{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,14]],"date-time":"2026-07-14T16:07:56Z","timestamp":1784045276032,"version":"3.55.0"},"reference-count":107,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2022,6,10]],"date-time":"2022-06-10T00:00:00Z","timestamp":1654819200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Fund for Medical Research in Hainaut (F.R.M.H.)"},{"name":"UMons Research Institute for Biosciences under \u201cHSP70\u201d project"},{"name":"European Regional Development Fund and the Walloon Region, Belgium"},{"name":"UMHAP (UMons\/H\u00f4pital Ambroise Par\u00e9) Medical Research Centre-Scientific Inspiration for Medical Excellence in Mons"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>HSP70s constitute a family of chaperones, some isoforms of which appear to play a role in sperm function. Notably, global proteomic studies analyzing proteins deregulated in asthenozoospermia, a main cause of male infertility characterized by low sperm motility, showed the dysregulation of some HSP70 isoforms. However, to date, no clear trend has been established since the variations in the abundance of HSP70 isoforms differed between studies. The HSPA2 isoform has been reported to play a key role in fertilization, but its dysregulation and possible relocation during capacitation, a maturation process making the spermatozoon capable of fertilizing an oocyte, is debated in the literature. The aim of the present study was to investigate the fate of all sperm HSP70 isoforms during capacitation and in relation to sperm motility. Using Multiple-Reaction Monitoring (MRM) mass spectrometry, we showed that the relative abundance of all detected isoforms was stable between non-capacitated and capacitated spermatozoa. Immunofluorescence using two different antibodies also demonstrated the stability of HSP70 isoform localization during capacitation. We also investigated spermatozoa purified from 20 sperm samples displaying various levels of total and progressive sperm motility. We showed that the abundance of HSP70 isoforms is not correlated to sperm total or progressive motility.<\/jats:p>","DOI":"10.3390\/ijms23126497","type":"journal-article","created":{"date-parts":[[2022,6,10]],"date-time":"2022-06-10T10:25:12Z","timestamp":1654856712000},"page":"6497","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Targeted Analysis of HSP70 Isoforms in Human Spermatozoa in the Context of Capacitation and Motility"],"prefix":"10.3390","volume":"23","author":[{"given":"Sarah","family":"Grassi","sequence":"first","affiliation":[{"name":"Laboratory of Cell Biology, Research Institute for Biosciences, Research Institute for Health Sciences and Technology, University of Mons, Place du Parc 23, 7000 Mons, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marie","family":"Bisconti","sequence":"additional","affiliation":[{"name":"Laboratory of Cell Biology, Research Institute for Biosciences, Research Institute for Health Sciences and Technology, University of Mons, Place du Parc 23, 7000 Mons, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4369-8552","authenticated-orcid":false,"given":"Baptiste","family":"Martinet","sequence":"additional","affiliation":[{"name":"Evolutionary Biology & Ecology, Universit\u00e9 Libre de Bruxelles, Avenue Paul H\u00e9ger-CP 160\/12, 1000 Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vanessa","family":"Arcolia","sequence":"additional","affiliation":[{"name":"Clinique de Fertilit\u00e9 R\u00e9gionale de Mons, CHU Ambroise Par\u00e9 Hospital, Boulevard Kennedy 2, 7000 Mons, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean-Fran\u00e7ois","family":"Simon","sequence":"additional","affiliation":[{"name":"Clinique de Fertilit\u00e9 R\u00e9gionale de Mons, CHU Ambroise Par\u00e9 Hospital, Boulevard Kennedy 2, 7000 Mons, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruddy","family":"Wattiez","sequence":"additional","affiliation":[{"name":"Laboratory of Proteomics and Microbiology, CISMa, Research Institute for Biosciences, University of Mons, Place du Parc 23, 7000 Mons, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Baptiste","family":"Leroy","sequence":"additional","affiliation":[{"name":"Laboratory of Proteomics and Microbiology, CISMa, Research Institute for Biosciences, University of Mons, Place du Parc 23, 7000 Mons, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7911-4649","authenticated-orcid":false,"given":"Elise","family":"Hennebert","sequence":"additional","affiliation":[{"name":"Laboratory of Cell Biology, Research Institute for Biosciences, Research Institute for Health Sciences and Technology, University of Mons, Place du Parc 23, 7000 Mons, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,6,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1016\/S0092-8674(00)80928-9","article-title":"The Hsp70 and Hsp60 Chaperone Machines","volume":"92","author":"Bukau","year":"1998","journal-title":"Cell"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1653","DOI":"10.1042\/BCJ20170380","article-title":"Hsp70 molecular chaperones: Multifunctional allosteric holding and unfolding machines","volume":"476","author":"Clerico","year":"2019","journal-title":"Biochem. J."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"670","DOI":"10.1007\/s00018-004-4464-6","article-title":"Hsp70 chaperones: Cellular functions and molecular mechanism","volume":"62","author":"Mayer","year":"2005","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1038\/s41580-019-0133-3","article-title":"The Hsp70 chaperone network","volume":"20","author":"Rosenzweig","year":"2019","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"10689","DOI":"10.1074\/jbc.REV120.011666","article-title":"Post-translational modifications of Hsp70 family proteins: Expanding the chaperone code","volume":"295","author":"Nitika","year":"2020","journal-title":"J. Biol. Chem."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1007\/s12192-016-0676-6","article-title":"The human HSP70 family of chaperones: Where do we stand?","volume":"21","author":"Radons","year":"2016","journal-title":"Cell Stress Chaperones"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Brocchieri, L., De Macario, E.C., and Macario, A.J. (2008). hsp70 genes in the human genome: Conservation and differentiation patterns predict a wide array of overlapping and specialized functions. BMC Evol. Biol., 8.","DOI":"10.1186\/1471-2148-8-19"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/s12192-008-0068-7","article-title":"Guidelines for the nomenclature of the human heat shock proteins","volume":"14","author":"Kampinga","year":"2009","journal-title":"Cell Stress Chaperones"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1074\/mcp.M112.020552","article-title":"Human sperm tail proteome suggests new endogenous metabolic pathways","volume":"12","author":"Amaral","year":"2013","journal-title":"Mol. Cell. Proteom."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1002\/pmic.201200350","article-title":"Head and flagella subcompartmental proteomic analysis of human spermatozoa","volume":"13","author":"Baker","year":"2013","journal-title":"Proteomics"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1002\/prca.200601013","article-title":"Identification of gene products present in Triton X-100 soluble and insoluble fractions of human spermatozoa lysates using LC-MS\/MS analysis","volume":"1","author":"Baker","year":"2007","journal-title":"Proteom. Clin. Appl."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1007\/s10815-020-01707-8","article-title":"Obesity significantly alters the human sperm proteome, with potential implications for fertility","volume":"37","author":"Pini","year":"2020","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3998","DOI":"10.1021\/acs.jproteome.6b00400","article-title":"Looking for missing proteins in the proteome of human spermatozoa: An update","volume":"15","author":"Vandenbrouck","year":"2016","journal-title":"J. Proteome Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1016\/j.jprot.2012.12.008","article-title":"In-depth proteomic analysis of the human sperm reveals complex protein compositions","volume":"79","author":"Wang","year":"2013","journal-title":"J. Proteom."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"5670","DOI":"10.1021\/pr500652y","article-title":"Identification of proteins involved in human sperm motility using high-throughput differential proteomics","volume":"13","author":"Amaral","year":"2014","journal-title":"J. Proteome Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1016\/j.fertnstert.2007.06.021","article-title":"The role of heat shock protein 70 (Hsp 70) in male infertility: Is it a line of defense against sperm DNA fragmentation?","volume":"90","author":"Erata","year":"2007","journal-title":"Fertil. Steril."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1007\/s10815-015-0465-7","article-title":"A proteomic analysis on human sperm tail: Comparison between normozoospermia and asthenozoospermia","volume":"32","author":"Hashemitabar","year":"2015","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1002\/mrd.23113","article-title":"Decreased expression of heat shock protein A4L in spermatozoa is positively related to poor human sperm quality","volume":"86","author":"Liu","year":"2019","journal-title":"Mol. Reprod. Dev."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1186\/s43043-020-00036-1","article-title":"Effects of vitamin D3 on the level of heat shock protein 70 and oxidative stress in human sperm: A pilot study","volume":"25","author":"Moghadam","year":"2020","journal-title":"Middle East Fertil. Soc. J."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Redgrove, K.A., Nixon, B., Baker, M.A., Hetherington, L., Baker, G., Liu, D.-Y., and Aitken, R.J. (2012). The molecular chaperone HSPA2 plays a key role in regulating the expression of sperm surface receptors that mediate sperm-egg recognition. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0050851"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1095\/biolreprod63.3.925","article-title":"Putative Creatine Kinase M-Isoform in Human Sperm Is Identified as the 70-Kilodalton Heat Shock Protein HspA21","volume":"63","author":"Huszar","year":"2000","journal-title":"Biol. Reprod."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1016\/S0015-0282(16)54975-9","article-title":"Sperm creatine phosphokinase M-isoform ratios and fertilizing potential of men: A blinded study of 84 couples treated with in vitro fertilization","volume":"57","author":"Huszar","year":"1992","journal-title":"Fertil. Steril."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1111\/j.1439-0272.2012.01315.x","article-title":"Evaluation of HSPA2 in fertile and infertile individuals","volume":"45","author":"Motiei","year":"2013","journal-title":"Andrologia"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1016\/S0015-0282(01)02892-8","article-title":"Decreased expression of heat shock protein hsp70\u20132 is associated with the pathogenesis of male infertility","volume":"76","author":"Feng","year":"2001","journal-title":"Fertil. Steril."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1097\/01.gco.0000193018.98061.2f","article-title":"Hyaluronic acid binding ability of human sperm reflects cellular maturity and fertilizing potential: Selection of sperm for intracytoplasmic sperm injection","volume":"18","author":"Huszar","year":"2006","journal-title":"Curr. Opin. Obstet. Gynecol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1093\/molehr\/gav041","article-title":"Novel characterization of the HSPA2-stabilizing protein BAG6 in human spermatozoa","volume":"21","author":"Bromfield","year":"2015","journal-title":"Mol. Hum. Reprod."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1093\/molehr\/gas064","article-title":"Investigation of the mechanisms by which the molecular chaperone HSPA2 regulates the expression of sperm surface receptors involved in human sperm-oocyte recognition","volume":"19","author":"Redgrove","year":"2013","journal-title":"Mol. Hum. Reprod."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.jri.2009.09.006","article-title":"Heat shock proteins on the human sperm surface","volume":"84","author":"Herr","year":"2010","journal-title":"J. Reprod. Immunol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"103246","DOI":"10.1016\/j.jri.2020.103246","article-title":"Human sperm chaperone HSPA2 distribution during in vitro capacitation","volume":"143","author":"Romero","year":"2021","journal-title":"J. Reprod. Immunol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2651","DOI":"10.1002\/jcp.22615","article-title":"Proteomic and functional analysis of human sperm detergent resistant membranes","volume":"226","author":"Nixon","year":"2011","journal-title":"J. Cell. Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"3377","DOI":"10.1021\/pr900031r","article-title":"Protein profile of capacitated versus ejaculated human sperm","volume":"8","author":"Secciani","year":"2009","journal-title":"J. Proteome Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"295","DOI":"10.3389\/fcell.2019.00295","article-title":"Proteomic Changes in Human Sperm During Sequential In Vitro Capacitation and Acrosome Reaction","volume":"7","author":"Castillo","year":"2019","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"103478","DOI":"10.1016\/j.jprot.2019.103478","article-title":"Proteomics analysis of asthenozoospermia and identification of glucose-6-phosphate isomerase as an important enzyme for sperm motility","volume":"208","author":"Guo","year":"2019","journal-title":"J. Proteom."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1093\/humrep\/den024","article-title":"Identification of proteomic differences in asthenozoospermic sperm samples","volume":"23","author":"Ballesca","year":"2008","journal-title":"Hum. Reprod."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"5861","DOI":"10.1016\/j.jprot.2012.07.003","article-title":"Sperm phosphoproteome profiling by ultra performance liquid chromatography followed by data independent analysis (LC\u2013MS(E)) reveals altered proteomic signatures in asthenozoospermia","volume":"75","author":"Parte","year":"2012","journal-title":"J. Proteom."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1074\/mcp.M116.061028","article-title":"Human Spermatozoa Quantitative Proteomic Signature Classifies Normo- and Asthenozoospermia","volume":"16","author":"Saraswat","year":"2017","journal-title":"Mol. Cell. Proteom."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1093\/molehr\/gaq009","article-title":"Proteomics-based study on asthenozoospermia: Differential expression of proteasome alpha complex","volume":"16","author":"Siva","year":"2010","journal-title":"Mol. Hum. Reprod."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1039\/D1MO00257K","article-title":"4D-quantitative proteomics signature of asthenozoospermia and identification of extracellular matrix protein 1 as a novel biomarker for sperm motility","volume":"18","author":"Yang","year":"2022","journal-title":"Mol. Omics"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1594","DOI":"10.3892\/mmr.2016.5434","article-title":"Screening targeted testis-specific genes for molecular assessment of aberrant sperm quality","volume":"14","author":"Liu","year":"2016","journal-title":"Mol. Med. Rep."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1111\/andr.12279","article-title":"Identification of protein changes in human spermatozoa throughout the cryopreservation process","volume":"5","author":"Bogle","year":"2017","journal-title":"Andrology"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1186\/s12014-019-9244-2","article-title":"Differential motility parameters and identification of proteomic profiles of human sperm cryopreserved with cryostraw and cryovial","volume":"16","author":"Li","year":"2019","journal-title":"Clin. Proteom."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"672862","DOI":"10.3389\/fcell.2021.672862","article-title":"Unraveling Subcellular and Ultrastructural Changes During Vitrification of Human Spermatozoa: Effect of a Mitochondria-Targeted Antioxidant and a Permeable Cryoprotectant","volume":"9","author":"Kumar","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1002\/pmic.201300225","article-title":"Proteomic Characteristics of Human Sperm Cryopreservation","volume":"14","author":"Wang","year":"2014","journal-title":"Proteomics"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1229","DOI":"10.1016\/j.jchromb.2008.11.013","article-title":"Multiple reaction monitoring for quantitative biomarker analysis in proteomics and metabolomics","volume":"877","author":"Kitteringham","year":"2009","journal-title":"J. Chromatogr. B Analyt. Technol. Biomed. Life Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1093\/bfgp\/eln056","article-title":"Current affairs in quantitative targeted proteomics: Multiple reaction monitoring-mass spectrometry","volume":"8","author":"Yocum","year":"2009","journal-title":"Brief. Funct. Genom."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1002\/pmic.200900574","article-title":"Analysis of proteomic changes associated with sperm capacitation through the combined use of IPG-strip pre-fractionation followed by RP chromatography LC-MS\/MS analysis","volume":"10","author":"Baker","year":"2010","journal-title":"Proteomics"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"11579","DOI":"10.1074\/jbc.M202325200","article-title":"Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein\/p97 during capacitation","volume":"278","author":"Ficarro","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/j.theriogenology.2018.12.025","article-title":"Comparative proteomic identification buffalo spermatozoa during in vitro capacitation","volume":"126","author":"Hou","year":"2019","journal-title":"Theriogenology"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"13821","DOI":"10.1038\/srep13821","article-title":"Proteomic approaches for profiling negative fertility markers in inferior boar spermatozoa","volume":"5","author":"Kwon","year":"2005","journal-title":"Sci. Rep."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1095\/biolreprod.105.041533","article-title":"Isolation and Proteomic Analysis of Mouse Sperm Detergent-Resistant Membrane Fractions: Evidence for Dissociation of Lipid Rafts During Capacitation","volume":"73","author":"Sleight","year":"2005","journal-title":"Biol. Reprod."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1104","DOI":"10.1074\/mcp.M114.045468","article-title":"Quantitative phosphoproteomics analysis reveals a key role of insulin growth factor 1 receptor (IGF1R) tyrosine kinase in human sperm capacitation","volume":"14","author":"Wang","year":"2015","journal-title":"Mol. Cell. Proteom."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1385","DOI":"10.1002\/pmic.200800353","article-title":"Role of translation by mitochondrial-type ribosomes during sperm capacitation: An analysis based on a proteomic approach","volume":"9","author":"Zhao","year":"2009","journal-title":"Proteomics"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1016\/j.ijbiomac.2013.07.014","article-title":"Characterization of sperm surface protein patterns of ejaculated and capacitated boar sperm, with the detection of ZP binding candidates","volume":"61","author":"Zigo","year":"2013","journal-title":"Int. J. Biol. Macomol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1186\/1477-7827-2-75","article-title":"Role of tyrosine phosphorylation in sperm capacitation \/ acrosome reaction","volume":"2","author":"Naz","year":"2004","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"4865","DOI":"10.1242\/jcs.02604","article-title":"Evidence for the involvement of PECAM-1 in a receptor mediated signal-transduction pathway regulating capacitation-associated tyrosine phosphorylation in human spermatozoa","volume":"118","author":"Nixon","year":"2005","journal-title":"J. Cell Sci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1210\/en.2009-0964","article-title":"Prolactin Exerts a Prosurvival Effect on Human Spermatozoa via Mechanisms that Involve the Stimulation of Akt Phosphorylation and Suppression of Caspase Activation and Capacitation","volume":"151","author":"Pujianto","year":"2010","journal-title":"Endocrinology"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"254","DOI":"10.4103\/0974-1208.197691","article-title":"The quality of sperm preparation medium affects the motility, viability, and DNA integrity of human spermatozoa","volume":"9","author":"Anbari","year":"2016","journal-title":"J. Hum. Reprod. Sci."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1530\/rep.1.00584","article-title":"Capacitation-associated protein tyrosine phosphorylation and membrane fluidity changes are impaired in the spermatozoa of asthenozoospermic patients","volume":"129","author":"Buffone","year":"2005","journal-title":"Reproduction"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1093\/humrep\/deac011","article-title":"The changing tide of human fertility","volume":"37","author":"Aitken","year":"2022","journal-title":"Hum. Reprod."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1093\/humupd\/dmx022","article-title":"Temporal trends in sperm count: A systematic review and meta-regression analysis","volume":"23","author":"Levine","year":"2017","journal-title":"Hum. Reprod. Update"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1177\/0960327117703690","article-title":"Decline in sperm count in European men during the past 50 years","volume":"37","author":"Sengupta","year":"2018","journal-title":"Hum. Exp. Toxicol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.urology.2019.06.038","article-title":"Total Motile Sperm Count Trend over Time: Evaluation of Semen Analyses From 119,972 Men from Subfertile Couples","volume":"132","author":"Tiegs","year":"2019","journal-title":"Urology"},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Agarwal, A., Panner Selvam, M.K., and Baskaran, S. (2020). Proteomic Analyses of Human Sperm Cells: Understanding the Role of Proteins and Molecular Pathways Affecting Male Reproductive Health. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21051621"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1093\/humupd\/dmt046","article-title":"The combined human sperm proteome: Cellular pathways and implications for basic and clinical science","volume":"20","author":"Amaral","year":"2014","journal-title":"Hum. Reprod. Update"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1649","DOI":"10.7150\/ijms.6395","article-title":"Mammalian sperm fertility related proteins","volume":"10","author":"Ashrafzadeh","year":"2013","journal-title":"Int. J. Med. Sci."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Bisconti, M., Simon, J.-F., Grassi, S., Leroy, B., Martinet, B., Arcolia, V., Isachenko, V., and Hennebert, E. (2021). Influence of Risk Factors for Male Infertility on Sperm Protein Composition. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms222313164"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1093\/molehr\/gap077","article-title":"Sperm surface proteomics: From protein lists to biological function","volume":"16","author":"Brewis","year":"2010","journal-title":"Mol. Hum. Reprod."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1586\/14789450.2015.1040769","article-title":"Advances in sperm proteomics: Best-practise methodology and clinical potential","volume":"12","author":"Codina","year":"2015","journal-title":"Expert Rev. Proteom."},{"key":"ref_69","first-page":"e13711","article-title":"Proteomics and metabolomics\u2014Current and future perspectives in clinical andrology","volume":"53","author":"Finelli","year":"2021","journal-title":"Andrologia"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/0888-7543(92)90409-L","article-title":"The human heat-shock genes HSPA6 and HSPA7 are both expressed and localize to chromosome 1","volume":"12","author":"Leung","year":"1992","journal-title":"Genomics"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1379\/CSC-278e.1","article-title":"Hsp70B\u2032 regulation and function","volume":"12","author":"Noonan","year":"2007","journal-title":"Cell Stress Chaperones"},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Singh, R., and Singh, K. (2017). Sperm Capacitation: The Obligate Requirement for Male Fertility. Male Infertility: Understanding, Causes and Treatment, Springer.","DOI":"10.1007\/978-981-10-4017-7"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"3600","DOI":"10.18632\/oncotarget.12274","article-title":"Factors and pathways involved in capacitation: How are they regulated?","volume":"8","author":"Jin","year":"2017","journal-title":"Oncotarget"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"72","DOI":"10.3389\/fcell.2018.00072","article-title":"Molecular Basis of Human Sperm Capacitation","volume":"6","author":"Luque","year":"2018","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"3645","DOI":"10.1242\/jcs.01214","article-title":"Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition","volume":"117","author":"Asquith","year":"2004","journal-title":"J. Cell Sci."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1530\/REP-12-0316","article-title":"The function of chaperone proteins in the assemblage of protein complexes involved in gamete adhesion and fusion processes","volume":"145","author":"Bromfield","year":"2013","journal-title":"Reproduction"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1801","DOI":"10.1095\/biolreprod.103.017350","article-title":"Tyrosine phosphorylation of HSP-90 during mammalian sperm capacitation","volume":"69","author":"Ecroyd","year":"2003","journal-title":"Biol. Reprod."},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Li, K., Xue, Y., Chen, A., Jiang, Y., Xie, H., Shi, Q., Zhang, S., and Ni, Y. (2014). Heat shock protein 90 has roles in intracellular calcium homeostasis, protein tyrosine phosphorylation regulation, and progesterone-responsive sperm function in human sperm. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0115841"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1186\/s12958-021-00723-2","article-title":"Hsp90 modulates human sperm capacitation via the Erk1\/2 and p38 MAPK signaling pathways","volume":"19","author":"Sun","year":"2021","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1095\/biolreprod.107.066860","article-title":"Identification of the Molecular Chaperone, Heat Shock Protein 1 (Chaperonin 10), in the Reproductive Tract and in Capacitating Spermatozoa in the Male Mouse","volume":"78","author":"Walsh","year":"2008","journal-title":"Biol. Reprod."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1111\/j.1439-0272.2004.00629.x","article-title":"Immunolocalization of heat shock protein 70 in bovine spermatozoa","volume":"36","author":"Kamaruddin","year":"2004","journal-title":"Andrologia"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1574","DOI":"10.1016\/j.fertnstert.2008.12.132","article-title":"Glucose-regulated protein 78 (Grp78\/BiP) is secreted by human oviduct epithelial cells and the recombinant protein modulates sperm\u2013zona pellucida binding","volume":"93","author":"Munuce","year":"2010","journal-title":"Fertil. Steril."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1002\/mrd.20367","article-title":"Immunolocalization of heat shock protein 70 (Hsp 70) in boar spermatozoa and its role during fertilization","volume":"72","author":"Spinaci","year":"2005","journal-title":"Mol. Reprod. Dev."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1111\/j.1439-0531.2007.00918.x","article-title":"Comparative Immunolocalization of Heat Shock Proteins (Hsp)-60, -70, -90 in Boar, Stallion, Dog and Cat Spermatozoa","volume":"43","author":"Volpe","year":"2008","journal-title":"Reprod. Domest. Anim."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1093\/molehr\/gah226","article-title":"Bicarbonate and bovine serum albumin reversibly \u2018switch\u2019 capacitation-induced events in human spermatozoa","volume":"11","author":"Moseley","year":"2005","journal-title":"Mol. Hum. Reprod."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1093\/oxfordjournals.humrep.a138099","article-title":"Chemical composition and protein source in the capacitation medium significantly affect the ability of human spermatozoa to undergo follicular fluid induced acrosome reaction","volume":"8","author":"Calvo","year":"1993","journal-title":"Hum. Reprod."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"11039","DOI":"10.1073\/pnas.92.24.11039","article-title":"Sperm capacitation in humans is transient and correlates with chemotactic responsiveness to follicular factors","volume":"92","author":"Dor","year":"1995","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"447","DOI":"10.4103\/aja.aja_104_19","article-title":"Influence of in vitro capacitation time on structural and functional human sperm parameters","volume":"22","author":"Aizpurua","year":"2020","journal-title":"Asian J. Androl."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1111\/j.1365-2605.2008.00948.x","article-title":"Localization of Hsp60 and Grp78 in the human testis, epididymis and mature spermatozoa","volume":"33","author":"Lachance","year":"2010","journal-title":"Int. J. Androl."},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Lobo, V., Rao, P., Gajbhiye, R., Kulkarni, V., and Parte, P. (2015). Glucose Regulated Protein 78 Phosphorylation in Sperm Undergoes Dynamic Changes during Maturation. PLoS ONE, 30.","DOI":"10.1371\/journal.pone.0141858"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.gene.2017.03.005","article-title":"HSPA5 Gene encoding Hsp70 chaperone BiP in the endoplasmic reticulum","volume":"618","author":"Wang","year":"2017","journal-title":"Gene"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1007\/BF00261831","article-title":"Changes in endoplasmic reticulum during spermiogenesis in the mouse","volume":"257","author":"Nakamoto","year":"1989","journal-title":"Cell Tissue Res."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1159\/000145305","article-title":"Development of the endoplasmic reticulam during human spermatogenesis","volume":"108","author":"Nistal","year":"1980","journal-title":"Acta Anat."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1093\/molehr\/gar037","article-title":"Highly purified spermatozoal RNA obtained by a novel method indicates an unusual 28S\/18S rRNA ratio and suggests impaired ribosome assembly","volume":"17","author":"Schulze","year":"2011","journal-title":"Mol. Hum. Reprod."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"e12919","DOI":"10.1111\/and.12919","article-title":"Towards the identification of reliable sperm biomarkers for male infertility: A sperm proteomic approach","volume":"50","author":"Intasqui","year":"2018","journal-title":"Andrologia"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"2517","DOI":"10.1074\/mcp.M110.001719","article-title":"Systematic Mapping and Functional Analysis of a Family of Human Epididymal Secretory Sperm-Located Proteins","volume":"9","author":"Li","year":"2010","journal-title":"Mol. Cell. Proteom."},{"key":"ref_97","first-page":"e53913","article-title":"TMEM95 is a sperm membrane protein essential for mammalian fertilization","volume":"2","author":"Hamze","year":"2020","journal-title":"eLife"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1080\/01485010390219656","article-title":"Asthenozoospermia: Analysis of a large population","volume":"49","author":"Curi","year":"2003","journal-title":"Arch. Androl."},{"key":"ref_99","unstructured":"World Health Organization (2021). WHO Laboratory Manual for the Examination and Processing of Human Semen, World Health Organization. [6th ed.]."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"662","DOI":"10.1093\/humrep\/15.3.662","article-title":"Bacterial contamination and sperm recovery after semen preparation by density gradient centrifugation using silane-coated silica particles at different g forces","volume":"15","author":"Nicholson","year":"2000","journal-title":"Hum. Reprod."},{"key":"ref_101","doi-asserted-by":"crossref","unstructured":"Alqu\u00e9zar-Baeta, C., Gimeno-Martos, S., Miguel-Jim\u00e9nez, S., Santolaria, P., Y\u00e1niz, J., Palac\u00edn, I., Casao, A., \u00c1lvaro Cebri\u00e1n-P\u00e9rez, J., Mui\u00f1o-Blanco, T., and P\u00e9rez-P\u00e9, R. (2019). OpenCASA: A new open-source and scalable tool for sperm quality analysis. PLoS Comput. Biol., 15.","DOI":"10.1371\/journal.pcbi.1006691"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/0303-7207(95)03733-0","article-title":"The extragenomic action of progesterone on human spermatozoa is influenced by redox regulated changes in tyrosine phosphorylation during capacitation","volume":"117","author":"Aitken","year":"1996","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"e14226","DOI":"10.1111\/and.14226","article-title":"Identifying new sperm Western blot loading controls","volume":"53","author":"Feng","year":"2021","journal-title":"Andrologia"},{"key":"ref_104","doi-asserted-by":"crossref","unstructured":"Moscatelli, N., Lunetti, P., Braccia, C., Armirotti, A., Pisanello, F., De Vittorio, M., Zara, V., and Ferramosca, A. (2019). Comparative Proteomic Analysis of Proteins Involved in Bioenergetics Pathways Associated with Human Sperm Motility. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20123000"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"941","DOI":"10.1080\/14789450.2019.1693895","article-title":"Post-translational modifications of seminal proteins and their importance in male fertility potential","volume":"16","author":"Maciel","year":"2019","journal-title":"Expert Rev. Proteom."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"2839","DOI":"10.1074\/mcp.M116.059311","article-title":"A Human Lectin Microarray for Sperm Surface Glycosylation Analysis","volume":"15","author":"Sun","year":"2016","journal-title":"Mol. Cell. Proteom."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"2597","DOI":"10.1002\/pmic.201600233","article-title":"The human sperm proteome 2.0: An integrated resource for studying sperm functions at the level of posttranslational modification","volume":"16","author":"Wang","year":"2016","journal-title":"Proteomics"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/12\/6497\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:27:39Z","timestamp":1760138859000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/12\/6497"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,6,10]]},"references-count":107,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,6]]}},"alternative-id":["ijms23126497"],"URL":"https:\/\/doi.org\/10.3390\/ijms23126497","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-1580054\/v1","asserted-by":"object"}]},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,6,10]]}}}