Embryonic organizer formation disorder leads to multiorgan dysplasia in Down syndrome.


Journal

Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092

Informations de publication

Date de publication:
19 12 2022
Historique:
received: 17 08 2022
accepted: 12 12 2022
revised: 08 12 2022
entrez: 19 12 2022
pubmed: 20 12 2022
medline: 22 12 2022
Statut: epublish

Résumé

Despite the high prevalence of Down syndrome (DS) and early identification of the cause (trisomy 21), its molecular pathogenesis has been poorly understood and specific treatments have consequently been practically unavailable. A number of medical conditions throughout the body associated with DS have prompted us to investigate its molecular etiology from the viewpoint of the embryonic organizer, which can steer the development of surrounding cells into specific organs and tissues. We established a DS zebrafish model by overexpressing the human DYRK1A gene, a highly haploinsufficient gene located at the "critical region" within 21q22. We found that both embryonic organizer and body axis were significantly impaired during early embryogenesis, producing abnormalities of the nervous, heart, visceral, and blood systems, similar to those observed with DS. Quantitative phosphoproteome analysis and related assays demonstrated that the DYRK1A-overexpressed zebrafish embryos had anomalous phosphorylation of β-catenin and Hsp90ab1, resulting in Wnt signaling enhancement and TGF-β inhibition. We found an uncovered ectopic molecular mechanism present in amniocytes from fetuses diagnosed with DS and isolated hematopoietic stem cells (HSCs) of DS patients. Importantly, the abnormal proliferation of DS HSCs could be recovered by switching the balance between Wnt and TGF-β signaling in vitro. Our findings provide a novel molecular pathogenic mechanism in which ectopic Wnt and TGF-β lead to DS physical dysplasia, suggesting potential targeted therapies for DS.

Identifiants

pubmed: 36535930
doi: 10.1038/s41419-022-05517-x
pii: 10.1038/s41419-022-05517-x
pmc: PMC9763398
doi:

Substances chimiques

Transforming Growth Factor beta 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1054

Informations de copyright

© 2022. The Author(s).

Références

Proc Natl Acad Sci U S A. 2012 Oct 23;109(43):17579-84
pubmed: 23045701
Carcinogenesis. 2008 Jan;29(1):84-92
pubmed: 18048388
Dev Med Child Neurol. 2004 Apr;46(4):282-6
pubmed: 15077706
Genes Dev. 2000 Dec 15;14(24):3093-101
pubmed: 11124802
Proc Natl Acad Sci U S A. 2008 Jul 8;105(27):9244-9
pubmed: 18591668
Cytokine Growth Factor Rev. 2000 Mar-Jun;11(1-2):23-35
pubmed: 10708950
Biol Open. 2018 Apr 26;7(4):
pubmed: 29700199
Endocrinology. 2015 Mar;156(3):1171-80
pubmed: 25490145
J Invest Dermatol. 2019 Jul;139(7):1497-1505.e5
pubmed: 30684555
Sci Rep. 2017 Nov 10;7(1):15313
pubmed: 29127398
Nat Rev Genet. 2017 Mar;18(3):147-163
pubmed: 28029161
Genet Med. 2009 Sep;11(9):611-6
pubmed: 19636252
EMBO Rep. 2015 Jan;16(1):44-62
pubmed: 25520324
CNS Neurol Disord Drug Targets. 2014 Feb;13(1):26-33
pubmed: 24152332
PLoS Biol. 2004 Feb;2(2):E30
pubmed: 14966532
Eur J Hum Genet. 2009 Apr;17(4):454-66
pubmed: 19002211
Pharmacol Ther. 2019 Feb;194:199-221
pubmed: 30268771
Cancer Cell. 2007 Dec;12(6):514-27
pubmed: 18068629
Am J Physiol Renal Physiol. 2017 Jul 1;313(1):F30-F46
pubmed: 28298358
Biochemistry. 2004 Dec 14;43(49):15510-9
pubmed: 15581363
Aust Fam Physician. 2011 Apr;40(4):202-8
pubmed: 21597529
J Biol Chem. 2011 Dec 16;286(50):43250-8
pubmed: 21940632
Nat Rev Genet. 2007 May;8(5):353-67
pubmed: 17440532
Clin Proteomics. 2013 Feb 08;10(1):2
pubmed: 23394617
J Biol Chem. 2011 Dec 2;286(48):41589-41599
pubmed: 21984848
Annu Rev Genomics Hum Genet. 2007;8:17-35
pubmed: 17386002
Nat Genet. 2007 Feb;39(2):189-98
pubmed: 17237784
Am J Hum Genet. 2008 Oct;83(4):479-88
pubmed: 18940310
Nat Commun. 2019 Mar 8;10(1):1146
pubmed: 30850588
Dev Dyn. 2010 Jan;239(1):34-44
pubmed: 19623618
J Pediatr Health Care. 2014 Jan-Feb;28(1):105-10
pubmed: 23891027
Birth Defects Res. 2021 Mar;113(4):371-381
pubmed: 33470056
Genes Dev. 2014 Apr 15;28(8):858-74
pubmed: 24736844
Nat Commun. 2017 May 30;8:15494
pubmed: 28555642
Development. 2018 Mar 9;145(5):
pubmed: 29523654
Am J Transl Res. 2020 Aug 15;12(8):4757-4771
pubmed: 32913548
J Neurosci. 2016 Mar 30;36(13):3648-59
pubmed: 27030752
Trends Mol Med. 2006 Oct;12(10):473-9
pubmed: 16935027
Nature. 2018 Jun;558(7708):132-135
pubmed: 29795348
J Biol Chem. 2013 Oct 18;288(42):30708-30719
pubmed: 24005672
Oncol Lett. 2015 Dec;10(6):3722-3726
pubmed: 26788197
Int J Mol Cell Med. 2016 Summer;5(3):125-133
pubmed: 27942498
J Biol Chem. 2015 Jul 3;290(27):17029-40
pubmed: 25995454
Biomed Rep. 2014 Nov;2(6):787-792
pubmed: 25279146
PLoS One. 2015 May 08;10(5):e0126532
pubmed: 25955392
Exp Cell Res. 1995 Apr;217(2):404-9
pubmed: 7698241
Nature. 2006 Jun 1;441(7093):595-600
pubmed: 16554754
Trends Pharmacol Sci. 2010 Feb;31(2):66-73
pubmed: 19963286
J Perinatol. 2005 May;25(5):341-8
pubmed: 15861199
Science. 2018 Nov 23;362(6417):
pubmed: 30467143
Nature. 2000 May 18;405(6784):311-9
pubmed: 10830953
Oncotarget. 2019 Apr 26;10(31):2930-2946
pubmed: 31105876
Nat Cell Biol. 2010 Aug;12(8):781-90
pubmed: 20639871

Auteurs

Yanyan Liu (Y)

Prenatal Diagnosis Center, Department of Medical Genetics, Department of Obstetrics & Gynecologic, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Ziyuan Lin (Z)

SCU-CUHK Joint Laboratory for Reproductive Medicine, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Ying Peng (Y)

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, Sichuan Province, 610041, People's Republic of China.

Yan Jiang (Y)

Department of prenatal Diagnosis, Mianyang People's Hospital, Mianyang, 621000, Sichuan Province, People's Republic of China.

Xuan Zhang (X)

Prenatal Diagnosis Center, Department of Medical Genetics, Department of Obstetrics & Gynecologic, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Hongmei Zhu (H)

Prenatal Diagnosis Center, Department of Medical Genetics, Department of Obstetrics & Gynecologic, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Lili Zhang (L)

Prenatal Diagnosis Center, Department of Medical Genetics, Department of Obstetrics & Gynecologic, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Jiurong Chen (J)

Prenatal Diagnosis Center, Department of Medical Genetics, Department of Obstetrics & Gynecologic, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Xianghua Shu (X)

Department of Obstetrics, Mianyang People's Hospital, Mianyang, 621000, Sichuan Province, People's Republic of China.

Min Luo (M)

Prenatal Diagnosis Center, Department of Medical Genetics, Department of Obstetrics & Gynecologic, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Dan Xie (D)

Prenatal Diagnosis Center, Department of Medical Genetics, Department of Obstetrics & Gynecologic, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Yan Chen (Y)

SCU-CUHK Joint Laboratory for Reproductive Medicine, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Huijuan Liao (H)

SCU-CUHK Joint Laboratory for Reproductive Medicine, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Mingfeng Liu (M)

SCU-CUHK Joint Laboratory for Reproductive Medicine, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Xiaohu Zhang (X)

SCU-CUHK Joint Laboratory for Reproductive Medicine, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Shanling Liu (S)

Prenatal Diagnosis Center, Department of Medical Genetics, Department of Obstetrics & Gynecologic, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

He Wang (H)

Prenatal Diagnosis Center, Department of Medical Genetics, Department of Obstetrics & Gynecologic, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Bin Zhou (B)

Laboratory of Molecular Translational Medicine, Center for Translational Medicine, Department of Obstetrics and Gynecology, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China.

Huaqin Sun (H)

SCU-CUHK Joint Laboratory for Reproductive Medicine, Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu, 610041, People's Republic of China. sunhuaqin@scu.edu.cn.

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