Molecular mechanism of teratogenic effects induced by the fungicide triadimefon: Study of the expression of TGF-β mRNA and TGF-β and CRABPI proteins during rat in vitro development

Toxicology and Applied Pharmacology

Volumn 234, Issue 1, 2009, Pages 107-116

  Di Renzo, F ^a   Corsini, E ^a   Broccia, M L ^a   Marinovich, M ^a   Galli, C L ^a   Giavini, E ^a   Menegola, E ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

CRABP; Hindbrain; NCC; Teratogenesis; TGF ; Triazoles; Whole embryo culture

Indexed keywords

BINDING PROTEIN; CELLULAR RETINOIC ACID BINDING PROTEIN; FUNGICIDE; RETINOIC ACID; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; TRIADIMEFON; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRANIAL NERVE; CROWN RUMP LENGTH; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO CULTURE; EMBRYO DEVELOPMENT; GENE EXPRESSION; HEAD CIRCUMFERENCE; HISTOLOGY; IMMUNOHISTOCHEMISTRY; NEURAL CREST CELL; NONHUMAN; PROTEIN ANALYSIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHOMBENCEPHALON; SOMITE; TERATOGENICITY; WESTERN BLOTTING; YOLK SAC;

ANIMALS; BLOTTING, WESTERN; EMBRYO CULTURE TECHNIQUES; FEMALE; FUNGICIDES, INDUSTRIAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; PROTEIN-SERINE-THREONINE KINASES; PROTEOGLYCANS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, RETINOIC ACID; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TERATOGENS; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; TRIAZOLES;

MUS; RATTUS;

EID: 57149119051     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2008.09.025     Document Type: Article

References (64)

1. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
2. Brown N.A., and Fabro S. Quantitation of rat embryonic development in vitro: a morphological scoring system. Teratology 24 (1981) 65-78
3. Chai Y., Ito Y., and Han J. TGF-β signaling and its functional significance in regulating the fate of cranial neural crest cells. Crit. Rev. Oral Biol. Med. 14 (2003) 78-88
4. Chen F., Desai T.J., Qian J., Niederreither K., Lü J., and Cardoso W.V. Inhibition of Tgf beta signaling by endogenous retinoic acid is essential for primary lung bud induction. Development 134 (2007) 2969-2979
5. Colakoǧlu N., and Kükner A. Teratogenicity of retinoic acid and its effects on TGF-beta2 expression in the developing cerebral cortex of the rat. J. Mol. Histol. 35 (2004) 823-827
6. Colakoglu N., Kukner A., Oner J., Sonmez M.F., Oner H., and Ozan E. Effects of high dose retinoic acid on TGF-beta2 expression during pancreatic organogenesis. J. Mol. Histol. 36 (2005) 413-418
7. Dekker E.J., Vaessen M.J., van den Berg C., Timmermans A., Godsave S., Holling T., Nieuwkoop P., Geurts van Kessel A., and Durston A. Overexpression of a cellular retinoic acid binding protein (xCRABP) causes anteroposterior defects in developing Xenopus embryos. Development 120 (1994) 973-985
8. Di Renzo F., Broccia M.L., Giavini E., and Menegola E. Antifungal triazole derivative triadimefon induces ectopic maxillary cartilage by altering the morphogenesis of the first branchial arch. Birth Defects Res. B 80 (2007) 2-11
9. Di Renzo F., Broccia M.L., Giavini E., and Menegola E. Citral, an inhibitor of retinoic acid synthesis, attenuates the frequency and severity of branchial arch abnormalities induced by triazole-derivative fluconazole in rat embryos cultured in vitro. Reprod. Toxicol. 24 (2007) 326-332
10. Epperlein H., Meulemans D., Bronner-Fraser M., Steinbeisser H., and Selleck M.A. Analysis of cranial neural crest migratory pathways in axolotl using cell markers and transplantation. Development 127 (2000) 2751-2761
11. Francis P.H., Richardson M.K., Brickell P.M., and Tickle C. Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development 120 (1994) 209-218
12. Frenz D.A., and Liu W. Treatment with all-trans-retinoic acid decreases levels of endogenous TGF-beta(1) in the mesenchyme of the developing mouse inner ear. Teratology 61 (2000) 297-304
13. Giavini E., Broccia M.L., Prati M., Bellomo D., and Menegola E. Effects of ethanol and acetaldehyde on rat embryos developing in vitro. In Vitro Cell. Dev. Biol. 28 (1992) 205-210
14. Goumans M.J., and Mummery C. Functional analysis of the TGFbeta receptor/Smad pathway through gene ablation in mice. Int. J. Dev. Biol. 44 (2000) 253-265
15. Groppelli S., Pennati R., De Bernardi F., Menegola E., Giavini E., and Sotgia C. Teratogenic effects of two antifungal triazoles, triadimefon and triadimenol, on Xenopus laevis development: craniofacial defects. Aquat. Toxicol. 73 (2005) 370-381
16. Kessel M., and Gruss P. Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67 (1991) 89-104
17. Kloen P., Visker M.H., Olijve W., van Zoelen E.J., and Boersma C.J. Cell-type-specific modulation of Hox gene expression by members of the TGF-beta superfamily: a comparison between human osteosarcoma and neuroblastoma cell lines. Biochem. Biophys. Res. Commun. 233 (1997) 365-369
18. Le Douarin N.M., and Dupin E. Multipotentiality of the neural crest. Curr. Opin. Genet. Dev. 13 (2003) 529-536
19. Leonard L., Horton C., Maden M., and Pizzey J.A. Anteriorization of CRABP-I expression by retinoic acid in the developing mouse central nervous system and its relationship to teratogenesis. Dev. Biol. 168 (1995) 514-528
20. Li X., and Cao X. BMP signaling and HOX transcription factors in limb development. Front. Biosci. 8 (2003) 805-812
21. Li X., and Cao X. BMP signaling and skeletogenesis. Ann. N. Y. Acad. Sci. 1068 (2006) 26-40
22. Loeys B.L., Chen J., Neptune E.R., Judge D.P., Podowski M., Holm T., Meyers J., Leitch C.C., Katsanis N., Sharifi N., Xu F.L., Myers L.A., Spevak P.J., Cameron D.E., De Backer J., Hellemans J., Chen Y., Davis E.C., Webb C.L., Kress W., Coucke P., Rifkin D.B., De Paepe A.M., and Dietz H.C. A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nat. Genet. 37 (2005) 275-281
23. Lohnes D., Kastner P., Dierich A., Mark M., LeMeur M., and Chambon P. Function of retinoic acid receptor g (RAR g) in the mouse. Cell 73 (1993) 643-658
24. Lumsden A., Sprawson N., and Graham A. Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 113 (1991) 1281-1291
25. Mark M., Lohnes D., Mendelsohn C., Dupé V., Vonesch J.L., Kastner P., Rijli F., Bloch-Zupan A., and Chambon P. Roles of retinoic acid receptors and of Hox genes in the patterning of the teeth and of the jaw skeleton. Int. J. Dev. Biol. 39 (1995) 111-121
26. Maden M., Hunt P., Eriksson U., Kuroiwa A., Krumlauf R., and Summerbell D. Retinoic acid-binding protein, rhombomeres and the neural crest. Development 111 (1991) 35-43
27. Mahmood R., Flanders K.C., and Morriss-Kay G.M. Interactions between retinoids and TGF beta s in mouse morphogenesis. Development 115 (1992) 67-74
28. Mahmood R., Flanders K.C., and Morriss-Kay G.M. The effects of retinoid status on TGF beta expression during mouse embryogenesis. Anat. Embryol. 192 (1995) 21-33
29. Marlétaz F., Holland L.Z., Laudet V., and Schubert M. Retinoic acid signaling and the evolution of chordates. Int. J. Biol. Sci. 2 (2006) 38-47
30. Massa V., Gaudenzi G., Sangiorgio L., Cotelli F., and Giavini E. Krox20 is down-regulated following triazole in vitro embryonic exposure: a polycompetitor-based assay. Toxicol. Lett. 169 (2007) 196-204
31. McGinnis W., and Krumlauf R. Homeobox genes and axial patterning. Cell 68 (1992) 283-302
32. Mendelsohn C., Lohnes D., Decimo D., Lufkin T., LeMeur M., Chambon P., and Mark M. Function of the retinoic acid receptors (RARs) during development. II. Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120 (1994) 2749-2771
33. Menegola E., Broccia M.L., Di Renzo F., Prati M., and Giavini E. In vitro teratogenic potential of two antifungal triazoles: triadimefon and triadimenol. In Vitro Cell. Dev. Biol., Anim. 36 (2000) 88-95
34. Menegola E., Broccia M.L., Di Renzo F., and Giavini E. Antifungal triazoles induce malformations in vitro. Reprod. Toxicol 15 (2001) 421-427
35. Menegola E., Broccia M.L., Di Renzo F., and Giavini E. Pathogenic pathways in fluconazole-induced branchial arch malformations. Birth Defects Res. A 67 (2003) 116-124
36. Menegola E., Broccia M.L., Di Renzo F., Massa V., and Giavini E. Relationship between hindbrain segmentation, neural crest cell migration and branchial arch abnormalities in rat embryos exposed to fluconazole and retinoic acid in vitro. Reprod. Toxicol 18 (2004) 121-130
37. Menegola E., Broccia M.L., Di Renzo F., Massa V., and Giavini E. Study on the common teratogenic pathway elicited by the fungicides triazole-derivatives. Toxicol. In Vitro 19 (2005) 737-748
38. Menegola E., Broccia M.L., Di Renzo F., Massa V., and Giavini E. Craniofacial and axial skeletal defects induced by the fungicide triadimefon in the mouse. Birth Defects Res. B 74 (2005) 185-195
39. Menegola E., Broccia M.L., Di Renzo F., and Giavini E. Postulated pathogenic pathway in triazole fungicide induced dysmorphogenic effects. Reprod. Toxicol. 22 (2006) 186-195
40. Menegola E., Broccia M.L., Di Renzo F., and Giavini E. Dysmorphogenic effects of some fungicides derived from the imidazole on rat embryos cultured in vitro. Reprod. Toxicol. 21 (2006) 74-82
41. Meulemans D., and Bronner-Fraser M. Amphioxus and lamprey AP-2 genes: implications for neural crest evolution and migration patterns. Development 129 (2002) 4953-4962
42. Morriss-Kay G. Retinoic acid and development. Pathobiology 60 (1992) 264-270
43. Morriss-Kay G.M., Murphy P., Hill R.E., and Davidson D.R. Effects of retinoic acid excess on expression of Hox-2.9 and Krox-20 and on morphological segmentation in the hindbrain of mouse embryos. EMBO J. 10 (1991) 2985-2995
44. Moudgal V.V., and Sobel J.D. Antifungal drugs in pregnancy: a review. Expert Opin. Drug. Saf. 2 (2003) 475-483
45. New D.A.T. Whole embryo culture and the study of mammalian embryos during organogenesis. Biol. Rev. 53 (1978) 81-122
46. Nugent P., and Greene R.M. Interactions between the transforming growth factor beta (TGF beta) and retinoic acid signal transduction pathways in murine embryonic palatal cells. Differentiation 58 (1994) 149-155
47. Nugent P., Potchinsky M., Lafferty C., and Greene R.M. TGF-beta modulates the expression of retinoic acid-induced RAR-beta in primary cultures of embryonic palate cells. Exp. Cell Res. 220 (1995) 495-500
48. Osumi-Yamashita N., Ninomiya Y., Doi H., and Eto K. The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos. Dev. Biol. 164 (1994) 409-419
49. Papis E., Bernardini G., Gornati R., and Prati M. Triadimefon causes branchial arch malformations in Xenopus laevis embryos. Environ. Sci. Pollut. Res. Int. 13 (2006) 251-255
50. Ruberte E., Friederich V., Morriss-Kay G., and Chambon P. Differential distribution patterns of CRABP I and CRABP II transcripts during mouse embryogenesis. Development 115 (1992) 973-987
51. Sanford L.P., Ormsby I., Gittenberger-de Groot A.C., Sariola H., Friedman R., Boivin G.P., Cardell E.L., and Doetschman T. TGF-b 2 knockout mice have multiple developmental defects that are non-overlapping with other TGF-b knockout phenotypes. Development 124 (1997) 2659-2670
52. Santagati F., and Rijli F.M. Cranial neural crest and the building of the vertebrate head. Nat. Rev. Neurosci. 4 (2003) 806-818
53. Schneider R.A., Hu D., Rubenstein J.L., Maden M., and Helms J.A. Local retinoid signaling coordinates forebrain and facial morphogenesis by maintaining FGF8 and SHH. Development 128 (2001) 2755-2767
54. Suzuki T., Bessho K., Segami N., Nojima T., and Iizuka T. Bone morphogenetic protein-2 in temporomandibular joints with internal derangement. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 88 (1999) 670-673
55. Tabin C. The initiation of the limb bud: growth factors, Hox genes, and retinoids. Cell 80 (1995) 671-674
56. Taylor L.E., Bennett G.D., and Finnell R.H. Altered gene expression in murine branchial arches following in utero exposure to retinoic acid. J. Craniofac. Genet. Dev. Biol. 15 (1995) 13-25
57. Tiboni G.M. Second branchial arch anomalies induced by fluconazole, a bis-triazole antifungal agent, in cultured mouse embryos. Res. Commun. Chem. Pathol. Pharmacol. 79 (1993) 381-384
58. Tiboni G.M., and Giampietro F. Murine teratology of fluconazole: evaluation of developmental phase specificity and dose dependence. Pediatr. Res. 58 (2005) 94-99
59. Tiboni G.M., Iammarrone E., Giampietro F., La monaca D., Bellati U., and Di Ilio C. Teratological interaction between the bis-triazole antifungal agent fluconazole and the anticonvulsant drug phenytoin. Teratology 59 (1999) 81-87
60. Tiboni G.M., Giampietro F., Angelucci S., Moio P., Bellati U., and Di Ilio C. Additional investigation on the potentiation of phenytoin teratogenicity by fluconazole. Toxicol. Lett. 145 (2003) 219-229
61. Trainor P.A., Sobieszczuk D., Wilkinson D., and Krumlauf R. Signalling between the hindbrain and paraxial tissues dictates neural crest migration pathways. Development 129 (2002) 433-442
62. Wang Y.L., and Brown N.A. Expression patterns of HOX-B1, -B2 and KROX 20 in triazole-treated rat embryos suggest rhombomere reductions and loss. Teratology 49 (1994) 358-420
63. Whiting J. Craniofacial abnormalities induced by the ectopic expression of homeobox genes. Mutat. Res. 396 (1997) 97-112
64. Yu Z., and Xing Y. All-trans retinoic acid inhibited chondrogenesis of mouse embryonic palate mesenchymal cells by down-regulation of TGF-beta/Smad signaling. Biochem. Biophys. Res. Commun. 340 (2006) 929-934