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Volumn 13, Issue 3, 2006, Pages 209-217

Close membrane-membrane proximity induced by Ca2+-dependent multivalent binding of synaptotagmin-1 to phospholipids

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PHOSPHOLIPID; PROTEIN KINASE C; SNARE PROTEIN; SYNAPTOTAGMIN; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

EID: 33644804207     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1056     Document Type: Article
Times cited : (216)

References (49)
  • 1
    • 2942556680 scopus 로고    scopus 로고
    • The synaptic vesicle cycle
    • Sudhof, T.C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547 (2004).
    • (2004) Annu. Rev. Neurosci. , vol.27 , pp. 509-547
    • Sudhof, T.C.1
  • 2
    • 0036304982 scopus 로고    scopus 로고
    • Synaptotagmin: A Ca(2+) sensor that triggers exocytosis?
    • Chapman, E.R. Synaptotagmin: a Ca(2+) sensor that triggers exocytosis? Nat. Rev. Mol. Cell Biol. 3, 498-508 (2002).
    • (2002) Nat. Rev. Mol. Cell Biol. , vol.3 , pp. 498-508
    • Chapman, E.R.1
  • 3
    • 0028986240 scopus 로고
    • Structure of the first C2 domain of synaptotagmin I: A novel Ca2+/phospholipid-binding fold
    • Sutton, R.B., Davletov, B.A., Berghuis, A.M., Sudhof, T.C. & Sprang, S.R. Structure of the first C2 domain of synaptotagmin I: a novel Ca2+/phospholipid-binding fold. Cell 80, 929-938 (1995).
    • (1995) Cell , vol.80 , pp. 929-938
    • Sutton, R.B.1    Davletov, B.A.2    Berghuis, A.M.3    Sudhof, T.C.4    Sprang, S.R.5
  • 4
    • 0032541943 scopus 로고    scopus 로고
    • Solution structures of the Ca2+-free and Ca2+-bound C2A domain of synaptotagmin I: Does Ca2+ induce a conformational change?
    • Shao, X., Fernandez, I., Sudhof, T.C. & Rizo, J. Solution structures of the Ca2+-free and Ca2+-bound C2A domain of synaptotagmin I: does Ca2+ induce a conformational change? Biochemistry 37, 16106-16115 (1998).
    • (1998) Biochemistry , vol.37 , pp. 16106-16115
    • Shao, X.1    Fernandez, I.2    Sudhof, T.C.3    Rizo, J.4
  • 5
    • 0035924571 scopus 로고    scopus 로고
    • Three-dimensional structure of the synaptotagmin 1 c(2)b-domain. Synaptotagmin 1 as a phospholipid binding machine
    • Fernandez, I. et al. Three-dimensional structure of the synaptotagmin 1 c(2)b-domain. Synaptotagmin 1 as a phospholipid binding machine. Neuron 32, 1057-1069 (2001).
    • (2001) Neuron , vol.32 , pp. 1057-1069
    • Fernandez, I.1
  • 6
    • 0029666292 scopus 로고    scopus 로고
    • Bipartite Ca2+-binding motif in C2 domains of synaptotagmin and protein kinase C
    • Shao, X., Davletov, B.A., Sutton, R.B., Sudhof, T.C. & Rizo, J. Bipartite Ca2+-binding motif in C2 domains of synaptotagmin and protein kinase C. Science 273, 248-251 (1996).
    • (1996) Science , vol.273 , pp. 248-251
    • Shao, X.1    Davletov, B.A.2    Sutton, R.B.3    Sudhof, T.C.4    Rizo, J.5
  • 7
    • 0032527312 scopus 로고    scopus 로고
    • Ca2+ binding to synaptotagmin: How many Ca2+ ions bind to the tip of a C2-domain?
    • Ubach, J., Zhang, X., Shao, X., Sudhof, T.C. & Rizo, J. Ca2+ binding to synaptotagmin: how many Ca2+ ions bind to the tip of a C2-domain? EMBO J. 17, 3921-3930 (1998).
    • (1998) EMBO J. , vol.17 , pp. 3921-3930
    • Ubach, J.1    Zhang, X.2    Shao, X.3    Sudhof, T.C.4    Rizo, J.5
  • 8
    • 0027332736 scopus 로고
    • A single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding
    • Davletov, B.A. & Sudhof, T.C. A single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding. J. Biol. Chem. 268, 26386-26390 (1993).
    • (1993) J. Biol. Chem. , vol.268 , pp. 26386-26390
    • Davletov, B.A.1    Sudhof, T.C.2
  • 9
    • 0032577067 scopus 로고    scopus 로고
    • Direct interaction of a Ca2+-binding loop of synaptotagmin with lipid bilayers
    • Chapman, E.R. & Davis, A.F. Direct interaction of a Ca2+-binding loop of synaptotagmin with lipid bilayers. J. Biol. Chem. 273, 13995-14001 (1998).
    • (1998) J. Biol. Chem. , vol.273 , pp. 13995-14001
    • Chapman, E.R.1    Davis, A.F.2
  • 10
    • 0032497406 scopus 로고    scopus 로고
    • Mechanism of phospholipid binding by the C2A-domain of synaptotagmin I
    • Zhang, X., Rizo, J. & Sudhof, T.C. Mechanism of phospholipid binding by the C2A-domain of synaptotagmin I. Biochemistry 37, 12395-12403 (1998).
    • (1998) Biochemistry , vol.37 , pp. 12395-12403
    • Zhang, X.1    Rizo, J.2    Sudhof, T.C.3
  • 11
    • 0035282457 scopus 로고    scopus 로고
    • Synaptotagmin I functions as a calcium regulator of release probability
    • Fernandez-Chacon, R. et al. Synaptotagmin I functions as a calcium regulator of release probability. Nature 410, 41-49 (2001).
    • (2001) Nature , vol.410 , pp. 41-49
    • Fernandez-Chacon, R.1
  • 12
    • 29444436513 scopus 로고    scopus 로고
    • 2+-affinity of synaptotagmin 1
    • 2+-affinity of synaptotagmin 1. Proc. Natl. Acad. Sci. USA 102, 18664-18669 (2005).
    • (2005) Proc. Natl. Acad. Sci. USA , vol.102 , pp. 18664-18669
    • Rhee, J.S.1
  • 13
    • 0036307988 scopus 로고    scopus 로고
    • Synaptotagmin function in dense core vesicle exocytosis studied in cracked PC12 cells
    • Shin, O.H., Rizo, J. & Sudhof, T.C. Synaptotagmin function in dense core vesicle exocytosis studied in cracked PC12 cells. Nat. Neurosci. 5, 649-656 (2002).
    • (2002) Nat. Neurosci. , vol.5 , pp. 649-656
    • Shin, O.H.1    Rizo, J.2    Sudhof, T.C.3
  • 14
    • 0037452955 scopus 로고    scopus 로고
    • Facile detection of protein-protein interactions by one-dimensional NMR spectroscopy
    • Arac, D., Murphy, T. & Rizo, J. Facile detection of protein-protein interactions by one-dimensional NMR spectroscopy. Biochemistry 42, 2774-2780 (2003).
    • (2003) Biochemistry , vol.42 , pp. 2774-2780
    • Arac, D.1    Murphy, T.2    Rizo, J.3
  • 15
    • 0037427025 scopus 로고    scopus 로고
    • Sr2+ binding to the Ca2+ binding site of the synaptotagmin 1 C2B domain triggers fast exocytosis without stimulating SNARE interactions
    • Shin, O.H. et al. Sr2+ binding to the Ca2+ binding site of the synaptotagmin 1 C2B domain triggers fast exocytosis without stimulating SNARE interactions. Neuron 37, 99-108 (2003).
    • (2003) Neuron , vol.37 , pp. 99-108
    • Shin, O.H.1
  • 16
    • 0030740252 scopus 로고    scopus 로고
    • Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy
    • Hanson, P.I., Roth, R., Morisaki, H., Jahn, R. & Heuser, J.E. Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell 90, 523-535 (1997).
    • (1997) Cell , vol.90 , pp. 523-535
    • Hanson, P.I.1    Roth, R.2    Morisaki, H.3    Jahn, R.4    Heuser, J.E.5
  • 17
    • 0030807735 scopus 로고    scopus 로고
    • Structural organization of the synaptic exocytosis core complex
    • Lin, R.C. & Scheller, R.H. Structural organization of the synaptic exocytosis core complex. Neuron 19, 1087-1094 (1997).
    • (1997) Neuron , vol.19 , pp. 1087-1094
    • Lin, R.C.1    Scheller, R.H.2
  • 18
    • 0031668972 scopus 로고    scopus 로고
    • The synaptic SNARE complex is a parallel four-stranded helical bundle
    • Poirier, M.A. et al. The synaptic SNARE complex is a parallel four-stranded helical bundle. Nat. Struct. Biol. 5, 765-769 (1998).
    • (1998) Nat. Struct. Biol. , vol.5 , pp. 765-769
    • Poirier, M.A.1
  • 19
    • 3543096759 scopus 로고    scopus 로고
    • Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution
    • Sutton, R.B., Fasshauer, D., Jahn, R. & Brunger, A.T. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395, 347-353 (1998).
    • (1998) Nature , vol.395 , pp. 347-353
    • Sutton, R.B.1    Fasshauer, D.2    Jahn, R.3    Brunger, A.T.4
  • 20
    • 0032549708 scopus 로고    scopus 로고
    • SNAREpins: Minimal machinery for membrane fusion
    • Weber, T. et al. SNAREpins: minimal machinery for membrane fusion. Cell 92, 759-772 (1998).
    • (1998) Cell , vol.92 , pp. 759-772
    • Weber, T.1
  • 21
    • 0037033997 scopus 로고    scopus 로고
    • Vesicular restriction of synaptobrevin suggests a role for calcium in membrane fusion
    • Hu, K. et al. Vesicular restriction of synaptobrevin suggests a role for calcium in membrane fusion. Nature 415, 646-650 (2002).
    • (2002) Nature , vol.415 , pp. 646-650
    • Hu, K.1
  • 22
    • 0038103601 scopus 로고    scopus 로고
    • Regulation of neuronal SNARE assembly by the membrane
    • Kweon, D.H., Kim, C.S. & Shin, Y.K. Regulation of neuronal SNARE assembly by the membrane. Nat. Struct. Biol. 10, 440-447 (2003).
    • (2003) Nat. Struct. Biol. , vol.10 , pp. 440-447
    • Kweon, D.H.1    Kim, C.S.2    Shin, Y.K.3
  • 23
    • 0037022308 scopus 로고    scopus 로고
    • The SNARE protein SNAP-25 is linked to fast calcium triggering of exocytosis
    • Sorensen, J.B. et al. The SNARE protein SNAP-25 is linked to fast calcium triggering of exocytosis. Proc. Natl. Acad. Sci. USA 99, 1627-1632 (2002).
    • (2002) Proc. Natl. Acad. Sci. USA , vol.99 , pp. 1627-1632
    • Sorensen, J.B.1
  • 24
    • 14144253310 scopus 로고    scopus 로고
    • Are neuronal SNARE proteins Ca2+ sensors?
    • Chen, X., Tang, J., Sudhof, T.C. & Rizo, J. Are neuronal SNARE proteins Ca2+ sensors? J. Mol. Biol. 347, 145-158 (2005).
    • (2005) J. Mol. Biol. , vol.347 , pp. 145-158
    • Chen, X.1    Tang, J.2    Sudhof, T.C.3    Rizo, J.4
  • 25
    • 1842477457 scopus 로고    scopus 로고
    • Synaptotagmin interaction with the syntaxin/SNAP-25 dimer is mediated by an evolutionarily conserved motif and is sensitive to inositol hexakisphosphate
    • Rickman, C. et al. Synaptotagmin interaction with the syntaxin/SNAP-25 dimer is mediated by an evolutionarily conserved motif and is sensitive to inositol hexakisphosphate. J. Biol. Chem. 279, 12574-12579 (2004).
    • (2004) J. Biol. Chem. , vol.279 , pp. 12574-12579
    • Rickman, C.1
  • 26
    • 0032484205 scopus 로고    scopus 로고
    • Delineation of the oligomerization, AP-2 binding, and synprint binding region of the C2B domain of synaptotagmin
    • Chapman, E.R., Desai, R.C., Davis, A.F. & Tornehl, C.K. Delineation of the oligomerization, AP-2 binding, and synprint binding region of the C2B domain of synaptotagmin. J. Biol. Chem. 273, 32966-32972 (1998).
    • (1998) J. Biol. Chem. , vol.273 , pp. 32966-32972
    • Chapman, E.R.1    Desai, R.C.2    Davis, A.F.3    Tornehl, C.K.4
  • 27
    • 0034705042 scopus 로고    scopus 로고
    • Calcium triggers an intramolecular association of the C2 domains in synaptotagmin
    • Garcia, R.A., Forde, C.E. & Godwin, H.A. Calcium triggers an intramolecular association of the C2 domains in synaptotagmin. Proc. Natl. Acad. Sci. USA 97, 5883-5888 (2000).
    • (2000) Proc. Natl. Acad. Sci. USA , vol.97 , pp. 5883-5888
    • Garcia, R.A.1    Forde, C.E.2    Godwin, H.A.3
  • 28
    • 0035918350 scopus 로고    scopus 로고
    • The C2B domain of synaptotagmin I is a Ca2+-binding module
    • Ubach, J. et al. The C2B domain of synaptotagmin I is a Ca2+-binding module. Biochemistry 40, 5854-5860 (2001).
    • (2001) Biochemistry , vol.40 , pp. 5854-5860
    • Ubach, J.1
  • 29
    • 0037130255 scopus 로고    scopus 로고
    • The C(2)B Ca(2+)-binding motif of synaptotagmin is required for synaptic transmission in vivo
    • Mackler, J.M., Drummond, J.A., Loewen, C.A., Robinson, I.M. & Reist, N.E. The C(2)B Ca(2+)-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 418, 340-344 (2002).
    • (2002) Nature , vol.418 , pp. 340-344
    • Mackler, J.M.1    Drummond, J.A.2    Loewen, C.A.3    Robinson, I.M.4    Reist, N.E.5
  • 30
    • 0037130260 scopus 로고    scopus 로고
    • Synaptotagmins I and IV promote transmitter release independently of Ca(2+) binding in the C(2)A domain
    • Robinson, I.M., Ranjan, R. & Schwarz, T.L. Synaptotagmins I and IV promote transmitter release independently of Ca(2+) binding in the C(2)A domain. Nature 418, 336-340 (2002).
    • (2002) Nature , vol.418 , pp. 336-340
    • Robinson, I.M.1    Ranjan, R.2    Schwarz, T.L.3
  • 31
    • 0036813665 scopus 로고    scopus 로고
    • Structure/function analysis of Ca2+ binding to the C2A domain of synaptotagmin 1
    • Fernandez-Chacon, R. et al. Structure/function analysis of Ca2+ binding to the C2A domain of synaptotagmin 1. J. Neurosci. 22, 8438-8446 (2002).
    • (2002) J. Neurosci. , vol.22 , pp. 8438-8446
    • Fernandez-Chacon, R.1
  • 32
    • 4744344106 scopus 로고    scopus 로고
    • Dual roles of the C2B domain of synaptotagmin I in synchronizing Ca2+-dependent neurotransmitter release
    • Nishiki, T. & Augustine, G.J. Dual roles of the C2B domain of synaptotagmin I in synchronizing Ca2+-dependent neurotransmitter release. J. Neurosci. 24, 8542-8550 (2004).
    • (2004) J. Neurosci. , vol.24 , pp. 8542-8550
    • Nishiki, T.1    Augustine, G.J.2
  • 33
    • 0037452791 scopus 로고    scopus 로고
    • Visualization of synaptotagmin I oligomers assembled onto lipid monolayers
    • Wu, Y. et al. Visualization of synaptotagmin I oligomers assembled onto lipid monolayers. Proc. Natl. Acad. Sci. USA 100, 2082-2087 (2003).
    • (2003) Proc. Natl. Acad. Sci. USA , vol.100 , pp. 2082-2087
    • Wu, Y.1
  • 34
    • 0037022307 scopus 로고    scopus 로고
    • C2A activates a cryptic Ca(2+)-triggered membrane penetration activity within the C2B domain of synaptotagmin I
    • Bai, J., Wang, P. & Chapman, E.R. C2A activates a cryptic Ca(2+)-triggered membrane penetration activity within the C2B domain of synaptotagmin I. Proc. Natl. Acad. Sci. USA 99, 1665-1670 (2002).
    • (2002) Proc. Natl. Acad. Sci. USA , vol.99 , pp. 1665-1670
    • Bai, J.1    Wang, P.2    Chapman, E.R.3
  • 35
    • 0036318064 scopus 로고    scopus 로고
    • Role of electrostatic and hydrophobic interactions in ca(2+)-dependent phospholipid binding by the c(2)a-domain from synaptotagmin I
    • Gerber, S.H., Rizo, J. & Sudhof, T.C. Role of electrostatic and hydrophobic interactions in ca(2+)-dependent phospholipid binding by the c(2)a-domain from synaptotagmin I. Diabetes 51 Suppl 1, S12-S18 (2002).
    • (2002) Diabetes , vol.51 , Issue.1 SUPPL.
    • Gerber, S.H.1    Rizo, J.2    Sudhof, T.C.3
  • 36
    • 11844254393 scopus 로고    scopus 로고
    • Membrane-bound orientation and position of the synaptotagmin C2B domain determined by site-directed spin labeling
    • Rufener, E., Frazier, A.A., Wieser, C.M., Hinderliter, A. & Cafiso, D.S. Membrane-bound orientation and position of the synaptotagmin C2B domain determined by site-directed spin labeling. Biochemistry 44, 18-28 (2005).
    • (2005) Biochemistry , vol.44 , pp. 18-28
    • Rufener, E.1    Frazier, A.A.2    Wieser, C.M.3    Hinderliter, A.4    Cafiso, D.S.5
  • 37
    • 0037435606 scopus 로고    scopus 로고
    • Membrane-bound orientation and position of the synaptotagmin I C2A domain by site-directed spin labeling
    • Frazier, A.A., Roller, C.R., Havelka, J.J., Hinderliter, A. & Cafiso, D.S. Membrane-bound orientation and position of the synaptotagmin I C2A domain by site-directed spin labeling. Biochemistry 42, 96-105 (2003).
    • (2003) Biochemistry , vol.42 , pp. 96-105
    • Frazier, A.A.1    Roller, C.R.2    Havelka, J.J.3    Hinderliter, A.4    Cafiso, D.S.5
  • 38
    • 0027162564 scopus 로고
    • The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation
    • Crowley, K.S., Reinhart, G.D. & Johnson, A.E. The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation. Cell 73, 1101-1115 (1993).
    • (1993) Cell , vol.73 , pp. 1101-1115
    • Crowley, K.S.1    Reinhart, G.D.2    Johnson, A.E.3
  • 39
    • 0028295796 scopus 로고
    • Resonance energy transfer: Methods and applications
    • Wu, P. & Brand, L. Resonance energy transfer: methods and applications. Anal. Biochem. 218, 1-13 (1994).
    • (1994) Anal. Biochem. , vol.218 , pp. 1-13
    • Wu, P.1    Brand, L.2
  • 40
    • 0842291506 scopus 로고    scopus 로고
    • PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane
    • Bai, J., Tucker, W.C. & Chapman, E.R. PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane. Nat. Struct. Mol. Biol. 11, 36-44 (2004).
    • (2004) Nat. Struct. Mol. Biol. , vol.11 , pp. 36-44
    • Bai, J.1    Tucker, W.C.2    Chapman, E.R.3
  • 42
    • 1942520207 scopus 로고    scopus 로고
    • Reconstitution of Ca2+-regulated membrane fusion by synaptotagmin and SNAREs
    • Tucker, W.C., Weber, T. & Chapman, E.R. Reconstitution of Ca2+-regulated membrane fusion by synaptotagmin and SNAREs. Science 304, 435-438 (2004).
    • (2004) Science , vol.304 , pp. 435-438
    • Tucker, W.C.1    Weber, T.2    Chapman, E.R.3
  • 43
    • 33646007069 scopus 로고    scopus 로고
    • SNARE mediated lipid mixing depends on the physical state of the vesicles
    • published online 16 December 2005 (doi:10.1529/biophysj.105.071415)
    • Chen, X. et al. SNARE mediated lipid mixing depends on the physical state of the vesicles Biophys. J. published online 16 December 2005 (doi:10.1529/biophysj.105.071415).
    • Biophys. J.
    • Chen, X.1
  • 44
    • 0023636677 scopus 로고
    • Biomembrane fusion: A new concept derived from model studies using two interacting planar lipid bilayers
    • Chernomordik, L.V., Melikyan, G.B. & Chizmadzhev, Y.A. Biomembrane fusion: a new concept derived from model studies using two interacting planar lipid bilayers. Biochim. Biophys. Acta 906, 309-352 (1987).
    • (1987) Biochim. Biophys. Acta , vol.906 , pp. 309-352
    • Chernomordik, L.V.1    Melikyan, G.B.2    Chizmadzhev, Y.A.3
  • 45
    • 0017859530 scopus 로고
    • Binding of polylysine to charged bilayer membranes: Molecular organization of a lipid.peptide complex
    • Hartmann, W. & Galla, H.J. Binding of polylysine to charged bilayer membranes: molecular organization of a lipid.peptide complex. Biochim. Biophys. Acta 509, 474-490 (1978).
    • (1978) Biochim. Biophys. Acta , vol.509 , pp. 474-490
    • Hartmann, W.1    Galla, H.J.2
  • 46
    • 20444370233 scopus 로고    scopus 로고
    • Synaptotagmin mutants Y311N and K326/327A alter the calcium dependence of neurotransmission
    • Borden, C.R., Stevens, C.F., Sullivan, J.M. & Zhu, Y. Synaptotagmin mutants Y311N and K326/327A alter the calcium dependence of neurotransmission. Mol. Cell. Neurosci. 29, 462-470 (2005).
    • (2005) Mol. Cell. Neurosci. , vol.29 , pp. 462-470
    • Borden, C.R.1    Stevens, C.F.2    Sullivan, J.M.3    Zhu, Y.4
  • 47
    • 0035940689 scopus 로고    scopus 로고
    • A 11.5 A single particle reconstruction of GroEL using EMAN
    • Ludtke, S.J., Jakana, J., Song, J.L., Chuang, D.T. & Chiu, W. A 11.5 A single particle reconstruction of GroEL using EMAN. J. Mol. Biol. 314, 253-262 (2001).
    • (2001) J. Mol. Biol. , vol.314 , pp. 253-262
    • Ludtke, S.J.1    Jakana, J.2    Song, J.L.3    Chuang, D.T.4    Chiu, W.5
  • 48
    • 0029879295 scopus 로고    scopus 로고
    • Computer visualization of three-dimensional image data using IMOD
    • Kremer, J.R., Mastronarde, D.N. & McIntosh, J.R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76 (1996).
    • (1996) J. Struct. Biol. , vol.116 , pp. 71-76
    • Kremer, J.R.1    Mastronarde, D.N.2    McIntosh, J.R.3
  • 49
    • 0026319199 scopus 로고
    • Protein folding and association - Insights from the interfacial and thermodynamic properties of hydrocarbons
    • Nicholls, A., Sharp, K.A. & Honig, B. Protein folding and association - insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct. Funct. Genet. 11, 281-296 (1991).
    • (1991) Proteins Struct. Funct. Genet. , vol.11 , pp. 281-296
    • Nicholls, A.1    Sharp, K.A.2    Honig, B.3


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