Adaptor protein Src-homology 2 domain containing E (SH2E) deficiency induces heart defect in zebrafish.

CRISPR/Cas9 Src-homology 2 domain containing E cardiac development pericardial edema zebrafish

Journal

Acta pharmacologica Sinica
ISSN: 1745-7254
Titre abrégé: Acta Pharmacol Sin
Pays: United States
ID NLM: 100956087

Informations de publication

Date de publication:
23 Sep 2024
Historique:
received: 03 05 2024
accepted: 05 09 2024
revised: 04 09 2024
medline: 24 9 2024
pubmed: 24 9 2024
entrez: 23 9 2024
Statut: aheadofprint

Résumé

Adaptor proteins play crucial roles in signal transduction across diverse signaling pathways. Src-homology 2 domain-containing E (SH2E) is the adaptor protein highly expressed in vascular endothelial cells and myocardium during zebrafish embryogenesis. In this study we investigated the function and mechanisms of SH2E in cardiogenesis. We first analyzed the spatiotemporal expression of SH2E and then constructed zebrafish lines with SH2E deficiency using the CRISPR-Cas9 system. We showed that homozygous mutants developed progressive pericardial edema (PCE), dilated atrium, abnormal atrioventricular looping and thickened atrioventricular wall from 3 days post fertilization (dpf) until death; inducible overexpression of SH2E was able to partially rescue the PCE phenotype. Using transcriptome sequencing analysis, we demonstrated that the MAPK/ERK and NF-κB signaling pathways might be involved in SH2E-deficiency-caused PCE. This study underscores the pivotal role of SH2E in cardiogenesis, and might help to identify innovative diagnostic techniques and therapeutic strategies for congenital heart disease.

Identifiants

pubmed: 39313516
doi: 10.1038/s41401-024-01392-8
pii: 10.1038/s41401-024-01392-8
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Shanghai Institute of Materia Medica, Chinese Academy of Sciences and Chinese Pharmacological Society.

Références

Waksman G, Kumaran S, Lubman O. SH2 domains: role, structure and implications for molecular medicine. Expert Rev Mol Med. 2004;6:1–18.
pubmed: 14987415 doi: 10.1017/S1462399404007331
Huang YJ, Zhu L, Tan JY, Guo WC, Yang Z, Shi WH, et al. Correlation between SHP-1 and carotid plaque vulnerability in humans. Cardiovasc Pathol. 2020;49:107258.
pubmed: 32674045 doi: 10.1016/j.carpath.2020.107258
Pandit B, Sarkozy A, Pennacchio LA, Carta C, Oishi K, Martinelli S, et al. Gain-of-function RAF1 mutations cause Noonan and LEOPARD syndromes with hypertrophic cardiomyopathy. Nat Genet. 2007;39:1007–12.
pubmed: 17603483 doi: 10.1038/ng2073
Tartaglia M, Mehler EL, Goldberg R, Zampino G, Brunner HG, Kremer H, et al. Mutations in PTPN11, encoding the protein tyrosine phosphatase SHP-2, cause Noonan syndrome. Nat Genet. 2001;29:465–8.
pubmed: 11704759 doi: 10.1038/ng772
Legius E, Schrander-Stumpel C, Schollen E, Pulles-Heintzberger C, Gewillig M, Fryns JP. PTPN11 mutations in LEOPARD syndrome. J Med Genet. 2002;39:571–4.
pubmed: 12161596 pmcid: 1735195 doi: 10.1136/jmg.39.8.571
Lu YG, Tan H, Ma Q, Li XX, Cui J, Zhang X, et al. SH2 domain-containing protein tyrosine phosphatase-2 (SHP-2) prevents cardiac remodeling after myocardial infarction through ERK/SMAD signaling pathway. Hum Cell. 2021;34:325–34.
pubmed: 33415691 doi: 10.1007/s13577-020-00430-x
Kontaridis MI, Yang WT, Bence KK, Cullen Darragh, Wang B, Bodyak N, et al. Deletion of Ptpn11 (Shp2) in cardiomyocytes causes dilated cardiomyopathy via effects on the extracellular signal–regulated kinase/mitogen-activated protein kinase and RhoA signaling pathways. Circulation. 2008;117:1423–35.
pubmed: 18316486 pmcid: 2394674 doi: 10.1161/CIRCULATIONAHA.107.728865
Bonetti M, Paardekooper Overman J, Tessadori F, Noël E, Bakkers J, den Hertog J. Noonan and LEOPARD syndrome Shp2 variants induce heart displacement defects in zebrafish. Development. 2014;141:1961–70.
pubmed: 24718990 doi: 10.1242/dev.106310
Flynn DC. Adaptor proteins. Oncogene. 2001;20:6270–2.
pubmed: 11607828 doi: 10.1038/sj.onc.1204769
Diogo CV, Suski JM, Lebiedzinska M, Karkucinska-Wieckowska A, Wojtala A, Pronicki M, et al. Cardiac mitochondrial dysfunction during hyperglycemia—the role of oxidative stress and p66Shc signaling. Int J Biochem Cell Biol. 2013;45:114–22.
pubmed: 22776741 doi: 10.1016/j.biocel.2012.07.004
Akhmedov A, Montecucco F, Braunersreuther V, Camici GG, Jakob P, Reiner MF, et al. Genetic deletion of the adaptor protein p66Shc increases susceptibility to short-term ischaemic myocardial injury via intracellular salvage pathways. Eur Heart J. 2015;36:516–26.
pubmed: 25336219 doi: 10.1093/eurheartj/ehu400
Oda T, Kujovich J, Reis M, Newman B, Druker BJ, et al. Identification and characterization of two novel SH2 domain-containing proteins from a yeast two hybrid screen with the ABL tyrosine kinase. Oncogene. 1997;15:1255–62.
pubmed: 9315092 doi: 10.1038/sj.onc.1201299
Wong KS, Proulx K, Rost MS, Sumanas S. Identification of vasculature‐specific genes by microarray analysis of Etsrp/Etv2 overexpressing zebrafish embryos. Dev Dyn. 2009;238:1836–50.
pubmed: 19504456 doi: 10.1002/dvdy.21990
Chen J, Zhu RF, Li FF, Liang YL, Wang C, Qin YW, et al. MicroRNA-126a directs lymphangiogenesis through interacting with chemokine and Flt4 signaling in zebrafish. Arterioscler Thromb Vasc Biol. 2016;36:2381–93.
pubmed: 27789478 doi: 10.1161/ATVBAHA.116.308120
Olson EN. Gene regulatory networks in the evolution and development of the heart. Science. 2006;313:1922–7.
pubmed: 17008524 pmcid: 4459601 doi: 10.1126/science.1132292
Fahed AC, Gelb BD, Seidman JG, Seidman CE. Genetics of congenital heart disease: the glass half empty. Circ Res. 2013;112:707–20.
pubmed: 23410880 doi: 10.1161/CIRCRESAHA.112.300853
Asnani A, Peterson RT. The zebrafish as a tool to identify novel therapies for human cardiovascular disease. Dis Model Mech. 2014;7:763–7.
pubmed: 24973746 pmcid: 4073266 doi: 10.1242/dmm.016170
Huang CJ, Tu CT, Hsiao CD, Hsieh FJ, Tsai HJ. Germ‐line transmission of a myocardium‐specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish. Dev Dyn. 2003;228:30–40.
pubmed: 12950077 doi: 10.1002/dvdy.10356
Kawakami K, Takeda H, Kawakami N, Kobasashi M, Matsuda N, Mishina M. A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell. 2004;7:133–44.
pubmed: 15239961 doi: 10.1016/j.devcel.2004.06.005
Brown DR, Samsa LA, Qian L, Liu JD. Advances in the study of heart development and disease using zebrafish. J Cardiovasc Dev Dis. 2016;3:13.
pubmed: 27335817 pmcid: 4913704
Stainier DY. Zebrafish genetics and vertebrate heart formation. Nat Rev Genet. 2001;2:39–48.
pubmed: 11253067 doi: 10.1038/35047564
Bakkers J. Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc Res. 2011;91:279–88.
pubmed: 21602174 pmcid: 3125074 doi: 10.1093/cvr/cvr098
González-Rosa JM. Zebrafish models of cardiac disease: From fortuitous mutants to precision medicine. Cir Res. 2022;130:1803–26.
doi: 10.1161/CIRCRESAHA.122.320396
Doyon Y, McCammon JM, Miller JC, Faraji F, Ngo C, Katibah GE, et al. Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat Biotechnol. 2008;26:702–8.
pubmed: 18500334 pmcid: 2674762 doi: 10.1038/nbt1409
Bedell VM, Wang Y, Campbell JM, Poshusta TL, Starker CG, Krug II RG, et al. In vivo genome editing using a high-efficiency TALEN system. Nature. 2012;491:114–8.
pubmed: 23000899 pmcid: 3491146 doi: 10.1038/nature11537
Hwang WY, Fu YF, Reyon D, Maeder ML, Tsai SQ, Sander JD, et al. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol. 2013;31:227–9.
pubmed: 23360964 pmcid: 3686313 doi: 10.1038/nbt.2501
Li FF, Liang YL, Han XS, Guan YN, Chen J, Wu P, et al. ADP receptor P2y12 prevents excessive primitive hematopoiesis in zebrafish by inhibiting Gata1. Acta Pharmacol Sin. 2021;42:414–21.
pubmed: 32555443 doi: 10.1038/s41401-020-0431-5
Thisse C, Thisse B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc. 2008;3:59–69.
pubmed: 18193022 doi: 10.1038/nprot.2007.514
He JB, Mo DS, Chen JY, Luo LF. Combined whole-mount fluorescence in situ hybridization and antibody staining in zebrafish embryos and larvae. Nat Protoc. 2020;15:3361–79.
pubmed: 32908315 doi: 10.1038/s41596-020-0376-7
Copper JE, Budgeon LR, Foutz CA, van Rossum DB, Vanselow DJ, hubley MJ, et al. Comparative analysis of fixation and embedding techniques for optimized histological preparation of zebrafish. Comp Biochem Physiol C Toxicol Pharmacol. 2018;208:38–46.
pubmed: 29157956 doi: 10.1016/j.cbpc.2017.11.003
Zhang RL, Yang JC, Zhu J, Xu XL. Depletion of zebrafish Tcap leads to muscular dystrophy via disrupting sarcomere–membrane interaction, not sarcomere assembly. Hum Mol Genet. 2009;18:4130–40.
pubmed: 19679566 pmcid: 2758143 doi: 10.1093/hmg/ddp362
French VM, van de Laar IM, Wessels MW, Rohe C, Roos-Hesselink JW, Wang GL, et al. NPHP4 variants are associated with pleiotropic heart malformations. Circ Res. 2012;110:1564–74.
pubmed: 22550138 pmcid: 3916111 doi: 10.1161/CIRCRESAHA.112.269795
Slanchev K, Pütz M, Schmitt A, Kramer-Zucker A, Walz G. Nephrocystin-4 is required for pronephric duct-dependent cloaca formation in zebrafish. Hum Mol Genet. 2011;20:3119–28.
pubmed: 21596840 doi: 10.1093/hmg/ddr214
Schleich JM, Abdulla T, Summers R, Houyel L. An overview of cardiac morphogenesis. Arch Cardiovasc Dis. 2013;106:612–23.
pubmed: 24138816 doi: 10.1016/j.acvd.2013.07.001
Desgrange A, Le Garrec JF, Meilhac SM. Left-right asymmetry in heart development and disease: forming the right loop. Development. 2018;145:dev162776.
pubmed: 30467108 doi: 10.1242/dev.162776
Hu B, Lelek S, Spanjaard B, EI-Sammak H, Simões MG, Mintcheva J, et al. Origin and function of activated fibroblast states during zebrafish heart regeneration. Nat Genet. 2022;54:1227–37.
pubmed: 35864193 pmcid: 7613248 doi: 10.1038/s41588-022-01129-5
de Sena-Tomás C, Aleman AG, Ford C, Varshney A, Yao D, Harrington JK, et al. Activation of Nkx2. 5 transcriptional program is required for adult myocardial repair. Nat Commun. 2022;13:2970.
pubmed: 35624100 pmcid: 9142600 doi: 10.1038/s41467-022-30468-4
Lints TJ, Parsons LM, Hartley L, Lyons I, Harvey RP. Nkx-2. 5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development. 1993;119:419–31.
pubmed: 7904557 doi: 10.1242/dev.119.2.419
Lepilina A, Coon AN, Kikuchi K, Holdway JE, Roberts RW, Burns CG, et al. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell. 2006;127:607–19.
pubmed: 17081981 doi: 10.1016/j.cell.2006.08.052
Singleman C, Holtzman NG. Analysis of postembryonic heart development and maturation in the zebrafish, Danio rerio. Dev Dyn. 2012;241:1993–2004.
pubmed: 23074141 pmcid: 4446259 doi: 10.1002/dvdy.23882
Zenker M, Edouard T, Blair JC, Cappa M. Noonan syndrome: improving recognition and diagnosis. Arch Dis Child. 2022;107:1073–8.
pubmed: 35246453 doi: 10.1136/archdischild-2021-322858
Jiménez-Martínez M, Stamatakis K, Fresno M. The dual-specificity phosphatase 10 (DUSP10): its role in cancer, inflammation, and immunity. Int J Mol Sci. 2019;20:1626.
pubmed: 30939861 pmcid: 6480380 doi: 10.3390/ijms20071626
Gordon JW, Shaw JA, Kirshenbaum LA. Multiple facets of NF-κB in the heart: to be or not to NF-κB. Circ Res. 2011;108:1122–32.
pubmed: 21527742 doi: 10.1161/CIRCRESAHA.110.226928
Kim BY, Kang DO, Oh WK, Kim JH, Choi YK, Jang JS, et al. Involvement of SH2-SH2-SH3 domain of phospholipase Cγ1 in NF-κB signaling. FEBS Lett. 2000;472:45–9.
pubmed: 10781802 doi: 10.1016/S0014-5793(00)01415-0
Zelarayan L, Renger A, Noack C, Zafiriou MP, Gehrke C, van der Nagel R, et al. NF-κB activation is required for adaptive cardiac hypertrophy. Cardiovasc Res. 2009;84:416–24.
pubmed: 19620128 doi: 10.1093/cvr/cvp237
Ishida H, Kogaki S, Narita J, Ichimori H, Nawa N, Okada Y, et al. LEOPARD-type SHP2 mutant Gln510Glu attenuates cardiomyocyte differentiation and promotes cardiac hypertrophy via dysregulation of Akt/GSK-3β/β-catenin signaling. Am J Physiol Heart Circ Physiol. 2011;301:H1531–9.
pubmed: 21803945 doi: 10.1152/ajpheart.00216.2011
Marin TM, Keith K, Davies B, Conner DA, Guha P, Kalaitzidis D, et al. Rapamycin reverses hypertrophic cardiomyopathy in a mouse model of LEOPARD syndrome–associated PTPN11 mutation. J Clin Invest. 2011;121:1026–43.
pubmed: 21339643 pmcid: 3049377 doi: 10.1172/JCI44972
Schramm C, Fine DM, Edwards MA, Reeb AN, Krenz M. The PTPN11 loss-of-function mutation Q510E-Shp2 causes hypertrophic cardiomyopathy by dysregulating mTOR signaling. Am J Physiol Heart Circ Physiol. 2012;302:H231–43.
pubmed: 22058153 doi: 10.1152/ajpheart.00665.2011

Auteurs

Yu-Lai Liang (YL)

Laboratory of Molecular Immunology, State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai, 200438, China.
CAS Key Laboratory of Tissue Microenvironment and Tumor, Innovation Center for Intervention of Chronic Disease and Promotion of Health, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai, 200031, China.

Yang-Xi Hu (YX)

Department of Cardiology, Second Affiliated Hospital of Naval Medical University, Shanghai, 200003, China.
Department of Pharmacy, Second Affiliated Hospital of Naval Medical University, Shanghai, 200003, China.

Fang-Fang Li (FF)

Department of Cardiology, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200080, China. lifang091001@163.com.

Hong-Min You (HM)

Department of Cardiovascular Medicine, Changhai Hospital, Naval Medical University, Shanghai, 200433, China.

Jian Chen (J)

CAS Key Laboratory of Tissue Microenvironment and Tumor, Innovation Center for Intervention of Chronic Disease and Promotion of Health, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai, 200031, China.

Chun Liang (C)

Department of Cardiology, Second Affiliated Hospital of Naval Medical University, Shanghai, 200003, China.

Zhi-Fu Guo (ZF)

Department of Cardiovascular Medicine, Changhai Hospital, Naval Medical University, Shanghai, 200433, China.

Qing Jing (Q)

CAS Key Laboratory of Tissue Microenvironment and Tumor, Innovation Center for Intervention of Chronic Disease and Promotion of Health, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai, 200031, China. qjing@sibs.ac.cn.

Classifications MeSH