Maternal exposure to cadmium during gestation perturbs the vascular system of the adult rat offspring

Toxicology and Applied Pharmacology

Volumn 251, Issue 2, 2011, Pages 137-145

  Ronco, Ana Maria ^a   Montenegro, Marcela ^a   Castillo, Paula ^a   Urrutia, Manuel ^a   Saez, Daniel ^a   Hirsch, Sandra ^a   Zepeda, Ramiro ^b   Llanos, Miguel N ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

Author keywords

Cadmium; Developmental programming of cardiovascular system; Endothelial vascular reactivity; HO 1; NF B; VCAM 1

Indexed keywords

CADMIUM; CIGARETTE SMOKE; HEME OXYGENASE 1; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; ARTICLE; BLOOD VESSEL REACTIVITY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR SYSTEM; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENVIRONMENTAL EXPOSURE; FEMALE; HEART LEFT VENTRICLE HYPERTROPHY; NONHUMAN; PREGNANCY; PROGENY; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE;

ANIMALS; ANIMALS, NEWBORN; AORTA, THORACIC; CADMIUM; FEMALE; MALE; MATERNAL EXPOSURE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; VASOMOTOR SYSTEM;

RATTUS;

EID: 79851516019     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.01.001     Document Type: Article

References (64)

1. Barker D.J., Eriksson J.G., Forsen T., Osmond C. Fetal origins of adult disease: strength of effects and biological basis. Int. J. Epidemiol. 2002, 31:1235-1239.
2. Bateson P., Barker D., Clutton-Brock T., Deb D., D'Udine B., Foley R.A., Gluckman P., Godfrey K., Kirkwood T., Lahr M.M., McNamara J., Metcalfe N.B., Monaghan P., Spencer H.G., Sultan S.E. Developmental plasticity and human health. Nature 2004, 430:419-421.
3. Bhattacharyya M.H., Wilson A.K., Rajan S.S., Jonah M. Biochemical pathways in cadmium toxicity. Molecular Biology and Toxicology of Metals 2000, 1-74. Taylor and Francis, London. R.K. Zalup, J. Joropatnick (Eds.).
4. Chen Y.S., Zhu X., Zhao X., Xing H., Li Y. Hemin, a heme oxygenase-1 inducer, improves aortic endothelial dysfunction in insulin resistant rats. Chin. Med. J. 2008, 112:241-247.
5. Cuypers A., Plusquin M., Remans T., Jozefczak M., Keunen E., Gielen H., Opdenakker K., Nair A.R., Munters E., Artois T.J., Nawrot T., Vangronsveld J., Smeets K. Cadmium stress: an oxidative challenge. Biometals 2010, 23:927-940. 10.1007/s10534-010-9329-x.
6. Eneman J.D., Potts R.J., Osier M., Shukla G.S., Lee C.H., Chin J.F. Suppressed oxidant induced apoptosis in cadmium adapted alveolar epithelial cells and its potential involvement in cadmium carcinogenesis. Toxicology 2000, 147:215-228.
7. Favatier F., Polla B.S. Tobacco-smoke-inducible human haem oxygenase-1 gene expression: role of distinct transcription factors and reactive oxygen intermediates. Biochem. J. 2001, 353:475-482.
8. Gallagher C.M., Meliker J.R. Blood and urine cadmium, blood pressure, and hypertension: a systematic review and meta-analysis. Environ. Health Perspect. 2010, 118:1676-1684. (available at http://dx.doi.org/. 10.1289/ehp.1002077.
9. Galley H.F., Webster N.R. Physiology of the endothelium. Br. J. Anaesth. 2004, 93:105-113.
10. Galli C., Risé P. Fish consumption, omega 3 fatty acids and cardiovascular disease. The science and the clinical trials. Nutr. Health 2009, 20:11-20.
11. Gluckman P.D., Hanson M.A., Beedle A.S. Early events and their consequences for later diseases: a life history and evolutionary perspective. Am. J. Hum. Biol. 2007, 19:1-19.
12. Göcmen C., Kumcu E.K., Seçilmiş A., Uçar P., Dikmen A., Baysal F. Restorative effects of zinc and selenium on nitrergic relaxations impaired by cadmium in the mouse corpus cavernosum. Toxicol. Lett. 2000, 111:229-234.
13. Hawkins P., Steyn C., Ozaki T., Saito T., Noakes D.E., Hanson M.A. Effect of maternal undernutrition in early gestation on ovine fetal blood pressure and cardiovascular reflexes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2000, 279:340-348.
14. Henson M.C., Chedrese P.J. Endocrine disruption by cadmium, a common environmental toxicant with paradoxical effects on reproduction. Exp. Biol. Med. 2004, 229:383-392.
15. Hill-Kapturczak N., Sikorski E., Voakes C., Garcia J., Nick H.S., Agarwal A. An internal enhancer regulates heme- and cadmium-mediated induction of human heme oxygenase-1. Am. J. Physiol. Renal. Physiol. 2003, 285:F515-F523.
16. Hoet J.J., Hanson M.A. Intrauterine nutrition: its importance during critical periods for cardiovascular and endocrine development. J. Physiol. Lond. 1999, 514:617-627.
17. Immenschuh S., Schröder H. Heme oxygenase-1 and cardiovascular disease. Histol. Histopathol. 2006, 21:679-685.
18. Isobe N., Taniguchi K., Oshima S., Ono Z., Adachi H., Toyama T., Naito S., Hoshizaki H., Kamiyama H. Candesartan cilexetil improves left ventricular function, left ventricular hypertrophy, and endothelial function in patients with hypertensive heart disease. Circ. J. 2002, 66:993-999.
19. Jaddoe V.W.V., de Ridder M.A.J., van den Elzen A.P.M., Hofmana A., Cuno, Uiterwaal C.S.P.M., Witteman J.C.M. Maternal smoking in pregnancy is associated with cholesterol development in the offspring: a 27-years follow-up study. Atherosclerosis 2008, 196:42-48.
20. Juric D., Wojciechowski P., Das D.K., Netticadan T. Prevention of concentric hypertrophy and diastolic impairment in aortic-banded rats treated with resveratrol. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H2138-H2143.
21. Kayali R., Cakatay U., Tekeli F. Male rats exhibit higher oxidative protein damage than females of the same chronological age. Mech. Ageing Dev. 2007, 128:365-369.
22. Kippler M., Lönnerdal B., Goessler W., Ekström E.C., Arifeen S.E., Vahter M. Cadmium interacts with the transport of essential micronutrients in the mammary gland-a study in rural Bangladeshi women. Toxicology 2009, 257:64-69.
23. Kolluru G.K., Tamilarasan K.P., Priya S.G., Durgha N.P., Chatterjee S. Consequence of defective migratory pattern of endothelial cells in association with poor nitric oxide availability under cadmium challenge. Cell Biol. Int. 2006, 30:427-438.
24. Kopf P.G., Huwe J.K., Walker M.K. Hypertension, cardiac hypertrophy, and impaired vascular relaxation induced by 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin are associated with increased superoxide. Cardiovasc. Toxicol. 2008, 8:181-193.
25. Kovacs I.B., Jahangiri M., Rees G.M., Gorog P. Elevated plasma lipid hydroperoxides in patients with coronary artery disease. Am. Heart J. 1997, 134:572-576.
26. Kummerow F.A., Olinescu R.M., Fleischer L., Handler B., Shinkareva S.V. The relationship of oxidized lipids to coronary artery stenosis. Atherosclerosis 2000, 149:181-190.
27. Kuriwaki J., Nishijo M., Hond R., Tawara K., Nakagawa H., Hori E., Nishijo H. Effects of cadmium exposure during pregnancy on trace elements in fetal rat liver and kidney. Toxicol. Lett. 2005, 156:369-376.
28. Liu J., Qu W., Kadiiska M.B. Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol. Appl. Pharmacol. 2009, 238:209-214.
29. Llanos M.N., Ronco A.M. Fetal growth restriction is related to placental levels of cadmium, lead and arsenic but not with antioxidant activities. Reprod. Toxicol. 2009, 27:88-92.
30. Loboda A., Jazwa A., Grochot-Przedzek A., Rutkowsli A.J., Cisowski J., Agarwal A., Jozkowicz A., Dulak J. Heme oxygenase-1 and the vascular bed: from molecular mechanisms to therapeutic opportunities. Antioxid. Redox Signal. 2008, 10:1767-1812.
31. Louey S., Thornburg K.L. The prenatal environment and later cardiovascular disease. Early Hum. Dev. 2005, 81:745-751.
32. Macías C., Villaescusa R., del Valle L., Boffil V., Cordero G., Hernández A., Hernández P., Ballester J.M. Endothelial adhesion molecules ICAM-1, VCAM-1 and E-selectin in patients with acute coronary syndrome. Rev. Esp. Cardiol. 2003, 56:137-144.
33. Majumder S., Muley A., Kolluru G.K., Saurabh S., Tamilarasan K.P., Chandrasekhar S., Reddy H.B., Purohit S., Chatterjee S. Cadmium reduces nitric oxide production by impairing phosphorylation of endothelial nitric oxide synthase. Biochem. Cell Biol. 2008, 86:1-10.
34. Malling T.H., Sigsgaard T., Andersen H.R., Deguchi Y., Brandslund O. Differences in associations between markers of antioxidative defense and asthma are sex specific. Gend. Med. 2010, 7:115-124.
35. McMillen I.C., Robinson J.S. Developmental origins of the metabolic syndrome: prediction, plasticity and programming. Physiol. Rev. 2005, 85:571-633.
36. Messner B., Knoflach M., Seubert A., Ritsch A., Pfaller K., Henderson B., Shen Y.H., Zeller I., Willeit J., Laufer G., Wick G., Kiechl S., Bernhard D. Cadmium is a novel and independent risk factor for early atherosclerosis mechanisms and in vivo relevance. Arterioscler. Thromb. Vasc. Biol. 2009, 29:1392-1398.
37. Mollaoglu H., Gokcimenb A., Ozguner F., Oktemd F., Koyu A., Kocak A., Demirin H., Gokalp O., Cicek E. Caffeic acid phenethyl ester prevents cadmium-induced cardiac impairment in rat. Toxicology 2006, 227:15-20.
38. Nishijo M., Satarug S., Honda R., Tsuritani I., Aoshima K. The gender differences in health effects of environmental cadmium exposure and potential mechanisms. Mol. Cell. Biochem. 2004, 255:87-92.
39. Nyby M., Abedi K., Smutko V., Eslami P., Tuck M.L. Vascular angiotensin Type 1 receptor expression is associated with vascular dysfunction, oxidative stress and inflammation in fructose-fed rats. Hypertens. Res. 2007, 30:451-457.
40. Park S.L., Kim Y.M., Ahn J.H., Lee S.H., Baik E.J., Moon C.H., Jung Y.S. Cadmium stimulates the expression of vascular cell adhesion molecule-1 (VCAM-1) via p38 mitogen-activated protein kinase (MAPK) and JNK activation in cerebrovascular endothelial cells. J. Pharmacol. Sci. 2009, 110:405-409.
41. Peters J.L., Perlstein T.S., Perry M.J., McNeely E., Weuve J. Cadmium exposure in association with history of stroke and heart failure. Environ. Res. 2010, 110:199-206. http://www.sciencedirect.com/dx.doi.org/10.1016/j.envres.2009.12.004.
42. Pillai P., Patel R., Pandya C., Guptai S. Sex-specific effects of gestational and lactational coexposure to lead and cadmium on hepatic phase I and phase II xenobiotic/steroid-metabolizing enzymes and antioxidant status. J. Biochem. Mol. Toxicol. 2009, 23:419-431.
43. Pinardi G., Brieva C., Vinet R., Penna M. Effects of chronic ethanol consumption on alpha-adrenergic-induced contractions in rat thoracic aorta. Gen. Pharmacol. 1992, 23:245-248.
44. Power C., Atherton K., Thomas C. Maternal smoking in pregnancy, adult adiposity and other risk factors for cardiovascular disease. Atherosclerosis 2010, 211:643-648.
45. Prozialeck W., Edwards J.R., Woods J.M. The vascular endothelium as a target of cadmium toxicity. Life Sci. 2006, 79:1493-1506.
46. Prozialeck W.C., Edwards J.R., Nebert D.W., Woods J.M., Barchowsky A., Atchison W.D. The vascular system as a target of metal toxicity. Toxicol. Sci. 2008, 102:207-218.
47. Report of the AVMA Panel on Euthanasia. J. Am. Vet. Med. Assoc. 2001, 218:669-696.
48. Robert R., Chagneau-Derrode C., Carretier M., Mauco G., Silvain C. Gender differences in vascular reactivity of aortas from rats with and without portal hypertension. J. Gastroenterol. Hepatol. 2005, 20:890-894.
49. Rodford J.L., Torrens C., Siow R.C.M., Mann G.E., Hanson M.A., Clough G.F. Endothelial dysfunction and reduced antioxidant protection in an animal model of the developmental origins of cardiovascular disease. J. Physiol. 2008, 586:4709-4720.
50. Röllin H.B., Rudge C.V., Thomassen Y., Mathee A., Odland J.O. Levels of toxic and essential metals in maternal and umbilical cord blood from selected areas of South Africa-results of a pilot study. J. Environ. Monit. 2009, 11:618-627.
51. Ronco A.M., Arguello G., Munoz L., Gras N., Llanos M. Metals content in placentas from moderate cigarette consumers. Correlation with newborn birth weight. Biometals 2005, 18:233-241.
52. Ronco A.M., Urrutia M., Montenegro M., Llanos M.N. Cadmium exposure during pregnancy reduces birth weight and increases maternal and foetal glucocorticoids. Toxicol. Lett. 2009, 188:186-191.
53. Sano M., Minamino T., Toko H., Miyauchi H., Orimo M., Qin Y., Akazawa H., Tateno K., Kayama Y., Harada M., Shimizu I., Asahara T., Hamada H., Tomita S., Molkentin J.D., Zou Y., Komuro I. p53-induced inhibition of Hif-1 causes cardiac dysfunction during pressure overload. Nature 2007, 446:444-448.
54. Sartori-Valinotti J.C., Iliescu R., Fortepiani L.A., Yanes L.L., Reckelhoff J.F. Sex differences in oxidative stress and the impact on blood pressure control and cardiovascular disease. Clin. Exp. Pharmacol. Physiol. 2007, 34:938-945.
55. Satarug S., Nishijo M., Ujjin P., Vanavanitkun Y., Moore M.R. Cadmium-induced nephropathy in the development of high blood pressure. Toxicol. Lett. 2005, 157:57-68.
56. Soares M.P., Seldon M.P., Gregoire I.P., Vassilevskaia T., Berberat P.O., Yu J., Tsui T.-Y., Bach F.H. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J. Immunol. 2004, 172:3553-3563.
57. Stec D.E., Vera T., McLemore G.R., Kelsen S., Rimoldi J.M., Gadepalli R.S.V., Ryan M.J. Heme oxygenase-1 induction does not improve vascular relaxation in angiotensin II hypertensive mice. Am. J. Hypertens. 2008, 21:189-193.
58. Tzotzes V., Tzilalis V., Giannakakis S., Saranteas T., Papas A., Mourouzis I., Mourouzis C., Zarros A., Pantos C., Cokkinos D., Carageorgiou H. Effects of acute and chronic cadmium administration on the vascular reactivity of rat aorta. Biometals 2007, 20:83-91.
59. Vahter M., Akesson A., Liden C., Ceccatelli S., Berglund M. Gender differences in the disposition and toxicity of metals. Environ. Res. 2007, 104:85-95.
60. Walker B.J., Houseman J., Seddon L., McMullen E., Tofflemire K., Mills C., Corriveau A., Weber J.P., LeBlanc A., Walker M., Donaldson S.G., Van Oostdam J. Maternal and umbilical cord blood levels of mercury, lead, cadmium, and essential trace elements in Arctic Canada. Environ. Res. 2006, 100:295-318.
61. Wolf M.B., Baynes J.W. Cadmium and mercury cause an oxidative stress induced endothelial dysfunction. Biometals 2007, 20:73-81.
62. Yang Z., Yang S., Qian S.Y., Hong J.S., Kadiiska M.B., Tennant R.W., Waalkes M.P., Liu J. Cadmium-induced toxicity in rat primary mid-brain neuroglia cultures: role of oxidative stress from microglia. Toxicol. Sci. 2007, 98:488-494.
63. Yoon Y.S., Uchida S., Masuo O., Cejna M., Park J.S., Gwon H.C., Kirchmair R., Bahlman F., Walter D., Curry C., Hanley A., Isner J.M., Losordo D.W. Progressive attenuation of myocardial vascular endothelial growth factor expression is a seminal event in diabetic cardiomyopathy: restoration of microvascular homeostasis and recovery of cardiac function in diabetic cardiomyopathy after replenishment of local vascular endothelial growth factor. Circulation 2005, 111:2073-2085.
64. Yoopan N., Watcharasit P., Wongsawatkul O., Piyachaturawat P., Satayavivad J. Attenuation of eNOS expression in cadmium-induced hypertensive rats. Toxicol. Lett. 2008, 176:157-161.