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Published in: Brain Structure and Function 8/2017

01-11-2017 | Review

The birth of the synapse

Author: Saak V. Ovsepian

Published in: Brain Structure and Function | Issue 8/2017

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Abstract

It has long been held that the rise of neurons as a specialized cell type also marked the onset of the grand evolutionary journey for chemical synapses. Research over recent decades has shown, however, that the most dynamic chapters of synaptic history have been ‘written’ out of the context of neurobiology and neuronal evolution, dating back to the early metazoa and unicellular living forms. Here, I consider and discuss emerging evidence suggesting the exaptive origin of chemical synapses, via tinkering and neo-functionalization of already existent junctional morphologies and constituents of primeval paracrine signalling. Through combination and collateral use of long-established structures and functions, a remarkable enrichment of regulatory and control mechanisms of complex living organisms was achieved, without large-scale reorganization of the genome, with tremendous impact on the evolution and life on our planet.
Literature
go back to reference Abascal F, Zardoya R (2013) Evolutionary analyses of gap junction protein families. Biochim Et Biophys Acta Biomembr 1828:4–14CrossRef Abascal F, Zardoya R (2013) Evolutionary analyses of gap junction protein families. Biochim Et Biophys Acta Biomembr 1828:4–14CrossRef
go back to reference Bennett MV (1972) Electrical versus chemical neurotransmission. Res Publ Assoc Res Nerv Mental Dis 50:58–90 Bennett MV (1972) Electrical versus chemical neurotransmission. Res Publ Assoc Res Nerv Mental Dis 50:58–90
go back to reference Bennett MV (2000) Electrical synapses, a personal perspective (or history). Brain Res Brain Res Rev 32(1):16–28CrossRefPubMed Bennett MV (2000) Electrical synapses, a personal perspective (or history). Brain Res Brain Res Rev 32(1):16–28CrossRefPubMed
go back to reference Bennett MV, Zukin RS (2004) Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron 41:495–511CrossRefPubMed Bennett MV, Zukin RS (2004) Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron 41:495–511CrossRefPubMed
go back to reference Bittman K, Owens DF, Kriegstein AR, LoTurco JJ (1997) Cell coupling and uncoupling in the ventricular zone of developing neocortex. J Neurosci 17:7037–7044PubMed Bittman K, Owens DF, Kriegstein AR, LoTurco JJ (1997) Cell coupling and uncoupling in the ventricular zone of developing neocortex. J Neurosci 17:7037–7044PubMed
go back to reference Bonner J (2000) First signal: the evolution of multicellular development. Princeton University Press, Oxford Bonner J (2000) First signal: the evolution of multicellular development. Princeton University Press, Oxford
go back to reference Buhl DL, Buzsaki G (2005) Developmental emergence of hippocampal fast-field “ripple” oscillations in the behaving rat pups. Neuroscience 134:1423–1430CrossRefPubMedPubMedCentral Buhl DL, Buzsaki G (2005) Developmental emergence of hippocampal fast-field “ripple” oscillations in the behaving rat pups. Neuroscience 134:1423–1430CrossRefPubMedPubMedCentral
go back to reference Cohen-Cory S (2002) The developing synapse: construction and modulation of synaptic structures and circuits. Science 298:770–776CrossRefPubMed Cohen-Cory S (2002) The developing synapse: construction and modulation of synaptic structures and circuits. Science 298:770–776CrossRefPubMed
go back to reference Cowan W, Kandel E (2001) A brief history of synapse and synaptic transmission. The John Hopkins University Press, Baltimore Cowan W, Kandel E (2001) A brief history of synapse and synaptic transmission. The John Hopkins University Press, Baltimore
go back to reference Darwin C (1859) On the origin of species by means of natural selection. J. Murray, London Darwin C (1859) On the origin of species by means of natural selection. J. Murray, London
go back to reference Darwin C (1862) On the various contrivances by which British and foreign Orchids are fertilised by Insects, and on the good effects of intercrossing. John Murray, London Darwin C (1862) On the various contrivances by which British and foreign Orchids are fertilised by Insects, and on the good effects of intercrossing. John Murray, London
go back to reference Emes RD, Grant SG (2012) Evolution of synapse complexity and diversity. Annu Rev Neurosci 35:111–131CrossRefPubMed Emes RD, Grant SG (2012) Evolution of synapse complexity and diversity. Annu Rev Neurosci 35:111–131CrossRefPubMed
go back to reference Gould S (2002) The structure of evolutionary theory. Belknap Press of Harvard University Press, Cambridge Gould S (2002) The structure of evolutionary theory. Belknap Press of Harvard University Press, Cambridge
go back to reference Gould S, Vrba E (1982) Exaptation—a missing term in the science of form. Paleobiology 8:4–15CrossRef Gould S, Vrba E (1982) Exaptation—a missing term in the science of form. Paleobiology 8:4–15CrossRef
go back to reference Grant SG (2009) A general basis for cognition in the evolution of synapse signaling complexes. Cold Spring Harb Symp Quant Biol 74:249–257CrossRefPubMed Grant SG (2009) A general basis for cognition in the evolution of synapse signaling complexes. Cold Spring Harb Symp Quant Biol 74:249–257CrossRefPubMed
go back to reference Grosberg RK, Strathmann RR (2007) The evolution of multicellularity: a minor major transition? Annu Rev Ecol Evol Syst 38:621–654CrossRef Grosberg RK, Strathmann RR (2007) The evolution of multicellularity: a minor major transition? Annu Rev Ecol Evol Syst 38:621–654CrossRef
go back to reference Hormuzdi SG, Filippov MA, Mitropoulou G, Monyer H, Bruzzone R (2004) Electrical synapses: a dynamic signaling system that shapes the activity of neuronal networks. Biochim Biophys Acta 1662:113–137CrossRefPubMed Hormuzdi SG, Filippov MA, Mitropoulou G, Monyer H, Bruzzone R (2004) Electrical synapses: a dynamic signaling system that shapes the activity of neuronal networks. Biochim Biophys Acta 1662:113–137CrossRefPubMed
go back to reference Kloepper TH, Kienle CN, Fasshauer D (2007) An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol Biol Cell 18:3463–3471CrossRefPubMedPubMedCentral Kloepper TH, Kienle CN, Fasshauer D (2007) An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol Biol Cell 18:3463–3471CrossRefPubMedPubMedCentral
go back to reference Kosik KS (2009) Exploring the early origins of the synapse by comparative genomics. Biol Lett 5:108–111CrossRefPubMed Kosik KS (2009) Exploring the early origins of the synapse by comparative genomics. Biol Lett 5:108–111CrossRefPubMed
go back to reference Lalli C, Parson T (2006) Biological oceanography: an introduction. Elsevier, Amsterdam Lalli C, Parson T (2006) Biological oceanography: an introduction. Elsevier, Amsterdam
go back to reference Lane N (2015) The vital question: why is life the way it is?. W.W. Notron & Company, Inc., New York Lane N (2015) The vital question: why is life the way it is?. W.W. Notron & Company, Inc., New York
go back to reference Niculescu D, Lohmann C (2014) Gap junctions in developing thalamic and neocortical neuronal networks. Cereb Cortex 24:3097–3106CrossRefPubMed Niculescu D, Lohmann C (2014) Gap junctions in developing thalamic and neocortical neuronal networks. Cereb Cortex 24:3097–3106CrossRefPubMed
go back to reference Ovsepian SV, Vesselkin NP (2014) Wiring prior to firing: the evolutionary rise of electrical and chemical modes of synaptic transmission. Rev Neurosci 25:821–832CrossRefPubMed Ovsepian SV, Vesselkin NP (2014) Wiring prior to firing: the evolutionary rise of electrical and chemical modes of synaptic transmission. Rev Neurosci 25:821–832CrossRefPubMed
go back to reference Rash JE, Dillman RK, Bilhartz BL, Duffy HS, Whalen LR, Yasumura T (1996) Mixed synapses discovered and mapped throughout mammalian spinal cord. Proc Natl Acad Sci USA 93:4235–4239CrossRefPubMedPubMedCentral Rash JE, Dillman RK, Bilhartz BL, Duffy HS, Whalen LR, Yasumura T (1996) Mixed synapses discovered and mapped throughout mammalian spinal cord. Proc Natl Acad Sci USA 93:4235–4239CrossRefPubMedPubMedCentral
go back to reference Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang IF, Tidor B, Degnan BM, Oakley TH, Kosik KS (2007) A post-synaptic scaffold at the origin of the animal kingdom. PLoS One 2:e506CrossRefPubMedPubMedCentral Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang IF, Tidor B, Degnan BM, Oakley TH, Kosik KS (2007) A post-synaptic scaffold at the origin of the animal kingdom. PLoS One 2:e506CrossRefPubMedPubMedCentral
go back to reference Shepherd GM (1988) Neurobiology, 2nd edn. Oxford University Press, New York Shepherd GM (1988) Neurobiology, 2nd edn. Oxford University Press, New York
go back to reference Shestopalov VI, Panchin Y (2008) Pannexins and gap junction protein diversity. Cell Mol Life Sci 65:376–394CrossRefPubMed Shestopalov VI, Panchin Y (2008) Pannexins and gap junction protein diversity. Cell Mol Life Sci 65:376–394CrossRefPubMed
go back to reference Szabo TM, Faber DS, Zoran MJ (2004) Transient electrical coupling delays the onset of chemical neurotransmission at developing synapses. J Neurosci 24:112–120CrossRefPubMed Szabo TM, Faber DS, Zoran MJ (2004) Transient electrical coupling delays the onset of chemical neurotransmission at developing synapses. J Neurosci 24:112–120CrossRefPubMed
go back to reference Westfall IA (1996) Ultrastructure of synapses in the first-evolved nervous systems. J Neurocytol 25:735–746CrossRefPubMed Westfall IA (1996) Ultrastructure of synapses in the first-evolved nervous systems. J Neurocytol 25:735–746CrossRefPubMed
go back to reference Yuste R, Nelson DA, Rubin WW, Katz LC (1995) Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron 14:7–17CrossRefPubMed Yuste R, Nelson DA, Rubin WW, Katz LC (1995) Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron 14:7–17CrossRefPubMed
Metadata
Title
The birth of the synapse
Author
Saak V. Ovsepian
Publication date
01-11-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 8/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1459-2

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