Flightless-I regulates proinflammatory caspases by selectively modulating intracellular localization and caspase activity

Journal of Cell Biology

Volumn 181, Issue 2, 2008, Pages 321-333

  Li, Juying ^a   Yin, Helen L ^b   Yuan, Junying ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 11; GELSOLIN; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEIN FLIGHTLESS 1; TRITON X 100; UNCLASSIFIED DRUG; ACTIN; CASP11 PROTEIN, MOUSE; CASPASE; CYTOSKELETON PROTEIN; FLIIH PROTEIN, MOUSE; PEPTIDE FRAGMENT;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN TARGETING; AMINO ACID SEQUENCE; ANIMAL; BIOTINYLATION; CHEMISTRY; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; MOUSE; OPEN READING FRAME; PLASMID;

COWPOX VIRUS;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; BIOTINYLATION; CASPASE 1; CASPASES; CYTOSKELETAL PROTEINS; ENZYME ACTIVATION; INTERLEUKIN-1BETA; KINETICS; MICE; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PEPTIDE FRAGMENTS; PLASMIDS;

EID: 42449153825     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200711082     Document Type: Article

References (45)

1. Acehan, D., X. Jiang, D.G. Morgan, J.E. Heuser, X. Wang, and C.W. Akey. 2002. Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol. Cell. 9:423-432
2. Annand, R.R., J.R. Dahlen, C.A. Sprecher, P. De Dreu, D.C. Foster, J.A. Mankovich, R.V. Talanian, W. Kisiel, and D.A. Giegel. 1999. Caspase-1 (interleukin-1beta-converting enzyme) is inhibited by the human serpin analogue proteinase inhibitor 9. Biochem. J. 342:655-665.
3. Boatright, K.M., and G.S. Salvesen. 2003. Mechanisms of caspase activation. Curr. Opin. Cell Biol. 15:725-731.
4. Campbell, H.D., T. Schimansky, C. Claudianos, N. Ozsarac, A.B. Kasprzak, J.N. Cotsell, I.G. Young, H.G. de Couet, and G.L. Miklos. 1993. The Drosophila melanogaster flightless-I gene involved in gastrulation and muscle degeneration encodes gelsolin-like and leucine-rich repeat domains and is conserved in Caenorhabditis elegans and humans. Proc. Natl. Acad. Sci. USA. 90:11386-11390 .
5. Campbell, H.D., S. Fountain, I.S. McLennan, L.A. Berven, M.F. Crouch, D.A. Davy, J.A. Hooper, K. Waterford, K.S. Chen, J.R. Lupski, et al. 2002. Fliih, a gelsolin-related cytoskeletal regulator essential for early mammalian embryonic development. Mol. Cell. Biol. 22:3518-3526.
6. Chang, D.W., Z. Xing, V.L. Capacio, M.E. Peter, and X. Yang. 2003. Interdimer processing mechanism of procaspase-8 activation. EMBO J. 22:4132-4142.
7. Chen, K.S., P.H. Gunaratne, J.D. Hoheisel, I.G. Young, G.L. Miklos, F. Greenberg, L.G. Shaffer, H.D. Campbell, and J.R. Lupski. 1995. The human homologue of the Drosophila melanogaster flightless-I gene (flil) maps within the Smith-Magenis microdeletion critical region in 17p11.2. Am. J. Hum. Genet. 56:175-182.
8. Clem, R.J., M. Fechheimer, and L.K. Miller. 1991. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science. 254:1388-1390.
9. Cogswell, J.P., M.M. Godlevski, G.B. Wisely, W.C. Clay, L.M. Leesnitzer, J.P. Ways, and J.G. Gray. 1994. NF-kappa B regulates IL-1 beta transcription through a consensus NF-kappa B binding site and a nonconsensus CRE-like site. J. Immunol. 153:712-723.
10. Cryns, V., and J. Yuan. 1998. Proteases to die for. Genes Dev. 12:1551-1570.
11. Davy, D.A., H.D. Campbell, S. Fountain, D. de Jong, and M.F. Crouch. 2001. The flightless I protein colocalizes with actin- and microtubule-based structures in motile Swiss 3T3 fibroblasts: evidence for the involvement of PI 3-kinase and Ras-related small GTPases. J. Cell Sci. 114:549-562.
12. Deveraux, Q.L., and J.C. Reed. 1999. IAP family proteins-suppressors of apoptosis. Genes Dev. 13:239-252.
13. Druilhe, A., S.M. Srinivasula, M. Razmara, M. Ahmad, and E.S. Alnemri. 2001. Regulation of IL-1beta generation by Pseudo-ICE and ICEBERG, two dominant negative caspase recruitment domain proteins. Cell Death Differ. 8:649-657.
14. Fong, K.S., and H.G. de Couet. 1999. Novel proteins interacting with the leucine-rich repeat domain of human flightless-I identified by the yeast two-hybrid system. Genomics. 58:146-157.
15. Frangioni, J.V., and B.G. Neel. 1993. Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Anal. Biochem. 210:179-187.
16. Ghayur, T., S. Banerjee, M. Hugunin, D. Butler, L. Herzog, A. Carter, L. Quintal, L. Sekut, R. Talanian, M. Paskind, et al. 1997. Caspase-1 processes IFN-gamma-inducing factor and regulates LPS-induced IFN-gamma production. Nature. 386:619-623.
17. Gu, Y., K. Kuida, H. Tsutsui, G. Ku, K. Hsiao, M.A. Fleming, N. Hayashi, K. Higashino, H. Okamura, K. Nakanishi, et al. 1997. Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme. Science. 275:206-209.
18. Huang, X., A. Masselli, S.M. Frisch, I.C. Hunton, Y. Jiang, and J.Y. Wang. 2007. Blockade of tumor necrosis factor-induced Bid cleavage by caspase-resistant Rb. J. Biol. Chem. 282:29401-29413.
19. Humke, E.W., S.K. Shriver, M.A. Starovasnik, W.J. Fairbrother, and V.M. Dixit. 2000. ICEBERG: a novel inhibitor of interleukin-1beta generation. Cell. 103:99-111.
20. Kang, S.J., S. Wang, H. Hara, E.P. Peterson, S. Namura, S. Amin-Hanjani, Z. Huang, A. Srinivasan, K.J. Tomaselli, N.A. Thornberry, et al. 2000. Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions. J. Cell Biol. 149:613-622.
21. Komiyama, T., C.A. Ray, D.J. Pickup, A.D. Howard, N.A. Thornberry, E.P. Peterson, and G. Salvesen . 1994 . Inhibition of interleukin-1 beta converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition. J. Biol. Chem. 269:19331-19337.
22. Kuida, K., J.A. Lippke, G. Ku, M.W. Harding, D.J. Livingston, M.S. Su, and R.A. Flavell . 1995 . Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science. 267:2000-2003.
23. Kummer, J.A., O. Micheau, P. Schneider, N. Bovenschen, R. Broekhuizen, R. Quadir, M.C. Strik, C.E. Hack, and J. Tschopp . 2007 . Ectopic expression of the serine protease inhibitor PI9 modulates death receptor-mediated apoptosis. Cell Death Differ. 14:1486-1496.
24. Lee, S.H., C. Stehlik, and J.C. Reed. 2001. Cop, a caspase recruitment domain-containing protein and inhibitor of caspase-1 activation processing. J. Biol. Chem. 276:34495-34500.
25. Li, J., W.M. Brieher, M.L. Scimone, S.J. Kang, H. Zhu, H. Yin, U.H. von Andrian, T. Mitchison, and J. Yuan. 2007. Caspase-11 regulates cell migration by promoting Aip1-Cofilin-mediated actin depolymerization. Nat. Cell Biol. 9:276-286.
26. Li, P., H. Allen, S. Banerjee, S. Franklin, L. Herzog, C. Johnston, J. McDowell, M. Paskind, L. Rodman, J. Salfeld, et al. 1995 . Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell. 80:401-411.
27. Liu, Y.T., and H.L. Yin. 1998. Identification of the binding partners for flightless I, a novel protein bridging the leucine-rich repeat and the gelsolin superfamilies. J. Biol. Chem. 273:7920-7927.
28. Marsden, V.S., L. O'Connor, L.A. O'Reilly, J. Silke, D. Metcalf, P.G. Ekert, D.C. Huang, F. Cecconi, K. Kuida, K.J. Tomaselli, et al. 2002. Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome. Nature. 419:634-637.
29. Martinon, F., and J. Tschopp. 2004. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell. 117:561-574.
30. Ono, S. 2003. Regulation of actin filament dynamics by actin depolymerizing factor/cofilin and actin-interacting protein 1: new blades for twisted filaments. Biochemistry. 42:13363-13370.
31. Pinson, K.I., L. Dunbar, L. Samuelson, and D.L. Gumucio. 1998. Targeted disruption of the mouse villin gene does not impair the morphogenesis of microvilli. Dev. Dyn. 211:109-121.
32. Ray, C.A., R.A. Black, S.R. Kronheim, T.A. Greenstreet, P.R. Sleath, G.S. Salvesen, and D.J. Pickup. 1992. Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme. Cell. 69:597-604.
33. Schauvliege, R., J. Vanrobaeys, P. Schotte, and R. Beyaert. 2002. Caspase-11 gene expression in response to lipopolysaccharide and interferon-gamma requires nuclear factor-kappa B and signal transducer and activator of transcription (STAT) 1. J. Biol. Chem. 277:41624-41630.
34. Silacci, P., L. Mazzolai, C. Gauci, N. Stergiopulos, H.L. Yin, and D. Hayoz. 2004. Gelsolin superfamily proteins: key regulators of cellular functions. Cell. Mol. Life Sci. 61:2614-2623.
35. Sprecher, C.A., K.A. Morgenstern, S. Mathewes, J.R. Dahlen, S.K. Schrader, D.C. Foster, and W. Kisiel. 1995. Molecular cloning, expression, and partial characterization of two novel members of the ovalbumin family of serine proteinase inhibitors. J. Biol. Chem. 270:29854-29861.
36. Thornberry, N.A., H.G. Bull, J.R. Calaycay, K.T. Chapman, A.D. Howard, M.J. Kostura, D.K. Miller, S.M. Molineaux, J.R. Weidner, J. Aunins, et al. 1992 . A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature. 356:768-774.
37. Thornberry, N.A., T.A. Rano, E.P. Peterson, D.M. Rasper, T. Timkey, M. Garcia-Calvo, V.M. Houtzager, P.A. Nordstrom, S. Roy, J.P. Vaillancourt, et al. 1997. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J. Biol. Chem. 272:17907-17911.
38. Wang, S., M. Miura, Y. Jung, H. Zhu, V. Gagliardini, L. Shi, A.H. Greenberg, and J. Yuan. 1996. Identification and characterization of Ich-3, a member of the interleukin-1beta converting enzyme (ICE)/Ced-3 family and an upstream regulator of ICE. J. Biol. Chem. 271:20580-20587.
39. Wang, S., M. Miura, Y.K. Jung, H. Zhu, E. Li, and J. Yuan. 1998. Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell. 92:501-509.
40. Wang, T., T.H. Chuang, T. Ronni, S. Gu, Y.C. Du, H. Cai, H.Q. Sun, H.L. Yin, and X. Chen. 2006. Flightless I homolog negatively modulates the TLR pathway. J. Immunol. 176:1355-1362.
41. Witke, W., A.H. Sharpe, J.H. Hartwig, T. Azuma, T.P. Stossel, and D.J. Kwiatkowski. 1995. Hemostatic, inflammatory, and fibroblast responses are blunted in mice lacking gelsolin. Cell. 81:41-51.
42. Witke, W., W. Li, D.J. Kwiatkowski, and F.S. Southwick. 2001. Comparisons of CapG and gelsolin-null macrophages: demonstration of a unique role for CapG in receptor-mediated ruffling, phagocytosis, and vesicle rocketing. J. Cell Biol. 154:775-784.
43. Yamamoto, M., D.H. Hilgemann, S. Feng, H. Bito, H. Ishihara, Y. Shibasaki, and H.L. Yin. 2001. Phosphatidylinositol 4,5-bisphosphate induces actin stress-fiber formation and inhibits membrane ruffling in CV1 cells. J. Cell Biol. 152:867-876.
44. Young, J.L., G.K. Sukhova, D. Foster, W. Kisiel, P. Libby, and U. Schonbeck. 2000. The serpin proteinase inhibitor 9 is an endogenous inhibitor of interleukin 1beta-converting enzyme (caspase-1) activity in human vascular smooth muscle cells. J. Exp. Med. 191:1535-1544.
45. Zhou, Q., J.F. Krebs, S.J. Snipas, A. Price, E.S. Alnemri, K.J. Tomaselli, and G.S. Salvesen. 1998. Interaction of the baculovirus anti-apoptotic protein p35 with caspases. Specificity, kinetics, and characterization of the caspase/p35 complex. Biochemistry. 37:10757-10765.