Caspase-2 Is Localized at the Golgi Complex and Cleaves Golgin-160 during Apoptosis

Journal of Cell Biology - Tập 149 Số 3 - Trang 603-612 - 2000
Marie Mancini1, Carolyn E. Machamer2, Sophie Roy3, Donald W. Nicholson3, Nancy A. Thornberry4, Livia Casciola‐Rosen2,5, Antony Rosen6,2,7
1aDepartment of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205
2bDepartment of Cell Biology and Anatomy, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205
3eDepartment of Biochemistry and Molecular Biology, Merck Frosst Center for Therapeutic Research, Pointe Claire-Dorval, Quebec, H9R 4P8, Canada
4fDepartment of Biochemistry, Merck Research Laboratories, Rahway, New Jersey 07065
5cDepartment of Dermatology, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205
6Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205
7dDepartment of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205

Tóm tắt

Caspases are an extended family of cysteine proteases that play critical roles in apoptosis. Animals deficient in caspases-2 or -3, which share very similar tetrapeptide cleavage specificities, exhibit very different phenotypes, suggesting that the unique features of individual caspases may account for distinct regulation and specialized functions. Recent studies demonstrate that unique apoptotic stimuli are transduced by distinct proteolytic pathways, with multiple components of the proteolytic machinery clustering at distinct subcellular sites. We demonstrate here that, in addition to its nuclear distribution, caspase-2 is localized to the Golgi complex, where it cleaves golgin-160 at a unique site not susceptible to cleavage by other caspases with very similar tetrapeptide specificities. Early cleavage at this site precedes cleavage at distal sites by other caspases. Prevention of cleavage at the unique caspase-2 site delays disintegration of the Golgi complex after delivery of a pro-apoptotic signal. We propose that the Golgi complex, like mitochondria, senses and integrates unique local conditions, and transduces pro-apoptotic signals through local caspases, which regulate local effectors.

Từ khóa


Tài liệu tham khảo

Ashkenazi, 1998, Death receptorssignaling and modulation, Science., 281, 1305, 10.1126/science.281.5381.1305

Bennett, 1998, Cell surface trafficking of Fasa rapid mechanism of p53-mediated apoptosis, Science., 282, 290, 10.1126/science.282.5387.290

Bergeron, 1998, Defects in regulation of apoptosis in caspase-2-deficient mice, Genes Dev., 12, 1304, 10.1101/gad.12.9.1304

Butt, 1998, Dimerization and autoprocessing of the Nedd2 (caspase-2) precursor requires both the prodomain and the carboxyl-terminal regions, J. Biol. Chem., 273, 6763, 10.1074/jbc.273.12.6763

Casciola-Rosen, 1994, Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes, J. Exp. Med., 179, 1317, 10.1084/jem.179.4.1317

Casciola-Rosen, 1995, DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis, J. Exp. Med., 182, 1625, 10.1084/jem.182.6.1625

Casciola-Rosen, 1996, Apopain/CPP32 cleaves proteins that are essential for cellular repaira fundamental principle of apoptotic death, J. Exp. Med., 183, 1957, 10.1084/jem.183.5.1957

Casciola-Rosen, 1999, Cleavage by granzyme B is strongly predictive of autoantigen statusimplications for initiation of autoimmunity, J. Exp. Med., 190, 815, 10.1084/jem.190.6.815

Casiano, 1996, Selective cleavage of nuclear autoantigens during CD95 (Fas/APO-1)-mediated T cell apoptosis, J. Exp. Med., 184, 765, 10.1084/jem.184.2.765

Chan, 1998, Golginscoiled-coil-rich proteins associated with the Golgi complex, Electronic J. Biotech., 1, 1, 10.2225/vol1-issue2-fulltext-1

Chen, 1999, B cell apoptosis triggered by antigen receptor ligation proceeds via a novel caspase-dependent pathway, J. Immunol., 163, 2483, 10.4049/jimmunol.163.5.2483

Cockcroft, 1999, Mammalian phosphatidylinositol transfer proteinsemerging roles in signal transduction and vesicular traffic, Chem. Phys. Lipids., 98, 23, 10.1016/S0009-3084(99)00015-8

Colussi, 1998, Prodomain-dependent nuclear localization of the caspase-2 (Nedd2) precursor—a novel function for a caspase prodomain, J. Biol. Chem., 273, 24535, 10.1074/jbc.273.38.24535

Duan, 1997, RAIDD is a new ‘death’ adaptor molecule, Nature., 385, 86, 10.1038/385086a0

Garcia-Calvo, 1999, Purification and catalytic properties of human caspase family members, Cell Death Differ., 6, 362, 10.1038/sj.cdd.4400497

Gleeson, 1996, p230 is associated with vesicles budding from the trans-Golgi network, J. Cell Sci., 109, 2811, 10.1242/jcs.109.12.2811

Harvey, 1996, Processing of the Nedd2 precursor by ICE-like proteases and granzyme B, Genes Cells., 1, 673, 10.1046/j.1365-2443.1996.00255.x

Harvey, 1997, Functional activation of Nedd2/ICH-1 (Caspase-2) is an early process in apoptosis, J. Biol. Chem., 272, 13134, 10.1074/jbc.272.20.13134

Hauser, 1998, A giant ubiquitin-conjugating enzyme related to IAP apoptosis inhibitors, J. Cell Biol., 141, 1415, 10.1083/jcb.141.6.1415

Jacobson, 1996, Role of Ced3/ICE-family proteases in staurosporine-induced programmed cell death, J. Cell Biol., 133, 1041, 10.1083/jcb.133.5.1041

Jamora, 1999, Gbetagamma-mediated regulation of Golgi organization is through the direct activation of protein kinase D, Cell., 98, 59, 10.1016/S0092-8674(00)80606-6

Jones, 1999, TNF recruits TRADD to the plasma membrane but not the trans Golgi network, the principal subcellular location of TNF-R1, J. Immunol., 162, 1042, 10.4049/jimmunol.162.2.1042

Kluck, 1997, The release of cytochrome c from mitochondriaa primary site for Bcl-2 regulation of apoptosis, Science., 275, 1132, 10.1126/science.275.5303.1132

Kolesnick, 1999, Ceramide and apoptosis, Trends Biochem. Sci., 24, 224, 10.1016/S0968-0004(99)01408-5

Kondo, 1997, Cloning and molecular characterization of cDNA encoding a mouse male-enhanced antigen-2 (Mea-2)a putative family of the Golgi autoantigen, DNA Seq., 7, 71, 10.3109/10425179709020154

Krajewski, 1999, Release of caspase-9 from mitochondria during neuronal apoptosis and cerebral ischemia, Proc. Natl. Acad. Sci. USA., 96, 5752, 10.1073/pnas.96.10.5752

Krebs, 1999, Activation of membrane-associated procaspase-3 is regulated by Bcl-2, J. Cell Biol., 144, 915, 10.1083/jcb.144.5.915

Kuida, 1996, Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice, Nature., 384, 368, 10.1038/384368a0

Kumar, 1995, Inhibition of apoptosis by the expression of antisense Nedd2, FEBS (Fed. Eur. Biochem. Soc.) Lett., 368, 69, 10.1016/0014-5793(95)00602-6

Kumar, 1994, Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-1β-converting enzyme, Genes Dev., 8, 1613, 10.1101/gad.8.14.1613

Li, 1999, Deciphering the pathways of life and death, Curr. Opin. Cell Biol., 11, 261, 10.1016/S0955-0674(99)80035-0

Li, 1997, Activation of caspase-2 in apoptosis, J. Biol. Chem., 272, 21010, 10.1074/jbc.272.34.21010

Linstedt, 1993, Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa, Mol. Biol. Cell., 4, 679, 10.1091/mbc.4.7.679

Liu, 1996, Induction of apoptotic program in cell-free extractsrequirement for dATP and cytochrome c, Cell., 86, 147, 10.1016/S0092-8674(00)80085-9

Los, 1999, The role of caspases in development, immunity, and apoptotic signal transuctionlessons from knockout mice, Immunity., 10, 629, 10.1016/S1074-7613(00)80062-X

Lowe, 1998, Cdc2 kinase directly phosphorylates the cis-Golgi matrix protein GM130 and is required for Golgi fragmentation in mitosis, Cell., 94, 783, 10.1016/S0092-8674(00)81737-7

Maceyka, 1997, Ceramide accumulation uncovers a cycling pathway for the cis-Golgi network marker, infectious bronchitis virus M protein, J. Cell Biol., 139, 1411, 10.1083/jcb.139.6.1411

Mancini, 1998, The caspase-3 precursor has a cytosolic and mitochondrial distributionimplications for apoptotic signaling, J. Cell Biol., 140, 1485, 10.1083/jcb.140.6.1485

Martin, 1998, Membrane oligomerization and cleavage activates the caspase-8 (FLICE/MACHα1) death signal, J. Biol. Chem., 273, 4345, 10.1074/jbc.273.8.4345

Misumi, 1997, Molecular characterization of GCP170, a 170-kDa protein associated with the cytoplasmic face of the Golgi membrane, J. Biol. Chem., 272, 23851, 10.1074/jbc.272.38.23851

Muzio, 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, 10.1016/S0092-8674(00)81266-0

Nakamura, 1997, The vesicle docking protein p115 binds GM130, a cis-Golgi matrix protein, in a mitotically regulated manner, Cell., 89, 445, 10.1016/S0092-8674(00)80225-1

Nicholson, 1997, Caspaseskiller proteases, TIBS (Trends Biochem. Sci.)., 22, 299, 10.1016/S0968-0004(97)01085-2

Rosen, 1999, Autoantigens as substrates for apoptotic proteasesimplications for the pathogenesis of systemic autoimmune disease, Cell Death Differ., 6, 6, 10.1038/sj.cdd.4400460

Salvesen, 1997, Caspasesintracellular signaling by proteolysis, Cell., 91, 443, 10.1016/S0092-8674(00)80430-4

Samali, 1998, Detection of pro-caspase-3 in cytosol and mitochondria of various tissues, FEBS (Fed. Eur. Biochem. Soc.) Lett., 431, 167, 10.1016/S0014-5793(98)00740-6

Seelig, 1994, Macrogolgina new 376 kD Golgi complex outer membrane protein as target of antibodies in patients with rheumatic diseases and HIV infections, J. Autoimmunity., 7, 67, 10.1006/jaut.1994.1006

Sesso, 1999, Structural elements common to mitosis and apoptosis, Tissue Cell., 31, 357, 10.1054/tice.1999.0042

Sonnichsen, 1998, A role for giantin in docking COP1 vesicles to Golgi membranes, J. Cell Biol., 140, 1013, 10.1083/jcb.140.5.1013

Susin, 1999, Mitochondrial release of caspase-2 and -9 during the apoptotic process, J. Exp. Med., 189, 381, 10.1084/jem.189.2.381

Thornberry, 1998, Caspasesenemies within, Science., 281, 1312, 10.1126/science.281.5381.1312

Thornberry, 1997, A combinatorial approach defines specificities of members of the caspase family and granzyme B, J. Biol. Chem., 272, 17907, 10.1074/jbc.272.29.17907

Troy, 1997, Nedd2 is required for apoptosis after trophic factor withdrawal, but not superoxide dismutase (SOD1) downregulation, in sympathetic neurons and PC12 cells, J. Neurosci., 17, 1911, 10.1523/JNEUROSCI.17-06-01911.1997

Wang, 1994, Ich-1, an Ice/ced-3-related gene, encodes both positive and negative regulators of programmed cell death, Cell., 78, 739, 10.1016/S0092-8674(94)90422-7

Weisz, 1993, Oligomerization of a membrane protein correlates with its retention in the Golgi complex, J. Cell Biol., 122, 1185, 10.1083/jcb.122.6.1185

Woo, 1998, Essential contribution of caspase 3/CPP32 to apoptosis and its associated nuclear changes, Genes Dev., 12, 806, 10.1101/gad.12.6.806

Wright, 1999, Toll, a new piece in the puzzle of innate immunity, J. Exp. Med., 189, 605, 10.1084/jem.189.4.605

Yang, 1998, Autoproteolytic activation of pro-caspases by oligomerization, Mol. Cell., 1, 319, 10.1016/S1097-2765(00)80032-5

Zheng, 1999, Caspase knockoutsmatters of life and death, Cell Death Differ., 6, 1043, 10.1038/sj.cdd.4400593

Thông tin
Thông tin xuất bản

Journal of Cell Biology

Tập 149 Số 3

603-612

Thông tin tác giả