Implications of TGFβ on transcriptome and cellular biofunctions of palatal mesenchyme

Frontiers in Physiology

Volumn 3 APR, Issue , 2012, Pages

  Zhu, Xiujuan ^a   Ozturk, Ferhat ^a   Pandey, Sanjit ^b   Guda, Chitti Babu ^b   Nawshad, Ali ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Craniofacial; HEPM; Mesenchyme; Microarray; Palate; Palatogenesis; TGF ; Transcriptome

Indexed keywords

EID: 84866405247     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00085     Document Type: Article

References (91)

1. Abad, M. A., Enguita, M., Degregorio-Rocasolano, N., Ferrer, I., and Trullas, R. (2006). Neuronal pentraxin 1 contributes to the neuronal damage evoked by amyloid-beta and is overexpressed in dystrophic neurites in Alzheimer's brain. J. Neurosci. 26, 12735-12747.
2. Abbott, B. D., and Pratt, R. M. (1988). Influence of retinoids and EGF on growth of embryonic mouse palatal epithelia in culture. In vitro Cell. Dev. Biol. 24, 343-352.
3. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E.,Ringwald,M.,Rubin,G. M.,and Sherlock, G. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29.
4. Babiarz, B. S., Wee, E. L., and Zimmerman, E. F. (1979). Palate morphogenesis. III. Changes in cell shape and orientation during shelf elevation. Teratology 20, 249-278.
5. Boccaccio, C., Ando, M., Tamagnone, L., Bardelli, A., Michieli, P., Battistini, C., and Comoglio, P. M. (1998). Induction of epithelial tubules by growth factor HGF depends on the STAT pathway. Nature 391, 285-288.
6. Bodo, M., Baroni, T., Carinci, F., Becchetti, E., Bellucci, C., Pezzetti, F., Conte, C., Evangelisti, R., and Carinci, P. (1999). TGFbeta isoforms and decorin gene expression are modified in fibroblasts obtained from non-syndromic cleft lip and palate subjects. J. Dent. Res. 78, 1783-1790.
7. Brunet, C. L., Sharpe, P. M., and 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.
8. Brunschwig, E. B., Wilson, K., Mack, D., Dawson, D., Lawrence, E., Willson, J. K., Lu, S., Nosrati, A., Rerko, R. M., Swinler, S., Beard, L., Lutterbaugh, J. D., Willis, J., Platzer, P., and Markowitz, S. (2003). PMEPA1, a transforming growth factor-betainduced marker of terminal colonocyte differentiation whose expression is maintained in primary and metastatic colon cancer. Cancer Res. 63, 1568-1575.
9. Chai, Y., and Maxson, R. E. Jr. (2006). Recent advances in craniofacial morphogenesis. Dev. Dyn. 235, 2353-2375.
10. Cucoranu, I., Clempus, R., Dikalova, A., Phelan, P. J., Ariyan, S., Dikalov, S., and Sorescu, D. (2005). NAD(P)H oxidase 4 mediates transforming growth factor-beta1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ. Res. 97, 900-907.
11. Davies, M., Robinson, M., Smith, E., Huntley, S., Prime, S., and Paterson, I. (2005). Induction of an epithelial to mesenchymal transition in human immortal and malignant keratinocytes by TGF-beta1 involves MAPK, Smad and AP-1 signalling pathways. J. Cell. Biochem. 95, 918-931.
12. Deng, Z. L., Sharff, K. A., Tang, N., Song, W. X., Luo, J., Luo, X., Chen, J., Bennett, E., Reid, R., Manning, D., Xue, A., Montag, A. G., Luu, H. H., Haydon, R. C., and He, T. C. (2008). Regulation of osteogenic differentiation during skeletal development. Front. Biosci. 13, 2001-2021.
13. Dhulipala, V. C., Maddali, K. K., Ray, B. K., Welshons, W. V., and Reddy, C. S. (2011). Role of p21 and cyclin E in normal and secalonic acid D-inhibited proliferation of human embryonic palatal mesenchymal cells. Hum. Exp. Toxicol. 30, 1222-1232.
14. Dhulipala, V. C., Welshons, W. V., and Reddy, C. S. (2004). Inhibition of human embryonic palatal mesenchymal cell cycle by secalonic acid D: a probable mechanism of its cleft palate induction. Orthod. Craniofac. Res. 7, 227-236.
15. Dixon, M. J., Marazita, M. L., Beaty, T. H., and Murray, J. C. (2011). Cleft lip and palate:understanding genetic and environmental influences. Nat. Rev. Genet. 12, 167-178.
16. Eickelberg, O., Centrella, M., Reiss, M., Kashgarian, M., and Wells, R. G. (2002). Betaglycan inhibits TGF-beta signaling by preventing type I-type II receptor complex formation. Glycosaminoglycan modifications alter betaglycan function. J. Biol. Chem. 277, 823-829.
17. Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 95, 14863-14868.
18. Farge, E. (2011). Mechanotransduction in development. Curr. Top. Dev. Biol. 95, 243-265.
19. Ferguson, M. W. (1988). Palate development. Development 103(Suppl.), 41-60.
20. Fitzpatrick, D. R., Denhez, F., Kondaiah, P., and Akhurst, R. J. (1990). Differential expression of TGF beta isoforms in murine palatogenesis. Development 109, 585-595.
21. Gehris, A. L., D'Angelo, M., and Greene, R. M. (1991). Immunodetection of the transforming growth factors beta 1 and beta 2 in the developing murine palate. Int. J. Dev. Biol. 35, 17-24.
22. Gehris, A. L., and Greene, R. M. (1992). Regulation of murine embryonic epithelial cell differentiation by transforming growth factors beta. Differentiation 49, 167-173.
23. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., Hornik, K., Hothorn, T., Huber, W., Iacus, S., Irizarry, R., Leisch, F., Li, C., Maechler, M., Rossini, A. J., Sawitzki, G., Smith, C., Smyth, G., Tierney, L., Yang, J. Y., and Zhang, J. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
24. Gimelli, S., Makrythanasis, P., Stouder, C., Antonarakis, S. E., Bottani, A., and Bena, F. (2011). A de novo 12q13.11 microdeletion in a patient with severe mental retardation, cleft palate, and high myopia. Eur. J. Med. Genet. 54, 94-96.
25. Goudy, S., Law, A., Sanchez, G., Baldwin, H. S., and Brown, C. (2010). Tbx1 is necessary for palatal elongation and elevation. Mech. Dev. 127, 292-300.
26. Greene, R. M., and Pisano, M. M. (2004). Perspectives on growth factors and orofacial development. Curr. Pharm. Des. 10, 2701-2717.
27. Greene, R. M., and Pisano, M. M. (2005). Recent advances in understanding transforming growth factor beta regulation of orofacial development. Hum. Exp. Toxicol. 24, 1-12.
28. Gritli-Linde, A. (2007). Molecular control of secondary palate development. Dev. Biol. 301, 309-326.
29. Guo, Z., Huang, C., Ding, K., Lin, J., and Gong, B. (2010). Transforming growth factor beta-3 and environmental factors and cleft lip with/without cleft palate. DNA Cell Biol. 29, 375-380.
30. Hajjar, K. A., and Nachman, R. L. (1996). The role of lipoprotein(a) in atherogenesis and thrombosis. Annu.Rev.Med.47, 423-442.
31. Hale, B. G., Randall, R. E., Ortin, J., and Jackson, D. (2008). The multifunctional NS1 protein of influenza A viruses. J. Gen. Virol. 89, 2359-2376.
32. Handl, J., Knowles, J., and Kell, D. B. (2005). Computational cluster validation in post-genomic data analysis. Bioinformatics 21, 3201-3212.
33. Innes, P. B. (1978). The ultrastructure of the mesenchymal element of the palatal shelves of the fetal mouse. J. Embryol. Exp. Morphol. 43, 185-194.
34. Iordanskaia, T., and Nawshad, A. (2011). Mechanisms of transforming growth factor beta induced cell cycle arrest in palate development. J. Cell. Physiol. 226, 1415-1424.
35. Ito, Y., Yeo, J. Y., Chytil, A., Han, J., Bringas, P. Jr., Nakajima, A., Shuler, C. F., Moses, H. L., and Chai, Y. (2003). Conditional inactivation of Tgfbr2 in cranial neural crest causes cleft palate and calvaria defects. Development 130, 5269-5280.
36. Iwata, J., Hosokawa, R., Sanchez-Lara, P. A., Urata, M., Slavkin, H., and Chai, Y. (2010). Transforming growth factor-beta regulates basal transcriptional regulatory machinery to control cell proliferation and differentiation in cranial neural crest-derived osteoprogenitor cells. J. Biol. Chem. 285, 4975-4982.
37. Iwata, J., Parada, C., and Chai,Y. (2011). The mechanism of TGF-beta signaling during palate development. Oral. Dis. 17, 733-744.
38. Jin, J. Z., Tan, M., Warner, D. R., Darling, D. S., Higashi, Y., Gridley, T., and Ding, J. (2010). Mesenchymal cell remodeling during mouse secondary palate reorientation. Dev. Dyn. 239, 2110-2117.
39. Kaartinen, V., Voncken, J. W., Shuler, C., Warburton, D., Bu, D., Heisterkamp, N., and 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.
40. Kestler, H. A., Muller, A., Gress, T. M., and Buchholz, M. (2005). Generalized Venn diagrams: a new method of visualizing complex genetic set relations. Bioinformatics 21, 1592-1595.
41. Kim, M. H., Kim, H. J., Choi, J. Y., and Nahm, D. S. (2003). Transforming growth factor-beta3 gene SfaN1 polymorphism in Korean nonsyndromic cleft lip and palate patients. J. Biochem. Mol. Biol. 36, 533-537.
42. Kurihara, Y., Kurihara, H., Suzuki, H., Kodama, T., Maemura, K., Nagai, R., Oda, H., Kuwaki, T., Cao, W. H., Kamada, N., Jishage, K., Ouchi, Y., Azuma, S., Toyoda, Y., Ishikawa, T., Kumada, M., and Yazaki, Y. (1994). Elevated blood pressure and craniofacial abnormalities in mice deficient in endothelin-1. Nature 368, 703-710.
43. Labbe, E., Lock, L., Letamendia, A., Gorska, A. E., Gryfe, R., Gallinger, S., Moses, H. L., and Attisano, L. (2007). Transcriptional cooperation between the transforming growth factor-beta and Wnt pathways in mammary and intestinal tumorigenesis. Cancer Res. 67, 75-84.
44. Lei, S., Dubeykovskiy, A., Chakladar, A., Wojtukiewicz, L., and Wang, T. C. (2004). The murine gastrin promoter is synergistically activated by transforming growth factor-beta/Smad and Wnt signaling pathways. J. Biol. Chem. 279, 42492-42502.
45. Letamendia, A., Labbe, E., and Attisano, L. (2001). Transcriptional regulation by Smads: crosstalk between the TGF-beta and Wnt pathways. J. Bone Joint Surg. Am. 83-A (Suppl. 1), S31-S39.
46. Li, C., and Wong, W. H. (2001). Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl. Acad. Sci. U.S.A. 98, 31-36.
47. Lidral, A. C., and Moreno, L. M. (2005). Progress toward discerning the genetics of cleft lip. Curr. Opin. Pediatr. 17, 731-739.
48. Lidral, A. C., Romitti, P. A., Basart, A. M., Doetschman, T., Leysens, N. J., Daack-Hirsch, S., Semina, E. V., Johnson, L. R., Machida, J., Burds, A., Parnell, T. J., Rubenstein, J. L., and Murray,J. C. (1998). Association of MSX1 and TGFB3 with nonsyndromic clefting in humans. Am. J. Hum. Genet. 63, 557-568.
49. Micalizzi, D. S., Farabaugh, S. M., and Ford, H. L. (2010). Epithelialmesenchymal transition in cancer: parallels between normal development and tumor progression. J. Mammary Gland Biol. Neoplasia 15, 117-134.
50. Mitchell, L. E., Murray, J. C., O'Brien, S., and Christensen, K. (2001). Evaluation of two putative susceptibility loci for oral clefts in the Danish population. Am. J. Epidemiol. 153, 1007-1015.
51. Mori, R., Xiong, S., Wang, Q., Tarabolous, C., Shimada, H., Panteris, E., Danenberg, K. D., Danenberg, P. V., and Pinski, J. K. (2009). Gene profiling and pathway analysis of neuroendocrine transdifferentiated prostate cancer cells. Prostate 69, 12-23.
52. Nakajima, A., Tanaka, E., Ito, Y., Maeno, M., Iwata, K., Shimizu, N., and Shuler, C. F. (2010). The expression of TGF-beta3 for epithelial-mesenchyme transdifferentiated MEE in palatogenesis. J. Mol. Histol. 41, 343-355.
53. Nawshad, A., Lagamba, D., and 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.
54. Omeis, I. A., Hsu, Y. C., and Perin, M. S. (1996). Mouse and human neuronal pentraxin 1 (NPTX1): conservation, genomic structure, and chromosomal localization. Genomics 36, 543-545.
55. Owens, P., Han, G., Li, A. G., and Wang, X. J. (2008). The role of Smads in skin development. J. Invest. Dermatol. 128, 783-790.
56. Pelton, R. W., Hogan, B. L., Miller, D. A., and 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.
57. Pfaffl, M. W., Horgan, G. W., and Dempfle, L. (2002). Relative expression software tool (REST) for groupwise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.
58. Pirooznia, M., Nagarajan, V., and Deng, Y. (2007). GeneVenn-awebapplication for comparing gene lists using Venn diagrams. Bioinformation 1, 420-422.
59. Porter, A. C., and Vaillancourt, R. R. (1998). Tyrosine kinase receptoractivated signal transduction pathways which lead to oncogenesis. Oncogene 17, 1343-1352.
60. Pradervand, S., Paillusson, A., Thomas, J., Weber, J., Wirapati, P., Hagenbuchle, O., and Harshman, K. (2008). Affymetrix whole-transcript human gene 1.0 ST array is highly concordant with standard 3′ expression arrays. BioTechniques 44, 759-762.
61. Proetzel, G., Pawlowski, S. A., Wiles, M. V., Yin, M., Boivin, G. P., Howles, P. N., Ding, J., Ferguson, M. W., and Doetschman, T. (1995). Transforming growth factor-beta 3 is required for secondary palate fusion. Nat. Genet. 11, 409-414.
62. Ramalho-Santos, M., Yoon, S., Matsuzaki, Y., Mulligan, R. C., and Melton, D. A. (2002). "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298, 597-600.
63. Reimers, M.,and Carey,V. J. (2006). Bioconductor: an open source framework for bioinformatics and computational biology. Meth. Enzymol. 411, 119-134.
64. Rhyu, D. Y., Yang, Y., Ha, H., Lee, G. T., Song, J. S., Uh, S. T., and Lee, H. B. (2005). Role of reactive oxygen species in TGF-beta1induced mitogen-activated protein kinase activation and epithelial transition in renal tubular epithelial cells. J. Am. Soc. Nephrol. 16, 667-675.
65. Richman, J. M., and Tickle, C. (1989). Epithelia are interchangeable between facial primordia of chick embryos and morphogenesis is controlled by the mesenchyme. Dev. Biol. 136, 201-210.
66. Rojas, A., Padidam, M., Cress, D., and Grady, W. M. (2009). TGF-beta receptor levels regulate the specificity of signaling pathway activation and biological effects of TGFbeta. Biochim. Biophys. Acta 1793, 1165-1173.
67. Rotzer, D., Roth, M., Lutz, M., Lindemann, D., Sebald, W., and Knaus, P. (2001). Type III TGF-beta receptorindependent signalling of TGFbeta2 via TbetaRII-B, an alternatively spliced TGF-beta type II receptor. EMBO J. 20, 480-490.
68. Rullo, R., Gombos, F., Ferraraccio, F., Farina, A., Morano, D., Festa, V. M., Guida, L., Martinelli, M., Scapoli, L., Pezzetti, F., and Carinci, F. (2006). TGFbeta3 expression in non-syndromic orofacial clefts. Int. J. Pediatr. Otorhinolaryngol. 70, 1759-1764.
69. Salahshourifar, I., Halim, A. S., Wan Sulaiman, W. A., and Zilfalil, B. A. (2011). Contribution of MSX1 variants to the risk of non-syndromic cleft lip and palate in a Malay population. J. Hum. Genet. 16, 755-758.
70. Sanford, L. P., Ormsby, I., Gittenberger De Groot, A. C., Sariola, H., Friedman, R., Boivin, G. P., Cardell, E. L., and Doetschman, T. (1997). TGFbeta2 knockout mice have multiple developmental defects that are nonoverlapping with other TGFbeta knockout phenotypes. Development 124, 2659-2670.
71. Sato, T., Kurihara, Y., Asai, R., Kawamura, Y., Tonami, K., Uchijima, Y., Heude, E., Ekker, M., Levi, G., and Kurihara, H. (2008). An endothelin1 switch specifies maxillomandibular identity. Proc. Natl. Acad. Sci. U.S.A. 105, 18806-18811.
72. Schutte, B. C., and Murray, J. C. (1999). The many faces and factors of orofacial clefts. Hum. Mol. Genet. 8, 1853-1859.
73. Sneath, P. H. A. (1973). Numerical Taxonomy: The Principles and Practice of Numerical Classification. San Francisco: Freeman.
74. Spritz, R. A. (2001). The genetics and epigenetics of orofacial clefts. Curr. Opin. Pediatr. 13, 556-560.
75. Stoll, C., Mengsteab, S., Stoll, D., Riediger, D., Gressner, A. M., and Weiskirchen, R. (2004). Analysis of polymorphic TGFB1 codons 10, 25, and 263 in a German patient group with non-syndromic cleft lip, alveolus, and palate compared with healthy adults. BMC Med. Genet. 5, 15. doi:10.1186/1471-2350-5-15
76. Sturrock, A., Cahill, B., Norman, K., Huecksteadt, T. P., Hill, K., Sanders, K., Karwande, S. V., Stringham, J. C., Bull, D. A., Gleich, M., Kennedy, T. P., and Hoidal, J. R. (2006). Transforming growth factor-beta1 induces Nox4 NAD(P)H oxidase and reactive oxygen species-dependent proliferation in human pulmonary artery smooth muscle cells. Am. J. Physiol. Lung Cell Mol. Physiol. 290, L661-L673.
77. Su, Y., Zhang, L., Gao, X., Meng, F., Wen, J., Zhou, H., Meng, A., and Chen, Y. G. (2007). The evolutionally conserved activity of Dapper2 in antagonizing TGF-beta signaling. FASEB J. 21, 682-690.
78. Subramaniam, N., Leong, G. M., Cock, T. A., Flanagan, J. L., Fong, C., Eisman, J. A., and Kouzmenko, A. P. (2001). Cross-talk between 1,25-dihydroxyvitamin D3 and transforming growth factorbeta signaling requires binding of VDR and Smad3 proteins to their cognate DNA recognition elements. J. Biol. Chem. 276, 15741-15746.
79. Sunil, N., Bennett, J. M., and Haslam, S. Z. (2002). Hepatocyte growth factor is required for progestininduced epithelial cell proliferation and alveolar-like morphogenesis in serum-free culture of normal mammary epithelial cells. Endocrinology 143, 2953-2960.
80. Takahara, M., Harada, M., Guan, D., Otsuji, M., Naruse, T., Takagi, M., and Ogino, T. (2004). Developmental failure of phalanges in the absence of growth/differentiation factor 5. Bone 35, 1069-1076.
81. Takechi, R., Taniguchi, A., Ebara, S., Fukui, T., and Watanabe, T. (2008). Biotin deficiency affects the proliferation of human embryonic palatal mesenchymal cells in culture. J. Nutr. 138, 680-684.
82. Vieira, A. R., Orioli, I. M., Castilla, E. E., Cooper, M. E., Marazita, M. L., and Murray, J. C. (2003). MSX1 and TGFB3 contribute to clefting in South America. J. Dent. Res. 82, 289-292.
83. Vilchis-Landeros, M. M., Montiel, J. L., Mendoza, V., Mendoza-Hernandez, G., and Lopez-Casillas, F. (2001). Recombinant soluble betaglycan is a potent and isoform-selective transforming growth factor-beta neutralizing agent. Biochem. J. 355, 215-222.
84. Vogel, T., Ahrens, S., Buttner, N., and Krieglstein, K. (2010). Transforming growth factor beta promotes neuronal cell fate of mouse cortical and hippocampal progenitors in vitro and in vivo: identification of Nedd9 as an essential signaling component. Cereb. Cortex 20, 661-671.
85. Wang, M., Huang, H., and Chen, Y. (2009). Smad2/3 is involved in growth inhibition of mouse embryonic palate mesenchymal cells induced by all-trans retinoic acid. Birth Defects Res. Part A Clin. Mol. Teratol. 85, 780-790.
86. Watanabe, T., Willis, W. D., and Pratt, R. M. (1990). Effect of retinoids on proliferation of human embryonic palatal mesenchymal cells in culture. J. Nutr. Sci. Vitaminol. 36, 311-325.
87. Waxman, J. S., Hocking, A. M., Stoick, C. L., and Moon, R. T. (2004). Zebrafish Dapper1 and Dapper2 play distinct roles in Wnt-mediated developmental processes. Development 131, 5909-5921.
88. Wilkie, A. O., and Morriss-Kay, G. M. (2001). Genetics of craniofacial development and malformation. Nat. Rev. Genet. 2, 458-468.
89. Wyszynski, D. F. (2002). Cleft Lip and Palate: From Origin to Treatment. New York: Oxford University Press.
90. Yanagisawa, J., Yanagi, Y., Masuhiro, Y., Suzawa, M., Watanabe, M., Kashiwagi, K., Toriyabe, T., Kawabata, M., Miyazono, K., and Kato, S. (1999). Convergence of transforming growth factor-beta and vitamin D signaling pathways on SMAD transcriptional coactivators. Science 283, 1317-1321.
91. Yoneda, T., and Pratt, R. M. (1981). Mesenchymal cells from the human embryonic palate are highly responsive to epidermal growth factor. Science 213, 563-565.