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Peptide motifs

Building the clathrin machinery

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Abstract

Clathrin-coated vesicles (CCVs) form at the plasma membrane, where they select cargo for endocytic entry into cells, and at the trans-Golgi network (TGN) and the endosomal system, where they generate carrier vesicles that transport proteins between these compartments. We have used subcellular fractionation and tandem mass spectrometry to identify proteins associated with brain CCVs. The resulting proteome contained a near complete inventory of the major functional proteins of synaptic vesicles (SVs), suggesting that clathrin-mediated endocytosis provides a major mechanism to recycle SV membrane proteins following neurotransmitter release. Additionally, we identified several new components of the machineries for clathrin-mediated membrane budding, including enthoprotin/epsinR and NECAP 1/2. These proteins bind with high specificity to the ear domains of the clathrin adaptor proteins (APs)-1 and-2, and, intriguingly, they each utilize novel peptide motifs based around the core sequence ØXXØ. Detailed mutational analysis of these motifs, coupled with structural studies of the ear domains, has revealed the basis of their specificity for clathrin adaptors. Moreover, the motifs have now been recognized in multiple proteins functioning in clathrin-mediated membrane trafficking, revealing new mechanisms in the formation and function of CCVs. Thus, proteomics analysis of isolated organelles can provide insights ranging from peptide motifs to global organelle function.

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References

  1. Conner S. D. and Schmid S. L. (2003). Regulated portals of entry into the cell. Nature 422, 37–44.

    Article  PubMed  CAS  Google Scholar 

  2. Ceresa B. P. and Schmid S. L. (2000). Regulation of signal transduction by endocytosis. Curr. Opin. Cell Biol. 12, 204–210.

    Article  PubMed  CAS  Google Scholar 

  3. McPherson P. S., Kay B. K., and Hussain N. K. (2001). Signaling on the endocytic pathway. Traffic 2, 375–384.

    Article  PubMed  CAS  Google Scholar 

  4. Rust M. J., Lakadamyali M., Zhang F., and Zhuang X. (2004). Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat. Struct. Mol. Biol. 11, 567–573.

    Article  PubMed  CAS  Google Scholar 

  5. Sandvig K. and van Deurs B. (1996). Endocytosis, intracellular transport, and cytotoxic action of Shiga toxin and ricin. Physiol. Rev. 76, 949–966.

    PubMed  CAS  Google Scholar 

  6. Hinners I. and Tooze S. A. (2003). Changing directions: clathrin-mediated transport between the Golgi and endosomes. J. Cell Sci. 116, 763–771.

    Article  PubMed  CAS  Google Scholar 

  7. Robinson M. S. (2004). Adaptable adaptors for coated vesicles. Trends Cell Biol. 14, 167–174.

    Article  PubMed  CAS  Google Scholar 

  8. Griffiths G., Hoflack B., Simons K., Mellman I., and Kornfeld S. (1988). The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 52, 329–341.

    Article  PubMed  CAS  Google Scholar 

  9. Ludwig T., Le Borgne R., and Hoflack B. (1995). Roles for mannose-6-phosphate receptors in lysosomal enzyme sorting, IGF-II binding and clathrin-coat assembly. Trends Cell Biol. 5, 202–206.

    Article  PubMed  CAS  Google Scholar 

  10. Meyer C., Zizioli D., Lausmann S., et al. (2000). mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J. 19, 2193–2203.

    Article  PubMed  CAS  Google Scholar 

  11. Pagano A., Crottet P., Presciunotto-Baschong C., and Spiess M. (2004). In vitro formation of recycling vesicles from endosomes requires adaptor protein-1/clathrin and is regulated by rab4 and the connector rabaptin-5 Mol. Biol. Cell 15, 4990–5000.

    Article  PubMed  CAS  Google Scholar 

  12. Ungewickell A., Ward M. E., Ungewickell E., and Majerus P. W. (2004). The inositol polyphosphate 5-phosphatase Ocr associates with endosomes that are partially coated with clathrin. Proc. Natl. Acad. Sci. USA 101, 13,501–13,506.

    Article  CAS  Google Scholar 

  13. Man H. Y., Ju W., Ahmadian G., and Wang Y. T. (2000). Intracellular trafficking of AMPA receptors in synaptic plasticity. Cell Mol. Life Sci. 57, 1526–1534.

    Article  PubMed  CAS  Google Scholar 

  14. Carroll R. C., Beattie E. C., von Zastrow M., and Malenka R. C. (2001). Role of AMPA receptor endocytosis in synaptic plasticity. Nat. Rev. Neurosci. 2, 315–324.

    Article  PubMed  CAS  Google Scholar 

  15. Kittler J. T., Delmas P., Jovanovic J. N., Brown D. A., Smart T. G., and Moss S. J. (2000). Constitutive endocytosis of GABAA receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J. Neurosci. 20, 7972–7977.

    PubMed  CAS  Google Scholar 

  16. Heuser J. E. and Reese T. S. (1973). Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315–344.

    Article  PubMed  CAS  Google Scholar 

  17. Takei K., Mundigl O., Daniell L., and De Camilli P. (1996). The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J. Cell Biol. 133, 1237–1250.

    Article  PubMed  CAS  Google Scholar 

  18. Palfrey H. C. and Artalejo C. R. (1998). Vesicle recycling revisited: rapid endocytosis may be the first step. Neuroscience 83, 969–989.

    Article  PubMed  CAS  Google Scholar 

  19. Wasiak S., Legendre-Guillemin V., Puertollano R., et al. (2002). Enthoprotin: a novel clathrin-associated protein identified through subcellular proteomics. J. Cell Biol. 158, 855–862.

    Article  PubMed  CAS  Google Scholar 

  20. Blondeau F., Ritter B., Allaire P. D., et al. (2004). Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc. Natl. Acad. Sci. USA 101, 3833–3838.

    Article  PubMed  CAS  Google Scholar 

  21. Huber L. A. (2003). Is proteomics heading in the wrong direction? Nat. Rev. Mol. Cell Biol. 4, 74–80.

    Article  PubMed  CAS  Google Scholar 

  22. Taylor S. W., Fahy E., and Ghosh S. S. (2003). Global organellar proteomics. Trends Biotech. 21, 82–88.

    Article  CAS  Google Scholar 

  23. Brunet S., Thibault P., Gagnon E., Kearney P., Bergeron J. J., and Desjardins M. (2003). Organelle proteomics: looking at less to see more. Trends Cell Biol. 13, 629–638.

    Article  PubMed  CAS  Google Scholar 

  24. Girard, M., Allaire, P. D., Blondeau, F., and McPherson, P. S. (2005) In: Current Protocols in Cell Biology, Subcellular Fractionation and Isolation of Organelles, Unit 3.13, Bonifacino J., Lippincott-Schwartz J., Dasso M., Harford J., and Yamada K., eds., Hoboken, NJ: John Wiley and Sons, Inc., pp. 1–30.

    Google Scholar 

  25. Brodsky F. M., Chen C. Y., Knuehl C., Towler M. C., and Wakeham D. E. (2001). Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17, 517–568.

    Article  PubMed  CAS  Google Scholar 

  26. Liu H., Sadygov R. G., and Yates J. R., 3rd. (2004). A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193–4201.

    Article  PubMed  CAS  Google Scholar 

  27. Gygi S. P., Rist B., Gerber S. A., Turecek F., Gelb M. H., and Aebersold R. (1999). Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17, 994–999.

    Article  PubMed  CAS  Google Scholar 

  28. Oda Y., Huang K., Cross F. R., Cowburn D., and Chait B. T. (1999). Accurate quantitation of protein expression and site-specific phosphorylation. Proc. Natl. Acad. Sci. USA 96, 6591–6596.

    Article  PubMed  CAS  Google Scholar 

  29. Girard M., Allaire P. D., McPherson P. S., and Blondeau F. (2005). Non-stoichiometric relationship between clathrin heavy and light chains revealed by quantitative comparative proteomics of clathrin-coated vesicles from brain and liver. Mol. Cell. Proteomics, epub ahead of print.

  30. Aravanis A. M., Pyle J. L., and Tsien R. W. (2003). Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423, 643–647.

    Article  PubMed  CAS  Google Scholar 

  31. Gandhi S. P. and Stevens C. F. (2003). Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423, 607–613.

    Article  PubMed  CAS  Google Scholar 

  32. Kirchhausen T. (1999). Adaptors for clathrin-mediated traffic. Annu. Rev. Cell Dev. Biol. 15, 705–732.

    Article  PubMed  CAS  Google Scholar 

  33. Collins B. M., McCoy A. J., Kent H. M., Evans P. R., and Owen D. J. (2002). Molecular architecture and functional model of the endocytic AP2 complex. Cell 109, 523–535.

    Article  PubMed  CAS  Google Scholar 

  34. Ritter B. and McPherson P. S. Molecular mechanisms in clathrin-mediated membrane budding. In: Topics in Current Genetics. Regulatory Mechanisms of Intracellular Membrane Transport. Sirkka Keräne and Jussi Jantti, eds., 2004, Springer-Verlag Berlin Heidelberg, pp. 9–37.

    Google Scholar 

  35. Gaidarov I. and Keen J. H. (1999). Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits. J. Cell Biol. 146, 755–764.

    Article  PubMed  CAS  Google Scholar 

  36. Krauss M., Kinuta M., Wenk M. R., De Camilli P., Takei K., and Haucke V. (2003). ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Igamma. J. Cell Biol. 162, 113–124.

    Article  PubMed  CAS  Google Scholar 

  37. Wang Y. J., Wang J., Sun H. Q., et al. (2003). Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114, 299–310.

    Article  PubMed  CAS  Google Scholar 

  38. Owen D. J., Vallis Y., Pearse B. M., McMahon H. T., and Evans P. R. (2000). The structure and function of the beta 2-adaptin appendage domain. EMBO J. 19, 4216–4227.

    Article  PubMed  CAS  Google Scholar 

  39. Traub L. M. (2003). Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J. Cell Biol. 163, 203–208.

    Article  PubMed  CAS  Google Scholar 

  40. Sorkin A. (2004). Cargo recognition during clathrin-mediated endocytosis: a team effort. Curr. Opin. Cell Biol. 16, 392–399.

    Article  PubMed  CAS  Google Scholar 

  41. Robinson M. S. and Bonifacino J. S. (2001). Adaptor-related proteins. Curr. Opin. Cell Biol. 13, 444–453.

    Article  PubMed  CAS  Google Scholar 

  42. McPherson P. S. (1999). Regulatory role of SH3 domain-mediated protein-protein interactions in synaptic vesicle endocytosis. Cell Signal. 11, 229–238.

    Article  PubMed  CAS  Google Scholar 

  43. Santolini E., Salcini A. E., Kay B. K., Yamabhai M., and Di Fiore P. P. (1999). The EH network. Exp. Cell Res. 253, 186–209.

    Article  PubMed  CAS  Google Scholar 

  44. Slepnev V. I. and De Camilli P. (2000). Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat. Rev. Neurosci. 1, 161–172.

    Article  PubMed  CAS  Google Scholar 

  45. Qualmann B., Kessels M. M., and Kelly R. B. (2000). Molecular links between endocytosis and the actin cytoskeleton. J. Cell Biol. 150, F111-F116.

    Article  PubMed  CAS  Google Scholar 

  46. McPherson P. S. (2002). The endocytic machinery at an interface with the actin cytoskeleton: a dynamic, hip intersection. Trends Cell Biol. 12, 312–315.

    Article  PubMed  CAS  Google Scholar 

  47. Engqvist-Goldstein A. E. and Drubin D. G. (2003). Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 19, 287–332.

    Article  PubMed  CAS  Google Scholar 

  48. Legendre-Guillemin V., Wasiak S., Hussain N. K., Angers A., and McPherson P. S. (2004). ENTH/ANTH proteins and clathrin-mediated membrane budding. J. Cell Sci. 117, 9–18.

    Article  PubMed  CAS  Google Scholar 

  49. McMahon H. T. and Mills I. G. (2004). COP and clathrin-coated vesicle budding: different pathways, common approaches. Curr. Opin. Cell Biol. 16, 379–391.

    Article  PubMed  CAS  Google Scholar 

  50. Praefcke G. J. and McMahon H. T. (2004). The dynamic superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5, 133–147.

    Article  PubMed  CAS  Google Scholar 

  51. Wenk M. R. and De Camilli P. (2004). Proteinlipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc. Natl. Acad. Sci. USA 101 8262–8269.

    Article  PubMed  CAS  Google Scholar 

  52. Mayer B. J. (2001). SH3 domains: complexity in moderation. J. Cell Sci. 114, 1253–1263.

    PubMed  CAS  Google Scholar 

  53. Schlessinger J. and Lemmon M. A. (2003). SH2 and PTB domains in tyrosine kinase signaling. Sci. STKE. 191, RE12.

    Google Scholar 

  54. Zhang B. and Zelhof A. C. (2002). Amphiphysins: raising the BAR for synaptic vesicle recycling and membrane dynamics. Traffic 3, 452–460.

    Article  PubMed  CAS  Google Scholar 

  55. Peter B. J., Kent H. M., Mills I. G., et al. (2004). BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495–499.

    Article  PubMed  CAS  Google Scholar 

  56. Ramjaun A. R. and McPherson P. S. (1998). Multiple amphiphysin II splice variants display differential clathrin binding: identification of two distinct clathrin-binding sites. J. Neurochem. 70, 2369–2376.

    Article  PubMed  CAS  Google Scholar 

  57. ter Haar E., Harrison S. C., and Kirchhausen T. (2000). Peptide-in-groove interactions link target proteins to the beta-propeller of clathrin. Proc. Natl. Acad. Sci. USA 97, 1096–1100.

    Article  PubMed  Google Scholar 

  58. Miele A. E., Watson P. J., Evans P. R., Traub L. M., and Owen D. J. (2004). Two distinct interaction motifs in amphiphysin bind two independent sites on the clathrin terminal domain beta-propeller. Nat. Struct. Mol. Biol. 11, 242–248.

    Article  PubMed  CAS  Google Scholar 

  59. Owen D. J., Vallis Y., Noble M. E., et al. (1999). A structural explanation for the binding of multiple ligands by the alpha-adaptin appendage domain. Cell 97, 805–815.

    Article  PubMed  CAS  Google Scholar 

  60. Traub L. M., Downs M. A., Westrich J. L., and Fremont D. H. (1999). Crystal structure of the alpha appendage of AP-2 reveals a recruitment platform for clathrin-coat assembly. Proc. Natl. Acad. Sci. USA 96, 8907–8912.

    Article  PubMed  CAS  Google Scholar 

  61. Brett T. J., Traub L. M., and Fremont D. H. (2002). Accessory protein recruitment motifs in clathrin-mediated endocytosis. Structure (Camb) 10, 797–809.

    Article  CAS  Google Scholar 

  62. Metzler M., Legendre-Guillemin V., Gan L., et al. (2001). HIP1 functions in clathrin-mediated endocytosis through binding to clathrin and adaptor protein 2. J. Biol. Chem. 276, 39,271–39,276.

    Article  CAS  Google Scholar 

  63. Mishra S. K., Agostinelli N. R., Brett T. J., Mizukami I., Ross T. S., and Traub L. M. (2001). Clathrin- and AP-2-binding sites in HIP1 uncover a general assembly role for endocytic accessory proteins. J. Biol. Chem. 276, 46,230–46,236.

    CAS  Google Scholar 

  64. Kent H. M., McMahon H. T., Evans P. R., Benmerah A., and Owen D. J. (2002). Gammadaptin appendage domain: structure and binding site for Eps15 and gamma-synergin. Structure (Camb) 10, 1139–1148.

    Article  CAS  Google Scholar 

  65. Nogi T., Shiba Y., Kawasaki M., et al. (2002). Structural basis for the accessory protein recruitment by the gamma-adaptin ear domain. Nat. Struct. Biol. 9, 527–531.

    PubMed  CAS  Google Scholar 

  66. Kalthoff C., Groos S., Kohl R., Mahrhold S., and Ungewickell E. J. (2002). Clint: a novel clathrin-binding ENTH-domain protein at the Golgi. Mol. Biol. Cell 13, 4060–4073.

    Article  PubMed  CAS  Google Scholar 

  67. Hirst J., Motley A., Harasaki K., Peak Chew S. Y., and Robinson M. S. (2003). EpsinR: an ENTH domain-containing protein that interacts with AP-1. Mol. Biol. Cell 14, 625–641.

    Article  PubMed  CAS  Google Scholar 

  68. Mills I. G., Praefcke G. J., Vallis Y., et al. (2003). EpsinR: an AP1/clathrin interacting protein involved in vesicle trafficking. J. Cell Biol. 160, 213–222.

    Article  PubMed  CAS  Google Scholar 

  69. Ford M. G., Pearse B. M., Higgins M. K., et al. (2001). Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291, 1051–1055.

    Article  PubMed  CAS  Google Scholar 

  70. Itoh T., Koshiba S., Kigawa T., Kikuchi A., Yokoyama S., and Takenawa T. (2001). Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis. Science 291, 1047–1051.

    Article  PubMed  CAS  Google Scholar 

  71. Ford M. G., Mills I. G., Peter B. J., et al. (2002). Curvature of clathrin-coated pits driven by epsin. Nature 419, 361–366.

    Article  PubMed  CAS  Google Scholar 

  72. Stahelin R. V., Long F., Peter B. J., et al. (2003). Contrasting membrane interaction mechanisms of AP180 ANTH and Epsin ENTH domains. J. Biol. Chem. 278, 28,993–28,999.

    CAS  Google Scholar 

  73. Saint-Pol A., Yelamos B., Amessou M., et al. (2004). Clathrin adaptor epsinR is required for retrograde sorting on early endosomal membranes. Dev. Cell 6, 525–538.

    Article  PubMed  CAS  Google Scholar 

  74. Chidambaram S., Mullers N., Wiederhold K., Haucke V., and von Mollard G. F. (2004). Specific interaction between SNAREs and epsin N-terminal homology (ENTH) domains of epsin-related proteins in trans-Golgi network to endosome transport. J. Biol. Chem. 279, 4175–4179.

    Article  PubMed  CAS  Google Scholar 

  75. Duncan M. C., Costaguta G., and Payne G. S. (2003). Yeast epsin-related proteins required for Golgi-endosome traffic define a gamma-adaptin ear-binding motif. Nat. Cell Biol. 5, 77–81.

    Article  PubMed  CAS  Google Scholar 

  76. Duncan M. C. and Payne G. S. (2003). ENTH/ANTH domains expand to the Golgi. Trends Cell Biol. 13, 211–215.

    Article  PubMed  CAS  Google Scholar 

  77. Wasiak S., Denisov A. Y., Han Z., et al. (2003). Characterization of a gamma-adaptin ear-binding motif in enthoprotin. FEBS Lett. 555, 437–442.

    Article  PubMed  CAS  Google Scholar 

  78. Lui W. W., Collins B. M., Hirst J., et al. (2003). Binding partners for the COOH-terminal appendage domains of the GGAs and gamma-adaptin. Mol. Biol. Cell 14, 2385–2398.

    Article  PubMed  CAS  Google Scholar 

  79. Mattera R., Arighi C. N., Lodge R., Zerial M., and Bonifacino J. S. (2003). Divalent interaction of the GGAs with the Rabaptin-5-Rabex-5 complex. EMBO J. 22, 78–88.

    Article  PubMed  CAS  Google Scholar 

  80. Mattera R., Ritter B., Sidhu S. S., McPherson P. S., and Bonifacino J. S. (2004). Definition of the consensus motif recognized by gamma-adaptin ear domains. J. Biol. Chem. 279, 8018–8028.

    Article  PubMed  CAS  Google Scholar 

  81. Burman J. L., Wasiak S., Ritter B., de Heuvel E., and McPherson P. S. (2005). Aftiphilin is a component of the clathrin machinery in neurons. FEBS Lett. 579, 2177–2184.

    Article  PubMed  CAS  Google Scholar 

  82. Hirst J., Borner G. H., Harbour M., and Robinson M. S. (2005) The aftiphilin /p200/ gamma-synergin complex. Mol. Biol. Cell 16, 2554–2565.

    Article  PubMed  CAS  Google Scholar 

  83. Miller G. J., Mattera R., Bonifacino J. S., and Hurley J. H. (2003). Recognition of accessory protein motifs by the gamma-adaptin ear domain of GGA3. Nat. Struct. Biol. 10, 599–606.

    Article  PubMed  CAS  Google Scholar 

  84. Collins B. M., Praefcke G. J., Robinson M. S., and Owen D. J. (2003). Structural basis for binding of accessory proteins by the appendage domain of GGAs. Nat. Struct. Biol. 10, 607–613.

    Article  PubMed  CAS  Google Scholar 

  85. Ritter B., Philie J., Girard M., Tung E. C., Blondeau F., and McPherson P. S. (2003). Identification of a family of endocytic proteins that define a new alpha-adaptin ear-binding motif. EMBO Rep. 4, 1089–1095.

    Article  PubMed  CAS  Google Scholar 

  86. Ritter, B., Denisov A. Y., Philie J., et al. (2004). Two WXXF-based motifs in NECAPs define the specificity of accessory protein binding to AP-1 and AP-2. EMBO J. 23, 3701–3710.

    Article  PubMed  CAS  Google Scholar 

  87. Mishra S. K., Hawryluk M. J., Brett T. J., et al. (2004). Dual-engagement regulation of protein interactions with the AP-2 adaptor alpha appendage. J. Biol. Chem. 279, 46,191–46,203.

    CAS  Google Scholar 

  88. Walther K., Diril M. K., Jung N., and Haucke V. (2004). Functional dissection of the interactions of stonin 2 with the adaptor complex AP-2 and synaptotagmin. Proc. Natl. Acad. Sci. USA 101, 964–969.

    Article  PubMed  CAS  Google Scholar 

  89. Jha A., Agostinelli N. R., Mishra S. K., Keyel P. A., Hawryluk M. J., and Traub L. M. (2004). A novel AP-2 adaptor interaction motif initially identified in the long-splice isoform of synaptojanin 1, SJ170. J. Biol. Chem. 279, 2281–2290.

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, H3A 2B4, Montreal, QC, Canada

    Peter S. McPherson & Brigitte Ritter

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Correspondence to Peter S. McPherson.

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McPherson, P.S., Ritter, B. Peptide motifs. Mol Neurobiol 32, 73–87 (2005). https://doi.org/10.1385/MN:32:1:073

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