In utero exposure to chloroquine alters sexual development in the male fetal rat

Toxicology and Applied Pharmacology

Volumn 237, Issue 3, 2009, Pages 366-374

  Clewell, Rebecca A ^a,b   Pluta, Linda ^b   Thomas, Russell S ^b   Andersen, Melvin E ^b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

Author keywords

Chloroquine; Fetal toxicity; Gestation; Rat; Testosterone

Indexed keywords

CHLOROQUINE; PROGESTERONE; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DOSE RESPONSE; DOWN REGULATION; DRUG BLOOD LEVEL; FATTY LIVER; FEMALE; FETUS; FETUS LIVER; FETUS WEIGHT; GENE CONTROL; GENE EXPRESSION; HISTOPATHOLOGY; HOMEOSTASIS; LIVER NECROSIS; LIVER TOXICITY; LOADING DRUG DOSE; MALE; MALE GENITAL SYSTEM; MICROARRAY ANALYSIS; MORPHOLOGY; NONHUMAN; PRENATAL EXPOSURE; PROGESTERONE BLOOD LEVEL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULE; SEXUAL DEVELOPMENT; TESTIS; VASCULARIZATION; WEIGHT CHANGE; WEIGHT REDUCTION;

ANIMALS; CHLOROQUINE; FEMALE; FETAL DEVELOPMENT; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; SEXUAL DEVELOPMENT; TESTIS;

RATTUS;

EID: 65749101324     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2009.04.013     Document Type: Article

References (44)

1. Acton S., Rigotti A., Landschulz K.T., Xu S., Hobbs H.H., and Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271 5248 (2006) 518-520
2. Adelusi S.A., and Salako L.A. Kinetics of the distribution and elimination of chloroquine in the rat. Gen. Pharmacol. 13 (1982) 433-437
3. Akintonwa A., Meyer M.C., and Yau M.K. Placental transfer of chloroquine in pregnant rabbits. Res. Commun. Chem. Pathol. Pharmacol. 40 3 (1983) 443-455
4. Akintonwa A., Gbajumo S.A., and Mabadeje A.F. Placental and milk transfer of chloroquine in humans. Ther. Drug Monit. 10 2 (1988) 147-149
5. Bennati A.M., Castelli M., Della Fazia M.A., Beccari T., Caruso D., Servillo G., and Roberti R. Sterol dependent regulation of human TM7SF2 gene expression: role of the encoded 3beta-hydroxysterol Delta14-reductase in human cholesterol biosynthesis. Biochim. Biophys. Acta 1761 7 (2006) 677-685
6. Borch J., Axelstad M., Vinggaard A.M., and Dalgaard M. Diisobutyl phthalate has comparable anti-androgenic effects to di-n-butyl phthalate in fetal rat testis. Toxicol. Lett. 163 3 (2006) 183-190
7. Collin O., Lissbrant E., and Bergh A. Atrial natriuretic peptide, brain natriuretic peptide and c-type natriuretic peptide: effects on testicular microcirculation and immunohistochemical localization. Int. J. Androl. 20 1 (1997) 55-60
8. Dass E.E., and Shah K.K. Paracetamol and conventional antimalarial drugs induced hepatotoxicity and its protection by methionine in rats. Indian J. Exp. Biol. 38 11 (2000) 1138-1142
9. Deng H., Liu H., Krogstad F.M., and Krogstad D.J. Sensitive fluorescence HPLC assay for AQ-13, a candidate aminoquinoline antimalarial, that also detects chloroquine and N-dealkylated metabolites. J. Chromatogr., B, Analyt. Technol. Biomed. Life Sci. 833 2 (2006) 122-128
10. Dobozy O., Brindak O., and Csaba G. Influence of pituitary hormones (hCG, TSH, Pr, GH) on testosterone level and on the functional activity of the Leydig cell in rat fetuses. Acta Physiol. Hung. 72 2 (1988) 159-163
11. Ebong P.E., Eyong E.U., Eteng M.U., and Ukwe C.N. Influence of chronic administration of chloroquine on Leydig cell integrity and testosterone profile of albino Wistar rats. Afr. J. Reprod. Health 3 2 (1999) 97-101
12. Edwards G., Looareesuwan S., Davies A.J., Wattanagoon Y., Phillips R.E., and Warrell D.A. Pharmacokinetics of chloroquine in Thais: plasma and red-cell concentrations following an intravenous infusion to healthy subjects and patients with Plasmodium vivax malaria. Br. J. Clin. Pharmacol. 25 4 (1988) 477-485
13. El-Gehani F., Tena-Sempere M., Ruskoaho H., and Huhtaniemi I. Natriuretic peptides stimulate steroidogenesis in the fetal rat testis. Biol. Reprod. 65 2 (2001) 595-600
14. Foster P.M., and McIntyre B.S. Endocrine active agents: implications of adverse and non-adverse changes. Toxicol. Pathol. 30 1 (2002) 59-65
15. Gräbner R. Influence of cationic amphiphilic drugs on the phosphatidylcholine hydrolysis by phospholipase A2. Biochem. Pharmacol. 36 7 (1987) 1063-1067
16. Lehmann K.P., Phillips S., Sar M., Foster P.M., and Gaido K.W. Dose-dependent alterations in gene expression and testosterone synthesis in the fetal testes of male rats exposed to di (n-butyl) phthalate. Toxicol. Sci. 81 1 (2004) 60-68
17. Lejeune D., Souletie I., Houzé S., Le bricon T., Le bras J., Gourmel B., and Houzé P. Simultaneous determination of monodesethylchloroquine, chloroquine, cycloguanil and proguanil on dried blood spots by reverse-phase liquid chromatography. J. Pharm. Biomed. Anal. 43 3 (2007) 1106-1115
18. Liu K., Lehmann K.P., Sar M., Young S.S., and Gaido K.W. Gene expression profiling following in utero exposure to phthalate esters reveals new gene targets in the etiology of testicular dysgenesis. Biol. Reprod. 73 1 (2005) 180-192
19. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-delta delta C(T)) method. Mehods 25 4 (2001) 402-408
20. Matsuzawa Y., and Hostetler K.Y. Studies on drug-induced lipidosis: subcellular localization of phospholipid and cholesterol in the liver of rats treated with chloroquine or 4,4′-bis (diethylaminoethoxy)alpha, beta-diethyldiphenylethane. J. Lipid Res. 21 2 (1980) 202-214
21. McIntyre B.S., Barlow N.J., and Foster P.M. Androgen-mediated development in male rat offspring exposed to flutamide in utero: permanence and correlation of early postnatal changes in anogenital distance and nipple retention with malformations in androgen-dependent tissues. Toxicol. Sci. 62 2 (2001) 236-249
22. Mgbodile M.U. Effects of perinatal exposure of albino rats to chloroquine. Biol. Neonate 51 5 (1987) 273-276
23. Miller W.L. Steroidogenic acute regulatory protein (StAR), a novel mitochondrial cholesterol transporter. Biochim. Biophys. Acta 1771 6 (2007) 663-676
24. Mylchreest E., Sar M., Cattley R.C., and Foster P.M. Disruption of androgen-regulated male reproductive development by di(n-butyl) phthalate during late gestation in rats is different from flutamide. Toxicol. Appl. Pharmacol. 156 2 (1999) 81-95
25. Ngaha E.O. Some biochemical changes in the rat during repeated chloroquine administration. Toxicol. Lett. 10 2-3 (1982) 145-149
26. Nicola W.G. Chloroquine therapy reduces oestrogen production in females. Boll. Chim. Farm. 136 5 (1997) 447-449
27. Nicola W.G., Khayria M.I., and Osfor M.M. Plasma testosterone level and the male genital system after chloroquine therapy. Boll. Chim. Farm. 136 1 (1997) 39-43
28. Nord J.E., Shah P.K., Rinaldi R.Z., and Weisman M.H. Hydroxychloroquine cardiotoxicity in systemic lupus erythematosus: a report of 2 cases and review of the literature. Semin. Arthritis Rheum. 33 5 (2004) 336-351
29. Nosten F., McGready R., d'Alessandro U., Bonell A., Verhoeff F., Menendez C., Mutabingwa T., and Brabin B. Antimalarial drugs in pregnancy: a review. Curr. Drug Saf. 1 1 (2006) 1-15
30. Ochsendorf F.R., and Runne U. Chloroquine and hydroxychloroquine: side effect profile of important therapeutic drugs. Hautarzt 42 (1991) 140-146
31. Okanlawon A.O., and Ashiru O.A. Effect of chloroquine on oestrus cycle and ovulation in cyclic rats. J. Appl. Toxicol. 12 1 (1992) 45-48
32. Okanlawon A.O., and Ashiru O.A. Sterological estimation of seminiferous tubular dysfunction in chloroquine treated rats. Afr. J. Med. & Med. Sci. 27 1-2 (1998) 101-106
33. Okanlawon A.O., Ejiwunmi A.B., Dada M.O., and Ashiru O.A. Chloroquine-induced retardation of foetal lung maturation in rats. Afr. J. Med. & Med. Sci. 22 2 (1993) 61-67
34. Okanlawon A.O., Noronha C.C., and Ashiru O.A. An investigation into the effects of chloroquine on fertility of male rats. West Afr. J. Med. 12 2 (1993) 118-121
35. Osifo N.G. The effect of pyrogen on the in vivo metabolism and initial kinetics of chloroquine in rats. J. Pharm. Pharmacol. 31 (1979) 747-751
36. Østensen M., Khamashta M., Lockshin M., Parke A., Brucato A., Carp H., Doria A., Rai R., Meroni P., Cetin I., Derksen R., Branch W., Motta M., Gordon C., Ruiz-Irastorza G., Spinillo A., Friedman D., Cimaz R., Czeizel A., Piette J.C., Cervera R., Levy R.A., Clementi M., De Carolis S., Petri M., Shoenfeld Y., Faden D., Valesini G., and Tincani A. Anti-inflammatory and immunosuppressive drugs and reproduction. Arthritis Res. Ther. 8 3 (2006) 209. http://arthritis-research.com/content/8/3/209 http://arthritis-research.com/content/8/3/209
37. Pearse A.G.E. Histotechnology: A Self-instructional Text (2006), ASCP Press, Chicago
38. Pussard E., Lepers J.P., Clavier F., Raharimalala L., Le Bras J., Frisk-Holmberg M., Bergqvist Y., and Verdier F. Efficacy of a loading dose of oral chloroquine in a 36-hour treatment schedule for uncomplicated Plasmodium falciparum malaria. Antimicrob. Agents Chemother. 35 3 (1991) 406-409
39. Romanelli F., Valenca M., Conte D., Isidori A., and Negro-Vilar A. Arachidonic acid and its metabolites effects on testosterone production by rat Leydig cells. J. Endocrinol. Invest. 18 3 (1995) 186-193
40. Sharma A., and Rawat A.K. Toxicological consequences of chloroquine and ethanol on the developing fetus. Pharmacol. Biochem. Behav. 34 1 (1989) 77-82
41. Shultz V.D., Phillips S., Sar M., Foster P.M., and Gaido K.W. Altered gene profiles in fetal rat testes after in utero exposure to di(n-butyl) phthalate. Toxicol. Sci. 64 2 (2001) 233-242
42. Wang X., Walsh L.P., and Stocco D.M. The role of arachidonic acid on LH-stimulated steroidogenesis and steroidogenic acute regulatory protein accumulation in MA-10 mouse Leydig tumor cells. Endocrine 10 1 (1999) 7-12
43. Yamamoto A., Adachi S., Matsuzawa Y., Kitani T., Hiraoka A., and Seki K. Studies on drug-induced lipidosis: VII. Effects of bis-beta-diethyl-aminoethylether of hexestrol, chloroquine, homochlorocyclizine, prenylamine, and diazacholesterol on the lipid composition of rat liver and kidney. Lipids 11 8 (1976) 616-622
44. Zahid A., and Abidi T.S. Effect of chloroquine on liver weight of developing albino rats. J. Pak. Med. Assoc. 53 1 (2003) 21-23