Abstract
Identification of new anti-apoptotic genes is important for understanding the molecular mechanisms underlying apoptosis and tumorigenesis. The present study identified a novel anti-apoptotic gene named AREL1, which encodes a HECT (homologous to E6-AP carboxyl terminus) family E3 ubiquitin ligase. AREL1 interacted with and ubiquitinated IAP antagonists such as SMAC, HtrA2, and ARTS. However, AREL1 was cytosolic and did not localize to nuclei or mitochondria. The interactions between AREL1 and the IAP antagonists were specific for apoptosis-stimulated cells, in which the IAP antagonists were released into the cytosol from mitochondria. Furthermore, the ubiquitination and degradation of SMAC, HtrA2, and ARTS were significantly enhanced in AREL1-expressing cells following apoptotic stimulation, indicating that AREL1 binds to and ubiquitinates cytosolic but not mitochondria-associated forms of IAP antagonists. Furthermore, the anti-apoptotic role of AREL1-mediated degradation of SMAC, HtrA2, and ARTS was shown by simultaneous knockdown of three IAP antagonists, which caused the inhibition of caspase-3 cleavage, XIAP degradation, and induction of apoptosis. Therefore, the present study suggests that AREL1-mediated ubiquitination and degradation of cytosolic forms of three IAP antagonists plays an important role in the regulation of apoptosis.
MeSH Terms
Amino Acid Sequence
Animals
Apoptosis/physiology
Apoptosis Regulatory Proteins
Carrier Proteins/genetics,metabolism
Cell Line, Tumor
High-Temperature Requirement A Serine Peptidase 2
Humans
Inhibitor of Apoptosis Proteins/genetics,metabolism
Intracellular Signaling Peptides and Proteins/genetics,metabolism
Mice
Mitochondrial Proteins/genetics,metabolism
Molecular Sequence Data
Proteolysis
Septins/genetics,metabolism
Serine Endopeptidases/genetics,metabolism
Ubiquitin-Protein Ligases/genetics,metabolism
Ubiquitination/physiology
Chemicals
Apoptosis Regulatory Proteins
Carrier Proteins
DIABLO protein, human
Diablo protein, mouse
Inhibitor of Apoptosis Proteins
Intracellular Signaling Peptides and Proteins
Mitochondrial Proteins
Ubiquitin-Protein Ligases
Serine Endopeptidases
HTRA2 protein, human
High-Temperature Requirement A Serine Peptidase 2
Htra2 protein, mouse
SEPTIN4 protein, human
Septins
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Kim Jung-Bin
Department of Microbiology and Immunology, College of Medicine, Dankook University, Cheonan 330-714, Korea.
Kim So Youn
Kim Byeong Mo
Lee Hunjin
Kim Insook
Yun Jeanho
Jo Yejin
Oh Taeheun
Jo Yongsam
Chae Hee-Don
Shin Deug Y
References (30)
30 references, click to expand
-
Nedd4-like proteins: an emerging family of ubiquitin-protein ligases implicated in diverse cellular functions.
Trends Cell Biol. 1999 May;9(5):166-9
PMID: 10322449
-
Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction.
J Biol Chem. 2002 Jan 4;277(1):432-8
PMID: 11606597
-
Identification of XAF1 as an antagonist of XIAP anti-Caspase activity.
Nat Cell Biol. 2001 Feb;3(2):128-33
PMID: 11175744
-
Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins.
Cell. 2000 Jul 7;102(1):43-53
PMID: 10929712
-
Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition.
Cell. 2000 Jul 7;102(1):33-42
PMID: 10929711
-
The mitochondrial serine protease HtrA2/Omi: an overview.
Cell Death Differ. 2008 Mar;15(3):453-60
PMID: 18174901
-
A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death.
Mol Cell. 2001 Sep;8(3):613-21
PMID: 11583623
-
A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase.
Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2563-7
PMID: 7708685
-
IAP-targeted therapies for cancer.
Oncogene. 2008 Oct 20;27(48):6252-75
PMID: 18931692
-
The mitochondrial ARTS protein promotes apoptosis through targeting XIAP.
EMBO J. 2004 Apr 7;23(7):1627-35
PMID: 15029247
-
A combined assay of cell viability and in vitro cytotoxicity with a highly water-soluble tetrazolium salt, neutral red and crystal violet.
Biol Pharm Bull. 1996 Nov;19(11):1518-20
PMID: 8951178
-
IAP family proteins--suppressors of apoptosis.
Genes Dev. 1999 Feb 1;13(3):239-52
PMID: 9990849
-
Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA.
Nature. 1993 Jan 28;361(6410):365-9
PMID: 8381212
-
Bcl-xL and E1B-19K proteins inhibit p53-induced irreversible growth arrest and senescence by preventing reactive oxygen species-dependent p38 activation.
J Biol Chem. 2004 Apr 23;279(17):17765-71
PMID: 14764594
-
Deregulation of Cdk2 causes Bim-mediated apoptosis in p53-deficient tumors following actin damage.
Oncogene. 2008 Jul 3;27(29):4115-21
PMID: 18345036
-
The serine protease Omi/HtrA2 is released from mitochondria during apoptosis. Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity.
Cell Death Differ. 2002 Jan;9(1):20-6
PMID: 11803371
-
Regulation of apoptosis in Drosophila.
Cell Death Differ. 2008 Jul;15(7):1132-8
PMID: 18437164
-
Smurf2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-beta signaling.
J Biol Chem. 2000 Nov 24;275(47):36818-22
PMID: 11016919
-
p53 and DNA-dependent protein kinase catalytic subunit independently function in regulating actin damage-induced tetraploid G1 arrest.
Exp Mol Med. 2012 Mar 31;44(3):236-40
PMID: 22198295
-
Direct interaction of Smac with NADE promotes TRAIL-induced apoptosis.
Biochem Biophys Res Commun. 2004 Jun 25;319(2):649-54
PMID: 15178455
-
Caspases: intracellular signaling by proteolysis.
Cell. 1997 Nov 14;91(4):443-6
PMID: 9390553
-
Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade.
Nature. 1995 Jan 5;373(6509):81-3
PMID: 7800044
-
An exegesis of IAPs: salvation and surprises from BIR motifs.
Trends Cell Biol. 1999 Aug;9(8):323-8
PMID: 10407412
-
Expression cloning, developmental expression and chromosomal localization of fibroblast growth factor-8.
Oncogene. 1995 May 18;10(10):2051-5
PMID: 7761105
-
The human anti-apoptotic proteins cIAP1 and cIAP2 bind but do not inhibit caspases.
J Biol Chem. 2006 Feb 10;281(6):3254-60
PMID: 16339151
-
Identification of the yeast 20S proteasome catalytic centers and subunit interactions required for active-site formation.
Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7156-61
PMID: 9207060
-
XIAP as a ubiquitin ligase in cellular signaling.
Cell Death Differ. 2010 Jan;17(1):54-60
PMID: 19590513
-
Autocrine TNFalpha signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis.
Cancer Cell. 2007 Nov;12(5):445-56
PMID: 17996648
-
X-linked IAP is a direct inhibitor of cell-death proteases.
Nature. 1997 Jul 17;388(6639):300-4
PMID: 9230442
-
Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family.
EMBO Rep. 2006 Oct;7(10):988-94
PMID: 17016456