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PMID: 10411904 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

TID1, a human homolog of the Drosophila tumor suppressor l(2)tid, encodes two mitochondrial modulators of apoptosis with opposing functions.

Syken J, De-Medina T, Münger K

Abstract

Mitochondria have emerged as central regulators of apoptosis. Here, we show that TID1, a human homolog of the Drosophila tumor suppressor lethal (2) tumorous imaginal discs, l(2)tid, encodes two mitochondrial matrix proteins, designated hTid-1(L) and hTid-1(S). These splice variants are both highly conserved members of the DnaJ family of proteins, which regulate the activity of and confer substrate specificity to Hsp70 proteins. Both hTid-1(L) and hTid-1(S) coimmunoprecipitate with mitochondrial Hsp70. Expression of hTid-1(L) or hTid-1(S) have no apparent capacity to induce apoptosis but have opposing effects on apoptosis induced by exogenous stimuli. Expression of hTid-1(L) increases apoptosis induced by both the DNA-damaging agent mitomycin c and tumor necrosis factor alpha. This activity is J domain-dependent, because a J domain mutant of hTid-1(L) can dominantly suppress apoptosis. In sharp contrast, expression of hTid-1(S) suppresses apoptosis, whereas expression of a J domain mutant of hTid-1(S) increases apoptosis. Hence, we propose that TID1 gene products act to positively and negatively modulate apoptotic signal transduction or effector structures within the mitochondrial matrix.

MeSH Terms
Alternative Splicing Amino Acid Sequence Animals Apoptosis/genetics Caspases/metabolism Cloning, Molecular Cytochrome c Group/metabolism Drosophila/genetics Drosophila Proteins Genes, Tumor Suppressor/genetics HSP40 Heat-Shock Proteins HSP70 Heat-Shock Proteins/metabolism Heat-Shock Proteins/chemistry,genetics Humans Microscopy, Fluorescence Mitochondria/chemistry Mitochondrial Proteins Mitomycin/pharmacology Molecular Sequence Data Signal Transduction Tumor Cells, Cultured Tumor Necrosis Factor-alpha/pharmacology
Chemicals
CG5504 protein, Drosophila Cytochrome c Group DNAJA3 protein, human Drosophila Proteins HSP40 Heat-Shock Proteins HSP70 Heat-Shock Proteins Heat-Shock Proteins Mitochondrial Proteins Tumor Necrosis Factor-alpha Mitomycin Caspases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Syken J
Department of Pathology and Harvard Center for Cancer Biology, Harvard Medical School, Boston, MA 02115, USA.
De-Medina T
Münger K
References (30)
30 references, click to expand
  1. The protein import machinery of the mitochondrial inner membrane.
    Trends Biochem Sci. 1994 Sep;19(9):368-72 PMID: 7985230
  2. DnaJ-like proteins: molecular chaperones and specific regulators of Hsp70.
    Trends Biochem Sci. 1994 Apr;19(4):176-81 PMID: 8016869
  3. A conserved HPD sequence of the J-domain is necessary for YDJ1 stimulation of Hsp70 ATPase activity at a site distinct from substrate binding.
    J Biol Chem. 1996 Apr 19;271(16):9347-54 PMID: 8621599
  4. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c.
    Cell. 1996 Jul 12;86(1):147-57 PMID: 8689682
  5. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease.
    J Exp Med. 1996 Oct 1;184(4):1331-41 PMID: 8879205
  6. Mitochondrial control of apoptosis.
    Immunol Today. 1997 Jan;18(1):44-51 PMID: 9018974
  7. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked.
    Science. 1997 Feb 21;275(5303):1129-32 PMID: 9027314
  8. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis.
    Science. 1997 Feb 21;275(5303):1132-6 PMID: 9027315
  9. Mitochondrial permeability transition is a central coordinating event of apoptosis.
    J Exp Med. 1996 Sep 1;184(3):1155-60 PMID: 9064332
  10. Apoptosis by death factor.
    Cell. 1997 Feb 7;88(3):355-65 PMID: 9039262
  11. Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system.
    EMBO J. 1997 Aug 1;16(15):4639-49 PMID: 9303308
  12. Cytochrome c: can't live with it--can't live without it.
    Cell. 1997 Nov 28;91(5):559-62 PMID: 9393848
  13. The Hsp70 and Hsp60 chaperone machines.
    Cell. 1998 Feb 6;92(3):351-66 PMID: 9476895
  14. Mitochondrial localization and temporal expression of the Drosophila melanogaster DnaJ homologous tumor suppressor Tid50.
    Cell Stress Chaperones. 1998 Mar;3(1):12-27 PMID: 9585178
  15. The Mitochondrial F0F1-ATPase proton pump is required for function of the proapoptotic protein Bax in yeast and mammalian cells.
    Mol Cell. 1998 Feb;1(3):327-36 PMID: 9660917
  16. A novel human DnaJ protein, hTid-1, a homolog of the Drosophila tumor suppressor protein Tid56, can interact with the human papillomavirus type 16 E7 oncoprotein.
    Virology. 1998 Jul 20;247(1):74-85 PMID: 9683573
  17. Mitochondria and apoptosis.
    Science. 1998 Aug 28;281(5381):1309-12 PMID: 9721092
  18. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors.
    Cell. 1998 Aug 21;94(4):481-90 PMID: 9727491
  19. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis.
    Cell. 1998 Aug 21;94(4):491-501 PMID: 9727492
  20. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis.
    Science. 1998 Sep 25;281(5385):2027-31 PMID: 9748162
  21. J proteins catalytically activate Hsp70 molecules to trap a wide range of peptide sequences.
    Mol Cell. 1998 Nov;2(5):593-603 PMID: 9844632
  22. Molecular characterization of mitochondrial apoptosis-inducing factor.
    Nature. 1999 Feb 4;397(6718):441-6 PMID: 9989411
  23. Nucleotide sequence of the Escherichia coli dnaJ gene and purification of the gene product.
    J Biol Chem. 1986 Feb 5;261(4):1778-81 PMID: 3003084
  24. The nucleotide sequence of the Escherichia coli K12 dnaJ+ gene. A gene that encodes a heat shock protein.
    J Biol Chem. 1986 Feb 5;261(4):1782-5 PMID: 3003085
  25. Transport into mitochondria and intramitochondrial sorting of the Fe/S protein of ubiquinol-cytochrome c reductase.
    Cell. 1986 Dec 26;47(6):939-51 PMID: 3022944
  26. Cleavage-site motifs in mitochondrial targeting peptides.
    Protein Eng. 1990 Oct;4(1):33-7 PMID: 2290832
  27. Eukaryotic homologues of Escherichia coli dnaJ: a diverse protein family that functions with hsp70 stress proteins.
    Mol Biol Cell. 1993 Jun;4(6):555-63 PMID: 8374166
  28. Role of the major heat shock proteins as molecular chaperones.
    Annu Rev Cell Biol. 1993;9:601-34 PMID: 8280473
  29. The NH2-terminal 108 amino acids of the Escherichia coli DnaJ protein stimulate the ATPase activity of DnaK and are sufficient for lambda replication.
    J Biol Chem. 1994 Feb 18;269(7):5446-51 PMID: 8106526
  30. Tumor suppression in Drosophila is causally related to the function of the lethal(2) tumorous imaginal discs gene, a dnaJ homolog.
    Dev Genet. 1995;16(1):64-76 PMID: 7758246
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1999-07-20
Pages
8499-504
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC17545
Subset
IM
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