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. 1996 Nov 1;135(3):661–672. doi: 10.1083/jcb.135.3.661

A new model for the interaction of dystrophin with F-actin

PMCID: PMC2121071  PMID: 8909541

Abstract

The F-actin binding and cross-linking properties of skeletal muscle dystrophin-glycoprotein complex were examined using high and low speed cosedimentation assays, microcapillary falling ball viscometry, and electron microscopy. Dystrophin-glycoprotein complex binding to F-actin saturated near 0.042 +/- 0.005 mol/ mol, which corresponds to one dystrophin per 24 actin monomers. Dystrophin-glycoprotein complex bound to F-actin with an average apparent Kd for dystrophin of 0.5 microM. These results demonstrate that native, full-length dystrophin in the glycoprotein complex binds F-actin with some properties similar to those measured for several members of the actin cross-linking super- family of proteins. However, we failed to observe dystrophin- glycoprotein complex-induced cross-linking of F-actin by three different methods, each positively controlled with alpha-actinin. Furthermore, high speed cosedimentation analysis of dystrophin- glycoprotein complex digested with calpain revealed a novel F-actin binding site located near the middle of the dystrophin rod domain. Recombinant dystrophin fragments corresponding to the novel actin binding site and the first 246 amino acids of dystrophin both bound F- actin but with significantly lower affinity and higher capacity than was observed with purified dystrophin-glycoprotein complex. Finally, dystrophin-glycoprotein complex was observed to significantly slow the depolymerization of F-actin, Suggesting that dystrophin may lie along side an actin filament through interaction with multiple actin monomers. These data suggest that although dystrophin is most closely related to the actin cross-linking superfamily based on sequence homology, dystrophin binds F-actin in a manner more analogous to actin side-binding proteins.

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Selected References

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  1. Ahn A. H., Kunkel L. M. The structural and functional diversity of dystrophin. Nat Genet. 1993 Apr;3(4):283–291. doi: 10.1038/ng0493-283. [DOI] [PubMed] [Google Scholar]
  2. Bard F., Franzini-Armstrong C. Extra actin filaments at the periphery of skeletal muscle myofibrils. Tissue Cell. 1991;23(2):191–197. doi: 10.1016/0040-8166(91)90073-3. [DOI] [PubMed] [Google Scholar]
  3. Beggs A. H., Hoffman E. P., Snyder J. R., Arahata K., Specht L., Shapiro F., Angelini C., Sugita H., Kunkel L. M. Exploring the molecular basis for variability among patients with Becker muscular dystrophy: dystrophin gene and protein studies. Am J Hum Genet. 1991 Jul;49(1):54–67. [PMC free article] [PubMed] [Google Scholar]
  4. Bonet-Kerrache A., Fabbrizio E., Mornet D. N-terminal domain of dystrophin. FEBS Lett. 1994 Nov 21;355(1):49–53. doi: 10.1016/0014-5793(94)01162-1. [DOI] [PubMed] [Google Scholar]
  5. Brenman J. E., Chao D. S., Gee S. H., McGee A. W., Craven S. E., Santillano D. R., Wu Z., Huang F., Xia H., Peters M. F. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell. 1996 Mar 8;84(5):757–767. doi: 10.1016/s0092-8674(00)81053-3. [DOI] [PubMed] [Google Scholar]
  6. Brooks S. P. A simple computer program with statistical tests for the analysis of enzyme kinetics. Biotechniques. 1992 Dec;13(6):906–911. [PubMed] [Google Scholar]
  7. Broschat K. O. Tropomyosin prevents depolymerization of actin filaments from the pointed end. J Biol Chem. 1990 Dec 5;265(34):21323–21329. [PubMed] [Google Scholar]
  8. Cano M. L., Cassimeris L., Fechheimer M., Zigmond S. H. Mechanisms responsible for F-actin stabilization after lysis of polymorphonuclear leukocytes. J Cell Biol. 1992 Mar;116(5):1123–1134. doi: 10.1083/jcb.116.5.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Comi G. P., Prelle A., Bresolin N., Moggio M., Bardoni A., Gallanti A., Vita G., Toscano A., Ferro M. T., Bordoni A. Clinical variability in Becker muscular dystrophy. Genetic, biochemical and immunohistochemical correlates. Brain. 1994 Feb;117(Pt 1):1–14. doi: 10.1093/brain/117.1.1-a. [DOI] [PubMed] [Google Scholar]
  10. Cooper J. A., Walker S. B., Pollard T. D. Pyrene actin: documentation of the validity of a sensitive assay for actin polymerization. J Muscle Res Cell Motil. 1983 Apr;4(2):253–262. doi: 10.1007/BF00712034. [DOI] [PubMed] [Google Scholar]
  11. Corrado K., Mills P. L., Chamberlain J. S. Deletion analysis of the dystrophin-actin binding domain. FEBS Lett. 1994 May 16;344(2-3):255–260. doi: 10.1016/0014-5793(94)00397-1. [DOI] [PubMed] [Google Scholar]
  12. Corrado K., Rafael J. A., Mills P. L., Cole N. M., Faulkner J. A., Wang K., Chamberlain J. S. Transgenic mdx mice expressing dystrophin with a deletion in the actin-binding domain display a "mild Becker" phenotype. J Cell Biol. 1996 Aug;134(4):873–884. doi: 10.1083/jcb.134.4.873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cox G. A., Sunada Y., Campbell K. P., Chamberlain J. S. Dp71 can restore the dystrophin-associated glycoprotein complex in muscle but fails to prevent dystrophy. Nat Genet. 1994 Dec;8(4):333–339. doi: 10.1038/ng1294-333. [DOI] [PubMed] [Google Scholar]
  14. Cullen M. J., Walsh J., Nicholson L. V., Harris J. B. Ultrastructural localization of dystrophin in human muscle by using gold immunolabelling. Proc R Soc Lond B Biol Sci. 1990 May 22;240(1297):197–210. doi: 10.1098/rspb.1990.0034. [DOI] [PubMed] [Google Scholar]
  15. D'Souza V. N., Nguyen T. M., Morris G. E., Karges W., Pillers D. A., Ray P. N. A novel dystrophin isoform is required for normal retinal electrophysiology. Hum Mol Genet. 1995 May;4(5):837–842. doi: 10.1093/hmg/4.5.837. [DOI] [PubMed] [Google Scholar]
  16. England S. B., Nicholson L. V., Johnson M. A., Forrest S. M., Love D. R., Zubrzycka-Gaarn E. E., Bulman D. E., Harris J. B., Davies K. E. Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature. 1990 Jan 11;343(6254):180–182. doi: 10.1038/343180a0. [DOI] [PubMed] [Google Scholar]
  17. Ervasti J. M., Campbell K. P. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol. 1993 Aug;122(4):809–823. doi: 10.1083/jcb.122.4.809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ervasti J. M., Campbell K. P. Dystrophin and the membrane skeleton. Curr Opin Cell Biol. 1993 Feb;5(1):82–87. doi: 10.1016/s0955-0674(05)80012-2. [DOI] [PubMed] [Google Scholar]
  19. Ervasti J. M., Campbell K. P. Membrane organization of the dystrophin-glycoprotein complex. Cell. 1991 Sep 20;66(6):1121–1131. doi: 10.1016/0092-8674(91)90035-w. [DOI] [PubMed] [Google Scholar]
  20. Ervasti J. M., Kahl S. D., Campbell K. P. Purification of dystrophin from skeletal muscle. J Biol Chem. 1991 May 15;266(14):9161–9165. [PubMed] [Google Scholar]
  21. Ervasti J. M., Ohlendieck K., Kahl S. D., Gaver M. G., Campbell K. P. Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature. 1990 May 24;345(6273):315–319. doi: 10.1038/345315a0. [DOI] [PubMed] [Google Scholar]
  22. Fabbrizio E., Bonet-Kerrache A., Leger J. J., Mornet D. Actin-dystrophin interface. Biochemistry. 1993 Oct 5;32(39):10457–10463. doi: 10.1021/bi00090a023. [DOI] [PubMed] [Google Scholar]
  23. Fukami K., Furuhashi K., Inagaki M., Endo T., Hatano S., Takenawa T. Requirement of phosphatidylinositol 4,5-bisphosphate for alpha-actinin function. Nature. 1992 Sep 10;359(6391):150–152. doi: 10.1038/359150a0. [DOI] [PubMed] [Google Scholar]
  24. Fukami K., Sawada N., Endo T., Takenawa T. Identification of a phosphatidylinositol 4,5-bisphosphate-binding site in chicken skeletal muscle alpha-actinin. J Biol Chem. 1996 Feb 2;271(5):2646–2650. doi: 10.1074/jbc.271.5.2646. [DOI] [PubMed] [Google Scholar]
  25. Goldberg M. E., Djavadi-Ohaniance L. Methods for measurement of antibody/antigen affinity based on ELISA and RIA. Curr Opin Immunol. 1993 Apr;5(2):278–281. doi: 10.1016/0952-7915(93)90018-n. [DOI] [PubMed] [Google Scholar]
  26. Greenberg D. S., Sunada Y., Campbell K. P., Yaffe D., Nudel U. Exogenous Dp71 restores the levels of dystrophin associated proteins but does not alleviate muscle damage in mdx mice. Nat Genet. 1994 Dec;8(4):340–344. doi: 10.1038/ng1294-340. [DOI] [PubMed] [Google Scholar]
  27. Helliwell T. R., Ellis J. M., Mountford R. C., Appleton R. E., Morris G. E. A truncated dystrophin lacking the C-terminal domains is localized at the muscle membrane. Am J Hum Genet. 1992 Mar;50(3):508–514. [PMC free article] [PubMed] [Google Scholar]
  28. Hemmings L., Kuhlman P. A., Critchley D. R. Analysis of the actin-binding domain of alpha-actinin by mutagenesis and demonstration that dystrophin contains a functionally homologous domain. J Cell Biol. 1992 Mar;116(6):1369–1380. doi: 10.1083/jcb.116.6.1369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hoffman E. P., Garcia C. A., Chamberlain J. S., Angelini C., Lupski J. R., Fenwick R. Is the carboxyl-terminus of dystrophin required for membrane association? A novel, severe case of Duchenne muscular dystrophy. Ann Neurol. 1991 Oct;30(4):605–610. doi: 10.1002/ana.410300414. [DOI] [PubMed] [Google Scholar]
  30. Hori S., Ohtani S., Nguyen T. M., Morris G. E. The N-terminal half of dystrophin is protected from proteolysis in situ. Biochem Biophys Res Commun. 1995 Apr 26;209(3):1062–1067. doi: 10.1006/bbrc.1995.1605. [DOI] [PubMed] [Google Scholar]
  31. Ibraghimov-Beskrovnaya O., Ervasti J. M., Leveille C. J., Slaughter C. A., Sernett S. W., Campbell K. P. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature. 1992 Feb 20;355(6362):696–702. doi: 10.1038/355696a0. [DOI] [PubMed] [Google Scholar]
  32. Jarrett H. W., Foster J. L. Alternate binding of actin and calmodulin to multiple sites on dystrophin. J Biol Chem. 1995 Mar 10;270(10):5578–5586. doi: 10.1074/jbc.270.10.5578. [DOI] [PubMed] [Google Scholar]
  33. Kahana E., Marsh P. J., Henry A. J., Way M., Gratzer W. B. conformation and phasing of dystrophin structural repeats. J Mol Biol. 1994 Jan 28;235(4):1271–1277. doi: 10.1006/jmbi.1994.1080. [DOI] [PubMed] [Google Scholar]
  34. Koenig M., Kunkel L. M. Detailed analysis of the repeat domain of dystrophin reveals four potential hinge segments that may confer flexibility. J Biol Chem. 1990 Mar 15;265(8):4560–4566. [PubMed] [Google Scholar]
  35. Koenig M., Monaco A. P., Kunkel L. M. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell. 1988 Apr 22;53(2):219–228. doi: 10.1016/0092-8674(88)90383-2. [DOI] [PubMed] [Google Scholar]
  36. Kramarcy N. R., Vidal A., Froehner S. C., Sealock R. Association of utrophin and multiple dystrophin short forms with the mammalian M(r) 58,000 dystrophin-associated protein (syntrophin). J Biol Chem. 1994 Jan 28;269(4):2870–2876. [PubMed] [Google Scholar]
  37. Lebart M. C., Casanova D., Benyamin Y. Actin interaction with purified dystrophin from electric organ of Torpedo marmorata: possible resemblance with filamin-actin interface. J Muscle Res Cell Motil. 1995 Oct;16(5):543–552. doi: 10.1007/BF00126438. [DOI] [PubMed] [Google Scholar]
  38. Li X., Bennett V. Identification of the spectrin subunit and domains required for formation of spectrin/adducin/actin complexes. J Biol Chem. 1996 Jun 28;271(26):15695–15702. doi: 10.1074/jbc.271.26.15695. [DOI] [PubMed] [Google Scholar]
  39. Lo S. H., Janmey P. A., Hartwig J. H., Chen L. B. Interactions of tensin with actin and identification of its three distinct actin-binding domains. J Cell Biol. 1994 Jun;125(5):1067–1075. doi: 10.1083/jcb.125.5.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. MacLean-Fletcher S. D., Pollard T. D. Viscometric analysis of the gelation of Acanthamoeba extracts and purification of two gelation factors. J Cell Biol. 1980 May;85(2):414–428. doi: 10.1083/jcb.85.2.414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. MacLean-Fletcher S., Pollard T. D. Identification of a factor in conventional muscle actin preparations which inhibits actin filament self-association. Biochem Biophys Res Commun. 1980 Sep 16;96(1):18–27. doi: 10.1016/0006-291x(80)91175-4. [DOI] [PubMed] [Google Scholar]
  42. Matsudaira P. Modular organization of actin crosslinking proteins. Trends Biochem Sci. 1991 Mar;16(3):87–92. doi: 10.1016/0968-0004(91)90039-x. [DOI] [PubMed] [Google Scholar]
  43. Matsumura K., Tomé F. M., Ionasescu V., Ervasti J. M., Anderson R. D., Romero N. B., Simon D., Récan D., Kaplan J. C., Fardeau M. Deficiency of dystrophin-associated proteins in Duchenne muscular dystrophy patients lacking COOH-terminal domains of dystrophin. J Clin Invest. 1993 Aug;92(2):866–871. doi: 10.1172/JCI116661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Menke A., Jockusch H. Decreased osmotic stability of dystrophin-less muscle cells from the mdx mouse. Nature. 1991 Jan 3;349(6304):69–71. doi: 10.1038/349069a0. [DOI] [PubMed] [Google Scholar]
  45. Meyer R. K., Aebi U. Bundling of actin filaments by alpha-actinin depends on its molecular length. J Cell Biol. 1990 Jun;110(6):2013–2024. doi: 10.1083/jcb.110.6.2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Méjean C., Lebart M. C., Roustan C., Benyamin Y. Inhibition of actin-dystrophin interaction by inositide phosphate. Biochem Biophys Res Commun. 1995 May 5;210(1):152–158. doi: 10.1006/bbrc.1995.1640. [DOI] [PubMed] [Google Scholar]
  47. Nicholson L. V., Davison K., Falkous G., Harwood C., O'Donnell E., Slater C. R., Harris J. B. Dystrophin in skeletal muscle. I. Western blot analysis using a monoclonal antibody. J Neurol Sci. 1989 Dec;94(1-3):125–136. doi: 10.1016/0022-510x(89)90223-2. [DOI] [PubMed] [Google Scholar]
  48. Pall E. A., Bolton K. M., Ervasti J. M. Differential heparin inhibition of skeletal muscle alpha-dystroglycan binding to laminins. J Biol Chem. 1996 Feb 16;271(7):3817–3821. doi: 10.1074/jbc.271.7.3817. [DOI] [PubMed] [Google Scholar]
  49. Pardee J. D., Spudich J. A. Purification of muscle actin. Methods Enzymol. 1982;85(Pt B):164–181. doi: 10.1016/0076-6879(82)85020-9. [DOI] [PubMed] [Google Scholar]
  50. Petrof B. J., Shrager J. B., Stedman H. H., Kelly A. M., Sweeney H. L. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3710–3714. doi: 10.1073/pnas.90.8.3710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Pollard T. D., Cooper J. A. Methods to characterize actin filament networks. Methods Enzymol. 1982;85(Pt B):211–233. doi: 10.1016/0076-6879(82)85022-2. [DOI] [PubMed] [Google Scholar]
  52. Pons F., Augier N., Heilig R., Léger J., Mornet D., Léger J. J. Isolated dystrophin molecules as seen by electron microscopy. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7851–7855. doi: 10.1073/pnas.87.20.7851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Porter G. A., Dmytrenko G. M., Winkelmann J. C., Bloch R. J. Dystrophin colocalizes with beta-spectrin in distinct subsarcolemmal domains in mammalian skeletal muscle. J Cell Biol. 1992 Jun;117(5):997–1005. doi: 10.1083/jcb.117.5.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Prior T. W., Papp A. C., Snyder P. J., Burghes A. H., Bartolo C., Sedra M. S., Western L. M., Mendell J. R. A missense mutation in the dystrophin gene in a Duchenne muscular dystrophy patient. Nat Genet. 1993 Aug;4(4):357–360. doi: 10.1038/ng0893-357. [DOI] [PubMed] [Google Scholar]
  55. Schafer D. A., Cooper J. A. Control of actin assembly at filament ends. Annu Rev Cell Dev Biol. 1995;11:497–518. doi: 10.1146/annurev.cb.11.110195.002433. [DOI] [PubMed] [Google Scholar]
  56. Sealock R., Froehner S. C. Dystrophin-associated proteins and synapse formation: is alpha-dystroglycan the agrin receptor? Cell. 1994 Jun 3;77(5):617–619. doi: 10.1016/0092-8674(94)90045-0. [DOI] [PubMed] [Google Scholar]
  57. Senter L., Luise M., Presotto C., Betto R., Teresi A., Ceoldo S., Salviati G. Interaction of dystrophin with cytoskeletal proteins: binding to talin and actin. Biochem Biophys Res Commun. 1993 Apr 30;192(2):899–904. doi: 10.1006/bbrc.1993.1500. [DOI] [PubMed] [Google Scholar]
  58. Stedman H. H., Sweeney H. L., Shrager J. B., Maguire H. C., Panettieri R. A., Petrof B., Narusawa M., Leferovich J. M., Sladky J. T., Kelly A. M. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature. 1991 Aug 8;352(6335):536–539. doi: 10.1038/352536a0. [DOI] [PubMed] [Google Scholar]
  59. Sunada Y., Bernier S. M., Kozak C. A., Yamada Y., Campbell K. P. Deficiency of merosin in dystrophic dy mice and genetic linkage of laminin M chain gene to dy locus. J Biol Chem. 1994 May 13;269(19):13729–13732. [PubMed] [Google Scholar]
  60. Suzuki A., Yoshida M., Hayashi K., Mizuno Y., Hagiwara Y., Ozawa E. Molecular organization at the glycoprotein-complex-binding site of dystrophin. Three dystrophin-associated proteins bind directly to the carboxy-terminal portion of dystrophin. Eur J Biochem. 1994 Mar 1;220(2):283–292. doi: 10.1111/j.1432-1033.1994.tb18624.x. [DOI] [PubMed] [Google Scholar]
  61. Suzuki A., Yoshida M., Yamamoto H., Ozawa E. Glycoprotein-binding site of dystrophin is confined to the cysteine-rich domain and the first half of the carboxy-terminal domain. FEBS Lett. 1992 Aug 17;308(2):154–160. doi: 10.1016/0014-5793(92)81265-n. [DOI] [PubMed] [Google Scholar]
  62. Tidball J. G., Law D. J. Dystrophin is required for normal thin filament-membrane associations at myotendinous junctions. Am J Pathol. 1991 Jan;138(1):17–21. [PMC free article] [PubMed] [Google Scholar]
  63. Tinsley J. M., Blake D. J., Roche A., Fairbrother U., Riss J., Byth B. C., Knight A. E., Kendrick-Jones J., Suthers G. K., Love D. R. Primary structure of dystrophin-related protein. Nature. 1992 Dec 10;360(6404):591–593. doi: 10.1038/360591a0. [DOI] [PubMed] [Google Scholar]
  64. Van Etten R. A., Jackson P. K., Baltimore D., Sanders M. C., Matsudaira P. T., Janmey P. A. The COOH terminus of the c-Abl tyrosine kinase contains distinct F- and G-actin binding domains with bundling activity. J Cell Biol. 1994 Feb;124(3):325–340. doi: 10.1083/jcb.124.3.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Way M., Pope B., Cross R. A., Kendrick-Jones J., Weeds A. G. Expression of the N-terminal domain of dystrophin in E. coli and demonstration of binding to F-actin. FEBS Lett. 1992 Apr 27;301(3):243–245. doi: 10.1016/0014-5793(92)80249-g. [DOI] [PubMed] [Google Scholar]
  66. Winder S. J., Gibson T. J., Kendrick-Jones J. Dystrophin and utrophin: the missing links! FEBS Lett. 1995 Aug 1;369(1):27–33. doi: 10.1016/0014-5793(95)00398-s. [DOI] [PubMed] [Google Scholar]
  67. Winder S. J., Kendrick-Jones J. Calcium/calmodulin-dependent regulation of the NH2-terminal F-actin binding domain of utrophin. FEBS Lett. 1995 Jan 3;357(2):125–128. doi: 10.1016/0014-5793(94)01347-4. [DOI] [PubMed] [Google Scholar]
  68. Winnard A. V., Klein C. J., Coovert D. D., Prior T., Papp A., Snyder P., Bulman D. E., Ray P. N., McAndrew P., King W. Characterization of translational frame exception patients in Duchenne/Becker muscular dystrophy. Hum Mol Genet. 1993 Jun;2(6):737–744. doi: 10.1093/hmg/2.6.737. [DOI] [PubMed] [Google Scholar]
  69. Worton R. Muscular dystrophies: diseases of the dystrophin-glycoprotein complex. Science. 1995 Nov 3;270(5237):755–756. doi: 10.1126/science.270.5237.755. [DOI] [PubMed] [Google Scholar]
  70. Yang B., Jung D., Motto D., Meyer J., Koretzky G., Campbell K. P. SH3 domain-mediated interaction of dystroglycan and Grb2. J Biol Chem. 1995 May 19;270(20):11711–11714. doi: 10.1074/jbc.270.20.11711. [DOI] [PubMed] [Google Scholar]
  71. Yoshida M., Ozawa E. Glycoprotein complex anchoring dystrophin to sarcolemma. J Biochem. 1990 Nov;108(5):748–752. doi: 10.1093/oxfordjournals.jbchem.a123276. [DOI] [PubMed] [Google Scholar]
  72. Yoshida M., Suzuki A., Yamamoto H., Noguchi S., Mizuno Y., Ozawa E. Dissociation of the complex of dystrophin and its associated proteins into several unique groups by n-octyl beta-D-glucoside. Eur J Biochem. 1994 Jun 15;222(3):1055–1061. doi: 10.1111/j.1432-1033.1994.tb18958.x. [DOI] [PubMed] [Google Scholar]

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