Impact of cigarette smoking on histone (H2B) to protamine ratio in human spermatozoa and its relation to sperm parameters
Open accessAbstract
Summary: Smoking is strongly associated with abnormalities in histone‐to‐protamine transition and with alteration of protamine expression in human spermatozoa. A proper protamine to histone ratio is, however, essential for sperm chromatin maturity and DNA integrity. Alterations in these sperm nuclear proteins were observed in infertile men. The present prospective study is aimed at evaluating the possible relationship among smoking, semen quality and the histone‐to‐protamine transition ratio in mature spermatozoa. Histone H2B and protamine 1 (P1) and 2 (P2) were quantified using acid‐urea polyacrylamide gel electrophoresis in the spermatozoa of 35 smokers and 19 non‐smokers. Levels of lipid peroxidation marker malondialdehyde (MDA) were measured in seminal plasma by thiobarbituric acid assay. Cotinine concentrations were determined in seminal plasma using an enzyme‐linked immunosorbent assay. Histone H2B levels in smokers (292.27 ± 58.24 ng/10 6) were significantly higher (p = 0.001) than that of non‐smokers (109.1 ± 43.70 ng/10 6), besides, a significant difference (p > 0.0001) was found for the P1 and P2 ratio between smokers (1.71 ± 0.071) and non‐smokers (1.05 ± 0.033). The H2B/(H2B+P1 + P2) ratio (0.29 ± 0.71) of smokers were significantly higher (p = <0.0001) than that of non‐smokers (0.12 ± 0.01). The concentrations of MDA (μ m) (7.13 ± 1.15) and cotinine (ng/mL) (60.44 ± 31.32) in seminal plasma of smokers were significantly higher (p = 0.001) than those in the samples of the non‐smoker group (4.42 ± 1.16 and 2.01 ± 2.84 respectively). In addition, smokers showed significantly (p ≤ 0.002) lower sperm count, motility (p = 0.018), vitality (p = 0.009) and membrane integrity (p = 0.0001) than non‐smokers. These results reveal that patients who smoke possess a higher proportion of spermatozoa with an alteration of the histone to protamine ratio than patients who do not smoke, and suggest that cigarette smoking may inversely affect male fertility.
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Smoking was later found to be associated with reduced sperm count, motility and morphology, and altered sperm microRNA, mitochondria and protein in the smoker parent.
“was later found to be associated with reduced sperm count, motility and morphology, and altered sperm microRNA, mitochondria and protein in the smoker parent 201,202”
From Intergenerational transmission of trauma effects: putative role of epigenetic mechanisms (2018) · cites this paper as [201]
The Results and Discussion (page numbers unavailable) report lower sperm count and motility in smokers, describe reduced normal morphology, and identify altered sperm nuclear proteins. The paper does not report altered sperm microRNA or mitochondria in smokers, so those parts of the claim are unsupported. (LLM, conf=0.90)
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Cites
Lamb, D. J. (2000) · Journal of Andrology · doi:10.1002/j.1939-4640.2000.tb03272.x · Cited by 2,081 · see citing works
Role of sperm chromatin abnormalities and DNA damage in male infertility.
Agarwal, A., & Said, T. (2003) · Human Reproduction Update · doi:10.1093/humupd/dmg027 · Cited by 889 · see citing works
Protamines and male infertility
Oliva, R. (2006) · Human Reproduction Update · doi:10.1093/humupd/dml009 · Cited by 814 · see citing works
DNA Integrity in Human Spermatozoa: Relationships With Semen Quality
Irvine, D. S., Twigg, J., Gordon, E., Fulton, N., MILNE, P. A., & Aitken, R. J. (2000) · Journal of Andrology · doi:10.1002/j.1939-4640.2000.tb03273.x · Cited by 735 · see citing works
Sperm chromatin damage impairs human fertility
Spanò, M., Bonde, J. ., Hjøllund, N. H., Kolstad, H. A., Cordelli, E., & Leter, G. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00462-8 · Cited by 719 · see citing works
Oxidative stress, DNA damage and the Y chromosome
Aitken, R. J., & Krausz, C. G. (2001) · Reproduction · doi:10.1530/rep.0.1220497 · Cited by 686 · see citing works
Haploinsufficiency of protamine-1 or -2 causes infertility in mice
Cho, C., Willis, W. D., Goulding, E. H., Jung-Ha, H., Choi, Y.-C., Hecht, N. B., & Eddy, E. M. (2001) · Nature Genetics · doi:10.1038/ng0501-82 · Cited by 544 · see citing works
DNA damage to spermatozoa has impacts on fertilization and pregnancy
Lewis, S., & Aitken, R. (2005) · Cell and Tissue Research · doi:10.1007/s00441-005-1097-5 · Cited by 532 · see citing works
Origin of DNA damage in ejaculated human spermatozoa
Sakkas, D. (1999) · Reviews of Reproduction · doi:10.1530/ror.0.0040031 · Cited by 522 · see citing works
Morris, I. D. (2002) · Human Reproduction · doi:10.1093/humrep/17.4.990 · Cited by 521 · see citing works
Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART
Borini, A., Tarozzi, N., Bizzaro, D., Bonu, M. A., Fava, L., Flamigni, C., & Coticchio, G. (2006) · Human Reproduction · doi:10.1093/humrep/del251 · Cited by 462 · see citing works
Moustafa, M. H., Sharma, R., Thornton, J., Mascha, E., Abdel-Hafez, M., Thomas, A., & Agarwal, A. (2004) · Human Reproduction · doi:10.1093/humrep/deh024 · Cited by 449 · see citing works
Zini, A. S., Bielecki, R., Phang, D., & Zenzes, M. T. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01796-9 · Cited by 447 · see citing works
Chromatin remodelling and epigenetic features of germ cells
Kimmins, S., & Sassone‐Corsi, P. (2005) · Nature · doi:10.1038/nature03368 · Cited by 446 · see citing works
Nature of DNA Damage in Ejaculated Human Spermatozoa and the Possible Involvement of Apoptosis1
Sakkas, D., Moffatt, O., Manicardi, G. C., et al. (2002) · Biology of Reproduction · doi:10.1095/biolreprod66.4.1061 · Cited by 446 · see citing works
Semen quality of male smokers and nonsmokers in infertile couples
Künzle, R., Mueller, M. D., Hänggi, W., Birkhäuser, M., Drescher, H., & Bersinger, N. A. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(02)04664-2 · Cited by 396 · see citing works
Smoking and reproduction: gene damage to human gametes and embryos
Zenzes, M. T. (2000) · Human Reproduction Update · doi:10.1093/humupd/6.2.122 · Cited by 396 · see citing works
Aitken, R. J., Iuliis, G. N. D., Finnie, J. M., Hedges, A., & McLachlan, R. I. (2010) · Human Reproduction · doi:10.1093/humrep/deq214 · Cited by 395 · see citing works
Altered protamine expression and diminished spermatogenesis: what is the link?
Carrell, D. T., Emery, B. R., & Hammoud, S. S. (2007) · Human Reproduction Update · doi:10.1093/humupd/dml057 · Cited by 395 · see citing works
Saleh, R. A., Agarwal, A. K., Sharma, R. K., Nelson, D. R., & Thomas, A. J., Jr. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03294-6 · Cited by 394 · see citing works
Sperm DNA quality predicts intrauterine insemination outcome: a prospective cohort study
Duran, E. H. (2002) · Human Reproduction · doi:10.1093/humrep/17.12.3122 · Cited by 383 · see citing works
Sequence-Specific Packaging of DNA in Human Sperm Chromatin
Gatewood, J. M., Cook, G. R., Balhorn, R., Bradbury, E. M., & Schmid, C. W. (1987) · Science · doi:10.1126/science.3576213 · Cited by 382 · see citing works
Protamine 2 Deficiency Leads to Sperm DNA Damage and Embryo Death in Mice1
Cho, C., Jung-Ha, H., Willis, W., Goulding, E., Stein, P., Xu, Z., Schultz, R., Hecht, N., & Eddy, E. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.102.015115 · Cited by 363 · see citing works
Are Tests of Sperm DNA Damage Clinically Useful? Pros and Cons
Zini, A. S., & Sigman, M. (2009) · Journal of Andrology · doi:10.2164/jandrol.108.006908 · Cited by 349 · see citing works
Sakkas, D., Mariéthoz, E., & John, J. C. S. (1999) · Experimental Cell Research · doi:10.1006/excr.1999.4586 · Cited by 348 · see citing works
The Structural Organization of Sperm Chromatin
Wykes, S. M., & Krawetz, S. A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304545200 · Cited by 335 · see citing works
Manicardi, G. C., Bianchi, P. G., Pantano, S., et al. (1995) · Biology of Reproduction · doi:10.1095/biolreprod52.4.864 · Cited by 332 · see citing works
Jarvis, M. J., Russell, M. A., Benowitz, N. L., et al. (1988) · American Journal of Public Health · doi:10.2105/ajph.78.6.696 · Cited by 319 · see citing works
Analysis of lipid peroxidation mechanisms in human spermatozoa
Aitken, R. J., Harkiss, D., & Buckingham, D. W. (1993) · Molecular Reproduction and Development · doi:10.1002/mrd.1080350313 · Cited by 319 · see citing works
A laboratory method for diagnosing predominance of homo- or hetero- erotic interest in the male
Freund, K. B. (1963) · Behaviour Research and Therapy · doi:10.1016/0005-7967(63)90012-3 · Cited by 309 · see citing works
Lung Cancer Rates in Men and Women With Comparable Histories of Smoking
Bain, C., Feskanich, D., Speizer, F. E., Thun, M. J., Hertzmark, E., ROSNER, B. A., & Colditz, G. A. (2004) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djh143 · Cited by 299 · see citing works
Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis
Govin, J., Escoffier, E., Rousseaux, S., Kühn, L., Ferro, M., Thévenon, J., Catena, R., Davidson, I., Garin, J., Khochbin, S., et al. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200604141 · Cited by 297 · see citing works
Wang, X., Sharma, R. K., Gupta, A. K., George, V. K., Thomas, A. J., Jr., Falcone, T., & Agarwal, A. K. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)00983-x · Cited by 297 · see citing works
Carrell, D. T., & Liu, L. (2001) · Journal of Andrology · doi:10.1002/j.1939-4640.2001.tb02220.x · Cited by 294 · see citing works
Aberrant protamine 1/protamine 2 ratios in sperm of infertile human males
Balhorn, R., Reed, S., & Tanphaichitr, N. (1988) · Cellular and Molecular Life Sciences · doi:10.1007/bf01960243 · Cited by 292 · see citing works
Is smoking a risk factor for decreased semen quality? A cross-sectional analysis
Ramlau-Hansen, C. H., Thulstrup, A. M., Aggerholm, A. S., Jensen, M. S., Toft, G., & Bonde, J. P. (2007) · Human Reproduction · doi:10.1093/humrep/del364 · Cited by 289 · see citing works
Lifestyle factors in people seeking infertility treatment – A review
Anderson, K. J., Nisenblat, V., & NORMAN, R. (2010) · Australian and New Zealand Journal of Obstetrics and Gynaecology · doi:10.1111/j.1479-828x.2009.01119.x · Cited by 275 · see citing works
History of febrile illness and variation in semen quality
Carlsen, E. (2003) · Human Reproduction · doi:10.1093/humrep/deg412 · Cited by 256 · see citing works
The role of histones in chromatin remodelling during mammalian spermiogenesis
Govin, J., Caron, C., Lestrat, C., Rousseaux, S., & Khochbin, S. (2004) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.2004.04266.x · Cited by 255 · see citing works
DNA integrity is compromised in protamine-deficient human sperm.
Aoki, V., Moskovtsev, S., Willis, J., Liu, L., Mullen, J., & Carrell, D. (2005) · Journal of Andrology · doi:10.2164/jandrol.05063 · Cited by 248 · see citing works
Sperm chromatin damage associated with male smoking
Potts, R. J., Newbury, C. J., Smith, G., et al. (1999) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(98)00242-5 · Cited by 234 · see citing works
Gatewood, J. M., Cook, G. R., Balhorn, R., Schmid, C. W., & Bradbury, E. M. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)30554-9 · Cited by 231 · see citing works
Aoki, V. W., Liu, L., & Carrell, D. T. (2005) · Human Reproduction · doi:10.1093/humrep/deh798 · Cited by 228 · see citing works
The human sperm epigenome and its potential role in embryonic development
Carrell, D. T., & Hammoud, S. S. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap090 · Cited by 228 · see citing works
Relationships between human sperm protamines, DNA damage and assisted reproduction outcomes
Simon, L., Castillo, J., Oliva, R., et al. (2011) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2011.08.010 · Cited by 228 · see citing works
Cigarette smoking and reproductive function
Soares, S. R., & de Melo, M. A. B. (2008) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e3282fc9c1e · Cited by 207 · see citing works
The impact of cigarette smoking on human semen parameters and hormones
Trummer, H., Habermann, H., Haas, J. G., & Pummer, K. (2002) · Human Reproduction · doi:10.1093/humrep/17.6.1554 · Cited by 202 · see citing works
The influence of cigarette smoking on human sperm quality and DNA fragmentation
Sepaniak, S., Forges, T., Gérard, H., Foliguet, B., Béné, M. C., & Monnier‐Barbarino, P. (2006) · Toxicology · doi:10.1016/j.tox.2006.03.001 · Cited by 199 · see citing works
Cigarette smoking and aneuploidy in human sperm
Shi, Q., Ko, E. M., Barclay, L., et al. (2001) · Molecular Reproduction and Development · doi:10.1002/mrd.1048 · Cited by 194 · see citing works
Complete selective absence of protamine P2 in humans
de Yebra, L., Ballescà, J. L., Vanrell, J. A., et al. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)82234-7 · Cited by 191 · see citing works
Chromatin Structure of Telomere Domain in Human Sperm
Zalenskaya, I. A., Bradbury, E. M., & Zalensky, A. O. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.3917 · Cited by 182 · see citing works
Expression of mammalian spermatozoal nucleoproteins
Dadoune, J. (2003) · Microscopy Research and Technique · doi:10.1002/jemt.10317 · Cited by 182 · see citing works
Sperm-derived histones contribute to zygotic chromatin in humans
van der Heijden, G. W., Ramos, L., Baart, E. B., van den Berg, I. M., Derijck, A. A. H. A., van der Vlag, J., Martini, E., & de Boer, P. (2008) · BMC Developmental Biology · doi:10.1186/1471-213x-8-34 · Cited by 181 · see citing works
Protamine 1: Protamine 2 stoichiometry in the sperm of eutherian mammals*
Corzett, M., Mazrimas, J. A., & Balhorn, R. (2002) · Molecular Reproduction and Development · doi:10.1002/mrd.10105 · Cited by 181 · see citing works
Human male infertility may be due to a decrease of the protamine P2 content in sperm chromatin
Belokopytova, I. A., Kostyleva, E. I., Tomilin, A. N., et al. (1993) · Molecular Reproduction and Development · doi:10.1002/mrd.1080340109 · Cited by 180 · see citing works
Kızıler, A. R., Aydemir, B., Onaran, İ., Alıcı, B., Özkara, H., Gülyaşar, T., & Akyolcu, M. C. (2007) · Biological Trace Element Research · doi:10.1007/s12011-007-8020-8 · Cited by 174 · see citing works
Effects of ejaculatory frequency and season on variations in semen quality
Carlsen, E., Petersen, J. H., Andersson, A., et al. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.01.039 · Cited by 170 · see citing works
Hsieh, Y.-Y., Chang, C.-C., & Lin, C.-S. (2006) · International Journal of Biological Sciences · doi:10.7150/ijbs.2.23 · Cited by 167 · cited 1× · see citing works
“These results are in close agreement with other reports (Tavilani et al., 2005; Hsieh et al., 2006; Ben Abdallah et al., 2009) which have demonstrated that high MDA levels correlate with other decreased sperm parameters such as concentration and motility.”
Resultde Yebra, L., Ballescá, J.-L., Vanrell, J. A., et al. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00012-0 · Cited by 166 · see citing works
Mengual, L., Ballescà, J. L., Ascaso, C., et al. (2003) · Journal of Andrology · doi:10.1002/j.1939-4640.2003.tb02692.x · Cited by 164 · see citing works
Zitzmann, M., Rolf, C., Nordhoff, V., Schräder, G., Rickert-Föhring, M., Gassner, P., Behre, H. M., Greb, R. R., Kiesel, L., & Nieschlag, E. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)00339-x · Cited by 163 · see citing works
Establishment of male-specific epigenetic information
Rousseaux, S., Caron, C., Govin, J., Lestrat, C., Faure, A.-K., & Khochbin, S. (2005) · Gene · doi:10.1016/j.gene.2004.12.004 · Cited by 160 · see citing works
Zhang, X., Gabriel, M. S., & Zini, A. S. (2006) · Journal of Andrology · doi:10.2164/jandrol.05171 · Cited by 157 · see citing works
Gardiner‐Garden, M., Ballesteros, M., Gordon, M. L., & Tam, P. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.6.3350 · Cited by 150 · see citing works
Human Testis/Sperm-specific Histone H2B (hTSH2B)
Zalensky, A. O., Siino, J. S., Gineitis, A. A., Zalenskaya, I. A., Tomilin, N., Yau, P. M., & Bradbury, E. M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206065200 · Cited by 149 · see citing works
The clinical content of preconception care: preconception care for men
Frey, K. A., Navarro, S. M., Kotelchuck, M., & Lu, M. C. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2008.10.024 · Cited by 147 · see citing works
McPherson, S., & Longo, F. J. (1993) · PubMed · Cited by 145 · see citing works
Is prenatal exposure to tobacco smoking a cause of poor semen quality? A follow-up study
Ramlau-Hansen, C. H., Thulstrup, A. M., Storgaard, L., Toft, G., Olsen, J., & Bonde, J. P. (2007) · American Journal of Epidemiology · doi:10.1093/aje/kwm032 · Cited by 139 · see citing works
Protamine contents and P1/P2 ratio in human spermatozoa from smokers and non-smokers
Hammadeh, M. E., Hamad, M. F., Montenarh, M., & Fischer‐Hammadeh, C. (2010) · Human Reproduction · doi:10.1093/humrep/deq226 · Cited by 138 · see citing works
Self-citationPatterns, mechanisms, and functions of translation regulation in mammalian spermatogenic cells
Kleene, K. C. (2003) · Cytogenetic and Genome Research · doi:10.1159/000076807 · Cited by 138 · see citing works
Protamine 1 to protamine 2 ratio correlates with dynamic aspects of DNA fragmentation in human sperm
García-Peiró, A., Martínez‐Heredia, J., Oliver‐Bonet, M., et al. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.06.053 · Cited by 131 · see citing works
Influence of the abstinence period on human sperm quality.
Jonge, C. D., Lafromboise, M., Bosmans, E., Ombelet, W., Cox, A., & Nijs, M. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.03.014 · Cited by 130 · see citing works
Cigarette smoking is related to a decrease in semen volume in a population of fertile men
Pasqualotto, F. F., Sobreiro, B. P., Hallak, J., Pasqualotto, E. B., & Lucón, A. M. (2005) · British Journal of Urology · doi:10.1111/j.1464-410x.2005.05906.x · Cited by 129 · see citing works
Human Sperm Telomere–Binding Complex Involves Histone H2b and Secures Telomere Membrane Attachment
Gineitis, A. A., Zalenskaya, I. A., Yau, P. M., Bradbury, E. M., & Zalensky, A. O. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.7.1591 · Cited by 128 · see citing works
Cotinine concentrations in semen, urine, and blood of smokers and nonsmokers.
Vine, M. F., Hulka, B., Margolin, B. H., Truong, Y. K., Hu, P. C., Schramm, M. M., Griffith, J., McCann, M. F., & Everson, R. B. (1993) · American Journal of Public Health · doi:10.2105/ajph.83.9.1335 · Cited by 126 · see citing works
Shorter abstinence decreases sperm deoxyribonucleic acid fragmentation in ejaculate
Gosálvez, J., González-Martínez, M., López‐Fernández, C., et al. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.08.027 · Cited by 123 · see citing works
Effect of cigarette smoking on semen quality of infertile men.
Gaur, D. S., Talekar, M., & Vp, P. (2007) · PubMed · Cited by 122 · see citing works
The effect of sperm DNA damage on assisted reproduction outcomes. A review.
Agarwal, A. K., & Allamaneni, S. S. R. (2004) · PubMed · Cited by 121 · see citing works
Virant‐Klun, I., Tomaževič, T., & Meden‐Vrtovec, H. (2002) · Journal of Assisted Reproduction and Genetics · doi:10.1023/a:1016006509036 · Cited by 120 · see citing works
Novel human testis-specific histone H2B encoded by the interrupted gene on the X chromosome
Churikov, D., Siino, J. S., Svetlova, M., et al. (2004) · Genomics · doi:10.1016/j.ygeno.2004.06.001 · Cited by 119 · see citing works
Decreased protamine-1 transcript levels in testes from infertile men
Steger, K. (2003) · Molecular Human Reproduction · doi:10.1093/molehr/gag041 · Cited by 118 · see citing works
Increased levels of oxidants and reduced antioxidants in semen of infertile men with varicocele
Abdelmoaty, M., Saleh, R. A., Sharma, R. K., et al. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.12.039 · Cited by 117 · see citing works
de Mateo, S., Gázquez, C., Guimerà, M., et al. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.12.047 · Cited by 111 · see citing works
Tavilani, H., Doosti, M., & Saeidi, H. (2005) · Clinica Chimica Acta · doi:10.1016/j.cccn.2005.01.017 · Cited by 107 · see citing works
Effect of smoking on seminal plasma ascorbic acid in infertile and fertile males
Mostafa, T., Tawadrous, G. A., Roaia, M. M. F., Amer, M. K., Kader, R. A., & Aziz, A. (2006) · Andrologia · doi:10.1111/j.1439-0272.2006.00744.x · Cited by 106 · see citing works
Wong, W. Y., Thomas, C. M. G., Merkus, H. M. W. M., Zielhuis, G. A., Doesburg, W. H., & Steegers‐Theunissen, R. P. M. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01567-3 · Cited by 105 · see citing works
Round spermatids from infertile men exhibit decreased protamine-1 and -2 mRNA
Steger, K., Failing, K., Klonisch, T. C., et al. (2001) · Human Reproduction · doi:10.1093/humrep/16.4.709 · Cited by 104 · see citing works
Oxidative stress, DNA damage and the Y chromosome
Aitken, R. J. (2001) · Reproduction · doi:10.1530/reprod/122.4.497 · Cited by 101 · see citing works
Szczygiel, M. A., & Ward, W. S. (2002) · Biology of Reproduction · doi:10.1095/biolreprod.101.002667 · Cited by 90 · see citing works
Recent cigarette smoking and assisted reproductive technologies outcome
Fuentes, A., Muñoz, A., Barnhart, K. T., Begoña Arguello, B., Díaz, M. M., & Pommer, R. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.09.073 · Cited by 88 · see citing works
Nasr‐Esfahani, M. H., Razavi, S., Mozdarani, H., et al. (2004) · Andrologia · doi:10.1111/j.1439-0272.2004.00612.x · Cited by 86 · see citing works
On the Nature and Origin of DNA Strand Breaks in Elongating Spermatids1
Laberge, R.-M., & Boissonneault, G. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.104.036939 · Cited by 82 · see citing works
Rogenhofer, N. N., Dansranjavin, T., Schorsch, M., et al. (2013) · Human Reproduction · doi:10.1093/humrep/des471 · Cited by 81 · see citing works
Hammadeh, M., Radwan, M., al-Hasani, S., Micu, R., Rosenbaum, P., Lorenz, M., & Schmidt, W. (2006) · Reproductive Biomedicine Online · doi:10.1016/s1472-6483(10)60661-x · Cited by 79 · see citing works
Self-citationThe effect of epigenetic sperm abnormalities on early embryo-genesis
Emery, B. R., & Carrell, D. T. (2006) · Asian Journal of Andrology · doi:10.1111/j.1745-7262.2006.00127.x · Cited by 78 · see citing works
Abdallah, F. B., Dammak, I., Attia, H., et al. (2009) · Journal of Clinical Laboratory Analysis · doi:10.1002/jcla.20297 · Cited by 74 · see citing works
Fariello, R. M., Pariz, J. R., Spaine, D. M., Gozzo, F. C., Pilau, E. J., Fraietta, R., Bertolla, R. P., Andreoni, C., & Cedenho, A. P. (2012) · Human Reproduction · doi:10.1093/humrep/des287 · Cited by 74 · see citing works
Characterization of nucleohistone and nucleoprotamine components in the mature human sperm nucleus
Li, Y., Lalancette, C., Miller, D., et al. (2008) · Asian Journal of Andrology · doi:10.1111/j.1745-7262.2008.00410.x · Cited by 67 · see citing works
Immunoexpression of testis-specific histone 2B in human spermatozoa and testis tissue
Roijen, H. V., Ooms, M., Spaargaren, M., et al. (1998) · Human Reproduction · doi:10.1093/humrep/13.6.1559 · Cited by 62 · see citing works
Semen quality of smoking and non-smoking men in infertile couples in a Turkish population
Özgür, K., Işıkoğlu, M., Seleker, M., & Dönmez, L. (2003) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-003-0572-z · Cited by 58 · see citing works
Effect of alcohol intake and cigarette smoking on sperm parameters and pregnancy
de Jong, A. M. E., Menkveld, R., Lens, J. W., Nienhuis, S. E., & Rhemrev, J. P. T. (2012) · Andrologia · doi:10.1111/and.12054 · Cited by 57 · see citing works
Factors affecting the variability of semen analysis results in infertile men
Baker, H. W. G., Burger, H., de Kretser, D. M., et al. (1981) · International Journal of Andrology · doi:10.1111/j.1365-2605.1981.tb00743.x · Cited by 56 · see citing works
Does Cigarette Smoking Affect Seminal Fluid Parameters? A Comparative Study
Meri, Z. B., Irshid, I. B., Migdadi, M., Irshid, A. B., & Mhanna, S. A. (2013) · Oman Medical Journal · doi:10.5001/omj.2013.03 · Cited by 50 · see citing works
The histone to protamine ratio in human spermatozoa: comparative study of whole and processed semen
Zini, A. S., Gabriel, M. S., & Zhang, X. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.05.070 · Cited by 48 · see citing works
Incomplete protection of genetic integrity of mature spermatozoa against oxidative stress
Linschooten, J. O., Laubenthal, J., Cemeli, E., Baumgartner, A., Anderson, D. C., Sipinen, V. E., Brunborg, G., Haenen, G. R. M. M., Fthenou, E., Briedé, J. J., et al. (2011) · Reproductive Toxicology · doi:10.1016/j.reprotox.2011.05.004 · Cited by 46 · see citing works
Singleton, S., Zalensky, A. O., Doncel, G. F., et al. (2006) · Human Reproduction · doi:10.1093/humrep/del439 · Cited by 46 · see citing works
Cytogenetic study of human oocytes uncleaved after in-vitro fertilization
Selva, J., Martin-Pont, B., Hugues, J., et al. (1991) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a137413 · Cited by 46 · see citing works
All roads lead to chromatin: Multiple pathways for histone deposition
Li, Q., Burgess, R. J., & Zhang, Z. (2011) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2011.06.013 · Cited by 42 · see citing works
Semen parameters of non-infertile smoker and non-smoker men.
Davar, R., Sekhavat, L., & Naserzadeh, N. (2012) · Europe PMC (PubMed Central) · Cited by 37 · see citing works
Tagami, T., & KAGAMI, H. (1998) · Molecular Reproduction and Development · doi:10.1002/(sici)1098-2795(199807)50:3 · Cited by 32 · see citing works
Sperm nuclear histone H2B: correlation with sperm DNA denaturation and DNA stainability
Zini, A. S., Zhang, X., & Gabriel, M. S. (2008) · Asian Journal of Andrology · doi:10.1111/j.1745-7262.2008.00415.x · Cited by 31 · see citing works
Clinical relevance of sperm DNA assessment: an update
Barratt, C. L. R., & Jonge, C. J. D. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.07.1050 · Cited by 30 · see citing works
Chronobiological Fluctuations in Semen Parameters with a Constant Abstinence Period
Ombelet, W., Maes, M. H. J., Vandeput, H., Cox, A., Janssen, M. A. C., Pollet, H., Fourie, F. L. R., Steeno, O., & Bosmans, E. (1996) · Archives of Andrology · doi:10.3109/01485019608988508 · Cited by 29 · see citing works
Characterisation of a human sperm cell subpopulation marked by the presence of the TSH2B histone
Singleton, S., Mudrak, O., Morshedi, M., et al. (2007) · Reproduction Fertility and Development · doi:10.1071/rd06099 · Cited by 27 · see citing works
Male reproductive system and antioxidants in oxidative stress induced by hypobaric hypoxia
Zepeda, A. B., Figueroa, C. A., Calaf, G. M., & Farías, J. G. (2012) · Andrologia · doi:10.1111/and.12039 · Cited by 25 · see citing works
Fawzy, I. A., Kamal, N. N., & Abdulla, A. M. (2011) · Research Journal of Environmental Toxicology · doi:10.3923/rjet.2011.282.292 · Cited by 19 · see citing works
Sangalli, L., Chiesa, L. M., Passerò, E., et al. (2003) · Journal of Chromatography B · doi:10.1016/j.jchromb.2003.08.004 · Cited by 17 · see citing works
Barratt, C. L. R. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap094 · Cited by 14 · see citing works
Evers, J. L. H. (2012) · Human Reproduction · doi:10.1093/humrep/des345 · Cited by 5 · see citing works
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Intergenerational transmission of trauma effects: putative role of epigenetic mechanisms
Yehuda, R., & Lehrner, A. (2018) · World Psychiatry · doi:10.1002/wps.20568 · Cited by 730 · see citing works
- Authors
- Hamad, M. F., Shelko, N., Kartarius, S., Montenarh, M., & Hammadeh, M. E.
- Affiliations
- King Saud bin Abdulaziz University for Health Sciences (SA)
- Saarland University (DE)
- Corresponding author
- Hammadeh, M. E.
- Venue
- Andrology
- Publisher
- Wiley
- Published
- 2014-07-14
- Volume
- 2
- Issue
- 5
- Pages
- 666-677
- ISSN
- 2047-2919 (ISSN-L)
- 2047-2927
- OpenAlex
- W2044937223
- Cited by
- 81
- References
- 119
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 7 · 2023: 6 · 2022: 7 · 2021: 7 · 2020: 9 · 2019: 8 · 2018: 11 · 2017: 10 · 2016: 5 · 2015: 3
- FWCI
- 7.27
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Andrology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Keywords
- cigarette smoking, histone H2B, protamine, histone-to-protamine transition, sperm chromatin, sperm DNA integrity, semen quality, sperm count, sperm motility, sperm viability, lipid peroxidation, malondialdehyde, cotinine, seminal plasma, male infertility, oxidative stress, sperm nuclear proteins, protamine 1, protamine 2, spermatozoa
- MeSH terms
- Adult, Cell Survival, Chromatin, Cotinine, Fertility, Histones, Humans, Infertility, Male, Male, Malondialdehyde, Prospective Studies, Protamines, Semen, Smoking, Sperm Count, Sperm Motility, Spermatozoa, Semen Analysis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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