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70 Years of Oxytocin: Updates on Groundbreaking Findings 70 Years after the Discovery of Oxytocin

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

Deadline for manuscript submissions: closed (20 April 2024) | Viewed by 11558

Special Issue Editor

Dr. Claudia Camerino

E-Mail Website
Guest Editor
Department of Precision and Regenerative Medicine, School of Medicine, University of Bari Aldo Moro, P.za G. Cesare 11, 70100 Bari, Italy
Interests: oxytocin; thermoregulation; skeletal muscle; obesity; Prader–Willi syndrome
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

The discovery of the pituitary neurohormone oxytocin led to the 1955 Nobel Prize in Chemistry being awarded to Vincent du Vigneaud. This represented the culmination of a research programme dating back to 1895, when Oliver and Schafer reported that a substance extracted from the pituitary gland elevates blood pressure when intravenously injected into dogs. Dale later reported on a neurohypophysial substance that triggers uterine contraction, stimulates lactation, and functions in antidiuresis. Purification of the pituitary gland extracts revealed that the vasopressor and antidiuretic activity could be attributed to one substance, vasopressin, and the uterotonic and lactation-promoting activity could be attributed to another substance, oxytocin. In 1950, the amino acid sequences of vasopressin and oxytocin were determined, and both peptides were chemically synthesised. This revealed that vasopressin (CYFQNCPRG-NH2) and oxytocin (CYIQNCPLG-NH2) are structurally very similar, with only two amino acids differing, which is indicative of their common evolutionary origin, and a disulphide bridge between the cysteine residues at positions 1 and 6 conserved in all vasopressin/oxytocin-type peptides. This characterisation and discovery of oxytocin led to the Nobel Prize being awarded to Vincent du Vigneaud in 1955. The common evolutionary origin of vasopressin and oxytocin, as indicated by their structural similarity, dates back to millions of years ago, which suggests that oxytocin has effects that go beyond uterine contractions and pregnancy. Nevertheless, such evidence was uncovered only 50 years after its discovery, in early 2000, when mice depleted of either oxytocin or its receptor were observed to develop late onset obesity and metabolic syndrome, thus establishing the involvement of oxytocin in the regulation of energy and metabolism. Interestingly, the metabolic phenotype of oxytocin and oxytocin receptor-deficient mice diverges in young versus older animals, taking time to reach full force, and is established in the absence of hyperphagia. The effects of oxytocin on fat and energy are both direct, since oxytocin is anorexigenic, and indirect, when oxytocin regulates the lean/fat mass composition in skeletal muscle, potentiating the the slow twitch muscle as it does in the uterus. Finally, while oxytocin negatively modulates adipogenesis, peripheral oxytocin promotes osteoblast differentiation and function, leading to increased bone formation through the direct effect of oxytocin binding to its receptor on osteoblasts. Connecting the dots downstream of these findings, it appears that oxytocin acts on the three components of body composition: fat, muscle, and bone. Evolutionarily, the anabolic effect of oxytocin, makes sense since oxytocin concentrations increase during challenging situations, including pregnancy and lactation in mammals, and triggers aggressive behaviour that, in females, is important for the protection of offspring after labour, when they are most vulnerable to predators, and plasma oxytocin concentration is at its peak. Taking a wider perspective, this demonstrates that the effects of oxytocin are beneficial in the management of osteoporosis, body fat gain, diabetes, sarcopenia, and all age-related diseases affecting elderly men and women, indicating the exciting therapeutic potential but also challenges, namely to find a single route, dosage, and schedule able to reach all the targets. Thus, let this be a mission that could be celebrated in 2055: the 100th anniversary of oxytocin’s discovery. Meanwhile, with this Special Issue here and now, we invite all colleagues that have made significant contributions to the studies of oxytocin in recent years to contribute with reviews or original research articles.

Dr. Claudia Camerino
Guest Editor

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Keywords

  • oxytocin
  • energy
  • metabolism
  • metabolic syndrome
  • skeletal muscle
  • bone
  • Prader–Willi syndrome
  • autism
  • body composition
  • thermoregulation

Published Papers (5 papers)

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Research

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25 pages, 10050 KiB  
Article
Oxytocin Modulates Osteogenic Commitment in Human Adipose-Derived Stem Cells
by Giovannamaria Petrocelli, Provvidenza Maria Abruzzo, Luca Pampanella, Riccardo Tassinari, Serena Marini, Elena Zamagni, Carlo Ventura, Federica Facchin and Silvia Canaider
Int. J. Mol. Sci. 2023, 24(13), 10813; https://doi.org/10.3390/ijms241310813 - 28 Jun 2023
Cited by 1 | Viewed by 959
Abstract
Human adipose-derived stem cells (hASCs) are commonly harvested in minimally invasive contexts with few ethical concerns, and exhibit self-renewal, multi-lineage differentiation, and trophic signaling that make them attractive candidates for cell therapy approaches. The identification of natural molecules that can modulate their biological [...] Read more.
Human adipose-derived stem cells (hASCs) are commonly harvested in minimally invasive contexts with few ethical concerns, and exhibit self-renewal, multi-lineage differentiation, and trophic signaling that make them attractive candidates for cell therapy approaches. The identification of natural molecules that can modulate their biological properties is a challenge for many researchers. Oxytocin (OXT) is a neurohypophyseal hormone that plays a pivotal role in the regulation of mammalian behavior, and is involved in health and well-being processes. Here, we investigated the role of OXT on hASC proliferation, migratory ability, senescence, and autophagy after a treatment of 72 h; OXT did not affect hASC proliferation and migratory ability. Moreover, we observed an increase in SA-β-galactosidase activity, probably related to the promotion of the autophagic process. In addition, the effects of OXT were evaluated on the hASC differentiation ability; OXT promoted osteogenic differentiation in a dose-dependent manner, as demonstrated by Alizarin red staining and gene/protein expression analysis, while it did not affect or reduce adipogenic differentiation. We also observed an increase in the expression of autophagy marker genes at the beginning of the osteogenic process in OXT-treated hASCs, leading us to hypothesize that OXT could promote osteogenesis in hASCs by modulating the autophagic process. Full article
(This article belongs to the Special Issue 70 Years of Oxytocin: Updates on Groundbreaking Findings 70 Years after the Discovery of Oxytocin)
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9 pages, 541 KiB  
Communication
Serum Oxytocin Levels Decrease 12 Months Following Sleeve Gastrectomy and Are Associated with Decreases in Lean Mass
by Imen Becetti, Vibha Singhal, Supritha Nimmala, Hang Lee, Elizabeth A. Lawson, Miriam A. Bredella and Madhusmita Misra
Int. J. Mol. Sci. 2023, 24(12), 10144; https://doi.org/10.3390/ijms241210144 - 14 Jun 2023
Cited by 2 | Viewed by 990
Abstract
Oxytocin (OXT), an anorexigenic hormone, is also bone anabolic. Further, OXT administration results in increases in lean mass (LM) in adults with sarcopenic obesity. We examine, for the first time, associations of OXT with body composition and bone endpoints in 25 youth 13–25 [...] Read more.
Oxytocin (OXT), an anorexigenic hormone, is also bone anabolic. Further, OXT administration results in increases in lean mass (LM) in adults with sarcopenic obesity. We examine, for the first time, associations of OXT with body composition and bone endpoints in 25 youth 13–25 years old with severe obesity who underwent sleeve gastrectomy (SG) and 27 non-surgical controls (NS). Forty participants were female. Subjects underwent fasting blood tests for serum OXT and DXA for areal bone mineral density (aBMD) and body composition. At baseline, SG vs. NS had higher median body mass index (BMI) but did not differ for age or OXT levels. Over 12 months, SG vs. NS had greater reductions in BMI, LM, and fat mass (FM). OXT decreased in SG vs. NS 12 months post-SG. While baseline OXT predicted a 12-month BMI change in SG, decreases in OXT levels 12 months post-SG were not associated with decreases in weight or BMI. In SG, decreases in OXT were positively associated with decreases in LM but not with decreases in FM or aBMD. Loss of LM, a strong predictor of BMD, after bariatric surgery may reduce functional and muscular capacity. OXT pathways may be targeted to prevent LM loss following SG. Full article
(This article belongs to the Special Issue 70 Years of Oxytocin: Updates on Groundbreaking Findings 70 Years after the Discovery of Oxytocin)
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13 pages, 2751 KiB  
Article
Highly Specific Detection of Oxytocin in Saliva
by Muhit Rana, Nimet Yildirim, Nancy E. Ward, Stephanie P. Vega, Michael J. Heffernan and Avni A. Argun
Int. J. Mol. Sci. 2023, 24(5), 4832; https://doi.org/10.3390/ijms24054832 - 02 Mar 2023
Cited by 3 | Viewed by 3037
Abstract
Oxytocin is a peptide neurophysin hormone made up of nine amino acids and is used in induction of one in four births worldwide (more than 13 percent in the United States). Herein, we have developed an antibody alternative aptamer-based electrochemical assay for real-time [...] Read more.
Oxytocin is a peptide neurophysin hormone made up of nine amino acids and is used in induction of one in four births worldwide (more than 13 percent in the United States). Herein, we have developed an antibody alternative aptamer-based electrochemical assay for real-time and point-of-care detection of oxytocin in non-invasive saliva samples. This assay approach is rapid, highly sensitive, specific, and cost-effective. Our aptamer-based electrochemical assay can detect as little as 1 pg/mL of oxytocin in less than 2 min in commercially available pooled saliva samples. Additionally, we did not observe any false positive or false negative signals. This electrochemical assay has the potential to be utilized as a point-of-care monitor for rapid and real-time oxytocin detection in various biological samples such as saliva, blood, and hair extracts. Full article
(This article belongs to the Special Issue 70 Years of Oxytocin: Updates on Groundbreaking Findings 70 Years after the Discovery of Oxytocin)
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12 pages, 1988 KiB  
Article
Mechanism of Oxytocin-Induced Contraction in Rat Gastric Circular Smooth Muscle
by Mohammad Alqudah, Rima Abdul Razzaq, Mahmoud A. Alfaqih, Othman Al-Shboul, Ahmed Al-Dwairi and Safa Taha
Int. J. Mol. Sci. 2023, 24(1), 441; https://doi.org/10.3390/ijms24010441 - 27 Dec 2022
Viewed by 2116
Abstract
Oxytocin produces an excitatory effect on gastric muscle through the activation of receptors present on stomach smooth muscle cells. However, the intracellular mechanisms that mediate oxytocin excitatory effects are still largely unknown. Therefore, we aimed to investigate the signaling pathways involved in oxytocin-induced [...] Read more.
Oxytocin produces an excitatory effect on gastric muscle through the activation of receptors present on stomach smooth muscle cells. However, the intracellular mechanisms that mediate oxytocin excitatory effects are still largely unknown. Therefore, we aimed to investigate the signaling pathways involved in oxytocin-induced contractions in gastric smooth muscle, shedding light on phospholipase C (PLC)-β1 signaling and its downstream molecules, including inositol 1,4,5- trisphosphate (IP3) and myosin light chain kinase (MLCK). The contractions of gastric smooth muscle from male rats were measured in an organ bath set up in response to exogenous oxytocin 10−7 M, in the presence and absence of inhibitors of the indicated signaling molecules. Oxytocin (10−9–10−5 M) induced dose-dependent stomach smooth muscle contraction. Pre-incubation with atosiban, an oxytocin receptor inhibitor, abolished the oxytocin-induced contraction. Moreover, PLC β1 inhibitor (U73122) and IP3 inhibitor Xestospongin C inhibited oxytocin-induced muscle contraction to various degrees. Verapamil, a calcium channel blocker, inhibited oxytocin-induced contraction, and pre-incubation of the strips, with both verapamil and Xestospongin C, further inhibited the excitatory effect of oxytocin. Chelation of intracellular calcium with BAPT-AM (1,2-bis-(o-aminophenoxy) ethane-N,N,N′,N′-tetraacetic acid) significantly inhibited the effect of oxytocin on muscle contraction. Finally, pre-incubation of the strips with the Ca2+/calmodulin-dependent protein kinase selective inhibitor STO-609 significantly inhibited the contraction induced by oxytocin. These results suggest that oxytocin directly stimulates its cell surface receptor to activate PLC β1, which in turn liberates IP3, which eventually elevates intracellular calcium, the prerequisite for smooth muscle contraction. Full article
(This article belongs to the Special Issue 70 Years of Oxytocin: Updates on Groundbreaking Findings 70 Years after the Discovery of Oxytocin)
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Review

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17 pages, 940 KiB  
Review
The Long Way of Oxytocin from the Uterus to the Heart in 70 Years from Its Discovery
by Claudia Camerino
Int. J. Mol. Sci. 2023, 24(3), 2556; https://doi.org/10.3390/ijms24032556 - 29 Jan 2023
Cited by 7 | Viewed by 3502
Abstract
The research program on oxytocin started in 1895, when Oliver and Schafer reported that a substance extracted from the pituitary gland elevates blood pressure when injected intravenously into dogs. Dale later reported that a neurohypophysial substance triggers uterine contraction, lactation, and antidiuresis. Purification [...] Read more.
The research program on oxytocin started in 1895, when Oliver and Schafer reported that a substance extracted from the pituitary gland elevates blood pressure when injected intravenously into dogs. Dale later reported that a neurohypophysial substance triggers uterine contraction, lactation, and antidiuresis. Purification of this pituitary gland extracts revealed that the vasopressor and antidiuretic activity could be attributed to vasopressin, while uterotonic and lactation activity could be attributed to oxytocin. In 1950, the amino-acid sequences of vasopressin and oxytocin were determined and chemically synthesized. Vasopressin (CYFQNCPRG-NH2) and oxytocin (CYIQNCPLG-NH2) differ by two amino acids and have a disulfide bridge between the cysteine residues at position one and six conserved in all vasopressin/oxytocin-type peptides. This characterization of oxytocin led to the Nobel Prize awarded in 1955 to Vincent du Vigneaud. Nevertheless, it was only 50 years later when the evidence that mice depleted of oxytocin or its receptor develop late-onset obesity and metabolic syndrome established that oxytocin regulates energy and metabolism. Oxytocin is anorexigenic and regulates the lean/fat mass composition in skeletal muscle. Oxytocin’s effect on muscle is mediated by thermogenesis via a pathway initiated in the myocardium. Oxytocin involvement in thermogenesis and muscle contraction is linked to Prader-Willi syndrome in humans, opening exciting therapeutic avenues. Full article
(This article belongs to the Special Issue 70 Years of Oxytocin: Updates on Groundbreaking Findings 70 Years after the Discovery of Oxytocin)
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