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Tropomyosin pp 187-200 | Cite as

Isoform Sorting of Tropomyosins

  • Claire Martin
  • Peter Gunning
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 644)

Abstract

Cytoskeletal tropomyosin (Tm) isoforms show extensive intracellular sorting, resulting in spatially distinct actin-filament populations. Sorting of Tm isoforms has been observed in a number of cell types, including fibroblasts, epithelial cells, osteoclasts, neurons and muscle cells. Different Tm isoforms have differential impact on the activity of a number of actin-binding proteins and can therefore differentially regulate actin filament function. Functionally distinct sub-populations of actin filaments can therefore be defined on the basis of the Tm isoforms associated with the filaments. The mechanisms that underlie Tm sorting are not yet well understood, but it is clear that Tm sorting is a very fluid and dynamic process, with changes in sorting occurring throughout development and cell differentiation. For this reason, it is unlikely that Tm localization is determined by an intrinsic sorting signal that directs particular isoforms to a single geographical location. Rather, a molecular sink model where isoforms accumulate in actin-based structures where they have the highest affinity, is most consistent with current data. This model would predict Tm sorting to be influenced by changes to actin filament dynamics and organization and collaboration with other actin-binding proteins.

Keywords

Growth Cone Myosin Light Chain Kinase Curr Opin Cell Biol Cleavage Furrow Tropomyosin Isoforms 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Lin JJ, Hegmann TE, Lin JL. Differential localization of tropomyosin isoforms in cultured nonmuscle cells. J Cell Biol 1988; 107(2):563–572.PubMedCrossRefGoogle Scholar
  2. 2.
    Schevzov G, Vrhovski B, Bryce NS et al. Tissue-specific tropomyosin isoform composition. J Histochem Cytochem 2005; 53(5):557–570.PubMedCrossRefGoogle Scholar
  3. 3.
    Percival JM, Thomas G, Cock TA et al. Sorting of tropomyosin isoforms in synchronised NIH 3T3 fibroblasts: evidence for distinct microfilament populations. Cell Motil Cytoskeleton 2000; 47(3):189–208.PubMedCrossRefGoogle Scholar
  4. 4.
    Percival JM, Hughes JA, Brown DL et al. Targeting of a tropomyosin isoform to short microfilaments associated with the Golgi complex. Mol Biol Cell 2004; 15(1):268–280.PubMedCrossRefGoogle Scholar
  5. 5.
    Pittenger MF, Helfman DM. In vitro and in vivo characterization of four fibroblast tropomyosins produced in bacteria: TM-2, TM-3, TM-5a and TM-5b are colocalized in interphase fibroblasts. J Cell Biol 1992; 118(4):841–858.PubMedCrossRefGoogle Scholar
  6. 6.
    Dalby-Payne JR, O’Loughlin EV, Gunning P. Polarization of specific tropomyosin isoforms in gastrointestinal epithelial cells and their impact on CFTR at the apical surface. Mol Biol Cell 2003; 14(11):4365–4375.PubMedCrossRefGoogle Scholar
  7. 7.
    Temm-Grove CJ, Jockusch BM, Weinberger RP et al. Distinct localizations of tropomyosin isoforms in LLC-PK1 epithelial cells suggests specialized function at cell-cell adhesions. Cell Motil Cytoskeleton 1998; 40(4):393–407.PubMedCrossRefGoogle Scholar
  8. 8.
    O’Hara SP, Lin JJ. Accumulation of tropomyosin isoform 5 at the infection sites of host cells during Cryptosporidium invasion. Parasitol Res 2006; 99(1):45–54.PubMedCrossRefGoogle Scholar
  9. 9.
    McMichael BK, Kotadiya P, Singh T et al. Tropomyosin isoforms localize to distinct microfilament populations in osteoclasts. Bone 2006; 39(4):694–705.PubMedCrossRefGoogle Scholar
  10. 10.
    Burgoyne RD, Norman KM. Immunocytochemical localization of tropomyosin in rat cerebellum. Brain Res 1985; 361(1–2):178–184.PubMedCrossRefGoogle Scholar
  11. 11.
    Burgoyne RD, Norman KM. Presence of tropomyosin in adrenal chromaffin cells and its association with chromaffin granule membranes. FEBS Lett 1985; 179(1):25–28.PubMedCrossRefGoogle Scholar
  12. 12.
    Had L, Faivre-Sarrailh C, Legrand C et al. Tropomyosin isoforms in rat neurons: the different developmental profiles and distributions of TM-4 and TMBr-3 are consistent with different functions. J Cell Sci 1994; 107 (Pt 10):2961–2973.PubMedGoogle Scholar
  13. 13.
    Weinberger R, Schevzov G, Jeffrey P et al. The molecular composition of neuronal microfilaments is spatially and temporally regulated. J Neurosci 1996; 16(1):238–252.PubMedGoogle Scholar
  14. 14.
    Schevzov G, Gunning P, Jeffrey PL et al. Tropomyosin localization reveals distinct populations of microfilaments in neurites and growth cones. Mol Cell Neurosci 1997; 8(6):439–454.PubMedCrossRefGoogle Scholar
  15. 15.
    Schevzov G, Bryce NS, Almonte-Baldonado R et al. Specific features of neuronal size and shape are regulated by tropomyosin isoforms. Mol Biol Cell 2005; 16(7):3425–3437.PubMedCrossRefGoogle Scholar
  16. 16.
    Vrhovski B, Schevzov G, Dingle S et al. Tropomyosin isoforms from the gamma gene differing at the C-terminus are spatially and developmentally regulated in the brain. J Neurosci Res 2003; 72(3):373–383.PubMedCrossRefGoogle Scholar
  17. 17.
    Perry SV. Vertebrate tropomyosin: distribution, properties and function. J Muscle Res Cell Motil 2001; 22(1):5–49.PubMedCrossRefGoogle Scholar
  18. 18.
    Kee AJ, Schevzov G, Nair-Shalliker V et al. Sorting of a nonmuscle tropomyosin to a novel cytoskeletal compartment in skeletal muscle results in muscular dystrophy. J Cell Biol 2004; 166(5):685–696.PubMedCrossRefGoogle Scholar
  19. 19.
    Vlahovich N, Schevzov G, Nair-Shalliker V et al. Tropomyosin 4 defines novel filaments in skeletal muscle associated with muscle remodelling/regeneration in normal and diseased muscle. Cell Motil Cytoskeleton 2008; 65(1):73–85.PubMedCrossRefGoogle Scholar
  20. 20.
    Heimann K, Percival JM, Weinberger R et al. Specific isoforms of actin-binding proteins on distinct populations of Golgi-derived vesicles. J Biol Chem 1999; 274(16):10743–10750.PubMedCrossRefGoogle Scholar
  21. 21.
    Rios RM, Bornens M. The Golgi apparatus at the cell centre. Curr Opin Cell Biol 2003; 15(1):60–66.PubMedCrossRefGoogle Scholar
  22. 22.
    Gao Y, Sztul E. A novel interaction of the Golgi complex with the vimentin intermediate filament cytoskeleton. J Cell Biol 2001; 152(5):877–894.PubMedCrossRefGoogle Scholar
  23. 23.
    Egea G, Lazaro-Dieguez F, Vilella M. Actin dynamics at the Golgi complex in mammalian cells. Curr Opin Cell Biol 2006; 18(2):168–178.PubMedCrossRefGoogle Scholar
  24. 24.
    DesMarais V, Ichetovkin I, Condeelis J et al. Spatial regulation of actin dynamics: a tropomyosin-free, actin-rich compartment at the leading edge. J Cell Sci 2002; 115 (Pt 23):4649–4660.PubMedCrossRefGoogle Scholar
  25. 25.
    Hillberg L, Zhao Rathje LS, Nyakern-Meazza M et al. Tropomyosins are present in lamellipodia of motile cells. Eur J Cell Biol 2006; 85(5):399–409.PubMedCrossRefGoogle Scholar
  26. 26.
    Hannan AJ, Schevzov G, Gunning P et al. Intracellular localization of tropomyosin mRNA and protein is associated with development of neuronal polarity. Mol Cell Neurosci 1995; 6(5):397–412.PubMedCrossRefGoogle Scholar
  27. 27.
    Du TG, Schmid M, Jansen RP. Why cells move messages: the biological functions of mRNA localization. Semin Cell Dev Biol 2007; 18(2):171–177.PubMedCrossRefGoogle Scholar
  28. 28.
    Hannan AJ, Gunning P, Jeffrey PL et al. Structural compartments within neurons: developmentally regulated organization of microfilament isoform mRNA and protein. Molecular & Cellular Neurosciences 1998; 11(5–6):289–304.CrossRefGoogle Scholar
  29. 29.
    Percival JM. Cell cycle regulation of actin and tropomyosin isoforms. [PhD thesis]. Sydney (NSW): University of Sydney 2002.Google Scholar
  30. 30.
    Schevzov G, Lloyd C, Hailstones D et al. Differential regulation of tropomyosin isoform organization and gene expression in response to altered actin gene expression. J Cell Biol 1993; 121(4):811–821.PubMedCrossRefGoogle Scholar
  31. 31.
    Hammell RL, Hitchcock-DeGregori SE. The sequence of the alternatively spliced sixth exon of alpha-tropomyosin is critical for cooperative actin binding but not for interaction with troponin. J Biol Chem 1997; 272(36):22409–22416.PubMedCrossRefGoogle Scholar
  32. 32.
    Pittenger MF, Kistler A, Helfman DM. Alternatively spliced exons of the beta tropomyosin gene exhibit different affinities for F-actin and effects with nonmuscle caldesmon. J Cell Sci 1995; 108 (Pt 10):3253–3265.PubMedGoogle Scholar
  33. 33.
    Vrhovski B, Lemckert F, Gunning P. Modification of the tropomyosin isoform composition of actin filaments in the brain by deletion of an alternatively spliced exon. Neuropharmacology 2004; 47(5):684–693.PubMedCrossRefGoogle Scholar
  34. 34.
    Gimona M, Watakabe A, Helfman DM. Specificity of dimer formation in tropomyosins: influence of alternatively spliced exons on homodimer and heterodimer assembly. Proc Natl Acad Sci USA 1995; 92(21):9776–9780.PubMedCrossRefGoogle Scholar
  35. 35.
    Ridley AJ, Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992; 70(3):389–399.PubMedCrossRefGoogle Scholar
  36. 36.
    Kozma R, Ahmed S, Best A et al. The Ras-related protein Cdc42 Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol Cell Biol 1995; 15(4):1942–1952.PubMedGoogle Scholar
  37. 37.
    Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005; 21:247–269.PubMedCrossRefGoogle Scholar
  38. 38.
    Bernard O. Lim kinases, regulators of actin dynamics. Int J Biochem Cell Biol 2006; b39(6):1071–1076.Google Scholar
  39. 39.
    Houle F, Rousseau S, Morrice N et al. Extracellular signal-regulated kinase mediates phosphorylation of tropomyosin-1 to promote cytoskeleton remodeling in response to oxidative stress: impact on membrane blebbing. Mol Biol Cell 2003; 14(4):1418–1432.PubMedCrossRefGoogle Scholar
  40. 40.
    Houle F, Huot J. Dysregulation of the endothelial cellular response to oxidative stress in cancer. Mol Carcinog 2006; 45(6):362–367.PubMedCrossRefGoogle Scholar
  41. 41.
    Lubit BW, Schwartz JH. An antiactin antibody that distinguishes between cytoplasmic and skeletal muscle actins. J Cell Biol 1980; 86(3):891–897.PubMedCrossRefGoogle Scholar
  42. 42.
    Herman IM. Actin isoforms. Curr Opin Cell Biol 1993; 5(1):48–55.PubMedCrossRefGoogle Scholar
  43. 43.
    Kolega J. Cytoplasmic dynamics of myosin IIA and IIB: spatial’ sorting’ of isoforms in locomoting cells. J Cell Sci 1998; 111(15):2085–2095.PubMedGoogle Scholar
  44. 44.
    Sabry JH, Moores SL, Ryan S et al. Myosin heavy chain phosphorylation sites regulate myosin localization during cytokinesis in live cells. Mol Biol Cell 1997; 8(12):2605–2615.PubMedGoogle Scholar
  45. 45.
    Dean SO, Rogers SL, Stuurman N et al. Distinct pathways control recruitment and maintenance of myosin II at the cleavage furrow during cytokinesis. Proc Natl Acad Sci USA 2005; 102(38):13473–13478.PubMedCrossRefGoogle Scholar
  46. 46.
    Komiyama M, Soldati T, von Arx P et al. The intracompartmental sorting of myosin alkali light chain isoproteins reflects the sequence of developmental expression as determined by double epitope-tagging competition. J Cell Sci 1996; 109(8):2089–2099.PubMedGoogle Scholar
  47. 47.
    Gunning PW, Schevzov G, Kee AJ et al. Tropomyosin isoforms: divining rods for actin cytoskeleton function. Trends Cell Biol 2005; 15(6):333–341.PubMedCrossRefGoogle Scholar
  48. 48.
    Bryce NS, Schevzov G, Ferguson V et al. Specification of actin filament function and molecular composition by tropomyosin isoforms. Mol Biol Cell 2003; 14(3):1002–1016.PubMedCrossRefGoogle Scholar
  49. 49.
    Drees B, Brown C, Barrell BG et al. Tropomyosin is essential in yeast yet the TPM1 and TPM2 products perform distinct functions. J Cell Biol 1995; 128(3):383–392.PubMedCrossRefGoogle Scholar
  50. 50.
    Blanchard EM, Iizuka K, Christe M et al. Targeted ablation of the murine alpha-tropomyosin gene. Circ Res 1997; 81(6):1005–1010.PubMedGoogle Scholar
  51. 51.
    Rethinasamy P, Muthuchamy M, Hewett T et al. Molecular and physiological effects of alpha-tropomyosin ablation in the mouse. Circ Res 1998; 82(1):116–123.PubMedGoogle Scholar
  52. 52.
    Hook J, Lemckert F, Qin H et al. Gamma tropomyosin gene products are required for embryonic development. Mol Cell Biol 2004; 24(6):2318–2323.PubMedCrossRefGoogle Scholar
  53. 53.
    Fanning AS, Wolenski JS, Mooseker MS et al. Differential regulation of skeletal muscle myosin-II and brush border myosin-I enzymology and mechanochemistry by bacterially produced tropomyosin isoforms. Cell Motil Cytoskeleton 1994; 29(1):29–45.PubMedCrossRefGoogle Scholar
  54. 54.
    Ishikawa R, Yamashiro S, Matsumura F. Differential modulation of actin-severing activity of gelsolin by multiple isoforms of cultured rat cell tropomyosin. Potentiation of protective ability of tropomyosins by 83-kDa nonmuscle caldesmon. J Biol Chem 1989; 264(13):7490–7497.PubMedGoogle Scholar
  55. 55.
    Wawro B, Greenfield NJ, Wear MA et al. Tropomyosin Regulates Elongation by Formin at the Fast-Growing End of the Actin Filament. Biochemistry 2007; 46(27):8146–8155.PubMedCrossRefGoogle Scholar
  56. 56.
    Gunning P, O’Neill G, Hardeman E. Tropomyosin-based regulation of the actin cytoskeleton in time and space. Physiological Reviews. 2008;88(1):1–35.PubMedCrossRefGoogle Scholar
  57. 57.
    Schevzov G, Fath T, Vrhovski B et al. Divergent regulation of the sarcomere and the cytoskeleton. J Biol Chem 2008; 283(1):275–283.PubMedCrossRefGoogle Scholar
  58. 58.
    Muthuchamy M, Grupp IL, Grupp G et al., Molecular and physiological effects of overexpressing striated muscle beta-tropomyosin in the adult murine heart. J Biol Chem 1995; 270(51):30593–30603.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2008

Authors and Affiliations

  1. 1.Oncology Research UnitThe Children’s Hospital at WestmeadWestmeadAustralia
  2. 2.Oncology Research Unit, Department of Pharmacology, School of Medical SciencesUniversity of New South WalesSydneyAustralia

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