Dynamic resolution of acrosomal exocytosis in human sperm
An essential step in mammalian fertilisation is the sperm acrosome reaction (AR) - exocytosis of a single large vesicle (the acrosome) that surrounds the nucleus at the apical sperm head. The acrosomal and plasma membranes fuse, resulting in both the release of factors that might facilitate penetrat...
Saved in:
Published in | Journal of cell science Vol. 121; no. 13; pp. 2130 - 2135 |
---|---|
Main Authors | , , , , |
Format | Journal Article |
Language | English |
Published |
England
The Company of Biologists Limited
01.07.2008
|
Subjects | |
Online Access | Get full text |
ISSN | 0021-9533 1477-9137 |
DOI | 10.1242/jcs.030379 |
Cover
Loading…
Abstract | An essential step in mammalian fertilisation is the sperm acrosome reaction (AR) - exocytosis of a single large vesicle (the acrosome) that surrounds the nucleus at the apical sperm head. The acrosomal and plasma membranes fuse, resulting in both the release of factors that might facilitate penetration of the zona pellucida (which invests the egg) and the externalisation of membrane components required for gamete fusion. Exocytosis in somatic cells is a rapid process - typically complete within milliseconds - yet acrosomal enzymes are required throughout zona penetration - a period of minutes. Here, we present the first studies of this crucial and complex event occurring in real-time in individual live sperm using time-lapse fluorescence microscopy. Simultaneous imaging of separate probes for acrosomal content and inner acrosomal membrane show that rapid membrane fusion, initiated at the cell apex, is followed by exceptionally slow dispersal of acrosomal content (up to 12 minutes). Cells that lose their acrosome prematurely (spontaneous AR), compromising their ability to penetrate the egg vestments, are those that are already subject to a loss of motility and viability. Cells undergoing stimulus-induced AR (progesterone or A23187) remain viable, with a proportion remaining motile (progesterone). These findings suggest that the AR is a highly adapted form of exocytosis. |
---|---|
AbstractList | An essential step in mammalian fertilisation is the sperm acrosome reaction (AR) - exocytosis of a single large vesicle (the acrosome) that surrounds the nucleus at the apical sperm head. The acrosomal and plasma membranes fuse, resulting in both the release of factors that might facilitate penetration of the zona pellucida (which invests the egg) and the externalisation of membrane components required for gamete fusion. Exocytosis in somatic cells is a rapid process - typically complete within milliseconds - yet acrosomal enzymes are required throughout zona penetration - a period of minutes. Here, we present the first studies of this crucial and complex event occurring in real-time in individual live sperm using time-lapse fluorescence microscopy. Simultaneous imaging of separate probes for acrosomal content and inner acrosomal membrane show that rapid membrane fusion, initiated at the cell apex, is followed by exceptionally slow dispersal of acrosomal content (up to 12 minutes). Cells that lose their acrosome prematurely (spontaneous AR), compromising their ability to penetrate the egg vestments, are those that are already subject to a loss of motility and viability. Cells undergoing stimulus-induced AR (progesterone or A23187) remain viable, with a proportion remaining motile (progesterone). These findings suggest that the AR is a highly adapted form of exocytosis.An essential step in mammalian fertilisation is the sperm acrosome reaction (AR) - exocytosis of a single large vesicle (the acrosome) that surrounds the nucleus at the apical sperm head. The acrosomal and plasma membranes fuse, resulting in both the release of factors that might facilitate penetration of the zona pellucida (which invests the egg) and the externalisation of membrane components required for gamete fusion. Exocytosis in somatic cells is a rapid process - typically complete within milliseconds - yet acrosomal enzymes are required throughout zona penetration - a period of minutes. Here, we present the first studies of this crucial and complex event occurring in real-time in individual live sperm using time-lapse fluorescence microscopy. Simultaneous imaging of separate probes for acrosomal content and inner acrosomal membrane show that rapid membrane fusion, initiated at the cell apex, is followed by exceptionally slow dispersal of acrosomal content (up to 12 minutes). Cells that lose their acrosome prematurely (spontaneous AR), compromising their ability to penetrate the egg vestments, are those that are already subject to a loss of motility and viability. Cells undergoing stimulus-induced AR (progesterone or A23187) remain viable, with a proportion remaining motile (progesterone). These findings suggest that the AR is a highly adapted form of exocytosis. An essential step in mammalian fertilisation is the sperm acrosome reaction (AR) - exocytosis of a single large vesicle (the acrosome) that surrounds the nucleus at the apical sperm head. The acrosomal and plasma membranes fuse, resulting in both the release of factors that might facilitate penetration of the zona pellucida (which invests the egg) and the externalisation of membrane components required for gamete fusion. Exocytosis in somatic cells is a rapid process - typically complete within milliseconds - yet acrosomal enzymes are required throughout zona penetration - a period of minutes. Here, we present the first studies of this crucial and complex event occurring in real-time in individual live sperm using time-lapse fluorescence microscopy. Simultaneous imaging of separate probes for acrosomal content and inner acrosomal membrane show that rapid membrane fusion, initiated at the cell apex, is followed by exceptionally slow dispersal of acrosomal content (up to 12 minutes). Cells that lose their acrosome prematurely (spontaneous AR), compromising their ability to penetrate the egg vestments, are those that are already subject to a loss of motility and viability. Cells undergoing stimulus-induced AR (progesterone or A23187) remain viable, with a proportion remaining motile (progesterone). These findings suggest that the AR is a highly adapted form of exocytosis. |
Author | White, Michael R.H Harper, Claire V Publicover, Stephen J Johnson, Peter M Cummerson, Joanne A |
Author_xml | – sequence: 1 fullname: Harper, Claire V – sequence: 2 fullname: Cummerson, Joanne A – sequence: 3 fullname: White, Michael R.H – sequence: 4 fullname: Publicover, Stephen J – sequence: 5 fullname: Johnson, Peter M |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/18522990$$D View this record in MEDLINE/PubMed |
BookMark | eNqF0DtPwzAUhmELFdELLPwAyMSAFDi24zoeUblKlRigs-U4NrhK4mInEv33pEphQEhMZ3nON7xTNGp8YxA6xXCFSUau1zpeAQXKxQGa4IzzVGDKR2gCQHAqGKVjNI1xDQCcCH6ExjhnhAgBEyRut42qnU6Cib7qWuebxNtE6eCjr1WVmE-vt62PLiauSd67WjVJ3JhQH6NDq6poTvZ3hlb3d6-Lx3T5_PC0uFmmOuOiTQtmrdWgAXDGTMZsRgrFLLGMgc3AGqZzWzJtuS1L2uP-MqqN5nNQXBV0hi6G3U3wH52Jraxd1KaqVGN8F-VcEEoZzf-FGZ_zOclJD8_2sCtqU8pNcLUKW_ldpQcwgF2FGIyV2rVq16YNylUSg9yFl314OYTvXy5_vfys_oXPB2yVl-otuChXLwQwBRDAcyHoFw1MjbQ |
CitedBy_id | crossref_primary_10_3389_fcell_2023_1125988 crossref_primary_10_1007_s10815_020_01854_y crossref_primary_10_1177_1933719116641766 crossref_primary_10_1074_jbc_M112_392803 crossref_primary_10_3389_fendo_2023_1135973 crossref_primary_10_1073_pnas_2212338120 crossref_primary_10_1111_j_1600_0897_2009_00758_x crossref_primary_10_1093_humrep_deu018 crossref_primary_10_4161_cib_3_6_13137 crossref_primary_10_1111_j_2047_2927_2013_00088_x crossref_primary_10_1074_jbc_M115_677799 crossref_primary_10_1002_jcp_21781 crossref_primary_10_3390_ijms231911253 crossref_primary_10_1016_j_theriogenology_2019_05_038 crossref_primary_10_1095_biolreprod_115_131201 crossref_primary_10_1091_mbc_e13_09_0523 crossref_primary_10_1093_humupd_dmz032 crossref_primary_10_1016_j_fertnstert_2012_03_002 crossref_primary_10_4161_cib_2_5_8716 crossref_primary_10_1002_mrd_23431 crossref_primary_10_1016_j_bbrc_2016_05_003 crossref_primary_10_1242_jcs_100867 crossref_primary_10_1093_molehr_gau110 crossref_primary_10_1074_jbc_M113_450981 crossref_primary_10_1095_biolreprod_114_119768 crossref_primary_10_1186_s12958_015_0118_9 crossref_primary_10_1530_REP_09_0434 crossref_primary_10_1242_jcs_058263 crossref_primary_10_1098_rsob_200322 crossref_primary_10_1039_C7MB00379J crossref_primary_10_1016_j_rbmo_2013_05_004 crossref_primary_10_1007_s00726_016_2211_6 crossref_primary_10_1007_s13577_020_00348_4 crossref_primary_10_1186_s12958_019_0531_6 crossref_primary_10_1002_jez_1718 crossref_primary_10_1093_humupd_dmw014 crossref_primary_10_1007_s00441_015_2238_0 crossref_primary_10_1530_REP_09_0134 crossref_primary_10_2478_v10042_009_0059_2 crossref_primary_10_4161_cib_27362 crossref_primary_10_1152_physrev_00028_2010 |
Cites_doi | 10.1242/jcs.32.1.177 10.1242/dev.02752 10.1016/j.ydbio.2006.12.023 10.1093/molehr/5.3.214 10.1095/biolreprod64.1.148 10.1016/0006-291X(89)92508-4 10.1016/S0006-3495(96)79368-2 10.1111/j.1365-2567.2006.02374.x 10.1074/jbc.M401194200 10.1016/S0021-9258(18)31772-1 10.3109/01485018108999319 10.1038/ncb0307-235 10.1093/molehr/8.8.722 10.1095/biolreprod.106.054627 10.1093/oxfordjournals.humrep.a136976 10.1074/jbc.M202856200 10.1530/jrf.0.0740383 10.1371/journal.pbio.0030323 10.1093/oxfordjournals.humrep.a137910 10.1111/j.0022-2720.2004.01404.x 10.1111/j.1365-2605.2006.00681.x 10.1016/S0015-0282(16)57072-1 10.1016/S0015-0282(16)60021-3 10.1016/S0015-0282(02)04555-7 10.1006/dbio.2000.9729 10.1126/science.7985030 10.1016/0012-1606(91)90133-N 10.1095/biolreprod.102.009175 10.1095/biolreprod41.2.285 10.1042/bj20021560 10.1002/mrd.1120200103 |
ContentType | Journal Article |
DBID | FBQ AAYXX CITATION CGR CUY CVF ECM EIF NPM 7S9 L.6 7X8 |
DOI | 10.1242/jcs.030379 |
DatabaseName | AGRIS CrossRef Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed AGRICOLA AGRICOLA - Academic MEDLINE - Academic |
DatabaseTitle | CrossRef MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) AGRICOLA AGRICOLA - Academic MEDLINE - Academic |
DatabaseTitleList | MEDLINE - Academic MEDLINE AGRICOLA CrossRef |
Database_xml | – sequence: 1 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database – sequence: 3 dbid: FBQ name: AGRIS url: http://www.fao.org/agris/Centre.asp?Menu_1ID=DB&Menu_2ID=DB1&Language=EN&Content=http://www.fao.org/agris/search?Language=EN sourceTypes: Publisher |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Biology |
EISSN | 1477-9137 |
EndPage | 2135 |
ExternalDocumentID | 18522990 10_1242_jcs_030379 US201300907899 |
Genre | Research Support, Non-U.S. Gov't Journal Article |
GrantInformation_xml | – fundername: Biotechnology and Biological Sciences Research Council grantid: BB/E012965/1 |
GroupedDBID | --- -DZ -~X .55 .GJ 0R~ 18M 2WC 34G 39C 3O- 4.4 4R4 53G 5GY 5RE 5VS 85S ABDNZ ABEFU ABJNI ABPPZ ABTAH ACGFO ACGFS ACIWK ACNCT ACPRK ACYGS ADBBV ADCOW ADVGF AEILP AENEX AETEA AFFNX AFRAH AGGIJ AI. ALMA_UNASSIGNED_HOLDINGS BAWUL BTFSW C1A CS3 DIK DU5 E3Z EBS EJD F5P F9R FBQ GX1 H13 HZ~ IH2 INIJC KQ8 MVM O9- OHT OK1 P2P R.V RCB RHI RNS SJN TN5 TR2 UPT VH1 W2D W8F WH7 WOQ X7M XOL YQI YQT ZGI ZXP ZY4 ~02 ~KM AAYXX CITATION CGR CUY CVF ECM EIF NPM 7S9 L.6 7X8 |
ID | FETCH-LOGICAL-c479t-b5fffc0c00145e45f42ba5f2f550f40fe5c8fd5cf7fdd35ff7fd53cec760a7ab3 |
ISSN | 0021-9533 |
IngestDate | Fri Jul 11 01:53:39 EDT 2025 Fri Jul 11 10:58:47 EDT 2025 Fri May 30 11:01:53 EDT 2025 Tue Jul 01 00:50:35 EDT 2025 Thu Apr 24 23:12:49 EDT 2025 Thu Apr 03 09:45:11 EDT 2025 |
IsDoiOpenAccess | false |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
Issue | 13 |
Language | English |
LinkModel | OpenURL |
MergedId | FETCHMERGED-LOGICAL-c479t-b5fffc0c00145e45f42ba5f2f550f40fe5c8fd5cf7fdd35ff7fd53cec760a7ab3 |
Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
OpenAccessLink | https://journals.biologists.com/jcs/article-pdf/121/13/2130/1506142/2130.pdf |
PMID | 18522990 |
PQID | 47676282 |
PQPubID | 24069 |
PageCount | 6 |
ParticipantIDs | proquest_miscellaneous_69233538 proquest_miscellaneous_47676282 pubmed_primary_18522990 crossref_citationtrail_10_1242_jcs_030379 crossref_primary_10_1242_jcs_030379 fao_agris_US201300907899 |
ProviderPackageCode | CITATION AAYXX |
PublicationCentury | 2000 |
PublicationDate | 2008-07-01 |
PublicationDateYYYYMMDD | 2008-07-01 |
PublicationDate_xml | – month: 07 year: 2008 text: 2008-07-01 day: 01 |
PublicationDecade | 2000 |
PublicationPlace | England |
PublicationPlace_xml | – name: England |
PublicationTitle | Journal of cell science |
PublicationTitleAlternate | J Cell Sci |
PublicationYear | 2008 |
Publisher | The Company of Biologists Limited |
Publisher_xml | – name: The Company of Biologists Limited |
References | 2021042520190512200_REF8 2021042520190512200_REF9 2021042520190512200_REF6 2021042520190512200_REF7 2021042520190512200_REF16 2021042520190512200_REF15 2021042520190512200_REF14 2021042520190512200_REF13 2021042520190512200_REF19 2021042520190512200_REF18 2021042520190512200_REF17 2021042520190512200_REF30 2021042520190512200_REF12 2021042520190512200_REF34 2021042520190512200_REF11 2021042520190512200_REF33 2021042520190512200_REF10 2021042520190512200_REF32 2021042520190512200_REF31 2021042520190512200_REF27 2021042520190512200_REF26 2021042520190512200_REF25 2021042520190512200_REF24 2021042520190512200_REF29 2021042520190512200_REF28 2021042520190512200_REF1 2021042520190512200_REF4 2021042520190512200_REF23 2021042520190512200_REF5 2021042520190512200_REF22 2021042520190512200_REF2 2021042520190512200_REF21 2021042520190512200_REF3 2021042520190512200_REF20 |
References_xml | – ident: 2021042520190512200_REF8 doi: 10.1242/jcs.32.1.177 – ident: 2021042520190512200_REF5 doi: 10.1242/dev.02752 – ident: 2021042520190512200_REF15 doi: 10.1016/j.ydbio.2006.12.023 – ident: 2021042520190512200_REF13 doi: 10.1093/molehr/5.3.214 – ident: 2021042520190512200_REF16 doi: 10.1095/biolreprod64.1.148 – ident: 2021042520190512200_REF22 doi: 10.1016/0006-291X(89)92508-4 – ident: 2021042520190512200_REF23 doi: 10.1016/S0006-3495(96)79368-2 – ident: 2021042520190512200_REF6 doi: 10.1111/j.1365-2567.2006.02374.x – ident: 2021042520190512200_REF10 doi: 10.1074/jbc.M401194200 – ident: 2021042520190512200_REF4 doi: 10.1016/S0021-9258(18)31772-1 – ident: 2021042520190512200_REF14 doi: 10.3109/01485018108999319 – ident: 2021042520190512200_REF24 doi: 10.1038/ncb0307-235 – ident: 2021042520190512200_REF33 – ident: 2021042520190512200_REF27 doi: 10.1093/molehr/8.8.722 – ident: 2021042520190512200_REF11 doi: 10.1095/biolreprod.106.054627 – ident: 2021042520190512200_REF12 doi: 10.1093/oxfordjournals.humrep.a136976 – ident: 2021042520190512200_REF32 doi: 10.1074/jbc.M202856200 – ident: 2021042520190512200_REF31 – ident: 2021042520190512200_REF28 doi: 10.1530/jrf.0.0740383 – ident: 2021042520190512200_REF7 doi: 10.1371/journal.pbio.0030323 – ident: 2021042520190512200_REF1 doi: 10.1093/oxfordjournals.humrep.a137910 – ident: 2021042520190512200_REF25 doi: 10.1111/j.0022-2720.2004.01404.x – ident: 2021042520190512200_REF21 doi: 10.1111/j.1365-2605.2006.00681.x – ident: 2021042520190512200_REF3 doi: 10.1016/S0015-0282(16)57072-1 – ident: 2021042520190512200_REF29 doi: 10.1016/S0015-0282(16)60021-3 – ident: 2021042520190512200_REF20 doi: 10.1016/S0015-0282(02)04555-7 – ident: 2021042520190512200_REF17 doi: 10.1006/dbio.2000.9729 – ident: 2021042520190512200_REF26 doi: 10.1126/science.7985030 – ident: 2021042520190512200_REF18 doi: 10.1016/0012-1606(91)90133-N – ident: 2021042520190512200_REF30 doi: 10.1095/biolreprod.102.009175 – ident: 2021042520190512200_REF2 doi: 10.1095/biolreprod41.2.285 – ident: 2021042520190512200_REF9 doi: 10.1042/bj20021560 – ident: 2021042520190512200_REF19 – ident: 2021042520190512200_REF34 doi: 10.1002/mrd.1120200103 |
SSID | ssj0007297 |
Score | 2.1274426 |
Snippet | An essential step in mammalian fertilisation is the sperm acrosome reaction (AR) - exocytosis of a single large vesicle (the acrosome) that surrounds the... An essential step in mammalian fertilisation is the sperm acrosome reaction (AR) – exocytosis of a single large vesicle (the acrosome) that surrounds the... |
SourceID | proquest pubmed crossref fao |
SourceType | Aggregation Database Index Database Enrichment Source Publisher |
StartPage | 2130 |
SubjectTerms | Acrosome - physiology Acrosome Reaction Animals Exocytosis Female Humans Kinetics Male Membrane Fusion Microscopy, Fluorescence Sperm Capacitation Sperm-Ovum Interactions Spermatozoa - physiology Spermatozoa - ultrastructure Zona Pellucida - physiology |
Title | Dynamic resolution of acrosomal exocytosis in human sperm |
URI | https://www.ncbi.nlm.nih.gov/pubmed/18522990 https://www.proquest.com/docview/47676282 https://www.proquest.com/docview/69233538 |
Volume | 121 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnR1ra9UwNLiJ4BfxvatTA_pFLp29TdLHR5nKmCg-dmHfSpImY7DbXrZecP76nZOkzS7ugvqlLU1Iyjmn55HzIuSNzAsty0YkhZRVwrXGIACVJgqEg2mqkhkXTfjla34w54fH4jj2bHXZJb3a079vzCv5H6zCO8ArZsn-A2bHReEFPAN-4QoYhutf4fiDbyc_BZM57OPc-ij5ugXA3vzq9GXfYc2R0za048PK4IsNKime4k-DTIys6XwZkgXPJPDHGBW7v3KH3t5tf9hJ4NjxZHRsvBfi8qc_YhqEPyocYkdDnFnwTw0HEOUYrBoTAmboBWZrTDWbXaOeb_10xtbYpHfG_MG_QWFA_q0v9oD5MN9m5hoilwuHSUz4RjEaZdgYWTgMbZHbGRgO2NPi8_dYPx5MidDE139yKFgL276Lm2Ih2bDMmrayZWW32RBxCsnRfXIvoI2-92TxgNwy7UNyx_cWvXxEqkAcNBIH7SwdiYNG4qCnLXXEQR1xPCbzTx-P9g-S0Ccj0byo-kQJa61ONZq7wnBheaaksJkF69Py1BqhS9sIbQvbNAwmw10wbXSRp7KQij0h223Xmh1CZ6YBDRYW1JkB1bKSloMGzBUTKYPfXU3I2wEetQ5F5LGXyVmNxiSAsQYw1h6ME_J6nLv0pVNunLUDYK3lCci0ev4zQ096WmETBBh6NcC6BqaH_4BsTbe6qHmRgxAvs80zcjBcGAjzCXnqkRQ_IaD22caR5-RupPNdst2fr8wLUD179dJR0xXxYoHW |
linkProvider | Colorado Alliance of Research Libraries |
openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Dynamic+resolution+of+acrosomal+exocytosis+in+human+sperm&rft.jtitle=Journal+of+cell+science&rft.au=Harper%2C+Claire+V&rft.au=Cummerson%2C+Joanne+A&rft.au=White%2C+Michael+R+H&rft.au=Publicover%2C+Stephen+J&rft.date=2008-07-01&rft.issn=0021-9533&rft.volume=121&rft.issue=Pt+13&rft.spage=2130&rft_id=info:doi/10.1242%2Fjcs.030379&rft_id=info%3Apmid%2F18522990&rft.externalDocID=18522990 |
thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0021-9533&client=summon |
thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0021-9533&client=summon |
thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0021-9533&client=summon |