Follistatin antagonizes transforming growth factor-β3-induced epithelial-mesenchymal transition in vitro: Implications for murine palatal development supported by microarray analysis

Differentiation

Volumn 76, Issue 4, 2008, Pages 404-416

  Nogai, Hendrik ^a   Rosowski, Mark ^b   Grün, Joachim ^a   Rietz, Anika ^a   Debus, Nils ^c   Schmidt, Gül ^d   Lauster, Carola ^d   Janitz, Michal ^e   Vortkamp, Andrea ^e   Lauster, Roland ^b  

^a German Arthritis Research Center   (Germany)

^b TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^c BAYER PHARMA AG   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

Cleft palate; EMT; Follistatin; Palatal fusion; TGF

Indexed keywords

FOLLISTATIN; TRANSFORMING GROWTH FACTOR BETA3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL DIFFERENTIATION; CELL TRANSFORMATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; IN SITU HYBRIDIZATION; IN VITRO STUDY; MAMMARY GLAND; MESENCHYME CELL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PALATE; PRIORITY JOURNAL;

MURINAE;

EID: 42049113862     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1111/j.1432-0436.2007.00223.x     Document Type: Article

References (63)

1. Anderson, L. Seilhamer, J. (1997) A comparison of selected mRNA and protein abundances in human liver. Electrophoresis 18 : 533 537.
2. Bartholin, L., Maguer-Satta, V., Hayette, S., Martel, S., Gadoux, M., Corbo, L., Magaud, J.P. Rimokh, R. (2002) Transcription activation of FLRG and follistatin by activin A, through Smad proteins, participates in a negative feedback loop to modulate activin A function. Oncogene 21 : 2227 2235.
3. Botchkarev, V.A., Botchkareva, N.V., Nakamura, M., Huber, O., Funa, K., Lauster, R. Paus, R. (2001) Gilchrest BA. Noggin is required for induction of the hair follicle growth phase in postnatal skin. FASEB J 15 : 2205 2214.
4. Brunet, C.L., Sharpe, P.M. Ferguson, M.W. (1995) Inhibition of TGF-beta 3 (but not TGF-beta 1 or TGF-beta 2) activity prevents normal mouse embryonic palate fusion. Int J Dev Biol 39 : 345 355.
5. Caccamo, A.E., Scaltriti, M., Caporali, A., Dárca, D., Scorcioni, F., Astancolle, S., Mangiola, M. Bettuzzi, S. (2004) Cell detachment and apoptosis induction of immortalized human prostate epithelial cells are associated with early accumulation of a 45 kDa nuclear isoform of clusterin. Biochem J 382 : 157 168.
6. Carver, E.A., Jiang, R., Lan, Y., Oram, K.F. Gridley, T. (2001) The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol Cell Biol 21 : 8184 8188.
7. Chen, G., Gharib, T.G., Huang, C.C., Taylor, J.M., Misek, D.E., Kardia, S.L., Giordano, T.J., Iannettoni, M.D., Orringer, M.B., Hanash, S.M. Beer, D.G. (2002) Discordant protein and mRNA expression in lung adenocarcinomas. Mol. Cell Proteomics. 1 : 304 313.
8. Cuervo, R. Covarrubias, L. (2004) Death is the major fate of medial edge epithelial cells and the cause of basal lamina degradation during palatogenesis. Development 131 : 15 24.
9. Cui, X.M., Shiomi, N., Chen, J., Saiti, T., Yamamoto, T., Ito, Y., Bringas, P., Chai, Y. Shuler, C.F. (2005) Overexpression of Smad2 in Tgf-beta3-null mutant mice rescues cleft palate. Dev Biol 278 : 193 202.
10. De Crescenzo, G., Pham, P.L., Durocher, Y. O'Connor-McCourt, M.D. (2003) Transforming growth factor-beta (TGF-beta) binding to the extracellular domain of the type II TGF-beta receptor: receptor capture on a biosensor surface using a new coiled-coil capture system demonstrates that avidity contributes significantly to high affinity binding. J Mol Biol 328 : 1173 1183.
11. Ferguson, M.W. (1988) Palate development. Development 103 : 41 60.
12. Ferguson, M.W. (1987) Palate development: mechanisms and malformations. Ir J Med Sci 156 : 309 315.
13. Gleave, M. Jansen, B. (2005) Knock-down of the cytoprotective gene, clusterin, to enhance hormone and chemosensitivity in prostate and other cancers. Ann NY Acad Sci 1058 : 1 15.
14. Greene, R.M. Pratt, R.M. (1976) Developmental aspects of secondary palate formation. J Embryol Exp Morphol 36 : 225 245.
15. Gupta, M., Gupta, S.K., Hoffman, B. Liebermann, D.A. (2006) Gadd45a and Gadd45b protect hematopoietic cells from UV-induced apoptosis via distinct signaling pathways, including p38 activation and JNK inhibition. J Biol Chem 281 : 17552 17558.
16. Hayashi, K., Carpenter, K.D., Gray, C.A. Spencer, T.E. (2003) The activin-follistatin system in the neonatal ovine uterus. Biol Reprod 69 : 843 850.
17. Hoeller, C., Pratscher, B., Thallinger, C., Winter, D., Fink, D., Kovacic, B., Sexl, V., Wacheck, V., Gleave, M.E., Pehamberger, H. Jansen, B. (2005) Clusterin regulates drug-resistance in melanoma cells. J Invest Dermatol 124 : 1300 1307.
18. Iwano, M., Plieth, D., Danoff, T.M., Xue, C., Okada, H. Neilson, E.G. (2002) Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110 : 341 350.
19. Janitz, M., Heiser, V., Bottcher, U., Landt, O. Lauster, R. (1998) Three alternatively spliced variants of the gene coding for the human bone morphogenetic protein-1. J Mol Med 76 : 141 146.
20. Kaartinen, V., Voncken, J.W., Shuler, C., Warburton, D., Bu, D., Heisterkamp, N. Groffen, J. (1995) Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelial-mesenchymal interaction. Nat Genet 11 : 415 421.
21. Kang, P. Svoboda, K.K. (2005) Epithelial-mesenchymal transformation during craniofacial development. J Dent Res 84 : 678 690.
22. Katoh, M. (2005) Epithelial-mesenchymal transition in gastric cancer. Int J Oncol 27 : 1677 1683.
23. Kern, W., Kohlmann, A., Wuchter, C., Schnittger, S., Schoch, C., Mergenthaler, S., Ratei, R., Ludwig, W.D., Hiddemann, W. Haferlach, T. (2003) Correlation of protein expression and gene expression in acute leukemia. Cytometry B Clin Cytom 55 : 29 36.
24. LaGamba, D., Nawshad, A. Hay, E.D. (2005) Microarray analysis of gene expression during epithelial-mesenchymal transformation. Dev Dyn 234 : 132 142.
25. Levi, G., Mantero, S., Barbieri, O., Cantore, D., Paleari, L., Beverdam, A., Genova, F., Robert, B. Merlo, G.R. (2006) Msx1 and Dlx5 act independently in development of craniofacial skeleton, but converge on the regulation of Bmp signaling in palate formation. Mech Dev 123 : 3 16.
26. Maeshima, A., Nojima, Y. Kojima, I. (2001) The role of the activin-follistatin system in the developmental and regeneration processes of the kidney. Cytokine Growth Factor Rev 12 : 289 298.
27. Martinez-Alvarez, C., Blanco, M., Perez, R., Rabadan, M.A., Aparicio, M., Resel, E., Martinez, T. Nieto, A. (2004) Snail familiy members and cell survival in physiological and pathological cleft palates. Dev Biol 265 : 207 218.
28. Martinez-Alvarez, C., Tudela, C., Perez-Miguelsanz, J., O'Kane, S., Puerta, J. Ferguson, M.W. (2000) Medial edge epithelial cell fate during palatal fusion. Dev Biol 220 : 343 357.
29. Matzuk, M.M., Kumar, T.R., Vassalli, A., Bickenbach, J.R., Roop, D.R., Jaenisch, R. Bradley, A. (1995a) Functional analysis of activins during mammalian development. Nature 374 : 354 356.
30. Matzuk, M.M., Lu, N., Vogel, H., Sellheyer, K., Roop, D.R. Bradley, A. (1995b) Multiple defects and perinatal death in mice deficient in follistatin. Nature 374 : 360 363.
31. Miettinen, P.J., Ebner, R., Lopez, A.R. Derynck, R. (1994) TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 127 : 2021 2036.
32. Minina, E., Schneider, S., Rosowski, M., Lauster, R. Vortkamp, A. (2005) Expression of FGF and TGFbeta signaling related genes during embryonic endochondral ossification. Gene Expr Patterns 6 : 102 109.
33. Murray, J.C. Schutte, B.C. (2004) Cleft palate: players, pathways, and pursuits. J Clin Invest 113 : 1676 1678.
34. Nakamura, M., Matzuk, M.M., Gerstmayer, B., Bosio, A., Lauster, R., Miyachi, Y., Werner, S. Paus, R. (2003) Control of pelage hair follicle development and cycling by complex interactions between follistatin and activin. FASEB J 17 : 497 499.
35. Nawshad, A., LaGamba, D. Hay, E.D. (2004) Transforming growth factor beta (TGFbeta) signalling in palatal growth, apoptosis and epithelial mesenchymal transformation (EMT). Arch Oral Biol 49 : 675 689.
36. O'Connor-McCourt, M.D., Segarubu, O., Grothe, S., Tsang, M. Weatherbee, JA. (1995) Analysis of the interaction between two TGF-beta-binding proteins and three TGF-beta isoforms using surface plasmon resonance. Ann NY Acad Sci 766 : 300 302.
37. Otsuka, F., Moore, R.K., Iemura, S., Ueno, N. Shimasaki, S. (2001) Follistatin inhibits the function of the oocyte-derived factor BMP-15. Biochem Biophys Res Commun 289 : 961 966.
38. Parrinello, S., Lin, C.Q., Murata, K., Itahana, Y., Singh, J., Krtolica, A., Campisi, J. Desprez, P.Y. (2001) Id-1, ITF-2, and Id-2 comprise a network of helix-loop-helix proteins that regulate mammary epithelial cell proliferation, differentiation, and apoptosis. J Biol Chem 276 : 39213 39219.
39. Pelton, R.W., Hogan, B.L., Miller, D.A. Moses, H.L. (1990) Differential expression of genes encoding TGFs beta 1, beta 2, and beta 3 during murine palate formation. Dev Biol 141 : 456 460.
40. Peng, Y., Kang, Q., Luo, Q., Jiang, W., Si, W., Liu, B.A., Luu, H.H., Park, J.K., Li, X., Luo, J., Montag, A.G., Haydon, R.C. He, T.C. (2004) Inhibitor of DNA binding/ differentiation helix-loop-helix proteins mediate bone morphogenetic protein-induced osteoblast differentiation of mesenchymal stem cells. J Biol Chem 279 : 32941 32941.
41. Piccolo, S., Agius, E., Lu, B., Goodman, S., Dale, L. De Robertis, E.M. (1997) Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity. Cell 91 : 407 416.
42. Piek, E., Moustakas, A., Kurisaki, A., Heldin, C.H. ten Dijke, P. (1999) TGF-(beta) type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. J Cell Sci 112 : 4557 4568.
43. Proetzel, G., Pawlowski, S.A., Wiles, M.V., Yin, M., Boivin, G.P., Howles, P.N., Ding, J., Ferguson, M.W. Doetschman, T. (1995) Transforming growth factor-beta 3 is required for secondary palate fusion. Nat Genet 11 : 409 414.
44. Rosivatz, E., Becker, I., Specht, K., Fricke, E., Luber, B., Busch, R., Hofler, H. Becker, K.F. (2002) Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, and twist in gastric cancer. Am J Pathol 161 : 1881 1891.
45. Satokata, I. Maas, R. (1994) Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat Genet 6 : 348 356.
46. Scaltriti, M., Bettuzzi, S., Sharrard, R.M., Caporali, A., Caccamo, A.E. Maitland, N.J. (2004) Clusterin overexpression in both malignant and nonmalignant prostate epithelial cells induces cell cycle arrest and apoptosis. Br J Cancer 91 : 1842 1850.
47. Sun, D., Vanderburg, C.R., Odierna, G.S. Hay, E.D. (1998) TGFbeta3 promotes transformation of chicken palate medial edge epithelium to mesenchyme in vitro. Development 125 : 95 105.
48. Suzuki, N., Labosky, P.A., Furuta, Y., Hargett, L., Dunn, R., Fogo, A.B., Takahara, K., Peters, D.M., Greenspan, D.S. Hogan, B.L. (1996) Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid. Development 122 : 3587 3595.
49. Takahara, S., Takigawa, T. Shiota, K. (2004) Programmed cell death is not a necessary prerequisite for fusion of the fetal mouse palate. Int J Dev Biol 2004 48 : 39 46.
50. Tam, P.P. Behringer, R.R. (1997) Mouse gastrulation: the formation of a mammalian body plan. Mech Dev 68 : 3 25.
51. Tano, M., Minegishi, T., Nakamura, K., Nakamura, M., Karino, S., Miyamoto, K. Ibuki, Y. (1995) Regulation of follistatin messenger ribonucleic acid in cultured rat granulosa cells. Mol Cell Endocrinol 109 : 167 174.
52. Taya, Y., O'Kane, S. Ferguson, M.W. (1999) Pathogenesis of cleft palate in TGF-beta3 knockout mice. Development 126 : 3869 3879.
53. Thesleff, I. Aberg, T. (1999) Molecular regulation of tooth development. Bone 25 : 123 125.
54. Thiery, J.P. (2003) Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol 15 : 740 746.
55. Thomsen, G.H. (1997) Antagonism within and around the organizer: BMP inhibitors in vertebrate body patterning. Trends Genet 13 : 209 211.
56. Valcourt, U., Kowanetz, M., Niimi, H., Heldin, C.-H. Moustakas, A. (2005) TGF-β and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol Biol Cell 16 : 1987 2002.
57. Vaziri Sani, F., Hallberg, K., Harfe, B.D., McMahon, A.P., Linde, A. Gritli-Linde, A. (2005) Fate-mapping of the epithelial seam during palatal fusion rules out epithelial-mesenchymal transformation. Dev Biol 285 : 490 495.
58. Wilkie, A.O. Morris-Kay, G.M. (2001) Genetics of craniofacial development and malformation. Nat Rev Genet 2 : 458 468.
59. Zavadil, J. Bottinger, E.P. (2005) TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24 : 764 774.
60. Zeisberg, M. Kalluri, R. (2004) The role of epithelial-to-mesenchymal transition in renal fibrosis. J Mol Med 82 : 175 181.
61. Zeisberg, M., Sha, A.A. Kalluri, R. (2005) Bone morphogenic protein-7 induces mesenchymal to epithelial transition in adult renal fibroblasts and facilitates regeneration of injured kidney. J Biol Chem 280 : 8094 8100.
62. Zhang, H., Kim, J.K., Edwards, C.A., Xu, Z., Taichman, R. Wang, C.Y. (2005) Clusterin inhibits apoptosis by interacting with activated Bax. Nat Cell Biol 7 : 909 915.
63. Zhang, H., Ozaki, I., Mizuta, T., Hamajima, H., Yasutake, T., Eguchi, Y., Ideguchi, H., Yamamoto, K. Matsuhashi, S. (2006) Involvement of programmed cell death 4 in transforming growth factor-beta1-induced apoptosis in human hepatocellular carcinoma. Oncogene 25 : 6101 6112.