Hyaluronan: A critical regulator of endothelial-to-mesenchymal transition during cardiac valve formation

Trends in Cardiovascular Medicine

Volumn 23, Issue 5, 2013, Pages 135-142

  Lagendijk, Anne Karine ^a   Szabó, András ^b,c   Merks, Roeland M H ^b,c,d   Bakkers, Jeroen ^e,f  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b CWI   (Netherlands)

^c Netherlands Institute for Systems Biology   (Netherlands)

^d LEIDEN UNIVERSITY   (Netherlands)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^f ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GLUCURONIC ACID; HYALURONAN SYNTHASE; HYALURONIC ACID; N ACETYLGLUCOSAMINE; SYNTHETASE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GLUCOSE DEHYDROGENASE; VASCULOTROPIN;

AORTA VALVE; BIOSYNTHESIS; CELL MEMBRANE; DEGRADATION; ENDOCARDIAL CUSHION; EPITHELIAL MESENCHYMAL TRANSITION; EXOSOME; EXTRACELLULAR MATRIX; HEART VALVE; HOMEOSTASIS; HUMAN; MITRAL VALVE; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ANIMALS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCURONOSYLTRANSFERASE; HEART VALVE DISEASES; HEART VALVES; HUMANS; HYALURONIC ACID; MICRORNAS; SIGNAL TRANSDUCTION;

EID: 84878872407     PISSN: 10501738     EISSN: 18732615     Source Type: Journal    
DOI: 10.1016/j.tcm.2012.10.002     Document Type: Review

References (52)

1. Aruffo A., Stamenkovic I., Melnick M., Underhill C.B., Seed B. CD44 is the principal cell surface receptor for hyaluronate. Cell 1990, 61(7):1303-1313.
2. Bakkers J., Kramer C., Pothof J., Quaedvlieg N.E., Spaink H.P., Hammerschmidt M. Has2 is required upstream of Rac1 to govern dorsal migration of lateral cells during zebrafish gastrulation. Development 2004, 131(3):525-537.
3. Banerji S., Ni J., Wang S.X., Clasper S., Su J., Tammi R., et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. Journal of Cell Biology 1999, 144(4):789-801.
4. Belle A., Tanay A., Bitincka L., Shamir R., O'Shea E.K. Quantification of protein half-lives in the budding yeast proteome. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(35):13004-13009.
5. Bernanke D.H., Orkin R.W. Hyaluronate binding and degradation by cultured embryonic chick cardiac cushion and myocardial cells. Developmental Biology 1984, 106(2):360-367.
6. Bernanke D.H., Orkin R.W. Hyaluronidase activity in embryonic chick heart muscle and cushion tissue and cells. Developmental Biology 1984, 106(2):351-359.
7. Bourguignon L.Y., Peyrollier K., Gilad E., Brightman A. Hyaluronan-CD44 interaction with neural Wiskott-Aldrich syndrome protein (N-WASP) promotes actin polymerization and ErbB2 activation leading to beta-catenin nuclear translocation, transcriptional up-regulation, and cell migration in ovarian tumor cells. Journal of Biological Chemistry 2007, 282(2):1265-1280.
8. Bourguignon L.Y., Zhu H., Chu A., Iida N., Zhang L., Hung M.C. Interaction between the adhesion receptor, CD44, and the oncogene product, p185HER2, promotes human ovarian tumor cell activation. Journal of Biological Chemistry 1997, 272(44):27913-27918.
9. Camenisch T.D., Biesterfeldt J., Brehm-Gibson T., Bradley J., McDonald J.A. Regulation of cardiac cushion development by hyaluronan. Experimental and Clinical Cardiology 2001, 6(1):4-10.
10. Camenisch T.D., Schroeder J.A., Bradley J., Klewer S.E., McDonald J.A. Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors. Nature Medicine 2002, 8(8):850-855.
11. Camenisch T.D., Spicer A.P., Brehm-Gibson T., Biesterfeldt J., Augustine M.L., Calabro A., et al. Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. Journal of Clinical Investigation 2000, 106(3):349-360.
12. Chang C.P., Neilson J.R., Bayle J.H., Gestwicki J.E., Kuo A., Stankunas K., et al. A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis. Cell 2004, 118(5):649-663.
13. Chao H., Spicer A.P. Natural antisense mRNAs to hyaluronan synthase 2 inhibit hyaluronan biosynthesis and cell proliferation. Journal of Biological Chemistry 2005, 280(30):27513-27522.
14. Cickovski T., Aras K., Swat M., Merks R.M.H., Glimm T., George H., et al. From genes to organisms via the cell: a problem-solving environment for multicellular development. Computing in Science and Engineering 2007, 9:50-60.
15. Collino F., Deregibus M.C., Bruno S., Sterpone L., Aghemo G., Viltono L., et al. Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS One 2010, 5(7):e11803.
16. Contreras E.G., Gaete M., Sanchez N., Carrasco H., Larrain J. Early requirement of hyaluronan for tail regeneration in Xenopus tadpoles. Development 2009, 136(17):2987-2996.
17. Csoka A.B., Frost G.I., Stern R. The six hyaluronidase-like genes in the human and mouse genomes. Matrix Biology 2001, 20(8):499-508.
18. Ebert M.S., Sharp P.A. Roles for microRNAs in conferring robustness to biological processes. Cell 2012, 149(3):515-524.
19. Erickson S.L., O'Shea K.S., Ghaboosi N., Loverro L., Frantz G., Bauer M., et al. ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice. Development 1997, 124(24):4999-5011.
20. Gierer A., Meinhardt H. A theory of biological pattern formation. Kybernetik 1972, 12(1):30-39.
21. Girish K.S., Kemparaju K. The magic glue hyaluronan and its eraser hyaluronidase: a biological overview. Life Sciences 2007, 80(21):1921-1943.
22. Gupta V., Barzilla J.E., Mendez J.S., Stephens E.H., Lee E.L., Collard C.D., et al. Abundance and location of proteoglycans and hyaluronan within normal and myxomatous mitral valves. Cardiovascular Pathology 2009, 18(4):191-197.
23. Hardwick C., Hoare K., Owens R., Hohn H.P., Hook M., Moore D., et al. Molecular cloning of a novel hyaluronan receptor that mediates tumor cell motility. Journal of Cell Biology 1992, 117(6):1343-1350.
24. Heinrich E.M., Dimmeler S. MicroRNAs and stem cells: control of pluripotency, reprogramming, and lineage commitment. Circulation Research 2012, 110(7):1014-1022.
25. Hergenreider E., Heydt S., Tréguer K., Boettger T., Horrevoets A.J.G., Zeiher A.M., et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nature Cell Biology 2012, 14(3):249-256.
26. Hurlstone A.F., Haramis A.P., Wienholds E., Begthel H., Korving J., Van Eeden F., et al. The Wnt/beta-catenin pathway regulates cardiac valve formation. Nature 2003, 425(6958):633-637.
27. Hyde A.S., Farmer E., Easley K.E., van Lammeren K., Christoffels V.M., Barycki J.J., et al. UDP-Glucose dehydrogenase polymorphisms from patients with congenital heart valve defects disrupt enzyme stability and quaternary assembly. Journal of Biological Chemistry 2012, epub july 2012, 10.1074/jbc.M112.395202.
28. Johansson B., Holmgren A., Hedstrom M., Engstrom-Laurent A., Engstrom K.G. Evaluation of hyaluronan and calcifications in stenotic and regurgitant aortic valves. European Journal of Cardiothoracic Surgery 2011, 39(1):27-32.
29. Kamikura D.M., Khoury H., Maroun C., Naujokas M.A., Park M. Enhanced transformation by a plasma membrane-associated met oncoprotein: activation of a phosphoinositide 3'-kinase-dependent autocrine loop involving hyaluronic acid and CD44. Molecular and Cellular Biology 2000, 20(10):3482-3496.
30. Lagendijk A.K., Goumans M.J., Burkhard S.B., Bakkers J. MicroRNA-23 restricts cardiac valve formation by inhibiting Has2 and extracellular hyaluronic acid production. Circulation Research 2011, 109(6):649-657.
31. Liebner S., Cattelino A., Gallini R., Rudini N., Iurlaro M., Piccolo S., et al. Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. Journal of Cell Biology 2004, 166(3):359-367.
32. Lin F., Butcher E. T cell chemotaxis in a simple microfluidic device. Lab on a Chip 2006, 6(11):1462-1469.
33. Little C.D., Piquet D.M., Davis L.A., Walters L., Drake C.J. Distribution of laminin, collagen type IV, collagen type I, and fibronectin in chicken cardiac jelly/basement membrane. Anatomical Record 1989, 224(3):417-425.
34. Ma L., Lu M.F., Schwartz R.J., Martin J.F. Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 2005, 132(24):5601-5611.
35. Maroski J., Vorderwulbecke B.J., Fiedorowicz K., Da Silva-Azevedo L., Siegel G., Marki A., et al. Shear stress increases endothelial hyaluronan synthase 2 and hyaluronan synthesis especially in regard to an atheroprotective flow profile. Experimental Physiology 2011, 96(9):977-986.
36. Martinez N.J., Ow M.C., Barrasa M.I., Hammell M., Sequerra R., Doucette-Stamm L., et al. A C. elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity. Genes & Development 2008, 22(18):2535-2549.
37. Michael D.R., Phillips A.O., Krupa A., Martin J., Redman J.E., Altaher A., et al. The human hyaluronan synthase 2 (HAS2) gene and its natural antisense RNA exhibit coordinated expression in the renal proximal tubular epithelial cell. Journal of Biological Chemistry 2011, 286(22):19523-19532.
38. Morelli L.G., Urju K., Ares S., Oates A.C. Computational approaches to developmental patterning. Science 2012, 336(6078):187-191.
39. Ori M., Nardini M., Casini P., Perris R., Nardi I. XHas2 activity is required during somitogenesis and precursor cell migration in Xenopus development. Development 2006, 133(4):631-640.
40. Rodgers L.S., Lalani S., Hardy K.M., Xiang X., Broka D., Antin P.B., et al. Depolymerized hyaluronan induces vascular endothelial growth factor, a negative regulator of developmental epithelial-to-mesenchymal transformation. Circulation Research 2006, 99(6):583-589.
41. Rodriguez K.J., Piechura L.M., Masters K.S. Regulation of valvular interstitial cell phenotype and function by hyaluronic acid in 2-D and 3-D culture environments. Matrix Biology 2011, 30(1):70-82.
42. Schroeder J.A., Jackson L.F., Lee D.C., Camenisch T.D. Form and function of developing heart valves: coordination by extracellular matrix and growth factor signaling. Journal of Molecular Medicine (Berlin) 2003, 81(7):392-403.
43. Sugi Y., Yamamura H., Okagawa H., Markwald R.R. Bone morphogenetic protein-2 can mediate myocardial regulation of atrioventricular cushion mesenchymal cell formation in mice. Developmental Biology 2004, 269(2):505-518.
44. Swat M.H., Thomas G.L., Belmonte J.M., Shirinifard A., Hmeljak D., Glazier J.A. Multiscale modeling of tissues using CompuCell3D. Methods in Cell Biology 2012, 325-366.
45. Toole B.P. Hyaluronan and its binding proteins, the hyaladherins. Current Opinion in Cell Biology 1990, 2(5):839-844.
46. Toole B.P. Hyaluronan: from extracellular glue to pericellular cue. Nature Reviews Cancer 2004, 4(7):528-539.
47. Turing A.M. The chemical basis of morphogenesis. Philosophical Transactions of the Royal Society B: Biological Sciences 1952, 237(641):37-72.
48. Valadi H., Ekström K., Bossios A., Sjöstrand M., Lee J.J., Lötvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology 2007, 9(6):654-659.
49. Vermot J., Forouhar A.S., Liebling M., Wu D., Plummer D., Gharib M., et al. Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biology 2009, 7(11):e1000246.
50. Walsh E.C., Stainier D.Y. UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish. Science 2001, 293(5535):1670-1673.
51. Weigel P.H., DeAngelis P.L. Hyaluronan synthases: a decade-plus of novel glycosyltransferases. Journal of Biological Chemistry 2007, 282(51):36777-36781.
52. Wienholds E., Kloosterman W.P., Miska E., Alvarez-Saavedra E., Berezikov E., de Bruijn E., et al. MicroRNA expression in zebrafish embryonic development. Science 2005, 309(5732):310-311.