Apollon ubiquitinates SMAC and caspase-9, and has an essential cytoprotection function

Apollon (also known as BRUCE or BIRC6) is a large protein containing baculoviral-IAP-repeat (BIR) and ubiquitin-conjugating enzyme (UBC) domains at the amino- and carboxy termini, respectively. Apollon inhibits apoptosis, but its molecular and physiological function remains unclear. Here we report t...

Full description

Saved in:

Bibliographic Details
Published in	Nature cell biology Vol. 6; no. 9; pp. 849 - 860
Main Authors	Hao, Yanyan, Sekine, Keiko, Kawabata, Atsushi, Nakamura, Hitoshi, Ishioka, Toshiyasu, Ohata, Hirokazu, Katayama, Ryohei, Hashimoto, Chizuko, Zhang, Xiaodong, Noda, Tetsuo, Tsuruo, Takashi, Naito, Mikihiko
Format	Journal Article
Language	English
Published	London Nature Publishing Group UK 01.09.2004 Nature Publishing Group
Subjects	Animals Apoptosis Cancer Research Carrier Proteins - metabolism Caspase 9 Caspases - metabolism Cell Biology Cellular proteins Cysteine Endopeptidases - metabolism Cytochromes Developmental Biology Fetal Death Humans Inhibitor of Apoptosis Proteins Intracellular Signaling Peptides and Proteins Life Sciences Mice Mice, Knockout Mitochondrial Proteins - metabolism Neoplasm Proteins - genetics Neoplasm Proteins - metabolism Neoplasm Proteins - physiology Physiological aspects Physiology Protective Agents Stem Cells U937 Cells Ubiquitin-Conjugating Enzymes - metabolism Japan
Online Access	Get full text
ISSN	1465-7392 1476-4679
DOI	10.1038/ncb1159

Cover

Abstract	Apollon (also known as BRUCE or BIRC6) is a large protein containing baculoviral-IAP-repeat (BIR) and ubiquitin-conjugating enzyme (UBC) domains at the amino- and carboxy termini, respectively. Apollon inhibits apoptosis, but its molecular and physiological function remains unclear. Here we report that Apollon binds to, ubiquitinates and facilitates proteasomal degradation of SMAC and caspase-9, which both contain IAP-binding motifs. Targeted disruption of Apollon in mice caused embryonic and neonatal lethality. Notably, SMAC induced apoptosis in Apollon -deficient cells, but not in Apollon -expressing cells. Furthermore, the IAP-binding motif of SMAC was required to induce apoptosis in Apollon -deficient cells. These results suggest that Apollon has an essential function in preventing SMAC-induced apoptosis.
AbstractList	Apollon (also known as BRUCE or BIRC6) is a large protein containing baculoviral-IAP-repeat (BIR) and ubiquitin-conjugating enzyme (UBC) domains at the amino- and carboxy termini, respectively. Apollon inhibits apoptosis, but its molecular and physiological function remains unclear. Here we report that Apollon binds to, ubiquitinates and facilitates proteasomal degradation of SMAC and caspase-9, which both contain IAP-binding motifs. Targeted disruption of Apollon in mice caused embryonic and neonatal lethality. Notably, SMAC induced apoptosis in Apollon -deficient cells, but not in Apollon -expressing cells. Furthermore, the IAP-binding motif of SMAC was required to induce apoptosis in Apollon -deficient cells. These results suggest that Apollon has an essential function in preventing SMAC-induced apoptosis. Apollon (also known as BRUCE or BIRC6) is a large protein containing baculoviral-IAP-repeat (BIR) and ubiquitin-conjugating enzyme (UBC) domains at the amino- and carboxy termini, respectively. Apollon inhibits apoptosis, but its molecular and physiological function remains unclear. Here we report that Apollon binds to, ubiquitinates and facilitates proteasomal degradation of SMAC and caspase-9, which both contain IAP-binding motifs. Targeted disruption of Apollon in mice caused embryonic and neonatal lethality. Notably, SMAC induced apoptosis in Apollon-deficient cells, but not in Apollon-expressing cells. Furthermore, the IAP-binding motif of SMAC was required to induce apoptosis in Apollon-deficient cells. These results suggest that Apollon has an essential function in preventing SMAC-induced apoptosis.Apollon (also known as BRUCE or BIRC6) is a large protein containing baculoviral-IAP-repeat (BIR) and ubiquitin-conjugating enzyme (UBC) domains at the amino- and carboxy termini, respectively. Apollon inhibits apoptosis, but its molecular and physiological function remains unclear. Here we report that Apollon binds to, ubiquitinates and facilitates proteasomal degradation of SMAC and caspase-9, which both contain IAP-binding motifs. Targeted disruption of Apollon in mice caused embryonic and neonatal lethality. Notably, SMAC induced apoptosis in Apollon-deficient cells, but not in Apollon-expressing cells. Furthermore, the IAP-binding motif of SMAC was required to induce apoptosis in Apollon-deficient cells. These results suggest that Apollon has an essential function in preventing SMAC-induced apoptosis. Apollon (also known as BRUCE or BIRC6) is a large protein containing baculoviral-IAP-repeat (BIR) and ubiquitin-conjugating enzyme (UBC) domains at the amino- and carboxy termini, respectively. Apollon inhibits apoptosis, but its molecular and physiological function remains unclear. Here we report that Apollon binds to, ubiquitinates and facilitates proteasomal degradation of SMAC and caspase-9, which both contain IAP-binding motifs. Targeted disruption of Apollon in mice caused embryonic and neonatal lethality. Notably, SMAC induced apoptosis in Apollon-deficient cells, but not in Apollon-expressing cells. Furthermore, the IAP-binding motif of SMAC was required to induce apoptosis in Apollon-deficient cells. These results suggest that Apollon has an essential function in preventing SMAC-induced apoptosis.
Audience	Academic
Author	Tsuruo, Takashi Zhang, Xiaodong Hashimoto, Chizuko Kawabata, Atsushi Ishioka, Toshiyasu Ohata, Hirokazu Sekine, Keiko Naito, Mikihiko Nakamura, Hitoshi Katayama, Ryohei Noda, Tetsuo Hao, Yanyan
Author_xml	– sequence: 1 givenname: Yanyan surname: Hao fullname: Hao, Yanyan organization: Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku – sequence: 2 givenname: Keiko surname: Sekine fullname: Sekine, Keiko organization: Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku – sequence: 3 givenname: Atsushi surname: Kawabata fullname: Kawabata, Atsushi organization: Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku – sequence: 4 givenname: Hitoshi surname: Nakamura fullname: Nakamura, Hitoshi organization: Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku, Takeda Chemical Industries Ltd – sequence: 5 givenname: Toshiyasu surname: Ishioka fullname: Ishioka, Toshiyasu organization: Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku – sequence: 6 givenname: Hirokazu surname: Ohata fullname: Ohata, Hirokazu organization: Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku – sequence: 7 givenname: Ryohei surname: Katayama fullname: Katayama, Ryohei organization: Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku – sequence: 8 givenname: Chizuko surname: Hashimoto fullname: Hashimoto, Chizuko organization: Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku – sequence: 9 givenname: Xiaodong surname: Zhang fullname: Zhang, Xiaodong organization: Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku, Institute for Molecular Biology, College of Life Sciences, Nankai University – sequence: 10 givenname: Tetsuo surname: Noda fullname: Noda, Tetsuo organization: Cancer Institute, Japanese Foundation for Cancer Research, 1-37-1, Kami-Ikebukuro, Toshima-ku – sequence: 11 givenname: Takashi surname: Tsuruo fullname: Tsuruo, Takashi organization: Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku, Cancer Chemotherapy Center, Japanese Foundation for Cancer Research, 1-37-1, Kami-Ikebukuro, Toshima-ku – sequence: 12 givenname: Mikihiko surname: Naito fullname: Naito, Mikihiko email: mnaito@iam.u-tokyo.ac.jp organization: Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/15300255$$D View this record in MEDLINE/PubMed
BookMark	eNptkm2L1DAQx4OceA-K30CKBz6APZNmkrYvl8WHgxPBU9-GNJmuObrJXpOC9-1Nb1dlVwlhJuE3f_7MzCk58sEjIU8ZvWCUN2-96RgT7QNywqCWJci6PZpzKcqat9UxOY3xhlIGQOtH5JgJTmklxAn5vtiEYQi-mDp3O7nkvE4Yi-tPi2WhvS2MjhsdsWzf3D9_6JhjgTGiT04PhblLYTOGhCa5rNJP_j55TB72eoj4ZBfPyLf3774uP5ZXnz9cLhdXpRHQpBIBpbWmAyo5NEJixW0PwhoDlANtbKuBMVuDbC30giNCx2su64Zih5TxM_Jiq5s93E4Yk1q7aHAYtMcwRSVlw2VbiQw-PwBvwjT67E1VVcVrgJZn6HwLrfSAyvk-pFGbWVEtWMOrZr6ZuvgPlY_FtTN5Lr3L_3sFr_cKMpPwZ1rpKUZ1ef1ln3228zl1a7RqM7q1Hu_U74lloNwCZgwxjtgr45Kee55duEExquaNULuNyPzLA_6P5D_kqy0ZM-FXOP5t0SH6C0Zavv0
CitedBy_id	crossref_primary_10_1517_14728222_11_11_1459 crossref_primary_10_4161_23723548_2014_964037 crossref_primary_10_1074_jbc_M113_536854 crossref_primary_10_1016_j_tcb_2018_10_003 crossref_primary_10_1186_s12858_016_0065_x crossref_primary_10_12688_f1000research_10625_1 crossref_primary_10_1158_2159_8290_CD_22_1230 crossref_primary_10_3892_ol_2016_5349 crossref_primary_10_3892_mmr_2016_5473 crossref_primary_10_1517_14728222_12_8_981 crossref_primary_10_3389_fcell_2021_806482 crossref_primary_10_1038_nrm1621 crossref_primary_10_1097_JTO_0b013e31827d5237 crossref_primary_10_18632_oncotarget_2293 crossref_primary_10_3390_cancers14071671 crossref_primary_10_1038_s41467_024_45222_1 crossref_primary_10_1186_1756_9966_27_48 crossref_primary_10_18632_oncotarget_7617 crossref_primary_10_1016_j_tplants_2019_05_002 crossref_primary_10_3390_pharmaceutics14112523 crossref_primary_10_1038_s43016_023_00820_y crossref_primary_10_1080_07357900701508041 crossref_primary_10_1016_j_biocel_2011_12_005 crossref_primary_10_1371_journal_pone_0055837 crossref_primary_10_3390_cancers14246246 crossref_primary_10_1016_j_semcdb_2014_03_001 crossref_primary_10_1111_pce_14839 crossref_primary_10_1371_journal_pone_0177871 crossref_primary_10_1007_s11033_012_2261_0 crossref_primary_10_1242_jcs_212753 crossref_primary_10_1002_ijc_29194 crossref_primary_10_1111_j_1742_4658_2005_04966_x crossref_primary_10_1111_j_1349_7006_2010_01697_x crossref_primary_10_1152_japplphysiol_01540_2005 crossref_primary_10_1016_j_bbrc_2005_09_197 crossref_primary_10_1038_gt_2008_6 crossref_primary_10_1186_1471_2407_12_285 crossref_primary_10_1371_journal_pone_0090737 crossref_primary_10_1016_j_molcel_2008_03_008 crossref_primary_10_1104_pp_106_079707 crossref_primary_10_1002_cncr_20947 crossref_primary_10_3390_ph3040839 crossref_primary_10_1038_s41388_022_02319_5 crossref_primary_10_1038_sj_cdd_4401729 crossref_primary_10_1016_S1016_8478_23_13252_3 crossref_primary_10_1007_s10059_011_0137_0 crossref_primary_10_3390_cells9041012 crossref_primary_10_1016_j_anndiagpath_2016_07_003 crossref_primary_10_1016_j_jconrel_2010_07_114 crossref_primary_10_1016_j_fob_2015_06_005 crossref_primary_10_1111_j_1600_0609_2011_01734_x crossref_primary_10_1038_sj_bjc_6604927 crossref_primary_10_1248_cpb_c18_00567 crossref_primary_10_18632_oncotarget_2229 crossref_primary_10_3390_cells1040711 crossref_primary_10_1007_s10330_011_0935_z crossref_primary_10_1016_j_molcel_2012_07_033 crossref_primary_10_1038_cdd_2008_90 crossref_primary_10_1074_jbc_M116_768853 crossref_primary_10_1126_science_ade8840 crossref_primary_10_1242_jcs_038513 crossref_primary_10_1016_j_tplants_2014_06_004 crossref_primary_10_1016_j_ceb_2009_09_005 crossref_primary_10_1007_s12029_016_9874_9 crossref_primary_10_1002_med_21502 crossref_primary_10_7554_eLife_50034 crossref_primary_10_1080_15216540500389013 crossref_primary_10_1371_journal_pone_0105023 crossref_primary_10_1016_j_semcdb_2014_12_004 crossref_primary_10_1074_jbc_M411430200 crossref_primary_10_1111_j_1582_4934_2010_01218_x crossref_primary_10_1128_JVI_03159_12 crossref_primary_10_1016_j_semcdb_2014_12_002 crossref_primary_10_1038_srep21968 crossref_primary_10_1073_pnas_1418335112 crossref_primary_10_1084_jem_20061681 crossref_primary_10_1074_jbc_M110_125955 crossref_primary_10_3389_fonc_2022_922596 crossref_primary_10_4155_fmc_09_116 crossref_primary_10_1016_j_healun_2010_03_011 crossref_primary_10_1038_sj_onc_1209776 crossref_primary_10_1016_j_febslet_2009_06_018 crossref_primary_10_1126_science_ade8873 crossref_primary_10_1158_0008_5472_CAN_05_3248 crossref_primary_10_1016_j_bbrc_2010_06_016 crossref_primary_10_1038_s41418_020_0513_4 crossref_primary_10_1038_nrd2755 crossref_primary_10_1074_jbc_M709525200 crossref_primary_10_3389_fgene_2022_834935 crossref_primary_10_1002_smll_201907686 crossref_primary_10_1016_j_ddtec_2018_12_002 crossref_primary_10_1152_ajpheart_00338_2008 crossref_primary_10_3724_abbs_2023005 crossref_primary_10_7554_eLife_77461 crossref_primary_10_1016_j_bmc_2011_03_057 crossref_primary_10_1016_j_ctrv_2006_11_002 crossref_primary_10_1073_pnas_1901039116 crossref_primary_10_1097_TP_0b013e3181c3c690 crossref_primary_10_1158_1078_0432_CCR_07_0693 crossref_primary_10_1038_s41467_018_02823_x crossref_primary_10_1016_j_bbamcr_2005_03_002 crossref_primary_10_1091_mbc_e04_11_0971 crossref_primary_10_1016_j_bmhime_2017_11_034 crossref_primary_10_1038_ncb0904_804 crossref_primary_10_1126_science_ade5750 crossref_primary_10_1016_j_bbamcr_2008_03_006 crossref_primary_10_1007_s13238_014_0089_1 crossref_primary_10_1038_sj_cdd_4401959 crossref_primary_10_1104_pp_105_067983 crossref_primary_10_1007_s10495_007_0087_3 crossref_primary_10_1073_pnas_0408744102 crossref_primary_10_1038_s41435_019_0078_8 crossref_primary_10_1186_s13000_019_0875_4 crossref_primary_10_1002_mgg3_605 crossref_primary_10_1007_s10753_016_0387_2 crossref_primary_10_1002_bit_20872 crossref_primary_10_1007_s13402_024_01007_8 crossref_primary_10_1073_pnas_1306179110 crossref_primary_10_1186_s12929_020_0627_5 crossref_primary_10_1074_jbc_RA117_001091 crossref_primary_10_1096_fj_09_136259 crossref_primary_10_1038_cddis_2010_26 crossref_primary_10_1016_j_bmhimx_2016_10_004 crossref_primary_10_1016_j_devcel_2010_06_009 crossref_primary_10_1007_s10495_017_1375_1 crossref_primary_10_1016_j_cell_2008_01_012 crossref_primary_10_1038_cdd_2011_116 crossref_primary_10_1016_j_ajhg_2015_11_017 crossref_primary_10_3390_diagnostics13233560 crossref_primary_10_3892_etm_2016_3356 crossref_primary_10_1016_j_febslet_2012_03_033 crossref_primary_10_1371_journal_pone_0216553 crossref_primary_10_1016_j_omtn_2021_09_011 crossref_primary_10_1016_j_fgb_2012_09_011 crossref_primary_10_1002_path_2399 crossref_primary_10_1016_j_bbrc_2005_02_165 crossref_primary_10_1016_j_tcb_2009_01_004 crossref_primary_10_1158_1078_0432_CCR_11_2232 crossref_primary_10_1002_bdrc_20053 crossref_primary_10_1186_2162_3619_1_25 crossref_primary_10_1242_jcs_02902 crossref_primary_10_3892_ijo_2016_3634 crossref_primary_10_1016_j_drup_2005_12_001 crossref_primary_10_1016_j_envexpbot_2014_05_011 crossref_primary_10_15252_embj_2020107341 crossref_primary_10_1038_sj_onc_1208876 crossref_primary_10_4254_wjh_v13_i3_343 crossref_primary_10_3390_cancers13040624 crossref_primary_10_1071_RD09112 crossref_primary_10_1016_j_matbio_2020_11_004 crossref_primary_10_1242_dev_050088 crossref_primary_10_3389_fcell_2020_00830 crossref_primary_10_3390_ijms22041820 crossref_primary_10_1016_j_canlet_2011_12_024 crossref_primary_10_1016_j_ceb_2006_08_015 crossref_primary_10_1038_onc_2008_302 crossref_primary_10_1038_sj_embor_7400795 crossref_primary_10_1200_CCI_22_00093 crossref_primary_10_1074_jbc_M113_514430 crossref_primary_10_1007_s11010_014_2182_4 crossref_primary_10_1016_j_cellsig_2013_06_003 crossref_primary_10_1016_j_ydbio_2018_10_015 crossref_primary_10_1073_pnas_2007366117 crossref_primary_10_1111_jipb_12017 crossref_primary_10_1080_17386357_2005_9647269 crossref_primary_10_1007_s13277_014_1641_6
Cites_doi	10.1038/sj.onc.1202423 10.1038/40901 10.1038/sj.cdd.4400777 10.1016/S0960-9822(02)00935-1 10.1083/jcb.141.6.1415 10.1006/bbrc.1997.7111 10.1016/S0092-8674(00)80434-1 10.1016/S0092-8674(00)81874-7 10.1038/nrm830 10.1016/S0092-8674(00)00009-X 10.1016/S0092-8674(00)80085-9 10.1038/35022514 10.1126/science.288.5467.874 10.1016/S0968-0004(97)01085-2 10.1016/S0092-8674(00)00008-8 10.1200/JCO.1999.17.9.2941 10.1093/emboj/16.23.6914 10.1016/S1097-2765(00)80386-X 10.1128/MCB.22.10.3509-3517.2002 10.1016/S1097-2765(01)00341-0 10.1038/35065125 10.1126/science.7878463 10.1073/pnas.161506698 10.1038/42867 10.1038/nrm731 10.1038/44617 10.1016/S0092-8674(00)80430-4 10.1038/74994 10.1074/jbc.C200695200 10.1002/jcp.10254 10.1038/35037710 10.1016/S1534-5807(03)00120-5 10.1182/blood.V89.6.2060 10.1006/bbrc.1999.1585 10.1016/S0896-6273(03)00601-9 10.1016/S0092-8674(00)80501-2 10.1038/sj.emboj.7600075 10.1038/nsb989 10.1038/sj.cdd.4400765 10.1093/emboj/18.19.5242 10.1101/gad.13.3.239
ContentType	Journal Article
Copyright	Springer Nature Limited 2004 COPYRIGHT 2004 Nature Publishing Group Copyright Nature Publishing Group Sep 2004
Copyright_xml	– notice: Springer Nature Limited 2004 – notice: COPYRIGHT 2004 Nature Publishing Group – notice: Copyright Nature Publishing Group Sep 2004
DBID	AAYXX CITATION CGR CUY CVF ECM EIF NPM ISR 3V. 7QL 7QP 7QR 7T5 7TK 7TM 7TO 7U9 7X7 7XB 88A 88E 8AO 8FD 8FE 8FH 8FI 8FJ 8FK ABUWG AEUYN AFKRA AZQEC BBNVY BENPR BHPHI C1K CCPQU DWQXO FR3 FYUFA GHDGH GNUQQ H94 HCIFZ K9. LK8 M0S M1P M7N M7P P64 PHGZM PHGZT PJZUB PKEHL PPXIY PQEST PQGLB PQQKQ PQUKI PRINS RC3 7X8
DOI	10.1038/ncb1159
DatabaseName	CrossRef Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed Gale In Context: Science ProQuest Central (Corporate) Bacteriology Abstracts (Microbiology B) Calcium & Calcified Tissue Abstracts Chemoreception Abstracts Immunology Abstracts Neurosciences Abstracts Nucleic Acids Abstracts Oncogenes and Growth Factors Abstracts Virology and AIDS Abstracts Health & Medical Collection ProQuest Central (purchase pre-March 2016) Biology Database (Alumni Edition) Medical Database (Alumni Edition) ProQuest Pharma Collection Technology Research Database ProQuest SciTech Collection ProQuest Natural Science Collection Hospital Premium Collection Hospital Premium Collection (Alumni Edition) ProQuest Central (Alumni) (purchase pre-March 2016) ProQuest Central (Alumni) ProQuest One Sustainability ProQuest Central UK/Ireland ProQuest Central Essentials Biological Science Collection ProQuest Central Natural Science Collection Environmental Sciences and Pollution Management ProQuest One Community College ProQuest Central Engineering Research Database Health Research Premium Collection Health Research Premium Collection (Alumni) ProQuest Central Student AIDS and Cancer Research Abstracts SciTech Premium Collection ProQuest Health & Medical Complete (Alumni) Biological Sciences ProQuest Health & Medical Collection Medical Database Algology Mycology and Protozoology Abstracts (Microbiology C) Biological Science Database Biotechnology and BioEngineering Abstracts ProQuest Central Premium ProQuest One Academic (New) ProQuest Health & Medical Research Collection ProQuest One Academic Middle East (New) ProQuest One Health & Nursing ProQuest One Academic Eastern Edition (DO NOT USE) ProQuest One Applied & Life Sciences ProQuest One Academic ProQuest One Academic UKI Edition ProQuest Central China Genetics Abstracts MEDLINE - Academic
DatabaseTitle	CrossRef MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) ProQuest Central Student Oncogenes and Growth Factors Abstracts ProQuest Central Essentials Nucleic Acids Abstracts SciTech Premium Collection ProQuest Central China Environmental Sciences and Pollution Management ProQuest One Applied & Life Sciences ProQuest One Sustainability Health Research Premium Collection Natural Science Collection Health & Medical Research Collection Biological Science Collection Chemoreception Abstracts ProQuest Central (New) ProQuest Medical Library (Alumni) Virology and AIDS Abstracts ProQuest Biological Science Collection ProQuest One Academic Eastern Edition ProQuest Hospital Collection Health Research Premium Collection (Alumni) Biological Science Database Neurosciences Abstracts ProQuest Hospital Collection (Alumni) Biotechnology and BioEngineering Abstracts ProQuest Health & Medical Complete ProQuest One Academic UKI Edition Engineering Research Database ProQuest One Academic Calcium & Calcified Tissue Abstracts ProQuest One Academic (New) Technology Research Database ProQuest One Academic Middle East (New) ProQuest Health & Medical Complete (Alumni) ProQuest Central (Alumni Edition) ProQuest One Community College ProQuest One Health & Nursing ProQuest Natural Science Collection ProQuest Pharma Collection ProQuest Biology Journals (Alumni Edition) ProQuest Central ProQuest Health & Medical Research Collection Genetics Abstracts Health and Medicine Complete (Alumni Edition) ProQuest Central Korea Bacteriology Abstracts (Microbiology B) Algology Mycology and Protozoology Abstracts (Microbiology C) AIDS and Cancer Research Abstracts ProQuest SciTech Collection ProQuest Medical Library Immunology Abstracts ProQuest Central (Alumni) MEDLINE - Academic
DatabaseTitleList	MEDLINE - Academic MEDLINE ProQuest Central Student
Database_xml	– sequence: 1 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database – sequence: 3 dbid: BENPR name: ProQuest Central url: http://www.proquest.com/pqcentral?accountid=15518 sourceTypes: Aggregation Database
DeliveryMethod	fulltext_linktorsrc
Discipline	Biology
EISSN	1476-4679
EndPage	860
ExternalDocumentID	992140791 A183288328 15300255 10_1038_ncb1159
Genre	Research Support, Non-U.S. Gov't Journal Article
GeographicLocations	Japan
GeographicLocations_xml	– name: Japan
GroupedDBID	--- .55 .GJ 0R~ 123 29M 36B 39C 3V. 4.4 53G 5BI 5RE 7X7 88A 88E 8AO 8FE 8FH 8FI 8FJ 8R4 8R5 AAEEF AARCD AAYZH ABAWZ ABCQX ABDBF ABEFU ABJNI ABLJU ABNNU ABUWG ACBWK ACGFS ACIWK ACNCT ACPRK ACRPL ACUHS ADBBV ADNMO AENEX AEUYN AFFNX AFKRA AFRAH AFSHS AFWHJ AGAYW AGGDT AGHTU AHBCP AHMBA AHSBF AIYXT ALFFA ALIPV ALMA_UNASSIGNED_HOLDINGS ASPBG AVWKF AXYYD AZFZN B0M BBNVY BENPR BHPHI BKKNO BPHCQ BVXVI CCPQU CS3 D0L DB5 DU5 EAD EAP EBC EBD EBS EJD EMB EMK EMOBN EPL ESX EXGXG F5P FEDTE FQGFK FSGXE FYUFA HCIFZ HMCUK HVGLF HZ~ IAO IGS IHR INH INR ISR ITC L-9 L7B LK8 M0L M1P M7P N9A O9- P2P PQQKQ PROAC PSQYO Q2X QF4 QM4 QN7 QO4 RNS RNT RNTTT SNYQT SOJ SV3 TAOOD TBHMF TDRGL TSG TUS UKHRP X7M Y6R ~02 ~8M AAYXX ABFSG ACSTC AFANA AGQPQ ALPWD ATHPR CITATION PHGZM PHGZT 70F AAZLF ADQMX AFBBN AHOSX AIBTJ ARMCB CGR CUY CVF ECM EE. EIF J5H NNMJJ NPM ODYON SHXYY SIXXV SKT ZGI AEIIB PMFND 7QL 7QP 7QR 7T5 7TK 7TM 7TO 7U9 7XB 8FD 8FK AZQEC C1K DWQXO FR3 GNUQQ H94 K9. M7N P64 PJZUB PKEHL PPXIY PQEST PQGLB PQUKI PRINS RC3 7X8 PUEGO
ID	FETCH-LOGICAL-c548t-e4e6ddcb40634856e23df45dcc403408d9a411d7469d4f53ee4b3736780ebe013
IEDL.DBID	7X7
ISSN	1465-7392
IngestDate	Fri Sep 05 09:09:16 EDT 2025 Wed Aug 20 23:58:00 EDT 2025 Tue Jun 17 22:20:36 EDT 2025 Tue Jun 10 21:23:13 EDT 2025 Fri Jun 27 05:29:12 EDT 2025 Wed Feb 19 01:54:50 EST 2025 Thu Apr 24 23:08:41 EDT 2025 Tue Jul 01 00:57:12 EDT 2025 Fri Feb 21 02:43:33 EST 2025
IsPeerReviewed	true
IsScholarly	true
Issue	9
Language	English
License	http://www.springer.com/tdm
LinkModel	DirectLink
MergedId	FETCHMERGED-LOGICAL-c548t-e4e6ddcb40634856e23df45dcc403408d9a411d7469d4f53ee4b3736780ebe013
Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23
PMID	15300255
PQID	222374493
PQPubID	45779
PageCount	12
ParticipantIDs	proquest_miscellaneous_66836925 proquest_journals_222374493 gale_infotracmisc_A183288328 gale_infotracacademiconefile_A183288328 gale_incontextgauss_ISR_A183288328 pubmed_primary_15300255 crossref_citationtrail_10_1038_ncb1159 crossref_primary_10_1038_ncb1159 springer_journals_10_1038_ncb1159
ProviderPackageCode	CITATION AAYXX
PublicationCentury	2000
PublicationDate	2004-09-01
PublicationDateYYYYMMDD	2004-09-01
PublicationDate_xml	– month: 09 year: 2004 text: 2004-09-01 day: 01
PublicationDecade	2000
PublicationPlace	London
PublicationPlace_xml	– name: London – name: England
PublicationTitle	Nature cell biology
PublicationTitleAbbrev	Nat Cell Biol
PublicationTitleAlternate	Nat Cell Biol
PublicationYear	2004
Publisher	Nature Publishing Group UK Nature Publishing Group
Publisher_xml	– name: Nature Publishing Group UK – name: Nature Publishing Group
References	DW Nicholson (BFncb1159_CR6) 1997; 22 J Chai (BFncb1159_CR34) 2000; 406 XB Qiu (BFncb1159_CR35) 2004; 23 H Steller (BFncb1159_CR3) 1995; 267 AM Verhagen (BFncb1159_CR13) 2000; 102 S Dan (BFncb1159_CR42) 1999; 18 JC Reed (BFncb1159_CR17) 1997; 387 Y Tsujimoto (BFncb1159_CR18) 2003; 195 X Wang (BFncb1159_CR10) 2001; 15 E Arama (BFncb1159_CR37) 2003; 4 QL Deveraux (BFncb1159_CR22) 1999; 18 SY Vernooy (BFncb1159_CR30) 2002; 12 Z Chen (BFncb1159_CR28) 1999; 264 M Naito (BFncb1159_CR43) 1997; 89 P Li (BFncb1159_CR16) 1997; 91 QL Deveraux (BFncb1159_CR19) 1999; 13 L Yang (BFncb1159_CR33) 2003; 63 K Sakai (BFncb1159_CR41) 1997; 237 N Roy (BFncb1159_CR23) 1997; 16 X Liu (BFncb1159_CR11) 1996; 86 S Nagata (BFncb1159_CR1) 1997; 88 H Okada (BFncb1159_CR40) 2002; 22 GS Salvesen (BFncb1159_CR21) 2002; 3 BFncb1159_CR38 MO Hengartner (BFncb1159_CR2) 2000; 407 Y Yang (BFncb1159_CR26) 2000; 288 JC Reed (BFncb1159_CR8) 2000; 7 HP Hauser (BFncb1159_CR29) 1998; 141 JC Reed (BFncb1159_CR4) 1999; 17 GS Salvesen (BFncb1159_CR7) 1997; 91 QL Deveraux (BFncb1159_CR24) 1997; 388 C Du (BFncb1159_CR12) 2000; 102 SM Srinivasula (BFncb1159_CR31) 2001; 410 Y Suzuki (BFncb1159_CR14) 2001; 8 H Zou (BFncb1159_CR15) 1997; 90 V Jesenberger (BFncb1159_CR36) 2002; 3 J Yuan (BFncb1159_CR5) 2003; 40 G Kroemer (BFncb1159_CR9) 2000; 6 BA Hay (BFncb1159_CR20) 2000; 7 C Sun (BFncb1159_CR25) 1999; 401 H Kanuka (BFncb1159_CR39) 1999; 4 AM Hunter (BFncb1159_CR32) 2003; 278 Y Suzuki (BFncb1159_CR27) 2001; 98 15340445 - Nat Cell Biol. 2004 Sep;6(9):804-6
References_xml	– volume: 18 start-page: 1277 year: 1999 ident: BFncb1159_CR42 publication-title: Oncogene doi: 10.1038/sj.onc.1202423 – volume: 388 start-page: 300 year: 1997 ident: BFncb1159_CR24 publication-title: Nature doi: 10.1038/40901 – volume: 7 start-page: 1145 year: 2000 ident: BFncb1159_CR8 publication-title: Cell Death Differ. doi: 10.1038/sj.cdd.4400777 – volume: 12 start-page: 1164 year: 2002 ident: BFncb1159_CR30 publication-title: Curr. Biol. doi: 10.1016/S0960-9822(02)00935-1 – volume: 141 start-page: 1415 year: 1998 ident: BFncb1159_CR29 publication-title: J. Cell Biol. doi: 10.1083/jcb.141.6.1415 – volume: 237 start-page: 318 year: 1997 ident: BFncb1159_CR41 publication-title: Biochem. Biophys. Res. Commun. doi: 10.1006/bbrc.1997.7111 – volume: 91 start-page: 479 year: 1997 ident: BFncb1159_CR16 publication-title: Cell doi: 10.1016/S0092-8674(00)80434-1 – volume: 88 start-page: 355 year: 1997 ident: BFncb1159_CR1 publication-title: Cell doi: 10.1016/S0092-8674(00)81874-7 – volume: 3 start-page: 401 year: 2002 ident: BFncb1159_CR21 publication-title: Nature Rev. Mol. Cell Biol. doi: 10.1038/nrm830 – volume: 102 start-page: 43 year: 2000 ident: BFncb1159_CR13 publication-title: Cell doi: 10.1016/S0092-8674(00)00009-X – volume: 86 start-page: 147 year: 1996 ident: BFncb1159_CR11 publication-title: Cell doi: 10.1016/S0092-8674(00)80085-9 – volume: 406 start-page: 855 year: 2000 ident: BFncb1159_CR34 publication-title: Nature doi: 10.1038/35022514 – volume: 288 start-page: 874 year: 2000 ident: BFncb1159_CR26 publication-title: Science doi: 10.1126/science.288.5467.874 – volume: 22 start-page: 299 year: 1997 ident: BFncb1159_CR6 publication-title: Trends Biochem. Sci. doi: 10.1016/S0968-0004(97)01085-2 – volume: 102 start-page: 33 year: 2000 ident: BFncb1159_CR12 publication-title: Cell doi: 10.1016/S0092-8674(00)00008-8 – volume: 17 start-page: 2941 year: 1999 ident: BFncb1159_CR4 publication-title: J. Clin. Oncol. doi: 10.1200/JCO.1999.17.9.2941 – volume: 16 start-page: 6914 year: 1997 ident: BFncb1159_CR23 publication-title: EMBO J. doi: 10.1093/emboj/16.23.6914 – volume: 4 start-page: 757 year: 1999 ident: BFncb1159_CR39 publication-title: Mol. Cell doi: 10.1016/S1097-2765(00)80386-X – volume: 22 start-page: 3509 year: 2002 ident: BFncb1159_CR40 publication-title: Mol. Cell. Biol. doi: 10.1128/MCB.22.10.3509-3517.2002 – volume: 8 start-page: 613 year: 2001 ident: BFncb1159_CR14 publication-title: Mol. Cell doi: 10.1016/S1097-2765(01)00341-0 – volume: 410 start-page: 112 year: 2001 ident: BFncb1159_CR31 publication-title: Nature doi: 10.1038/35065125 – volume: 267 start-page: 1445 year: 1995 ident: BFncb1159_CR3 publication-title: Science doi: 10.1126/science.7878463 – volume: 98 start-page: 8662 year: 2001 ident: BFncb1159_CR27 publication-title: Proc. Natl Acad. Sci. USA doi: 10.1073/pnas.161506698 – volume: 387 start-page: 773 year: 1997 ident: BFncb1159_CR17 publication-title: Nature doi: 10.1038/42867 – volume: 3 start-page: 112 year: 2002 ident: BFncb1159_CR36 publication-title: Nature Rev. Mol. Cell Biol. doi: 10.1038/nrm731 – volume: 401 start-page: 818 year: 1999 ident: BFncb1159_CR25 publication-title: Nature doi: 10.1038/44617 – volume: 91 start-page: 443 year: 1997 ident: BFncb1159_CR7 publication-title: Cell doi: 10.1016/S0092-8674(00)80430-4 – volume: 6 start-page: 513 year: 2000 ident: BFncb1159_CR9 publication-title: Nature Med. doi: 10.1038/74994 – volume: 278 start-page: 7494 year: 2003 ident: BFncb1159_CR32 publication-title: J. Biol. Chem. doi: 10.1074/jbc.C200695200 – volume: 195 start-page: 158 year: 2003 ident: BFncb1159_CR18 publication-title: J. Cell. Physiol. doi: 10.1002/jcp.10254 – volume: 407 start-page: 770 year: 2000 ident: BFncb1159_CR2 publication-title: Nature doi: 10.1038/35037710 – volume: 4 start-page: 687 year: 2003 ident: BFncb1159_CR37 publication-title: Dev. Cell doi: 10.1016/S1534-5807(03)00120-5 – volume: 89 start-page: 2060 year: 1997 ident: BFncb1159_CR43 publication-title: Blood doi: 10.1182/blood.V89.6.2060 – volume: 15 start-page: 2922 year: 2001 ident: BFncb1159_CR10 publication-title: Genes Dev. – volume: 264 start-page: 847 year: 1999 ident: BFncb1159_CR28 publication-title: Biochem. Biophys. Res. Commun. doi: 10.1006/bbrc.1999.1585 – volume: 40 start-page: 401 year: 2003 ident: BFncb1159_CR5 publication-title: Neuron doi: 10.1016/S0896-6273(03)00601-9 – volume: 90 start-page: 405 year: 1997 ident: BFncb1159_CR15 publication-title: Cell doi: 10.1016/S0092-8674(00)80501-2 – volume: 63 start-page: 831 year: 2003 ident: BFncb1159_CR33 publication-title: Cancer Res. – volume: 23 start-page: 800 year: 2004 ident: BFncb1159_CR35 publication-title: EMBO J. doi: 10.1038/sj.emboj.7600075 – ident: BFncb1159_CR38 doi: 10.1038/nsb989 – volume: 7 start-page: 1045 year: 2000 ident: BFncb1159_CR20 publication-title: Cell Death Differ. doi: 10.1038/sj.cdd.4400765 – volume: 18 start-page: 5242 year: 1999 ident: BFncb1159_CR22 publication-title: EMBO J. doi: 10.1093/emboj/18.19.5242 – volume: 13 start-page: 239 year: 1999 ident: BFncb1159_CR19 publication-title: Genes Dev. doi: 10.1101/gad.13.3.239 – reference: 15340445 - Nat Cell Biol. 2004 Sep;6(9):804-6
SSID	ssj0014407
Score	2.2568033
Snippet	Apollon (also known as BRUCE or BIRC6) is a large protein containing baculoviral-IAP-repeat (BIR) and ubiquitin-conjugating enzyme (UBC) domains at the amino-...
SourceID	proquest gale pubmed crossref springer
SourceType	Aggregation Database Index Database Enrichment Source Publisher
StartPage	849
SubjectTerms	Animals Apoptosis Cancer Research Carrier Proteins - metabolism Caspase 9 Caspases - metabolism Cell Biology Cellular proteins Cysteine Endopeptidases - metabolism Cytochromes Developmental Biology Fetal Death Humans Inhibitor of Apoptosis Proteins Intracellular Signaling Peptides and Proteins Life Sciences Mice Mice, Knockout Mitochondrial Proteins - metabolism Neoplasm Proteins - genetics Neoplasm Proteins - metabolism Neoplasm Proteins - physiology Physiological aspects Physiology Protective Agents Stem Cells U937 Cells Ubiquitin-Conjugating Enzymes - metabolism
Title	Apollon ubiquitinates SMAC and caspase-9, and has an essential cytoprotection function
URI	https://link.springer.com/article/10.1038/ncb1159 https://www.ncbi.nlm.nih.gov/pubmed/15300255 https://www.proquest.com/docview/222374493 https://www.proquest.com/docview/66836925
Volume	6
hasFullText	1
inHoldings	1
isFullTextHit
isPrint
link	http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfR1dT9RAcKIQE1-I-FlAXI3RFze03e3XkzkJBE0gBsTcW7NflUtIe9D2gX_vTLt3cGfiQ9M2O91td2fno_MF8JFyZIm0yLmKUs2lTmKuhTI8DFWuXKziRFDs8OlZenIpf0yTqffNab1b5YImDoTaNob-kR8QH8ukLMTX-Q2nolFkXPUVNB7DZoSCCFVuyKZLfYvMltkYXJTwDOWAMWaWMoIf1EajKFSsMKN1kvyAJ60ZSQfec_wMtrzQyCbjKm_DI1c_hydjGcm7F_B7Mm_IfM56PbvpZ92sJgGSXZxODpmqLTMKyUbrePFluL1SLZ4ZJQ2vcX9fM3PXNT5fA64SI1ZHFy_h8vjo1-EJ9_USuEG9o-NOutRao5FHC5knqYuFrWRijZGhkGFuCyWjyGaoEVtZJcI5qUUmkF2FuJQoC76Cjbqp3RtgurAauworkWqJIKpQkTRVLHVYVSaMA_i0mLjS-GTiVNPiuhyM2iIv_QwHwJaA8zF_xr8gH2jmS8pGUZO7yx_Vt235_eK8nBDByekI4LMHqhocyCgfPYCvSwmsViD3ViBxu5iV5t3FApd-u7blErkCeLdspQfJA612Td-WaZojTsdJAK9HrLj_nEQMmlkA7xdoct_z2rfu_Hf0XXg6OgaRC9sebHS3vXuLMk-n9wfM3ofNb0dnP8__AsILAGA
linkProvider	ProQuest
linkToHtml	http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1Lb9NAEB6VVAguiDemhRrE44JVx7t27EOFQmmV0CZCfaDezL4MkZCdYlsoP47_xoy9TkmQuPUQOZHH6-x4dmbWM_MNwCvCyGJREnuiH0mPyzDwJBPK830RCxOIIGRUOzyZRqNz_ukivNiA310tDKVVdjqxUdS6UPSOfJfs2IDzhL2fX3rUNIqCq10HDWE7K-i9BmHM1nUcmcUv3MGVe-OP-LhfB8Hhwdn-yLNNBjyFznrlGW4irZVEw8Z4HEYmYDrjoVaK-4z7sU4E7_f1ALeRmmchM4ZLNmCo432cPzpQOO4N2OT0_qQHmx8Opp9PlmEMzpt6bdRGoTdAT6St2iVM8t1cSXTGkhVzuG4U_rKKa2Haxvod3oU71m11h62c3YMNk9-Hm20jy8UD-DKcFxTAd2s5u6xn1SwnF9Y9nQz3XZFrVwlUXKXxknfNz--ixKNLsOXIThxXLarCIkagnLhkbOnLQzi_FmY-gl5e5OYJuDLREofyMxZJjiQiEX2usoBLP8uUHzjwpmNcqiycOXXV-JE2YXUWp5bDDrhLwnmL4PEvyUvifEp4GDkl3HwTdVmm49OTdEgqL6aPA28tUVbgjZSw9Qv4dwlCa4Vye4USF6xaOb3VPeDUKowyXYq3AzvLs3Qh5cDlpqjLNIpiXFVB6MDjViquphOyZm_owItOTK5GXpvr0__efQdujc4mx-nxeHq0BbfbNCVKqNuGXvWzNs_QA6vkcyvnLny97qX1B8X_QbQ
linkToPdf	http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3db9NADLfGJhAviG_CBguIjxeiprlLmjxMqGyrVsaqaWNob-G-slVCSUcSof6J_FfYyaWjReJtD1Uaxbkkjs_2xfbPAG8II4tFSeyJfiQ9LsPAk0woz_dFLEwggpBR7fDRJDo445_Pw_M1-N3VwlBaZacTG0WtC0XfyHtkxwacJ6yX2ayI473Rx9mVRw2kKNDaddMQtsuC3mnQxmyNx6GZ_8LVXLkz3sNX_zYIRvtfdw8823DAU-i4V57hJtJaSTRyjMdhZAKmMx5qpbjPuB_rRPB-Xw9wSal5FjJjuGQDhvreR16gM4Xj3oKNARp9XAdufNqfHJ8sQhqcN7XbqJlCDymCtoKX8Ml7uZLomCVLpnHVQPxlIVdCto0lHN2He9aFdYetzD2ANZM_hNttU8v5I_g2nBUUzHdrOb2qp9U0J3fWPT0a7roi164SqMRK4yUfmt1LUeLWJQhzZCeOq-ZVYdEjUGZcMrz05zGc3Qgzn8B6XuTmGbgy0RKH8jMWSY4kIhF9rrKASz_LlB848K5jXKostDl12PiRNiF2FqeWww64C8JZi-bxL8lr4nxK2Bg5idmFqMsyHZ-epENSfzH9HHhvibICL6SErWXA2yU4rSXKrSVKnLxq6fBm94JTqzzKdCHqDmwvjtKJlA-Xm6Iu0yiKcYYFoQNPW6m4fpyQNetEB151YnI98sqzPv_v1bfhDk6x9Mt4crgJd9uMJcqt24L16mdtXqAzVsmXVsxd-H7TM-sP-25F-A
openUrl	ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Apollon+ubiquitinates+SMAC+and+caspase-9%2C+and+has+an+essential+cytoprotection+function&rft.jtitle=Nature+cell+biology&rft.au=Hao%2C+Yanyan&rft.au=Sekine%2C+Keiko&rft.au=Kawabata%2C+Atsushi&rft.au=Nakamura%2C+Hitoshi&rft.date=2004-09-01&rft.issn=1465-7392&rft.volume=6&rft.issue=9&rft.spage=849&rft_id=info:doi/10.1038%2Fncb1159&rft_id=info%3Apmid%2F15300255&rft.externalDocID=15300255
thumbnail_l	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1465-7392&client=summon
thumbnail_m	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1465-7392&client=summon
thumbnail_s	http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1465-7392&client=summon