Abstract
For some time the view that the actin cytoskeleton acts primarily as a scaffold, to be assembled in response to a signaling cascade as an end point in the pathway, has prevailed. However, it is now clear that the dynamic nature of the cytoskeleton is linked to downstream signaling events that further modulate cellular activity, and which can determine cell fate. Examples of this lie within the regulation of programmed cell death, the maintenance of homeostasis and the process of cellular ageing. In yeast the actin cytoskeleton has been shown to interact directly with signaling pathways known to be important in the regulation of both ageing and cell death. For example it has been discovered that the level of damage sustained by the actin cytoskeleton under conditions of oxidative stress is directly linked to apoptosis. Further evidence comes from the finding that actin based propulsion mechanisms are required for the inheritance of mitochondria and anti-ageing factors into newly formed cells. In addition to this actin is known to directly influence the formation of protein aggregations. In this chapter we will discuss these points and postulate as to their significance with respect to the maintenance of cellular homeostasis.
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References
Adams AEM, Pringle JR (1984) Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenic-mutant Saccharomyces cerevisiae. J Cell Biol 98:934.
Amatruda JF et al (1990) Disruption of the actin cytoskeleton in yeast capping protein mutants. Nature 344(6264):352–354.
Ayscough KR, Drubin DG (1996) ACTIN: general principles from studies in yeast. Annu Rev Cell Dev Biol 12:129–160.
Ayscough KR et al (1997) High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J Cell Biol 137(2):399–416.
Bailleul PA et al (1999) Genetic study of interactions between the cytoskeletal assembly protein sla1 and prion-forming domain of the release factor Sup35 (eRF3) in Saccharomyces cerevisiae. Genetics 153(1):81–94.
Balcer HI et al (2003) Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1. Curr Biol 13(24):2159–2169.
Bellomo G et al (1990) Cytoskeleton as a target in menadione-induced oxidative stress in cultured mammalian cells. I. Biochemical and immunocytochemical features. J Cell Physiol 143(1):118–128.
Bencsath FA et al (1996) Identification of the disulfide-linked peptide in irreversibly sickled cell ß-actin. Biochemistry 35:4403–4408.
Bettinger BT, Gilbert DM, Amberg DC (2004) Actin up in the nucleus. Nat Rev Mol Cell Biol 5(5):410–415.
Bi E et al (1998) Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J Cell Biol 142(5):1301–1312.
Blander G, Guarente L (2004) The Sir2 family of protein deacetylases. Annu Rev Biochem 73:417–435.
Boldogh I et al (1998) Interaction between mitochondria and the actin cytoskeleton in budding yeast requires two integral mitochondrial outer membrane proteins, Mmm1p and Mdm10p. J Cell Biol 141(6):1371–1381.
Boldogh IR et al (2003) A protein complex containing Mdm10p, Mdm12p, and Mmm1p links mitochondrial membranes and DNA to the cytoskeleton-based segregation machinery. Mol Biol Cell 14(11):4618–4627.
Boldogh IR et al (2004) A type V myosin (Myo2p) and a Rab-like G-protein (Ypt11p) are required for retention of newly inherited mitochondria in yeast cells during cell division. Mol Biol Cell 15(9):3994–4002.
Boldogh IR, Pon LA (2006) Interactions of mitochondria with the actin cytoskeleton. Biochim Biophys Acta 1763(5–6):450–462.
Bretscher A (2003) Polarized growth and organelle segregation in yeast: the tracks, motors, and receptors. J Cell Biol 160(6):811–816.
Casamayor A, Snyder M (2002) Bud-site selection and cell polarity in budding yeast. Curr Opin Microbiol 5(2):179–186.
Chada S, Hollenbeck PJ (2003) Mitochondrial movement and positioning in axons: the role of growth factor signaling. J Exp Biol 206:1985–1992.
Chada S, Hollenbeck PJ (2004) Nerve growth factor signalling regulates motility and docking of axonal mitochondria. Curr Biol 14:1272–1276.
Chai YC et al (1994) S-thiolation of individual human neutrophil proteins including actin by stimulation of the respiratory burst: evidence against a role for glutathione disulfide. Arch Biochem Biophys 310(1):273–281.
Chang DTW et al (2006) Mutant huntingtin aggregates impair mitochondrial movement and trafficking in cortical neurons. Neurobiol Dis 22(2):388–400.
Chang DTW, Reynolds IJ (2006) Mitochondrial trafficking and morphology in healthy and injured neurons. Progr Neurobiol 80:241–268.
Chevtzoff C et al (2005) The yeast cAMP protein kinase Tpk3p is involved in the regulation of mitochondrial enzymatic content during growth. Biochim Biophys Acta 1706(1–2):117–125.
Dalle-Donne I et al (2001) The actin cytoskeleton response to oxidants: from small heat shock protein phosphorylation to changes in the redox state of actin itself. Free Rad Biol Med 31:1624–1632.
Dalle-Donne I et al (2003) Reversible S-glutathionylation of Cys 374 regulates actin filament formation by inducing structural changes in the actin molecule. Free Radic Biol Med 34(1):23–32.
Dalle-Donne I, Milzani A, Colombo R (1995) H2O2-treated actin: assembly and polymer interactions with cross-linking proteins. Biophys J 69(6):2710–2719.
Davis AF, Clayton DA (1996) In situ localization of mitochondrial DNA replication in intact mammalian cells. J Cell Biol 135(4):883–893.
Davis RC, Furukawa R, Fechheimer M (2008) A cell culture model for investigation of Hirano bodies. Acta Neuropathol 115(2):205–217.
Dong Y, Pruyne D, Bretscher A (2003) Formin-dependent actin assembly is regulated by distinct modes of Rho signaling in yeast. J Cell Biol 161(6):1081–1092.
Drewes G, Faulstich H (1990) The enhanced ATPase activity of glutathione-substituted actin provides a quantitative approach to filament stabilization. J Biol Chem 265(6):3017–3021.
Evangelista M et al (1997) Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276(5309):118–122.
Evangelista M et al (2002) Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat Cell Biol 4(3):260–269.
Evans LL, Bridgman PC (1995) Particles move along actin filament bundles in nerve growth cones. Proc Natl Acad Sci 92(24):10954–10958.
Faulstich H, Heintz D, Drewes G (1992) Interchain and intrachain crosslinking of actin thiols by a bifunctional thiol reagent. FEBS Lett 302(3):201–205.
Fechheimer M et al (2002) Hirano bodies in health and disease. Trends Mol Med 8(12):590–591.
Fehrenbacher KL et al (2004) Live cell imaging of mitochondrial movement along actin cables in budding yeast. Curr Biol 14(22):1996–2004.
Franklin-Tong VE, Gourlay CW (2008) A role for actin in regulating apoptosis/programmed cell death: evidence spanning yeast, plants and animals. Biochem J 413(3):389–404.
Freeman NL et al (1996) A conserved proline-rich region of the Saccharomyces cerevisiae cyclase-associated protein binds SH3 domains and modulates cytoskeletal localization. Mol Cell Biol 16(2):548–556.
Garcia-Rodriguez LJ, Gay AC, Pon LA (2007) Puf3p, a Pumilio family RNA binding protein, localizes to mitochondria and regulates mitochondrial biogenesis and motility in budding yeast. J Cell Biol 176(2):197–207.
Gerst JE et al (1991) CAP is a bifunctional component of the Saccharomyces cerevisiae adenylyl cyclase complex. Mol Cell Biol 11(3):1248–1257.
Gourlay CW, Ayscough KR (2005) Identification of an upstream regulatory pathway controlling actin-mediated apoptosis in yeast. J Cell Sci 118(Pt 10):2119–2132.
Gourlay CW, Ayscough KR (2006) Actin-induced hyperactivation of the Ras signaling pathway leads to apoptosis in Saccharomyces cerevisiae. Mol Cell Biol 26(17):6487–6501.
Gourlay CW et al (2004) A role for the actin cytoskeleton in cell death and aging in yeast. J Cell Biol 164(6):803–809.
Gray MW (1993) Origin and, evolution of organelle genomes. Curr Opin Genet Dev 3(6):884–890.
Haarer BK, Amberg DC (2004) Old yellow enzyme protects the actin cytoskeleton from oxidative stress. Mol Biol Cell 15(10):4522–4531.
Haarer BK et al (1990) Purification of profilin from Saccharomyces cerevisiae and analysis of profilin-deficient cells. J Cell Biol 110(1):105–114.
He C et al (2006) Recruitment of Atg9 to the preautophagosomal structure by Atg11 is essential for selective autophagy in budding yeast. J Cell Biol 175(6):925–935.
Hebbel RP et al (1982) Spontaneous oxygen radical generation by sickle erythrocytes. J Clin Invest 70(6):1253–1259.
Hebbel RP et al (1988) Accelerated autoxidation and heme loss due to instability of sickle hemoglobin. Proc Natl Acad Sci USA 85(1):237–241.
Heeren G et al (2004) The role of respiration, reactive oxygen species and oxidative stress in mother cell-specific ageing of yeast strains defective in the RAS signalling pathway. FEMS Yeast Res 5(2):157–167.
Herrero E, Belli G, Casa C (2010) Structural and functional diversity of glutaredoxins in yeast. Curr Protein Pept Sci 11(8):659–668.
Hinshaw DB et al (1986) Cytoskeletal and morphologic impact of cellular oxidant injury. Am J Pathol 123(3):454–464.
Hinshaw DB et al (1988) ATP and microfilaments in cellular oxidant injury. Am J Pathol 132(3):479–488.
Hlavata L et al (2003) The oncogenic RAS2(val19) mutation locks respiration, independently of PKA, in a mode prone to generate ROS. EMBO J 22(13):3337–3345.
Huckaba TM et al (2004) Live cell imaging of the assembly, disassembly, and actin cable-dependent movement of endosomes and actin patches in the budding yeast, Saccharomyces cerevisiae. J Cell Biol 167(3):519–530.
Huckaba TM, Lipkin T, Pon LA (2006) Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast. J Cell Biol 175(6):957–969.
Johnston GC, Prendergast JA, Singer RA (1991) The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J Cell Biol 113(3):539–551.
Kaksonen M, Sun Y, Drubin DG (2003) A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115(4):475–487.
Kaksonen M, Toret CP, Drubin DG (2005) A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123(2):305–320.
Kandl KA et al (2002) Identification of a role for actin in translational fidelity in yeast. Mol Genet Genomics 268(1):10–18.
Kanki T, Klionsky DJ (2008) Mitophagy in yeast occurs through a selective mechanism. J Biol Chem 283(47):32386–32393.
Kaul DK et al (1983) Erythrocytes in sickle cell anemia are heterogeneous in their rheological and hemodynamic characteristics. J Clin Invest 72:22–31.
Klinger H et al (2010) Quantitation of (a)symmetric inheritance of functional and of oxidatively damaged mitochondrial aconitase in the cell division of old yeast mother cells. Exp Gerontol 45(7–8):533–542.
Lachant NA, Davidson WD, Tanaka KR (1983) Impaired pentose phosphate shunt function in sickle cell disease: a potential mechanism for increased Heinz body formation and membrane lipid peroxidation. Am J Hematol 15(1):1–13.
Lassing I et al (2007) Molecular and structural basis for redox regulation of beta-Actin. J Mol Biol 370(2):331–348.
Lazzarino DA et al (1994) Yeast mitochondria contain ATP-sensitive, reversible actin-binding activity. Mol Biol Cell 5(7):807–818.
Lippincott J, Li R (1998) Sequential assembly of myosin II, an IQGAP-like protein, and filamentous actin to a ring structure involved in budding yeast cytokinesis. J Cell Biol 140(2):355–366.
Liu B et al (2010) The polarisome is required for segregation and retrograde transport of protein aggregates. Cell 140(2):257–267.
Longo VD, Kennedy BK (2006) Sirtuins in aging and age-related disease. Cell 126(2):257–268.
Longtine MS et al (1996) The septins: roles in cytokinesis and other processes. Curr Opin Cell Biol 8(1):106–119.
Lux SE, John KM, Karnovsky MJ (1976) Irreversible deformation of the spectrin-actin lattice in irreversibly sickled cells. J Clin Invest 58:955–963.
Maselli A et al (2003) Formation of Hirano bodies induced by expression of an actin cross-linking protein with a gain-of-function mutation. Eukaryot Cell 2(4):778–787.
Maselli AG et al (2002) Formation of Hirano bodies in Dictyostelium and mammalian cells induced by expression of a modified form of an actin-crosslinking protein. J Cell Sci 115(Pt 9):1939–1949.
Mashima T et al (1995) Identification of actin as a substrate of ICE and an ICE-like protease and involvement of an ICE-like protease but not ICE in VP-16-induced U937 apoptosis. Biochem Biophys Res Commun 217(3):1185–1192.
Mattila PK et al (2004) A high-affinity interaction with ADP-actin monomers underlies the mechanism and in vivo function of Srv2/cyclase-associated protein. Mol Biol Cell 15(11):5158–5171.
Meriin AB et al (2003) Aggregation of expanded polyglutamine domain in yeast leads to defects in endocytosis. Mol Cell Biol 23(21):7554–7565.
Metzler M et al (2001) HIP1 functions in clathrin-mediated endocytosis through binding to clathrin and adaptor protein 2. J Biol Chem 276(42):39271–39276.
Mintzer KA, Field J (1994) Interactions between adenylyl cyclase, CAP and RAS from Saccharomyces cerevisiae. Cell Signal 6(6):681–694.
Mirabelli F et al (1988) Menadione-induced bleb formation in hepatocytes is associated with the oxidation of thiol groups in actin. Arch Biochem Biophys 264(1):261–269.
Mirabelli F et al (1989) Cytoskeletal alterations in human platelets exposed to oxidative stress are mediated by oxidative and Ca2+-dependent mechanisms. Arch Biochem Biophys 270(2):478–488.
Monastyrska I et al (2008) Arp2 links autophagic machinery with the actin cytoskeleton. Mol Biol Cell 19(5):1962–1975.
Moon AL et al (1993) Cofilin is an essential component of the yeast cortical cytoskeleton. J Cell Biol 120(2):421–435.
Morris RL, Hollenbeck PJ (1995) Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J Cell Biol 131(5):1315–1326.
Moseley JB, Goode BL (2006) The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol Mol Biol Rev 70(3):605–645.
Mulholland J et al (1994) Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J Cell Biol 125(2):381–391.
Naqvi SN et al (1998) The WASp homologue Las17p functions with the WIP homologue End5p/verprolin and is essential for endocytosis in yeast. Curr Biol 8(17):959–962.
Nicholson-Dykstra S, Higgs HN, Harris ES (2005) Actin dynamics: growth from dendritic branches. Curr Biol 15(9):R346–R357.
Okada K et al (2006) Aip1 and cofilin promote rapid turnover of yeast actin patches and cables: a coordinated mechanism for severing and capping filaments. Mol Biol Cell 17(7):2855–2868.
Omann GM et al (1994) H2O2-induced increases in cellular F-actin occur without increases in actin nucleation activity. Arch Biochem Biophys 308(2):407–412.
Pollard TD (1986) Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. J Cell Biol 103(6 Pt 2):2747–2754.
Pollard TD (2007) Regulation of actin filament assembly by Arp2/3 complex and formins. Annu Rev Biophys Biomol Struct 36:451–477.
Pollard TD, Blanchoin L, Mullins RD (2000) Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29:545–576.
Pruyne D, Bretscher A (2000) Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J Cell Sci 113(Pt 3):365–375.
Pruyne D et al (2002) Role of formins in actin assembly: nucleation and barbed-end association. Science 297(5581):612–615.
Pruyne D et al (2004) Mechanisms of polarized growth and organelle segregation in yeast. Annu Rev Cell Dev Biol 20:559–591.
Pruyne DW, Schott DH, Bretscher A (1998) Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. J Cell Biol 143(7):1931–1945.
Rokutan K, Johnston RB Jr, Kawai K (1994) Oxidative stress induces S-thiolation of specific proteins in cultured gastric mucosal cells. Am J Physiol 266(2 Pt 1):G247–G254.
Rolland F, Winderickx J, Thevelein JM (2002) Glucose-sensing and -signalling mechanisms in yeast. FEMS Yeast Res 2(2):183–201.
Sagot I et al (2006) Actin bodies in yeast quiescent cells: an immediately available actin reserve? Mol Biol Cell 17(11):4645–4655.
Sagot I, Klee SK, Pellman D (2002) Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat Cell Biol 4(1):42–50.
Schott DH, Collins RN, Bretscher A (2002) Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J Cell Biol 156(1):35–39.
Sept D, McCammon JA (2001) Thermodynamics and kinetics of actin filament nucleation. Biophys J 81(2):667–674.
Shartava A et al (1995) A posttranslational modification of ß-actin contributes to the slow dissociation of the spectrin-protein 4.1-actin complex of irreversibly sickled cells. J Cell Biol 128:805–818.
Shartava A et al (1997) Irreversibly sickled cell ß-actin: defective filament formation. Am J Hemat 55:97–103.
Sheu YJ et al (1998) Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis. Mol Cell Biol 18(7):4053–4069.
Shortle D, Haber JE, Botstein D (1982) Lethal disruption of the yeast actin gene by integrative DNA transformation. Science 217(4557):371–373.
Singaraja RR et al (2002) HIP14, a novel ankyrin domain-containing protein, links huntingtin to intracellular trafficking and endocytosis. Hum Mol Genet 11(23):2815–2828.
Smythe E, Ayscough KR (2003) The Ark1/Prk1 family of protein kinases. Regulators of endocytosis and the actin skeleton. EMBO Rep 4(3):246–251.
Smythe E, Ayscough KR (2006) Actin regulation in endocytosis. J Cell Sci 119(Pt 22):4589–4598.
Sokolov S et al (2006) Expression of an expanded polyglutamine domain in yeast causes death with apoptotic markers. Biochim Biophys Acta 1757(5–6):660–666.
Solans A et al (2006) Cytotoxicity of a mutant huntingtin fragment in yeast involves early alterations in mitochondrial OXPHOS complexes II and III. Hum Mol Genet 15(20):3063–3081.
Stournaras C et al (1990) Glutathionyl(cysteine-374) actin forms filaments of low mechanical stability. Biochim Biophys Acta 1037(1):86–91.
Tang JX et al (1999) Thiol oxidation of actin produces dimers that enhance the elasticity of the F-actin network. Biophys J 76(4):2208–2215.
Thevelein JM, de Winde JH (1999) Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol 33(5):904–918.
Velier J et al (1998) Wild-type and mutant huntingtins function in vesicle trafficking in the secretory and endocytic pathways. Exp Neurol 152(1):34–40.
Wang J et al (2001) Reversible glutathionylation regulates actin polymerization in A431 cells. J Biol Chem 276:47763–47766.
Welch MD, Mullins RD (2002) Cellular control of actin nucleation. Annu Rev Cell Dev Biol 18:247–288.
Whitacre J et al (2001) Generation of an isogenic collection of yeast actin mutants and identification of three interrelated phenotypes. Genetics 157(2):533–543.
Wolven AK et al (2000) In vivo importance of actin nucleotide exchange catalyzed by profilin. J Cell Biol 150(4):895–904.
Yang HC, Pon LA (2002) Actin cable dynamics in budding yeast. Proc Natl Acad Sci USA 99(2):751–756.
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Amberg, D., Leadsham, J.E., Kotiadis, V., Gourlay, C.W. (2011). Cellular Ageing and the Actin Cytoskeleton. In: Breitenbach, M., Jazwinski, S., Laun, P. (eds) Aging Research in Yeast. Subcellular Biochemistry, vol 57. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2561-4_15
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