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Mechanisms of Nausea and Vomiting: Current Knowledge and Recent Advances in Intracellular Emetic Signaling Systems

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Mechanisms of Nausea and Vomiting: Current Knowledge and Recent Advances in Intracellular Emetic Signaling Systems International Journal of Molecular Sciences Review Mechanisms of Nausea and Vomiting: Current Knowledge and Recent Advances in Intracellular Emetic Signaling Systems Weixia Zhong 1, Omar Shahbaz 2, Garrett Teskey 1, Abrianna Beever 3, Nala Kachour 3, Vishwanath Venketaraman 1,3 and Nissar A. Darmani 1,* 1 Department of Basic Medical Sciences, College of Osteopathic Medicine of the Pacific, Western University of Health Sciences, 309 East Second Street, Pomona, CA 91766, USA; [email protected] (W.Z.); [email protected] (G.T.); [email protected] (V.V.) 2 School of Medicine, Universidad Iberoamericana, Av. Francia 129, Santo Domingo 10203, Dominican Republic; [email protected] 3 Graduate College of Biomedical Sciences, Western University of Health Sciences, Pomona, CA 91766, USA; [email protected] (A.B.); [email protected] (N.K.) * Correspondence: [email protected]; Tel.: +1-909-469-5654 Abstract: Nausea and vomiting are common gastrointestinal complaints that can be triggered by diverse emetic stimuli through central and/or peripheral nervous systems. Both nausea and vomiting are considered as defense mechanisms when threatening toxins/drugs/bacteria/viruses/fungi enter the body either via the enteral (e.g., the gastrointestinal tract) or parenteral routes, including the blood, skin, and respiratory systems. While vomiting is the act of forceful removal of gastrointestinal contents, nausea is believed to be a subjective sensation that is more difficult to study in nonhuman species. In this review, the authors discuss the anatomical structures, neurotransmitters/mediators, Citation: Zhong, W.; Shahbaz, O.; and corresponding receptors, as well as intracellular emetic signaling pathways involved in the Teskey, G.; Beever, A.; Kachour, N.; processes of nausea and vomiting in diverse animal models as well as humans. While blockade Venketaraman, V.; Darmani, N.A. of emetic receptors in the prevention of vomiting is fairly well understood, the potential of new Mechanisms of Nausea and Vomiting: classes of antiemetics altering postreceptor signal transduction mechanisms is currently evolving, Current Knowledge and Recent which is also reviewed. Finally, future directions within the field will be discussed in terms of Advances in Intracellular Emetic Signaling Systems. Int. J. Mol. Sci. important questions that remain to be resolved and advances in technology that may help provide 2021, 22, 5797. https://doi.org/ potential answers. 10.3390/ijms22115797 Keywords: nausea; vomiting; emesis; G-protein coupled receptors; signaling pathway; Ca2+; brain- Academic Editor: Henrique Girao stem; the gastrointestinal tract Received: 6 April 2021 Accepted: 21 May 2021 Published: 28 May 2021 1. Introduction Nausea and vomiting are essential protective defense processes by which humans as Publisher’s Note: MDPI stays neutral well as vomit-competent animals tend to avoid ingestion and/or digestion of potentially with regard to jurisdictional claims in toxic substances. Nausea is the unpleasant sensation of having the urge to vomit, whereas published maps and institutional affil- vomiting (emesis) is a physical event and is the forceful expulsion of intestinal and gastric iations. contents through the mouth [1]. Vomiting is often preceded by retching, where the content of gastrointestinal tract is forced into the esophagus, without expulsion of the vomitus [1]. Oftentimes, nausea and vomiting occur on a temporal continuum, but this is not always the case. Sometimes, severe nausea can be present without emesis, and, less frequently, Copyright: © 2021 by the authors. vomiting may be present without nausea. Thus, nausea is no longer considered only a Licensee MDPI, Basel, Switzerland. penultimate step of vomiting [2]. This article is an open access article Nausea and vomiting can be triggered by several mechanisms, as depicted in Figure1 , distributed under the terms and including: (i) toxins/drugs/bacteria/viruses/fungi that enter the lumen of the gastroin- conditions of the Creative Commons testinal and, subsequently, indirectly stimulate the brainstem emetic nuclei located in the Attribution (CC BY) license (https:// dorsal vagal complex via release of local emetic neurotransmitters in the upper gastroin- creativecommons.org/licenses/by/ 4.0/). testinal tract and subsequent activation of corresponding receptors present on vagus nerves Int. J. Mol. Sci. 2021, 22, 5797. https://doi.org/10.3390/ijms22115797 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 34 Int. J. Mol. Sci. 2021, 22, 5797 2 of 33 dorsal vagal complex via release of local emetic neurotransmitters in the upper gastroin- testinal tract and subsequent activation of corresponding receptors present on vagus and/ornerves splanchnic and/or splanchnic nerves; nerves; (ii) toxic (ii) toxic agents/drugs agents/drugs or or infectious infectious organisms organisms that enter enter the bodythe body systemically systemically and and that that may may act act directly directly on on the the dorsal dorsal vagalvagal complex emetic emetic nuclei nuclei in thein brainstem; the brainstem; (iii) (iii) pathologies pathologies in in the the gastrointestinal gastrointestinal tract, tract, whichwhich stimulate vagal vagal affer- afferents orents other or visceral other visceral organs organs (e.g., cardiac), (e.g., cardiac), which which stimulate stimulate visceral visceral afferents; afferents; (iv)emotional (iv) emo- and cognitivetional and stimuli cognitive within stimuli the centralwithin the nervous central system nervous (CNS), system including (CNS), including cerebral cerebral cortex and thecortex limbic and system; the limbic and system; (v) disturbances and (v) disturbanc of the vestibulares of the vestibular nuclei and nuclei cerebellum and cerebellum in motion sicknessin motion [3– 8sickness]. The processes [3–8]. The ofprocesses nausea andof nausea vomiting and vomiting result from result continuous from continuous interactions interactions between the gastrointestinal tract, including its enteric nervous system, the between the gastrointestinal tract, including its enteric nervous system, the CNS, and the CNS, and the autonomic nervous system [9,10]. autonomic nervous system [9,10]. Figure 1. Central and peripheral anatomical sites involved in nausea and vomiting induced by various stimuli. Nausea and vomitingFigure 1. Central can be and generated peripheral by diverseanatomical stimuli sites involved and are mediatedin nausea and by thevomiting bidirectional induced interactionby various stimuli. between Nausea brain and and vomiting can be generated by diverse stimuli and are mediated by the bidirectional interaction between brain and gut. In brief: (1) The brainstem area postrema in the floor of the fourth ventricle lacks blood brain barrier and thus serves gut. In brief: (1) The brainstem area postrema in the floor of the fourth ventricle lacks blood brain barrier and thus serves as directas direct central central receptor receptor sites sites for for circulating circulating and and systemic systemic emeticemetic stimuli stimuli in in the the cerebrospinal cerebrospinal fluid fluid and and the blood the blood [11]. [(2)11 ]. (2) SystemicallySystemically administered administered drugs drugs can can activate activate corresponding corresponding receptors present present on on vagal vagal afferents, afferents, which which project project sensory sensory signalssignals to the to nucleusthe nucleus of theof the solitary solitary tract tract [11 [11,12].,12]. (3) (3) PeripheralPeripheral stimuli stimuli such such as as toxic toxic drugs drugs and and microbials microbials (e.g., (e.g., bacteria bacteria,, viruses,viruses, fungi) fungi) that enterthat enter the lumenthe lumen of the of gastrointestinalthe gastrointestinal tract tract (GIT) (GIT) and and pathologies pathologies in thein the GIT GIT cause cause release release of of local local emetic emetic neurotransmitters/modulators, which subsequently act on the corresponding receptors present on vagal afferents neurotransmitters/modulators, which subsequently act on the corresponding receptors present on vagal afferents and/or and/or stimulate the brainstem area postrema via circulating blood [9,10]. Besides the area postrema and the sensory vagal stimulateafferents, the brainstem the nucleus area of the postrema solitary tract via circulating is also the recipient blood [9 of:,10 (i)]. Besidesdirect neural the area inputs postrema from the and splanchnic the sensory nerves vagal carrying afferents, the nucleus of the solitary tract is also the recipient of: (i) direct neural inputs from the splanchnic nerves carrying sensation caused by diseases of visceral organs (e.g., cardiac, kidney); (ii) brainstem vestibular nuclei collecting signals from vestibular apparatus in inner ear and/or cerebellum, caused by stimuli related to motion sickness and opioid analgesics [13,14]; and (iii) the cerebral cortex and limbic system, which accept and process emotional and cognitive stimuli [3–8]. The nucleus of the solitary tract has output pathways to the dorsal motor nucleus of the vagus, which further project to the upper gastrointestinal tract to produce the vomiting reflex [11]. In addition, the nucleus of the solitary tract has projections to the mid- and forebrain for the perception of nausea [15]. Int. J. Mol. Sci. 2021, 22, 5797 3 of 33 In this article, we will initially describe the underlying neuroanatomical, neurochemi- cal, and receptor basis of diverse causes of nausea
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