Smooth muscle α-actinin binds tightly to fesselin and attenuates its activity toward actin polymerization

Article

Abstract

Fesselin is an actin binding protein from smooth muscle that nucleates actin polymerization in a Ca++-calmodulin dependent manner, bundles actin and inhibits the actin-activated ATPase activity of myosin S1. We now report that fesselin binds to smooth muscle α-actinin. Binding was measured by blot overlay, affinity chromatography and sedimentation methods. Binding was moderate with an association constant of 1–4×107 M−1 assuming a 1:1 association of fesselin with α-actinin. Fesselin binds to the central spectrin domain repeat region of α-actinin but not to the CH1–CH2 domain. Fesselin accelerates the polymerization of actin. This activity of fesselin was attenuated by α-actinin. These observations support the role of fesselin in organizing the cytoskeleton.

References

  1. Asanuma K, Kim K, Oh J, Giardino L, Chabanis S, Faul C, Reiser J, Mundel P, (2005). Synaptopodin regulates the actin-bundling activity of α-actinin in an isoform-specific manner J Clin Invest 115:1188–1198PubMedGoogle Scholar
  2. Baron MD, Davison MD, Jones P, Critchley DR, (1987). The sequence of chick alpha actinin reveals homologies to spectrin and calmodulin J Biol Chem 262:17623–17629PubMedGoogle Scholar
  3. Beall B, Chalovich JM, (2001). Fesselin a synaptopodin-like protein, stimulates actin nucleation and polymerization Biochemistry 40:14252–14259PubMedCrossRefGoogle Scholar
  4. Blanchard A, Ohanian V, Critchley D, (1989). The structure and function of alpha-actinin J Muscle Res Cell Motil 10:280–289PubMedCrossRefGoogle Scholar
  5. Brenner SL, Korn ED, (1983). On the mechanism of actin monomer–polymer subunit exchange at steady state J Biol Chem 258:5013–5020PubMedGoogle Scholar
  6. Critchley DR, Flood G, (1999). α-actinins In: Kreis T, Vale R, (eds). Guidebook to the Cytoskeletal and Motor Proteins (2nd ed). Oxford University Press New York 24–27Google Scholar
  7. Eisenberg E, Kielley WW, (1972). Evidence for a refractory state of heavy meromyosin and subfragment-1 unable to bind to actin in the presence of ATP Cold Spring Harbor Symp Quant Biol 37:145–152Google Scholar
  8. Feramisco JR, Burridge K, (1980). A rapid purification of a-actinin, filamin, and a 130,000-dalton protein from smooth muscle J Biol Chem 255:1194–1199PubMedGoogle Scholar
  9. Fraley TS, Tran TC, Corgan AM, Nash CA, Hao J, Critchley DR, Greenwood JA, (2003). Phosphoinositide binding inhibits α-actinin bundling activity J Biol Chem 278:24039–24045PubMedCrossRefGoogle Scholar
  10. Imamura M, Endo T, Kuroda M, Tanaka T, Masaki T (1988). Substructure and higher structure of chicken smooth muscle alpha-actinin molecule J Biol Chem 263:7800–7805PubMedGoogle Scholar
  11. Kolakowski J, Wrzosek A, Dabrowska R, (2004). Fesselin is a target protein for calmodulin in a calcium-dependent manner Biochem Biophys Res Commun 323:1251–1256PubMedCrossRefGoogle Scholar
  12. Kouyama T, Mihashi K, (1981). Fluorimetry study of N-(1-pyrenyl)iodoacetamide-labeled F-actin: local structural change of actin protomer both on polymerization and on binding of heavy meromyosin Eur J Biochem 114:33–38PubMedGoogle Scholar
  13. Kremerskothen J, Plaas C, Kindler S, Frotscher M, Barnekow A, (2005). Synaptopodin, a molecule involved in the formation of the dendritic spine apparatus, is a dual actin/α-actinin binding protein J Neurochem 92:597–606PubMedCrossRefGoogle Scholar
  14. Kuroda M, Kohira Y, Sasaki M, (1994). Conformational change of skeletal muscle alpha-actinin induced by salt Biochim Biophys Acta 1205:97–104PubMedGoogle Scholar
  15. Leinweber, B. (1997) Ph.D. thesis, Maintaining the localization of actin in smooth muscle: α-actinin, filamin, calponin and SM85/95. Brody School of Medicine at East Carolina University, Greenville, NCGoogle Scholar
  16. Leinweber BD, Fredricksen RS, Hoffman DR, Chalovich JM, (1999). Fesselin: a novel synaptopodin-like actin binding protein from muscle tissue J Muscle Res Cell Motil 20:539–545PubMedCrossRefGoogle Scholar
  17. Leinweber B, Tang JX, Stafford WF, Chalovich JM, (1999). Calponin interaction with α-actinin–actin: Evidence for a structural role for calponin Biophys J 77:3208–3217PubMedCrossRefGoogle Scholar
  18. Mundel P, Heid HW, Mundel TM, Krüger M, Reiser J, Kriz W, (1997). Synaptopodin: An actin-associated protein in telencephalic dendrites and renal podocytes J Cell Biol 139:193–204PubMedCrossRefGoogle Scholar
  19. Otey CA, Carpen O, (2004). α-Actinin revisited: a fresh look at an old player Cell Motil Cytoskel 58:104–111CrossRefGoogle Scholar
  20. Patrie KM, Drescher AJ, Welihinda A, Mundel P, Margolis B, (2002). Interaction of two actin-binding proteins, synaptopodin and α-actinin-4, with the tight junction protein MAGI-1, J Biol Chem 277:30183–30190PubMedCrossRefGoogle Scholar
  21. Pollard TD, Cooper JA (1982). Methods to characterize actin filament networks Method Enzymol 85:211–233Google Scholar
  22. Schroeter M, Chalovich JM, (2004). Ca2+-calmodulin regulates fesselin-induced actin polymerization Biochemistry 43:13875–13882PubMedCrossRefGoogle Scholar
  23. Schroeter MM and Chalovich JM (2005) Fesselin binds to actin and myosin and inhibits actin activated ATPase activity, J Muscle Res Cell Motil 26:183–189PubMedCrossRefGoogle Scholar
  24. Spudich JA, Watt S, (1971). The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin–troponin complex with actin and the proteolytic fragments of myosin J Biol Chem 246:4866–4871PubMedGoogle Scholar
  25. Weins A, Schwarz K, Faul C, Barisoni L, Linke WA, Mundel P, (2001). Differentiation- and stress-dependent nuclear cytoplasmic redistribution of myopodin, a novel actin-bundling protein J Cell Biol 155:393–404PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  1. 1.Brody School of Medicine at East Carolina UniversityGreenvilleUSA

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