Interactive effects of cadmium and all-Trans-retinoic acid on the induction of forelimb ectrodactyly in C57BL/6 mice

Birth Defects Research Part A - Clinical and Molecular Teratology

Volumn 76, Issue 1, 2006, Pages 19-28

  Lee, Grace S ^a,c   Liao, Xiaoyan ^a   Cantor, Rita M ^b   Collins, Michael D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Cadmium; Ectrodactyly; Interactive effect; Limb malformation; Mice; Retinoic acid; Subthreshold; Teratogenicity

Indexed keywords

ACETAZOLAMIDE; ALCOHOL; CADMIUM; CADMIUM CHLORIDE; DIMETHADIONE; ISOTRETINOIN; PHENYTOIN; RETINOIC ACID; VALPROIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; ECTRODACTYLY; EMBRYO DEVELOPMENT; EMBRYOTOXICITY; FETUS; FORELIMB; LIMB DEVELOPMENT; MAXIMUM TOLERATED DOSE; MOUSE; NONHUMAN; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; SKELETON MALFORMATION; TERATOGENICITY; TOXICOLOGY;

ANIMALS; CADMIUM; DRUG INTERACTIONS; DRUG SYNERGISM; FEMALE; FORELIMB; GESTATIONAL AGE; INJECTIONS, INTRAPERITONEAL; MICE; MICE, INBRED C57BL; PREGNANCY; TERATOGENS; TRETINOIN;

ANIMALIA;

EID: 32444444859     PISSN: 15420752     EISSN: None     Source Type: Journal    
DOI: 10.1002/bdra.20201     Document Type: Article

References (105)

1. Alfven T, Elinder CG, Carlsson MD, et al. 2000. Low-level cadmium exposure and osteoporosis. J Bone Miner Res 15:1579-1586.
2. Alsayed Y, Uddin S, Mahmud N, et al. 2001. Activation of Rac1 and the p38 mitogen-activated protein kinase pathway in response to all-trans-retinoic acid. J Biol Chem 276:4012-4019.
3. Balmer JE, Blomhoff R. 2002. Gene expression regulation by retinoic acid. J Lipid Res 43:1773-1808.
4. Bartosiewicz M, Penn S, Buckpitt A. 2001. Applications of gene arrays in environmental toxicology: fingerprints of gene regulation associated with cadmium chloride, benzo(a)pyrene, and trichloroethylene. Environ Health Perspect 109:71-74.
5. Beamer WG, Donahue LR, Rosen CJ, Baylink DJ. 1996. Genetic variability in adult bone density among inbred strains of mice. Bone 18:397-403.
6. Beyersmann D, Hechtenberg S. 1997. Cadmium, gene regulation, and cellular signalling in mammalian cells. Toxicol Appl Pharmacol 144:247-261.
7. Bhasin N, Kernick E, Luo X, et al. 2004. Differential regulation of chondrogenic differentiation by the serotonin2B receptor and retinoic acid in the embryonic mouse hindlimb. Dev Dyn 230:201-209.
8. Binkley N, Krueger D. 2000. Hypervitaminosis A and bone. Nutr Rev 58:138-144.
9. Bohne M, Struy H, Gerber A, Gollnick H. 1997. Effects of retinoids on the generation of neutrophil-derived reactive oxygen species studied by EPR spin trapping techniques. Inflamm Res 46:423-424.
10. Brent RL. 2001. Addressing environmentally caused human birth defects. Pediatr Rev 22:153-165.
11. Brown PD, Benya PD. 1988. Alterations in chondrocyte cytoskeletal architecture during phenotypic modulation by retinoic acid and dihydrocytochalasin B-induced reexpression. J Cell Biol 106:171-179.
12. Brzoska MM, Moniuszko-Jakoniuk J. 2005. Effect of low-level lifetime exposure to cadmium on calciotropic hormones in aged female rats. Arch Toxicol. Epublished June 7, 2005.
13. Canon E, Cosgaya JM, Scsucova S, Aranda A. 2004. Rapid effects of retinoic acid on CREB and ERK phosphorylation in neuronal cells. Mol Biol Cell 15:5583-5592.
14. Cassee FR, Groten JP, van Bladeren PJ, Feron VJ. 1998. Toxicological evaluation and risk assessment of chemical mixtures. Crit Rev Toxicol 28:73-101.
15. Cho SH, Oh CD, Kim SJ, et al. 2003. Retinoic acid inhibits chondrogenesis of mesenchymal cells by sustaining expression of N-cadherin and its associated proteins. J Cell Biochem 89:837-847.
16. Cohen-Tanugi A, Forest N. 1998. Retinoic acid suppresses the osteogenic differentiation capacity of murine osteoblast-like 3/A/1D-1M cell cultures. Differentiation 63:115-123.
17. Collins MD, Eckhoff Ch., Weiss R, Resnick E, Nau H, and Scott WJ Jr. (in press) Differential teratogenesis of all-trans-retinoic acid in SWV and C57BL/6N mice administered at gestational day 9.5: emphasis on limb dysmorphology. Birth Defects Res A Clin Mol Teratol.
18. Collins MD, Walling KM, Resnick E, Scott WJ Jr. 1991. The effect of administration time on malformations induced by three anticonvulsant agents in C57BL/6J mice with emphasis on forelimb ectrodactyly. Teratology 44:617-627.
19. Collins MD, Mao GE. 1999. Teratology of retinoids. Annu Rev Pharmacol Toxicol 39:399-430.
20. Commission of the European Communities. 1978. Criteria (dose/effect relationships) for cadmium. Oxford: Pergamon Press. pp. 1-12.
21. Cowan CM, Aalami OO, Shi YY, et al. 2005. Bone morphogenetic protein 2 and retinoic acid accelerate in vivo bone formation, osteoclast recruitment, and bone turnover. Tissue Eng 11:645-658.
22. Dal-Pizzol F, Klamt F, Benfato MS, et al. 2001. Retinol supplementation induces oxidative stress and modulates antioxidant enzyme activities in rat sertoli cells. Free Radic Res 34:395-404.
23. Ding W, Templeton DM. 2000. Activation of parallel mitogen-activated protein kinase cascades and induction of c-fos by cadmium. Toxicol Appl Pharmacol 162:93-99.
24. Evrard L, Vanmuylder N, Dourov N, et al. 2000. Correlation of HSP110 expression with all-trans retinoic acid-induced apoptosis. J Craniofac Genet Dev Biol 20:183-192.
25. Friberg L, Elinder CG, Kjellstrom T, Nordberg GF. 1986. Cadmium and health: a toxicolgoical and epidemiological approach. Boca Raton: CRC Press. pp. 111-158.
26. Gennari A, Cortese E, Boveri M, et al. 2003. Sensitive endpoints for evaluating cadmium-induced acute toxicity in LLC-PK1 cells. Toxicology 183:211-220.
27. Guicheux J, Lemonnier J, Ghayor C, et al. 2003. Activation of p38 mitogen-activated protein kinase and c-Jun-NH2-terminal kinase by BMP-2 and their implication in the stimulation of osteoblastic cell differentiation. J Bone Miner Res 18:2060-2068.
28. Haghdoost NR, Newman LM, Johnson EM. 1997. Multiple chemical exposures: synergism vs. individual exposure levels. Reprod Toxicol 11:9-27.
29. Hansen DK, La Borde JB, Wall KS, et al. 2001. Dose-response of retinoic acid induced stress protein synthesis and teratogenesis in mice. Reprod Toxicol 15:31-41.
30. Hathcock JN. 2002. Does high intake of vitamin A pose a risk for osteoporotic fracture? JAMA 287:1396-1397.
31. Heegaard AM, Xie Z, Young MF, Nielsen KL. 2004. Transforming growth factor beta stimulation of biglycan gene expression is potentially mediated by sp1 binding factors. J Cell Biochem 93:463-475.
32. Heller LC, Li Y, Abrams KL, Rogers MB. 1999. Transcriptional regulation of the Bmp2 gene. Retinoic acid induction in F9 embryonal carcinoma cells and Saccharomyces cerevisiae. J Biol Chem 274:1394-1400.
33. Helvering LM, Sharp RL, Ou X, Geiser AG. 2000. Regulation of the promoters for the human bone morphogenetic protein 2 and 4 genes. Gene 256:123-138.
34. Hoffman LM, Weston AD, Underhill TM. 2003. Molecular mechanisms regulating chondroblast differentiation. J Bone Joint Surg Am 85-A Suppl 2:124-132.
35. Honda R, Tsuritani I, Noborisaka Y, et al. 2003. Urinary cadmium excretion is correlated with calcaneal bone mass in Japanese women living in an urban area. Environ Res 91:63-70.
36. Hovland DN Jr, Cantor RM, Lee GS, et al. 2000. Identification of a murine locus conveying susceptibility to cadmium-induced forelimb malformations. Genomics 63:193-201.
37. Hurnanen D, Chan HM, Kubow S. 1997. The protective effect of metallothionein against lipid peroxidation caused by retinoic acid in human breast cancer cells. J Pharmacol Exp Ther 283:1520-1528.
38. Iba K, Chiba H, Yamashita T, et al. 2001. Phase-independent inhibition by retinoic acid of mineralization correlated with loss of tetranectin expression in a human osteoblastic cell line. Cell Struct Funct 26:227-233.
39. Inouye M. 1976. Differential staining of cartilage and bone in fetal mouse skeleton by alcian blue and alizarin red. S Cong Anom 16:171-173.
40. Jarup L, Berglund M, Elinder CG, et al. 1998. Health effects of cadmium exposure-a review of the literature and a risk estimate. Scand J Work Environ Health 24(Suppl 1):1-51.
41. Jimenez MJ, Balbin M, Alvarez J, et al. 2001. A regulatory cascade involving retinoic acid, Cbfa1, and matrix metalloproteinases is coupled to the development of a process of perichondrial invasion and osteogenic differentiation during bone formation. J Cell Biol 155:1333-1344.
42. Johnson MD, Kenney N, Stoica A, et al. 2003. Cadmium mimics the in vivo effects of estrogen in the uterus and mammary gland. Nat Med 9:1081-1084.
43. Kato K, Ito H, Iwamoto I, et al. 2001. Protein kinase inhibitors can suppress stress-induced dissociation of Hsp27. Cell Stress Chaperones 6:16-20.
44. Kawamura J, Yoshida O, Nishino K, Itokawa Y. 1978. Disturbances in kidney functions and calcium and phosphate metabolism in cadmium-poisoned rats. Nephron 20:101-110.
45. Kim SD, Moon CK, Eun SY, et al. 2005. Identification of ASK1, MKK4, JNK, c-Jun, and caspase-3 as a signaling cascade involved in cadmium-induced neuronal cell apoptosis. Biochem Biophys Res Commun 328: 326-334.
46. Kimmel CA, Trammell C. 1981. A rapid procedure for routine double staining of cartilage and bone in fetal and adult animals. Stain Technol 56:271-273.
47. Kitching R, Qi S, Li V, et al. 2002. Coordinate gene expression patterns during osteoblast maturation and retinoic acid treatment of MC3T3-E1 cells. J Bone Miner Metab 20:269-280.
48. Kjellstrom T. 1992. Mechanism and epidemiology of bone effects of cadmium. IARC Sci Publ 118:301-310.
49. Kneissel M, Studer A, Cortesi R, Susa M. 2005. Retinoid-induced bone thinning is caused by subperiosteal osteoclast activity in adult rodents. Bone 36:202-214.
50. Kuczuk MH, Scott WJ Jr. 1984. Potentiation of acetazolamide induced ectrodactyly in SWV and C57BL/6J mice by cadmium sulfate. Teratology 29:427-435.
51. Launay S, Gianni M, Diomede L, et al. 2003. Enhancement of ATRA-induced cell differentiation by inhibition of calcium accumulation into the endoplasmic reticulum: cross-talk between RAR alpha and calcium-dependent signaling. Blood 101:3220-3228.
52. Layton WM Jr, Hallesy DW. 1965. Deformity of forelimb in rats: association with high doses of acetazolamide Science 149:306-308.
53. Layton WM Jr, Layton MW. 1979. Cadmium induced limb defects in mice: strain associated differences in sensitivity. Teratology 19:229-235.
54. Lee GS, Cantor RM, Abnoosian A, et al. 2005. A gene(s) for all-trans-retinoic acid-induced forelimb defects mapped and confirmed to murine chromosome 11. Genetics 170:345-353.
55. Lemarie A, Lagadic-Gossmann D, Morzadec C, et al. 2004. Cadmium induces caspase-independent apoptosis in liver Hep3B cells: role for calcium in signaling oxidative stress-related impairment of mitochondria and relocation of endonuclease G and apoptosis-inducing factor. Free Radic Biol Med 36:1517-1531.
56. Li J, Molkentin JD, Colbert MC. 2001. Retinoic acid inhibits cardiac neural crest migration by blocking c-Jun N-terminal kinase activation. Dev Biol 232:351-361.
57. Lian K, Zmuda JM, Nevitt MC, et al. 2005. Type I collagen alpha1 Sp1 transcription factor binding site polymorphism is associated with reduced risk of hip osteoarthritis defined by severe joint space narrowing in elderly women. Arthritis Rheum 52:1431-1436.
58. Liu PY, Lu Y, Long JR, et al. 2004. Common variants at the PCOL2 and Sp1 binding sites of the COL1A1 gene and their interactive effect influence bone mineral density in Caucasians. J Med Genet 41:752-757.
59. Mehta K. 2003. Retinoids as regulators of gene transcription. J Biol Regul Homeost Agents 17:1-12.
60. Miguel BG, Rodriguez ME, Aller P, et al. 2005. Regulation of cadmium-induced apoptosis by PKCdelta in U937 human promonocytic cells. Biochim Biophys Acta 1743:215-222.
61. Murata M, Kawanishi S. 2000. Oxidative DNA damage by vitamin A and its derivative via superoxide generation. J Biol Chem 275:2003-2008.
62. Nagy L, Thomazy VA, Heyman RA, Davies PJ. 1998. Retinoid-induced apoptosis in normal and neoplastic tissues. Cell Death Differ 5:11-19.
63. Nelson BK. 1994. Interactions in developmental toxicology: a literature-review and terminology proposal. Teratology 49:33-71.
64. Nishijo M, Nakagawa H, Honda R, et al. 2002. Effects of maternal exposure to cadmium on pregnancy outcome and breast milk. Occup Environ Med 59:394-396; discussion 397.
65. Nordberg G, Jin T, Bernard A, et al. 2002. Low bone density and renal dysfunction following environmental cadmium exposure in China. Ambio 31:478-481.
66. Ogston N, Harrison AJ, Cheung HF, et al. 2002. Dexamethasone and retinoic acid differentially regulate growth and differentiation in an immortalised human clonal bone marrow stromal cell line with osteoblastic characteristics. Steroids 67:895-906.
67. Prozialeck WC, Grunwald GB, Dey PM, et al. 2002. Cadherins and NCAM as potential targets in metal toxicity. Toxicol Appl Pharmacol 182:255-265.
68. Qu W, Liu J, Fuquay R, et al. 2005. The nitric oxide prodrug, V-PYRRO/NO, protects against cadmium toxicity and apoptosis at the cellular level. Nitric Oxide 12:114-120.
69. Raouf A, Li V, Kola I, et al. 2000. The Ets1 proto-oncogene is upregulated by retinoic acid: characterization of a functional retinoic acid response element in the Ets1 promoter. Oncogene 19:1969-1974.
70. Regunathan A, Glesne DA, Wilson AK, et al. 2003. Microarray analysis of changes in bone cell gene expression early after cadmium gavage in mice. Toxicol Appl Pharmacol 191:272-293.
71. Ritchie HE, Brown-Woodman PD, Korabelnikoff A. 2003. Effect of co-administration of retinoids on rat embryo development in vitro. Birth Defects Res Part A Clin Mol Teratol 67:444-451.
72. Rohde CM, DeLuca H. 2003. Bone resorption activity of all-trans retinoic acid is independent of vitamin D in rats. J Nutr 133:777-783.
73. Ross SA, McCaffery PJ, Drager UC, De Luca LM. 2000. Retinoids in embryonal development. Physiol Rev 80:1021-1054.
74. Sacco-Gibson N, Chaudhry S, Brock A, et al. 1992. Cadmium effects on bone metabolism: accelerated resorption in ovariectomized, aged beagles. Toxicol Appl Pharmacol 113:274-283.
75. Sakurai A, Nishimoto M, Himeno S, et al. 2005. Transcriptional regulation of thioredoxin reductase 1 expression by cadmium in vascular endothelial cells: role of NF-E2-related factor-2. J Cell Physiol 203:529-537.
76. Saneshige S, Mano H, Tezuka K, et al. 1995. Retinoic acid directly stimulates osteoclastic bone resorption and gene expression of cathepsin K/OC-2. Biochem J 309(Pt 3):721-724.
77. Sauer JM, Waalkes MP, Hooser SB, et al. 1997. Tolerance induced by all-trans-retinol to the hepatotoxic effects of cadmium in rats: role of metallothionein expression. Toxicol Appl Pharmacol 143:110-119.
78. Sen Gupta R, Sen Gupta E, Dhakal BK, et al. 2004. Vitamin C and vitamin E protect the rat testes from cadmium-induced reactive oxygen species. Mol Cells 17:132-139.
79. Shenefelt RE. 1972. Morphogenesis of malformations in hamsters caused by retinoic acid: relation to dose and stage at treatment. Teratology 5:103-118.
80. Shimo T, Koyama E, Sugito H, et al. 2005. Retinoid signaling regulates CTGF expression in hypertrophic chondrocytes with differential involvement of MAP kinases. J Bone Miner Res 20:867-877.
81. Shiota K, Shionoya Y, Ide M, Uenobe F, Kuwahara C, and Fukui Y. 1988. Teratogenic interaction of ethanol and hyperthermia in mice. Proc Soc Exp Biol Med 187:142-148.
82. Shury T, Rousseaux CG, Keiner J, Politis M. 1994. Interactive effects of cadmium and retinoic acid on mouse limb bud development in vitro. Bull Environ Contam Toxicol 53:570-576.
83. Son MH, Kang KW, Lee CH, Kim SG. 2001. Potentiation of cadmium-induced cytotoxicity by sulfur amino acid deprivation through activation of extracellular signal-regulated kinase1/2 (ERK1/2) in conjunction with p38 kinase or c-jun N-terminal kinase (JNK). Complete inhibition of the potentiated toxicity by U0126 an ERK1/2 and p38 kinase inhibitor. Biochem Pharmacol 62:1379-1390.
84. Soprano DR, Soprano KJ. 1995. Retinoids as teratogens. Annu Rev Nutr 15:111-132.
85. Sporn MB, Roberts AB, Goodman DS. 1994. The retinoids. New York: Raven Press.
86. Staessen JA, Roels HA, Emelianov D, et al. 1999. Environmental exposure to cadmium, forearm bone density, and risk of fractures: prospective population study. Public Health and Environmental Exposure to Cadmium (PheeCad) Study Group. Lancet 353:1140-1144.
87. Stewart D, Killeen E, Naquin R, et al. 2003. Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J Biol Chem 278:2396-2402.
88. Sulik KK, Dehart DB. 1988. Retinoic-acid-induced limb malformations resulting from apical ectodermal ridge cell death. Teratology 37:527-537.
89. Tabatabai NM, Blumenthal SS, Petering DH. 2005. Adverse effect of cadmium on binding of transcription factor Sp1 to the GC-rich regions of the mouse sodium-glucose cotransporter 1, SGLT1, promoter. Toxicology 207:369-382.
90. Tsuchiya K. 1976. Epidemiological studies on cadmium in the environment in Japan: etiology of itai-itai disease. Fed Proc 35:2412-2418.
91. Villarroya F, Iglesias R, Giralt M. 2004. Retinoids and retinoid receptors in the control of energy balance: novel pharmacological strategies in obesity and diabetes. Curr Med Chem 11:795-805.
92. Waalkes MP. 2000. Cadmium carcinogenesis in review. J Inorg Biochem 79:241-244.
93. Wang C, Bhattacharyya MH. 1993. Effect of cadmium on bone calcium and 45Ca in nonpregnant mice on a calcium-deficient diet: evidence of direct effect of cadmium on bone. Toxicol Appl Pharmacol 120: 228-239.
94. Wang H, Zhu G, Shi Y, et al. 2003. Influence of environmental cadmium exposure on forearm bone density. J Bone Miner Res 18:553-560.
95. Wang Z, Templeton DM. 1996. Cellular factors mediate cadmium-dependent actin depolymerization. Toxicol Appl Pharmacol 139:115-121.
96. Wang Z, Templeton DM. 1998. Induction of c-fos proto-oncogene in mesangial cells by cadmium. J Biol Chem 273:73-79.
97. Weaver TE, Scott WJ Jr. 1984. Acetazolamide teratogenesis: association of maternal respiratory acidosis and ectrodactyly in C57BL/6J mice. Teratology 30:187-193.
98. Webster WS, Walsh DA, McEwen SE, Lipson AH. 1983. Some teratogenic properties of ethanol and acetaldehyde in C57BL/6J mice: implications for the study of the fetal alcohol syndrome. Teratology 27:231-243.
99. Webster W. 1990. The teratololgy and developmental toxicity of cadmium. New York: Plenum Press. p 255-282.
100. Weston AD, Chandraratna RA, Torchia J, Underhill TM. 2002. Requirement for RAR-mediated gene repression in skeletal progenitor differentiation. J Cell Biol 158:39-51.
101. Wilson JG, Jordan RL, Schumacher H. 1969. Potentiation of the teratogenic effects of 5-fluorouracil by natural pyrimidines. I. Biological aspects. Teratology 2:91-97.
102. Wilson JG. 1973. Environment and birth defects. New York: Academic Press, Inc. pp. 23-26 and pp. 102-103.
103. Wong CH, Mruk DD, Lui WY, Cheng CY. 2004. Regulation of blood-testis barrier dynamics: an in vivo study. J Cell Sci 117(Pt 5):783-798.
104. Yang MS, Yu LC, Gupta RC. 2004. Analysis of changes in energy and redox states in HepG2 hepatoma and C6 glioma cells upon exposure to cadmium. Toxicology 201:105-113.
105. Youn CK, Kim SH, Lee DY, et al. 2005. Cadmium down-regulates hOGG1 through suppression of Sp1 activity. J Biol Chem 208:25185-25195.