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Article ; Online: The Thermodynamically Expensive Contribution of Three Calcium Sources to Somatic Release of Serotonin.

De-Miguel, Francisco F

International journal of molecular sciences

2022 Volume 23, Issue 3

Abstract: The soma, dendrites and axon of neurons may display calcium-dependent release of transmitters and peptides. Such release is named extrasynaptic for occurring in absence of synaptic structures. This review describes the cooperative actions of three ... ...

Abstract	The soma, dendrites and axon of neurons may display calcium-dependent release of transmitters and peptides. Such release is named extrasynaptic for occurring in absence of synaptic structures. This review describes the cooperative actions of three calcium sources on somatic exocytosis. Emphasis is given to the somatic release of serotonin by the classical leech Retzius neuron, which has allowed detailed studies on the fine steps from excitation to exocytosis. Trains of action potentials induce transmembrane calcium entry through L-type channels. For action potential frequencies above 5 Hz, summation of calcium transients on individual action potentials activates the second calcium source: ryanodine receptors produce calcium-induced calcium release. The resulting calcium tsunami activates mitochondrial ATP synthesis to fuel transport of vesicles to the plasma membrane. Serotonin that is released maintains a large-scale exocytosis by activating the third calcium source: serotonin autoreceptors coupled to phospholipase C promote IP3 production. Activated IP3 receptors in peripheral endoplasmic reticulum release calcium that promotes vesicle fusion. The Swiss-clock workings of the machinery for somatic exocytosis has a striking disadvantage. The essential calcium-releasing endoplasmic reticulum near the plasma membrane hinders the vesicle transport, drastically reducing the thermodynamic efficiency of the ATP expenses and elevating the energy cost of release.
MeSH term(s)	Action Potentials ; Animals ; Calcium/metabolism ; Calcium Signaling ; Exocytosis ; Gene Expression Regulation ; Humans ; Mitochondria/metabolism ; Neurons/metabolism ; Serotonin/metabolism ; Thermodynamics
Chemical Substances	Serotonin (333DO1RDJY) ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2022-01-28
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms23031495
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Article: Dynamics of Neuromuscular Transmission Reproduced by Calcium-Dependent and Reversible Serial Transitions in the Vesicle Fusion Complex.

Martínez-Valencia, Alejandro / Ramírez-Santiago, Guillermo / De-Miguel, Francisco F

Frontiers in synaptic neuroscience

2022 Volume 13, Page(s) 785361

Abstract: Neuromuscular transmission, from spontaneous release to facilitation and depression, was accurately reproduced by a mechanistic kinetic model of sequential maturation transitions in the molecular fusion complex. The model incorporates three predictions. ... ...

Abstract	Neuromuscular transmission, from spontaneous release to facilitation and depression, was accurately reproduced by a mechanistic kinetic model of sequential maturation transitions in the molecular fusion complex. The model incorporates three predictions. First, calcium-dependent forward transitions take vesicles from docked to preprimed to primed states, followed by fusion. Second, prepriming and priming are reversible. Third, fusion and recycling are unidirectional. The model was fed with experimental data from previous studies, whereas the backward (β) and recycling (ρ) rate constant values were fitted. Classical experiments were successfully reproduced with four transition states in the model when every forward (α) rate constant had the same value, and both backward rate constants were 50-100 times larger. Such disproportion originated an abruptly decreasing gradient of resting vesicles from docked to primed states. By contrast, a three-state version of the model failed to reproduce the dynamics of transmission by using the same set of parameters. Simulations predict the following: (1) Spontaneous release reflects primed to fusion spontaneous transitions. (2) Calcium elevations synchronize the series of forward transitions that lead to fusion. (3) Facilitation reflects a transient increase of priming following the calcium-dependent maturation transitions. (4) The calcium sensors that produce facilitation are those that evoke the transitions form docked to primed states. (5) Backward transitions and recycling restore the resting state. (6) Depression reflects backward transitions and slow recycling after intense release. Altogether, our results predict that fusion is produced by one calcium sensor, whereas the modulation of the number of vesicles that fuse depends on the calcium sensors that promote the early transition states. Such finely tuned kinetics offers a mechanism for collective non-linear transitional adaptations of a homogeneous vesicle pool to the ever-changing pattern of electrical activity in the neuromuscular junction.
Language	English
Publishing date	2022-02-15
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2592086-8
ISSN	1663-3563
ISSN	1663-3563
DOI	10.3389/fnsyn.2021.785361
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Article: Thermodynamic Efficiency of Somatic Exocytosis of Serotonin.

Noguez, Paula / Rubí, J Miguel / De-Miguel, Francisco F

Frontiers in physiology

2019 Volume 10, Page(s) 473

Abstract: Through somatic exocytosis neurons liberate immense amounts of transmitter molecules that modulate the functioning of the nervous system. A stream of action potentials triggers an ATP-dependent transport of transmitter-containing vesicles to the plasma ... ...

Abstract	Through somatic exocytosis neurons liberate immense amounts of transmitter molecules that modulate the functioning of the nervous system. A stream of action potentials triggers an ATP-dependent transport of transmitter-containing vesicles to the plasma membrane, that ends with a large-scale exocytosis. It is commonly assumed that biological processes use metabolic energy with a high thermodynamic efficiency, meaning that most energy generates work with minor dissipation. However, the intricate ultrastructure underlying the pathway for the vesicle flow necessary for somatic exocytosis challenges this possibility. To study this problem here we first applied thermodynamic theory to quantify the efficiency of somatic exocytosis of the vital transmitter serotonin. Then we correlated the efficiency to the ultrastructure of the transport pathway of the vesicles. Exocytosis was evoked in cultured Retzius neurons of the leech by trains of 10 impulses delivered at 20 Hz. The kinetics of exocytosis was quantified from the gradual fluorescence increase of FM1-43 dye as it became incorporated into vesicles that underwent their exo-endocytosis cycle. By fitting a model of the vesicle transport carried by motor forces to the kinetics of exocytosis, we calculated the thermodynamic efficiency of the ATP expenses per vesicle, as the power of the transport divided by total energy ideally produced by the hydrolysis of ATP during the process. The efficiency was remarkably low (0.1-6.4%) and the values formed a W-shape distribution with the transport distances of the vesicles. Electron micrographs and fluorescent staining of the actin cortex indicated that the slopes of the W chart could be explained by the interaction of vesicles with the actin cortex and the calcium-releasing endoplasmic reticulum. We showed that the application of thermodynamic theory permitted to predict aspects of the intracellular structure. Our results suggest that the distribution of subcellular structures that are essential for somatic exocytosis abates the thermodynamic efficiency of the transport by hampering vesicle mobilization. It is remarkable that the modulation of the nervous system occurs at the expenses of an efficient use of metabolic energy.
Language	English
Publishing date	2019-05-31
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2564217-0
ISSN	1664-042X
ISSN	1664-042X
DOI	10.3389/fphys.2019.00473
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Article: Extrasynaptic Neurotransmission Mediated by Exocytosis and Diffusive Release of Transmitter Substances.

Del-Bel, Elaine / De-Miguel, Francisco F

Frontiers in synaptic neuroscience

2018 Volume 10, Page(s) 13

Abstract: This review article deals with the mechanisms of extrasynaptic release of transmitter substances, namely the release from the soma, axon and dendrites in the absence of postsynaptic counterparts. Extrasynaptic release occurs by exocytosis or diffusion. ... ...

Abstract	This review article deals with the mechanisms of extrasynaptic release of transmitter substances, namely the release from the soma, axon and dendrites in the absence of postsynaptic counterparts. Extrasynaptic release occurs by exocytosis or diffusion. Spillover from the synaptic cleft also contributes to extrasynaptic neurotransmission. Here, we first describe two well-known examples of exocytosis from the neuronal soma, which may release copious amounts of transmitter for up to hundreds of seconds after electrical stimulation. The mechanisms for somatic exocytosis of the low molecular weight transmitter serotonin, and the peptides oxytocin and vasopressin have been studied in detail. Serotonin release from leech neurons and oxytocin and vasopressin from rodent neurons have a common multi-step mechanism, which is completely different from that for exocytosis from presynaptic endings. Most transmitters and peptides released extrasynaptically seem to follow this same mechanism. Extrasynaptic exocytosis may occur onto glial cells, which act as intermediaries for long-term and long-distance transmission. The second part of this review article focuses on the release upon synthesis of the representative diffusible molecules nitric oxide (NO) and endocannabinoids. Diffusible molecules are synthesized "on demand" from postsynaptic terminals in response to electrical activity and intracellular calcium elevations. Their effects include the retrograde modulation of presynaptic electrical activity and transmitter release. Extrasynaptic neurotransmission is well exemplified in the retina. Light-evoked extrasynaptic communication sets the gain for visual responses and integrates the activity of neurons, glia and blood vessels. Understanding how extrasynaptic communication changes the function of hard-wired circuits has become fundamental to understand the function of the nervous system.
Language	English
Publishing date	2018-06-08
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2592086-8
ISSN	1663-3563
ISSN	1663-3563
DOI	10.3389/fnsyn.2018.00013
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Article ; Online: Release of chemical transmitters from cell bodies and dendrites of nerve cells.

De-Miguel, Francisco F / Nicholls, John G

Philosophical transactions of the Royal Society of London. Series B, Biological sciences

2015 Volume 370, Issue 1672

Abstract: Papers in this issue concern extrasynaptic transmission, namely release of signalling molecules by exocytosis or diffusion from neuronal cell bodies, dendrites, axons and glia. Problems discussed concern the molecules, their secretion and importance for ... ...

Abstract	Papers in this issue concern extrasynaptic transmission, namely release of signalling molecules by exocytosis or diffusion from neuronal cell bodies, dendrites, axons and glia. Problems discussed concern the molecules, their secretion and importance for normal function and disease. Molecules secreted extrasynaptically include transmitters, peptides, hormones and nitric oxide. For extrasynaptic secretion, trains of action potentials are required, and the time course of release is slower than at synapses. Questions arise concerning the mechanism of extrasynaptic secretion: how does it differ from the release observed at synaptic terminals and gland cells? What kinds of vesicles take part? Is release accomplished through calcium entry, SNAP and SNARE proteins? A clear difference is in the role of molecules released synaptically and extrasynaptically. After extrasynaptic release, molecules reach distant as well as nearby cells, and thereby produce long-lasting changes over large volumes of brain. Such changes can affect circuits for motor performance and mood states. An example with clinical relevance is dyskinesia of patients treated with l-DOPA for Parkinson's disease. Extrasynaptically released transmitters also evoke responses in glial cells, which in turn release molecules that cause local vasodilatation and enhanced circulation in regions of the brain that are active.
MeSH term(s)	Cell Body/metabolism ; Dendrites/metabolism ; Exocytosis/physiology ; Neurons/cytology ; Neurons/metabolism ; Neurotransmitter Agents/metabolism
Chemical Substances	Neurotransmitter Agents
Language	English
Publishing date	2015-05-24
Publishing country	England
Document type	Journal Article
ZDB-ID	208382-6
ISSN	1471-2970 ; 0080-4622 ; 0264-3839 ; 0962-8436
ISSN (online)	1471-2970
ISSN	0080-4622 ; 0264-3839 ; 0962-8436
DOI	10.1098/rstb.2014.0181
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Article ; Online: A tale of two leeches: Toward the understanding of the evolution and development of behavioral neural circuits.

Kuo, Dian-Han / De-Miguel, Francisco F / Heath-Heckman, Elizabeth A C / Szczupak, Lidia / Todd, Krista / Weisblat, David A / Winchell, Christopher J

Evolution & development

2020 Volume 22, Issue 6, Page(s) 471–493

Abstract: In the animal kingdom, behavioral traits encompass a broad spectrum of biological phenotypes that have critical roles in adaptive evolution, but an EvoDevo approach has not been broadly used to study behavior evolution. Here, we propose that, by ... ...

Abstract	In the animal kingdom, behavioral traits encompass a broad spectrum of biological phenotypes that have critical roles in adaptive evolution, but an EvoDevo approach has not been broadly used to study behavior evolution. Here, we propose that, by integrating two leech model systems, each of which has already attained some success in its respective field, it is possible to take on behavioral traits with an EvoDevo approach. We first identify the developmental changes that may theoretically lead to behavioral evolution and explain why an EvoDevo study of behavior is challenging. Next, we discuss the pros and cons of the two leech model species, Hirudo, a classic model for invertebrate neurobiology, and Helobdella, an emerging model for clitellate developmental biology, as models for behavioral EvoDevo research. Given the limitations of each leech system, neither is particularly strong for behavioral EvoDevo. However, the two leech systems are complementary in their technical accessibilities, and they do exhibit some behavioral similarities and differences. By studying them in parallel and together with additional leech species such as Haementeria, it is possible to explore the different levels of behavioral development and evolution.
MeSH term(s)	Animals ; Behavior, Animal ; Biological Evolution ; Leeches/embryology ; Leeches/growth & development ; Leeches/physiology ; Models, Animal ; Species Specificity
Language	English
Publishing date	2020-11-23
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2020288-X
ISSN	1525-142X ; 1520-541X
ISSN (online)	1525-142X
ISSN	1520-541X
DOI	10.1111/ede.12358
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Article: Corrigendum: On the Basis of Synaptic Integration Constancy during Growth of a Neuronal Circuit.

De-La-Rosa Tovar, Adriana / Mishra, Prashant K / De-Miguel, Francisco F

Frontiers in cellular neuroscience

2017 Volume 11, Page(s) 399

Abstract: This corrects the article on p. 198 in vol. 10, PMID: 27587998.]. ...

Abstract	[This corrects the article on p. 198 in vol. 10, PMID: 27587998.].
Language	English
Publishing date	2017-12-12
Publishing country	Switzerland
Document type	Journal Article ; Published Erratum
ZDB-ID	2452963-1
ISSN	1662-5102
ISSN	1662-5102
DOI	10.3389/fncel.2017.00399
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Article ; Online: Octopamine cyclic release and its modulation of visual sensitivity in crayfish.

Rodríguez-Sosa, Leonardo / Calderón-Rosete, Gabina / Ortega-Cambranis, Aída / De-Miguel, Francisco F

Comparative biochemistry and physiology. Part A, Molecular & integrative physiology

2017 Volume 203, Page(s) 83–90

Abstract: The biogenic amine octopamine (OA) modulates invertebrate behavior by changing neuronal responses from sensory inputs to motor outputs. However, the OA modulation of visual sensitivity and its possible coupling to diurnal cycles remains unexplored. Here ... ...

Abstract	The biogenic amine octopamine (OA) modulates invertebrate behavior by changing neuronal responses from sensory inputs to motor outputs. However, the OA modulation of visual sensitivity and its possible coupling to diurnal cycles remains unexplored. Here we studied the diurnal variations in the OA levels in the hemolymph of the crayfish Procambarus clarkii, its release from the structures in the eyestalk and its modulation of the retinal light sensitivity. The hemolymph concentration of OA and its amino acid precursor tyrosine was measured by high-resolution liquid chromatography; OA varied along the 24-hcycle. The peak value appeared about 2h before the light offset which preceded the peak locomotor activity. OA was found in every structure of the eyestalk but displayed higher levels in the retina-lamina ganglionaris. Moreover, OA was released from isolated eyestalks at a rate of 92nmol/eyestalk/min and a calcium-dependent release was evoked by incubation in a high potassium solution. OA injected into dark-adapted crayfish or applied to the isolated retina at concentrations of 1, 10 and 100μM produced a proportionally increasing reduction in the amplitude of the photoreceptor light responses. These OA concentrations did not affect the position of the visual accessory pigments. Our results suggest that OA release in the crayfish eyestalk is coupled to the 24-hcycle to regulate the diurnal reduction of the photoreceptor sensitivity and to favor the expression of exploratory locomotion during the dark phase of the circadian cycle.
MeSH term(s)	Animals ; Astacoidea/metabolism ; Chromatography, Liquid ; Octopamine/metabolism ; Retina/physiology
Chemical Substances	Octopamine (14O50WS8JD)
Language	English
Publishing date	2017-01
Publishing country	United States
Document type	Journal Article
ZDB-ID	121246-1
ISSN	1531-4332 ; 0300-9629 ; 1095-6433
ISSN (online)	1531-4332
ISSN	0300-9629 ; 1095-6433
DOI	10.1016/j.cbpa.2016.08.032
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Article ; Online: Transcriptional profiling of identified neurons in leech.

Heath-Heckman, Elizabeth / Yoo, Shinja / Winchell, Christopher / Pellegrino, Maurizio / Angstadt, James / Lammardo, Veronica B / Bautista, Diana / De-Miguel, Francisco F / Weisblat, David

BMC genomics

2021 Volume 22, Issue 1, Page(s) 215

Abstract: Background: While leeches in the genus Hirudo have long been models for neurobiology, the molecular underpinnings of nervous system structure and function in this group remain largely unknown. To begin to bridge this gap, we performed RNASeq on pools of ...

Abstract	Background: While leeches in the genus Hirudo have long been models for neurobiology, the molecular underpinnings of nervous system structure and function in this group remain largely unknown. To begin to bridge this gap, we performed RNASeq on pools of identified neurons of the central nervous system (CNS): sensory T (touch), P (pressure) and N (nociception) neurons; neurosecretory Retzius cells; and ganglia from which these four cell types had been removed. Results: Bioinformatic analyses identified 3565 putative genes whose expression differed significantly among the samples. These genes clustered into 9 groups which could be associated with one or more of the identified cell types. We verified predicted expression patterns through in situ hybridization on whole CNS ganglia, and found that orthologous genes were for the most part similarly expressed in a divergent leech genus, suggesting evolutionarily conserved roles for these genes. Transcriptional profiling allowed us to identify candidate phenotype-defining genes from expanded gene families. Thus, we identified one of eight hyperpolarization-activated cyclic-nucleotide gated (HCN) channels as a candidate for mediating the prominent sag current in P neurons, and found that one of five inositol triphosphate receptors (IP3Rs), representing a sub-family of IP3Rs absent from vertebrate genomes, is expressed with high specificity in T cells. We also identified one of two piezo genes, two of ~ 65 deg/enac genes, and one of at least 16 transient receptor potential (trp) genes as prime candidates for involvement in sensory transduction in the three distinct classes of leech mechanosensory neurons. Conclusions: Our study defines distinct transcriptional profiles for four different neuronal types within the leech CNS, in addition to providing a second ganglionic transcriptome for the species. From these data we identified five gene families that may facilitate the sensory capabilities of these neurons, thus laying the basis for future work leveraging the strengths of the leech system to investigate the molecular processes underlying and linking mechanosensation, cell type specification, and behavior.
MeSH term(s)	Animals ; Central Nervous System ; In Situ Hybridization ; Leeches/genetics ; Neurons
Language	English
Publishing date	2021-03-25
Publishing country	England
Document type	Journal Article
ISSN	1471-2164
ISSN (online)	1471-2164
DOI	10.1186/s12864-021-07526-0
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Article ; Online: Extrasynaptic exocytosis and its mechanisms: a source of molecules mediating volume transmission in the nervous system.

Trueta, Citlali / De-Miguel, Francisco F

Frontiers in physiology

2012 Volume 3, Page(s) 319

Abstract: We review the evidence of exocytosis from extrasynaptic sites in the soma, dendrites, and axonal varicosities of central and peripheral neurons of vertebrates and invertebrates, with emphasis on somatic exocytosis, and how it contributes to signaling in ... ...

Abstract	We review the evidence of exocytosis from extrasynaptic sites in the soma, dendrites, and axonal varicosities of central and peripheral neurons of vertebrates and invertebrates, with emphasis on somatic exocytosis, and how it contributes to signaling in the nervous system. The finding of secretory vesicles in extrasynaptic sites of neurons, the presence of signaling molecules (namely transmitters or peptides) in the extracellular space outside synaptic clefts, and the mismatch between exocytosis sites and the location of receptors for these molecules in neurons and glial cells, have long suggested that in addition to synaptic communication, transmitters are released, and act extrasynaptically. The catalog of these molecules includes low molecular weight transmitters such as monoamines, acetylcholine, glutamate, gama-aminobutiric acid (GABA), adenosine-5-triphosphate (ATP), and a list of peptides including substance P, brain-derived neurotrophic factor (BDNF), and oxytocin. By comparing the mechanisms of extrasynaptic exocytosis of different signaling molecules by various neuron types we show that it is a widespread mechanism for communication in the nervous system that uses certain common mechanisms, which are different from those of synaptic exocytosis but similar to those of exocytosis from excitable endocrine cells. Somatic exocytosis has been measured directly in different neuron types. It starts after high-frequency electrical activity or long experimental depolarizations and may continue for several minutes after the end of stimulation. Activation of L-type calcium channels, calcium release from intracellular stores and vesicle transport towards the plasma membrane couple excitation and exocytosis from small clear or large dense core vesicles in release sites lacking postsynaptic counterparts. The presence of synaptic and extrasynaptic exocytosis endows individual neurons with a wide variety of time- and space-dependent communication possibilities. Extrasynaptic exocytosis may be the major source of signaling molecules producing volume transmission and by doing so may be part of a long duration signaling mode in the nervous system.
Language	English
Publishing date	2012-09-04
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2564217-0
ISSN	1664-042X ; 1664-042X
ISSN (online)	1664-042X
ISSN	1664-042X
DOI	10.3389/fphys.2012.00319
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