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. 1995 Jul;69(1):228–241. doi: 10.1016/S0006-3495(95)79894-0

Interaction of the 47-kDa talin fragment and the 32-kDa vinculin fragment with acidic phospholipids: a computer analysis.

M Tempel 1, W H Goldmann 1, G Isenberg 1, E Sackmann 1
PMCID: PMC1236240  PMID: 7669900

Abstract

In recent in vitro experiments, it has been demonstrated that the 47-kDa fragment of the talin molecule and the 32-kDa fragment of the vinculin molecule interact with acidic phospholipids. By using a computer analysis method, we determined the hydrophobic and amphipathic stretches of these fragments and, by applying a purpose-written matrix method, we ascertained the molecular amphipathic structure of alpha-helices. Calculations for the 47-kDa mouse talin fragment (residues 1-433; NH2-terminal region) suggest specific interactions of residues 21-39, 287-342, and 385-406 with acidic phospholipids and a general lipid-binding domain for mouse talin (primary amino acid sequence 385-401) and for Dictyostelium talin (primary amino acid sequence 348-364). Calculations for the 32-kDa chicken embryo vinculin fragment (residues 858-1066; COOH-terminal region) and from nematode vinculin alignment indicate for chicken embryo vinculin residues 935-978 and 1020-1040 interactions with acidic phospholipids. Experimental confirmation has been given for vinculin (residues 916-970), and future detailed experimental analyses are now needed to support the remaining computational data.

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Selected References

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  1. Barstead R. J., Waterston R. H. The basal component of the nematode dense-body is vinculin. J Biol Chem. 1989 Jun 15;264(17):10177–10185. [PubMed] [Google Scholar]
  2. Beckerle M. C., O'Halloran T., Burridge K. Demonstration of a relationship between talin and P235, a major substrate of the calcium-dependent protease in platelets. J Cell Biochem. 1986;30(3):259–270. doi: 10.1002/jcb.240300307. [DOI] [PubMed] [Google Scholar]
  3. Beckerle M. C., Yeh R. K. Talin: role at sites of cell-substratum adhesion. Cell Motil Cytoskeleton. 1990;16(1):7–13. doi: 10.1002/cm.970160103. [DOI] [PubMed] [Google Scholar]
  4. Belkin A. M., Koteliansky V. E. Interaction of iodinated vinculin, metavinculin and alpha-actinin with cytoskeletal proteins. FEBS Lett. 1987 Aug 17;220(2):291–294. doi: 10.1016/0014-5793(87)80832-3. [DOI] [PubMed] [Google Scholar]
  5. Blobel G. Intracellular protein topogenesis. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1496–1500. doi: 10.1073/pnas.77.3.1496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Burridge K., Mangeat P. An interaction between vinculin and talin. Nature. 1984 Apr 19;308(5961):744–746. doi: 10.1038/308744a0. [DOI] [PubMed] [Google Scholar]
  7. Chou P. Y., Fasman G. D. Empirical predictions of protein conformation. Annu Rev Biochem. 1978;47:251–276. doi: 10.1146/annurev.bi.47.070178.001343. [DOI] [PubMed] [Google Scholar]
  8. Cohen A. M., Liu S. C., Lawler J., Derick L., Palek J. Identification of the protein 4.1 binding site to phosphatidylserine vesicles. Biochemistry. 1988 Jan 26;27(2):614–619. doi: 10.1021/bi00402a018. [DOI] [PubMed] [Google Scholar]
  9. Coutu M. D., Craig S. W. cDNA-derived sequence of chicken embryo vinculin. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8535–8539. doi: 10.1073/pnas.85.22.8535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Crawford A. W., Michelsen J. W., Beckerle M. C. An interaction between zyxin and alpha-actinin. J Cell Biol. 1992 Mar;116(6):1381–1393. doi: 10.1083/jcb.116.6.1381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dietrich C., Goldmann W. H., Sackmann E., Isenberg G. Interaction of NBD-talin with lipid monolayers. A film balance study. FEBS Lett. 1993 Jun 7;324(1):37–40. doi: 10.1016/0014-5793(93)81527-7. [DOI] [PubMed] [Google Scholar]
  13. Eimer W., Niermann M., Eppe M. A., Jockusch B. M. Molecular shape of vinculin in aqueous solution. J Mol Biol. 1993 Jan 5;229(1):146–152. doi: 10.1006/jmbi.1993.1014. [DOI] [PubMed] [Google Scholar]
  14. Eisenberg D., Schwarz E., Komaromy M., Wall R. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J Mol Biol. 1984 Oct 15;179(1):125–142. doi: 10.1016/0022-2836(84)90309-7. [DOI] [PubMed] [Google Scholar]
  15. Eisenberg D., Weiss R. M., Terwilliger T. C. The helical hydrophobic moment: a measure of the amphiphilicity of a helix. Nature. 1982 Sep 23;299(5881):371–374. doi: 10.1038/299371a0. [DOI] [PubMed] [Google Scholar]
  16. Engelman D. M., Steitz T. A., Goldman A. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu Rev Biophys Biophys Chem. 1986;15:321–353. doi: 10.1146/annurev.bb.15.060186.001541. [DOI] [PubMed] [Google Scholar]
  17. Fringeli U. P., Leutert P., Thurnhofer H., Fringeli M., Burger M. M. Structure-activity relationship in vinculin: an IR/attenuated total reflection spectroscopic and film balance study. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1315–1319. doi: 10.1073/pnas.83.5.1315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Garnier J., Osguthorpe D. J., Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol. 1978 Mar 25;120(1):97–120. doi: 10.1016/0022-2836(78)90297-8. [DOI] [PubMed] [Google Scholar]
  19. Geiger B., Ginsberg D. The cytoplasmic domain of adherens-type junctions. Cell Motil Cytoskeleton. 1991;20(1):1–6. doi: 10.1002/cm.970200102. [DOI] [PubMed] [Google Scholar]
  20. Geiger B., Tokuyasu K. T., Dutton A. H., Singer S. J. Vinculin, an intracellular protein localized at specialized sites where microfilament bundles terminate at cell membranes. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4127–4131. doi: 10.1073/pnas.77.7.4127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gibrat J. F., Garnier J., Robson B. Further developments of protein secondary structure prediction using information theory. New parameters and consideration of residue pairs. J Mol Biol. 1987 Dec 5;198(3):425–443. doi: 10.1016/0022-2836(87)90292-0. [DOI] [PubMed] [Google Scholar]
  22. Gilmore A. P., Jackson P., Waites G. T., Critchley D. R. Further characterisation of the talin-binding site in the cytoskeletal protein vinculin. J Cell Sci. 1992 Nov;103(Pt 3):719–731. doi: 10.1242/jcs.103.3.719. [DOI] [PubMed] [Google Scholar]
  23. Gilmore A. P., Wood C., Ohanian V., Jackson P., Patel B., Rees D. J., Hynes R. O., Critchley D. R. The cytoskeletal protein talin contains at least two distinct vinculin binding domains. J Cell Biol. 1993 Jul;122(2):337–347. doi: 10.1083/jcb.122.2.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Glenney J. R., Jr, Zokas L. Novel tyrosine kinase substrates from Rous sarcoma virus-transformed cells are present in the membrane skeleton. J Cell Biol. 1989 Jun;108(6):2401–2408. doi: 10.1083/jcb.108.6.2401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Goldmann W. H., Bremer A., Häner M., Aebi U., Isenberg G. Native talin is a dumbbell-shaped homodimer when it interacts with actin. J Struct Biol. 1994 Jan-Feb;112(1):3–10. doi: 10.1006/jsbi.1994.1002. [DOI] [PubMed] [Google Scholar]
  26. Goldmann W. H., Isenberg G. Kinetic determination of talin-actin binding. Biochem Biophys Res Commun. 1991 Jul 31;178(2):718–723. doi: 10.1016/0006-291x(91)90167-6. [DOI] [PubMed] [Google Scholar]
  27. Goldmann W. H., Käs J., Isenberg G. Talin decreases the bending elasticity of actin filaments. Biochem Soc Trans. 1994 Feb;22(1):46S–46S. doi: 10.1042/bst022046s. [DOI] [PubMed] [Google Scholar]
  28. Goldmann W. H., Niggli V., Kaufmann S., Isenberg G. Probing actin and liposome interaction of talin and talin-vinculin complexes: a kinetic, thermodynamic and lipid labeling study. Biochemistry. 1992 Aug 25;31(33):7665–7671. doi: 10.1021/bi00148a030. [DOI] [PubMed] [Google Scholar]
  29. Götter R., Goldmann W. H., Isenberg G. Internal actin filament dynamics in the presence of vinculin: a dynamic light scattering study. FEBS Lett. 1995 Feb 13;359(2-3):220–222. doi: 10.1016/0014-5793(95)00045-b. [DOI] [PubMed] [Google Scholar]
  30. Hazelrig J. B., Jones M. K., Segrest J. P. A mathematically defined motif for the radial distribution of charged residues on apolipoprotein amphipathic alpha helixes. Biophys J. 1993 Jun;64(6):1827–1832. doi: 10.1016/S0006-3495(93)81553-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Heise H., Bayerl T., Isenberg G., Sackmann E. Human platelet P-235, a talin-like actin binding protein, binds selectively to mixed lipid bilayers. Biochim Biophys Acta. 1991 Jan 30;1061(2):121–131. doi: 10.1016/0005-2736(91)90276-e. [DOI] [PubMed] [Google Scholar]
  32. Horwitz A., Duggan K., Buck C., Beckerle M. C., Burridge K. Interaction of plasma membrane fibronectin receptor with talin--a transmembrane linkage. Nature. 1986 Apr 10;320(6062):531–533. doi: 10.1038/320531a0. [DOI] [PubMed] [Google Scholar]
  33. Hunziker W., Spiess M., Semenza G., Lodish H. F. The sucrase-isomaltase complex: primary structure, membrane-orientation, and evolution of a stalked, intrinsic brush border protein. Cell. 1986 Jul 18;46(2):227–234. doi: 10.1016/0092-8674(86)90739-7. [DOI] [PubMed] [Google Scholar]
  34. Isenberg G. Actin binding proteins--lipid interactions. J Muscle Res Cell Motil. 1991 Apr;12(2):136–144. doi: 10.1007/BF01774032. [DOI] [PubMed] [Google Scholar]
  35. Isenberg G., Goldmann W. H. Actin-membrane coupling: a role for talin. J Muscle Res Cell Motil. 1992 Dec;13(6):587–589. doi: 10.1007/BF01738248. [DOI] [PubMed] [Google Scholar]
  36. Ito S., Werth D. K., Richert N. D., Pastan I. Vinculin phosphorylation by the src kinase. Interaction of vinculin with phospholipid vesicles. J Biol Chem. 1983 Dec 10;258(23):14626–14631. [PubMed] [Google Scholar]
  37. Jacobs R. E., White S. H. The nature of the hydrophobic binding of small peptides at the bilayer interface: implications for the insertion of transbilayer helices. Biochemistry. 1989 Apr 18;28(8):3421–3437. doi: 10.1021/bi00434a042. [DOI] [PubMed] [Google Scholar]
  38. Jennings M. L. Topography of membrane proteins. Annu Rev Biochem. 1989;58:999–1027. doi: 10.1146/annurev.bi.58.070189.005031. [DOI] [PubMed] [Google Scholar]
  39. Jockusch B. M., Isenberg G. Interaction of alpha-actinin and vinculin with actin: opposite effects on filament network formation. Proc Natl Acad Sci U S A. 1981 May;78(5):3005–3009. doi: 10.1073/pnas.78.5.3005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Johnson R. P., Craig S. W. An intramolecular association between the head and tail domains of vinculin modulates talin binding. J Biol Chem. 1994 Apr 29;269(17):12611–12619. [PubMed] [Google Scholar]
  41. Johnson R. P., Craig S. W. F-actin binding site masked by the intramolecular association of vinculin head and tail domains. Nature. 1995 Jan 19;373(6511):261–264. doi: 10.1038/373261a0. [DOI] [PubMed] [Google Scholar]
  42. Jones P., Jackson P., Price G. J., Patel B., Ohanion V., Lear A. L., Critchley D. R. Identification of a talin binding site in the cytoskeletal protein vinculin. J Cell Biol. 1989 Dec;109(6 Pt 1):2917–2927. doi: 10.1083/jcb.109.6.2917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kaufmann S., Käs J., Goldmann W. H., Sackmann E., Isenberg G. Talin anchors and nucleates actin filaments at lipid membranes. A direct demonstration. FEBS Lett. 1992 Dec 14;314(2):203–205. doi: 10.1016/0014-5793(92)80975-m. [DOI] [PubMed] [Google Scholar]
  44. Kaufmann S., Piekenbrock T., Goldmann W. H., Bärmann M., Isenberg G. Talin binds to actin and promotes filament nucleation. FEBS Lett. 1991 Jun 24;284(2):187–191. doi: 10.1016/0014-5793(91)80681-r. [DOI] [PubMed] [Google Scholar]
  45. Kreitmeier M., Gerisch G., Heizer C., Müller-Taubenberger A. A talin homologue of Dictyostelium rapidly assembles at the leading edge of cells in response to chemoattractant. J Cell Biol. 1995 Apr;129(1):179–188. doi: 10.1083/jcb.129.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Kroemker M., Rüdiger A. H., Jockusch B. M., Rüdiger M. Intramolecular interactions in vinculin control alpha-actinin binding to the vinculin head. FEBS Lett. 1994 Dec 5;355(3):259–262. doi: 10.1016/0014-5793(94)01216-4. [DOI] [PubMed] [Google Scholar]
  47. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  48. Levin J. M., Garnier J. Improvements in a secondary structure prediction method based on a search for local sequence homologies and its use as a model building tool. Biochim Biophys Acta. 1988 Aug 10;955(3):283–295. doi: 10.1016/0167-4838(88)90206-3. [DOI] [PubMed] [Google Scholar]
  49. Li S. C., Deber C. M. A measure of helical propensity for amino acids in membrane environments. Nat Struct Biol. 1994 Jun;1(6):368–373. doi: 10.1038/nsb0694-368. [DOI] [PubMed] [Google Scholar]
  50. Lupas A., Van Dyke M., Stock J. Predicting coiled coils from protein sequences. Science. 1991 May 24;252(5009):1162–1164. doi: 10.1126/science.252.5009.1162. [DOI] [PubMed] [Google Scholar]
  51. Maher P. A., Pasquale E. B., Wang J. Y., Singer S. J. Phosphotyrosine-containing proteins are concentrated in focal adhesions and intercellular junctions in normal cells. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6576–6580. doi: 10.1073/pnas.82.19.6576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Matsuzaki F., Matsumoto S., Yahara I., Yonezawa N., Nishida E., Sakai H. Cloning and characterization of porcine brain cofilin cDNA. Cofilin contains the nuclear transport signal sequence. J Biol Chem. 1988 Aug 15;263(23):11564–11568. [PubMed] [Google Scholar]
  53. McLachlan A. D., Stewart M., Hynes R. O., Rees D. J. Analysis of repeated motifs in the talin rod. J Mol Biol. 1994 Jan 28;235(4):1278–1290. doi: 10.1006/jmbi.1994.1081. [DOI] [PubMed] [Google Scholar]
  54. Menkel A. R., Kroemker M., Bubeck P., Ronsiek M., Nikolai G., Jockusch B. M. Characterization of an F-actin-binding domain in the cytoskeletal protein vinculin. J Cell Biol. 1994 Sep;126(5):1231–1240. doi: 10.1083/jcb.126.5.1231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Merlie J. P., Fagan D., Mudd J., Needleman P. Isolation and characterization of the complementary DNA for sheep seminal vesicle prostaglandin endoperoxide synthase (cyclooxygenase). J Biol Chem. 1988 Mar 15;263(8):3550–3553. [PubMed] [Google Scholar]
  56. Meyer R. K. Vinculin-lipid monolayer interactions: a model for focal contact formation. Eur J Cell Biol. 1989 Dec;50(2):491–499. [PubMed] [Google Scholar]
  57. Milam L. M. Electron microscopy of rotary shadowed vinculin and vinculin complexes. J Mol Biol. 1985 Aug 5;184(3):543–545. doi: 10.1016/0022-2836(85)90301-8. [DOI] [PubMed] [Google Scholar]
  58. Molony L., McCaslin D., Abernethy J., Paschal B., Burridge K. Properties of talin from chicken gizzard smooth muscle. J Biol Chem. 1987 Jun 5;262(16):7790–7795. [PubMed] [Google Scholar]
  59. Mrázek J., Kypr J. Computer program Jamsek combining statistical and stereochemical rules for the prediction of protein secondary structure. Comput Appl Biosci. 1988 Apr;4(2):297–302. doi: 10.1093/bioinformatics/4.2.297. [DOI] [PubMed] [Google Scholar]
  60. Niggli V., Dimitrov D. P., Brunner J., Burger M. M. Interaction of the cytoskeletal component vinculin with bilayer structures analyzed with a photoactivatable phospholipid. J Biol Chem. 1986 May 25;261(15):6912–6918. [PubMed] [Google Scholar]
  61. Niggli V., Kaufmann S., Goldmann W. H., Weber T., Isenberg G. Identification of functional domains in the cytoskeletal protein talin. Eur J Biochem. 1994 Sep 15;224(3):951–957. doi: 10.1111/j.1432-1033.1994.00951.x. [DOI] [PubMed] [Google Scholar]
  62. Niggli V., Sommer L., Brunner J., Burger M. M. Interaction in situ of the cytoskeletal protein vinculin with bilayers studied by introducing a photoactivatable fatty acid into living chicken embryo fibroblasts. Eur J Biochem. 1990 Jan 12;187(1):111–117. doi: 10.1111/j.1432-1033.1990.tb15283.x. [DOI] [PubMed] [Google Scholar]
  63. Otto J. J. Vinculin. Cell Motil Cytoskeleton. 1990;16(1):1–6. doi: 10.1002/cm.970160102. [DOI] [PubMed] [Google Scholar]
  64. Pavalko F. M., Otey C. A., Simon K. O., Burridge K. Alpha-actinin: a direct link between actin and integrins. Biochem Soc Trans. 1991 Nov;19(4):1065–1069. doi: 10.1042/bst0191065. [DOI] [PubMed] [Google Scholar]
  65. Picot D., Garavito R. M. Prostaglandin H synthase: implications for membrane structure. FEBS Lett. 1994 Jun 6;346(1):21–25. doi: 10.1016/0014-5793(94)00314-9. [DOI] [PubMed] [Google Scholar]
  66. Price G. J., Jones P., Davison M. D., Patel B., Bendori R., Geiger B., Critchley D. R. Primary sequence and domain structure of chicken vinculin. Biochem J. 1989 Apr 15;259(2):453–461. doi: 10.1042/bj2590453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Price G. J., Jones P., Davison M. D., Patel B., Eperon I. C., Critchley D. R. Isolation and characterization of a vinculin cDNA from chick-embryo fibroblasts. Biochem J. 1987 Jul 15;245(2):595–603. doi: 10.1042/bj2450595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Ptitsyn O. B., Finkelstein A. V. Theory of protein secondary structure and algorithm of its prediction. Biopolymers. 1983 Jan;22(1):15–25. doi: 10.1002/bip.360220105. [DOI] [PubMed] [Google Scholar]
  69. Rees D. J., Ades S. E., Singer S. J., Hynes R. O. Sequence and domain structure of talin. Nature. 1990 Oct 18;347(6294):685–689. doi: 10.1038/347685a0. [DOI] [PubMed] [Google Scholar]
  70. Ruddies R., Goldmann W. H., Isenberg G., Sackmann E. The viscoelasticity of entangled actin networks: the influence of defects and modulation by talin and vinculin. Eur Biophys J. 1993;22(5):309–321. doi: 10.1007/BF00213554. [DOI] [PubMed] [Google Scholar]
  71. Samuels M., Ezzell R. M., Cardozo T. J., Critchley D. R., Coll J. L., Adamson E. D. Expression of chicken vinculin complements the adhesion-defective phenotype of a mutant mouse F9 embryonal carcinoma cell. J Cell Biol. 1993 May;121(4):909–921. doi: 10.1083/jcb.121.4.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Sefton B. M., Hunter T., Ball E. H., Singer S. J. Vinculin: a cytoskeletal target of the transforming protein of Rous sarcoma virus. Cell. 1981 Apr;24(1):165–174. doi: 10.1016/0092-8674(81)90512-2. [DOI] [PubMed] [Google Scholar]
  73. Segrest J. P., De Loof H., Dohlman J. G., Brouillette C. G., Anantharamaiah G. M. Amphipathic helix motif: classes and properties. Proteins. 1990;8(2):103–117. doi: 10.1002/prot.340080202. [DOI] [PubMed] [Google Scholar]
  74. Segrest J. P., Jones M. K., De Loof H., Brouillette C. G., Venkatachalapathi Y. V., Anantharamaiah G. M. The amphipathic helix in the exchangeable apolipoproteins: a review of secondary structure and function. J Lipid Res. 1992 Feb;33(2):141–166. [PubMed] [Google Scholar]
  75. Turner C. E., Glenney J. R., Jr, Burridge K. Paxillin: a new vinculin-binding protein present in focal adhesions. J Cell Biol. 1990 Sep;111(3):1059–1068. doi: 10.1083/jcb.111.3.1059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Wachsstock D. H., Wilkins J. A., Lin S. Specific interaction of vinculin with alpha-actinin. Biochem Biophys Res Commun. 1987 Jul 31;146(2):554–560. doi: 10.1016/0006-291x(87)90564-x. [DOI] [PubMed] [Google Scholar]
  77. Weller P. A., Ogryzko E. P., Corben E. B., Zhidkova N. I., Patel B., Price G. J., Spurr N. K., Koteliansky V. E., Critchley D. R. Complete sequence of human vinculin and assignment of the gene to chromosome 10. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5667–5671. doi: 10.1073/pnas.87.15.5667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Wood C. K., Turner C. E., Jackson P., Critchley D. R. Characterisation of the paxillin-binding site and the C-terminal focal adhesion targeting sequence in vinculin. J Cell Sci. 1994 Feb;107(Pt 2):709–717. [PubMed] [Google Scholar]
  79. Yamamoto Y., Hake C. A., Martin B. M., Kretz K. A., Ahern-Rindell A. J., Naylor S. L., Mudd M., O'Brien J. S. Isolation, characterization, and mapping of a human acid beta-galactosidase cDNA. DNA Cell Biol. 1990 Mar;9(2):119–127. doi: 10.1089/dna.1990.9.119. [DOI] [PubMed] [Google Scholar]
  80. Yonezawa N., Homma Y., Yahara I., Sakai H., Nishida E. A short sequence responsible for both phosphoinositide binding and actin binding activities of cofilin. J Biol Chem. 1991 Sep 15;266(26):17218–17221. [PubMed] [Google Scholar]
  81. de Kruijff B. Anionic phospholipids and protein translocation. FEBS Lett. 1994 Jun 6;346(1):78–82. doi: 10.1016/0014-5793(94)00404-8. [DOI] [PubMed] [Google Scholar]

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