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Published online on March 25, 2005, 10.1073/pnas.0500941102
PNAS | April 5, 2005 | vol. 102 | no. 14 | 5210-5214


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NEUROSCIENCE
Three distinct kinetic groupings of the synaptotagmin family: Candidate sensors for rapid and delayed exocytosis

Enfu Hui *, Jihong Bai *, Ping Wang *, Mutsuyuki Sugimori {dagger}, Rodolfo R. Llinas {dagger}, and Edwin R. Chapman *, {ddagger}

*Department of Physiology, University of Wisconsin, Madison, WI 53706; and {dagger}Department of Physiology and Neuroscience, New York University Medical Center, New York, NY 10016

Contributed by Rodolfo R. Llinas, February 16, 2005

Synaptotagmins (syts) are a family of membrane proteins present on a variety of intracellular organelles. In vertebrates, 16 isoforms of syt have been identified. The most abundant isoform, syt I, appears to function as a Ca2+ sensor that triggers the rapid exocytosis of synaptic vesicles from neurons. The functions of the remaining syt isoforms are less well understood. The cytoplasmic domain of syt I binds membranes in response to Ca2+, and this interaction has been proposed to play a key role in secretion. Here, we tested the Ca2+-triggered membrane-binding activity of the cytoplasmic domains of syts I–XII; eight isoforms tightly bound to liposomes that contained phosphatidylserine as a function of the concentration of Ca2+. We then compared the disassembly kinetics of Ca2+·syt·membrane complexes upon rapid mixing with excess Ca2+ chelator and found that syts can be classified into three distinct kinetic groups. syts I, II, and III constitute the fast group; syts V, VI, IX, and X make up the medium group; and syt VII exhibits the slowest kinetics of disassembly. Thus, isoforms of syt, which have much slower disassembly kinetics than does syt I, might function as Ca2+ sensors for asynchronous release, which occurs after Ca2+ domains have collapsed. We also compared the temperature dependence of Ca2+·syt·membrane assembly and disassembly reactions by using squid and rat syt I. These results indicate that syts have diverged to release Ca2+ and membranes with distinct kinetics.

Ca2+ sensor | kinetics | liposome | disassembly | isoform

Author contributions: E.H., J.B., M.S., R.R.L., and E.R.C. designed research; E.H., J.B., P.W., M.S., R.R.L., and E.R.C. performed research; J.B., M.S., R.R.L., and E.R.C. analyzed data; and E.H. and E.R.C. wrote the paper.

Abbreviations: syt, synaptotagmin; PS, phosphatidylserine; PC, phosphatidylcholine; dansyl-PE, 1,2-dioleoyl-sn-glycero-3-phosphoethanolamine-N-(5-dimethylamino-1-naphthalenesulfonyl).

{ddagger} To whom correspondence should be addressed at: Department of Physiology, SMI 129, University of Wisconsin, 1300 University Avenue, Madison, WI 53706. E-mail: chapman{at}physiology.wisc.edu.

© 2005 by The National Academy of Sciences of the USA


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