BMP-2 Induces Versican and Hyaluronan That Contribute to Post-EMT AV Cushion Cell Migration

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Inai, Kei ^a,b   Burnside, Jessica L ^a   Hoffman, Stanley ^a   Toole, Bryan P ^a   Sugi, Yukiko ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; COLLAGEN GEL; HYALURONIC ACID; MESSENGER RNA; NOGGIN; VERSICAN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL MIGRATION; CHICK; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; ENDOCARDIAL CUSHION; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; HAS2 GENE; MESENCHYME; MESENCHYME CELL; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; VERSICAN GENE;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CELL MOVEMENT; CHICK EMBRYO; ENDOCARDIAL CUSHIONS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION; GLUCURONOSYLTRANSFERASE; HYALURONIC ACID; MESENCHYMAL STROMAL CELLS; MESODERM; RNA INTERFERENCE; RNA, MESSENGER; VERSICANS;

EID: 84885398149     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077593     Document Type: Article

References (57)

1. Eisenberg LM, Markwald RR, (1995) Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ Res 77: 1-6. doi:10.1161/01.RES.77.1.1. PubMed: 7788867.
2. Armstrong EJ, Bischoff J, (2004) Heart valve development: endothelial cell signaling and differentiation. Circ Res 95: 459-470. doi:10.1161/01.RES.0000141146.95728.da. PubMed: 15345668.
3. Person AD, Klewer SE, Runyan RB, (2005) Cell biology of cardiac cushion development. Int Rev Cytol 243: 287-335. doi:10.1016/S0074-7696(05)43005-3. PubMed: 15797462.
4. Combs MD, Yutzey KE, (2009) Heart valve development: Regulatory networks in development and disease. Circ Res 105: 408-421. doi:10.1161/CIRCRESAHA.109.201566. PubMed: 19713546.
5. Sugi Y, Yamamura H, Okagawa H, Markwald RR, (2004) Bone morphogenetic protein-2 can mediate myocardial regulation of atrioventricular cushion mesenchymal cell formation in mice. Dev Biol 269: 505-518. doi:10.1016/j.ydbio.2004.01.045. PubMed: 15110716.
6. Okagawa H, Markwald RR, Sugi Y, (2007) Functional BMP receptor in endocardial cells is required in atrioventricular cushion mesenchymal cell formation in chick. Dev Biol 306: 179-192. doi:10.1016/j.ydbio.2007.03.015. PubMed: 17449024.
7. Ma L, Lu MF, Schwartz RJ, Martin JF, (2005) Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 132: 5601-5611. doi:10.1242/dev.02156. PubMed: 16314491.
8. Rivera-Feliciano J, Tabin CJ, (2006) Bmp2 instructs cardiac progenitors to form the heart-valve-inducing field. Dev Biol 295: 580-588. doi:10.1016/j.ydbio.2006.03.043. PubMed: 16730346.
9. Park C, Lavine K, Mishina Y, Deng CX, Ornitz DM, et al. (2006) Bone morphogenetic protein receptor 1A signaling is dispensable for hematopoietic development but essential for vessel and atrioventricular endocardial cushion formation. Development 133: 3473-3484. doi:10.1242/dev.02499. PubMed: 16887829.
10. Song L, Faessler R, Mishina Y, Jiao K, Baldwin HS, (2007) Essential function of Alk3 during AV cushion morphogenesis in mouse embryonic hearts. Dev Biol 301: 271-286.
11. Wang J, Greene SB, Martin JF, (2011) BMP signaling in congenital heart disease: new developments and future directions. Birth Defects Res A Clin Mol Teratol 91: 441-448. doi:10.1002/bdra.20785. PubMed: 21384533.
12. Lincoln J, Alfieri CM, Yutzey KE, (2004) Development of heart valve leaflets and supporting apparatus in chicken and mouse embryos. Dev Dyn 230: 239-250. doi:10.1002/dvdy.20051. PubMed: 15162503.
13. Wang J, Sridurongrit S, Dudas M, Thomas P, Nagy A, et al. (2005) Atrioventricular cushion transformation is mediated by ALK2 in the developing mouse heart. Dev Biol 286: 299-310. doi:10.1016/j.ydbio.2005.07.035. PubMed: 16140292.
14. Inai K, Norris RA, Hoffman S, Markwald RR, Sugi Y, (2008) BMP-2 induces cell migration and periostin expression during atrioventricular valvulogenesis. Dev Biol 315: 383-396. doi:10.1016/j.ydbio.2007.12.028. PubMed: 18261719.
15. de la Cruz MV, Markwald RR, (1998) Living morphogenesis of the heart. New York: Birkhauser/springer-Verlag.
16. Oosthoek PW, Wenink AC, Vrolijk BC, Wisse LJ, DeRuiter MC, et al. (1998) Development of the atrioventricular valve tension apparatus in the human heart. Anat Embryol (Berl) 198: 317-329. doi:10.1007/s004290050187. PubMed: 9764545.
17. Lincoln J, Alfieri CM, Yutzey KE, (2006) BMP and FGF regulatory pathways control cell lineage diversification of heart valve precursor cells. Dev Biol 292: 290-302. doi:10.1016/j.ydbio.2005.12.042. PubMed: 16680829.
18. Shi S, Grothe S, Zhang Y, O'Connor-McCourt MD, Poole AR, et al. (2004) Link protein has greater affinity for versican than aggrecan. J Biol Chem 279: 12060-12066. PubMed: 14724283.
19. Matsumoto K, Kamiya N, Suwan K, Atsumi F, Shimizu K, et al. (2006) Identification and characterization of versican/PG-M aggregates in cartilage. J Biol Chem 281: 18257-18263. doi:10.1074/jbc.M510330200. PubMed: 16648631.
20. Yamamura H, Zhang M, Markwald RR, Mjaatvedt CH, (1997) A heart segmental defect in the anterior-posterior axis of a transgenic mutant mouse. Dev Biol 186: 58-72. doi:10.1006/dbio.1997.8559. PubMed: 9188753.
21. Mjaatvedt CH, Yamamura H, Capehart AA, Turner D, Markwald RR, (1998) The cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation. Dev Biol 202: 56-66. doi:10.1006/dbio.1998.9001. PubMed: 9758703.
22. Camenisch TD, Spicer AP, Brehm-Gibson T, Biesterfeldt J, Augustine ML, et al. (2000) Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J Clin Invest 106: 349-360. doi:10.1172/JCI10272. PubMed: 10930438.
23. Camenisch TD, Schroeder JA, Bradley J, Klewer SE, McDonald JA, (2002) Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors. Nat Med, 8: 850-855. PubMed: 12134143.
24. Schroeder JA, Jackson LF, Lee DC, Camenisch TD, (2003) Form and function of developing heart valves: coordination by extracellular matrix and growth factor signaling. J Mol Med 81: 392-403. doi:10.1007/s00109-003-0456-5. PubMed: 12827270.
25. Toole BP, Yu Q, Underhill CB, (2001) Hyaluronan and hyaluronan-binding proteins. Probes for specific detection. Methods Mol Biol 171: 479-485. PubMed: 11450261.
26. Zanin MK, Bundy J, Ernst H, Wessels A, Conway SJ, et al. (1999) Distinct spatial and temporal distributions of aggrecan and versican in the embryonic chick heart. Anat Rec 256: 366-380. doi:10.1002/(SICI)1097-0185(19991201)256:4. PubMed: 10589023.
27. Ghatak S, Misra S, Toole BP, (2002) Hyaluronan oligosaccharides inhibit anchorage-independent growth of tumor cells by suppressing the phosphoinositide 3-kinase/Akt cell survival pathway. J Biol Chem 277: 38013-38020. doi:10.1074/jbc.M202404200. PubMed: 12145277.
28. Ward JA, Huang L, Guo H, Ghatak S, Toole BP, (2003) Perturbation of hyaluronan interactions inhibits malignant properties of glioma cells. Am J Pathol 162: 1403-1409. doi:10.1016/S0002-9440(10)64273-3. PubMed: 12707023.
29. Zoltan-Jones A, Huang L, Ghatak S, Toole BP, (2003) Elevated hyaluronan production induces mesenchymal and transformed properties in epithelial cells. J Biol Chem 278: 45801-45810. doi:10.1074/jbc.M308168200. PubMed: 12954618.
30. LeBaron RG, (1996) Versican. Perspect Dev Neurobiol 3: 216-271.
31. Baldwin HS, Lloyd TR, Solursh M, (1994) Hyaluronate degradation affects ventricular function of the early postlooped embryonic rat heart in situ. Circ Res 74: 244-252. doi:10.1161/01.RES.74.2.244. PubMed: 8293563.
32. Kern CB, Twal WO, Mjaatvedt CH, Fairey SE, Toole BP, Iruela-Arispe ML, Argraves WS, (2006) Proteolytic cleavage of versican during cardiac cushion morphogenesis. Dev Dyn 235: 2238-2247. doi:10.1002/dvdy.20838. PubMed: 16691565.
33. Kern CB, Norris RA, Thompson RP, Argraves WS, Fairey SE, et al. (2007) Versican proteolysis mediates myocardial regression during outflow tract development. Dev Dyn 236: 671-683. doi:10.1002/dvdy.21059. PubMed: 17226818.
34. Craig EA, Parker P, Camenisch TD, (2009) Size-dependent regulation of Snail2 by hyaluronan: Its role in cellular invasion. Glycobiology 19: 890-898. doi:10.1093/glycob/cwp064. PubMed: 19451547.
35. Dupuis LE, McCulloch DR, McGarity JD, Bahan A, Wessels A, et al. (2011) Altered versican cleavage in ADAMTS5 deficient mice; a novel etiology of myxomatous valve disease. Dev Biol 357: 152-154. doi:10.1016/j.ydbio.2011.06.041. PubMed: 21749862.
36. Shirai M, Imanaka-Yoshida K, Schneider MD, Schwartz RJ, Morisaki T, (2009) T-box 2, a mediator of BMP-Smad signaling, induced hyaluronan synthase 2 and TGFbeta2 expression and endocardial cushion formation. Proc Natl Acad Sci USA 106: 18604-18609. doi:10.1073/pnas.0900635106. PubMed: 19846762.
37. Yamada M, Revelli J-P, Eichele G, Barron M, Schwartz RJ, (2000) Expression of chick Tbx-2 Tbx3, and Tbx-5 genes during early heart development: evidence for BMP2 induction of Tbx2. Dev Biol 228: 95-105.
38. Singh R, Hoogaars WM, Barnett P, Grieskamp T, Rana MS, et al. (2012) Tbx2 and Tbx3 induce atrioventricular myocardial development and endocardial cushion formation. Cell Mol Life Sci 69: 1377-1389. doi:10.1007/s00018-011-0884-2. PubMed: 22130515.
39. Klewer SE, Yatskievych T, Pogreba K, Stevens MV, Antin PB, et al. (2006) Has2 expression in heart forming regions is independent of BMP signaling. Gene Expr Patterns 6: 462-470. doi:10.1016/j.modgep.2005.11.005. PubMed: 16458617.
40. Sugi Y, Kern MJ, Markwald RR, Burnside JL, (2012) Periostin expression is altered in aortic valves in Smad6 mutant mice. J Neonatal Biol 1: 101.
41. Ricciardelli C, Russell DL, Ween MP, Mayne K, Suwiwat S, et al. (2007) Formation of hyaluronan- and versican-rich pericellular matrix by prostate cancer cells promotes cell motility. J Biol Chem 282: 10814-10825. doi:10.1074/jbc.M606991200. PubMed: 17293599.
42. Du WW, Yang BB, Shatseva TA, Yang BL, Deng Z, et al. (2010) Versican G3 promotes mouse mammary tumor cell growth, migration, and metastasis by influencing EGF receptor signaling. PLOS ONE 5: 1-14.
43. Ori M, Nardini M, Casini P, Perris R, Nardi I, (2005) XHas activity is required during somitogenesis and precursor cell migration in Xenopus development. Development 133: 631-640.
44. Dutt S, Kléber M, Matasci M, Sommer L, Zimmermann DR, (2006) Versican V0 and V1 guide migratory neural crest cells. J Biol Chem 281: 12123-12131. doi:10.1074/jbc.M510834200. PubMed: 16510447.
45. Casini P, Nardi I, Ori M, (2012) Hyaluronan is required for cranial neural crest cells migration and craniofacial development. Dev Dyn 241: 294-302. doi:10.1002/dvdy.23715. PubMed: 22184056.
46. Bourguignon LY, Wong G, Earle C, Krueger K, Spevak CC, (2010) Hyaluronan-CD44 interaction promotes c-Src-mediated twist signaling, microRNA-10b expression, and RhoA/RhoC up-regulation, leading to Rho-kinase-associated cytoskeleton activation and breast tumor cell invasion. J Biol Chem 285: 36721-36735. doi:10.1074/jbc.M110.162305. PubMed: 20843787.
47. Kim Y, Lee YS, Choe J, Lee H, Kim YM, (2008) CD44-epidermal growth factor receptor interaction mediates hyaluronic acid-promoted cell motility by activating protein kinase C signaling involving Akt, Rac1, Phox, reactive oxygen species, focal adhesion kinase, and MMP-2. J Biol Chem 283: 22513-22528. doi:10.1074/jbc.M708319200. PubMed: 18577517.
48. Park YS, Huh JW, Lee JH, Kim HR, (2012) shRNA against CD44 inhibits cell proliferation, invasion and migration, and promotes apoptosis of colon carcinoma cells. Oncol Rep 27: 339-346. PubMed: 22076607.
49. Shimabukuro Y, Terashima H, Takedachi M, Maeda K, Nakamura T, et al. (2011) Fibroblast growth factor-2 stimulates directed migration of periodontal ligament cells via PI3K/AKT signaling and CD44/hyaluronan interaction. J Cell Physiol 226: 809-821. doi:10.1002/jcp.22406. PubMed: 20857427.
50. Hatano S, Kimata K, Hiraiwa N, Kusakabe M, Isogai Z, et al. (2012) Versican/PG-M is essential for ventricular septal formation subsequent to cardiac atrioventricular cushion development. Glycobiology 22: 1268-1277. doi:10.1093/glycob/cws095. PubMed: 22692047.
51. Bourguignon LY, Gilad E, Peyrollier K, Brightman A, Swanson RA, (2007) Hyaluronan-CD44 interaction stimulates Rac1 signaling and PKN gamma kinase activation leading to cytoskeleton function and cell migration in astrocytes. J Neurochem 101: 1002-1017. doi:10.1111/j.1471-4159.2007.04485.x. PubMed: 17403031.
52. Pi X, Ren R, Kelley R, Zhang C, Moser M, et al. (2007) Sequential roles for myosin-X in BMP6-dependent filopodial extension, migration, and activation of BMP receptors. J Cell Biol 179: 1569-1582. doi:10.1083/jcb.200704010. PubMed: 18158328.
53. Gamell C, Susperregui AG, Bernard O, Rosa JL, Ventura F, (2011) The p38/MK2/Hsp25 pathway is required for BMP-2-induced cell migration. PLOS ONE 6: 1-11. PubMed: 21297993.
54. Butcher JT, Norris RA, Hoffman S, Mjaatvedt CH, Markwald RR, (2007) Periostin promotes atrioventricular mesenchyme matrix invasion and remodeling mediated by integrin signaling through Rho/PI 3-kinase. Dev Biol 302: 256-266. doi:10.1016/j.ydbio.2006.09.048. PubMed: 17070513.
55. Hamburger V, Hamilton HE, (1951) A series of normal stages in the development of the chick embryo. J Morphol 88: 49-92. doi:10.1002/jmor.1050880104.
56. Sugi Y, Ito N, Szebenyi G, Myers K, Fallon JF, et al. (2003) Fibroblast growth factor (FGF)-4 can induce proliferation of cardiac cushion mesenchymal cells during early valve leaflet formation. Dev Biol 258: 252-263. doi:10.1016/S0012-1606(03)00099-X. PubMed: 12798286.
57. Slomiany MG, Grass GD, Robertson AD, Yang XY, Maria BL, et al. (2009) Hyaluronan, CD44, and emmprin regulate lactate efflux and membrane localization of monocarboxylate transporters in human breast carcinoma cells. Cancer Res 69: 1293-1301. doi:10.1158/0008-5472.CAN-08-2491. PubMed: 19176383.