Suppression of spermatogenesis by bisdichloroacetyldiamines is mediated by inhibition of testicular retinoic acid biosynthesis

Journal of Andrology

Volumn 32, Issue 1, 2011, Pages 111-119

  Amory, John K ^a   Muller, Charles H ^b   Shimshoni, Jakob A ^a   Isoherranen, Nina ^a   Paik, Jisun ^a   Moreb, Jan S ^c   Amory Sr , David W ^a   Evanoff, Ryan ^d   Goldstein, Alex S ^e   Griswold, Michael D ^d  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d WASHINGTON STATE UNIVERSITY   (United States)

^e Focused Scientific   (United States)

Author keywords

Male contraception; Retinol; Sperm concentration; Vitamin A

Indexed keywords

ALDEHYDE DEHYDROGENASE; DIAMINE DERIVATIVE; FERTILYSIN; MALE CONTRACEPTIVE AGENT; RETINOIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CELL LOSS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GERM CELL; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; IN VIVO STUDY; MALE; MALE FERTILITY; MALE INFERTILITY; NONHUMAN; PRIORITY JOURNAL; RABBIT; SPERMATOGENESIS; SPERMATOZOON COUNT; TESTIS;

ANIMALS; CONTRACEPTIVE AGENTS, MALE; DIAMINES; MALE; RABBITS; RETINAL DEHYDROGENASE; SPERMATOGENESIS; TESTIS; TRETINOIN;

EID: 79251490725     PISSN: 01963635     EISSN: 19394640     Source Type: Journal    
DOI: 10.2164/jandrol.110.010751     Document Type: Article

References (47)

1. Amann RP. Detection of alterations in testicular and epididymal function in laboratory animals. Environ Health Perspect. 1986;70:149-158.
2. Asa C, Zaneveld LJD, Munson L, Callahan M, Byers AP. Efficacy, safety and reversibility of a bisdiamine male-directed oral contraceptive in grey wolves (Canis lupus). J Zoo Wildl Med. 1996;27:501-506. (Pubitemid 126674067)
3. Berberian DA, Slighter RG, Surrey AR. In vitro and in vivo amebicidal activity of N, N′Bis(dichloroacetyl)diamines. Antibiot Chemother. 1961;11:245-255.
4. Beyler AL, Potts GO, Coulston F, Surrey AR. The selective testicular effects of certain bis-(dichloroacetyl) diamines. Endocrinology. 1961;69:819-833.
5. Bishop PD, Griswold MD. Uptake and metabolism of retinol in cultured Sertoli cells: evidence for a kinetic model. Biochemistry. 1987;26:7511-7518.
6. Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, Yashiro K, Chawengsaksophak K, Wilson MJ, Rossant J, Hamada H, Koopman P. Retinoic signaling determines cell fate in mice. Science. 2006;312:596-600.
7. Choy M, Oltjen SL, Moon AJ, Armstrong MT, Armstrong PB. Bisdiamine inhibits extracellular matrix formation and cell proliferation of atrioventricular mesenchyme from developing chick heart valves. Teratology. 1999;59:148-155. (Pubitemid 29158611)
8. Chung SS, Choi C, Wang X, Hallock L, Wolgemuth DJ. Aberrant distribution of junctional complex components in retinoic acid receptor alpha-deficient mice. Micro Res Tech. 2010;73: 583-596.
9. Chung SS, Sung W, Wang X, Wolgemuth DJ. Retinoic acid receptor alpha is required for synchronization of spermatogenic cycles and its absence results in progressive breakdown of the spermatogenic process. Dev Dyn. 2004;230:754-766. (Pubitemid 38993874)
10. Coulston F, Beyler AL, Drobeck HP. The biologic actions of a new series of bis(dichloroacetyl)diamines. Toxicol Appl Pharmacol. 1960;2:715-721.
11. Deitrich RA, Petersen D, Vasiliou V. Removal of acetaldehyde from the body. Novartis Found Symp. 2007;285:23-40.
12. Department of Economic and Social Affairs of the United Nations Secretariat. World population prospects: the 2008 revision. http://esa.un.org/ unpp. Accessed February 24, 2010.
13. Foote RH, Carney EW. The rabbit as a model for reproductive and developmental toxicity studies. Reprod Toxicol. 2000;14:477-493.
14. Ghyselinck NB, Vernet N, Dennefeld C, Giese N, Nau H, Chambon P, Viville S, Mark M. Retinoids and spermatogenesis: lessons from mutant mice lacking the plasma retinol binding protein. Dev Dyn. 2006;235:1608-1622. (Pubitemid 43787963)
15. Goyal HO, Hutto V, Maloney MA. Effects of androgen deprivation in the goat epididymis. Acta Anat. 1994;150:127-135. (Pubitemid 24256947)
16. Heilig M, Egli M. Pharmacological treatment of alcohol dependence: target symptoms and target mechanisms. Pharmacol Ther. 2006;111:855-876. (Pubitemid 44118437)
17. Heller CG, Flageolle BY, Matson LJ. Histopathology of the human testes as affected by Bis (dichloroacetyl) diamines. Exp Mol Pathol. 1963;2:107-114.
18. Heller CG, Moore DJ, Paulsen CA. Suppression of spermatogenesis and chronic toxicity in men by a new series of bis (dichloroacetyl) diamines. Toxicol Appl Pharmacol. 1961;3:1-11.
19. Henshaw SK. Unintended pregnancy in the US. Fam Plann Perspect. 1998;30:24-29.
20. Kane MA, Chen N, Sparks S, Napoli JL. Quantification of endogenous retinoic acid in limited biological samples by LC/MS/MS. Biochem J. 2005;388:363-369.
21. Kastner P,Mark M, Leid M, Gansmuller A, Chin W, Grondona JM, Décimo D, Krezel W, Dierich A, Chambon P. Abnormal spermatogenesis in RXR beta mutant mice. Genes Dev. 1996;10:80-92.
22. Kurlandsky SB, Gamble MV, Ramakirshnan R, Blaner WS. Plasma delivery of retinoic acid to tissues in the rat. J Biol Chem. 1995;270:17850-17857.
23. Lohnes D, Kastner P, Dierich A, Mark M, LeMeur M, Chambon P. Function of retinoic acid receptor gamma in the mouse. Cell. 1993;73:643-658.
24. Lufkin T, Lohnes D, Mark M, Dierich A, Gorry P, Gaub MP, LeMeur M, Chambon P. High postnatal lethality and testis degeneration in retinoic acid receptor alpha mutant mice. Proc Natl Acad Sci U S A. 1993;90:7225-7229.
25. Marchitti SA, Brocker C, Stagos D, Vasiliou V. Non-P450 aldehyde oxidizing enzymes: the aldehyde dehydrogenase superfamily. Expert Opin Drug Metab Toxicol. 2008;4:697-720.
26. Moreb JS, Zucali JR, Ostmark B, Benson NA. Heterogeneity of aldehyde dehydrogenase expression in lung cancer cell lines is revealed by Aldefluor flow cytometry-based assay. Cytometry B. 2002;72:281-289.
27. Munson L, Chassy LM, Asa C. Efficacy, safety and reversibility of bisdiamine as a male contraceptive in cats. Theriogenology. 2004;62:81-92. (Pubitemid 38722357)
28. Napoli J. Retinoic acid: its biosynthesis and metabolism. In: Moldave K, ed. Progress in Nucleic Acid Research and Molecular Biology. San Diego, CA: Academic Press; 2000:139-188.
29. Nau H. Teratogenicity of isotretinoin revisited: species variation and the role of all-trans-retinoic acid. J Am Acad Dermatol. 2001;45: S183-S187.
30. Naughton CK, Nelson DR, Thomas AJ. Development of an inexpensive artificial vagina for semen collection from rabbits. J Androl. 2003;24:712-715.
31. Page ST, Kalhorn TF, Bremner WJ, Anawalt BD, Matsumoto AM, Amory JK. Intratesticular androgens and spermatogenesis during severe gonadotropin suppression induced by male hormonal contraceptive treatment. J Androl. 2007;28:734-741.
32. Paik J, Blaner WS, Swisshelm K. Cis-retinol dehydrogenase: 9-cisretinol metabolism and its effect on proliferation of human MCF7 breast cancer cells. Exp. Cell Res. 2005;303:183-196.
33. Paik J, Vogel S, Quadro L, Piantedosi R, Gottesman M, Lai K, Hamberger L, Vieria MM, Blaner WS. Vitamin A: overlapping delivery pathways to tissues from the circulation. J Nutr. 2004;134: S276-S280.
34. Pellegrini M, Filippani D, Gori M, Barrios F, Lolicato F, Grimaldi P, Rossi P, Jannini EA, Geremia R, Dolci S. ATRA and KL promote differentiation toward the meiotic program of male germ cells. Cell Cycle. 2008;7:3878-3888.
35. Schulze GE, Clay RJ, Mezza LE, Bregman CL, Buroker RA, Frantz JD. BMS-189453, a novel retinoid receptor antagonist, is a potent testicular toxin. Toxicol Sci. 2001;59:297-308.
36. Seed J, Chapin RE, Clegg ED, Dostal LA, Foote RH, Hurtt ME, Klinefelter GR, Makris SL, Perreault SD, Schrader S, Seyler D, Sprando R, Treinen KA, Veeramachaneni DN, Wise LD. Methods for assessing spermmotility, morphology, and counts in the rat, rabbit and dog: A consensus report. Reprod Toxicol. 1996;10:237-244.
37. Singh SK, Dominic CJ. Effect of N′N′-bis(dichloroacetyl)-1,8- octamethylenediamine (WIN 18,446) on the testis and epididymis of the musk shrew (Suncus murinus). Indian J Exp Biol. 1980;18:1217-1220.
38. Steward MJ, Malek K, Crabb DW. Distribution of messenger RNAs for aldehyde dehydrogenase 1, aldehyde dehydrogenase 2, and aldehyde dehydrogenase 5 in human tissues. J Investig Med. 1996;44:42-46. (Pubitemid 126820662)
39. Suh JJ, Pettinati HM, Kampman KM, O'Brien CP. The status of disulfiram: a half a century later. J Clin Psychopharmacol. 2006;26:290-302.
40. Tasaka H, Takenaka H, Okamoto N, Onitsuka T, Koga Y, Hamada M. Abnormal development of cardiovascular systems in rat embryos treated with bisdiamine. Teratology. 1991;43:191-200.
41. Vernet N, Dennefeld C, Guillou F, Chambon P, Ghyselinck NB, Mark M. Prepuberal testis development relies on retinoic acid but not rexinoid receptors in Sertoli cells. EMBO J. 2006a;25:5816-5825.
42. Vernet N, Dennefeld C, Rochett-Egly C, Oulad-Abdelghani M, Chambon P, Ghyselinck NB, Mark M. Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocrinology. 2006b;147:96-110.
43. Wang X, Penzes P, Napoli J. Cloning of a cDNA encoding an aldehyde dehydrogenase and its expression in Escherichia coli. J Biol Chem. 1996;27:16288-16293.
44. Wolbach SB, Howe PR. Tissue changes following deprivation of fat soluble A vitamin. J Exp Med. 1925;42:753-777.
45. Wu FC, Farley TM, Peregoudov A, Waites GM. Effects of testosterone enanthate in normal men: experience from a multicenter contraceptive efficacy study. World Health Organization Task Force on Methods for the Regulation of Male Fertility. Fertil Steril. 1996;65:626-636.
46. Zaiss AK, Son S, Chang LJ. RNA 3′ readthrough of oncoretrovirus and lentivirus: implications for vector safety and efficacy. J Virol. 2002;76:7209-7219.
47. Zhou Q, Li Y, Nie R, Friel P, Metchell D, Evanoff RM, Pouchnik D, Banasik B, McCarrey JR, Small C, Griswold MD. Expression of stimulated by retinoic acid gene 8 (Stra8) and maturation of murine gonocytes and spermatogonia induced by retinoic acid in vitro. Biol Reprod. 2008;78:537-545. (Pubitemid 351416482)