Overexpression of STIM1 in neurons in mouse brain improves contextual learning and impairs long-term depression

Majewski, Łukasz; Maciąg, Filip; Boguszewski, Paweł M.; Wasilewska, Iga; Wiera, Grzegorz; Wójtowicz, T.; Mozrzymas, Jerzy W.; Kuźnicki, Jacek

doi:10.1016/j.bbamcr.2016.11.025

Cited by 40 publications

(42 citation statements)

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“…Specifically, there are strong lines of evidence that the induction of bidirectional synaptic plasticity in the hippocampus is mediated by different calcium sources, with certain protocols requiring synergistic activation of multiple calcium sources (Brager & Johnston, ; Christie et al, ; Golding et al, ; Huber et al, ; Nishiyama, Hong, Mikoshiba, Poo, & Kato, ; Raymond, ). These studies show that plasticity induction is dependent on influx of calcium through NMDA receptors (Christie et al, ; Collingridge & Bliss, ; Collingridge, Kehl, & McLennan, ; Morris, Anderson, Lynch, & Baudry, ; Mulkey & Malenka, ; Nishiyama et al, ; Tsien, Huerta, & Tonegawa, ; Wang, Xu, Wu, Duan, & Poo, ), voltage‐gated calcium channels (Brager & Johnston, ; Christie et al, ; Christie, Schexnayder, & Johnston, ; Johnston, Williams, Jaffe, & Gray, ; Moosmang et al, ; Nicholson & Kullmann, ; Wang et al, ), store‐operated calcium channels (Baba et al, ; Garcia‐Alvarez et al, ; Majewski & Kuznicki, ; Majewski et al, ; Prakriya & Lewis, ) and receptors on the ER activated by metabotropic receptors on the plasma membrane (Huber et al, ; Jedlicka & Deller, ; Nishiyama et al, ; Padamsey, Foster, & Emptage, ; Verkhratsky, ). Additionally, voltage‐gated channels and their auxiliary subunits (Anirudhan & Narayanan, ; Brager, Lewis, Chetkovich, & Johnston, ; Chen et al, ; Chung, Ge, et al, ; Chung, Qian, et al, ; Johnston et al, ; Jung, Kim, & Hoffman, ; Kim et al, ; Lin et al, ; Lujan et al, ; Malik & Johnston, ; Nolan et al, ; Sehgal et al, ; Shah et al, ; Watanabe, Hoffman, Migliore, & Johnston, ) have also been shown to critically regulate the strength and direction of synaptic plasticity.…”

Section: Degeneracy At Multiple Scales In the Hippocampusmentioning

confidence: 99%

Degeneracy in hippocampal physiology and plasticity

2019

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Degeneracy, defined as the ability of structurally disparate elements to perform analogous function, has largely been assessed from the perspective of maintaining robustness of physiology or plasticity. How does the framework of degeneracy assimilate into an encoding system where the ability to change is an essential ingredient for storing new incoming information? Could degeneracy maintain the balance between the apparently contradictory goals of the need to change for encoding and the need to resist change towards maintaining homeostasis? In this review, we explore these fundamental questions with the mammalian hippocampus as an example encoding system. We systematically catalog lines of evidence, spanning multiple scales of analysis that point to the expression of degeneracy in hippocampal physiology and plasticity. We assess the potential of degeneracy as a framework to achieve the conjoint goals of encoding and homeostasis without cross‐interferences. We postulate that biological complexity, involving interactions among the numerous parameters spanning different scales of analysis, could establish disparate routes towards accomplishing these conjoint goals. These disparate routes then provide several degrees of freedom to the encoding‐homeostasis system in accomplishing its tasks in an input‐ and state‐dependent manner. Finally, the expression of degeneracy spanning multiple scales offers an ideal reconciliation to several outstanding controversies, through the recognition that the seemingly contradictory disparate observations are merely alternate routes that the system might recruit towards accomplishment of its goals.

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Section: Degeneracy At Multiple Scales In the Hippocampusmentioning

confidence: 99%

Degeneracy in hippocampal physiology and plasticity

2019

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“…Specifically, there are strong lines of evidence that the induction of bidirectional synaptic plasticity in the hippocampus is mediated by different calcium sources, with certain protocols requiring synergistic activation of multiple calcium 16, 2017; sources (Brager and Johnston, 2007;Christie et al, 1996;Golding et al, 2002;Huber et al, 1995;Nishiyama et al, 2000;Raymond, 2007). These studies show that plasticity induction is dependent on influx of calcium through NMDA receptors (Christie et al, 1996;Collingridge and Bliss, 1987;Collingridge et al, 1983;Morris et al, 1986;Mulkey and Malenka, 1992;Nishiyama et al, 2000;Tsien et al, 1996;Wang et al, 2003), voltage-gated calcium channels (Brager and Johnston, 2007;Christie et al, 1996;Christie et al, 1997;Johnston et al, 1992;Moosmang et al, 2005;Nicholson and Kullmann, 2017;Wang et al, 2003), store-operated calcium channels (Baba et al, 2003;Garcia-Alvarez et al, 2015;Majewski and Kuznicki, 2015;Majewski et al, 2016;Prakriya and Lewis, 2015) and receptors on the ER activated by metabotropic receptors on the plasma membrane (Huber et al, 2000;Nishiyama et al, 2000;Verkhratsky, 2002). Additionally, voltage-gated channels and their auxiliary subunits (Anirudhan and Narayanan, 2015;Brager et al, 2013;Chen et al, 2006;Chung et al, 2009a;Chung et al, 2009b;Johnston et al,...…”

Section: Degeneracy In Calcium Regulation and In The Induction Of Synmentioning

confidence: 99%

Degeneracy in hippocampal physiology and plasticity

Rathour

Narayanan

2017

Preprint

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Degeneracy, defined as the ability of structurally disparate elements to perform analogous function, has largely been assessed from the perspective of maintaining robustness of physiology or plasticity. How does the framework of degeneracy assimilate into an encoding system where the ability to change is an essential ingredient for storing new incoming information? Could degeneracy maintain the balance between the apparently contradictory goals of the need to change for encoding and the need to resist change towards maintaining homeostasis? In this review, we explore these fundamental questions with the mammalian hippocampus as an example encoding system. We systematically catalog lines of evidence, spanning multiple scales of analysis, that demonstrate the expression of degeneracy in hippocampal physiology and plasticity. We assess the potential of degeneracy as a framework to achieve encoding and homeostasis without cross-interferences, and postulate that multiscale parametric and interactional complexity could establish disparate routes towards accomplishing these conjoint goals. These disparate routes then provide several degrees of freedom to the encodinghomeostasis system in accomplishing its tasks in an input-and state-dependent manner. Finally, the expression of degeneracy spanning multiple scales offers an ideal reconciliation to several outstanding controversies, through the recognition that the seemingly contradictory disparate observations are merely alternate routes that the system might recruit towards accomplishment of its goals. Juxtaposed against the ubiquitous prevalence of degeneracy and its strong links to evolution, it is perhaps apt to add a corollary to Theodosius Dobzhansky's famous quote and state "nothing in physiology makes sense except in the light of degeneracy".peer-reviewed)

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“…Using optically controlled construct OptoSTIM1, Kyung et al demonstrated that expression and activation of this construct in mouse hippocampus is able to induce nSOC Ca 2+ influx and promote contextual memory formation [12]. Majewski et al observed improvements of contextual learning in STIM1 overexpressing mice [13]. These authors further demonstrated that overexpression of STIM1 does not influence long-term potentiaton (LTP) induction in acute hippocampal slices, however, blocks DHPG-dependent long-term depression (LTD) [13].…”

mentioning

confidence: 99%

“…Majewski et al observed improvements of contextual learning in STIM1 overexpressing mice [13]. These authors further demonstrated that overexpression of STIM1 does not influence long-term potentiaton (LTP) induction in acute hippocampal slices, however, blocks DHPG-dependent long-term depression (LTD) [13]. The mice with forebrain-specific knockout of STIM1 and STIM2 were analyzed by Garcia-Alvarez et al [14].…”

mentioning

confidence: 99%

“…Observed discrepancies are likely to be caused by differences in experimental models and protocols. Nevertheless, learning and synaptic plasticity phenotypes observed in STIM1 and STIM2 knockout and overexpression models [12][13][14]16] suggest that these proteins clearly play a role in neuronal function. It is likely that the main role of nSOC in neurons is signaling and not just refilling of the stores [23].…”

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confidence: 99%

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STIM Proteins As Regulators of Neuronal Store-Operated Calcium Influx

Попугаева

Bezprozvanny

2018

Neurodegener. Dis. Manag.

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The store-operated calcium channels (SOC) were initially described in nonexcitable cells, such as T cells in the immune system [1]. In neurons, the presence of SOC has been controversial [2]. The main argument against neuronal SOC (nSOC) is that neurons possess many other calcium-permeable channels with high conductance, such as NMDA receptors and voltage-gated calcium channels. The existence, functional relevance and molecular identity of nSOC are still under investigation. However, recent molecular analysis of nSOC provided support to its existence and importance for neuronal function.SOC is mediated by two main components: endoplasmic reticulum (ER) Ca 2+ sensors STIM1 or STIM2 proteins [3] and plasma membrane (PM) Ca 2+ channels from Orai and TRPC protein families [1]. SOC in nonexcitable cells is activated by ER Ca 2+ depletion in response to activation of inositol (1,4,5)-trisphosphate receptors and Ca 2+ release from the ER. ER Ca 2+ concentration is sensed by helix-loop-helix structural domain (EF hand domain) in the luminal portion of STIM1. Following Ca 2+ depletion from the ER, STIM1 forms oligomers and translocates to ER-PM junctions [1]. Once located to ER-PM junctions, STIM1 binds to Orai proteins and activate SOC Ca 2+ influx, leading to an increase in intracellular Ca 2+ concentration. This cytoplasmic Ca 2+ abundance is sequestered by SERCA pump to the ER, refilling the stores. The EF hand domain of STIM2 proteins has significantly lower affinity for Ca 2+ than STIM1, and it has been established that STIM2 proteins primarily control steady-state ER and cytosolic Ca 2+ homeostasis [4]. Both STIM1 and STIM2 proteins are expressed in hippocampal neurons [5], and both of these proteins have been implicated in control of nSOC. Klejman et al. observed that STIM1 is colocalized with Orai1 upon depletion of Ca 2+ stores in dendrites and soma [6]. More recent reports suggested that STIM1 and Orai1 are colocalized and may interact with synaptopodin, a protein that regulates synaptic plasticity in hippocampal dendritic spines [7]. Activation of STIM1 and nSOC was described in hippocampal neurons following activation of type I metabotropic glutamate receptors (mGluR) or muscarinic acetylcholine receptors (mAChR) [8]. Notably, nSOC-independent functions of STIM1 in hipocampal neurons were also reported. It was suggested that STIM1 directly controls level of phosphorylation and surface expression of the AMPAR [9]. The role of STIM1 in control of neuronal L-type Ca 2+ channel activity [10] and feedback regulation of Ca 2+ signals in presynaptic terminals was reported [11]. Using optically controlled construct OptoSTIM1, Kyung et al. demonstrated that expression and activation of this construct in mouse hippocampus is able to induce nSOC Ca 2+ influx and promote contextual memory formation [12]. Majewski et al. observed improvements of contextual learning in STIM1 overexpressing mice [13]. These authors further demonstrated that overexpression of STIM1 does not influence long-term potentiaton (LTP) induction in...

show abstract

Overexpression of STIM1 in neurons in mouse brain improves contextual learning and impairs long-term depression

Cited by 40 publications

References 115 publications

Degeneracy in hippocampal physiology and plasticity

Degeneracy in hippocampal physiology and plasticity

Degeneracy in hippocampal physiology and plasticity

STIM Proteins As Regulators of Neuronal Store-Operated Calcium Influx

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