CLC number: R71
On-line Access: 2013-05-04
Received: 2012-11-20
Revision Accepted: 2013-03-05
Crosschecked: 2013-04-15
Cited: 4
Clicked: 5808
Li-ya Wang, Ning Wang, Fang Le, Lei Li, Le-jun Li, Xiao-zhen Liu, Ying-ming Zheng, Hang-ying Lou, Xiang-rong Xu, Xiao-ming Zhu, Yi-min Zhu, He-feng Huang, Fan Jin. Persistence and intergenerational transmission of differentially expressed genes in the testes of intracytoplasmic sperm injection conceived mice[J]. Journal of Zhejiang University Science B, 2013, 14(5): 372-381.
@article{title="Persistence and intergenerational transmission of differentially expressed genes in the testes of intracytoplasmic sperm injection conceived mice",
author="Li-ya Wang, Ning Wang, Fang Le, Lei Li, Le-jun Li, Xiao-zhen Liu, Ying-ming Zheng, Hang-ying Lou, Xiang-rong Xu, Xiao-ming Zhu, Yi-min Zhu, He-feng Huang, Fan Jin",
journal="Journal of Zhejiang University Science B",
volume="14",
number="5",
pages="372-381",
year="2013",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1200321"
}
%0 Journal Article
%T Persistence and intergenerational transmission of differentially expressed genes in the testes of intracytoplasmic sperm injection conceived mice
%A Li-ya Wang
%A Ning Wang
%A Fang Le
%A Lei Li
%A Le-jun Li
%A Xiao-zhen Liu
%A Ying-ming Zheng
%A Hang-ying Lou
%A Xiang-rong Xu
%A Xiao-ming Zhu
%A Yi-min Zhu
%A He-feng Huang
%A Fan Jin
%J Journal of Zhejiang University SCIENCE B
%V 14
%N 5
%P 372-381
%@ 1673-1581
%D 2013
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1200321
TY - JOUR
T1 - Persistence and intergenerational transmission of differentially expressed genes in the testes of intracytoplasmic sperm injection conceived mice
A1 - Li-ya Wang
A1 - Ning Wang
A1 - Fang Le
A1 - Lei Li
A1 - Le-jun Li
A1 - Xiao-zhen Liu
A1 - Ying-ming Zheng
A1 - Hang-ying Lou
A1 - Xiang-rong Xu
A1 - Xiao-ming Zhu
A1 - Yi-min Zhu
A1 - He-feng Huang
A1 - Fan Jin
J0 - Journal of Zhejiang University Science B
VL - 14
IS - 5
SP - 372
EP - 381
%@ 1673-1581
Y1 - 2013
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1200321
Abstract: intracytoplasmic sperm injection (ICSI) is commonly used to solve male infertility problems. Previous studies showed that early environmental exposure of an embryo may influence postnatal development. To detect whether ICSI operations affect the reproductive health of a male or his offspring, we established assisted reproductive technologies (ART) conceived mouse models, and analyzed gene expression profiles in the testes of both ICSI and naturally conceived (NC) newborn F1 mice using micro-array analysis. Among the differentially expressed genes, we focused on the expression of eight male reproduction-related genes. Quantitative real-time reverse transcription-polymerase chain reaction (qRT-PCR) was used to analyze the expression of these genes in the testes of both adult and old F1 generation mice and adult F2 generation mice. Our results showed that down-regulated and somatic cell-expressed genes in newborn mice retained their differential expression patterns in adult and old F1 generation individuals, implying the persistence and fetal origin of the alteration in the expression of these genes. The intergenerational transmission of differential gene expression was observed, but most changes tended to be reduced in adult F2 generations. Controlled ovarian hyperstimulation (COH) and in vitro fertilization (IVF) mice models were added to explore the precise factors contributing to the differences in ICSI offspring. The data demonstrated that superovulation, in vitro culture, and mechanical stimulation involved in ICSI had a cumulative effect on the differential expression of these male reproductive genes.
[1]Abreu, A.P., Kaiser, U.B., Latronico, A.C., 2010. The role of prokineticins in the pathogenesis of hypogonadotropic hypogonadism. Neuroendocrinology, 91(4):283-290.
[2]Asklund, C., Jorgensen, N., Skakkebaek, N.E., Jensen, T.K., 2007. Increased frequency of reproductive health problems among fathers of boys with hypospadias. Hum. Reprod., 22(10):2639-2646.
[3]Barker, D.J., 1990. The fetal and infant origins of adult disease. BMJ, 301(6761):1111.
[4]Basciani, S., Mariani, S., Arizzi, M., Ulisse, S., Rucci, N., Jannini, E.A., Della Rocca, C., Manicone, A., Carani, C., Spera, G., et al., 2002. Expression of platelet-derived growth factor-A (PDGF-A), PDGF-B, and PDGF receptor-α and -β during human testicular development and disease. J. Clin. Endocrinol. Metab., 87(5):2310-2319.
[5]Basciani, S., Mariani, S., Spera, G., Gnessi, L., 2010. Role of platelet-derived growth factors in the testis. Endocr. Rev., 31(6):916-939.
[6]Bellani, M.A., Boateng, K.A., McLeod, D., Camerini-Otero, R.D., 2010. The expression profile of the major mouse SPO11 isoforms indicates that SPO11β introduces double strand breaks and suggests that SPO11α has an additional role in prophase in both spermatocytes and oocytes. Mol. Cell. Biol., 30(18):4391-4403.
[7]Boukari, K., Meduri, G., Brailly-Tabard, S., Guibourdenche, J., Ciampi, M.L., Massin, N., Martinerie, L., Picard, J.Y., Rey, R., Lombes, M., et al., 2009. Lack of androgen receptor expression in Sertoli cells accounts for the absence of anti-Mullerian hormone repression during early human testis development. J. Clin. Endocrinol. Metab., 94(5):1818-1825.
[8]Davies, M.J., Moore, V.M., Willson, K.J., van Essen, P., Priest, K., Scott, H., Haan, E.A., Chan, A., 2012. Reproductive technologies and the risk of birth defects. N. Engl. J. Med., 366(19):1803-1813.
[9]Denolet, E., de Gendt, K., Allemeersch, J., Engelen, K., Marchal, K., van Hummelen, P., Tan, K.A., Sharpe, R.M., Saunders, P.T., Swinnen, J.V., et al., 2006. The effect of a sertoli cell-selective knockout of the androgen receptor on testicular gene expression in prepubertal mice. Mol. Endocrinol., 20(2):321-334.
[10]Domanskyi, A., Zhang, F.P., Nurmio, M., Palvimo, J.J., Toppari, J., Janne, O.A., 2007. Expression and localization of androgen receptor-interacting protein-4 in the testis. Am. J. Physiol. Endocrinol. Metab., 292(2):E513-E522.
[11]Fatemi, N., Sanati, M.H., Zavarehei, M.J., Ayat, H., Esmaeili, V., Golkar-Narenji, A., Zarabi, M., Gourabi, H., 2012. Effect of tertiary-butyl hydroperoxide (TBHP)-induced oxidative stress on mice sperm quality and testis histopathology. Andrologia, in press.
[12]Fenichel, P., Rey, R., Poggioli, S., Donzeau, M., Chevallier, D., Pointis, G., 1999. Anti-Mullerian hormone as a seminal marker for spermatogenesis in non-obstructive azoospermia. Hum. Reprod., 14(8):2020-2024.
[13]Foix-L′Hélias, L., Aerts, I., Marchand, L., Lumbroso-le Rouic, L., Gauthier-Villars, M., Labrune, P., Bouyer, J., Doz, F., Kaminski, M., 2012. Are children born after infertility treatment at increased risk of retinoblastoma? Hum. Reprod., 27(7):2186-2192.
[14]Goulis, D.G., Iliadou, P.K., Tsametis, C., Gerou, S., Tarlatzis, B.C., Bontis, I.N., Papadimas, I., 2008. Serum anti-Mullerian hormone levels differentiate control from subfertile men but not men with different causes of subfertility. Gynecol. Endocrinol., 24(3):158-160.
[15]Hoile, S.P., Lillycrop, K.A., Thomas, N.A., Hanson, M.A., Burdge, G.C., 2011. Dietary protein restriction during F0 pregnancy in rats induces transgenerational changes in the hepatic transcriptome in female offspring. PLoS One, 6(7):e21668.
[16]Hu, Z., MacLean, J.A., Bhardwaj, A., Wilkinson, M.F., 2007. Regulation and function of the Rhox5 homeobox gene. Ann. N. Y. Acad. Sci., 1120(1):72-83.
[17]Jamen, F., Rodriguez-Henche, N., Pralong, F., Jegou, B., Gaillard, R., Bockaert, J., Brabet, P., 2000. PAC1 null females display decreased fertility. Ann. N. Y. Acad. Sci., 921(1):400-404.
[18]Jimenez-Chillaron, J.C., Isganaitis, E., Charalambous, M., Gesta, S., Pentinat-Pelegrin, T., Faucette, R.R., Otis, J.P., Chow, A., Diaz, R., Ferguson-Smith, A., et al., 2009. Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes, 58(2):460-468.
[19]Koh, P.O., Won, C.K., 2006. Decrease of pituitary adenylate cyclase activating polypeptide and its type I receptor mRNAs in rat testes by ethanol exposure. J. Vet. Med. Sci., 68(6):537-541.
[20]Lee, J., Yokota, T., Yamashita, M., 2002. Analyses of mRNA expression patterns of cohesin subunits Rad21 and Rec8 in mice: germ cell-specific expression of Rec8 mRNA in both male and female mice. Zoolog. Sci., 19(5):539-544.
[21]Lonergan, P., Fair, T., Corcoran, D., Evans, A.C., 2006. Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos. Theriogenology, 65(1):137-152.
[22]Lu, Y.H., Gao, H.J., Li, B.J., Zheng, Y.M., Ye, Y.H., Qian, Y.L., Xu, C.M., Huang, H.F., Jin, F., 2012. Different sperm sources and parameters can influence intracytoplasmic sperm injection outcomes before embryo implantation. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 13(1):1-10.
[23]Mau, C., Juul, A., Main, K.M., Loft, A., 2004. Children conceived after intracytoplasmic sperm injection (ICSI): is there a role for the paediatrician? Acta Paediatr., 93(9):1238-1244.
[24]Mau Kai, C., Main, K.M., Andersen, A.N., Loft, A., Skakkebaek, N.E., Juul, A., 2007. Reduced serum testosterone levels in infant boys conceived by intracytoplasmic sperm injection. J. Clin. Endocrinol. Metab., 92(7):2598-2603.
[25]Nurmio, M., Kallio, J., Toppari, J., Jahnukainen, K., 2008. Adult reproductive functions after early postnatal inhibition by imatinib of the two receptor tyrosine kinases, c-kit and PDGFR, in the rat testis. Reprod. Toxicol., 25(4):442-446.
[26]Prader, A., Tanner, J.M., von Harnack, G.A., 1963. Catch-up growth following illness or starvation: an example of developmental canalization in man. J. Pediatr., 62(5):646-659.
[27]Puverel, S., Barrick, C., Dolci, S., Coppola, V., Tessarollo, L., 2011. RanBPM is essential for mouse spermatogenesis and oogenesis. Development, 138(12):2511-2521.
[28]Ramlau-Hansen, C.H., Thulstrup, A.M., Olsen, J., Bonde, J.P., 2008. Parental subfecundity and risk of decreased semen quality in the male offspring: a follow-up study. Am. J. Epidemiol., 167(12):1458-1464.
[29]Rey, R., Lordereau-Richard, I., Carel, J.C., Barbet, P., Cate, R.L., Roger, M., Chaussain, J.L., Josso, N., 1993. Anti-mullerian hormone and testosterone serum levels are inversely during normal and precocious pubertal development. J. Clin. Endocrinol. Metab., 77(5):1220-1226.
[30]Rinaudo, P., Schultz, R.M., 2004. Effects of embryo culture on global pattern of gene expression in preimplantation mouse embryos. Reproduction, 128(3):301-311.
[31]Roseboom, T., de Rooij, S., Painter, R., 2006. The Dutch famine and its long-term consequences for adult health. Early Hum. Dev., 82(8):485-491.
[32]Schmahl, J., Rizzolo, K., Soriano, P., 2008. The PDGF signaling pathway controls multiple steroid-producing lineages. Genes Dev., 22(23):3255-3267.
[33]Storgaard, L., Bonde, J.P., Ernst, E., Andersen, C.Y., Spano, M., Christensen, K., Petersen, H.C., Olsen, J., 2006. Genetic and environmental correlates of semen quality: a twin study. Epidemiology, 17(6):674-681.
[34]Tsai-Morris, C.H., Sato, H., Gutti, R., Dufau, M.L., 2012. Role of gonadotropin regulated testicular RNA helicase (GRTH/Ddx25) on polysomal associated mRNAs in mouse testis. PLoS One, 7(3):e32470.
[35]van Abeelen, A.F., Elias, S.G., Bossuyt, P.M., Grobbee, D.E., van der Schouw, Y.T., Roseboom, T.J., Uiterwaal, C.S., 2012. Famine exposure in the young and the risk of type 2 diabetes in adulthood. Diabetes, 61(9):2255-2260.
[36]Wang, N., Wang, L., Le, F., Zhan, Q., Zheng, Y., Ding, G., Chen, X., Sheng, J., Dong, M., Huang, H., et al., 2011. Altered expression of Armet and Mrlp51 in the oocyte, preimplantation embryo, and brain of mice following oocyte in vitro maturation but postnatal brain development and cognitive function are normal. Reproduction, 142(3):401-408.
[37]Yu, Y., Zhao, C., Lv, Z., Chen, W., Tong, M., Guo, X., Wang, L., Liu, J., Zhou, Z., Zhu, H., et al., 2011. Microinjection manipulation resulted in the increased apoptosis of spermatocytes in testes from intracytoplasmic sperm injection (ICSI) derived mice. PLoS One, 6(7):e22172.
Open peer comments: Debate/Discuss/Question/Opinion
<1>