmitoyl protein thioesterase 1 is targeted to the axons in neurons. J. Comp. Neurol. 455 (2003) 368-377
46. Smotrys J.E., and Linder M.E. Palmitoylation of intracellular signaling proteins: regulation and function. Annu. Rev. Biochem. 73 (2004) 559-587
47. Resh M.D. Palmitoylation of ligands, receptors, and intracellular signaling molecules. Sci. STKE 2006 (2006) re14
48. Linder M.E., and Deschenes R.J. Palmitoylation: policing protein stability and traffic. Nat. Rev., Mol. Cell Biol. 8 (2007) 74-84
49. Ko Y.G., Lee J.S., Kang Y.S., Ahn J.H., and Seo J.S. TNF-alpha-mediated apoptosis is initiated in caveolae-like domains. J. Immunol. 162 (1999) 7217-7223
50. Veldman R.J., Maestre N., Aduib O.M., Medin J.A., Salvayre R., and Levade T. A neutral sphingomyelinase resides in sphingolipid-enriched microdomains and is inhibited by the caveolin-scaffolding domain: potential implications in tumour necrosis factor signalling. Biochem. J. 355 (2001) 859-868
51. Cottin V., Doan J.E., and Riches D.W. Restricted localization of the TNF receptor CD120a to lipid rafts: a novel role for the death domain. J. Immunol. 168 (2002) 4095-4102
52. Brown D.A., and London E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14 (1998) 111-136
53. Simons K., and Toomre D. Lipid rafts and signal transduction. Nat. Rev., Mol. Cell Biol. 1 (2000) 31-39
54. Chakrabandhu K., Herincs Z., Huault S., Dost B., Peng L., Conchonaud F., Marguet D., He H.T., and Hueber A.O. Palmitoylation is required for efficient Fas cell death signaling. EMBO J. 26 (2007) 209-220
55. Feig C., Tchikov V., Schutze S., and Peter M.E. Palmitoylation of CD95 facilitates formation of SDS-stable receptor aggregates that initiate apoptosis signaling. EMBO J. 26 (2007) 221-231
56. Lee K.H., Feig C., Tchikov V., Schickel R., Hallas C., Schutze S., Peter M.E., and Chan A.C. The role of receptor internalization in CD95 signaling. EMBO J. 25 (2006) 1009-1023
57. Schneider-Brachert W., Tchikov V., Merkel O., Jakob M., Hallas C., Kruse M.L., Groitl P., Lehn A., Hildt E., Held-Feindt J., Dobner T., Kabelitz D., Kronke M., and Schutze S. Inhibition of TNF receptor 1 internalization by adenovirus 14.7K as a novel immune escape mechanism. J. Clin. Invest. 116 (2006) 2901-2913
58. Ahtiainen L., Luiro K., Kauppi M., Tyynela J., Kopra O., and Jalanko A. Palmitoyl protein thioesterase 1 (PPT1) deficiency causes endocytic defects connected to abnormal saposin processing. Exp. Cell Res. 312 (2006) 1540-1553
59. Lyly A., Marjavaara S.K., Kyttala A., Uusi-Rauva K., Luiro K., Kopra O., Martinez L.O., Tanhuanpaa K., Kalkkinen N., Suomalainen A., Jauhiainen M., and Jalanko A. Deficiency of the INCL protein Ppt1 results in changes in ectopic F1-ATP synthase and altered cholesterol metabolism. Hum. Mol. Genet. 17 (2008) 1406-1417
60. Ahtiainen L., Kolikova J., Mutka A.L., Luiro K., Gentile M., Ikonen E., Khiroug L., Jalanko A., and Kopra O. Palmitoyl protein thioesterase 1 (Ppt1)-deficient mouse neurons show alterations in cholesterol metabolism and calcium homeostasis prior to synaptic dysfunction. Neurobiol. Dis. 28 (2007) 52-64
61. Goswami R., Ahmed M., Kilkus J., Han T., Dawson S.A., and Dawson G. Differential regulation of ceramide in lipid-rich microdomains (rafts): antagonistic role of palmitoyl:protein thioesterase and neutral sphingomyelinase 2. J. Neurosci. Res. 81 (2005) 208-217
62. Trent II J.C., McConkey D.J., Loughlin S.M., Harbison M.T., Fernandez A., and Ananthaswamy H.N. Ras signaling in tumor necrosis factor-induced apoptosis. EMBO J. 15 (1996) 4497-4505
63. Paumen M.B., Ishida Y., Muramatsu M., Yamamoto M., and Honjo T. Inhibition of carnitine palmitoyltransferase I augments sphingolipid synthesis and palmitate-induced apoptosis. J. Biol. Chem. 272 (1997) 3324-3329
64. Wiegmann K., Schutze S., Machleidt T., Witte D., and Kronke M. Functional dichotomy of neutral and acidic sphingomyelinases in tumor necrosis factor signaling. Cell 78 (1994) 1005-1015
65. Cooper J.D., Russell C., and Mitchison H.M. Progress towards understanding disease mechanisms in small vertebrate models of neuronal ceroid lipofuscinosis. Biochim. Biophys. Acta 1762 (2006) 873-889
66. Lyly A., von Schantz C., Salonen T., Kopra O., Saarela J., Jauhiainen M., Kyttala A., and Jalanko A. Glycosylation, transport, and complex formation of palmitoyl protein thioesterase 1 (PPT1)-distinct characteristics in neurons. BMC Cell Biol. 8 (2007) 22
67. Duncan J.A., and Gilman A.G. A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21(RAS). J. Biol. Chem. 273 (1998) 15830-15837
68. Zhang Z., Lee Y.C., Kim S.J., Choi M.S., Tsai P.C., Xu Y., Xiao Y.J., Zhang P., Heffer A., and Mukherjee A.B. Palmitoyl-protein thioesterase-1 deficiency mediates the activation of the unfolded protein response and neuronal apoptosis in INCL. Hum. Mol. Genet. 15 (2006) 337-346
69. Kim S.J., Zhang Z., Lee Y.C., and Mukherjee A.B. Palmitoyl-protein thioesterase-1 deficiency leads to the activation of caspase-9 and contributes to rapid neurodegeneration in INCL. Hum. Mol. Genet. 15 (2006) 1580-1586
70. Kim S.J., Zhang Z., Hitomi E., Lee Y.C., and Mukherjee A.B. Endoplasmic reticulum stress-induced caspase-4 activation mediates apoptosis and neurodegeneration in INCL. Hum. Mol. Genet. 15 (2006) 1826-1834
71. Wei H., Kim S.J., Zhang Z., Tsai P.C., Wisniewski K.E., and Mukherjee A.B. ER and oxidative stresses are common mediators of apoptosis in both neurodegenerative and non-neurodegenerative lysosomal storage disorders and are alleviated by chemical chaperones. Hum. Mol. Genet. 17 (2008) 469-477
72. Persaud-Sawin D.A., Mousallem T., Wang C., Zucker A., Kominami E., and Boustany R.M. Neuronal ceroid lipofuscinosis: a common pathway?. Pediatr. Res. 61 (2007) 146-152
73. von Schantz C., Saharinen J., Kopra O., Cooper J.D., Gentile M., Hovatta I., Peltonen L., and Jalanko A. Brain gene expression profiles of Cln1 and Cln5 deficient mice unravels common molecular pathways underlying neuronal degeneration in NCL diseases. BMC Genomics 9 (2008) 146
74. Tardy C., Tyynela J., Hasilik A., Levade T., and Andrieu-Abadie N. Stress-induced apoptosis is impaired in cells with a lysosomal targeting defect but is not affected in cells synthesizing a catalytically inactive cathepsin D. Cell Death Differ. 10 (2003) 1090-1100
75. Korey C.A., and MacDonald M.E. An over-expression system for characterizing Ppt1 function in Drosophila. BMC Neurosci. 4 (2003) 30