Proteolytic activation of angiomotin by DDI2 promotes angiogenesis.

Animals Mice Angiomotins Zebrafish / metabolism Microfilament Proteins / metabolism Peptide Hydrolases Intercellular Signaling Peptides and Proteins / genetics
AMOT DDI2 NF2 angiogenesis protease

Journal

The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664

Informations de publication

Date de publication:
01 08 2023
Historique:
revised: 23 05 2023
received: 24 10 2022
accepted: 06 06 2023
pmc-release: 23 06 2024
medline: 3 8 2023
pubmed: 23 6 2023
entrez: 23 6 2023
Statut: ppublish

Résumé

The scaffolding protein angiomotin (AMOT) is indispensable for vertebrate embryonic angiogenesis. Here, we report that AMOT undergoes cleavage in the presence of lysophosphatidic acid (LPA), a lipid growth factor also involved in angiogenesis. AMOT cleavage is mediated by aspartic protease DNA damage-inducible 1 homolog 2 (DDI2), and the process is tightly regulated by a signaling axis including neurofibromin 2 (NF2), tankyrase 1/2 (TNKS1/2), and RING finger protein 146 (RNF146), which induce AMOT membrane localization, poly ADP ribosylation, and ubiquitination, respectively. In both zebrafish and mice, the genetic inactivation of AMOT cleavage regulators leads to defective angiogenesis, and the phenotype is rescued by the overexpression of AMOT-CT, a C-terminal AMOT cleavage product. In either physiological or pathological angiogenesis, AMOT-CT is required for vascular expansion, whereas uncleavable AMOT represses this process. Thus, our work uncovers a signaling pathway that regulates angiogenesis by modulating a cleavage-dependent activation of AMOT.

Identifiants

DOI: 10.15252/embj.2022112900 PMID: 37350545 PMC: PMC10390880
pubmed: 37350545
doi: 10.15252/embj.2022112900
pmc: PMC10390880
doi:

Substances chimiques

Angiomotins 0
Microfilament Proteins 0
Peptide Hydrolases EC 3.4.-
Intercellular Signaling Peptides and Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e112900

Informations de copyright

© 2023 The Authors.

Références

J Biol Chem. 2013 Nov 22;288(47):34041-34051
pubmed: 24106267
Nat Rev Mol Cell Biol. 2016 Feb;17(2):97-109
pubmed: 26726037
Genes Cancer. 2011 Dec;2(12):1097-105
pubmed: 22866201
Mol Biol Cell. 2014 May;25(10):1676-85
pubmed: 24648494
Blood. 2009 Jan 1;113(1):244-53
pubmed: 18824598
Genes Dev. 2011 Jan 1;25(1):51-63
pubmed: 21205866
J Biol Chem. 2004 Mar 5;279(10):9417-23
pubmed: 14672936
Nat Med. 2003 Jun;9(6):653-60
pubmed: 12778163
Genes Dev. 2007 Aug 15;21(16):2055-68
pubmed: 17699752
Nat Cell Biol. 2006 Jan;8(1):27-36
pubmed: 16341207
Invest Ophthalmol Vis Sci. 2010 Jun;51(6):2813-26
pubmed: 20484600
Cell. 2019 Mar 7;176(6):1248-1264
pubmed: 30849371
Bio Protoc. 2018 Sep 05;8(17):e2995
pubmed: 34395793
Mol Cell. 2022 May 19;82(10):1850-1864.e7
pubmed: 35429439
J Clin Invest. 2017 Sep 1;127(9):3441-3461
pubmed: 28805663
Nat Med. 2003 Jun;9(6):677-84
pubmed: 12778166
Elife. 2016 Aug 16;5:
pubmed: 27528193
Nat Protoc. 2010 Sep;5(9):1518-34
pubmed: 20725067
J Biol Chem. 2013 Dec 27;288(52):37296-307
pubmed: 24225952
Cell. 2012 Aug 17;150(4):780-91
pubmed: 22863277
J Biol Chem. 2011 Dec 23;286(51):43972-43983
pubmed: 21971049
J Biol Chem. 2013 May 24;288(21):15181-93
pubmed: 23564455
J Vis Exp. 2009 May 07;(27):
pubmed: 19488022
FEBS Lett. 2014 Aug 19;588(16):2693-703
pubmed: 24548561
Proc Natl Acad Sci U S A. 2004 Mar 9;101(10):3338-45
pubmed: 14766969
FASEB J. 2015 Nov;29(11):4435-48
pubmed: 26169937
Biochem J. 2012 Jun 1;444(2):279-89
pubmed: 22385262
Blood. 2010 Dec 2;116(23):5060-70
pubmed: 20713964
Cell. 2006 May 5;125(3):535-48
pubmed: 16678097
Circ Res. 2018 Feb 16;122(4):591-605
pubmed: 29298775
Cell Rep. 2021 Aug 24;36(8):109596
pubmed: 34433060
Curr Biol. 2003 Apr 1;13(7):613-7
pubmed: 12676095
J Biol Chem. 2011 Feb 11;286(6):4364-70
pubmed: 21187284
Proc Natl Acad Sci U S A. 2017 Oct 10;114(41):10918-10923
pubmed: 28973878
Cell Signal. 2020 Nov;75:109775
pubmed: 32916277
Nat Protoc. 2009;4(11):1565-73
pubmed: 19816419
Annu Rev Biochem. 2004;73:321-54
pubmed: 15189145
J Cell Sci. 2016 Sep 15;129(18):3396-411
pubmed: 27521426
Science. 2019 Apr 12;364(6436):188-193
pubmed: 30975888
J Biol Chem. 2016 Jul 15;291(29):15256-66
pubmed: 27231341
Nat Rev Genet. 2003 Jul;4(7):544-58
pubmed: 12838346
Oncotarget. 2016 May 17;7(20):28765-82
pubmed: 27144834
Circ Res. 2009 Jul 31;105(3):260-70
pubmed: 19590046
Nat Commun. 2015 Oct 05;6:8357
pubmed: 26437443
EMBO Rep. 2012 Nov 6;13(11):984-91
pubmed: 23059978
FASEB J. 2008 Oct;22(10):3706-15
pubmed: 18606866
Annu Rev Physiol. 2017 Feb 10;79:43-66
pubmed: 27992732
Cell Rep. 2015 Oct 20;13(3):524-532
pubmed: 26456820
Elife. 2015 Jan 29;4:
pubmed: 25633977
Proc Natl Acad Sci U S A. 2013 Oct 22;110(43):17368-73
pubmed: 24101513
Mol Cell Biol. 2006 Jul;26(13):5015-22
pubmed: 16782887
Cancer Cell. 2016 Jun 13;29(6):783-803
pubmed: 27300434
Dev Cell. 2017 Sep 11;42(5):462-478.e7
pubmed: 28867486
Elife. 2016 Aug 16;5:
pubmed: 27528192
EMBO J. 2023 Aug 1;42(15):e112900
pubmed: 37350545
Cell Rep. 2021 Aug 24;36(8):109616
pubmed: 34433061
Nat Rev Cancer. 2003 Aug;3(8):582-91
pubmed: 12894246
Cell Res. 2019 Nov;29(11):895-910
pubmed: 31501519
Genes Dev. 2010 Aug 15;24(16):1718-30
pubmed: 20675406
Nat Commun. 2014 May 07;5:3743
pubmed: 24806444
J Biol Chem. 2011 Mar 4;286(9):7018-26
pubmed: 21224387
Genes Cancer. 2011 Dec;2(12):1117-33
pubmed: 22866203
Nat Rev Mol Cell Biol. 2007 Jun;8(6):464-78
pubmed: 17522591
Mol Biol Cell. 2011 Oct;22(19):3725-33
pubmed: 21832154
Dev Cell. 2010 Jul 20;19(1):27-38
pubmed: 20643348
Mol Cell. 2016 Dec 1;64(5):993-1008
pubmed: 27912098

Auteurs

Yu Wang (Y)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.
ORCID: 0000-0003-1070-2818

Yuwen Zhu (Y)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.
ORCID: 0000-0003-2059-075X

Yebin Wang (Y)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Yue Chang (Y)

School of Life Sciences, Fudan University, Shanghai, China.
TaiKang Medical School (School of Basic Medical Sciences), Hubei Provincial Key Laboratory of Developmentally Originated Disease, Wuhan University, Wuhan, China.

Fang Geng (F)

School of Life Sciences, Fudan University, Shanghai, China.
TaiKang Medical School (School of Basic Medical Sciences), Hubei Provincial Key Laboratory of Developmentally Originated Disease, Wuhan University, Wuhan, China.

Mingyue Ma (M)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Yuan Gu (Y)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Aijuan Yu (A)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Rui Zhu (R)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Pengcheng Yu (P)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Zhao Sha (Z)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Sixian Qi (S)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Jian Li (J)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Wencao Zhao (W)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.
Key Laboratory of Tissue Microenvironment and Tumor, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences (CAS), Shanghai, China.

Weijun Pan (W)

Key Laboratory of Tissue Microenvironment and Tumor, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences (CAS), Shanghai, China.

Ruilin Zhang (R)

TaiKang Medical School (School of Basic Medical Sciences), Hubei Provincial Key Laboratory of Developmentally Originated Disease, Wuhan University, Wuhan, China.
ORCID: 0000-0002-6594-450X

Fa-Xing Yu (FX)

Institute of Pediatrics, Children's Hospital of Fudan University, and the Shanghai Key Laboratory of Medical Epigenetics, the International Co-laboratory of Medical Epigenetics and Metabolism, the State Key Laboratory of Genetic Engineering, Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.
ORCID: 0000-0003-4834-9335

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Proteolytic activation of angiomotin by DDI2...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Proteolytic activation of angiomotin by DDI2...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Protéines adaptatrices de la transduction du signal › Angiomotines › Proteolytic activation of angiomotin by DDI2...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Poissons › Cypriniformes › Cyprinidae › Danio zébré › Proteolytic activation of angiomotin by DDI2...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines du cytosquelette › Protéines des microfilaments › Proteolytic activation of angiomotin by DDI2...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Hydrolases › Peptide hydrolases › Proteolytic activation of angiomotin by DDI2...
questionsmedicales.fr › Facteurs biologiques › Protéines et peptides de signalisation intercellulaire › Proteolytic activation of angiomotin by DDI2...