Local resources of polyribosomes and SER promote synapse enlargement and spine clustering after long-term potentiation in adult rat hippocampus

被引:52
作者
Chirillo, Michael A. [1 ,2 ]
Waters, Mikayla S. [1 ,3 ]
Lindsey, Laurence F. [1 ,4 ]
Bourne, Jennifer N. [1 ,5 ]
Harris, Kristen M. [1 ]
机构
[1] Univ Texas Austin, Dept Neurosci, Ctr Learning & Memory, Austin, TX 78712 USA
[2] Univ Belgrade, Fulbright US Scholar Program, Studentski Trg 1, Belgrade 11000, Serbia
[3] McGovern Med Sch Houston, 6431 Fannin St, Houston, TX 77030 USA
[4] Google Seattle, Seattle, WA 98103 USA
[5] Univ Colorado, Dept Cell & Dev Biol, Anschutz Med Campus, Aurora, CO 80045 USA
基金
美国国家科学基金会;
关键词
ENDOPLASMIC-RETICULUM; DENDRITIC SPINES; SECRETORY TRAFFICKING; INTEGRAL MEMBRANE; INPUT SPECIFICITY; CALCIUM-RELEASE; DIFFERENT FORMS; CA1; DENDRITES; MICE LACKING; SYNAPTOPODIN;
D O I
10.1038/s41598-019-40520-x
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Synapse clustering facilitates circuit integration, learning, and memory. Long-term potentiation (LTP) of mature neurons produces synapse enlargement balanced by fewer spines, raising the question of how clusters form despite this homeostatic regulation of total synaptic weight. Three-dimensional reconstruction from serial section electron microscopy (3DEM) revealed the shapes and distributions of smooth endoplasmic reticulum (SER) and polyribosomes, subcellular resources important for synapse enlargement and spine outgrowth. Compared to control stimulation, synapses were enlarged two hours after LTP on resource-rich spines containing polyribosomes (4% larger than control) or SER (15% larger). SER in spines shifted from a single tubule to complex spine apparatus after LTP. Negligible synapse enlargement (0.6%) occurred on resource-poor spines lacking SER and polyribosomes. Dendrites were divided into discrete synaptic clusters surrounded by asynaptic segments. Spine density was lowest in clusters having only resource-poor spines, especially following LTP. In contrast, resource-rich spines preserved neighboring resource-poor spines and formed larger clusters with elevated total synaptic weight following LTP. These clusters also had more shaft SER branches, which could sequester cargo locally to support synapse growth and spinogenesis. Thus, resources appear to be redistributed to synaptic clusters with LTP-related synapse enlargement while homeostatic regulation suppressed spine outgrowth in resource-poor synaptic clusters.
引用
收藏
页数:14
相关论文
共 91 条
[1]   Nuclear calcium signalling in the regulation of brain function [J].
Bading, Hilmar .
NATURE REVIEWS NEUROSCIENCE, 2013, 14 (09) :593-608
[2]   Nanoconnectomic upper bound on the variability of synaptic plasticity [J].
Bartol, Thomas M., Jr. ;
Bromer, Cailey ;
Kinney, Justin ;
Chirillo, Michael A. ;
Bourne, Jennifer N. ;
Harris, Kristen M. ;
Sejnowski, Terrence J. .
ELIFE, 2015, 4
[3]   Dynamics of Nascent and Active Zone Ultrastructure as Synapses Enlarge During Long-Term Potentiation in Mature Hippocampus [J].
Bell, Maria Elizabeth ;
Bourne, Jennifer N. ;
Chirillo, Michael A. ;
Mendenhall, John M. ;
Kuwajima, Masaaki ;
Harris, Kristen M. .
JOURNAL OF COMPARATIVE NEUROLOGY, 2014, 522 (17) :3861-3884
[4]   Neuronal calcium signaling [J].
Berridge, MJ .
NEURON, 1998, 21 (01) :13-26
[5]   Structural complexity and functional diversity of endoplasmic reticulum Ca2+ stores [J].
Blaustein, MR ;
Golovina, VA .
TRENDS IN NEUROSCIENCES, 2001, 24 (10) :602-608
[6]   Single excitatory axons form clustered synapses onto CA1 pyramidal cell dendrites [J].
Bloss, Erik B. ;
Cembrowski, Mark S. ;
Karsh, Bill ;
Colonell, Jennifer ;
Fetter, Richard D. ;
Spruston, Nelson .
NATURE NEUROSCIENCE, 2018, 21 (03) :353-+
[7]   Polyribosomes are increased in spines of CA1 dendrites 2 h after the induction of LTP in mature rat hippocampal slices [J].
Bourne, Jennifer N. ;
Sorra, Karin E. ;
Hurlburt, Jamie ;
Harris, Kristen M. .
HIPPOCAMPUS, 2007, 17 (01) :1-4
[8]   Coordination of Size and Number of Excitatory and Inhibitory Synapses Results in a Balanced Structural Plasticity Along Mature Hippocampal CA1 Dendrites During LTP [J].
Bourne, Jennifer N. ;
Harris, Kristen M. .
HIPPOCAMPUS, 2011, 21 (04) :354-373
[9]   The single dendritic branch as a fundamental functional unit in the nervous system [J].
Branco, Tiago ;
Hausser, Michael .
CURRENT OPINION IN NEUROBIOLOGY, 2010, 20 (04) :494-502
[10]   Long-term potentiation expands information content of hippocampal dentate gyrus synapses [J].
Bromer, Cailey ;
Bartol, Thomas M. ;
Bowden, Jared B. ;
Hubbard, Dusten D. ;
Hanka, Dakota C. ;
Gonzalez, Paola V. ;
Kuwajima, Masaaki ;
Mendenhall, John M. ;
Parker, Patrick H. ;
Abraham, Wickliffe C. ;
Sejnowski, Terrence J. ;
Harris, Kristen M. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2018, 115 (10) :E2410-E2418