دورية أكاديمية
أعرض في EDS

Egg multivesicular bodies elicit an LC3-associated phagocytosis-like pathway to degrade paternal mitochondria after fertilization.

التفاصيل البيبلوغرافية
العنوان: Egg multivesicular bodies elicit an LC3-associated phagocytosis-like pathway to degrade paternal mitochondria after fertilization.
المؤلفون: Ben-Hur S; Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel., Sernik S; Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel., Afar S; Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel., Kolpakova A; Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel., Politi Y; Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel., Gal L; Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel., Florentin A; Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel.; Department of Microbiology and Molecular Genetics, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel., Golani O; Department of Life Sciences Core Facilities, Weizmann Institute of Science, Rehovot, Israel., Sivan E; Department of Life Sciences Core Facilities, Weizmann Institute of Science, Rehovot, Israel., Dezorella N; Department of Chemical Research Support, Weizmann Institute of Science, Rehovot, Israel., Morgenstern D; de Botton Institute for Protein Profiling, The Nancy and Stephen Grand Israel National Center for Personalised Medicine, Weizmann Institute of Science, Rehovot, Israel., Pietrokovski S; Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel., Schejter E; Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel., Yacobi-Sharon K; Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel., Arama E; Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel. eli.arama@weizmann.ac.il.
المصدر: Nature communications [Nat Commun] 2024 Jul 08; Vol. 15 (1), pp. 5715. Date of Electronic Publication: 2024 Jul 08.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Pub. Group Country of Publication: England NLM ID: 101528555 Publication Model: Electronic Cited Medium: Internet ISSN: 2041-1723 (Electronic) Linking ISSN: 20411723 NLM ISO Abbreviation: Nat Commun Subsets: MEDLINE
أسماء مطبوعة: Original Publication: [London] : Nature Pub. Group
مواضيع طبية MeSH: Mitochondria*/metabolism , Fertilization* , Phagocytosis* , Drosophila Proteins*/metabolism , Drosophila Proteins*/genetics , Spermatozoa*/metabolism , Multivesicular Bodies*/metabolism, Animals ; Male ; Female ; Drosophila melanogaster/metabolism ; Microtubule-Associated Proteins/metabolism ; Microtubule-Associated Proteins/genetics ; Ovum/metabolism ; Lysosomes/metabolism ; Sperm Tail/metabolism ; Mitophagy
مستخلص: Mitochondria are maternally inherited, but the mechanisms underlying paternal mitochondrial elimination after fertilization are far less clear. Using Drosophila, we show that special egg-derived multivesicular body vesicles promote paternal mitochondrial elimination by activating an LC3-associated phagocytosis-like pathway, a cellular defense pathway commonly employed against invading microbes. Upon fertilization, these egg-derived vesicles form extended vesicular sheaths around the sperm flagellum, promoting degradation of the sperm mitochondrial derivative and plasma membrane. LC3-associated phagocytosis cascade of events, including recruitment of a Rubicon-based class III PI(3)K complex to the flagellum vesicular sheaths, its activation, and consequent recruitment of Atg8/LC3, are all required for paternal mitochondrial elimination. Finally, lysosomes fuse with strings of large vesicles derived from the flagellum vesicular sheaths and contain degrading fragments of the paternal mitochondrial derivative. Given reports showing that in some mammals, the paternal mitochondria are also decorated with Atg8/LC3 and surrounded by multivesicular bodies upon fertilization, our findings suggest that a similar pathway also mediates paternal mitochondrial elimination in other flagellated sperm-producing organisms.
(© 2024. The Author(s).)
References: Cell Res. 2016 Aug;26(8):865-6. (PMID: 27297234)
Biol Reprod. 1970 Jun;2:Suppl 2:177-20. (PMID: 4939239)
Cell Tissue Res. 1979 Jan 30;196(1):1-22. (PMID: 421242)
Sci Adv. 2022 Oct 28;8(43):eabo1274. (PMID: 36288315)
Development. 2015 May 1;142(9):1705-16. (PMID: 25922527)
Nat Rev Mol Cell Biol. 2023 Aug;24(8):560-575. (PMID: 36864290)
PeerJ. 2019 Jul 04;7:e7255. (PMID: 31309005)
Nat Cell Biol. 2011 Oct 16;13(11):1335-43. (PMID: 22002674)
Autophagy. 2021 Sep;17(9):2565-2575. (PMID: 33249988)
Sci Adv. 2022 Oct 28;8(43):eabo5600. (PMID: 36288306)
Biol Reprod. 2003 May;68(5):1793-800. (PMID: 12606393)
Genome Biol. 2007;8(7):R129. (PMID: 17615057)
Elife. 2023 Jul 03;12:. (PMID: 37395461)
Science. 1913 Oct 10;38(980):524-8. (PMID: 17813658)
J Cell Biol. 1994 Mar;124(5):677-88. (PMID: 8120091)
Nat Commun. 2022 Jul 1;13(1):3790. (PMID: 35778412)
Sci Adv. 2022 Oct 28;8(43):eabn3298. (PMID: 36288298)
J Biol Chem. 2011 Jan 7;286(1):185-91. (PMID: 21062745)
Mol Biol Cell. 2009 Mar;20(6):1705-14. (PMID: 19158398)
Science. 2016 Jul 22;353(6297):394-9. (PMID: 27338704)
Semin Cell Dev Biol. 2004 Apr;15(2):231-6. (PMID: 15209383)
Heredity (Edinb). 2022 Jul;129(1):31-43. (PMID: 35525886)
PLoS Biol. 2020 Nov 13;18(11):e3000953. (PMID: 33186358)
Gamete Res. 1988 Apr;19(4):369-80. (PMID: 3198057)
J Biol Chem. 2017 Aug 4;292(31):12754-12763. (PMID: 28615445)
Front Cell Dev Biol. 2023 Feb 23;11:1137870. (PMID: 36910139)
Nature. 1991 Jul 18;352(6332):255-7. (PMID: 1857422)
Hum Reprod. 2000 Jul;15 Suppl 2:92-101. (PMID: 11041517)
Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1382-7. (PMID: 16432229)
Sci Rep. 2020 Feb 12;10(1):2468. (PMID: 32051468)
Cell. 2019 Jul 25;178(3):536-551.e14. (PMID: 31257024)
Cell Microbiol. 2016 Sep;18(9):1208-16. (PMID: 27185357)
iScience. 2020 Dec 31;24(1):102029. (PMID: 33506190)
Dev Cell. 2012 Mar 13;22(3):660-8. (PMID: 22421049)
Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13859-63. (PMID: 8943026)
Trends Plant Sci. 2018 Feb;23(2):129-139. (PMID: 29170007)
Hum Reprod Update. 2001 Jul-Aug;7(4):428-35. (PMID: 11476356)
Reprod Fertil Dev. 2017 Jan;30(1):56-63. (PMID: 29539303)
Annu Rev Cell Dev Biol. 2011;27:107-32. (PMID: 21801009)
EMBO Rep. 2020 Mar 4;21(3):e49612. (PMID: 32073748)
Trends Cell Biol. 2021 Apr;31(4):269-283. (PMID: 33414051)
Mech Dev. 1998 Nov;78(1-2):113-8. (PMID: 9858703)
Front Cell Infect Microbiol. 2022 Jan 03;11:809121. (PMID: 35047422)
Elife. 2018 Nov 19;7:. (PMID: 30451685)
Cell. 2012 Oct 12;151(2):333-343. (PMID: 23063123)
Autophagy. 2011 Aug;7(8):814-28. (PMID: 21464618)
J Struct Biol. 2010 Oct;172(1):34-44. (PMID: 20600952)
Biochim Biophys Acta. 2009 May;1787(5):476-83. (PMID: 18840399)
Eur J Obstet Gynecol Reprod Biol. 2019 May;236:183-192. (PMID: 30954715)
Trends Cell Biol. 2010 Apr;20(4):196-204. (PMID: 20138522)
J Exp Med. 2019 Feb 4;216(2):253-266. (PMID: 30587505)
Genetics. 2018 Jun;209(2):381-387. (PMID: 29669732)
Int J Cell Biol. 2011;2011:713435. (PMID: 22013444)
J Microsc. 1994 Jul;175(Pt 1):34-43. (PMID: 7932676)
PLoS Biol. 2007 Oct;5(10):e251. (PMID: 17880263)
Proc Natl Acad Sci U S A. 2019 Feb 5;116(6):1821-1822. (PMID: 30674683)
Proc Natl Acad Sci U S A. 1995 May 9;92(10):4542-6. (PMID: 7753839)
Nat Methods. 2019 Dec;16(12):1226-1232. (PMID: 31570887)
J Proteome Res. 2018 Jan 5;17(1):386-391. (PMID: 29083185)
Science. 2011 Nov 25;334(6059):1144-7. (PMID: 22033522)
Cells. 2021 Nov 11;10(11):. (PMID: 34831348)
Nature. 1974 Oct 11;251(5475):536-8. (PMID: 4423884)
Semin Cell Dev Biol. 2020 Jan;97:156-166. (PMID: 31611080)
Nat Commun. 2023 May 29;14(1):3077. (PMID: 37248218)
EMBO J. 2018 Feb 15;37(4):. (PMID: 29317426)
Genome Res. 2017 Jul;27(7):1273-1285. (PMID: 28381612)
Nat Commun. 2016 Sep 01;7:12569. (PMID: 27581092)
Cell Immunol. 2022 Aug;378:104556. (PMID: 35700602)
Bioessays. 2008 Jun;30(6):579-89. (PMID: 18478537)
J Cell Sci. 2019 Feb 20;132(5):. (PMID: 30787029)
Open Biol. 2015 Aug;5(8):. (PMID: 26246493)
Genetics. 1998 Feb;148(2):851-7. (PMID: 9504930)
Mol Cell. 2021 May 6;81(9):2031-2040.e8. (PMID: 33909989)
Nat Methods. 2012 Jun 28;9(7):676-82. (PMID: 22743772)
Development. 2006 Dec;133(24):4871-9. (PMID: 17092953)
Semin Cell Dev Biol. 2020 May;101:68-76. (PMID: 31029766)
Mol Biol Cell. 1998 Sep;9(9):2655-65. (PMID: 9725918)
Front Cell Dev Biol. 2021 Mar 26;9:628991. (PMID: 33842458)
Science. 2011 Nov 25;334(6059):1141-4. (PMID: 21998252)
Proc Natl Acad Sci U S A. 2009 Apr 14;106(15):6226-31. (PMID: 19339495)
Autophagy. 2018;14(9):1499-1519. (PMID: 29940806)
Mol Cell. 2015 Jan 22;57(2):207-18. (PMID: 25533187)
Curr Protoc Mol Biol. 2015 Jul 01;111:31.2.1-31.2.20. (PMID: 26131852)
Nature. 2007 Dec 20;450(7173):1253-7. (PMID: 18097414)
Annu Rev Genet. 2001;35:125-48. (PMID: 11700280)
Nature. 1999 Nov 25;402(6760):371-2. (PMID: 10586873)
Dev Cell. 2018 Nov 5;47(3):377-387.e4. (PMID: 30399336)
Cell Host Microbe. 2010 Jun 25;7(6):500-8. (PMID: 20542253)
Curr Protoc Bioinformatics. 2012 Dec;Chapter 13:13.20.1-13.20.14. (PMID: 23255153)
Dev Biol. 2022 Jan;481:64-74. (PMID: 34627795)
Methods Mol Biol. 2023;2647:83-104. (PMID: 37041330)
Biol Reprod. 2000 Aug;63(2):582-90. (PMID: 10906068)
J Cell Biol. 2014 Sep 1;206(5):671-88. (PMID: 25154396)
Proc Natl Acad Sci U S A. 2008 Nov 4;105(44):16952-7. (PMID: 18971338)
Autophagy. 2014 Sep;10(9):1637-51. (PMID: 25046112)
Hum Reprod. 2002 Aug;17(8):1954-8. (PMID: 12151420)
PLoS Biol. 2008 Jan;6(1):e10. (PMID: 18232733)
J Mol Biol. 2017 Nov 24;429(23):3561-3576. (PMID: 28847720)
Nat Cell Biol. 2019 Mar;21(3):372-383. (PMID: 30778222)
J Endocrinol Invest. 2023 Jun;46(6):1079-1085. (PMID: 36633791)
J Cell Sci. 1998 Nov;111 ( Pt 22):3299-309. (PMID: 9788872)
Biochem Biophys Res Commun. 2008 Jul 4;371(3):405-10. (PMID: 18452703)
Annu Rev Biochem. 2007;76:781-821. (PMID: 17506638)
Biochim Biophys Acta Mol Cell Res. 2021 Feb;1868(2):118916. (PMID: 33276010)
Sci Adv. 2022 Oct 28;8(43):eabn1702. (PMID: 36288309)
Pathogens. 2022 Jul 30;11(8):. (PMID: 36014984)
Biol Cell. 2017 Oct;109(10):355-363. (PMID: 28755428)
Dev Cell. 2017 Dec 18;43(6):716-730.e7. (PMID: 29257951)
EMBO J. 2000 Sep 1;19(17):4577-88. (PMID: 10970851)
Nucleic Acids Res. 2018 Jan 4;46(D1):D809-D815. (PMID: 29069479)
Biochim Biophys Acta Mol Cell Res. 2021 Jan;1868(1):118867. (PMID: 32979421)
Nat Cell Biol. 2009 Apr;11(4):468-76. (PMID: 19270693)
FASEB J. 2012 Oct;26(10):4160-73. (PMID: 22767229)
Nat Biotechnol. 2004 Dec;22(12):1567-72. (PMID: 15558047)
Nat Cell Biol. 2020 Feb;22(2):187-199. (PMID: 31932738)
Nat Genet. 2023 Oct;55(10):1632-1639. (PMID: 37723262)
Spermatogenesis. 2012 Jul 1;2(3):197-212. (PMID: 23087837)
Mol Biol Cell. 2008 Dec;19(12):5360-72. (PMID: 18843052)
J Cell Biol. 2012 Feb 20;196(4):513-27. (PMID: 22351928)
Curr Opin Immunol. 2019 Oct;60:81-90. (PMID: 31247378)
Nature. 2011 Mar 24;471(7339):473-9. (PMID: 21179090)
J Cell Biol. 1973 Feb;56(2):580-9. (PMID: 4630197)
Methods. 2001 Dec;25(4):402-8. (PMID: 11846609)
Dev Cell. 2014 May 12;29(3):305-20. (PMID: 24823375)
Front Mol Biosci. 2022 Dec 19;9:1074701. (PMID: 36601581)
Reprod Biomed Online. 2004 Jan;8(1):34-44. (PMID: 14759285)
Insect Biochem Mol Biol. 2010 Nov;40(11):792-804. (PMID: 20727969)
G3 (Bethesda). 2013 Sep 04;3(9):1607-16. (PMID: 23893746)
Proc Natl Acad Sci U S A. 2013 Aug 6;110(32):13038-43. (PMID: 23878233)
Cell Mol Life Sci. 2020 Jan;77(2):323-330. (PMID: 31203379)
Cell Res. 2011 Dec;21(12):1662-9. (PMID: 22105480)
Mol Biol Cell. 2008 May;19(5):2092-100. (PMID: 18321988)
Science. 2004 May 14;304(5673):981. (PMID: 15143273)
Proc Natl Acad Sci U S A. 2018 Dec 18;115(51):13039-13044. (PMID: 30478036)
Nat Neurosci. 2006 Oct;9(10):1234-6. (PMID: 16980964)
Science. 2015 Jan 30;347(6221):543-8. (PMID: 25592419)
N Engl J Med. 2002 Aug 22;347(8):576-80. (PMID: 12192017)
BMC Genomics. 2018 Sep 24;19(1):697. (PMID: 30249207)
Nat Genet. 2014 Apr;46(4):393-7. (PMID: 24614071)
Cold Spring Harb Perspect Biol. 2014 Jan 01;6(1):. (PMID: 24384571)
Nucleus. 2022 Dec;13(1):116-128. (PMID: 35239464)
Nat Cell Biol. 2009 Apr;11(4):385-96. (PMID: 19270696)
J Biochem. 2017 Oct 1;162(4):247-253. (PMID: 28981751)
Nat Cell Biol. 2018 Jan;20(1):81-91. (PMID: 29255173)
Mech Dev. 2002 Jan;110(1-2):97-112. (PMID: 11744372)
Proc Natl Acad Sci U S A. 2019 Feb 5;116(6):1823-1824. (PMID: 30674682)
EMBO J. 2006 Jan 11;25(1):232-43. (PMID: 16362035)
Mol Biol Cell. 2018 Jun 15;29(12):1413-1421. (PMID: 29688792)
Nat Rev Mol Cell Biol. 2013 Dec;14(12):759-74. (PMID: 24201109)
Curr Opin Cell Biol. 2011 Aug;23(4):452-7. (PMID: 21570275)
J Cell Sci. 2005 Aug 15;118(Pt 16):3663-73. (PMID: 16046475)
Nat Rev Mol Cell Biol. 2020 Jul;21(7):398-414. (PMID: 32251387)
Cell Host Microbe. 2012 Mar 15;11(3):264-76. (PMID: 22423966)
Reprod Sci. 2022 Aug;29(8):2208-2222. (PMID: 35477840)
Trends Biochem Sci. 2021 Aug;46(8):673-686. (PMID: 33558127)
Genetics. 2015 Oct;201(2):631-49. (PMID: 26265702)
معلومات مُعتمدة: 616088 EC | EC Seventh Framework Programm | FP7 Ideas: European Research Council (FP7-IDEAS-ERC - Specific Programme: "Ideas" Implementing the Seventh Framework Programme of the European Community for Research, Technological Development and Demonstration Activities (2007 to 2013)); 1279/19 Israel Science Foundation (ISF)
المشرفين على المادة: 0 (Drosophila Proteins)
0 (Microtubule-Associated Proteins)
تواريخ الأحداث: Date Created: 20240708 Date Completed: 20240708 Latest Revision: 20240802
رمز التحديث: 20240802
مُعرف محوري في PubMed: PMC11231261
DOI: 10.1038/s41467-024-50041-5
PMID: 38977659
قاعدة البيانات: MEDLINE
الوصف
تدمد:2041-1723
DOI:10.1038/s41467-024-50041-5