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Molecular aspects of azoles-induced teratogenesis

, PhD & , MD
Pages 461-482 | Published online: 26 Jan 2010

Bibliography

  • Wilson JW. Environment and birth defects (environmental science series). Academic Press, London; 1973
  • Karnofsky DA. Drugs as teratogens in animals and man. Annu Rev Pharmacol 1965;10:447-72
  • Caputo R. Itraconazole (sporanox) in superficial and systemic fungal infections. Expert Rev Anti Infect Ther 2003;1:531-42
  • Zarn JA, Brüschweiler BJ, Schlatter JR. Azole fungicides affect mammalian steroidogenesis by inhibiting sterol 14alpha-demethylase and aromatase. Environ Health Perspect 2003;111:255-61
  • Dix DJ, Gallagher K, Benson WH, A framework for the use of genomics data at the EPA. Nat Biotechnol 2006;24:1108-11
  • Vanden Bossche H, Ausma J, Bohets H, The novel azole R126638 is a selective inhibitor of ergosterol synthesis in Candida albicans, Trichophyton spp., and Microsporum canis. Antimicrob Agents Chemother 2004;48:3272-8
  • Georgopapadakou NH. Antifungals: mechanism of action and resistance, established and novel drugs. Curr Opin Microbiol 1998;1:547-57
  • Yoshida Y, Aoyama Y, Noshiro M, Sterol 14-demethylase P450 (CYP51) provides a breakthrough for the discussion on the evolution of cytochrome P450 gene superfamily. Biochem Biophys Res Commun 2000;273:799-804
  • Czeizel AE, Kazy Z, Vargha P. A population-based case-control teratological study of vaginal econazole treatment during pregnancy. Eur J Obstet Gynecol Reprod Biol 2003;111:135-40
  • Rosa FW, Baum C, Shaw M. Pregnancy outcomes after first-trimester vaginitis drug therapy. Obstet Gynecol 1987;69:751-5
  • Inman W, Pearce G, Wilton L. Safety of fluconazole in the treatment of vaginal candidiasis. A prescription-event monitoring study, with special reference to the outcome of pregnancy. Eur J Clin Pharmacol 1994;46:115-8
  • Mastroiacovo P, Mazzone T, Botto LD, Prospective assessment of pregnancy outcomes after first-trimester exposure to fluconazole. Am J Obstet Gynecol 1996;175:1645-50
  • Sorensen HT, Nielsen GL, Olesen C, Risk of malformations and other outcomes in children exposed to fluconazole in utero. Br J Clin Pharmacol 1999;48:234-8
  • Jick SS. Pregnancy outcomes after maternal exposure to fluconazole. Pharmacotherapy 1999;19:221-22
  • Campomori A, Bonati M. Fluconazole treatment for vulvovaginal candidiasis during pregnancy. Ann Pharmacother 1997;31:118-9
  • Nørgaard M, Pedersen L, Gislum M, Maternal use of fluconazole and risk of congenital malformations: a Danish population-based cohort study. J Antimicrob Chemother 2008;62:172-6
  • Bar-Oz B, Moretti ME, Mareels G, G. Reporting bias in retrospective ascertainment of drug-induced embryopathy. Lancet 1999;354:1700-1
  • Bar-Oz B, Moretti ME, Bishai R, Pregnancy outcome after in utero exposure to itraconazole: a prospective cohort study. Am J Obstet Gynecol 2000;183:617-20
  • De Santis M, Di Gianantonio E, Cesari E, First-trimester itraconazole exposure and pregnancy outcome: a prospective cohort study of women contacting teratology information services in Italy. Drug Saf 2009;32:239-44
  • Rosa FW. Drugs in pregnancy and lactation. Michigan Medicaid Surveillance Study. 1993
  • Kazy Z, Puhó E, Czeizel AE. Population-based case-control study of oral ketoconazole treatment for birth outcomes. Congenit Anom (Kyoto) 2005;45:5-8
  • Carter TC, Druschel CM, Romitti PA, Antifungal drugs and the risk of selected birth defects. Am J Obstet Gynecol 2008;198:191;e1-7
  • Kazy Z, Puhó E, Czeizel AE. Teratogenic potential of vaginal metronidazole treatment during pregnancy. Eur J Obstet Gynecol Reprod Biol 2005;123:174-8
  • Czeizel AE, Kazy Z, Puhó E. Population-based case-control teratologic study of topical miconazole. Congenit Anom (Kyoto) 2004;44:41-5
  • Kazy Z, Puhó E, Czeizel AE. The possible association between the combination of vaginal metronidazole and miconazole treatment and polysyndactyly. Population-based case-control teratologic study. Reprod Toxicol 2005;20:89-94
  • EMEA 2008. Available from: www.emea.europa.eu/htm
  • Shepard TH. Proof of human teratogenicity. Teratology 1994;50:97-8
  • Carey JC, Martinez L, Balken E, Determination of human teratogenicity by the astute clinician method: review of illustrative agents and a proposal of guidelines. Birth Defects Res A Clin Mol Teratol 2009;85:63-8
  • Lopez-Rangel E, Van Allen MI. Prenatal exposure to fluconazole: an identifiable dysmorphic phenotype. Birth Defects Res A 2005;73:919-23
  • Reiners J, Wittfoht W, Nau H, Teratogenesis and pharmacokinetics of cyclophosphamide after drug infusion as compared to injection in the mouse during day 10 of gestation. In: Nau H, Scott WJ Jr, editor, Experimental aspects in vivo and in vitro. Pharmacokinetics in teratogenesis. (Volume 2). CRC Press, Boca Raton; 1987. p. 41-8
  • Nau H. Teratogenic valproic acid concentrations: infusion by implanted minipumps vs conventional injection regimen in the mouse. Toxicol Appl Pharmacol 1985;80:243-50
  • Ornoy A. Valproic acid in pregnancy: how much are we endangering the embryo and fetus? Reprod Toxicol 2009;28:1-10
  • Tiboni GM, Giampietro F. Murine teratology of fluconazole: evaluation of developmental phase specificity and dose dependence. Pediatr Res 2005;58:94-9
  • Tiboni GM, Marotta F, Del Corso A, Defining critical periods for itraconazole-induced cleft palate, limb defects and axial skeletal malformations in the mouse. Toxicol Lett 2006;167:8-18
  • Farag AT, Ibrahim HH. Developmental toxic effects of antifungal flusilazole administered by gavage to mice. Birth Defects Res B Dev Reprod Toxicol 2007;80:12-7
  • Amaral VCS, Nunes GP Jr. Ketoconazole-and Xuconazole-induced embryotoxicity and skeletal anomalies in Wistar rats: a comparative study. Braz Arch Biol Technol 2008;51:1153-61
  • Amaral VC, Nunes GP Jr. Prednisone reduces ketoconazole-induced skeletal defects in rat fetuses. Arch Toxicol 2009;83:863-71
  • Nishikawa S, Hara T, Miyazaki H, Reproduction studies of KW-1414 in rats and rabbits. Clin Rep 1984;18:1433-88
  • Machera K. Developmental toxicity of cyproconazole, an inhibitor of fungal ergosterol biosynthesis, in the rat. Bull Environ Contam Toxicol 1995;54:363-9
  • Menegola E, Di Renzo F, Broccia ML, Cleft palate and exposure to an azole derivative: triadimefon. Reprod Toxicol 2009;28:123
  • Menegola E, Broccia ML, Di Renzo F, 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 2004;18:121-30
  • Tiboni GM, Marotta F, Castigliego AP. Teratogenic effects in mouse fetuses subjected to the concurrent in utero exposure to miconazole and metronidazole. Reprod Toxicol 2008;26:254-61
  • Taxvig C, Vinggaard AM, Hass U, Endocrine-disrupting properties in vivo of widely used azole fungicides. Int J Androl 2008;31:170-7
  • Augustine-Rauch K. Alternative experimental approaches for interpreting skeletal findings in safety studies. Birth Defects Res B Dev Reprod Toxicol 2007;80:497-504
  • Flick B, Klug S. Whole embryo culture: an important tool in developmental toxicology today. Curr Pharm Des 2006;12:1467-88
  • Menegola E, Broccia ML, Di Renzo F, Dysmorphogenic effects of some fungicides derived from the imidazole on rat embryos cultured in vitro. Reprod Toxicol 2006;21:74-82
  • Tiboni GM. Second branchial arch anomalies induced by fluconazole, a bis-triazole antifungal agent, in cultured mouse embryos. Res Commun Chem Pathol Pharmacol 1993;79:381-4
  • Menegola E, Broccia ML, Di Renzo F, Antifungal triazoles induce malformations in vitro. Reprod Toxicol 2001;15:421-7
  • Menegola E, Broccia ML, Di Renzo F, Pathogenic pathways in fluconazole-induced branchial arch malformations. Birth Defects Res A Clin Mol Teratol 2003;67:116-24
  • Menegola E, Broccia ML, Di Renzo F, Study on the common teratogenic pathway elicited by the fungicides triazole-derivatives. Toxicol In Vitro 2005;19:737-48
  • Zega G, De Bernardi F, Groppelli S, Effects of the azole fungicide Imazalil on the development of the ascidian Ciona intestinalis (chordata, tunicata): morphological and molecular characterization of the induced phenotype. Aquat Toxicol 2009;91:255-61
  • Pennati R, Groppelli S, Zega G, Toxic effects of two pesticides, imazalil and triadimefon, on the early development of the ascidian Phallusia mammillata (chordata, ascidiacea). Aquat Toxicol 2006;79:205-12
  • Menegola E, Broccia ML, Di Renzo F, In vitro teratogenic potential of two antifungal triazoles: triadimefon and triadimenol. In Vitro Cell Dev Biol Anim 2000;36:88-95
  • Kaufman MH, Bard JBL. The anatomical basis of mouse development. Academic Press, San Diego; 1999
  • Groppelli S, Pennati R, De Bernardi F, Teratogenic effects of two antifungal triazoles, triadimefon and triadimenol, on Xenopus laevis development: craniofacial defects. Aquat Toxicol 2005;73:370-81
  • Nelson DR, Zeldin DC, Hoffman SM, Comparison of cytochrome P450 (CYP) genes from the mouse and human genomes, including nomenclature recommendations for genes, pseudogenes and alternative-splice variants. Pharmacogenetics 2004;14:1-18
  • Choudhary D, Jansson I, Stoilov I, Expression patterns of mouse and human CYP orthologs (families 1 – 4) during development and in different adult tissues. Arch Biochem Biophys 2005;436:50-61
  • Stoilov I. Cytochrome P450s: coupling development and environment. Trends Genet 2001;17:629-32
  • Libby RT, Kitamoto J, Holme RH, Cdh23 mutations in the mouse are associated with retinal dysfunction but not retinal degeneration. Exp Eye Res 2003;77:731-9
  • McCaffery P, Simons C. Prospective teratology of retinoic acid metabolic blocking agents (RAMBAs) and loss of CYP26 activity. Curr Pharm Des 2007;13:3020-37
  • Yaffe SJ, Rane A, Sjöqvist F, The presence of a monooxygenase system in human fetal liver microsomes. Life Sci II 1970;9:1189-200
  • Sun G, Thai SF, Lambert GR, Fluconazole-induced hepatic cytochrome P450 gene expression and enzymatic activities in rats and mice. Toxicol Lett 2006;164:44-53
  • Vinggaard AM, Hnida C, Breinholt V, Screening of selected pesticides for inhibition of CYP19 aromatase activity in vitro. Toxicol In Vitro 2004;14:227-34
  • Colburn DE, Giles FJ, Oladovich D, In vitro evaluation of cytochrome P450-mediated drug interactions between cytarabine, idarubicin, itraconazole and caspofungin. Hematology 2004;9:217-21
  • Venkatakrishnan K, von Moltke LL, Greenblatt DJ. Effects of the antifungal agents on oxidative drug metabolism: clinical relevance. Clin Pharmacokinet 2000;38:111-80
  • Niwa T, Shiraga T, Takagi A. Effect of antifungal drugs on cytochrome P450 (CYP) 2C9, CYP2C19, and CYP3A4 activities in human liver microsomes. Biol Pharm Bull 2005;28:1805-8
  • Gyllenhammar I, Eriksson H, Söderqvist A, Clotrimazole exposure modulates aromatase activity in gonads and brain during gonadal differentiation in Xenopus tropicalis frogs. Aquat Toxicol 2009;91:102-9
  • Engelhardt D, Weber MM, Miksch T, The influence of ketoconazole on human adrenal steroidogenesis: incubation studies with tissue slices. Clin Endocrinol (Oxf) 1991;35:163-8
  • AHFS, (American Hospital Formulary Service), Drug Information. American Society of Health-System Pharmacists, Bethesda MD; 1996
  • Iranmanesh A, Ovetsky RM, Lizarralde G, Effect of ketoconazole on the 11-hydroxylation step of adrenal steroidogenesis. South Med J 1987;80:725-8
  • Tiboni GM, Iammarrone E, Giampietro F, Teratological interaction between the bis-triazole antifungal agent fluconazole and the anticonvulsant drug phenytoin. Teratology 1999;59:81-7
  • Schwartz EL, Hallam S, Gallagher RE, Inhibition of all-trans-retinoic acid metabolism by fluconazole in vitro and in patients with acute promyelocytic leukemia. Biochem Pharmacol 1995;50:923-8
  • Vanier KL, Mattiussi AJ, Johnston DL. Interaction of all-trans-retinoic acid with fluconazole in acute promyelocytic leukemia. J Pediatr Hematol Oncol 2003;25:403-4
  • Kirby AJ, Le Lain R, Maharlouie F, Inhibition of retinoic acid metabolising enzymes by 2-(4-aminophenylmethyl)-6-hydroxy-3,4-dihydronaphthalen-1(2H)-one and related compounds. J Enzyme Inhib Med Chem 2003;18:27-33
  • Wouters W, van Dun J, Dillen A, Effects of liarozole, a new antitumoral compound, on retinoic acid-induced inhibition of cell growth and on retinoic acid metabolism in MCF-7 human breast cancer cells. Cancer Res 1992;52:2841-6
  • Pignatello MA, Kauffman FC, Levin AA. Liarozole markedly increases all trans-retinoic acid toxicity in mouse limb bud cell cultures: a model to explain the potency of the aromatic retinoid (E)-4-[2-(5,6,7,8-tetrahydro-5,5,8,8-tetramethyl-2-naphthylenyl)-1-propenyl] benzoic acid. Toxicol Appl Pharmacol 2002;178:186-94
  • Van Wauwe J, Van Nyen G, Coene MC, Liarozole, an inhibitor of retinoic acid metabolism, exerts retinoid-mimetic effects in vivo. J Pharmacol Exp Ther 1992;261:773-9
  • Van Heusden J, Van Ginckel R, Bruwiere H, Inhibition of all-trans-retinoic acid metabolism by R116010 induces antitumour activity. Br J Cancer 2002;86:605-11
  • Pavez Loriè E, Cools M, Borgers M, Topical treatment with CYP26 inhibitor talarozole (R115866) dose dependently alters the expression of retinoid-regulated genes in normal human epidermis. Br J Dermatol 2009;160:26-36
  • Campo-Paysaa F, Marlétaz F, Laudet V, Retinoic acid signaling in development: tissue-specific functions and evolutionary origins. Genesis 2008;46:640-56
  • White JC, Highland M, Kaiser M, Vitamin A deficiency results in the dose-dependent acquisition of anterior character and shortening of the caudal hindbrain of the rat embryo. Dev Biol 2000;220:263-84
  • Niederreither K, Vermot J, Schuhbaur B, Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development 2000;127:75-85
  • Morriss-Kay GM, Murphy P, Hill RE, 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 1991;10:2985-95
  • Armstrong RB, Kim HJ, Grippo JF, Levin AA. Retinoids for the future: investigational approaches for the identification of new compounds. J Am Acad Dermatol 1992;27:S38-42
  • Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J 1996;10:940-54
  • Niederreither K, Vermot J, Fraulob V, Retinaldehyde dehydrogenase 2 (RALDH2)- independent patterns of retinoic acid synthesis in the mouse embryo. Proc Natl Acad Sci USA 2002;99:16111-6
  • Abu-Abed SS, Beckett BR, Chiba H, Mouse P450RAI (CYP26) expression and retinoic acid-inducible retinoic acid metabolism in F9 cells are regulated by retinoic acid receptor gamma and retinoid X receptor alpha. J Biol Chem 1998;273:2409-15
  • MacLean G, Abu-Abed S, Dollé P, Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech Dev 2001;107:195-201
  • Reijntjes S, Blentic A, Gale E, The control of morphogen signalling: regulation of the synthesis and catabolism of retinoic acid in the developing embryo. Dev Biol 2005;285:224-37
  • Wang Y, Zolfaghari R, Ross AC. Cloning of rat cytochrome P450RAI (CYP26) cDNA and regulation of its gene expression by all-trans-retinoic acid in vivo. Arch Biochem Biophys 2002;401:235-43
  • Tahayato A, Dollé P, Petkovich M. Cyp26C1 encodes a novel retinoic acid-metabolizing enzyme expressed in the hindbrain, inner ear, first branchial arch and tooth buds during murine development. Gene Expr Patterns 2003;3:449-54
  • Reijntjes S, Gale E, Maden M. Expression of the retinoic acid catabolising enzyme CYP26B1 in the chick embryo and its regulation by retinoic acid. Gene Expr Patterns 2003;3:621-7
  • Reijntjes S, Gale E, Maden M. Generating gradients of retinoic acid in the chick embryo: Cyp26C1 expression and a comparative analysis of the Cyp26 enzymes. Dev Dyn 2004;230:509-17
  • de Roos K, Sonneveld E, Compaan B, Expression of retinoic acid 4-hydroxylase (CYP26) during mouse and Xenopus laevis embryogenesis. Mech Dev 1999;82:205-11
  • Emoto Y, Wada H, Okamoto H, Retinoic acid-metabolizing enzyme Cyp26a1 is essential for determining territories of hindbrain and spinal cord in zebrafish. Dev Biol 2005;278:415-27
  • Cañestro C, Postlethwait JH, Gonzàlez-Duarte R, Is retinoic acid genetic machinery a chordate innovation? Evol Dev 2006;8:394-406
  • Abu-Abed S, MacLean G, Fraulob V, Differential expression of the retinoic acid-metabolizing enzymes CYP26A1 and CYP26B1 during murine organogenesis. Mech Dev 2002;110:173-7
  • Uehara M, Yashiro K, Mamiya S, CYP26A1 and CYP26C1 cooperatively regulate anterior-posterior patterning of the developing brain and the production of migratory cranial neural crest cells in the mouse. Dev Biol 2007;302:399-411
  • Santner SJ, Pauley RJ, Tait L, Aromatase activity and expression in breast cancer and benign breast tissue stromal cells. J Clin Endocrinol Metab 1997;82:200-8
  • Buzdar AU, Robertson JF, Eiermann W, An overview of the pharmacology and pharmacokinetics of the newer generation aromatase inhibitors anastrozole, letrozole, and exemestane. Cancer 2002;95:2006-16
  • Tiboni GM, Marotta F, Carletti E. Fluconazole alters CYP26 gene expression in mouse embryos. Reprod Toxicol 2009;27:199-202
  • Klug S, Lewandowski C, Wildi L, All-trans retinoic acid and 13-cis-retinoic acid in the rat whole-embryo culture: abnormal development due to the all-trans isomer. Arch Toxicol 1989;63:440-4
  • Di Renzo F, Broccia ML, Giavini 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 2007;24:326-32
  • Yamamoto Y, Zolfaghari R, Ross AC. Regulation of CYP26 (cytochrome P450RAI) mRNA expression and retinoic acid metabolism by retinoids and dietary vitamin A in liver of mice and rats. FASEB J 2000;14:2119-27
  • White RJ, Schilling TF. How degrading: Cyp26s in hindbrain development. Dev Dyn 2008;237:2775-90
  • Dobbs-McAuliffe B, Zhao Q, Linney E. Feedback mechanisms regulate retinoic acid production and degradation in the zebrafish embryo. Mech Dev 2004;121:339-50
  • White RJ, Nie Q, Lander AD, Complex regulation of cyp26a1 creates a robust retinoic acid gradient in the zebrafish embryo. PLoS Biol 2007;5:e304
  • Serpente P, Tümpel S, Ghyselinck NB, Direct crossregulation between retinoic acid receptor {beta} and Hox genes during hindbrain segmentation. Development 2005;132:503-13
  • Taimi M, Helvig C, Wisniewski J, A novel human cytochrome P450, CYP26C1, involved in metabolism of 9-cis and all-trans isomers of retinoic acid. J Biol Chem 2004;279:77-85
  • Papis E, Bernardini G, Gornati R, Gene expression in Xenopus laevis embryos after triadimefon exposure. Gene Expr Patterns 2007;7:137-42
  • Chai Y, Ito Y, Han J. TGF-beta signaling and its functional significance in regulating the fate of cranial neural crest cells. Crit Rev Oral Biol Med. 2003;14:78-88
  • Colakoglu N, Kukner A, Oner J, Effects of high dose retinoic acid on TGF-beta2 expression during pancreatic organogenesis. J Mol Histol 2005;36:413-8
  • Di Renzo F, Corsini E, Broccia ML, Molecular mechanism of teratogenic effects induced by the fungicide triadimefon: study of the expression of TGF-beta mRNA and TGF-beta and CRABPI proteins during rat in vitro development. Toxicol Appl Pharmacol 2009;234:107-16
  • Chen F, Desai TJ, Qian J, Inhibition of Tgf beta signaling by endogenous retinoic acid is essential for primary lung bud induction. Development 2007;134:2969-79
  • Massa V, Gaudenzi G, Sangiorgio L, Krox20 is down-regulated following triazole in vitro embryonic exposure: a polycompetitor-based assay. Toxicol Lett 2007;169:196-204
  • De S, Turman JE Jr. Krox-20 gene expression: influencing hindbrain-craniofacial developmental interactions. Arch Histol Cytol 2005;68:227-34
  • Borday C, Chatonnet F, Thoby-Brisson M, Neural tube patterning by Krox20 and emergence of a respiratory control. Respir Physiol Neurobiol 2005;149:63-72
  • Warner LE, Mancias P, Butler IJ, Mutations in the early growth response 2 (EGR2) gene are associated with hereditary myelinopathies. Nat Genet 1998;18:382-4
  • Chun K, Siegel-Bartelt J, Chitayat D, FGFR2 mutation associated with clinical manifestations consistent with Antley-Bixler syndrome. Am J Med Genet 1998;77:219-24
  • Reardon W. Craniosynostosis. Diagnosis, evaluation and management. J Med Genet 2000;37:727
  • Adachi M, Asakura Y, Tachibana K, Abnormal steroidogenesis in three patients with Antley-Bixler syndrome: apparent decreased activity of 17alpha-hydroxylase, 17,20-lyase and 21-hydroxylase. Pediatr Int 2004;46:583-9
  • Flück CE, Tajima T, Pandey AV, Mutant P450 oxidoreductase causes disordered steroidogenesis with and without Antley-Bixler syndrome. Nat Genet 2004;36:228-30
  • Aleck KA, Bartley DL. Multiple malformation syndrome following fluconazole use in pregnancy: report of an additional patient. Am J Med Genet 1997;72:253-6
  • Csapo A, Dray F, Erdos T. Letter: oestradiol 17beta: inhibitor of placental growth. Lancet 1974;6:51-2
  • Furukawa S, Hayashi S, Usuda K, Histopathological effect of ketoconazole on rat placenta. Vet Med Sci 2008;70:1179-84
  • Pasanen M, Pellinen P, Stenbäck F, The role of CYP enzymes in cocaine-induced liver damage. Arch Toxicol 1995;69:287-90
  • Tiboni GM, Marotta F, Castigliego AP, Impact of estrogen replacement on letrozole-induced embryopathic effects. Hum Reprod 2009;24(11):2688-92

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