O-linked β-N-acetylglucosamine transferase plays an essential role in heart development through regulating angiopoietin-1

English version

Autoři: Yongxin Mu ^aff001; Houzhi Yu ^aff001; Tongbin Wu ^aff001; Jianlin Zhang ^aff001; Sylvia M. Evans ^aff001; Ju Chen ^aff001
Působiště autorů: Department of Medicine-Cardiology, University of California San Diego,Gilman Drive, Mail Code, La Jolla, California, United States of America ^aff001; Department of Cardiology, Shandong Provincial Hospital affiliated to Shandong University, Jinan, China ^aff002; Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California at San Diego, La Jolla, CA, United States of America ^aff003
Vyšlo v časopise: O-linked β-N-acetylglucosamine transferase plays an essential role in heart development through regulating angiopoietin-1. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008730
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008730

Souhrn

O-linked N-acetylglucosamine (GlcNAc) transferase (OGT) is the only enzyme catalyzing O-GlcNAcylation. Although it has been shown that OGT plays an essential role in maintaining postnatal heart function, its role in heart development remains unknown. Here we showed that loss of OGT in early fetal cardiomyocytes led to multiple heart developmental defects including hypertrabeculation, biventricular dilation, atrial septal defects, ventricular septal defects, and defects in coronary vessel development. In addition, RNA sequencing revealed that Angiopoietin-1, required within cardiomyocytes for both myocardial and coronary vessel development, was dramatically downregulated in cardiomyocyte-specific OGT knockout mouse hearts. In conclusion, our data demonstrated that OGT plays an essential role in regulating heart development through activating expression of cardiomyocyte Angiopoietin-1.

Klíčová slova:

Cardiomyocytes – Coronary arteries – Embryos – Heart – Heart development – Immunostaining – Mouse models – Ventricular septal defects

Zdroje

1. Bond MR, Hanover JA. A little sugar goes a long way: the cell biology of O-GlcNAc. J Cell Biol. 2015;208(7):869–80. Epub 2015/04/01. doi: 10.1083/jcb.201501101 25825515; PubMed Central PMCID: PMC4384737.

2. Torres CR, Hart GW. Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes. Evidence for O-linked GlcNAc. J Biol Chem. 1984;259(5):3308–17. Epub 1984/03/10. 6421821.

3. Hahne H, Gholami AM, Kuster B. Discovery of O-GlcNAc-modified proteins in published large-scale proteome data. Mol Cell Proteomics. 2012;11(10):843–50. Epub 2012/06/05. doi: 10.1074/mcp.M112.019463 22661428; PubMed Central PMCID: PMC3494142.

4. Hahne H, Sobotzki N, Nyberg T, Helm D, Borodkin VS, van Aalten DM, et al. Proteome wide purification and identification of O-GlcNAc-modified proteins using click chemistry and mass spectrometry. J Proteome Res. 2013;12(2):927–36. Epub 2013/01/11. doi: 10.1021/pr300967y 23301498; PubMed Central PMCID: PMC4946622.

5. Qin W, Lv P, Fan X, Quan B, Zhu Y, Qin K, et al. Quantitative time-resolved chemoproteomics reveals that stable O-GlcNAc regulates box C/D snoRNP biogenesis. Proc Natl Acad Sci U S A. 2017;114(33):E6749–E58. Epub 2017/08/02. doi: 10.1073/pnas.1702688114 28760965; PubMed Central PMCID: PMC5565422.

6. Mailleux F, Gelinas R, Beauloye C, Horman S, Bertrand L. O-GlcNAcylation, enemy or ally during cardiac hypertrophy development? Biochim Biophys Acta. 2016;1862(12):2232–43. Epub 2016/08/22. doi: 10.1016/j.bbadis.2016.08.012 27544701.

7. Yki-Jarvinen H, Vogt C, Iozzo P, Pipek R, Daniels MC, Virkamaki A, et al. UDP-N-acetylglucosamine transferase and glutamine: fructose 6-phosphate amidotransferase activities in insulin-sensitive tissues. Diabetologia. 1997;40(1):76–81. Epub 1997/01/01. doi: 10.1007/s001250050645 9028721.

8. Lunde IG, Aronsen JM, Kvaloy H, Qvigstad E, Sjaastad I, Tonnessen T, et al. Cardiac O-GlcNAc signaling is increased in hypertrophy and heart failure. Physiol Genomics. 2012;44(2):162–72. Epub 2011/12/01. doi: 10.1152/physiolgenomics.00016.2011 22128088.

9. Watson LJ, Facundo HT, Ngoh GA, Ameen M, Brainard RE, Lemma KM, et al. O-linked beta-N-acetylglucosamine transferase is indispensable in the failing heart. Proc Natl Acad Sci U S A. 2010;107(41):17797–802. Epub 2010/09/30. doi: 10.1073/pnas.1001907107 20876116; PubMed Central PMCID: PMC2955091.

10. Watson LJ, Long BW, DeMartino AM, Brittian KR, Readnower RD, Brainard RE, et al. Cardiomyocyte Ogt is essential for postnatal viability. Am J Physiol Heart Circ Physiol. 2014;306(1):H142–53. Epub 2013/11/05. doi: 10.1152/ajpheart.00438.2013 24186210; PubMed Central PMCID: PMC3920156.

11. Augustin HG, Koh GY, Thurston G, Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol. 2009;10(3):165–77. Epub 2009/02/24. doi: 10.1038/nrm2639 19234476.

12. Fukuhara S, Sako K, Noda K, Zhang J, Minami M, Mochizuki N. Angiopoietin-1/Tie2 receptor signaling in vascular quiescence and angiogenesis. Histol Histopathol. 2010;25(3):387–96. Epub 2010/01/08. doi: 10.14670/HH-25.387 20054809.

13. Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V, et al. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell. 1996;87(7):1161–9. Epub 1996/12/27. doi: 10.1016/s0092-8674(00)81812-7 8980223.

14. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, et al. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell. 1996;87(7):1171–80. Epub 1996/12/27. doi: 10.1016/s0092-8674(00)81813-9 8980224.

15. Arita Y, Nakaoka Y, Matsunaga T, Kidoya H, Yamamizu K, Arima Y, et al. Myocardium-derived angiopoietin-1 is essential for coronary vein formation in the developing heart. Nat Commun. 2014;5 : 4552. Epub 2014/07/30. doi: 10.1038/ncomms5552 25072663; PubMed Central PMCID: PMC4124867.

16. Jeansson M, Gawlik A, Anderson G, Li C, Kerjaschki D, Henkelman M, et al. Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J Clin Invest. 2011;121(6):2278–89. Epub 2011/05/25. doi: 10.1172/JCI46322 21606590; PubMed Central PMCID: PMC3104773.

17. Jiao K, Kulessa H, Tompkins K, Zhou Y, Batts L, Baldwin HS, et al. An essential role of Bmp4 in the atrioventricular septation of the mouse heart. Genes Dev. 2003;17(19):2362–7. Epub 2003/09/17. doi: 10.1101/gad.1124803 12975322; PubMed Central PMCID: PMC218073.

18. Moses KA, DeMayo F, Braun RM, Reecy JL, Schwartz RJ. Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis. 2001;31(4):176–80. Epub 2002/01/10. doi: 10.1002/gene.10022 11783008.

19. Zhang Z, Mu Y, Zhang J, Zhou Y, Cattaneo P, Veevers J, et al. Kindlin-2 Is Essential for Preserving Integrity of the Developing Heart and Preventing Ventricular Rupture. Circulation. 2019;139(12):1554–6. Epub 2019/03/19. doi: 10.1161/CIRCULATIONAHA.118.038383 30883226; PubMed Central PMCID: PMC6424132.

20. Arima Y, Miyagawa-Tomita S, Maeda K, Asai R, Seya D, Minoux M, et al. Preotic neural crest cells contribute to coronary artery smooth muscle involving endothelin signalling. Nat Commun. 2012;3 : 1267. Epub 2012/12/13. doi: 10.1038/ncomms2258 23232397.

21. Agah R, Frenkel PA, French BA, Michael LH, Overbeek PA, Schneider MD. Gene recombination in postmitotic cells. Targeted expression of Cre recombinase provokes cardiac-restricted, site-specific rearrangement in adult ventricular muscle in vivo. J Clin Invest. 1997;100(1):169–79. Epub 1997/07/01. doi: 10.1172/JCI119509 9202069; PubMed Central PMCID: PMC508177.

22. Davis J, Maillet M, Miano JM, Molkentin JD. Lost in transgenesis: a user's guide for genetically manipulating the mouse in cardiac research. Circ Res. 2012;111(6):761–77. Epub 2012/09/01. doi: 10.1161/CIRCRESAHA.111.262717 22935533; PubMed Central PMCID: PMC3466061.

23. Zimna A, Kurpisz M. Hypoxia-Inducible Factor-1 in Physiological and Pathophysiological Angiogenesis: Applications and Therapies. Biomed Res Int. 2015;2015 : 549412. Epub 2015/07/07. doi: 10.1155/2015/549412 26146622; PubMed Central PMCID: PMC4471260.

24. Guimaraes-Camboa N, Stowe J, Aneas I, Sakabe N, Cattaneo P, Henderson L, et al. HIF1alpha Represses Cell Stress Pathways to Allow Proliferation of Hypoxic Fetal Cardiomyocytes. Dev Cell. 2015;33(5):507–21. Epub 2015/06/02. doi: 10.1016/j.devcel.2015.04.021 26028220; PubMed Central PMCID: PMC4509618.

25. Dupays L, Shang C, Wilson R, Kotecha S, Wood S, Towers N, et al. Sequential Binding of MEIS1 and NKX2-5 on the Popdc2 Gene: A Mechanism for Spatiotemporal Regulation of Enhancers during Cardiogenesis. Cell Rep. 2015;13(1):183–95. Epub 2015/09/29. doi: 10.1016/j.celrep.2015.08.065 26411676; PubMed Central PMCID: PMC4597108.

26. Kim HS, Woo JS, Joo HJ, Moon WK. Cardiac transcription factor Nkx2.5 is downregulated under excessive O-GlcNAcylation condition. PLoS One. 2012;7(6):e38053. Epub 2012/06/22. doi: 10.1371/journal.pone.0038053 22719862; PubMed Central PMCID: PMC3376112.

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