دورية أكاديمية
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Dynamin 2-dependent endocytosis is essential for mouse oocyte development and fertility.

التفاصيل البيبلوغرافية
العنوان: Dynamin 2-dependent endocytosis is essential for mouse oocyte development and fertility.
المؤلفون: Mihalas BP; School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW, Australia.; Priority Research Centre for Reproductive Science, University of Newcastle, Callaghan, NSW, Australia.; Pregnancy and Reproduction Program, Hunter Medial Research Institute, New Lambton Heights, NSW, Australia., Redgrove KA; School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW, Australia.; Priority Research Centre for Reproductive Science, University of Newcastle, Callaghan, NSW, Australia.; Pregnancy and Reproduction Program, Hunter Medial Research Institute, New Lambton Heights, NSW, Australia., Bernstein IR; School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW, Australia.; Priority Research Centre for Reproductive Science, University of Newcastle, Callaghan, NSW, Australia.; Pregnancy and Reproduction Program, Hunter Medial Research Institute, New Lambton Heights, NSW, Australia., Robertson MJ; School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW, Australia.; Priority Research Centre in Chemical Biology, University of Newcastle, Callaghan, NSW, Australia., McCluskey A; School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW, Australia.; Priority Research Centre in Chemical Biology, University of Newcastle, Callaghan, NSW, Australia., Nixon B; School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW, Australia.; Priority Research Centre for Reproductive Science, University of Newcastle, Callaghan, NSW, Australia.; Pregnancy and Reproduction Program, Hunter Medial Research Institute, New Lambton Heights, NSW, Australia., Holt JE; Priority Research Centre for Reproductive Science, University of Newcastle, Callaghan, NSW, Australia.; School of Biomedical Sciences & Pharmacy, University of Newcastle, Callaghan, NSW, Australia., McLaughlin EA; School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW, Australia.; Priority Research Centre for Reproductive Science, University of Newcastle, Callaghan, NSW, Australia.; Pregnancy and Reproduction Program, Hunter Medial Research Institute, New Lambton Heights, NSW, Australia.; School of Science, Western Sydney University, Penrith, NSW, Australia.; School of Biological Sciences, The University of Auckland, Auckland, New Zealand., Sutherland JM; Priority Research Centre for Reproductive Science, University of Newcastle, Callaghan, NSW, Australia.; Pregnancy and Reproduction Program, Hunter Medial Research Institute, New Lambton Heights, NSW, Australia.; School of Biomedical Sciences & Pharmacy, University of Newcastle, Callaghan, NSW, Australia.
المصدر: FASEB journal : official publication of the Federation of American Societies for Experimental Biology [FASEB J] 2020 Apr; Vol. 34 (4), pp. 5162-5177. Date of Electronic Publication: 2020 Feb 17.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Federation of American Societies for Experimental Biology Country of Publication: United States NLM ID: 8804484 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1530-6860 (Electronic) Linking ISSN: 08926638 NLM ISO Abbreviation: FASEB J Subsets: MEDLINE
أسماء مطبوعة: Publication: 2020- : [Bethesda, Md.] : Hoboken, NJ : Federation of American Societies for Experimental Biology ; Wiley
Original Publication: [Bethesda, Md.] : The Federation, [c1987-
مواضيع طبية MeSH: Endocytosis* , Fertility*, Dynamin I/*physiology , Dynamin II/*physiology , Oocytes/*cytology , Ovarian Follicle/*cytology, Animals ; Female ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Mice, Transgenic ; Oocytes/physiology ; Ovarian Follicle/physiology
مستخلص: During folliculogenesis, oocytes are dependent on metabolic and molecular support from surrounding somatic cells. Here, we examined the role of the dynamin (DNM) family of mechanoenzymes in mediating endocytotic uptake into growing follicular oocytes. We found DNM1 and DNM2 to be highly expressed in growing follicular oocytes as well as in mature germinal vesicle (GV) and metaphase II (MII) stage oocytes. Moreover, oocyte-specific conditional knockout (cKO) of DNM2 (DNM2Δ) led to complete sterility, with follicles arresting at the preantral stage of development. In addition, DNM2Δ ovaries were characterized by disrupted follicular growth as well as oocyte and follicle apoptosis. Further, the loss of DNM activity, either through DNM2 cKO or through pharmacological inhibition (Dyngo 6a) led to the impairment of endocytotic pathways in preantral oocytes as well as in mature GV and MII oocytes, respectively. Loss of DNM activity resulted in the redistribution of endosomes and the misslocalization of clathrin and actin, suggesting dysfunctional endocytosis. Notably, there was no observable effect on the fertility of DNM1Δ females. Our study has provided new insight into the complex and dynamic nature of oocyte growth during folliculogenesis, suggesting a role for DNM2 in mediating the endocytotic events that are essential for oocyte development.
(© 2020 University of Newcastle. The FASEB Journal published by Wiley Periodicals, Inc. © 2020 Federation of American Societies for Experimental Biology.)
References: Kaksonen M, Roux A. Mechanisms of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 2018;19:313.
Doherty GJ, McMahon HT. Mechanisms of Endocytosis. Annu. Rev. Biochem. 2009;78:857-902.
Henley JR, Krueger EW, Oswald BJ, McNiven MA. Dynamin-mediated internalization of caveolae. J. Cell Biol. 1998;141:85-99.
Hinshaw JE. Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 2000;16:483-519.
Sundborger AC, Hinshaw JE. Regulating dynamin dynamics during endocytosis. F1000Prime. Rep. 2014;6:85-85.
Jimah JR, Hinshaw JE. Structural Insights into the Mechanism of Dynamin Superfamily Proteins. Trends Cell Biol. 2019;29:257-273.
Ramachandran R, Schmid SL. The dynamin superfamily. Curr. Biol. 2018;28:R411-R416.
Ferguson SM, Raimondi A, Paradise S, et al. Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev. Cell. 2009;17:811-822.
Cao H, Garcia F, McNiven MA. Differential distribution of dynamin isoforms in mammalian cells. Mol. Biol. Cell. 1998;9:2595-2609.
Ferguson SM, Brasnjo G, Hayashi M, et al. A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science. 2007;316:570-574.
Nakata T, Iwamoto A, Noda Y, Takemura R, Yoshikura H, Hirokawa N. Predominant and developmentally regulated expression of dynamin in neurons. Neuron. 1991;7:461-469.
Cook TA, Urrutia R, McNiven MA. Identification of dynamin 2, an isoform ubiquitously expressed in rat tissues. Proc. Natl. Acad. Sci. USA. 1994;91:644-648.
Vaid KS, Guttman JA, Babyak N, et al. The role of dynamin 3 in the testis. J. Cell. Physiol. 2007;210:644-654.
Zhou W, Anderson AL, Turner AP, et al. Characterization of a novel role for the dynamin mechanoenzymes in the regulation of human sperm acrosomal exocytosis. Mol. Hum. Reproduction. 2017;23:657-673.
Reid AT, Anderson AL, Roman SD, et al. Glycogen synthase kinase 3 regulates acrosomal exocytosis in mouse spermatozoa via dynamin phosphorylation. FASEB J. 2015;29:2872-2882.
Reid AT, Lord T, Stanger SJ, et al. Dynamin regulates specific membrane fusion events necessary for acrosomal exocytosis in mouse spermatozoa. J. Biol. Chem. 2012;287:37659-37672.
Redgrove KA, Bernstein IR, Pye VJ, et al. Dynamin 2 is essential for mammalian spermatogenesis. Sci. Rep. 2016;6:35084-35084.
Wang QC, Liu J, Wang ZB, et al. Dynamin 2 regulates actin-mediated spindle migration in mouse oocytes. Biol. Cell. 2014;106:193-202.
Zhang Y, Wang QC, Han J, et al. Involvement of Dynamin 2 in actin-based polar-body extrusion during porcine oocyte maturation. Mol. Reprod. Dev. 2014;81:725-734.
Lowther KM, Nikolaev VO, Mehlmann LM. Endocytosis in the mouse oocyte and its contribution to cAMP signaling during meiotic arrest. Reproduction. 2011;141:737.
Rimon-Dahari N, Yerushalmi-Heinemann L, Alyagor L, Dekel N. Ovarian Folliculogenesis. Results Probl Cell Differ. 2016;58:167-190.
Thomas FH, Vanderhyden BC. Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reprod. Biol. Endocrin. 2006;4:19.
Fortune JE. The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim. Reprod. Sci. 2003;78:135-163.
McLaughlin EA, McIver SC. Awakening the oocyte: controlling primordial follicle development. Reproduction. 2009;137:1-11.
Palma GA, Argañaraz ME, Barrera AD, Rodler D, Mutto AÁ, Sinowatz F. Biology and biotechnology of follicle development. Sci. World J. 2012;2012:938138-938138.
van den Hurk R, Zhao J. Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology. 2005;63:1717-1751.
Eppig JJJB. Intercommunication between mammalian oocytes and companion somatic cells. BioEssays. 1991;13:569-574.
Fair T. Follicular oocyte growth and acquisition of developmental competence. Anim. Reprod. Sci. 2003;78:203-216.
Donahue RP, Stern S. Follicular cell support of oocyte maturation: production of pyruvate in vitro. J. Reprod. Fertil. 1968;17:395-398.
Leese HJ, Barton AM. Production of pyruvate by isolated mouse cumulus cells. J. Exp. Zool. 1985;234:231-236.
Colonna R, Mangia F. Mechanisms of amino acid uptake in cumulus-enclosed mouse oocytes. Biol. Reprod. 1983;28:797-803.
Yeo CX, Gilchrist RB, Lane M. Disruption of Bidirectional Oocyte-Cumulus Paracrine Signaling During In Vitro Maturation Reduces Subsequent Mouse Oocyte Developmental Competence1. Biol. Reprod. 2009;80:1072-1080.
Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121:647-653.
El-Hayek S, Yang Q, Abbassi L, FitzHarris G, Clarke HJ. Mammalian Oocytes Locally Remodel Follicular Architecture to Provide the Foundation for Germline-Soma Communication. Curr. Biol. 2018;28:1124-1131.e1123.
Eppig JJ. Reproduction: Oocytes Call, Granulosa Cells Connect. Curr. Biol. 2018;28:R354-r356.
McCluskey A, Daniel JA, Hadzic G, et al. Building a Better Dynasore: The Dyngo Compounds Potently Inhibit Dynamin and Endocytosis. Traffic. 2013;12:1272-1289.
de Vries WN, Binns LT, Fancher KS, et al. Expression of Cre recombinase in mouse oocytes: a means to study maternal effect genes. Genesis. 2000;26:110-112.
Holt JE, Lane SI, Jennings P, Garcia-Higuera I, Moreno S, Jones KT. APC(FZR1) prevents nondisjunction in mouse oocytes by controlling meiotic spindle assembly timing. Mol. Biol. Cell. 2012;23:3970-3981.
Fischer AH, Jacobson KA, Rose J, Zeller R. Hematoxylin and eosin staining of tissue and cell sections. Cold Spring Harbor Protocols. 2008;2008:pdb.prot4986.
Mihalas BP, De Iuliis GN, Redgrove KA, McLaughlin EA, Nixon B. The lipid peroxidation product 4-hydroxynonenal contributes to oxidative stress-mediated deterioration of the ageing oocyte. Sci. Rep. 2017;7:6247.
Nixon B, Stanger SJ, Mihalas BP, et al. Next Generation Sequencing Analysis Reveals Segmental Patterns of microRNA Expression in Mouse Epididymal Epithelial Cells. PLoS ONE. 2015;10:e0135605.
Mihalas BP, Western PS, Loveland KL, McLaughlin EA, Holt JE. Changing expression and subcellular distribution of karyopherins during murine oogenesis. Reproduction. 2015;150:485-496.
Camlin NJ, McLaughlin EA, Holt JE. Kif4 Is Essential for Mouse Oocyte Meiosis. PLoS ONE. 2017;12:e0170650.
Raimondi A, Ferguson SM, Lou X, et al. Overlapping role of dynamin isoforms in synaptic vesicle endocytosis. Neuron. 2011;70:1100-1114.
Mu F-T, Callaghan JM, Steele-Mortimer O, et al. EEA1, an early endosome-associated protein. EEA1 is a conserved α-helical peripheral membrane protein flanked by cysteine “fingers” and contains a calmodulin-binding IQ motif. J. Biol. Chem. 1995;270:13503-13511.
McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 2011;12:517.
Mooren OL, Galletta BJ, Cooper JA. Roles for actin assembly in endocytosis. Annu. Rev. Biochem. 2012;81:661-686.
Monniaux D. Driving folliculogenesis by the oocyte-somatic cell dialog: Lessons from genetic models. Theriogenology. 2016;86:41-53.
Carabatsos MJ, Sellitto C, Goodenough DA, Albertini DF. Oocyte-granulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence. Dev. Biol. 2000;226:167-179.
Gittens JEI, Kidder GM. Differential contributions of connexin37 and connexin43 to oogenesis revealed in chimeric reaggregated mouse ovaries. J. Cell Sci. 2005;118:5071-5078.
Simon AM, Goodenough DA, Li E, Paul DL. Female infertility in mice lacking connexin 37. Nature. 1997;385:525-529.
Elkin SR, Lakoduk AM, Schmid SL. Endocytic pathways and endosomal trafficking: a primer. Wien. Med. Wochenschr. 2016;166:196-204.
Kaur G, Lakkaraju A. Early Endosome Morphology in Health and Disease. Adv. Exp. Med. Biol. 2018;1074:335-343.
Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell. Biol. 1994;127:915-934.
Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update. 2008;14:159-177.
Matzuk MM, Burns KH, Viveiros MM, Eppig JJ. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science. 2002;296:2178-2180.
Adhikari D, Liu K. Molecular Mechanisms Underlying the Activation of Mammalian Primordial Follicles. Endocr. Rev. 2009;30:438-464.
Hirobe S, He WW, Lee MM, Donahoe PKJE. Mullerian inhibiting substance messenger ribonucleic acid expression in granulosa and Sertoli cells coincides with their mitotic activity. Endocrinology. 1992;131:854-862.
Baarends WM, Uilenbroek J, Kramer P, et al. Anti-Müllerian hormone and anti-Müllerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology. 1995;136:4951-4962.
Zhao M, Maani N, Dowling JJ. Dynamin 2 (DNM2) as Cause of, and Modifier for, Human Neuromuscular Disease. Neurotherapeutics. 2018;15:966-975.
McNiven MA. Dynamin in disease. Nat. Gen. 2005;37:215-216.
Bitoun M, Durieux AC, Prudhon B, et al. Dynamin 2 mutations associated with human diseases impair clathrin-mediated receptor endocytosis. Hum. Mutat. 2009;30:1419-1427.
فهرسة مساهمة: Keywords: dynamin; endocytosis; folliculogenesis; oocyte; oogenesis
المشرفين على المادة: EC 3.5.1.50 (Dynamin I)
EC 3.6.5.5 (DNM2 protein, mouse)
EC 3.6.5.5 (Dynamin II)
تواريخ الأحداث: Date Created: 20200218 Date Completed: 20210119 Latest Revision: 20210119
رمز التحديث: 20231215
DOI: 10.1096/fj.201902184R
PMID: 32065700
قاعدة البيانات: MEDLINE
الوصف
تدمد:1530-6860
DOI:10.1096/fj.201902184R