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Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Bioactives and Nutraceuticals".

Deadline for manuscript submissions: closed (31 December 2019) | Viewed by 60291

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Prof. Dr. Juan C. Mayo

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Departamento de Morfologia y Biologia Celular, Instituto Universitario Oncologico del Principado de Asturias (IUOPA), Universidad de Oviedo, 33006 Oviedo, Spain
Interests: redox regulation; antioxidant enzymes; oxidative stress; prostate cancer; melatonin
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Prof. Dr. Rosa M. Sainz

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Universidad de Oviedo, Oviedo, Spain
Interests: redox regulation; antioxidant enzymes; cell signaling; prostate cancer; cell metabolism
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Dear Colleagues,

Melatonin, the primary product of the pineal gland, was discovered in the late 1950s as a hormonal factor that lightens the skin of tadpoles. This effect, the first reported biological function of melatonin, is far from revealing the actual role of the indole. In the mid-1960s, Hoffman and Reiter found that seasonal fluctuations of melatonin synchronize reproductive activities in seasonal breeding animals. Since then, researchers’ knowledge about the indole has changed dramatically. Not only is the essential function of the cell questioned, but also where the indole can be found, and how it is synthesized.

Melatonin is released at night with a duration inverse to that of the photoperiod, participating in the transmission of the circadian and seasonal message to the organism. In humans, the pineal hormone is also used to readjust the circadian phases, after time shifts derived from jet lag or maladapted shift work, in sleep disorders, blind people or in circadian-related mood disorders. Additionally, melatonin was found to be an endogenous potent-free radical scavenger and enhancer of the antioxidant system, thus protecting cells from the harmful effect of pro-oxidants. This protecting effect should be added to the immunomodulatory and anti-proliferative actions widely reported in many cell and animal models. More recently, the physiological interaction between melatonin and glucose metabolism has been the focus of attention of several research groups. Melatonin controls the daily rhythms of glucose levels by altering insulin release, or by inhibiting glucose uptake. Melatonin functions are mediated by membrane receptors MT1 and MT2, intracellular binding sites or as a consequence of receptor-independent actions.

All papers related to any aspect of melatonin physiology, biochemistry and molecular biology, as well as clinical reports, will be considered for this Special Issue.

Prof. Dr. Juan C. Mayo
Prof. Dr. Rosa M. Sainz
Guest Editors

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Keywords

animal
plant
microbiota
metabolism
glucose
cancer
diabetes
insulin resistance
stem cells
genomics, metabolomics, proteomics
cell growth
cell death
differentiation
apoptosis
oxidative stress
redox signalling

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Editorial

Jump to: Research, Review

4 pages, 180 KiB

Open AccessEditorial

Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019

by Juan C. Mayo and Rosa M. Sainz

Int. J. Mol. Sci. 2020, 21(10), 3645; https://doi.org/10.3390/ijms21103645 - 21 May 2020

Cited by 7 | Viewed by 2400

Abstract

During the last 25 years we have accomplished great advances in melatonin research, regarding antioxidant or anti-inflammatory functions, oncostatic actions, glucose metabolism regulation or plant physiology, among others. Of course, we should not forget the classical, circadian-related functions of the indole, which has recently brought up new and important findings. All together these new discoveries will likely lead the way in the next decade in terms of melatonin research. This special issue collects some of these new advances focused on different aspects of the indole Full article

(This article belongs to the Special Issue Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019)

Research

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16 pages, 3858 KiB

Open AccessArticle

Reperfusion Arrhythmias Increase after Superior Cervical Ganglionectomy Due to Conduction Disorders and Changes in Repolarization

by Natalia Jorgelina Prado, Estela Maris Muñoz, Luz Estefanía Farias Altamirano, Francisco Aguiar, Amira Zulma Ponce Zumino, Francisco Javier Sánchez, Roberto Miguel Miatello, Esther Pueyo and Emiliano Raúl Diez

Int. J. Mol. Sci. 2020, 21(5), 1804; https://doi.org/10.3390/ijms21051804 - 6 Mar 2020

Cited by 6 | Viewed by 3953

Abstract

Pharmacological concentrations of melatonin reduce reperfusion arrhythmias, but less is known about the antiarrhythmic protection of the physiological circadian rhythm of melatonin. Bilateral surgical removal of the superior cervical ganglia irreversibly suppresses melatonin rhythmicity. This study aimed to analyze the cardiac electrophysiological effects of the loss of melatonin circadian oscillation and the role played by myocardial melatonin membrane receptors, SERCA_2A, TNFα, nitrotyrosine, TGFβ, K_ATP channels, and connexin 43. Three weeks after bilateral removal of the superior cervical ganglia or sham surgery, the hearts were isolated and submitted to ten minutes of regional ischemia followed by ten minutes of reperfusion. Arrhythmias, mainly ventricular tachycardia, increased during reperfusion in the ganglionectomy group. These hearts also suffered an epicardial electrical activation delay that increased during ischemia, action potential alternants, triggered activity, and dispersion of action potential duration. Hearts from ganglionectomized rats showed a reduction of the cardioprotective MT₂ receptors, the MT₁ receptors, and SERCA_2A. Markers of nitroxidative stress (nitrotyrosine), inflammation (TNFα), and fibrosis (TGFβ and vimentin) did not change between groups. Connexin 43 lateralization and the pore-forming subunit (Kir6.1) of K_ATP channels increased in the experimental group. We conclude that the loss of the circadian rhythm of melatonin predisposes the heart to suffer cardiac arrhythmias, mainly ventricular tachycardia, due to conduction disorders and changes in repolarization. Full article

(This article belongs to the Special Issue Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019)

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15 pages, 3679 KiB

Open AccessArticle

Melatonin Modulates Dendrite Maturation and Complexity in the Dorsal- and Ventral- Dentate Gyrus Concomitantly with Its Antidepressant-Like Effect in Male Balb/C Mice

by Gerardo Bernabé Ramírez-Rodríguez, Diana Montserrat Palacios-Cabriales, Leonardo Ortiz-López, Erika Montserrat Estrada-Camarena and Nelly Maritza Vega-Rivera

Int. J. Mol. Sci. 2020, 21(5), 1724; https://doi.org/10.3390/ijms21051724 - 3 Mar 2020

Cited by 16 | Viewed by 3613

Abstract

Adult neurogenesis occurs in the dentate gyrus (DG) of the hippocampus. New neurons help to counteract the effects of stress and several interventions including antidepressant drugs, environmental modifications and internal factors act pro-neurogenic with consequences in the dorsal and ventral DG. Melatonin, the main product synthesized by the pineal gland, induces antidepressant-like effects and modulates several events of the neurogenic process. However, the information related to the capability of melatonin to modulate dendrite maturation and complexity in the dorsal and ventral regions of the DG and their correlation with its antidepressant-like effect is absent. Thus, in this study, we analyzed the impact of melatonin (0, 0.5, 1, 2.5, 5 or 10 mg/kg) administered daily for fourteen days on the number, dendrite complexity and distribution of doublecortin (DCX)-cells in the dorsal-ventral regions of the DG in male Balb/C mice. Doublecortin is a microtubule-associated protein that is expressed during the course of dendritic maturation of newborn neurons. Also, we analyzed the impact of melatonin on despair-like behavior in the forced swim test. We first found a significant increase in the number and higher dendrite complexity, mainly with the doses of 2.5, 5 and 10 mg/kg of melatonin (81%, 122%, 78%). These cells showed more complex dendritic trees in the ventral- and the dorsal- DG. Concomitantly, the doses of 5 and 10 mg/kg of melatonin decreased depressant-like behavior (76%, 82%). Finally, the data corroborate the antidepressant-like effect of melatonin and the increasing number of doublecortin-associated cells. Besides, the data indicate that melatonin favors the number and dendrite complexity of DCX-cells in the dorsal- and ventral- region of the DG, which may explain part of the antidepressant-like effect of melatonin. Full article

(This article belongs to the Special Issue Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019)

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20 pages, 5619 KiB

Open AccessArticle

Melatonin-Induced Cytoskeleton Reorganization Leads to Inhibition of Melanoma Cancer Cell Proliferation

by Alejandro Alvarez-Artime, Rafael Cernuda-Cernuda, Francisco-Artime-Naveda, Vanesa Cepas, Pedro Gonzalez-Menendez, Sheila Fernadez-Vega, Isabel Quiros-Gonzalez, Rosa M. Sainz and Juan C. Mayo

Int. J. Mol. Sci. 2020, 21(2), 548; https://doi.org/10.3390/ijms21020548 - 15 Jan 2020

Cited by 38 | Viewed by 5127

Abstract

Neuroindole melatonin, a hormone synthesized during the night mainly—but not exclusively—by the pineal gland of all vertebrates, functions as an adapting signal to the light-dark cycle. Its antioxidant, neuroprotective, anti-inflammatory, and antitumor properties are all well-known and widely reported. Melanoma is one of the most common carcinomas among developed countries and a type of tumor particularly difficult to fight back in medium/advanced stages. In contrast to other types of cancer, influence of melatonin on melanoma has been scarcely investigated. Thus, we have chosen the murine melanoma model B16-F10 cell line to study antiproliferative and antitumoral actions of melatonin. For this purpose, we combined both, cell culture and in vivo models. Melatonin reduced either, growth rate or migration of B16-F10 cells. Furthermore, melanin synthesis was altered by melatonin, promoting its synthesis. Melatonin also induced a G2/M cell cycle arrest and altered the cytoskeletal organization. To corroborate these results, we tested the effect of melatonin in the in vivo model of B16-F10 cell injection in the tail vein, which causes numerous lung metastases. Two different strategies of melatonin administration were used, namely, in drinking water, or daily intraperitoneal injection. However, contrary to what occurred in cell culture, no differences were observed between control and melatonin treated groups. Results obtained led us to conclude that melatonin exerts an antiproliferative and anti-migrating effect on this melanoma model by interfering with the cytoskeleton organization, but this pharmacological effect cannot be translated in vivo as the indole did not prevent metastasis in the murine model, suggesting that further insights into the effects of the indole in melanoma cells should be approached to understand this apparent paradox. Full article

(This article belongs to the Special Issue Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019)

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17 pages, 2136 KiB

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Embryonic Ontogeny of 5-Hydroxyindoles and 5-Methoxyindoles Synthesis Pathways in the Goose Pineal Organ

by Maria Hanuszewska, Magdalena Prusik and Bogdan Lewczuk

Int. J. Mol. Sci. 2019, 20(16), 3948; https://doi.org/10.3390/ijms20163948 - 14 Aug 2019

Cited by 9 | Viewed by 3312

Abstract

The aim of this study was to characterize the embryonic ontogeny of 5-hydroxyindoles and 5-methoxyindoles synthesis pathways in the goose pineal organ. The study was performed on embryos aged 14–28 days, which have been incubated under a 12L:12D cycle. The pineal organs were collected for measurements of indole content by HPLC every 6 h on embryonic day (ED) 14, ED 16, ED 18 and ED 22 or every 2 h on ED 24, ED 26 and ED 28. The level of tryptophan showed no significant changes during development and no day-night variations. The content of 5-hydroxytryptophan increased between ED 14 and ED 26. It was significantly higher during scotophase than during photophase starting from ED 14. The serotonin content was low during the early stages of development (ED 14–ED 18) and prominently increased from ED 20. The serotonin levels also showed day-night differences; however, they were less conspicuous than those of 5-hydroxytryptophan. The changes in the level of 5-hydroxyindole acetic acid were similar to those of serotonin. 5-Hydroxytryptophol was measurable from ED 18. Levels of N-acetylserotonin, which were detectable for the first time on ED 16, prominently increased between ED 22 and ED 28 and showed significant day–night differences from ED 20. Melatonin was detectable from ED 18. Like N-acetylserotonin, its content increased rapidly between ED 22 and ED 28, and from ED 20 showed diurnal variations. 5-Methoxyindole acetic acid and 5-methoxytryptophol occurred at measurable levels from ED 18 and ED 26, respectively. The obtained results showed that embryonic development of indole metabolism in the goose pineal organ starts with the beginning of serotonin synthesis. The processes of serotonin acetylation and 5-hydroxyindoles methylation were turned on later. Diurnal rhythmicity develops very early in the embryonic pineal organ of the goose when the eggs are incubated under a 12 h light: 12 h dark schedule. Two processes are responsible for generation of the diurnal rhythms of 5-hydroxyindoles and 5-methoxyindoles: (i) hydroxylation of tryptophan and (ii) acetylation of serotonin. Full article

(This article belongs to the Special Issue Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019)

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22 pages, 7878 KiB

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Melatonin Abrogates the Anti-Developmental Effect of the AKT Inhibitor SH6 in Bovine Oocytes and Embryos

by Marwa El Sheikh, Ayman Mesalam, Ahmed Atef Mesalam, Muhammad Idrees, Kyeong-Lim Lee and Il-Keun Kong

Int. J. Mol. Sci. 2019, 20(12), 2956; https://doi.org/10.3390/ijms20122956 - 17 Jun 2019

Cited by 35 | Viewed by 6041

Abstract

Melatonin, a nighttime-secreted antioxidant hormone produced by the pineal gland, and AKT, a serine/threonine-specific protein kinase, have been identified as regulators for several cellular processes essential for reproduction. The current study aimed to investigate the potential interplay between melatonin and AKT in bovine oocytes in the context of embryo development. Results showed that the inclusion of SH6, a specific AKT inhibitor, during in vitro maturation (IVM) significantly reduced oocyte maturation, cumulus cell expansion, cleavage, and blastocyst development that were rescued upon addition of melatonin. Oocytes treated with SH6 in the presence of melatonin showed lower levels of reactive oxygen species (ROS) and blastocysts developed exhibited low apoptosis while the mitochondrial profile was significantly improved compared to the SH6-treated group. The RT-qPCR results showed up-regulation of the mRNA of maturation-, mitochondrial-, and cumulus expansion-related genes including GDF-9, BMP-15, MARF1, ATPase, ATP5F1E, POLG2, HAS2, TNFAIP6, and PTGS2 and down-regulation of Bcl-2 associated X apoptosis regulator (BAX), caspase 3, and p21 involved in apoptosis and cell cycle arrest in melatonin-SH6 co-treated group compared to SH6 sole treatment. The immunofluorescence showed high levels of caspase 3 and caspase 9, and low AKT phosphorylation in the SH6-treated group compared to the control and melatonin-SH6 co-treatment. Taken together, our results showed the importance of both melatonin and AKT for overall embryonic developmental processes and, for the first time, we report that melatonin could neutralize the deleterious consequences of AKT inhibition, suggesting a potential role in regulation of AKT signaling in bovine oocytes. Full article

(This article belongs to the Special Issue Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019)

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13 pages, 3072 KiB

Open AccessArticle

Melatonin Reduces Excitability in Dorsal Root Ganglia Neurons with Inflection on the Repolarization Phase of the Action Potential

by Klausen Oliveira-Abreu, Nathalia Maria Silva-dos-Santos, Andrelina Noronha Coelho-de-Souza, Francisco Walber Ferreira-da-Silva, Kerly Shamyra da Silva-Alves, Ana Carolina Cardoso-Teixeira, José Cipolla-Neto and José Henrique Leal-Cardoso

Int. J. Mol. Sci. 2019, 20(11), 2611; https://doi.org/10.3390/ijms20112611 - 28 May 2019

Cited by 11 | Viewed by 3246

Abstract

Melatonin is a neurohormone produced and secreted at night by pineal gland. Many effects of melatonin have already been described, for example: Activation of potassium channels in the suprachiasmatic nucleus and inhibition of excitability of a sub-population of neurons of the dorsal root ganglia (DRG). The DRG is described as a structure with several neuronal populations. One classification, based on the repolarizing phase of the action potential (AP), divides DRG neurons into two types: Without (N₀) and with (N_inf) inflection on the repolarization phase of the action potential. We have previously demonstrated that melatonin inhibits excitability in N₀ neurons, and in the present work, we aimed to investigate the melatonin effects on the other neurons (N_inf) of the DRG neuronal population. This investigation was done using sharp microelectrode technique in the current clamp mode. Melatonin (0.01–1000.0 nM) showed inhibitory activity on neuronal excitability, which can be observed by the blockade of the AP and by the increase in rheobase. However, we observed that, while some neurons were sensitive to melatonin effect on excitability (excitability melatonin sensitive—EMS), other neurons were not sensitive to melatonin effect on excitability (excitability melatonin not sensitive—EMNS). Concerning the passive electrophysiological properties of the neurons, melatonin caused a hyperpolarization of the resting membrane potential in both cell types. Regarding the input resistance (R_in), melatonin did not change this parameter in the EMS cells, but increased its values in the EMNS cells. Melatonin also altered several AP parameters in EMS cells, the most conspicuously changed was the (dV/dt)_max of AP depolarization, which is in coherence with melatonin effects on excitability. Otherwise, in EMNS cells, melatonin (0.1–1000.0 nM) induced no alteration of (dV/dt)_max of AP depolarization. Thus, taking these data together, and the data of previous publication on melatonin effect on N₀ neurons shows that this substance has a greater pharmacological potency on N_inf neurons. We suggest that melatonin has important physiological function related to N_inf neurons and this is likely to bear a potential relevant therapeutic use, since N_inf neurons are related to nociception. Full article

(This article belongs to the Special Issue Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019)

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11 pages, 989 KiB

Open AccessArticle

Melatonin Levels in Preterm and Term Infants and Their Mothers

by Valérie Biran, Fabrice Decobert, Nathalie Bednarek, Priscilla Boizeau, Jean-François Benoist, Bruno Claustrat, Jérôme Barré, Marina Colella, Alice Frérot, Roselyne Garnotel, Olivier Graesslin, Bassam Haddad, Jean-Marie Launay, Thomas Schmitz, Julien Schroedt, Anne-Laure Virlouvet, Sophie Guilmin-Crépon, Adyla Yacoubi, Evelyne Jacqz-Aigrain, Pierre Gressens, Corinne Alberti and Olivier Baud Show full author list Hide full author list

Int. J. Mol. Sci. 2019, 20(9), 2077; https://doi.org/10.3390/ijms20092077 - 27 Apr 2019

Cited by 43 | Viewed by 4926

Abstract

The prevention of perinatal brain damage following preterm birth remains a public health priority. Melatonin has been shown to be a promising neuroprotectant in neonatal preclinical models of brain damage, but few studies have investigated melatonin secretion in newborns. We hypothesized that melatonin circulating levels would be lower in preterm compared to term infants. We conducted a prospective, longitudinal, multicenter study to assess melatonin, and 6-sulfatoxy-melatonin (aMT6s) concentrations, measured by radioimmunoassay. Among 209 neonates recruited, 110 were born before 34 gestational weeks (GW) and 99 born after 34 GW. Plasma melatonin concentrations, measured at birth and on Day 3 were below detectable levels (≤7 pg/mL) in 78% and 81%, respectively, of infants born before 34 GW compared to 57% and 34%, respectively, of infants born after 34 GW. The distribution of plasma melatonin concentrations was found to be correlated with gestational age at both time-points (p < 0.001). Median urine aMT6s concentrations were significantly lower in infants born before 34 GW, both on Day 1 (230 ng/L vs. 533 ng/L, p < 0.0001) and on Day 3 (197 ng/L vs. 359 ng/L, p < 0.0001). In conclusion, melatonin secretion appears very low in preterm infants, providing the rationale for testing supplemental melatonin as a neuroprotectant in clinical trials. Full article

(This article belongs to the Special Issue Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019)

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Review

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Open AccessReview

Importance of Melatonin in Assisted Reproductive Technology and Ovarian Aging

by Hiroshi Tamura, Mai Jozaki, Manabu Tanabe, Yuichiro Shirafuta, Yumiko Mihara, Masahiro Shinagawa, Isao Tamura, Ryo Maekawa, Shun Sato, Toshiaki Taketani, Akihisa Takasaki, Russel J. Reiter and Norihiro Sugino

Int. J. Mol. Sci. 2020, 21(3), 1135; https://doi.org/10.3390/ijms21031135 - 8 Feb 2020

Cited by 138 | Viewed by 16583

Abstract

Melatonin is probably produced in all cells but is only secreted by the pineal gland. The pineal secretion of melatonin is determined by the light–dark cycle, and it is only released at night. Melatonin regulates biological rhythms via its receptors located in the suprachiasmatic nuclei of the hypothalamus. Melatonin also has strong antioxidant activities to scavenge free radicals such as reactive oxygen species (ROS). The direct free radical scavenging actions are receptor independent. ROS play an important role in reproductive function including in the ovulatory process. However, excessive ROS can also have an adverse effect on oocytes because of oxidative stress, thereby causing infertility. It is becoming clear that melatonin is located in the ovarian follicular fluid and in the oocytes themselves, which protects these cells from oxidative damage as well as having other beneficial actions in oocyte maturation, fertilization, and embryo development. Trials on humans have investigated the improvement of outcomes of assisted reproductive technology (ART), such as in vitro fertilization and embryo transfer (IVF-ET), by way of administering melatonin to patients suffering from infertility. In addition, clinical research has examined melatonin as an anti-aging molecule via its antioxidative actions, and its relationship with the aging diseases, e.g., Alzheimer’s and Parkinson’s disease, is also underway. Melatonin may also reduce ovarian aging, which is a major issue in assisted reproductive technology. This review explains the relationship between melatonin and human reproductive function, as well as the clinical applications expected to improve the outcomes of assisted reproductive technology such as IVF, while also discussing possibilities for melatonin in preventing ovarian aging. Full article

(This article belongs to the Special Issue Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019)

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17 pages, 941 KiB

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Melatonin Mediates Enhancement of Stress Tolerance in Plants

by Biswojit Debnath, Waqar Islam, Min Li, Yueting Sun, Xiaocao Lu, Sangeeta Mitra, Mubasher Hussain, Shuang Liu and Dongliang Qiu

Int. J. Mol. Sci. 2019, 20(5), 1040; https://doi.org/10.3390/ijms20051040 - 27 Feb 2019

Cited by 184 | Viewed by 9850

Abstract

Melatonin is a multifunctional signaling molecule, ubiquitously distributed in different parts of plants and responsible for stimulating several physiological responses to adverse environmental conditions. In the current review, we showed that the biosynthesis of melatonin occurred in plants by themselves, and accumulation of melatonin fluctuated sharply by modulating its biosynthesis and metabolic pathways under stress conditions. Melatonin, with its precursors and derivatives, acted as a powerful growth regulator, bio-stimulator, and antioxidant, which delayed leaf senescence, lessened photosynthesis inhibition, and improved redox homeostasis and the antioxidant system through a direct scavenging of reactive oxygen species (ROS) and reactive nitrogen species (RNS) under abiotic and biotic stress conditions. In addition, exogenous melatonin boosted the growth, photosynthetic, and antioxidant activities in plants, confirming their tolerances against drought, unfavorable temperatures, salinity, heavy metals, acid rain, and pathogens. However, future research, together with recent advancements, would support emerging new approaches to adopt strategies in overcoming the effect of hazardous environments on crops and may have potential implications in expanding crop cultivation against harsh conditions. Thus, farming communities and consumers will benefit from elucidating food safety concerns. Full article

(This article belongs to the Special Issue Melatonin from an Antioxidant to a Classic Hormone or a Tissue Factor: Experimental and Clinical Aspects 2019)

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