nach oben

Journal of Assisted Reproduction and Genetics

Erschienen in:

01.05.2015 | Reproductive Physiology and Disease

Scrotal heat stress causes sperm chromatin damage and cysteinyl aspartate-spicific proteinases 3 changes in fertile men

verfasst von: Mei-Hua Zhang, Zhi-Da Shi, Jian-Chun Yu, Yan-Ping Zhang, Lei-Guang Wang, Yi Qiu

Erschienen in: Journal of Assisted Reproduction and Genetics | Ausgabe 5/2015

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To observe changes in semen parameters, sperm DNA integrity, chromatin condensation and cysteinyl aspartate-spicific proteinases (Caspase-3) in adult healthy men after scrotal heat stress (SHS).

Methods

The scrotums of 19 healthy male volunteers were exposed to the condition of 40–43 °C SHS belt warming 40 min each day for successive 2 days per week. The course of SHS was continuously 3 months. Routine semen analysis, hypo-osmotic swelling (HOS) test, eosin Y (EY) staining sperm HOS and chromatin dispersion (HOS/SCD) test, HOS and aniline blue (HOS/AB) staining test were carried out before, during and after SHS. The activated Caspase 3 levels of spermatozoa were determined with a microtiter plate reader.

Results

The mean parameters of sperm concentration, motility and normal morphological sperm were significantly decreased in groups with sperm being collected during SHS 1, 2 and 3 months when compared with those in groups of pre-SHS (P < 0.01). Statistically significant differences of sperm DNA fragmentation, normal sperm membrane and vitality, and Caspase-3 activity were observed between the groups of before SHS and after SHS 3 months and the groups of during SHS 1, 2 and 3 months (P < 0.001). Three months the SHS stopped, various parameters recovered to the level before SHS. Abnormal sperm with HOS/AB and HOS/SCD showed a negatively significant correlation with normal sperm by HOS/EY test, and WBC in semen showed a positively significant correlation with Caspase-3 activity. The percentage of abnormal sperm by using the test of HOS/SCD showed a positively significant correlation with that of HOS/AB.

Conclusions

The continuously constant SHS can impact the semen quality, sperm DNA integrity, chromatin condensation and Caspase-3, and the combination of HOS plus AB test may simultaneously determine the integrity of membrane and chromatin condensation at the same spermatozoon.

Paul C, Murray AA, Spears N, Saunders PT. A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reproduction. 2008;136:73–84.CrossRefPubMed

Banks S, King SA, Irvine DS, Saunders PT. Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa. Reproduction. 2005;129:505–14.CrossRefPubMed

Liu YX. Control of spermatogenesis in primate and prospect of male contraception. Arch Androl. 2005;51:77–92.CrossRefPubMed

Garolla A, Torino M, Sartini B, Cosci I, Patassini C, Carraro U, et al. Seminal and molecular evidence that sauna exposure affects human spermatogenesis. Hum Reprod. 2013;28:877–85.CrossRefPubMed

Shrivastava V, Pekar M, Grosser E, Im J, Vigodner M. SUMO proteins are involved in the stress response during spermatogenesis and are localized to DNA double-strand breaks in germ cells. Reproduction. 2010;139:999–1010.CrossRefPubMed

Li XX, Chen SR, Shen B, Yang JL, Ji SY, Wen Q, et al. The Heat-Induced Reversible Change in the blood-testis barrier (BTB) is regulated by the androgen receptor (AR) via the partitioning-defective protein (Par) polarity complex in the mouse. Biol Reprod. 2013;89:1–10.CrossRef

Sakkas D, Mariethoz E, St John JC. Abnormal sperm parameters in humans are indicative of an abortive apoptotic mechanism linked to the Fas mediated pathway. Exp Cell Res. 1999;251:350–5.CrossRefPubMed

Shen HM, Dai J, Chia SE, Lim A, Ong CN. Detection of apoptotic alterations in sperm in subfertile patients and their correlations with sperm quality. Hum Reprod. 2002;17:1266–73.CrossRefPubMed

Love CC, Kenney RM. Scrotal heat stress induces altered sperm chromatin structure associated with a decrease in protamine disulfide bonding in the stallion. Biol Reprod. 1999;60(3):615–20.CrossRefPubMed

10.

Karabinus DS, Vogler CJ, Saacke RG, Evenson DP. Chromatin structural changes in sperm after scrotal insulation of Holstein bulls. J Androl. 1997;18(5):549–55.PubMed

11.

Wang C, Cui YG, Wang XH, Jia Y, et al. Transient scrotal hyperthermia and levonorgestrel enhance testosterone-induced spermatogenesis suppression in men through increased germ cell apoptosis. J Clin Endocrinol Metab. 2007;92(8):3292–304.CrossRefPubMed

12.

Qiu Y, Wang LG, Jia YF, Yang DT, Zhang MH, Zhang YP, et al. The effects of the extract of Chinese Polygala tennuidolia willd on human sperm in vitro. J Zhejiang Univ Sci B. 2011;12:448–54.CrossRefPubMedCentralPubMed

13.

Qiu Y, Wang LG, Zhang LH, Li J, Zhang AD, Zhang MH. Sperm chromosomal aneuploidy and DNA integrity of infertile men with anejaculation. J Assist Reprod Genet. 2012;29:185–94.CrossRefPubMedCentralPubMed

14.

Qiu Y, Wang LG, Zhang LH, Zhang AD. Quality of sperm obtained by penile vibratory bratory stimulation and percutaneous vasal sperm aspiration in men with spinal cord injury. J Androl. 2012;33:1036–46.CrossRefPubMed

15.

Zhang LH, Qiu Y, Wang KH, Wang Q, Tao G, Wang LG. Measurement of sperm DNA fragmentation using bright-field microscopy: comparison between sperm chromatin dispersion test and terminal uridine nick-end labeling assay. Fertil Steril. 2010;94:102732.

16.

Fariello RM, Del Giudice PT, Spaine DM, Fraietta R, Bertolla RP, Cedenho AP. Effect of leukocytospermia and processing by discontinuous density gradient on sperm nuclear DNA fragmentation and mitochondrial activity. J Assist Reprod Genet. 2009;26:151–7.CrossRefPubMedCentralPubMed

17.

Liu DY, Baker HW. Human sperm bound to the zona pellucida have normal nuclear chromatin as assessed by acridine orange fluorescence. Hum Reprod. 2007;22:1597–602.CrossRefPubMed

18.

Fernández JL, Muriel L, Rivero MT, Goyanes V, Vazquez R, Alvarez JG. The sperm chromatin dispersion test: a simple method for the determination of sperm DNA fragmentation. J Androl. 2003;24:59–66.PubMed

19.

Fernández JL, Muriel L, Goyanes V, Segrelles E, Gosálvez J, Enciso M, et al. Simple determination of human sperm DNA fragmentation with an improved sperm chromatin dispersion test. Fertil Steril. 2005;84:833–42.CrossRefPubMed

20.

Evenson DP, Darzynkiewicz Z, Melamed MR. Relation of mammalian sperm chromatin heterogeneity to fertility. Science. 1980;210:1131.CrossRefPubMed

21.

Paasch U, Grunewald S, Fitzl G, Glander HJ. Deterioration of plasma membrane is associated with activation of caspases in human spermatozoa. J Androl. 2003;24:246–52.PubMed

22.

Faleiro L, Lazebnik Y. Caspases disrupt the nuclear-cytoplasmic barrier. J Cell Biol. 2000;151:951–9.CrossRefPubMedCentralPubMed

23.

Beyret E, Lin H. Pinpointing the expression of piRNAs and function of the PIWI protein subfamily during spermatogenesis in the mouse. Dev Biol. 2011;14215–26.

24.

World Health Organisation. Laboratory manual for the examination of human semen and sperm-cervical mucus interaction. 4th ed. New York: Cambridge University Press; 1999.

25.

World Health Organisation 2010 WHO laboratory manual for the Examination and processing of human semen. 5th ed. WHO Press, Prepublication version. p30–32.

26.

Sellami A, Chakroun N, Ben Zarrouk S, Sellami H, Kebaili S, Rebai T, et al. Assessment of chromatin maturity in human spermatozoa: useful aniline blue assay for routine diagnosis of male infertility. Adv Urol. 2013;578–631.

27.

Alkhayal A, San Gabriel M, Zeidan K, Alrabeeah K, Noel D, McGraw R, et al. Sperm DNA and chromatin integrity in semen samples used for intrauterine insemination. J Assist Reprod Genet. 2013;30:1519–24.CrossRefPubMedCentralPubMed

28.

Setchell BP. The Parkes Lecture. Heat and the testis. J Reprod Fertil. 1998;114:179–94.CrossRefPubMed

29.

Liu YX. Temperature control of spermatogenesis and prospect of male contraception. Front Biosci (Schol Ed). 2010;1:730–55.CrossRef

30.

Lue YH, Hikim AP, Swerdloff RS, Im P, Taing KS, Bui T, et al. Single exposure to heat induces stage-specific germ cell apoptosis in rats: role of intratesticular testosterone on stage specificity. Endocrinology. 1999;140:1709–17.PubMed

31.

Lue Y, Hikim AP, Wang C, Im M, Leung A, Swerdloff RS. Testicular heat exposure enhances the suppression of spermatogenesis by testosterone in rats: the “two-hit” approach to male contraceptive development. Endocrinology. 2000;141:1414–24.PubMed

32.

Lue Y, Wang C, Liu Y-X, Hikim AP, Zhang XS, Ng CM, et al. Transient testicular warming enhances the suppressive effect of testosterone on spermatogenesis in adult cynomolgus monkeys (Macaca fascicularis). J Clin Endocrinol Metab. 2006;91:539–45.CrossRefPubMed

33.

Guo J, Tao SX, Chen M, Shi YQ, Zhang ZQ, Li YC, et al. Heat treatment induces liver receptor homolog-1 expression in monkey and rat Sertoli cells. Endocrinology. 2007;131:1137–48.

34.

Zhang XS, Lue YH, Guo SH, Yuan JX, Hu ZY, Han CS, et al. Expression of HSP105 and HSP60 during germ cell apoptosis in the heat-treated testes of adult cynomolgus monkeys (MACACA FASCICULARIS). Front Biosci. 2005;10:3110–21.CrossRefPubMed

35.

Kandeel FR, Swerdloff RS. Role of temperature in regulation of spermatogenesis and the use of heating as a method for contraception. Fertil Steril. 1988;49:1–23.PubMed

36.

McNitt JL, First NL. Effects of 72-hour heat stress on semen quality in boars. Int J Biometeorol. 1970;14:373–80.CrossRefPubMed

37.

Wettemann RP, Wells ME, Johnson RK. Reproductive characteristics of boars during and after exposure to increased ambient temperature. J Anim Sci. 1979;49:1501–5.

38.

Stone BA. Thermal characteristics of the testis and epididymis of the boar. J Reprod Fertil. 1981;63:551–7.CrossRefPubMed

39.

Larsson K, Einarsson S. Seminal changes in boars after heat stress. Acta Vet Scand. 1984;25:57–66.PubMed

40.

Malmgren L, Larsson K. Semen quality and fertility after heat stress in boars. Acta Vet Scand. 1984;25:425–35.PubMed

41.

Chihara M, Nakamura T, Sakakibara N, Otsuka S, Ichii O, Kon Y. The onset of heat-induced testicular calcification in mice: involvement of the telomeric locus on chromosome 1. Am J Pathol. 2014;184:2480–92.CrossRefPubMed

42.

Paul C, Teng S, Saunders PT. A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod. 2009;80:913–9.CrossRefPubMedCentralPubMed

43.

Hjollund NH, Storgaard L, Ernst E, Bonde JP, Olsen J. Impact of diurnal scrotal temperature on semen quality. Reprod Toxicol. 2002;16:215–21.CrossRefPubMed

44.

Zhang ZH, Hu ZY, Song XX, Xiao LJ, Zou RJ, Han CS, et al. Disrupted expression of intermediate filaments in the testis of rhesus monkey after experimental cryptorchidism. Int J Androl. 2004;27:234–9.CrossRefPubMed

45.

Chen M, Cai H, Yang JL, Lu CL, Liu T, Yang W, et al. Effect of heat stress on expression of junction-associated molecules and upstream factors androgen receptor and Wilms’ tumor 1 in monkey sertoli cells. Endocrinology. 2008;149:4871–82.CrossRefPubMed

46.

Chen M, Yuan JX, Shi YQ, Zhang XS, Hu ZY, Gao F, et al. Effect of 43 degrees treatment on expression of heat shock proteins 105, 70 and 60 in cultured monkey Sertoli cells. Asian J Androl. 2008;10:474–85.CrossRefPubMed

47.

Wang DH, Hu JR, Wang LY, Hu YJ, Tan FQ, Zhou H, et al. The apoptotic function analysis of p53, Apaf1, Caspase3 and Caspase7 during the spermatogenesis of the Chinese fire-bellied newt Cynops orientalis. PLoS One. 2012;7e39920.

48.

Simon L, Liu L, Murphy K, Ge S, Hotaling J, Aston KI, et al. Comparative analysis of three sperm DNA damage assays and sperm nuclear protein content in couples undergoing assisted reproduction treatment. Hum Reprod. 2014;29:904–17.CrossRefPubMed

49.

Dadoune JP. The nuclear status of human sperm cells. Micron. 1995;26:323–45.CrossRefPubMed

50.

Morel F, Mercier S, Roux C, Elmrini T, Clavequin MC, Bresson JL. Interindividual variations in the disomy frequencies of human spermatozoa and their correlation with nuclear maturity as evaluated by aniline blue staining. Fertil Steril. 1998;69:1122–7.CrossRefPubMed

51.

Morel F, Roux C, Bresson JL. Disomy frequency estimated by multicolour fluorescence in situ hybridization, degree of nuclear maturity and teratozoospermia in human spermatozoa. Reproduction. 2001;121:783–9.CrossRefPubMed

Titel: Scrotal heat stress causes sperm chromatin damage and cysteinyl aspartate-spicific proteinases 3 changes in fertile men
verfasst von: Mei-Hua Zhang
Zhi-Da Shi
Jian-Chun Yu
Yan-Ping Zhang
Lei-Guang Wang
Yi Qiu
Publikationsdatum: 01.05.2015
Verlag: Springer US
Erschienen in: Journal of Assisted Reproduction and Genetics / Ausgabe 5/2015
Print ISSN: 1058-0468
Elektronische ISSN: 1573-7330
DOI: https://doi.org/10.1007/s10815-015-0451-0

Update Gynäkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert – ganz bequem per eMail.

Newsletter bestellen

Springer Medizin

Scrotal heat stress causes sperm chromatin damage and cysteinyl aspartate-spicific proteinases 3 changes in fertile men