Maternal LPS exposure during pregnancy impairs testicular development, steroidogenesis and spermatogenesis in male offspring

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Wang, Hua ^a,b   Yang, Lu Lu ^a   Hu, Yong Fang ^a   Wang, Bi Wei ^a   Huang, Yin Yin ^a   Zhang, Cheng ^a,b   Chen, Yuan Hua ^a,b   Xu, De Xiang ^a,b  

^a ANHUI MEDICAL UNIVERSITY   (China)

^b ANHUI PROVINCIAL KEY LABORATORY OF POPULATION HEALTH AND ARISTOGENICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; LIPOPOLYSACCHARIDE; TESTOSTERONE; LUTEINIZING HORMONE; STEROID;

ADULT; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOGENITAL DISTANCE; ARTICLE; CELL AGGREGATION; CONTROLLED STUDY; FEMALE; FETUS; FETUS DEVELOPMENT; GERM CELL; GESTATION PERIOD; LEYDIG CELL; MALE; MOUSE; NONHUMAN; PERINATAL PERIOD; PREGNANCY; PROGENY; PROSTATE WEIGHT; SEMINAL VESICLE; SEMINIFEROUS TUBULE; SPERMATOGENESIS; SPERMATOZOON COUNT; STEROIDOGENESIS; TESTIS DEVELOPMENT; TESTIS WEIGHT; TESTOSTERONE BLOOD LEVEL; TESTOSTERONE SYNTHESIS; WEIGHT REDUCTION; ADVERSE EFFECTS; ANIMAL; BIOSYNTHESIS; BLOOD; BODY WEIGHT; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; ENVIRONMENTAL EXPOSURE; GROWTH, DEVELOPMENT AND AGING; ORGAN SIZE; PATHOLOGY; PRENATAL EXPOSURE; PROSTATE; SPERMATOZOON; TESTIS;

ANIMALS; BODY WEIGHT; FEMALE; FETUS; LEYDIG CELLS; LIPOPOLYSACCHARIDES; LUTEINIZING HORMONE; MALE; MATERNAL EXPOSURE; MICE; ORGAN SIZE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROSTATE; SEMINAL VESICLES; SPERM COUNT; SPERMATOGENESIS; SPERMATOZOA; STEROIDS; TESTIS; TESTOSTERONE;

EID: 84907463603     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106786     Document Type: Article

References (42)

1. Adachi Y, Moore LE, Bradford BU, Gao W, Thurman RG (1995) Antibiotics prevent liver injury in rats following long-term exposure to ethanol. Gastroenterology 108: 218-224.
2. Hurley JC (1994) Concordance of endotoxemia with gram-negative bacteremia in patients with gram-negative sepsis: a meta-analysis. J Clin Microbiol 32: 2120-2127.
3. Platz-Christensen JJ, Mattsby-Baltzer I, Thomsen P, Wiqvist N (1993) Endotoxin and interleukin-1 alpha in the cervical mucus and vaginal fluid of pregnant women with bacterial vaginosis. Am J Obstet Gynecol 169: 1161-1166.
4. Romero R, Roslansky P, Oyarzun E, Wan M, Emamian M, et al. (1988) Labor and infection. II. Bacterial endotoxin in amniotic fluid and its relationship to the onset of preterm labor. Am J Obstet Gynecol 158: 1044-1049.
5. Hazan Y, Mazor M, Horowitz S, Leiberman JR, Glezerman M (1995) The diagnostic value of amniotic fluid Gram stain examination and limulus amebocyte lysate assay in patients with preterm birth. Acta Obstet Gynecol Scand 74: 275-280.
6. Aisemberg J, Vercelli C, Billi S, Ribeiro ML, Ogando D, et al. (2007) Nitric oxide mediates prostaglandins' deleterious effect on lipopolysaccharide-triggered murine fetal resorption. Proc Natl Acad Sci U S A 104: 7534-7539.
7. Ogando DG, Paz D, Cella M, Franchi AM (2003) The fundamental role of increased production of nitric oxide in lipopolysaccharide-induced embryonic resorption in mice. Reproduction 125: 95-110.
8. Leazer TM, Barbee B, Ebron-McCoy M, Henry-Sam GA, Rogers JM (2002) Role of the maternal acute phase response and tumor necrosis factor alpha in the developmental toxicity of lipopolysaccharide in the CD-1 mouse. Reprod Toxicol 16: 173-179.
9. Xu DX, Chen YH, Wang H, Zhao L, Wang JP, et al. (2005) Effect of N-acetylcysteine on lipopolysaccharide-induced intra-uterine fetal death and intra-uterine growth retardation in mice. Toxicol Sci 88: 525-533.
10. Xu DX, Chen YH, Zhao L, Wang H, Wei W (2006) Reactive oxygen species are involved in lipopolysaccharide-induced intrauterine growth restriction and skeletal development retardation in mice. Am J Obstet Gynecol 195: 1707-1714.
11. Xu DX, Wang H, Zhao L, Ning H, Chen YH, et al. (2007) Effects of low-dose lipopolysaccharide (LPS) pretreatment on LPS-induced intra-uterine fetal death and preterm labor. Toxicology 234: 167-175.
12. Zhao M, Chen YH, Dong XT, Zhou J, Chen X, et al. (2013) Folic acid protects against lipopolysaccharide-induced preterm delivery and intrauterine growth restriction through its anti-inflammatory effect in mice. PLoS One 8: e82713.
13. Chen YH, Zhao M, Chen X, Zhang Y, Wang H, et al. (2012) Zinc supplementation during pregnancy protects against lipopolysaccharide-induced fetal growth restriction and demise through its anti-inflammatory effect. J Immunol 189: 454-463.
14. Ornoy A, Altshuler G (1976) Maternal endotoxemia, fetal anomalies, and central nervous system damage: a rat model of a human problem. Am J Obstet Gynecol 124: 196-204.
15. Zhao L, Chen YH, Wang H, Ji YL, Ning H, et al. (2008) Reactive oxygen species contribute to lipopolysaccharide-induced teratogenesis in mice. Toxicol Sci 103: 149-157.
16. Zhao M, Chen YH, Chen X, Dong XT, Zhou J, et al. (2014) Folic acid supplementation during pregnancy protects against lipopolysaccharide-induced neural tube defects in mice. Toxicol Lett 224: 201-208.
17. Collins JG, Smith MA, Arnold RR, Offenbacher S (1994) Effects of Escherichia coli and Porphyromonas gingivalis lipopolysaccharide on pregnancy outcome in the golden hamster. Infect Immun 62: 4652-4655.
18. Boksa P (2010) Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav Immun 24: 881-897.
19. Romero E, Guaza C, Castellano B, Borrell J (2010) Ontogeny of sensorimotor gating and immune impairment induced by prenatal immune challenge in rats: implications for the etiopathology of schizophrenia. Mol Psychiatry 15: 372-383.
20. Wang H, Meng XH, Ning H, Zhao XF, Wang Q, et al. (2010) Age- and gender-dependent impairments of neurobehaviors in mice whose mothers were exposed to lipopolysaccharide during pregnancy. Toxicol Lett 192: 245-251.
21. Chen GH, Wang H, Yang QG, Tao F, Wang C, et al. (2011) Acceleration of age-related learning and memory decline in middle-aged CD-1 mice due to maternal exposure to lipopolysaccharide during late pregnancy. Behav Brain Res 218: 267-279.
22. Hurley JC (2010) Does gram-negative bacteraemia occur without endotoxae-mia? A meta-analysis using hierarchical summary ROC curves. Eur J Clin Microbiol Infect Dis 29: 207-215.
23. Mahood IK, Scott HM, Brown R, Hallmark N, Walker M, et al. (2007) In utero exposure to di(n-butyl) phthalate and testicular dysgenesis: comparison of fetal and adult end points and their dose sensitivity. Environ Health Perspect 115 Suppl 1: 55-61.
24. Reddy MM, Mahipal SV, Subhashini J, Reddy MC, Roy KR, et al. (2006) Bacterial lipopolysaccharide-induced oxidative stress in the impairment of steroidogenesis and spermatogenesis in rats. Reprod Toxicol 22: 493-500.
25. Liew SH, Meachem SJ, Hedger MP (2007) A stereological analysis of the response of spermatogenesis to an acute inflammatory episode in adult rats. J Androl 28: 176-185.
26. O'Bryan MK, Schlatt S, Phillips DJ, de Kretser DM, Hedger MP (2000) Bacterial lipopolysaccharide-induced inflammation compromises testicular function at multiple levels in vivo. Endocrinology 141: 238-246.
27. Walker AK, Hiles SA, Sominsky L, McLaughlin EA, Hodgson DM (2011) Neonatal lipopolysaccharide exposure impairs sexual development and reproductive success in the Wistar rat. Brain Behav Immun 25: 674-684.
28. Smith LB, Walker WH (2014) The regulation of spermatogenesis by androgens. Semin Cell Dev Biol 30C: 2-13.
29. Joensen UN, Jorgensen N, Rajpert-De Meyts E, Skakkebaek NE (2008) Testicular dysgenesis syndrome and Leydig cell function. Basic Clin Pharmacol Toxicol 102: 155-161.
30. Chang C, Lee SO, Wang RS, Yeh S, Chang TM (2013) Androgen receptor (AR) physiological roles in male and female reproductive systems: lessons learned from AR-knockout mice lacking AR in selective cells. Biol Reprod 89: 21.
31. Xu Q, Lin HY, Yeh SD, Yu IC, Wang RS, et al. (2007) Infertility with defective spermatogenesis and steroidogenesis in male mice lacking androgen receptor in Leydig cells. Endocrine 32: 96-106.
32. Chang C, Chen YT, Yeh SD, Xu Q, Wang RS, et al. (2004) Infertility with defective spermatogenesis and hypotestosteronemia in male mice lacking the androgen receptor in Sertoli cells. Proc Natl Acad Sci U S A 101: 6876-6881.
33. Bosmann HB, Hales KH, Li X, Liu Z, Stocco DM, et al. (1996) Acute in vivo inhibition of testosterone by endotoxin parallels loss of steroidogenic acute regulatory (StAR) protein in Leydig cells. Endocrinology 137: 4522-4525.
34. Biswas B, Yenugu S (2011) Antimicrobial responses in the male reproductive tract of lipopolysaccharide challenged rats. Am J Reprod Immunol 65: 557-568.
35. Haider SG (2004) Cell biology of Leydig cells in the testis. Int Rev Cytol 233: 181-241.
36. Mendis-Handagama SM, Ariyaratne HB (2001) Differentiation of the adult Leydig cell population in the postnatal testis. Biol Reprod 65: 660-671.
37. Mahood IK, Hallmark N, McKinnell C, Walker M, Fisher JS, et al. (2005) Abnormal Leydig Cell aggregation in the fetal testis of rats exposed to di (n-butyl) phthalate and its possible role in testicular dysgenesis. Endocrinology 146: 613-623.
38. Gow RM, O'Bryan MK, Canny BJ, Ooi GT, Hedger MP (2001) Differential effects of dexamethasone treatment on lipopolysaccharide-induced testicular inflammation and reproductive hormone inhibition in adult rats. J Endocrinol 168: 193-201.
39. Iwasa T, Matsuzaki T, Murakami M, Kinouchi R, Ogata R, et al. (2009) Neonatal lipopolysaccharide exposure attenuates the homotypic stress-induced suppression of LH secretion in adulthood in male rat. Int J Dev Neurosci 27: 345-349.
40. Fisch H, Braun SR (2013) Trends in global semen parameter values. Asian J Androl 15: 169-173.
41. Jurewicz J, Radwan M, Merecz-Kot D, Sobala W, Ligocka D, et al. (2014) Occupational, life stress and family functioning: does it affect semen quality? Ann Hum Biol 41: 220-228.
42. Bonde JP, Giwercman A (2014) Environmental xenobiotics and male reproductive health. Asian J Androl 16: 3-4.