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Visualization and Analyses of Cytoplasmic Streaming in C. elegans Zygotes.

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Τίτλος: Visualization and Analyses of Cytoplasmic Streaming in C. elegans Zygotes.
Συγγραφείς: Kimura K; Division of Developmental Physiology, Institute for Genetic Medicine, Hokkaido University, Hokkaido, Japan. kekimura@igm.hokudai.ac.jp., Motegi F; Division of Developmental Physiology, Institute for Genetic Medicine, Hokkaido University, Hokkaido, Japan. motegi@igm.hokudai.ac.jp.
Πηγή: Methods in molecular biology (Clifton, N.J.) [Methods Mol Biol] 2025; Vol. 2872, pp. 131-139.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Humana Press Country of Publication: United States NLM ID: 9214969 Publication Model: Print Cited Medium: Internet ISSN: 1940-6029 (Electronic) Linking ISSN: 10643745 NLM ISO Abbreviation: Methods Mol Biol Subsets: MEDLINE
Imprint Name(s): Publication: Totowa, NJ : Humana Press
Original Publication: Clifton, N.J. : Humana Press
Ιατρικοί όροι (MeSH): Caenorhabditis elegans*/metabolism , Caenorhabditis elegans*/cytology , Zygote*/cytology , Zygote*/metabolism , Cytoplasmic Streaming*/physiology, Microtubules/metabolism ; Oocytes/metabolism ; Oocytes/cytology ; Cytoplasm/metabolism ; Animals ; Oogenesis
Περίληψη: Cytoplasmic streaming is the bulk flow of cytoplasm observed, not only in plants but also in animal oocytes and embryos. The flow of viscous fluid within the cytoplasm generates forces that re-arrange intracellular organelles, such as mitotic spindles and nuclei, to regulate cell growth, migration, and polarity. Cytoplasmic streaming is established by motor proteins and the viscoelastic cytoskeleton, including the actin filaments and microtubules. The mode of action can be changed in response to cell fate and developmental stage; however, its regulatory mechanism is unclear. The nematode Caenorhabditis elegans is a valuable model organism for analyzing cytoplasmic streaming because actin- and microtubule-dependent flows occur during oogenesis and embryogenesis, respectively. In this chapter, we describe methods for visualizing and quantitatively analyzing cytoplasmic streaming in C. elegans oocytes and embryos.
(© 2025. The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature.)
References: Kimura K, Motegi F (2021) Fluid flow dynamics in cellular patterning. Semin Cell Dev Biol 120:3–9. (PMID: 34274213)
Yi K, Unruh JR, Deng M et al (2011) Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3-complex-driven cytoplasmic streaming in mouse oocytes. Nat Cell Biol 13(10):1252–1258. (PMID: 218740093523671)
Kimura K, Kimura A (2020) Cytoplasmic streaming drifts the polarity cue and enables posteriorization of the Caenorhabditis elegans zygote at the side opposite of sperm entry. Mol Biol Cell 31(16):1765–1773. (PMID: 324595527521852)
Shamipour S, Kardos R, Xue SL et al (2019) Bulk actin dynamics drive phase segregation in Zebrafish oocytes. Cell 177(6):1463–1479. (PMID: 31080065)
Ishii H, Tani T (2021) Dynamic organization of cortical actin filaments during the ooplasmic segregation of ascidian Ciona eggs. Mol Biol Cell 32(3):274–288. (PMID: 332962258098833)
Serbus LR, Cha BJ, Theurkauf WE et al (2005) Dynein and the actin cytoskeleton control kinesin-driven cytoplasmic streaming in Drosophila oocytes. Development 132(16):3743–3752. (PMID: 16077093)
Lu W, Winding M, Lakonishok M et al (2016) Microtubule-microtubule sliding by kinesin-1 is essential for normal cytoplasmic streaming in Drosophila oocytes. Proc Natl Acad Sci USA 113(34):E4995–E5004. (PMID: 275120345003289)
Wolke U, Jezuit EA, Priess JR (2007) Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development 134(12):2227–2236. (PMID: 17507392)
Kimura K, Mamane A, Sasaki T et al (2017) Endoplasmic-reticulum-mediated microtubule alignment governs cytoplasmic streaming. Nat Cell Biol 19(4):399–406. (PMID: 28288129)
McNally KL, Martin JL, Ellefson M et al (2010) Kinesin-dependent transport results in polarized migration of the nucleus in oocytes and inward movement of yolk granules in meiotic embryos. Dev Biol 339(1):126–140. (PMID: 20036653)
Yang HY, McNally K, McNally FJ (2003) MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C. elegans. Dev Biol 260(1):245–259. (PMID: 12885567)
Munro E, Nance J, Priess JR (2004) Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev Cell 7(3):413–424. (PMID: 15363415)
Niwayama R, Shinohara K, Kimura A (2011) Hydrodynamic property of the cytoplasm is sufficient to mediate cytoplasmic streaming in the Caenorhabditis elegans embryo. Proc Natl Acad Sci USA 108(29):11900–11905. (PMID: 217301853141991)
Stiernagle T (2006) Maintenance of C. elegans. WormBook:1–11.
Chai Y, Li W, Feng G et al (2012) Live imaging of cellular dynamics during Caenorhabditis elegans postembryonic development. Nat Protoc 7(12):2090–2102. (PMID: 23138350)
Dickinson DJ, Goldstein B (2016) CRISPR-based methods for Caenorhabditis elegans genome engineering. Genetics 202(3):885–901. (PMID: 269532684788126)
Paix A, Folkmann A, Seydoux G (2017) Precision genome editing using CRISPR-Cas9 and linear repair templates in C. elegans. Methods 121–122:86–93. (PMID: 283922636788293)
Kimura K, Tanaka N, Nakamura N et al (2007) Knockdown of mitochondrial heat shock protein 70 promotes progeria-like phenotypes in Caenorhabditis elegans. J Biol Chem 282(8):5910–5918. (PMID: 17189267)
Kimura K, Kimura A (2011) Intracellular organelles mediate cytoplasmic pulling force for centrosome centration in the Caenorhabditis elegans early embryo. Proc Natl Acad Sci USA 108(1):137–142. (PMID: 21173218)
Farnebäck G (2003) Two-frame motion estimation based on polynomial expansion. In: Bigun J, Gustavsson T (eds) Image analysis, vol 2749. Springer, Berlin/Heidelberg, pp 363–370.
Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77(1):71–94. (PMID: 43664761213120)
Burnett K, Edsinger E, Albrecht DR (2018) Rapid and gentle hydrogel encapsulation of living organisms enables long-term microscopy over multiple hours. Commun Biol 1:73. (PMID: 302719546123791)
Suzuki M, Sakashita T, Funayama T (2019) Immobilization of live Caenorhabditis elegans individuals using an ultra-thin polydimethylsiloxane microfluidic chip with water retention. J Vis Exp 145.
Dong L, Cornaglia M, Krishnamani G et al (2018) Reversible and long-term immobilization in a hydrogel-microbead matrix for high-resolution imaging of Caenorhabditis elegans and other small organisms. PLoS One 13(3):e0193989. (PMID: 295098125839568)
Keil W, Kutscher LM, Shaham S et al (2017) Long-term high-resolution imaging of developing C. elegans larvae with microfluidics. Dev Cell 40(2):202–214. (PMID: 28041904)
Zellag RM, Zhao Y, Gerhold AR (2022) Live-cell imaging and analysis of germline stem cell mitosis in Caenorhabditis elegans. Bio Protoc 12(1):e4272. (PMID: 351181658769765)
Niwa S (2017) Immobilization of Caenorhabditis elegans to analyze intracellular transport in neurons. J Vis Exp 128.
Applegate KT, Besson S, Matov A et al (2011) plusTipTracker: quantitative image analysis software for the measurement of microtubule dynamics. J Struct Biol 176(2):168–184. (PMID: 218211303298692)
Poteryaev D, Squirrell JM, Campbell JM et al (2005) Involvement of the actin cytoskeleton and homotypic membrane fusion in ER dynamics in Caenorhabditis elegans. Mol Biol Cell 16(5):2139–2153. (PMID: 157163561087224)
Grant B, Hirsh D (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10(12):4311–4326. (PMID: 1058866025760)
Andrews R, Ahringer J (2007) Asymmetry of early endosome distribution in C. elegans embryos. PLoS One 2(6):e493. (PMID: 175515741876258)
Sato K, Sato M, Audhya A et al (2006) Dynamic regulation of caveolin-1 trafficking in the germ line and embryo of Caenorhabditis elegans. Mol Biol Cell 17(7):3085–3094. (PMID: 166723741483042)
Fan X, De Henau S, Feinstein J et al (2020) SapTrap assembly of Caenorhabditis elegans MosSCI transgene vectors. G3 (Bethesda) 10(2):635–644. (PMID: 31848219)
Contributed Indexing: Keywords: Actin; C. elegans; Cytoplasmic streaming; Fluid flow; Microtubules; Oocyte; Zygote
Entry Date(s): Date Created: 20241201 Date Completed: 20241201 Latest Revision: 20260909
Update Code: 20260909
DOI: 10.1007/978-1-0716-4224-5_9
PMID: 39616573
Βάση Δεδομένων: MEDLINE
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  Data: <searchLink fieldCode="AU" term="%22Kimura+K%22">Kimura K</searchLink>; Division of Developmental Physiology, Institute for Genetic Medicine, Hokkaido University, Hokkaido, Japan. kekimura@igm.hokudai.ac.jp.<br /><searchLink fieldCode="AU" term="%22Motegi+F%22">Motegi F</searchLink>; Division of Developmental Physiology, Institute for Genetic Medicine, Hokkaido University, Hokkaido, Japan. motegi@igm.hokudai.ac.jp.
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  Data: <searchLink fieldCode="MM" term="%22Caenorhabditis+elegans%22">Caenorhabditis elegans*</searchLink>/<searchLink fieldCode="MM" term="%22Caenorhabditis+elegans+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Caenorhabditis+elegans%22">Caenorhabditis elegans*</searchLink>/<searchLink fieldCode="MM" term="%22Caenorhabditis+elegans+cytology%22">cytology</searchLink> <br /><searchLink fieldCode="MM" term="%22Zygote%22">Zygote*</searchLink>/<searchLink fieldCode="MM" term="%22Zygote+cytology%22">cytology</searchLink> <br /><searchLink fieldCode="MM" term="%22Zygote%22">Zygote*</searchLink>/<searchLink fieldCode="MM" term="%22Zygote+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Cytoplasmic+Streaming%22">Cytoplasmic Streaming*</searchLink>/<searchLink fieldCode="MM" term="%22Cytoplasmic+Streaming+physiology%22">physiology</searchLink><br /><searchLink fieldCode="MH" term="%22Microtubules%22">Microtubules</searchLink>/<searchLink fieldCode="MH" term="%22Microtubules+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Oocytes%22">Oocytes</searchLink>/<searchLink fieldCode="MH" term="%22Oocytes+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Oocytes%22">Oocytes</searchLink>/<searchLink fieldCode="MH" term="%22Oocytes+cytology%22">cytology</searchLink> ; <searchLink fieldCode="MH" term="%22Cytoplasm%22">Cytoplasm</searchLink>/<searchLink fieldCode="MH" term="%22Cytoplasm+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Animals%22">Animals</searchLink> ; <searchLink fieldCode="MH" term="%22Oogenesis%22">Oogenesis</searchLink>
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  Data: Cytoplasmic streaming is the bulk flow of cytoplasm observed, not only in plants but also in animal oocytes and embryos. The flow of viscous fluid within the cytoplasm generates forces that re-arrange intracellular organelles, such as mitotic spindles and nuclei, to regulate cell growth, migration, and polarity. Cytoplasmic streaming is established by motor proteins and the viscoelastic cytoskeleton, including the actin filaments and microtubules. The mode of action can be changed in response to cell fate and developmental stage; however, its regulatory mechanism is unclear. The nematode Caenorhabditis elegans is a valuable model organism for analyzing cytoplasmic streaming because actin- and microtubule-dependent flows occur during oogenesis and embryogenesis, respectively. In this chapter, we describe methods for visualizing and quantitatively analyzing cytoplasmic streaming in C. elegans oocytes and embryos.<br /> (© 2025. The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature.)
– Name: Ref
  Label: References
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  Data: Kimura K, Motegi F (2021) Fluid flow dynamics in cellular patterning. Semin Cell Dev Biol 120:3–9. (PMID: <searchLink fieldCode="PM" term="%2234274213%22">34274213)</searchLink><br />Yi K, Unruh JR, Deng M et al (2011) Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3-complex-driven cytoplasmic streaming in mouse oocytes. Nat Cell Biol 13(10):1252–1258. (PMID: <searchLink fieldCode="PM" term="%22218740093523671%22">218740093523671)</searchLink><br />Kimura K, Kimura A (2020) Cytoplasmic streaming drifts the polarity cue and enables posteriorization of the Caenorhabditis elegans zygote at the side opposite of sperm entry. Mol Biol Cell 31(16):1765–1773. (PMID: <searchLink fieldCode="PM" term="%22324595527521852%22">324595527521852)</searchLink><br />Shamipour S, Kardos R, Xue SL et al (2019) Bulk actin dynamics drive phase segregation in Zebrafish oocytes. Cell 177(6):1463–1479. (PMID: <searchLink fieldCode="PM" term="%2231080065%22">31080065)</searchLink><br />Ishii H, Tani T (2021) Dynamic organization of cortical actin filaments during the ooplasmic segregation of ascidian Ciona eggs. Mol Biol Cell 32(3):274–288. (PMID: <searchLink fieldCode="PM" term="%22332962258098833%22">332962258098833)</searchLink><br />Serbus LR, Cha BJ, Theurkauf WE et al (2005) Dynein and the actin cytoskeleton control kinesin-driven cytoplasmic streaming in Drosophila oocytes. Development 132(16):3743–3752. (PMID: <searchLink fieldCode="PM" term="%2216077093%22">16077093)</searchLink><br />Lu W, Winding M, Lakonishok M et al (2016) Microtubule-microtubule sliding by kinesin-1 is essential for normal cytoplasmic streaming in Drosophila oocytes. Proc Natl Acad Sci USA 113(34):E4995–E5004. (PMID: <searchLink fieldCode="PM" term="%22275120345003289%22">275120345003289)</searchLink><br />Wolke U, Jezuit EA, Priess JR (2007) Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development 134(12):2227–2236. (PMID: <searchLink fieldCode="PM" term="%2217507392%22">17507392)</searchLink><br />Kimura K, Mamane A, Sasaki T et al (2017) Endoplasmic-reticulum-mediated microtubule alignment governs cytoplasmic streaming. Nat Cell Biol 19(4):399–406. (PMID: <searchLink fieldCode="PM" term="%2228288129%22">28288129)</searchLink><br />McNally KL, Martin JL, Ellefson M et al (2010) Kinesin-dependent transport results in polarized migration of the nucleus in oocytes and inward movement of yolk granules in meiotic embryos. Dev Biol 339(1):126–140. (PMID: <searchLink fieldCode="PM" term="%2220036653%22">20036653)</searchLink><br />Yang HY, McNally K, McNally FJ (2003) MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C. elegans. Dev Biol 260(1):245–259. (PMID: <searchLink fieldCode="PM" term="%2212885567%22">12885567)</searchLink><br />Munro E, Nance J, Priess JR (2004) Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev Cell 7(3):413–424. (PMID: <searchLink fieldCode="PM" term="%2215363415%22">15363415)</searchLink><br />Niwayama R, Shinohara K, Kimura A (2011) Hydrodynamic property of the cytoplasm is sufficient to mediate cytoplasmic streaming in the Caenorhabditis elegans embryo. Proc Natl Acad Sci USA 108(29):11900–11905. (PMID: <searchLink fieldCode="PM" term="%22217301853141991%22">217301853141991)</searchLink><br />Stiernagle T (2006) Maintenance of C. elegans. WormBook:1–11.<br />Chai Y, Li W, Feng G et al (2012) Live imaging of cellular dynamics during Caenorhabditis elegans postembryonic development. Nat Protoc 7(12):2090–2102. (PMID: <searchLink fieldCode="PM" term="%2223138350%22">23138350)</searchLink><br />Dickinson DJ, Goldstein B (2016) CRISPR-based methods for Caenorhabditis elegans genome engineering. Genetics 202(3):885–901. (PMID: <searchLink fieldCode="PM" term="%22269532684788126%22">269532684788126)</searchLink><br />Paix A, Folkmann A, Seydoux G (2017) Precision genome editing using CRISPR-Cas9 and linear repair templates in C. elegans. Methods 121–122:86–93. (PMID: <searchLink fieldCode="PM" term="%22283922636788293%22">283922636788293)</searchLink><br />Kimura K, Tanaka N, Nakamura N et al (2007) Knockdown of mitochondrial heat shock protein 70 promotes progeria-like phenotypes in Caenorhabditis elegans. J Biol Chem 282(8):5910–5918. (PMID: <searchLink fieldCode="PM" term="%2217189267%22">17189267)</searchLink><br />Kimura K, Kimura A (2011) Intracellular organelles mediate cytoplasmic pulling force for centrosome centration in the Caenorhabditis elegans early embryo. Proc Natl Acad Sci USA 108(1):137–142. (PMID: <searchLink fieldCode="PM" term="%2221173218%22">21173218)</searchLink><br />Farnebäck G (2003) Two-frame motion estimation based on polynomial expansion. In: Bigun J, Gustavsson T (eds) Image analysis, vol 2749. Springer, Berlin/Heidelberg, pp 363–370.<br />Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77(1):71–94. (PMID: <searchLink fieldCode="PM" term="%2243664761213120%22">43664761213120)</searchLink><br />Burnett K, Edsinger E, Albrecht DR (2018) Rapid and gentle hydrogel encapsulation of living organisms enables long-term microscopy over multiple hours. Commun Biol 1:73. (PMID: <searchLink fieldCode="PM" term="%22302719546123791%22">302719546123791)</searchLink><br />Suzuki M, Sakashita T, Funayama T (2019) Immobilization of live Caenorhabditis elegans individuals using an ultra-thin polydimethylsiloxane microfluidic chip with water retention. J Vis Exp 145.<br />Dong L, Cornaglia M, Krishnamani G et al (2018) Reversible and long-term immobilization in a hydrogel-microbead matrix for high-resolution imaging of Caenorhabditis elegans and other small organisms. PLoS One 13(3):e0193989. (PMID: <searchLink fieldCode="PM" term="%22295098125839568%22">295098125839568)</searchLink><br />Keil W, Kutscher LM, Shaham S et al (2017) Long-term high-resolution imaging of developing C. elegans larvae with microfluidics. Dev Cell 40(2):202–214. (PMID: <searchLink fieldCode="PM" term="%2228041904%22">28041904)</searchLink><br />Zellag RM, Zhao Y, Gerhold AR (2022) Live-cell imaging and analysis of germline stem cell mitosis in Caenorhabditis elegans. Bio Protoc 12(1):e4272. (PMID: <searchLink fieldCode="PM" term="%22351181658769765%22">351181658769765)</searchLink><br />Niwa S (2017) Immobilization of Caenorhabditis elegans to analyze intracellular transport in neurons. J Vis Exp 128.<br />Applegate KT, Besson S, Matov A et al (2011) plusTipTracker: quantitative image analysis software for the measurement of microtubule dynamics. J Struct Biol 176(2):168–184. (PMID: <searchLink fieldCode="PM" term="%22218211303298692%22">218211303298692)</searchLink><br />Poteryaev D, Squirrell JM, Campbell JM et al (2005) Involvement of the actin cytoskeleton and homotypic membrane fusion in ER dynamics in Caenorhabditis elegans. Mol Biol Cell 16(5):2139–2153. (PMID: <searchLink fieldCode="PM" term="%22157163561087224%22">157163561087224)</searchLink><br />Grant B, Hirsh D (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10(12):4311–4326. (PMID: <searchLink fieldCode="PM" term="%221058866025760%22">1058866025760)</searchLink><br />Andrews R, Ahringer J (2007) Asymmetry of early endosome distribution in C. elegans embryos. PLoS One 2(6):e493. (PMID: <searchLink fieldCode="PM" term="%22175515741876258%22">175515741876258)</searchLink><br />Sato K, Sato M, Audhya A et al (2006) Dynamic regulation of caveolin-1 trafficking in the germ line and embryo of Caenorhabditis elegans. Mol Biol Cell 17(7):3085–3094. (PMID: <searchLink fieldCode="PM" term="%22166723741483042%22">166723741483042)</searchLink><br />Fan X, De Henau S, Feinstein J et al (2020) SapTrap assembly of Caenorhabditis elegans MosSCI transgene vectors. G3 (Bethesda) 10(2):635–644. (PMID: <searchLink fieldCode="PM" term="%2231848219%22">31848219)</searchLink>
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  Data: <i>Keywords: </i>Actin; C. elegans; Cytoplasmic streaming; Fluid flow; Microtubules; Oocyte; Zygote
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      – SubjectFull: Oocytes metabolism
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      – SubjectFull: Oocytes cytology
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