The hypothalamic-pituitary-gonadal axis is target of cadmium toxicity. An update of recent studies and potential therapeutic approaches

Food and Chemical Toxicology

Volumn 59, Issue , 2013, Pages 395-404

  Lafuente, Anunciación ^a  

^a UNIVERSITY OF VIGO   (Spain)

Author keywords

Cadmium; Hypothalamic pituitary gonadal axis; Neuroendocrine toxicity

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCYSTEINE; ALLYL SULFIDE; ALPHA TOCOPHEROL; ASPARTIC ACID; CADMIUM CHLORIDE; DOPAMINE; GLUTAMIC ACID; GONADOTROPIN; MELATONIN; NORADRENALIN; REACTIVE OXYGEN METABOLITE; SELENIUM; SEROTONIN; TAURINE; THEAFLAVIN; THIOCTIC ACID; TROLOX C; UBIDECARENONE; ZINC;

ANTIOXIDANT ACTIVITY; BIOACCUMULATION; CIRCADIAN RHYTHM; HUMAN; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; LIPID PEROXIDATION; NEUROENDOCRINE DISEASE; NEUROMODULATION; NEUROPATHOLOGY; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OVARY FUNCTION; OXIDATIVE STRESS; PREMATURE AGING; REPRODUCTIVE TOXICITY; REVIEW; TREATMENT OUTCOME;

CADMIUM; HYPOTHALAMIC-PITUITARY-GONADAL AXIS; NEUROENDOCRINE TOXICITY;

AGE FACTORS; ANIMALS; ANTIOXIDANTS; CADMIUM; CADMIUM POISONING; CIRCADIAN RHYTHM; FEMALE; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MODELS, BIOLOGICAL; NEUROSECRETORY SYSTEMS; OVARY; OXIDATIVE STRESS; TESTIS;

EID: 84880356589     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2013.06.024     Document Type: Review

References (112)

1. Åkesson A., Bjellerup P., Lundh T., Lidfeldt J., Nerbrand C., Samsioe G., Skerfving S., Vahter M. Cadmium-induced effects on bone in a population-based study of women. Environ. Health Perspect. 2006, 114:830-834.
2. Akinloye O., Arowojolu A.O., Shittu O.B., Anetor J.I. Cadmium toxicity: a possible cause of male infertility in Nigeria. Reprod. Biol. 2006, 6:17-30.
3. Ali I., Penttinen-Damdimopoulou P.E., Mäkelä S.I., Berglund M., Stenius U., Akesson A., Håkansson H., Halldin K. Estrogen-like effects of cadmium in vivo do not appear to be mediated via the classical estrogen receptor transcriptional pathway. Environ. Health Perspect. 2010, 118:1389-1394.
4. Allanson M., Deanesly R. Observations on cadmium damage and repair in rat testes and the effects on the pituitary gonadotrophs. J. Endocrinol. 1962, 24:453-462.
5. Antonio M.T., Peinado V., González J.C., Leret M.L. Effects of maternal cadmium administration on development of monoaminergic, GABAergic and glutamatergic systems. Environ. Toxicol. Pharmacol. 2010, 29:87-90.
6. Apostoli P., Catalani S. Metal ions affecting reproduction and development. Met. Ions Life Sci. 2011, 8:263-303.
7. Arito H., Sudo A., Suzuki Y. Aggressive behavior of the rat induced by repeated administration of cadmium. Toxicol. Lett. 1981, 7:457-461.
8. Borisova T., Krisanova N., Sivko R., Kasatkina L., Borysov A., Griffin S., Wireman M. Presynaptic malfunction: the neurotoxic effects of cadmium and lead on the proton gradient of synaptic vesicles and glutamate transport. Neurochem. Int. 2011, 59:272-279.
9. Byrne C., Divekar S.D., Storchan G.B., Parodi D.A., Martin M.B. Metals and Breast Cancer. J Mammary Gland Biol Neoplasia 2013, 18:163-173.
10. Calderoni A.M., Oliveros L., Jahn G., Anton R., Luco J., Giménez M.S. Alterations in the lipid content of pituitary gland and serum prolactin and growth hormone in cadmium treated rats. Biometals 2005, 18:213-220.
11. Calderoni A.M., Biaggio V., Acosta M., Oliveros L., Mohamed F., Giménez M.S. Cadmium exposure modifies lactotrophs activity associated to genomic and morphological changes in rat pituitary anterior lobe. BioMetals 2010, 23:135-143.
12. Cano P., Poliandri A.H., Jiménez V., Cardinali D.P., Esquifino A.I. Cadmium-induced changes in Per 1 and Per 2 gene expression in rat hypothalamus and anterior pituitary: effect of melatonin. Toxicol. Lett. 2007, 172:131-136.
13. Caride A., Fernández-Pérez B., Cabaleiro T., Bernandez G., Lafuente A. Cadmium chloride exposure modifies amino acid daily pattern in the mediobasal hypothalamus in adult male rat. J. Appl. Toxicol. 2009, 30:84-90.
14. Caride A., Fernández-Pérez B., Cabaleiro T., Esquifino A.I., Lafuente A. Cadmium exposure disrupts GABA and taurine regulation of prolactin secretion in adult male rats. Toxicol. Lett. 2009, 185:175-179.
15. Caride A., Fernández-Pérez B., Cabaleiro T., Tarasco M., Esquifino A.I., Lafuente A. Cadmium chronotoxicity at pituitary level: effects on plasma ACTH, GH, and TSH daily pattern. J. Physiol. Biochem. 2010, 66:213-220.
16. Caride A., Fernández-Pérez B., Cabaleiro T., Lafuente A. Daily pattern of pituitary glutamine, glutamate and aspartate content disrupted by cadmium exposure. Amino Acids 2010, 328:1165-1172.
17. Chwełatiuk E., Włostowski T., Krasowska A., Bonda E. The effect of orally administered melatonin on tissue accumulation and toxicity of cadmium in mice. J. Trace Elem. Med. Biol. 2006, 19:259-265.
18. Ciarrocca M., Capozzella A., Tomei F., Tomei G., Caciari T. Exposure to cadmium in male urban and rural workers and effects on FSH, LH and testosterone. Chemosphere 2013, 90:2077-2084.
19. 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.
20. Denier X., Hill E.M., Rotchell J., Minier C. Estrogenic activity of cadmium, copper and zinc in the yeast estrogen screen. Toxicol. In Vitro 2009, 23:569-573.
21. El-Maraghy S.A., Nassar N.N. Modulatory effects of lipoic acid and selenium against cadmium-induced biochemical alterations in testicular steroidogenesis. J. Biochem. Mol. Toxicol. 2011, 25:15-25.
22. Esquifino A.I., Seara R., Fernández-Rey E., Lafuente A. Alternate cadmium exposure differentially affects the content of gamma-aminobutyric acid (GABA) and taurine within the hypothalamus, median eminence, striatum and prefrontal cortex of male rats. Arch. Toxicol. 2001, 75:127-133.
23. Fagerberg B., Bergström G., Borén J., Barregard L. Cadmium exposure is accompanied by increased prevalence and future growth of atherosclerotic plaques in 64-year-old women. J. Int. Med. 2012, 272:601-610.
24. Gallagher C.M., Chen J.J., Kovach J.S. Environmental cadmium and breast cancer risk. Aging (Albany, NY) 2010, 2:804-814.
25. García-Santos S., Fontaínhas-Fernandes A., Monteiro S.M., Wilson J.M. Effects of Exposure to Cadmium on Some Endocrine Parameters in Tilapia, Oreochromisniloticus. Bull. Environ. Contam. Toxicol. 2013, 90:55-59.
26. Genuis S.J., Schwalfenberg G., Siy A.K., Rodushkin I. Toxic element contamination of natural health products and pharmaceutical preparations. PLoS One 2012, 7:e49676.
27. Girod C. Study of the antehypophysial gonadotropic cells of the monkey macacusirus f. Cuv., after cadmium chloride administration. C.R. Seances Soc. Biol. Fil. 1964, 158:948-949.
28. Gollenberg A.L., Hediger M.L., Lee P.A., Himes J.H., Louis G.M. Association between lead and cadmium and reproductive hormones in peripubertal US girls. Environ. Health Perspect. 2010, 118:1782-1787.
29. Gonçalves J.F., Nicoloso F.T., da Costa P., Farias J.G., Carvalho F.B., da Rosa M.M., Gutierres J.M., Abdalla F.H., Pereira J.S., Dias G.R., Barbosa N.B., Dressler V.L., Rubin M.A., Morsch V.M., Schetinger M.R. Behavior and brain enzymatic changes after long-term intoxication with cadmium salt or contaminated potatoes. Food Chem. Toxicol. 2012, 50:3709-3718.
30. González-Carracedo, A., 2005. Aging and neuroendocrine chronotoxicity induced by exposure to cadmium, doctoral thesis. University of Vigo, Spain.
31. Gunnarsson D., Nordberg G., Selstam G. Differential effects of cadmium on the gene expression of seven-transmembrane-spanning receptors and GAPDH in the rat testis. Toxicol. Lett. 2007, 168:51-57.
32. Hachfi L., Sakly R. Effect of Cd transferred via food product on spermatogenesis in the rat. Andrologia 2010, 42:62-64.
33. Han X.Y., Huang Q.C., Liu B.J., Xu Z.R., Wang Y.Z. Changes of porcine growth hormone and pituitary nitrogen monoxide production as a response to cadmium toxicity. Biol. Trace Elem. Res. 2007, 119:128-136.
34. Holásková I., Elliott M., Hanson M.L., Schafer R., Barnett J.B. Prenatal cadmium exposure produces persistent changes to thymus and spleen cell phenotypic repertoire as well as the acquired immune response. Toxicol. Appl. Pharmacol. 2012, 265:181-189.
35. Honda A., Watanabe C., Yoshida M., Nagase H., Satoh M. Microarray analysis of neonatal brain exposed to cadmium during gestation and lactation. J. Toxicol. Sci. 2013, 38:151-153.
36. Hrdina P.D., Peters D.A., Singhal R.L. Effects of chronic exposure to cadmium, lead and mercury of brain biogenic amines in the rat. Res. Commun. Chem. Pathol. Pharmacol. 1976, 15:483-493.
37. Iavicoli I., Fontana L., Bergamaschi A. The effects of metals as endocrine disruptors. J. Toxicol. Environ. Health Part B 2009, 12:206-223.
38. Izzo G., Francesco A., Ferrara D., Campitiello M.R., Serino I., Minucci S., d'Istria M. Expression of melatonin (MT1, MT2) and melatonin-related receptors in the adult rat testes and during development. Zygote 2010, 18:257-264.
39. Ji Y.L., Wang H., Zhang Y., Zhao M., Chen Y.H., Xu D.X. N-acetylcysteine protects against cadmium-induced germ cell apoptosis by inhibiting endoplasmic reticulum stress in testes. Asian J. Androl. 2013, 15:290-296.
40. Jiménez-Ortega V., Cardinali D.P., Fernández-Mateos M.P., Ríos-Lugo M.J., Scacchi P.A., Esquifino A.I. Effect of cadmium on 24-hour pattern in expression of redox enzyme and clock genes in rat medial basal hypothalamus. Biometals 2010, 23:327-337.
41. Jiménez-Ortega V., Cano-Barquilla P., Scacchi P.A., Cardinali D.P., Esquifino A.I. Cadmium-induced disruption in 24-h expression of clock and redox enzyme genes in rat medial basal hypothalamus: prevention by melatonin. Front. Neurol. 2011, 16:2-13.
42. Jiménez-Ortega V., Cano Barquilla P., Fernández-Mateos P., Cardinali, Daniel P., Esquifino A.I. Cadmium as an endocrine disruptor: correlation with anterior pituitary redox and circadian clock mechanisms and prevention by melatonin. Free Rad. Biol. Med. 2012, 53:2287-2297.
43. Jou M.J., Peng T.I., Reiter R.J., Jou S.B., Wu H.Y., Wen S.T. Visualization of the antioxidative effects of melatonin at the mitochondrial level during oxidative stress-induced apoptosis of rat brain astrocytes. J. Pineal Res. 2004, 37:55-70.
44. Julin B., Wolk A., Johansson J.E., Andersson S.O., Andrén O., Akesson A. Dietary cadmium exposure and prostate cancer incidence: a population-based prospective cohort study. Br. J. Cancer 2012, 21:895-900.
45. Kang M.Y., Cho S.H., Lim Y.H., Seo J.C., Hong Y.C. Effects of environmental cadmium exposure on liver function in adults. Occup. Environ. Med. 2013, 70:268-273.
46. Kaur G., Phillips C., Wong K., Saini B. Timing is important in medication administration: a timely review of chronotherapy research. Int. J. Clin. Pharm. 2013, 35:344-358.
47. Kim S., Cheon H.S., Kim S.Y., Juhnn Y.S., Kim Y.Y. Cadmium induces neuronal cell death through reactive oxygen species activated by GADD153. BMC Cell Biol. 2013, 14:4.
48. Kus I., Akpolat N., Ozen O.A., Songur A., Kavakli A., Sarsilmaz M. Effects of melatonin on Leydig cells in pinealectomized rat: an immunohistochemical study. Acta Histochem. 2002, 104:93-97.
49. Lafuente A., Esquifino A.I. Cadmium effects on hypothalamic activity and pituitary hormone secretion in the male. Toxicol. Lett. 1999, 110:209-218.
50. Lafuente A., Esquifino A.I. Effects of oral cadmium exposure through puberty on plasma prolactin and gonadotropin levels and amino acid content in various brain areas in pubertal male rats. Neurotoxicology 2002, 23:207-213.
51. Lafuente A., Esquifino A.I. Possible role of glutamate, aspartate, glutamine, GABA or taurine on cadmium toxicity on the hypothalamic pituitary axis activity in adult male rats. BioMetals 2002, 15:183-187.
52. Lafuente A., Márquez N., Piquero S., Esquifino A.I. Cadmium affects the episodic luteinizing hormone secretion in male rats: possible age-dependent effects. Toxicol. Lett. 1999, 104:27-33.
53. Lafuente A., Alvarez-Demanuel E., Márquez N., Esquifino A.I. Pubertal dependent effects of cadmium on episodic prolactin secretion in male rats. Arch. Toxicol. 1999, 73:60-63.
54. Lafuente A., Marquez N., Perez-Lorenzo M., Pazo D., Esquifino A.I. Pubertal and postpubertal cadmium exposure differentially affects the hypothalamus-pituitary-testicular axis function in the rat. Food Chem. Toxicol. 2000, 38:913-923.
55. Lafuente A., Marquez N., Pazo D., Esquifino A.I. Effects of subchronic alternating cadmium exposure on dopamine turnover and plasma levels of prolactin, GH and ACTH. Biometals 2000, 13:47-55.
56. Lafuente A., Marquez N., Pérez-Lorenzo M., Pazo D., Esquifino A.I. Cadmium effects on hypothalamic-pituitary-testicular axis in male rats. Exp. Biol. Med. 2001, 226:605-611.
57. Lafuente A., Fenández-Rey E., Seara R., Pérez-Lorenzo M., Esquifino A.I. Alternate cadmium exposure differentially affects amino acid metabolism within the hypothalamus, median eminence, striatum and prefrontal cortex of male rats. Neurochem. Int. 2001, 39:187-192.
58. Lafuente A., González-Carracedo A., Marquez N., Pazo D., Esquifino A.I. Oral cadmium exposure throughout puberty does not inhibit secretion of prolactin, GH and ACTH through dopamine metabolism changes in male rat. J. Trace Elem. Med. Biol. 2002, 16:249-254.
59. Lafuente A., Cano P., Esquifino A. Are cadmium effects on plasma gonadotropins, prolactin, ACTH, GH and TSH levels, dose-dependent?. BioMetals 2003, 16:243-250.
60. Lafuente A., González-Carracedo A., Romero A., Esquifino A.I. Effect of cadmium on lymphocyte subsets distribution in thymus and spleen. J. Physiol. Biochem. 2003, 59:43-48.
61. Lafuente A., González-Carracedo A., Romero A., Esquifino A.I. Effect of cadmium on 24-h variations in hypothalamic dopamine and serotonin metabolism in adult male rats. Exp. Brain Res. 2003, 1489:200-206.
62. Lafuente A., González-Carracedo A., Romero A., Cano P., Esquifino A.I. Cadmium exposure differentially modifies the circadian patterns of norepinephrine at the median eminence and plasma LH, FSH and testosterone levels. Toxicol. Lett. 2004, 146:175-182.
63. Lafuente A., González-Carracedo A., Romero A., Cabaleiro T., Esquifino A.I. Toxic effects of cadmium on the regulatory mechanism of dopamine and serotonin on prolactin secretion in adult male rats. Toxicol. Lett. 2005, 155:87-96.
64. Lafuente A., Cabaleiro T., Caride A., Esquifino A.I. Toxic effects of methoxychlor administered subcutaneously on the hypothalamic-pituitary-testicular axis in adult rats. Food Chem. Toxicol. 2008, 246:1570-1575.
65. Lee B.K., Kim Y. Association of blood cadmium with hypertension in the Korean general population: analysis of the 2008-2010 Korean National Health and Nutrition Examination Survey data. Am. J. Ind. Med. 2012, 55:1060-1067.
66. Li X., Lv Y., Yu S., Zhao H., Yao L. The effect of cadmium on Aβ levels in APP/PS1 transgenic mice. Exp. Ther. Med. 2012, 4:125-130.
67. Lin Y.S., Caffrey J.L., Lin J.W., Bayliss D., Faramawi M.F., Bateson T.F., Sonawane B. Increased risk of cancer mortality associated with cadmium exposures in older Americans with low zinc intake. J. Toxicol. Environ. Health A 2013, 76:1-15.
68. Liu Y.P., Yang C.S., Tzeng S.F. Inhibitory regulation of glutamate aspartate transporter (GLAST) expression in astrocytes by cadmium-induced calcium influx. J. Neurochem. 2008, 105:137-150.
69. Lubo-Palma A., Nava-Leal C., Villasmil V., Quevedo A.L., Montiel M., Simoes D., Faría C. Effects of cadmium on the ovarian parenchyma in Swiss albino mice. Invest Clin. 2006, 47:219-231.
70. Luckett B.G., Su L.J., Rood J.C., Fontham E.T. Cadmium exposure and pancreatic cancer in South louisiana. J. Environ. Public Health 2012, Article ID 180186.
71. Manna P., Sinha M., Sil P.C. Cadmium induced testicular pathophysiology: prophylactic role of taurine. Reprod. Toxicol. 2008, 26:282-291.
72. Mendiola J., Moreno J.M., Roca M., Vergara-Juárez N., Martínez-García M.J., García-Sánchez A., Elvira-Rendueles B., Moreno-Grau S., López-Espín J.J., Ten J., Bernabeu R., Torres-Cantero A.M. Relationships between heavy metal concentrations in three different body fluids and male reproductive parameters: a pilot study. Environ. Health 2011, 10:6-12.
73. Miler E.A., Nudler S.I., Quinteros F.A., Cabilla J.P., Ronchetti S.A., Duvilanski B.H. Cadmium induced-oxidative stress in pituitary gland is reversed by removing the contamination source. Hum. Exp. Toxicol. 2010, 29:873-880.
74. Miura N., Yanagiba Y., Ohtani K., Mita M., Togawa M., Hasegawa T. Diurnal variation of cadmium-induced mortality in mice. J. Toxicol. Sci. 2012, 37:191-196.
75. Moore J.W., Ramamoorthy S. Heavy Metals in Natural Water: Applied Monitoring and Impact Assessment 1984, Springer-Verlag, New York.
76. Nagata C., Nagao Y., Nakamura K., Wada K., Tamai Y., Tsuji M., Yamamoto S., Kashiki Y. Cadmium exposure and the risk of breast cancer in Japanese women. Breast Cancer Res. Treat. 2013, 138:235-239.
77. Ognjanović B.I., Marković S.D., Ethordević N.Z., Trbojević I.S., Stajn A.S., Saicić Z.S. Cadmium-induced lipid peroxidation and changes in antioxidant defense system in the rat testes: protective role of coenzyme Q(10) and vitamin E. Reprod. Toxicol. 2010, 29:191-197.
78. Ohtani K., Yanagiba Y., Ashimori A., Takeuchi A., Takada N., Togawa M., Hasegawa T., Ikeda M., Miura N. Influence of injection timing on severity of cadmium-induced testicular toxicity in mice. J. Toxicol. Sci. 2013, 38:145-150.
79. Pacini S., Fiore M.G., Magherini S., Morucci G., Branca J.J., Gulisano M., Ruggiero M. Could cadmium be responsible for some of the neurological signs and symptoms of Myalgic Encephalomyelitis/Chronic Fatigue Syndrome. Med. Hypotheses 2012, 79:403-407.
80. Paksy K., Rajczy K., Forgács Z., Lázár P., Bernard A., Gáti I., Kaáli G.S. Effect of cadmium on morphology and steroidogenesis of cultured human ovarian granulosa cells. J. Appl. Toxicol. 1997, 17:321-327.
81. Paxinos G. Tha Rat Nervous System 2004, Elsevier Academic Press, San Diego, pp. 335.
82. Pereriro, N., 2012. Evaluation of neuroendocrine toxicity of perfluorinated compounds, Doctoral Thesis. University of Vigo, Spain.
83. Petrochelli Banzato T., Godinho A.F., da Silva Zacarin E.C., Perobelli J.E., Dal Bianco Fernandez C., Favareto A.P., De Grava Kempinas W. Sperm quality in adult male rats exposed to cadmium in utero and lactation. J. Toxicol. Environ. Health A 2012, 75:1047-1058.
84. Piasek M., Laskey J.W. Acute cadmium exposure and ovarian steroidogenesis in cycling and pregnant rats. Reprod. Toxicol. 1994, 8:495-507.
85. Piasek M., Laskey J.W. Effects of in vitro cadmium exposure on ovarian steroidogenesis in rats. J. Appl. Toxicol. 1999, 19:211-217.
86. Pillai A., Laxmi Priya P.N., Gupta S. Effects of combined exposure to lead and cadmium on pituitary membrane of female rats. Arch. Toxicol. 2002, 76:671-675.
87. Pillai A., Priya L., Gupta S. Effects of combined exposure to lead and cadmium on the hypothalamic-pituitary axis function in proestrous rats. Food Chem. Toxicol. 2003, 41:379-384.
88. Pillai P., Pandya C., Gupta S., Gupta S. Biochemical and molecular effects of gestational and lactationalcoexposure to lead and cadmium on ovarian steroidogenesis are associated with oxidative stress in F1 generation rats. J. Biochem. Mol. Toxicol. 2010, 24:384-394.
89. Poliandri A.H., Cabilla J.P., Velardez M.O., Bodo C.C., Duvilanski B.H. Cadmium induces apoptosis in anterior pituitary cells that can be reversed by treatment with antioxidants. Toxicol. Appl. Pharmacol. 2003, 190:17-24.
90. Poliandri A.H., Esquifino A.I., Cano P., Jiménez V., Lafuente A., Cardinali D.P., Duvilanski B.H. In vivo protective effect of melatonin on cadmium-induced changes in redox balance and gene expression in rat hypothalamus and anterior pituitary. J. Pineal Res. 2006, 4:238-246.
91. Pollack A.Z., Schisterman E.F., Goldman L.R., Mumford S.L., Albert P.S., Jones R.L., Wactawski-Wende J. Cadmium, lead, and mercury in relation to reproductive hormones and anovulation in premenopausal women. Environ. Health Perspect. 2011, 119:1156-1161.
92. Reiter R.J., Tan D.X., Terron M.P., Flores L.J., Czarnocki Z. Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochim. Pol. 2007, 54:1-9.
93. Romero A., Caride A., Pereiro N., Lafuente A. Modulatory effects of melatonin on cadmium-induced changes in biogenic amines in rat hypothalamus. Neurotox. Res. 2011, 20:240-249.
94. Sadik N.A. Effects of diallyl sulfide and zinc on testicular steroidogenesis in cadmium-treated male rats. J. Biochem. Mol. Toxicol. 2008, 22:345-353.
95. Samuel J.B., Stanley J.A., Princess R.A., Shanthi P., Sebastian M.S. Gestational cadmium exposure-induced ovotoxicity delays puberty through oxidative stress and impaired steroid hormone levels. J. Med. Toxicol. 2011, 7:195-204.
96. Satarug S., Garrett S.H., Sens M.A., Sens D.A. Cadmium, environmental exposure, and health outcomes. Environ. Health Perspect. 2010, 118:182-190.
97. Shargorodsky J., Curhan S.G., Henderson E., Eavey R., Curhan G.C. Heavy metals exposure and hearing loss in US adolescents. Arch. Otolaryngol. Head Neck Surg. 2011, 137:1183-1189.
98. Silva R.F., Falcão A.S., Fernandes A., Gordo A.C., Brito M.A., Brites D. Dissociated primary nerve cell cultures as models for assessment of neurotoxicity. Toxicol. Lett. 2006, 163:1-9.
99. Smida A.D., Valderrama X.P., Agostini M.C., Furlan M.A., Chedrese J. Cadmium stimulates transcription of the cytochrome p450 side chain cleavage gene in genetically modified stable porcine granulosa cells. Biol. Reprod. 2004, 70:25-31.
100. Sommar J.N., Svensson M.K., Björ B.M., Elmståhl S.I., Hallmans G., Lundh T., Schön S.M., Skerfving S., Bergdahl I.A. End-stage renal disease and low level exposure to lead, cadmium and mercury; a population-based, prospective nested case-referent study in Sweden. Environ. Health 2013, 12:9-19.
101. Tellez-Plaza M., Navas-Acien A., Crainiceanu C.M., Guallar E. Cadmium exposure and hypertension in the 1999-2004 National Health and Nutrition Examination Survey (NHANES). Environ. Health Perspect. 2008, 116:51-56.
102. Tellez-Plaza M., Navas-Acien A., Menke A., Crainiceanu C.M., Pastor-Barriuso R., Guallar E. Cadmium exposure and all-cause and cardiovascular mortality in the US general population. Environ. Health Perspect. 2012, 120:1017-1022.
103. Varga B., Paksy K., Náray M. Distribution of cadmium in ovaries, adrenals and pituitary gland after chronic administration in rats. Acta Physiol, Hung. 1991, 78:221-226.
104. Velásquez, M., 2008. Cadmium chronotoxicity on aminoacidergic metabolism in old male rat, Doctoral Thesis. University of Vigo, Spain.
105. Wang S., Hu P., Wang H.L., Wang M., Chen J.T., Tang J.L., Ruan D.Y. Effects of Cd(2+) on AMPA receptor-mediated synaptic transmission in rat hippocampal CA1 area. Toxicol. Lett. 2008, 176:215-222.
106. Wang W., Sun Y., Liu J., Wang J., Li Y., Li H., Zhang W., Liao H. Protective effect of theaflavins on cadmium-induced testicular toxicity in male rats. Food Chem. Toxicol. 2012, 50:3243-3250.
107. Williams W.P., Kriegsfeld L.J. Circadian control of neuroendocrine circuits regulating female reproductive function. Front. Endocrinol. 2012, 3:60-74.
108. Yan Y., Bian J.C., Zhong L.X., Zhang Y., Sun Y., Liu Z.P. Oxidative stress and apoptotic changes of rat cerebral cortical neurons exposed to cadmium in vitro. Biomed. Environ. Sci. 2012, 25:172-181.
109. 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.
110. Zeng X., Jin T., Buchet J.P., Jiang X., Kong Q., Ye T., Bernard A., Nordberg G.F. Impact of cadmium exposure on male sex hormones: a population-based study in China. Environ. Res. 2004, 96:338-344.
111. Zhang W., Pang F., Huang Y., Yan P., Lin W. Cadmium exerts toxic effects on ovarian steroid hormone release in rats. Toxicol.Lett. 2008, 182:l18-123.
112. Zhang H., Cai C., Shi C., Cao H., Han Z., Jia X. Cadmium-induced oxidative stress and apoptosis in the testes of frog Ranalimnocharis. Aquat. Toxicol. 2012, 122:67-74.