{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T00:08:47Z","timestamp":1788307727012,"version":"build-2803163510"},"reference-count":47,"publisher":"Ovid Technologies (Wolters Kluwer Health)","issue":"2","content-domain":{"domain":["lww.com","ovid.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2024,3]]},"abstract":"<jats:p>\n                    Aberrant sperm protamination is linked to sperm dysmorphology and nuclear chromatin condensation. Yet, its effects on sperm cytoplasmic maturation remain largely unexplored. The relationships of protamines, sperm morphology, DNA damage, and cytoplasmic remodeling were illustrated in this study to provide fresh perspectives on the mechanisms of male infertility. A total of 205 infertile males were allocated into 5 groups according to the percentage of spermatozoa exhibiting abnormal morphology within their samples. Sperm concentration, motility, abnormal sperm morphology, cytoplasmic droplets (CDs), and excess residual cytoplasm (ERC) were analyzed according to the World Health Organization manual (2010). Sperm nuclear vacuoles (NVs) were determined by propidium iodide (PI) staining. Sperm protamine expressions (P1 and P2) were detected by western blot. DNA damage was measured by acridine orange test (AOT) to calculate the proportion of sperm with single-strand DNA breaks (SSBs). Our data showed that sperm concentration and motility in infertile males significantly decreased with the severity of abnormal sperm morphology (both\n                    <jats:italic toggle=\"yes\">P<\/jats:italic>\n                    &lt; 0.01). P1 level, P1\/P2 ratio, and SSB rate increased with the severity of sperm dysmorphology, whilst the P2 level decreased (all\n                    <jats:italic toggle=\"yes\">P<\/jats:italic>\n                    &lt; 0.01). NVs, CDs, and ERC were more common in males with sperm dysmorphology and positively correlated with the SSB rate (all\n                    <jats:italic toggle=\"yes\">P<\/jats:italic>\n                    &lt; 0.01). The relationships between the SSB rate and the P1\/P2 ratio were also significant (\n                    <jats:italic toggle=\"yes\">P<\/jats:italic>\n                    &lt; 0.01). Aberrant protamination may cause sperm dysmorphology and compromise male fertility by impairing sperm\u2019s nucleus and cytoplasm maturation, with the P1\/P2 ratio potentially serving as a valuable indicator of sperm quality and male fertility.\n                  <\/jats:p>","DOI":"10.4103\/aja202360","type":"journal-article","created":{"date-parts":[[2023,10,31]],"date-time":"2023-10-31T00:37:12Z","timestamp":1698712632000},"page":"183-188","update-policy":"https:\/\/doi.org\/10.1097\/lww.0000000000001000","source":"Crossref","is-referenced-by-count":2,"title":["Aberrant protamination in sperm correlates to anomalous nuclear and cytoplasmic architectures in infertile males with sperm dysmorphology"],"prefix":"10.4103","volume":"26","author":[{"given":"Huan","family":"Jiang","sequence":"first","affiliation":[{"name":"Department of Reproductive Endocrinology, Longgang District Maternity & Child Healthcare Hospital of Shenzhen City (Longgang Maternity and Child Institute of Shantou University Medical College), Shenzhen 518172, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chu-Jie","family":"Huang","sequence":"additional","affiliation":[{"name":"Institute of Reproductive Immunology, College of Life Science and Technology, Jinan University, Guangzhou 510632, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"276","published-online":{"date-parts":[[2023,10,31]]},"reference":[{"key":"R1-20240829","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.gene.2019.05.027","article-title":"The dynamics and regulation of chromatin remodeling during spermiogenesis","volume":"706","author":"Hao","year":"2019","journal-title":"Gene"},{"key":"R2-20240829","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1007\/s00441-010-1007-3","article-title":"The making of abnormal spermatozoa:cellular and molecular mechanisms underlying pathological spermiogenesis","volume":"341","author":"Chemes","year":"2010","journal-title":"Cell Tissue Res"},{"key":"R3-20240829","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1111\/andr.12500","article-title":"An illustration of human sperm morphology and their functional ability among different group of subfertile males","volume":"6","author":"Sunanda","year":"2018","journal-title":"Andrology"},{"key":"R4-20240829","doi-asserted-by":"crossref","first-page":"1705","DOI":"10.1016\/j.fertnstert.2011.01.008","article-title":"Sperm chromatin condensation in infertile men with varicocele before and after surgical repair","volume":"95","author":"Sadek","year":"2011","journal-title":"Fertil Steril"},{"key":"R5-20240829","doi-asserted-by":"crossref","first-page":"105","DOI":"10.3390\/genes10020105","article-title":"Single and double strand sperm DNA damage:different reproductive effects on male fertility","volume":"10","author":"Ribas-Maynou","year":"2019","journal-title":"Genes"},{"key":"R6-20240829","first-page":"882","article-title":"Protamine-1 and -2 polymorphisms and gene expression in male infertility:an Italian study","volume":"35","author":"Grassetti","year":"2012","journal-title":"J Endocrinol Invest"},{"key":"R7-20240829","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1111\/andr.12610","article-title":"Detection of protamine 2 in bovine spermatozoa and testicles","volume":"7","author":"Hamilton","year":"2019","journal-title":"Andrology"},{"key":"R8-20240829","doi-asserted-by":"crossref","first-page":"2708","DOI":"10.1093\/humrep\/deq226","article-title":"Protamine contents and P1\/P2 ratio in human spermatozoa from smokers and non-smokers","volume":"25","author":"Hammadeh","year":"2010","journal-title":"Hum Reprod"},{"key":"R9-20240829","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1111\/and.12258","article-title":"Nuclear degraded sperm subpopulation is affected by poor chromatin compaction and nuclease activity","volume":"47","author":"Ribas-Maynou","year":"2015","journal-title":"Andrologia"},{"key":"R10-20240829","doi-asserted-by":"crossref","first-page":"e12823","DOI":"10.1111\/and.12823","article-title":"Sperm chromatin quality and DNA integrity in partial versus total globozoospermia","volume":"50","author":"Talebi","year":"2018","journal-title":"Andrologia"},{"key":"R11-20240829","doi-asserted-by":"crossref","first-page":"13775","DOI":"10.1007\/s11356-018-1417-4","article-title":"Investigation on the origin of sperm morphological defects:oxidative attacks, chromatin immaturity, and DNA fragmentation","volume":"25","author":"Oumaima","year":"2018","journal-title":"Environ Sci Pollut Res Int"},{"key":"R12-20240829","doi-asserted-by":"crossref","first-page":"e12843","DOI":"10.1111\/and.12843","article-title":"Association between total globozoospermia and sperm chromatin defects","volume":"50","author":"Eskandari","year":"2018","journal-title":"Andrologia"},{"key":"R14-20240829","doi-asserted-by":"crossref","first-page":"2374","DOI":"10.1093\/humrep\/deu225","article-title":"Morphological alterations in protamine-deficient spermatozoa","volume":"29","author":"Utsuno","year":"2014","journal-title":"Hum Reprod"},{"key":"R15-20240829","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1111\/j.1365-2605.2011.01154.x","article-title":"Large nuclear vacuoles are indicative of abnormal chromatin packaging in human spermatozoa","volume":"35","author":"Franco","year":"2012","journal-title":"Int J Androl"},{"key":"R16-20240829","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1080\/19396368.2018.1543481","article-title":"Teratozoospermia with amorphous sperm head associate with abnormal chromatin condensation in a Chinese family","volume":"65","author":"Ma","year":"2019","journal-title":"Syst Biol Reprod Med"},{"key":"R17-20240829","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1093\/humupd\/dmaa004","article-title":"Haploid male germ cells-the Grand Central Station of protein transport","volume":"26","author":"Pleuger","year":"2020","journal-title":"Hum Reprod Update"},{"key":"R18-20240829","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1002\/aja.1001780109","article-title":"Comparative study of cytoplasmic elimination in spermatids of selected mammalian species","volume":"178","author":"Sprando","year":"1987","journal-title":"Am J Anat"},{"key":"R19-20240829","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1186\/1477-7827-4-36","article-title":"Detection of estrogen receptors ER-alpha and ER-beta in human ejaculated immature spermatozoa with excess residual cytoplasm","volume":"4","author":"Rago","year":"2006","journal-title":"Reprod Biol Endocrinol"},{"key":"R20-20240829","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1093\/humrep\/deh555","article-title":"Cytoplasmic droplets:the good, the bad or just confusing?","volume":"20","author":"Cooper","year":"2005","journal-title":"Hum Reprod"},{"key":"R21-20240829","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1093\/molehr\/gap059","article-title":"On the possible origins of DNA damage in human spermatozoa","volume":"16","author":"Aitken","year":"2010","journal-title":"Mol Hum Reprod"},{"key":"R22-20240829","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1186\/s12958-018-0425-z","article-title":"Decline in seminal quality in Indian men over the last 37 years","volume":"16","author":"Mishra","year":"2018","journal-title":"Reprod Biol Endocrinol"},{"key":"R23-20240829","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.ucl.2019.12.001","article-title":"Cutting-edge evaluation of male infertility","volume":"47","author":"Pathak","year":"2020","journal-title":"TUrol Clin North Am"},{"key":"R24-20240829","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1111\/and.12328","article-title":"A simple sperm nuclear vacuole assay with propidium iodide","volume":"47","author":"Zhu","year":"2015","journal-title":"Andrologia"},{"key":"R25-20240829","doi-asserted-by":"crossref","first-page":"1","DOI":"10.5152\/tud.2018.49321","article-title":"Sperm DNA and detection of DNA fragmentations in sperm","volume":"44","author":"K\u00fc\u00e7\u00fck","year":"2018","journal-title":"Turk J Urol"},{"key":"R26-20240829","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/S0015-0282(16)47963-X","article-title":"A test for the practical evaluation of male fertility by acridine orange (AO) fluorescence","volume":"42","author":"Tejada","year":"1984","journal-title":"Fertil Steril"},{"key":"R27-20240829","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.3390\/jcm9041029","article-title":"Sperm parameters before and after swim-up of a second ejaculate after a short period of abstinence","volume":"9","author":"Manna","year":"2020","journal-title":"J Clin Med"},{"key":"R28-20240829","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/aja.2010.67","article-title":"Measurement and significance of sperm morphology","volume":"13","author":"Menkveld","year":"2011","journal-title":"Asian J Androl"},{"key":"R29-20240829","doi-asserted-by":"crossref","first-page":"780","DOI":"10.3389\/fgene.2020.00780","article-title":"The interplay between replacement and retention of histones in the sperm genome","volume":"11","author":"Torres-Flores","year":"2020","journal-title":"Front Genet"},{"key":"R30-20240829","doi-asserted-by":"crossref","first-page":"e13400","DOI":"10.1111\/and.13400","article-title":"An additional marker for sperm DNA quality evaluation in spermatozoa of male partners of couples undergoing assisted reproduction technique (IVF\/ICSI):protamine ratio","volume":"51","author":"Amor","year":"2019","journal-title":"Andrologia"},{"key":"R31-20240829","doi-asserted-by":"crossref","first-page":"778","DOI":"10.2174\/092986611795713998","article-title":"Protamine 2 precursors and processing","volume":"18","author":"de Mateo","year":"2011","journal-title":"Protein Pept Lett"},{"key":"R32-20240829","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1093\/humupd\/dml009","article-title":"Protamines and male infertility","volume":"12","author":"Oliva","year":"2006","journal-title":"Hum Reprod Update"},{"key":"R33-20240829","doi-asserted-by":"crossref","first-page":"e13936","DOI":"10.1111\/and.13936","article-title":"Protamine 1\/protamine 2 mRNA ratio in nonobstructive azoospermic patients","volume":"53","author":"Amjad","year":"2021","journal-title":"Andrologia"},{"key":"R34-20240829","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1002\/mrd.10105","article-title":"Protamine 1:protamine 2 stoichiometry in the sperm of eutherian mammals","volume":"61","author":"Corzett","year":"2002","journal-title":"Mol Reprod Dev"},{"key":"R35-20240829","doi-asserted-by":"crossref","first-page":"80","DOI":"10.3109\/14647273.2014.915347","article-title":"Aberrant protamine content in sperm and consequential implications for infertility treatment","volume":"17","author":"Francis","year":"2014","journal-title":"Hum Fertil (Camb)"},{"key":"R36-20240829","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1016\/j.fertnstert.2007.12.047","article-title":"Protamine 2 precursors (Pre-P2), protamine 1 to protamine 2 ratio (P1\/P2), and assisted reproduction outcome","volume":"91","author":"de Mateo","year":"2009","journal-title":"Fertil Steril"},{"key":"R37-20240829","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1111\/andr.12216","article-title":"The impact of sperm protamine deficiency and sperm DNA damage on human male fertility:a systematic review and meta-analysis","volume":"4","author":"Ni","year":"2016","journal-title":"Andrology"},{"key":"R38-20240829","doi-asserted-by":"crossref","first-page":"405","DOI":"10.21037\/tau.2020.01.31","article-title":"Relationship between sperm morphology and sperm DNA dispersion","volume":"9","author":"Jakubik-Uljasz","year":"2020","journal-title":"Transl Androl Urol"},{"key":"R39-20240829","doi-asserted-by":"crossref","first-page":"1308","DOI":"10.1016\/j.fertnstert.2021.06.016","article-title":"Quantitative selection of single human sperm with high DNA integrity for intracytoplasmic sperm injection","volume":"116","author":"Zhang","year":"2021","journal-title":"Fertil Steril"},{"key":"R40-20240829","doi-asserted-by":"crossref","first-page":"e13316","DOI":"10.1111\/and.13316","article-title":"Diagnostics of DNA fragmentation in human spermatozoa:are sperm chromatin structure analysis and sperm chromatin dispersion tests (SCD-HaloSpermG2\u00ae) comparable?","volume":"51","author":"Liffner","year":"2019","journal-title":"Andrologia"},{"key":"R41-20240829","doi-asserted-by":"crossref","first-page":"e13718","DOI":"10.1111\/and.13718","article-title":"Comparative analysis of tests used to assess sperm chromatin integrity and DNA fragmentation","volume":"53","author":"Dutta","year":"2021","journal-title":"Andrologia"},{"key":"R42-20240829","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1007\/s00404-009-1140-y","article-title":"Sperm morphological abnormalities as indicators of DNA fragmentation and fertilization in ICSI","volume":"281","author":"Daris","year":"2010","journal-title":"Arch Gynecol Obstet"},{"key":"R43-20240829","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1017\/S0967199419000595","article-title":"Sperm DNA fragmentation:causes and identification","volume":"28","author":"Hamilton","year":"2020","journal-title":"Zygote"},{"key":"R44-20240829","first-page":"325","article-title":"Sperm structure and its relevance to infertility. An electron microscopic study","volume":"116","author":"Zamboni","year":"1992","journal-title":"Arch Pathol Lab Med"},{"key":"R45-20240829","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1111\/andr.12324","article-title":"An investigation of the potential effect of sperm nuclear vacuoles in human spermatozoa on DNA fragmentation using a neutral and alkaline Comet assay","volume":"5","author":"Pastuszek","year":"2017","journal-title":"Andrology"},{"key":"R46-20240829","doi-asserted-by":"crossref","first-page":"1765","DOI":"10.1016\/j.celrep.2015.10.066","article-title":"Exogenous expression of human protamine 1 (hPrm1) remodels fibroblast nuclei into spermatid-like structures","volume":"13","author":"Iuso","year":"2015","journal-title":"Cell Rep"},{"key":"R47-20240829","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1186\/1477-7827-10-92","article-title":"An investigation of excess residual cytoplasm in human spermatozoa and its distinction from the cytoplasmic droplet","volume":"10","author":"Rengan","year":"2012","journal-title":"Reprod Biol Endocrinol"},{"key":"R48-20240829","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1111\/andr.12469","article-title":"Transmission electron microscopy analysis of the origin and incidence of sperm intranuclear cytoplasmic retention in fertile and teratozoospermia men","volume":"6","author":"Zhu","year":"2018","journal-title":"Andrology"}],"container-title":["Asian Journal of Andrology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.ovid.com\/10.4103\/aja202360","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,26]],"date-time":"2026-08-26T16:48:56Z","timestamp":1787762936000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.ovid.com\/10.4103\/aja202360"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10,31]]},"references-count":47,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2024]]}},"URL":"https:\/\/doi.org\/10.4103\/aja202360","relation":{},"ISSN":["1745-7262","1008-682X"],"issn-type":[{"value":"1745-7262","type":"print"},{"value":"1008-682X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,10,31]]},"assertion":[{"value":"2023-05-25","name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2023-09-21","name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}}]}}