Recent advances in understanding transforming growth factor β regulation of orofacial development

Human and Experimental Toxicology

Volumn 24, Issue 1, 2005, Pages 1-12

  Greene, Robert M ^a   Pisano, M Michele ^a  

^a UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Cleft; Embryo; Orofacial; Retinoids; Smad; TGF

Indexed keywords

RETINOIC ACID; SMAD PROTEIN; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; SMAD6 PROTEIN; SMAD7 PROTEIN; SMAD8 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

BRANCHIAL ARCH; CELL DIVISION; CELL INTERACTION; DNA BINDING; FACE DEVELOPMENT; HUMAN; IMMUNOBLOTTING; MORPHOGENESIS; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TISSUE DIFFERENTIATION; TISSUE INTERACTION; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

ANIMALS; DNA-BINDING PROTEINS; FETAL DEVELOPMENT; HUMANS; MOUTH; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 13644270443     PISSN: 09603271     EISSN: None     Source Type: Journal    
DOI: 10.1191/0960327105ht492oa     Document Type: Review

References (113)

1. Graham A. Development of the pharyngeal arches. Am J Med Genet 2003; 119A: 251-56
2. Helms JA, Schneider RA. Cranial skeletal biology. Nature 2003; 423: 326-31.
3. Bronner-Fraser M. Mechanisms of neural crest migration. Bioessays 1993; 15: 221-30.
4. LaBonne C, Bronner-Fraser M. Molecular mechanisms of neural crest formation. Annu Rev Cell Dev Biol 1999; 15: 81-112.
5. Trainor P, Ariza-McNaughton L, Krumlauf R. Role of the isthmus and FGFs in resolving the paradox of neural crest plasticity and prepatterning. Science 2002; 295: 1288-91.
6. Golding JP, Trainor P, Krumlauf R, Glassman M. Defects in pathfinding by cranial neural crest cells in mice lacking the neuregulin receptor bB4. Nat Cell Biol 2000; 2: 103-109.
7. Couly G, Bennaceur S, Vincent C, LeDouarin N. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 2002; 129: 1061-73.
8. Derynck R, Feng X. TGF-β receptor signaling. Biochim Biophys Acta 1997; 1333: F105-50.
9. Linask KK, D'Angelo M, Gehris AL, Greene RM. Transforming growth factor-β receptor profiles of human and murine embryonic palate mesenchymal cells. Exp Cell Res 1991; 192: 1-9.
10. Cui X, Shuler C. The TGF-beta type III receptor is localized to the medial edge epithelium during palatal fusion. Int J Dev Biol 2002; 44: 397-402.
11. D'Angelo M, Greene RM. Transforming growth factor-β modulation of glycosaminoglycan production by mesenchymal cells of the developing murine secondary palate. Dev Biol 1991; 145: 374-78.
12. D'Angelo M, Chen J-M, Ugen K, Greene RM. TGFβ1 regulation of collagen metabolism by embryonic palate mesenchymal cells. J Exp Zool 1994; 270: 189-201.
13. Brown NL, Yarram SJ, Mansell JP, Sandy J. Matrix metalloproteinases have a role in palatogenesis. J Dent Res 1993; 81: 826-30.
14. Brauer P, Yee J. Cranial neural crest cells synthesize and secrete a latent form of transforming growth factor β that can be activated by neural crest cell proteolysis. Dev Biol 1993; 155: 281-85.
15. Schmid P, Cox D, Bilbe G, Maier R, McMaster GK. Differential expression of TGF beta 1, beta 2 and beta 3 genes during mouse embryogenesis. Development 1991; 111: 117-30.
16. Gehris AL, Pisano MM, Nugent P, Greene RM. Regulation of TGFβ gene expression in embryonic palatal tissue. In Vitro Dev Biol 1994; 30A: 671-79.
17. Potchinsky M, Nugent P, Lafferty C, Greene RM. Effects of dexamethasone on the expression of transforming growth factor-β in mouse embryonic palate mesenchyme cells. J Cell Physiol 1996; 166: 380-86.
18. Nugent P, Lafferty C, Greene RM. Differential expression and biological activity of retinoic acid-induced TGFβ isoforms in embryonic palate mesenchymal cells. J Cell Physiol 1998; 177: 36-46.
19. Fitzpatrick D, Denhez F, Kondaiah P, Akhurst R. Differential expression of TGFβ isoforms in murine palatogenesis. Development 1990; 109: 585-95.
20. Pelton RW, Saxena B, Jones M, Moses HL, Gold LI. Immunohistochemical localization of TGF-β1, TGF-β2, and TGF-β3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development. J Cell Biol 1991; 115: 1091-105.
21. 2 in the developing murine palate. Int J Dev Biol 1991; 35: 1-8.
22. Jaskoll T, Choy H, Chen H, Melnick R. Developmental expression and CORT-regulation of TGF-beta and EGF receptor mRNA during mouse palatal morphogenesis: correlation between CORT-induced cleft palate and TGF-beta 2 mRNA expression. Teratology 1996; 54: 34-44.
23. Kaartinen V, Voncken J W, Shuler C, Warburton D, Bu D, Heisterkamp N, Groffen J. Abnormal lung development and cleft palate in mice lacking TGF-β3 indicates defects of epithelial-mesenchymal interaction. Nature Genetics, 1995; 11: 415-21.
24. Proetzel G, Pawlowski SA, Wiles MV, Yin M, Boivin GP, Howles PN, et al. Transforming growth factor-β3 is required for secondary palate fusion. Nat Genet 1995; 11: 409-14.
25. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, et al. TGF-β2 knockout mice have multiple developmental defects that are non-overlapping with other TGF-β knockout phenotypes. Development 1997; 124: 2659-70.
26. Doetschman T. Interpretation of phenotype in genetically engineered mice. Lab Anim Sci 1999; 49: 137-43.
27. Lidral AC, Murray JC, Buetow KH, Basart AM, Schearer H, Shiang R, et al. Studies of the candidate genes TGFβ-2, MSX1, TGF-α, and TGFβ-3 in the etiology of cleft lip and palate in the Philippines. Cleft Palate Craniofac J 1997; 34: 1-6.
28. Lidral AC, Romitti PA, Basart AM, Doetschman T, Leysens NJ, Daack-Hirsch S, et al. Association of MSX1 and TGFβ3 with nonsyndromic clefting in humans. Am J Hum Genet 1998; 63: 557-68.
29. Romitti PA, Lidral AC, Munger RG, Daack-Hirsch S, Burns TL, Murray JC. Candidate genes for nonsyndromic cleft lip and palate and maternal cigarette smoking and alcohol consumption: evaluation of genotype-environment interactions from a population-based case-control study of orofacial clefts. Teratology 1999; 59: 39-50.
30. Sato F, Natsume N, Machida J, Suzuki S, Kawai T. Association between transforming growth factor beta 3 and cleft lip and/or cleft palate in the Japanese population. Plast Reconstr Surg 2001; 107: 1909-10.
31. Gehris AL, Greene RM. Regulation of murine embryonic epithelial cell differentiation by transforming growth factors β. Differentiation 1992; 49: 167-73.
32. Brunet C, Sharpe P, Ferguson M. Inhibition of TGFβ3 (but not TGFβ1 or TGFβ2) actively prevents normal mouse embryonic palate fusion. Int J Dev Biol 1993; 39: 345-55.
33. Greene RM, Pisano MM. Analysis of cell proliferation in developing orofacial tissue. In Kimmel GL, Kochhar DM eds. In vitro techniques in developmental toxicology: use in defining mechanisms and risk parameters. Boca Raton, FL: CRC Press, 1989.
34. Derynck R, Zhang Y, Feng X-H. Smads: transcriptional activators of TGF-β responses. Cell 1998; 95: 737-40.
35. Massagué J. TGF-β signal transduction. Annu Rev Biochem 1998; 67: 753-91.
36. Itoh S, Itoh F, Goumans M-J, ten Dijke P. Signaling of transforming growth factor-β family members through Smad proteins. Eur J Biochem 2000; 267: 6954-67.
37. Shi Y. Structural insights on Smad function in TGF-β signaling. Bioessays 2001; 23: 223-32.
38. Attisano L, Wrana J. Smads as transcriptional co-modulators. Curr Opin Cell Biol 2000; 12: 235-43.
39. Imamura T, Takase M, Nishihara A, Oeda I, Hanai J-I, Kawabata M, et al. Smad6 inhibits signalling by the TGF-β superfamily. Nature 1997; 389: 622-26.
40. Hayashi H, Abdollah S, Qiu Y, Cai J, Xu YY, Grinnell BW, et al. The MAD-related protein Smad7 associates with the TGFβ receptor and functions as an antagonist of TGFβ signaling. Cell 1997; 89: 1165-73.
41. LaSueur J, Fortuno E, Mckay R, Graff J. Smad 10 is required for formation of the frog nervous system. Dev Cell 2002; 2: 771-83.
42. Watanabe TK, Suzuki M, Omori Y, Hishigaki H, Horie M, Kanemoto N, et al. Cloning and characterization of a novel member of the human Mad gene family. Genomics 1997; 42: 446-51.
43. Nomura M, Li E. Smad2 role in mesoderm formation, left-right patterning and craniofacial development. Nature 1998; 393: 786-90.
44. Cacheux V, Dastot-Le Moal F, Kääriäinen H, Bondurand N, Rintala R, Boissier B, et al. Loss-of-function mutations in SIP1 Smad interacting protein 1 results in a syndromic Hirschsprung disease. Hum Mol Genet 2001; 10: 1503-10.
45. Hoodless P, Haerry T, Abdollah S, Stapleton M, O'Connor M, Attisano L, et al. MADR1, a MAD-related protein that functions in BMP2 signalling pathways. Cell 1996; 85: 489-500.
46. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, et al. TGF-β receptor-mediated signalling through Smad2, SmadS and Smad4. EMBO J 1997; 16: 5353-62.
47. Zhang Y, Feng X, Derynck R. Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-beta-induced transcription. Nature 1998; 394: 909-13.
48. Macias-Silva M, Abdollah S, Hoodless PA, Pirone R, Attisano L, Wrana JL. MADR2 is a substrate of the TGF-β receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 1996; 87: 1215-24.
49. Shi Y, Wang Y-F, Jayaraman L, Yang H, Massagué J, Pavletich NP. Crystal structure of a Smad MH1 domain bound to DNA: insights on DNA binding in TGF-β signaling. Cell 1998; 94: 585-94.
50. Cui X-M, Chai Y, Chen J, Yamamoto T, Ito Y, Bringas P, et al. TGF-β3-dependent SMAD2 phosphorylation and inhibition of MEE proliferation during palatal fusion. Dev Dyn 2003; 227: 387-94.
51. Wrana J. Regulation of Smad activity. Cell 2000; 100: 189-92.
52. Wu R, Zhang Y, Feng X, Derynck R. Heteromeric and homomeric interactions correlate with signaling activity and functional cooperativity of Smad3 and Smad4 (DPC4). Mol Cell Biol 1997; 17: 2521-28.
53. Massagué J, Wotton D. Transcriptional control by the TGF-β/Smad signaling system. EMBO J 2000; 19: 1745-54.
54. Greene RM, Nugent P, Mukhopadhyay P, Warner DR, Pisano MM. Intracellular dynamics of Smad-mediated TGFβ signaling. J Cell Physiol 2003; 197: 261-71.
55. Reisdorf P, Lawrence DA, Sivan V, Klising E, Martin MT. Alteration of transforming growth factor-beta1 response involves down-regulation of Smad3 in myofibroblasts from skin fibrosis. Am J Pathol 2001; 159: 263-72.
56. Pouponnot C, Jayaraman L, Massague J. Physical and functional interaction of SMADs and p300/CBP. J Biol Chem 1998; 273: 22865-68.
57. Stroschein SL, Wang W, Zhou S, Zhou Q, Luo K. Negative feedback regulation of TGF-β signaling by the SnoN oncoprotein. Science 1999; 286: 771-74.
58. Xu W, Angelis K, Danielpour D, Haddad MM, Bischof O, Campisi J, et al. Ski acts as a co-repressor with Smad2 and Smad3 to regulate the response to type β transforming growth factor. Proc Natl Acad Sci USA 2000; 97: 5924-29.
59. ten Dijke P, Miyazono K, Heldin C. Signaling inputs converge on nuclear effectors in TGF-β signaling. Trends Biochem Sci 2000; 25: 64-70.
60. Warner D, Pisano MM, Greene RM. Nuclear convergence of the TGFβ and cAMP signal transduction pathways in murine embryonic palate mesenchymal cells. Cell Signal 2003; 15: 235-42.
61. Warner D, Pisano MM, Roberts E, Greene RM. Identification of novel Smad 3 binding proteins containing PDZ domains. FEBS Lett 2003; 539: 167-73.
62. Bhowmick NA, Ghiassa M, Bakin A, Aakre M, Lundquist CA, Engel ME, et al. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell 2001; 12: 27-36.
63. Miettinen PJ, Chin JR, Shum L, Slavkin HC, Shuler CF, Derynck R, Werb Z. Epidermal growth factor receptor function is necessary for normal craniofacial development and palate closure. Nat Genet 1999; 22: 69-73.
64. Piek E, Moustakas A, Kurisaki A, Heldin CH, ten Dijke P. TGF-(beta) type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. J Cell Sci 1999; 112: 4557-68.
65. Sellers WR, Kaelin WG. RB as a modulator of transcription. Biochim Biophys Acta 1996; 1288: M1-5.
66. Stiegler P, Kasten M, Giordano A. The RB family of cell cycle regulatory factors. J Cell Biochem (Suppl) 1998; 30/31: 30-36.
67. Bonaiti-Pellie C, Briard-Guillemot L, Feingold J, Frezal J. Associated congenital malformations in retinoblastoma. Clin Genet 1975; 7: 37-39.
68. Leezer J, Hackmiller RC, Greene RM, Pisano MM. Expression of the retinoblastoma family of tumor suppressors during murine embryonic orofacial development. Orthod Craniofac Res 2003; 6: 32-47.
69. Lavia P, Jansen-Dürr P. E2F target genes and cell-cycle checkpoint control. BioEssays 1999; 21: 221-30.
70. Lukas J, Petersen BO, Holm K, Bartek J, Helin K. Deregulated expression of E2F family members induces S-phase entry and overcomes p16INK4A-mediated growth suppression. Mol Cell Biol 1996; 16: 1047-57.
71. Schwarz JK, Bassing CH, Kovesdi I, Datto MB, Blazing M, George S, et al. Expression of the E2F1 transcription factor overcomes type b transforming growth factor-mediated growth suppression. Proc Natl Acad Sci USA 1995; 92: 483-87.
72. Kusek J, Greene RM, Nugent P, Pisano MM. Expression of the E2F family of transcription factors in murine development. Int J Dev Biol 2000; 44: 267-77.
73. Jochheim A, Cieslak A, Hillemann T, Cantz T, Scharf J, Manns MP, et al. Multi-stage analysis of differential gene expression in BALB/C mouse liver development by high-density microarrays. Differentiation 2003; 71: 62-72.
74. Richards J, Le Naour F, Hanash S, Beretta L. Integrated genomic and proteomic analysis of signaling pathways in dendritic cell differentiation and maturation. Ann NY Acad Sci 2002; 975: 91-100.
75. Pisano MM, Mukhopadhyay P, Greene RM. Molecular fingerprinting of TGFβ-treated embryonic palate mesenchymal cells. Orthod Craniofac Res 2003 (in press).
76. Beaty TH, Hetmanski JB, Zeiger JS, Fan YT, Liang KY, VanderKolk CA, et al. Testing candidate genes for non-syndromic oral clefts using a case-parent trio design. Genet Epidemiol 2002; 22: 1-11.
77. Maestri NE, Beaty TH, Hetmanski J, Smith EA, McIntosh I, Wyszynski DF, et al. Application of transmission disequilibrium tests to nonsyndromic oral clefts: including candidate genes and environmental exposures in the models. Am J Med Genet 1997; 73: 337-44.
78. Beaty TH, Wang H, Hetmanski JB, Fan YT, Zeiger JS, Liang KY, et al. A case-control study of nonsyndromic oral clefts in Maryland. Ann Epidemiol 2001; 11: 434-42.
79. Jugessur A, Lie RT, Wilcox AJ, Murray JC, Taylor JA, Saugstad OD, et al. Variants of developmental genes (TGFA, TGFβ3, and MSX1) and their associations with orofacial clefts: A case-parent triad analysis. Genet Epidemiol 2003; 24: 230-39.
80. Janknecht R, Hunter T. A growing coactivator network. Nature 1996; 383: 22-23.
81. Glick AB, Flanders KC, Danielpour D, Yuspa SH, Sporn MB. Retinoic acid induces transforming growth factor β2 in cultured keratinocytes and mouse epidermis. Cell Regul 1989; 1: 87-97.
82. Valette A, Botanch C. Transforming growth factor beta (TGF-β) potentiates the inhibitory effect of retinoic acid on human breast carcinoma (MCF-7) cell proliferation. Growth Factors 1990; 2: 283-87.
83. Falk LA, De Benedetti F, Lohrey N, Birchenall-Roberts MC, Ellingsworth LW, Faltynek CR, et al. Induction of transforming growth factor-β1 (TGF-β1) receptor expression and TGF-β1 protein production in retinoic acid-treated HL-60 cells: possible TGF-β1-mediated autocrine inhibition. Blood 1991; 77: 1248-55.
84. Mahmood R, Flanders KC, Morriss-Kay GM. The effects of retinoid status on TGF β expression during mouse embryogenesis. Anat Embryol 1995; 192: 21-33.
85. Han G-R, Dohi DF, Lee H-Y, Rajah R, Walsh GL, Hong WK, et al. All-trans-retinoic acid increases transforming growth factor-β2 and insulin-like growth factor binding protein-3 expression through retinoic acid receptor-a-dependent signaling pathway. J Biol Chem 1997; 272: 13711-16.
86. Degitz S, Morriss D, Foley G, Francis BM. Role of TGF-β in RA-induced cleft palate in CD-1 mice. Teratology 1998; 58: 197-204.
87. Danielpour D. Induction of transforming growth factor-β autocrine activity by all-trans-retinoic acid and 1,25-dihydroxyvitamin D3 in NRP-152 rat prostatic epithelial cells. J Cell Physiol 1996; 166: 231-39.
88. Nunes I, Kojima S, Rifkin DB. Effects of endogenously activated transforming growth factor-β on growth and differentiation of retinoic acid-treated HL-60 cells. Cancer Res 1996; 56: 495-99.
89. Borger DR, Mi Y, Geslani G, Zyzak LL, Batova A, Engin TS, et al. Retinoic acid resistance at late stages of human papillomavirus type 16-mediated transformation of human keratinocytes arises despite intact retinoid signaling and is due to a loss of sensitivity to transforming growth factor-beta. Virology 2000; 270: 397-407.
90. Mercier T, Gaillard-Sanchez I, Martel P, Heberden C. TGF-beta receptors are diminished after retinoid exposure in rat liver epithelial cells. J Cell Biochem 1996; 61: 230-37.
91. Ang HL, Deltour L, Hayamizu TF, Zgombic-Knight M, Duester G. Retinoic acid synthesis in mouse embryos during gastrulation and craniofacial development linked to class IV alcohol dehydrogenase gene expression. J Biol Chem 1996; 271: 9526-34.
92. Niederreither K, Subbarayan V, Dolle P, Chambon P. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 1999; 21: 444-48.
93. Eichele G. A vital role for vitamin A. Nat Genet 1999; 21: 346-47.
94. Nugent P, Greene RM. Interactions between the TGFβ and retinoic acid signal transduction pathways in embryonic palatal cells. Differentiation 1994; 58: 149-55.
95. Nugent P, Potchinsky M, Lafferty C, Greene RM. TGF-β modulates the expression of retinoic acid-induced RAR-β in primary cultures of embryonic palate cells. Exp Cell Res 1995; 220: 495-500.
96. Nugent P, Kusek J, Pisano MM, Greene RM. Convergence of cAMP, TGFβ and retinoic acid signaling pathways in cells of the embryonic palate. Life Sci 2001; 69: 2091-102.
97. Lammer EJ, Chen DT, Hoar RM, Agnish ND, Benke PJ, Braun JT, et al. Retinoic acid embryopathy. N Engl J Med 1985; 313: 837-41.
98. Rothman KJ, Moore LL, Singer MR, Nguyen U-S, Mannino S, Milunsky A. Teratogenicity of high vitamin A intake. N Engl J Med 1995; 333: 1369-415.
99. Collins MD, Mao GE. Teratology of retinoids. Annu Rev Pharmacol and Toxicol 1999; 39: 399-430.
100. Giguere V. Retinoic acid receptors and cellular retinoid binding proteins: complex interplay in retinoid signaling. Endocrine Rev 1994; 15: 61-79.
101. Leid M, Kastner P, Durand B, Krust A, Leroy P, Lyons R, et al. Retinoic acid signal transduction pathways. Ann NY Acad Sci 1993; 684: 19-34.
102. Mangelsdorf DJ, Kliewer SA, Kakizuka A, Umesono K, Evans RM. Retinoid receptors. Recent Prog Horm Res 1993; 48: 99-121.
103. Kastner P, Mark M, Ghyselinck N, Krezel W, Dupe V, Grondona JM, et al. Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development 1997; 124: 313-26.
104. Giannini G, Dawson M, Zhang X-K, Thiele CJ. Activation of three distinct RXR/RAR heterodimers induces growth arrest and differentiation of neuroblastoma cells. J Biol Chem 1997; 272: 26693-701.
105. Chiba H, Clifford J, Metzger D, Chambon P. Distinct retinoid X receptor-retinoic acid receptor heterodimers are differentially involved in the control of expression of retinoid target genes in F9 embryonal carcinoma cells. Mol Cell Biol 1997; 17: 3013-20.
106. Damm K, Heyman R, Umesono K, Evans RM. Functional inhibition of retinoic acid response by dominant negative retinoic acid receptor mutants. Proc Natl Acad Sci USA 1993; 90: 2989-93.
107. Iulianella A, Lohnes D. Contribution of retinoic acid receptor gamma to retinoid-induced craniofacial and axial defects. Dev Dyn 1997; 209: 92-104.
108. Matt N, Ghyselinck NB, Wendling O, Chambon P, Mark M. Retinoic acid-induced developmental defects are mediated by RAR beta/RXR heterodimers in the pharyngeal endoderm. Development 2003; 130: 2083-93.
109. Mendelsohn C, Lohnes D, Decimo D, Lufkin T, LeMeur M, Chambon P et al. Function of the retinoic acid receptors (RARs) during development. II. Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 1994; 120: 2749-71.
110. Lohnes D, Kastner P, Dierich A, Mark M, LeMeur M, Chambon P. Function of retinoic acid receptor γ (RAR γ) in the mouse. Cell 1993; 73: 643-58.
111. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, et al. TGF-β2 knockout mice have multiple developmental defects that are non-overlapping with other TGF-β knockout phenotypes. Development 1997; 124: 2659-70.
112. Kallapur S, Ormsby I, Doetschman T. Strain dependency of TGF-β1 function during embryogenesis. Mol Reprod Dev 1999; 52: 341-49.
113. Nugent P, Pisano MM, Weinreich M, Greene RM. Increased susceptibility of TGFβ2 knockout mice to retinoid-induced teratogenesis. Reprod Toxicol 2002; 16: 741-47.