دورية أكاديمية

β1 integrins regulate cellular behaviour and cardiomyocyte organization during ventricular wall formation.

التفاصيل البيبلوغرافية
العنوان: β1 integrins regulate cellular behaviour and cardiomyocyte organization during ventricular wall formation.
المؤلفون: Miao L; Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204-5039, USA., Lu Y; Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204-5039, USA., Nusrat A; Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204-5039, USA., Zhao L; Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204-5039, USA., Castillo M; Department of Biology and Biochemistry, University of Houston Sequencing and Gene Editing Core, University of Houston, Houston, TX 77204-5001, USA., Xiao Y; Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204-5039, USA., Guo H; Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204-5039, USA., Liu Y; Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204-5039, USA., Gunaratne P; Department of Biology and Biochemistry, University of Houston Sequencing and Gene Editing Core, University of Houston, Houston, TX 77204-5001, USA., Schwartz RJ; Department of Biology and Biochemistry, University of Houston Sequencing and Gene Editing Core, University of Houston, Houston, TX 77204-5001, USA., Burns AR; College of Optometry, University of Houston, Houston, TX 77204-2020, USA., Kumar A; Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204-5039, USA., DiPersio CM; Department of Surgery, Albany Medical College, Albany, NY 12208, USA., Wu M; Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204-5039, USA.
المصدر: Cardiovascular research [Cardiovasc Res] 2024 Sep 21; Vol. 120 (11), pp. 1279-1294.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Oxford Journals Country of Publication: England NLM ID: 0077427 Publication Model: Print Cited Medium: Internet ISSN: 1755-3245 (Electronic) Linking ISSN: 00086363 NLM ISO Abbreviation: Cardiovasc Res Subsets: MEDLINE
أسماء مطبوعة: Publication: 2008- : Oxford : Oxford Journals
Original Publication: London, British Medical Assn.
مواضيع طبية MeSH: Integrin beta1*/metabolism , Integrin beta1*/genetics , Myocytes, Cardiac*/metabolism , Mice, Knockout* , Heart Ventricles*/metabolism , Extracellular Matrix*/metabolism , Fibronectins*/metabolism , Fibronectins*/genetics, Animals ; Gene Expression Regulation, Developmental ; Homeobox Protein Nkx-2.5/metabolism ; Homeobox Protein Nkx-2.5/genetics ; Cell Movement ; Signal Transduction ; Cell Shape ; Cell Proliferation ; Morphogenesis
مستخلص: Aims: The mechanisms regulating the cellular behaviour and cardiomyocyte organization during ventricular wall morphogenesis are poorly understood. Cardiomyocytes are surrounded by extracellular matrix (ECM) and interact with ECM via integrins. This study aims to determine whether and how β1 integrins regulate cardiomyocyte behaviour and organization during ventricular wall morphogenesis in the mouse.
Methods and Results: We applied mRNA deep sequencing and immunostaining to determine the expression repertoires of α/β integrins and their ligands in the embryonic heart. Integrin β1 subunit (β1) and some of its ECM ligands are asymmetrically distributed and enriched in the luminal side of cardiomyocytes, and fibronectin surrounds cardiomyocytes, creating a network for them. Itgb1, which encodes the β1, was deleted via Nkx2.5Cre/+ to generate myocardial-specific Itgb1 knockout (B1KO) mice. B1KO hearts display an absence of a trabecular zone but a thicker compact zone. The levels of hyaluronic acid and versican, essential for trabecular initiation, were not significantly different between control and B1KO. Instead, fibronectin, a ligand of β1, was absent in the myocardium of B1KO hearts. Furthermore, B1KO cardiomyocytes display a random cellular orientation and fail to undergo perpendicular cell division, be organized properly, and establish the proper tissue architecture to form trabeculae. Mosaic clonal lineage tracing showed that Itgb1 regulates cardiomyocyte transmural migration and proliferation autonomously.
Conclusion: β1 is asymmetrically localized in the cardiomyocytes, and some of its ECM ligands are enriched along the luminal side of the myocardium, and fibronectin surrounds cardiomyocytes. β1 integrins are required for cardiomyocytes to attach to the ECM network. This engagement provides structural support for cardiomyocytes to maintain shape, undergo perpendicular division, and establish cellular organization. Deletion of Itgb1 leads to loss of β1 and fibronectin and prevents cardiomyocytes from engaging the ECM network, resulting in failure to establish tissue architecture to form trabeculae.
Competing Interests: Conflict of interest: none declared.
(© The Author(s) 2024. Published by Oxford University Press on behalf of the European Society of Cardiology.)
التعليقات: Update of: bioRxiv. 2023 Aug 29:2023.08.28.555112. doi: 10.1101/2023.08.28.555112. (PMID: 37693495)
References: Nature. 2007 Nov 1;450(7166):56-62. (PMID: 17972876)
Dev Biol. 2004 May 1;269(1):81-94. (PMID: 15081359)
J Bone Miner Res. 2005 Jan;20(1):58-66. (PMID: 15619670)
J Supramol Struct Cell Biochem. 1981;16(4):345-8. (PMID: 6273596)
Genesis. 2007 Sep;45(9):593-605. (PMID: 17868096)
Circ Res. 2002 Mar 8;90(4):458-64. (PMID: 11884376)
Mol Cell Biol. 2000 Feb;20(3):755-9. (PMID: 10629031)
Cell Rep. 2016 Dec 6;17(10):2687-2699. (PMID: 27926871)
Dev Biol. 1996 May 1;175(2):301-13. (PMID: 8626034)
Genes Dev. 1995 Aug 1;9(15):1896-908. (PMID: 7544313)
Am J Pathol. 2012 Mar;180(3):952-962. (PMID: 22248583)
Proc Natl Acad Sci U S A. 2016 Jul 5;113(27):7569-74. (PMID: 27339140)
Dev Biol. 2016 Oct 1;418(1):157-165. (PMID: 27333774)
J Mol Cell Cardiol. 2001 Mar;33(3):521-32. (PMID: 11181020)
J Cell Biol. 2000 Sep 4;150(5):1149-60. (PMID: 10974002)
Dev Cell. 2009 Feb;16(2):233-44. (PMID: 19217425)
Anat Rec. 2000 Apr 1;258(4):319-37. (PMID: 10737851)
Pediatr Cardiol. 2018 Aug;39(6):1082-1089. (PMID: 29594501)
Development. 2011 Jan;138(2):303-15. (PMID: 21177343)
Dev Dyn. 1995 Nov;204(3):240-58. (PMID: 8573717)
Anat Rec A Discov Mol Cell Evol Biol. 2003 Sep;274(1):773-7. (PMID: 12923887)
Dev Cell. 2010 Jan 19;18(1):39-51. (PMID: 20152176)
Development. 2004 May;131(9):2219-31. (PMID: 15073151)
Proc Natl Acad Sci U S A. 2015 May 5;112(18):5726-31. (PMID: 25908119)
PLoS Genet. 2023 Jan 27;19(1):e1010630. (PMID: 36706168)
Proc Natl Acad Sci U S A. 2019 Jul 30;116(31):15560-15569. (PMID: 31300538)
Pediatr Res. 1999 May;45(5 Pt 1):635-42. (PMID: 10231856)
J Cardiovasc Pharmacol. 2010 Jun;55(6):567-73. (PMID: 20224428)
Biomol Concepts. 2015 Apr;6(2):137-48. (PMID: 25883210)
Circ Res. 2001 Jun 8;88(11):1112-9. (PMID: 11397776)
Dev Biol. 2001 Feb 15;230(2):230-42. (PMID: 11161575)
Development. 1995 Feb;121(2):549-60. (PMID: 7539359)
Cell Rep. 2014 Dec 24;9(6):2071-83. (PMID: 25497097)
Nat Genet. 1996 Jul;13(3):370-3. (PMID: 8673141)
Dev Cell. 2007 Mar;12(3):415-29. (PMID: 17336907)
Dev Dyn. 1994 Oct;201(2):108-20. (PMID: 7873784)
Science. 1999 Aug 13;285(5430):1028-32. (PMID: 10446041)
Aging Cell. 2014 Jun;13(3):431-40. (PMID: 24400780)
Circulation. 2019 Mar 19;139(12):1554-1556. (PMID: 30883226)
Sci Rep. 2018 Feb 8;8(1):2678. (PMID: 29422515)
Cell Rep. 2016 Apr 5;15(1):158-170. (PMID: 27052172)
Genesis. 2001 Dec;31(4):176-80. (PMID: 11783008)
Development. 2014 Jan;141(2):281-95. (PMID: 24335256)
Dev Dyn. 1996 May;206(1):100-11. (PMID: 9019241)
Cell. 2002 Sep 20;110(6):673-87. (PMID: 12297042)
Cell. 2008 Feb 22;132(4):583-97. (PMID: 18295577)
Bioessays. 1996 Jul;18(7):607. (PMID: 8757939)
Birth Defects Res A Clin Mol Teratol. 2011 Jun;91(6):535-50. (PMID: 21618406)
J Cell Biol. 2002 May 27;157(5):873-82. (PMID: 12021259)
Development. 2008 Jun;135(12):2193-202. (PMID: 18480158)
Nat Med. 2004 May;10(5):467-74. (PMID: 15122248)
Int J Dev Biol. 2002;46(4):431-9. (PMID: 12141429)
J Morphol. 1968 Jul;125(3):329-65. (PMID: 5678904)
Mol Cell Biol. 2008 Jan;28(2):794-802. (PMID: 17984225)
Blood. 1997 Oct 15;90(8):3073-81. (PMID: 9376588)
Dev Biol. 2014 Nov 15;395(2):232-44. (PMID: 25242040)
N Engl J Med. 1999 Mar 25;340(12):966-7. (PMID: 10094647)
J Cell Sci. 1996 Dec;109 ( Pt 13):2989-99. (PMID: 9004034)
J Neurosci. 2003 Mar 15;23(6):2314-22. (PMID: 12657690)
Cell Rep. 2016 Feb 23;14(7):1662-1672. (PMID: 26876178)
Circ Res. 2014 Jan 31;114(3):572-586. (PMID: 24481847)
Genes Dev. 1995 Aug 1;9(15):1883-95. (PMID: 7544312)
Am J Med Genet C Semin Med Genet. 2013 Aug;163C(3):144-56. (PMID: 23843320)
Nature. 2018 May;557(7705):439-445. (PMID: 29743679)
Dev Biol. 2013 Sep 1;381(1):73-82. (PMID: 23791818)
Development. 2010 Nov;137(22):3867-75. (PMID: 20978078)
J Vis Exp. 2016 Oct 7;(116):. (PMID: 27768060)
Dev Cell. 2010 Jul 20;19(1):114-25. (PMID: 20643355)
معلومات مُعتمدة: P30 EY007551 United States EY NEI NIH HHS; R01 AR081487 United States AR NIAMS NIH HHS; R01 AR059810 United States AR NIAMS NIH HHS; P30EY007551 United States EY NEI NIH HHS; R01 HL121700 United States HL NHLBI NIH HHS; 2R01HL121700-06A1 United States HL NHLBI NIH HHS; 20TPA35490051 American Heart Association
فهرسة مساهمة: Keywords: Cell behaviour; Cellular organization; Integrin-extracellular matrix interaction; Trabecular morphogenesis; Ventricular wall specification
المشرفين على المادة: 0 (Integrin beta1)
0 (Itgb1 protein, mouse)
0 (Fibronectins)
0 (Nkx2-5 protein, mouse)
0 (Homeobox Protein Nkx-2.5)
تواريخ الأحداث: Date Created: 20240525 Date Completed: 20240921 Latest Revision: 20240923
رمز التحديث: 20240923
مُعرف محوري في PubMed: PMC11416060
DOI: 10.1093/cvr/cvae111
PMID: 38794925
قاعدة البيانات: MEDLINE
الوصف
تدمد:1755-3245
DOI:10.1093/cvr/cvae111