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A nicotinic hypothesis for Covid-19 with preventive and therapeutic implications
[Une hypothèse nicotinique pour Covid 19 et ses implications préventives et thérapeutiques]
Comptes Rendus. Biologies, Volume 343 (2020) no. 1, pp. 33-39.

Résumés

SARS-CoV-2 epidemics raises a considerable issue of public health at the planetary scale. There is a pressing urgency to find treatments based upon currently available scientific knowledge. Therefore, we tentatively propose a hypothesis which hopefully might ultimately help save lives. Based on the current scientific literature and on new epidemiological data which reveal that current smoking status appears to be a protective factor against the infection by SARS-CoV-2 [1], we hypothesize that the nicotinic acetylcholine receptor (nAChR) plays a key role in the pathophysiology of Covid-19 infection and might represent a target for the prevention and control of Covid-19 infection.

L’épidémie de SARS-Cov-2 pose un problème considérable de santé publique à l’échelle planétaire. Il y a urgence extrême de découvrir des traitements qui se fondent sur les connaissances scientifiques disponibles. Nous proposons donc une hypothèse plausible mais provisoire qui puisse le moment venu contribuer à sauver des vies. Elle se fonde sur la littérature scientifique disponible et sur des données épidémiologiques nouvelles qui révèlent que le statut de fumeur parait être un facteur de protection contre l’infection par SARS-Cov-2 [1]. Nous proposons l’hypothèse que le récepteur nicotinique de l’acétylcholine (nAChR) joue un rôle critique dans la pathophysiologie de l’infection Covid-19 et puisse représenter une cible pour la prévention et le contrôle de l’infection.

Métadonnées
Reçu le :
Accepté le :
Publié le :
DOI : 10.5802/crbiol.8
Keywords: Covid-19, smoking, nicotinic receptors, clinical trials of nicotine patches
Mots-clés : Covid-19, fumeurs, récepteurs nicotinique, essais clinique patch nicotine

Jean-Pierre Changeux 1 ; Zahir Amoura 2, 3 ; Felix A. Rey 4 ; Makoto Miyara 2, 5

1 Institut Pasteur CNRS UMR 3571 Department of Neuroscience and Collège de France, Paris France
2 Sorbonne Université, Inserm UMRS, Centre d’Immunologie et des Maladies Infectieuses (CIMI-Paris)
3 Assistance Publique-Hôpitaux de Paris, Groupement Hospitalier Pitié-Salpêtrière, Service de Médecine Interne 2, Maladies auto-immune et systémiques Institut E3M
4 Institut Pasteur, Structural Virology Unit, Department of Virology, CNRS UMR 3569, Institut Pasteur Paris France
5 Assistance Publique-Hôpitaux de Paris, Groupement Hospitalier Pitié-Salpêtrière, Département d’Immunologie, Paris, France
Licence : CC-BY 4.0
Droits d'auteur : Les auteurs conservent leurs droits
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     title = {A nicotinic hypothesis for {Covid-19} with preventive and therapeutic implications},
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     pages = {33--39},
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Jean-Pierre Changeux; Zahir Amoura; Felix A. Rey; Makoto Miyara. A nicotinic hypothesis for Covid-19 with preventive and therapeutic implications. Comptes Rendus. Biologies, Volume 343 (2020) no. 1, pp. 33-39. doi : 10.5802/crbiol.8. https://comptes-rendus.academie-sciences.fr/biologies/articles/10.5802/crbiol.8/

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Symptomatic Covid-19 disease (as caused by SARS-CoV-2 virus) is observed in 2.5 percent of infected individuals [2] indicating an individual variability in the clinical presentation. Among the epidemiological and clinical features of Covid-19, the following features are of special interest for understanding the patho-physiolology, namely: (1) in outpatients with favorable outcome : neurological/psychiatric disorders, especially loss of sense of smell which is specific of the disease and (2) in hospitalized older patients with a poor prognosis : systemic hyperinflammatory syndrome with increased levels of circulating cytokines and atypical acute respiratory distress syndrome with loss of neurological control of lung perfusion regulation and hypoxic vasoconstriction [3]. This raises the issue of the basis of inter-individual variability for the susceptibility to infection.

The nAChR appears as a hypothetical clue for the main clinical manifestations of Covid-19. It is accepted that the angiotensin converting enzyme 2 (ACE2), represents the principal receptor molecule for SARS-CoV-2 [4, 5, 6]. ACE2 is expressed at the transcriptomic level in the lung, the small intestine and colon, in the kidney, in the testis, in the heart muscle and in the brain, yet the protein is not detected in the lung [7]. In the brain, ACE2 is expressed in both neurons and glia and particularly present in the brain stem and in the regions responsible for the regulation of cardiovascular functions, including the subfornical organ, paraventricular nucleus, nucleus of the tractus solitarius, and rostral ventrolateral medulla [8]. Additional receptors or co-receptors are, however, not excluded. The relationship between nicotine and ACE2 has been explored in the framework of cardiovascular and pulmonary diseases [9]. Accordingly, in the ACE/ANG II/AT1R arm, nicotine increases the expression and/or activity of renin, ACE and AT1R, whereas in the compensatory ACE2/ANG-(1–7)/MasR arm, nicotine down regulates the expression and/or activity of ACE2 and AT2R, thus suggesting a possible contribution of acetylcholine receptors in ACE2 regulation. This possibility has not yet been explored in the framework of viral neuroinfections.

There is strong evidence for a neurotropic action of SARS-CoV-2 infection. It has been demonstrated that β-coronaviruses to which the SARS-CoV-2 belongs, do not limit their presence to the respiratory tract and have been shown to frequently invade the CNS [10]. This propensity has been convincingly documented for the SARS-CoV-1, MERS-CoV and the coronavirus responsible for porcine hemagglutinating encephalomyelitis (HEV 67N). In light of the high similarity between SARS-CoV-1 and SARS-CoV-2, it is quite likely that SARS-CoV-2 also possesses a similar potential. Neuroinfection has been proposed to potentially contribute to the pathophysiology and clinical manifestations of Covid-19 [10] with the neuroinvasive potential of SARS-CoV-2 suggested to play a role in the respiratory failure of Covid-19 patients [11, 12]. Our nicotinic hypothesis proposes that the virus could enter the body through neurons of the olfactory system and/or through the lung leading to different clinical features with different outcome, and contrasts with the currently accepted view that ACE2 is the principal receptor of SARS-CoV-2 for its entry into cells.

As mentioned, loss of sense of smell frequently occurs in Covid-19 patients [13]. Furthermore, several studies have reported that some patients infected with SARS-CoV-2 show neurologic signs such as headache (about 8 %), nausea and vomiting (1 %) [11]. More recently, a study of 214 Covid-19 patients [14] further found that about 88 % (78/88) of the severe patients displayed neurologic manifestations including acute cerebrovascular diseases and impaired consciousness. Based on an epidemiological survey on Covid-19, the median time from the first symptom to dyspnea was 5.0 days, to hospital admission was 7.0 days, and to the intensive care was 8.0 days [15]. Therefore, the latency period may be adequate for the virus to enter the nervous system, invade the brain stem and affect the medullary neurons of the respiratory centers. However, variability of the neurological signs was observed with patients having anosmia, showing in general a mild evolution without pulmonary attack, in contrast with those without anosmia suggesting a diversity in the mode of proliferation and /or progression of the virus.

More than 20 years ago, Mohammed, Norrby & Kristensson [16], in a pioneering study, showed with a broad diversity of viruses (Poliovirus, Herpes simplex virus, West Nile virus , Vesicular Stomatitis Virus, influenza H1N1 virus [17]), that viruses enter the olfactory epithelium and progress first through the olfactory pathway in an anterograde direction and then in a retrograde manner to the reticular neurons projecting to the olfactory bulbs, the median raphe neurons (serotoninergic) and the ventral and horizontal diagonal band (cholinergic) [16, 18]. This olfactory infection route scheme [18] has been recently extended to Covid-19 infection [2, 11]. To further investigate the molecular aspects of Covid-19 propagation in the brain and its pharmacology, we have been aided by abundant studies on rabies virus (RABV) a negative polarity, single-strand RNA virus that is distinct from the coronaviruses [18, 19, 20]. nAChRs were shown to be the first receptors for RABV [21]. Structural studies further revealed that a short region in the ectodomain of the rabies virus glycoprotein shows sequence similarity to some snake toxins [20, 22] that were initially used to isolate the nAChR from fish electric organs [23]. These snake toxins [24] are known to bind with high affinity and exquisite selectivity to the peripheral muscle receptor, while also to some brain receptors [25, 26]. The neurotoxin-like region of the rabies virus glycoprotein inhibited acetylcholine responses of α4β2 nAChRs in vitro, as did the full length ectodomain of the rabies virus glycoprotein [20]. The same peptides significantly altered a nAChR elicited behaviour in C. elegans and increased locomotor activity levels when injected into the CNS of mice [20]. The nAChR thus plays a critical role in the host-pathogen interaction in the case of the RABV. Furthermore, a broad variety of nAChR oligomers are distributed throughout the brain, including the reticular core neurons and the spinal cord, with the α4β2 and α7 nAChR oligomers being the most frequent [27]. The hypothesis we wish to explore is to what implications these data may hold for SARS-CoV-2 infection and we suggest a strong role of nAChR in the disorder.

The nAChR pathway is hypothesized to be engaged in the Covid-19 inflammatory syndrome. The nervous system, through the vagus nerve, can significantly and rapidly inhibit the release of macrophage TNF, and attenuate systemic inflammatory responses [28]. This physiological mechanism, termed the ‘cholinergic anti-inflammatory pathway’ has major implications in immunology and in therapeutics. The cytokine production of macrophages—one of the main cell types found in the bronchoalveolar fluid—is under the physiological control of auto/paracrine acetylcholine through their nAChRs [29]. Following dysregulation of macrophage nAChRs, the profile of cytokines massively secreted include Il1, Il6, TNF et Il18. This cytokine profile shows striking analogies with the cytokine storm syndrome, leading to the hyperinflammatory syndrome described in a subgroup of Covid-19 patients [30]. Systemic coagulopathy with venous and arterial thrombosis is one of the critical aspects of the morbidity and mortality of Covid-19. In line with our hypothesis, one should note that hematopoietic α7-nAChR defficiency increases platelet reactive status, which could explain the thrombogenic presentation of Covid-19 [31]. Although selective cytokine blockers (eg, IL1-receptor antagonist anakinra or anti-IL6 tocilizumab) have been proposed for the control of Covid-19 cytokine storm, their efficacy is still to be explored. Interestingly, α7 agonists, including nicotine, have proven to be effective in reducing macrophage cytokine production and inflammation in animal models of pancreatitis [32] and peritonitis [33]. In this setting, a nicotinic treatment that might possibly antagonize the blocking action of SARS-CoV-2 on the AChR through a possible modulation of the ACE2 – nAChR interaction, would act earlier than anti-cytokine therapies. nAChR modulation by Covid-19 might tentatively account for the hyperinflammatory features observed in a subgroup of Covid-19 patients, mimicking bona fide the macrophage activation syndrome.

Of note, our hypothesis could explain the high prevalence of obesity and diabetes mellitus observed in severe forms of Covid19. The diminished vagus nerve activity previously described in these two illnesses could be potentiated by the Covid-19 elicited nicotinic receptor dysregulation, leading to a hyperinflammatory state often reported in obese patients [29].

nAChRs are present in the lung epithelium. The non-neuronal cholinergic system contributes to the regulation of cell functions such as cell-cell interaction, apoptosis, and proliferation and it is well established that human bronchial epithelial cells contain nAChRs. The airway epithelium expresses α3, α4, α5, α7, α9, β2, and β4-nAChRs subunits [34, 35, 36, 37] and their contribution has been discussed in the framework of airway epithelial basal cell proliferation-differentiation and their alteration in lung cancers [38]. These nAChRs are mentioned here as possible targets of Covid-19 infection of the lung, which would take place concomitantly with, and/or as a consequence of, the neuro-infection. Additionally, nAChRs are involved in lung perfusion regulation, which seems to be disrupted in the atypical acute respiratory distress syndrome reported in Covid-19 patients [3].

A potential protective effect of smoking and of nicotine on SARS-CoV-2 infection has been noted. Until recently [39], no firm conclusions could be drawn from studies evaluating the rates of current smokers in Covid-19. All these studies [40, 41, 42, 43, 44, 45, 46, 47, 48], although reporting low rates of current smokers, ranging from 1.4 % to 12.5 %, did not take into account the main potential confounders of smoking including age and sex. In the study that two of us are reporting [1], the rates of current smoking remain below 5 % even when main confounders for tobacco consumption, i.e. age and sex, in- or outpatient status, were considered. Compared to the French general population, the Covid-19 population exhibited a significantly weaker current daily smoker rate by 80.3 % for outpatients and by 75.4 % for inpatients. Thus, current smoking status appears to be a protective factor against the infection by SARS-CoV-2. Although the chemistry of tobacco smoke is complex, these data are consistent with the hypothesis that its protective role takes place through direct action on various types of nAChRs expressed in neurons, immune cells (including macrophages), cardiac tissue, lungs, and blood vessels.

Mechanisms engaged in Covid-19 as nAChR disease might be tentatively suggested. There is structural evidence supporting the hypothesis that SARS-CoV-2 virus is a nicotinic agent. The recently reported X-ray structure of the RABV glycoprotein (G) ectodomain [49] shows that the region corresponding to the neurotoxin-like peptide is exposed at the G surface, in agreement with the fact that this region is part of the major antigenic region II of RABV [50]. The recently published cryo-EM structure of the trimeric SARS-CoV-2 spike (S) protein [51, 52] revealed an insertion with respect to that of SARS-CoV-1, in a loop that is disordered in the reported structure, and which has a polybasic sequence that corresponds to a furin site. Importantly, this exposed loop of the SARS-CoV-2 S protein also contains a motif that is homologous to that of snake neurotoxins and to the RABV neurotoxin-like region (Figure 1). This observation supports the hypothesis that SARS-CoV-2 virus itself is a nAChR blocker.

Figure 1.

The neurotoxin motifs. Amino acid sequence alignment of the motifs found in toxins from snakes of the Ophiophagus (cobra) and Bungarus genera, in G from three RABV strains and in S from SARS-CoV-2.

Nicotine may be suggested as a potential preventive agent against Covid-19 infection. Both the epidemiological/clinical evidence and the in silico findings may suggest that Covid-19 infection is a nAChR disease that could be prevented and may be controlled by nicotine. Nicotine would then sterically or allosterically compete with the SARS-CoV-2 binding to the nAChR. This legitimates the use of nicotine as a protective agent against SARS-CoV-2 infection and the subsequent deficits it causes in the CNS. Thus, in order to prevent the infection and the retro-propagation of the virus through the CNS, we plan a therapeutic assay against Covid-19 with nicotine (and other nicotinic agents) patches or other delivery methods (like sniffing/chewing) in hospitalized patients and in the general population.

In conclusion, we propose, and try to justify, the hypothesis that nAChRs play a critical role in the pathophysiology of SARS-CoV-2 infection and as a consequence propose nicotine and nicotinic orthosteric and/or allosteric agents as a possible therapy for SARS-CoV-2 infection. Interestingly, ivermectin, which has been recently shown to inhibit the replication of SARS-CoV-2 in cells in vitro [53], is a positive allosteric modulator of α7 nAChR [54]. The nicotinic hypothesis might be further challenged by additional clinical studies and by experimental observations determining whether SARS-CoV-2 physically interacts with the nAChR in vitro, for instance by electrophysiological recordings, high resolution EM and by animal model studies. Further work should also specify the still enigmatic relationships between ACE2 and nAChRs in the nervous system.

One should not forget that nicotine is a drug of abuse [55] responsible for smoking addiction. Smoking has severe pathological consequences and remains a serious danger for health. Yet under controlled settings, nicotinic agents could provide an efficient treatment for an acute infection such as Covid-19.

Acknowledgments

We would like to specially thank Pr. Serge Haroche for establishing the contact between JPC and ZA. We thank Dr. Pablo Guardado Calvo (Institut Pasteur, Paris) for the amino acid sequence analysis of the neurotoxin motif, Pr. Florence Tubach for fruitful discussions, Pr. Gérard Orth for valuable support and discussions, Pr. Daniel Louvard and Pr. Henri Korn for encouragements. JPC acknowledges useful exchanges with Dr. Abdul Mohammed and Dr. Kister Kristensson at early stages of the reflection and the Pasteur Institute shared discussions network organized by the Neuroscience Department and its former Chairman Pr. PM Lledo. We thank Dr. Kurt Sailor for carefully editing the text.

Competing financial interests

The authors declare no competing financial interests.


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  • Maral Aminpour; Marco Cannariato; Jordane Preto; M. Ehsan Safaeeardebili; Alexia Moracchiato; Domiziano Doria; Francesca Donato; Eric Adriano Zizzi; Marco Agostino Deriu; David E. Scheim; Alessandro D. Santin; Jack Adam Tuszynski In Silico Analysis of the Multi-Targeted Mode of Action of Ivermectin and Related Compounds, Computation, Volume 10 (2022) no. 4, p. 51 | DOI:10.3390/computation10040051
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  • Magali Noval Rivas; Rebecca A. Porritt; Mary Hongying Cheng; Ivet Bahar; Moshe Arditi Multisystem Inflammatory Syndrome in Children and Long COVID: The SARS-CoV-2 Viral Superantigen Hypothesis, Frontiers in Immunology, Volume 13 (2022) | DOI:10.3389/fimmu.2022.941009
  • Makoto Miyara; Florence Tubach; Valérie Pourcher; Capucine Morélot-Panzini; Julie Pernet; Julien Haroche; Said Lebbah; Elise Morawiec; Guy Gorochov; Eric Caumes; Pierre Hausfater; Alain Combes; Thomas Similowski; Zahir Amoura Lower Rate of Daily Smokers With Symptomatic COVID-19: A Monocentric Self-Report of Smoking Habit Study, Frontiers in Medicine, Volume 8 (2022) | DOI:10.3389/fmed.2021.668995
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  • Guylaine Labro; Florence Tubach; Lisa Belin; Jean-Louis Dubost; David Osman; Grégoire Muller; Jean-Pierre Quenot; Daniel Da Silva; Jonathan Zarka; Matthieu Turpin; Julien Mayaux; Christian Lamer; Denis Doyen; Guillaume Chevrel; Gaétan Plantefeve; Sophie Demeret; Gaël Piton; Cyril Manzon; Evelina Ochin; Raphael Gaillard; Bertrand Dautzenberg; Mathieu Baldacini; Said Lebbah; Makoto Miyara; Marc Pineton de Chambrun; Zahir Amoura; Alain Combes; Jessica Palmyre; Linda Gimeno; Assitan Kone; Cedric Vialette; Ouramdane Slimi; Juliette Chommeloux; Lucie Lefevre; Matthieu Schmidt; Guillaume Hekimian; Charles-Edouard Luyt; Laure Stiel; Anne-Florence Dureau; Kuteifan Khaldoun; Hanna Eid; Matthieu Baldacini; Cecile Zyberfajn; Julien Manson; Nathanael Charrier; Angelique Balabanian; Damien Contou; Olivier Pajot; Megan Fraisse; Paul Desaint; Florence Sarfati; Muriel Fartoukh; Guillaume Voirot; Alexandre Elabbabi; Michel Djibre; Cyrielle Desnos; Pierre Garcon; Ly van Vong; Andrea Issad; Bertrand Pillot; Delphine Reither; Patrick Rouge; Pascale Foliot; Lynda Bendjamar; Valentin Pointurier; Hadrien Winiszewski; Gilles Capellier; Jean-Christophe Navellou; Romain Tapponnier; Emilie Panicucci; Lucas Morand; Jean Dellamonica; Clement Saccheri; Nicolas Weiss; Clemence Marois; Loic Le Guennec; Benjamin Rohaut; Luis Ensenat; Cecilia Billiou; Maria Aroca; Marie Baron; Alexandre Demoule; Alexandra Beurton; Come Bureau; Maxens Decavele; Martin Dres; Frederique Bayle; Quoc Viet Le; Lionel Liron; Jean-Baptiste Putegnat; Francois Salord; Pascal Andreu; Hakim Slimani; Baptiste Roudeau; Marie Labruyere; Marine Jacquier; Nadia Anguel; Soufia Ayed; Edgard Durand; Laurent Guerin; Christopher Lai; Jerome Aboab; Sophie Alviset; Laurent Laine; Mathilde Azzi; Tazime Issoufaly; Laurent Tric; Lyes Knani; Chahrazad Bey Boumezrag; Nicolas Viault; Francois Barbier; Thierry Boulain; Toufik Kamel; Mai-Anh Nay; Sophie Tollec; An Hung Nguyen Nicotine patches in patients on mechanical ventilation for severe COVID-19: a randomized, double-blind, placebo-controlled, multicentre trial, Intensive Care Medicine, Volume 48 (2022) no. 7, p. 876 | DOI:10.1007/s00134-022-06721-1
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  • Dimitra Kale; Olga Perski; Aleksandra Herbec; Emma Beard; Lion Shahab Changes in Cigarette Smoking and Vaping in Response to the COVID-19 Pandemic in the UK: Findings from Baseline and 12-Month Follow up of HEBECO Study, International Journal of Environmental Research and Public Health, Volume 19 (2022) no. 2, p. 630 | DOI:10.3390/ijerph19020630
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  • Min Gao; Paul Aveyard; Nicola Lindson; Jamie Hartmann-Boyce; Peter Watkinson; Duncan Young; Carol Coupland; Ashley K Clift; David Harrison; Doug Gould; Ian D Pavord; Margaret Smith; Julia Hippisley-Cox Association between smoking, e-cigarette use and severe COVID-19: a cohort study, International Journal of Epidemiology, Volume 51 (2022) no. 4, p. 1062 | DOI:10.1093/ije/dyac028
  • Luigi Sansone; Antonio de Iure; Mario Cristina; Manuel Belli; Laura Vitiello; Federica Marcolongo; Alfredo Rosellini; Lisa Macera; Pietro Giorgio Spezia; Carlo Tomino; Stefano Bonassi; Matteo A. Russo; Fabrizio Maggi; Patrizia Russo Nicotine in Combination with SARS-CoV-2 Affects Cells Viability, Inflammatory Response and Ultrastructural Integrity, International Journal of Molecular Sciences, Volume 23 (2022) no. 16, p. 9488 | DOI:10.3390/ijms23169488
  • Marta Kopańska; Marta Batoryna; Paulina Bartman; Jacek Szczygielski; Agnieszka Banaś-Ząbczyk Disorders of the Cholinergic System in COVID-19 Era—A Review of the Latest Research, International Journal of Molecular Sciences, Volume 23 (2022) no. 2, p. 672 | DOI:10.3390/ijms23020672
  • David E. Scheim A Deadly Embrace: Hemagglutination Mediated by SARS-CoV-2 Spike Protein at Its 22 N-Glycosylation Sites, Red Blood Cell Surface Sialoglycoproteins, and Antibody, International Journal of Molecular Sciences, Volume 23 (2022) no. 5, p. 2558 | DOI:10.3390/ijms23052558
  • Simona Di Lascio; Diego Fornasari; Roberta Benfante The Human-Restricted Isoform of the α7 nAChR, CHRFAM7A: A Double-Edged Sword in Neurological and Inflammatory Disorders, International Journal of Molecular Sciences, Volume 23 (2022) no. 7, p. 3463 | DOI:10.3390/ijms23073463
  • Fabrizio Virgili; Raffaella Nenna; Shira Ben David; Enrica Mancino; Greta Di Mattia; Luigi Matera; Laura Petrarca; Fabio Midulla E-cigarettes and youth: an unresolved Public Health concern, Italian Journal of Pediatrics, Volume 48 (2022) no. 1 | DOI:10.1186/s13052-022-01286-7
  • Attapon Cheepsattayakorn; Ruangrong Cheepsattayakorn; Porntep Siriwanarangsun Severe and non-severe Covid-19 patients with postintubation tracheal stenosis, Journal of Human Virology Retrovirology, Volume 9 (2022) no. 3, p. 75 | DOI:10.15406/jhvrv.2022.09.00246
  • Mohammad Z Haider; Amna Al-Mannai; Sally Al-Sirhan; Ahmed Elsabagh; Nasser Nasser; Noora Al-Quraishi; Amr Ouda; Khadija Erradi; Anas A Ashour; Ishita Gupta; Jazeel Abdulmajeed; Hamad E Al-Romaihi; Devendra Bansal; Omran AH Musa; Elmoubasher Abu Baker Abd Farag; Mohammed HJ Al-Thani; Ala-Eddin Al Moustafa Impact of Smoking on COVID-19 Symptoms in Non-Vaccinated Patients: A Matched Observational Study from Qatar, Journal of Multidisciplinary Healthcare, Volume Volume 15 (2022), p. 531 | DOI:10.2147/jmdh.s347130
  • D. Batifol; P.J. Finiels; S. Galmiche; P. Jammet; M. de Boutray Could treatment with botulinum toxin protect against subsequent infection with COVID-19?, Journal of Stomatology, Oral and Maxillofacial Surgery, Volume 123 (2022) no. 2, p. 98 | DOI:10.1016/j.jormas.2021.06.003
  • Yue He; Yangai He; Qinghui Hu; Sheng Yang; Jun Li; Yuan Liu; Jun Hu Association between smoking and COVID-19 severity: A multicentre retrospective observational study, Medicine, Volume 101 (2022) no. 29, p. e29438 | DOI:10.1097/md.0000000000029438
  • Juan Facundo Chrestia; Ana Sofia Oliveira; Adrian J. Mulholland; Timothy Gallagher; Isabel Bermúdez; Cecilia Bouzat A Functional Interaction Between Y674-R685 Region of the SARS-CoV-2 Spike Protein and the Human α7 Nicotinic Receptor, Molecular Neurobiology, Volume 59 (2022) no. 10, p. 6076 | DOI:10.1007/s12035-022-02947-8
  • Bijaya Nanda Naik; Chandramani Singh; Bijit Biswas; Sanjay Pandey; Santosh Kumar Nirala; Neha Chaudhary Perceived Risk of Tobacco Use in COVID-19 Disease Causation and Severity among Healthcare Professionals: A Pan India Online Survey, National Journal of Community Medicine, Volume 12 (2022) no. 06, p. 140 | DOI:10.5455/njcm.20210607111817
  • Fang Zheng; Elena Lian; Gaby Ramirez; Carley McAlister; Shuo Zhou; Wen Zhang; Chunming Liu; Rushika Perera; Chang-Guo Zhan; Claudio Andaloro Nicotine has no significant cytoprotective activity against SARS-CoV-2 infection, PLOS ONE, Volume 17 (2022) no. 8, p. e0272941 | DOI:10.1371/journal.pone.0272941
  • Abdullah Mohammed Abdulkarim; Mustafa Salim Ibrahim; Majid Mohammed Mahmood, PROCEEDING OF THE 1ST INTERNATIONAL CONFERENCE ON ADVANCED RESEARCH IN PURE AND APPLIED SCIENCE (ICARPAS2021): Third Annual Conference of Al-Muthanna University/College of Science, Volume 2398 (2022), p. 040024 | DOI:10.1063/5.0094376
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  • Petar Atanasov; Maria Moneva-Sakelarieva; Yozlem Kobakova; Danka Obreshkova; Ivaylo Ivanov; Mariya Chaneva; Mihaela Popova; Valentina Petkova; Stefka Ivanova Tobacco smokers as target group for complicated coronavirus infection, Pharmacia, Volume 69 (2022) no. 3, p. 791 | DOI:10.3897/pharmacia.69.e91095
  • Nicole E. Godellas; Gisela D. Cymes; Claudio Grosman An experimental test of the nicotinic hypothesis of COVID-19, Proceedings of the National Academy of Sciences, Volume 119 (2022) no. 44 | DOI:10.1073/pnas.2204242119
  • Moulay Abdelmonaim El Hidan; Mohamed Rhazi; Mohamed Merzouki; Mustapha Agnaou; Moulay Abdeljalil Ait Baamrane; Ahmed Draoui; Lahcen Tamegart; Karima Warda Pathophysiological Basis of COVID-19, Public Health and Economic Resiliency in the Post-COVID-19 Era (2022), p. 38 | DOI:10.4018/978-1-7998-8202-2.ch003
  • Pierre Hausfater; David Boutolleau; Karine Lacombe; Alexandra Beurton; Margaux Dumont; Jean-Michel Constantin; Jade Ghosn; Alain Combes; Nicolas Cury; Romain Guedj; Michel Djibré; Rudy Bompard; Sandie Mazerand; Valérie Pourcher; Linda Gimeno; Clémence Marois; Elisa Teyssou; Anne-Geneviève Marcelin; David Hajage; Florence Tubach Cumulative incidence of SARS-CoV-2 infection and associated risk factors among frontline health care workers in Paris: the SEROCOV cohort study, Scientific Reports, Volume 12 (2022) no. 1 | DOI:10.1038/s41598-022-10945-y
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  • Jonathan Grigg Smoking, nicotine, and COVID-19, The Lancet Respiratory Medicine, Volume 10 (2022) no. 9, p. 818 | DOI:10.1016/s2213-2600(22)00258-2
  • Neal L Benowitz; Maciej L Goniewicz; Bonnie Halpern-Felsher; Suchitra Krishnan-Sarin; Pamela M Ling; Richard J O'Connor; Mary Ann Pentz; Rose Marie Robertson; Aruni Bhatnagar Tobacco product use and the risks of SARS-CoV-2 infection and COVID-19: current understanding and recommendations for future research, The Lancet Respiratory Medicine, Volume 10 (2022) no. 9, p. 900 | DOI:10.1016/s2213-2600(22)00182-5
  • Chakkraphan Phetphum; Atchara Prajongjeep; Orawan Keeratisiroj; Kanyarat Thawatchaijareonying Communication intervention to improve perceived threat of smoking-related COVID-19 and intentions to quit smoking during the COVID-19 pandemic in Thailand, Tobacco Induced Diseases, Volume 20 (2022) no. July, p. 1 | DOI:10.18332/tid/150363
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  • Mohammad-Reza Sohrabi; Rozhin Amin; Ali Maher; Ayad Bahadorimonfared; Shahriar Janbazi; Khatereh Hannani; Ali-Asghar Kolahi; Ali-Reza Zali Sociodemographic determinants and clinical risk factors associated with COVID-19 severity: a cross-sectional analysis of over 200,000 patients in Tehran, Iran, BMC Infectious Diseases, Volume 21 (2021) no. 1 | DOI:10.1186/s12879-021-06179-4
  • Claire Lugnier; Hayder M. Al-Kuraishy; Eric Rousseau PDE4 inhibition as a therapeutic strategy for improvement of pulmonary dysfunctions in Covid-19 and cigarette smoking, Biochemical Pharmacology, Volume 185 (2021), p. 114431 | DOI:10.1016/j.bcp.2021.114431
  • David A. Jans; Kylie M. Wagstaff The broad spectrum host-directed agent ivermectin as an antiviral for SARS-CoV-2 ?, Biochemical and Biophysical Research Communications, Volume 538 (2021), p. 163 | DOI:10.1016/j.bbrc.2020.10.042
  • Olena Kalashnyk; Olena Lykhmus; Mykhailo Izmailov; Lyudmyla Koval; Serhiy Komisarenko; Maryna Skok SARS-Cov-2 spike protein fragment 674–685 protects mitochondria from releasing cytochrome c in response to apoptogenic influence, Biochemical and Biophysical Research Communications, Volume 561 (2021), p. 14 | DOI:10.1016/j.bbrc.2021.05.018
  • Relationship of smoking with COVID-19 and its adverse effects, Biomedical Letters, Volume 7 (2021) no. 2 | DOI:10.47262/bl/7.2.20210903
  • A. Sofia F. Oliveira; Amaurys Avila Ibarra; Isabel Bermudez; Lorenzo Casalino; Zied Gaieb; Deborah K. Shoemark; Timothy Gallagher; Richard B. Sessions; Rommie E. Amaro; Adrian J. Mulholland A potential interaction between the SARS-CoV-2 spike protein and nicotinic acetylcholine receptors, Biophysical Journal, Volume 120 (2021) no. 6, p. 983 | DOI:10.1016/j.bpj.2021.01.037
  • Ahmad Besaratinia COVID-19: a pandemic converged with global tobacco epidemic and widespread vaping—state of the evidence, Carcinogenesis, Volume 42 (2021) no. 8, p. 1009 | DOI:10.1093/carcin/bgab061
  • Juan Facundo Chrestia; Ariana Bruzzone; María del Carmen Esandi; Cecilia Bouzat Tyrosine phosphorylation differentially fine-tunes ionotropic and metabotropic responses of human α7 nicotinic acetylcholine receptor, Cellular and Molecular Life Sciences, Volume 78 (2021) no. 13, p. 5381 | DOI:10.1007/s00018-021-03853-3
  • Félix Rey Structure-function relations of the SARS-CoV-2 spike protein and impact of mutations in the variants of concern, Comptes Rendus. Biologies, Volume 344 (2021) no. 1, p. 77 | DOI:10.5802/crbiol.53
  • Christopher A. Beaudoin; Arian R. Jamasb; Ali F. Alsulami; Liviu Copoiu; Andries J. van Tonder; Sharif Hala; Bridget P. Bannerman; Sherine E. Thomas; Sundeep Chaitanya Vedithi; Pedro H.M. Torres; Tom L. Blundell Predicted structural mimicry of spike receptor-binding motifs from highly pathogenic human coronaviruses, Computational and Structural Biotechnology Journal, Volume 19 (2021), p. 3938 | DOI:10.1016/j.csbj.2021.06.041
  • Mehmet Durgun; Emine Kübra Dindar Demiray; Sevil Alkan Çeviker The relationship between COVID-19 and smoking, Demiroglu Science University Florence Nightingale Journal of Medicine, Volume 7 (2021) no. 1, p. 77 | DOI:10.5606/fng.btd.2021.25051
  • Carlos Chaccour; Aina Casellas; Andrés Blanco-Di Matteo; Iñigo Pineda; Alejandro Fernandez-Montero; Paula Ruiz-Castillo; Mary-Ann Richardson; Mariano Rodríguez-Mateos; Carlota Jordán-Iborra; Joe Brew; Francisco Carmona-Torre; Miriam Giráldez; Ester Laso; Juan C. Gabaldón-Figueira; Carlota Dobaño; Gemma Moncunill; José R. Yuste; Jose L. Del Pozo; N.Regina Rabinovich; Verena Schöning; Felix Hammann; Gabriel Reina; Belen Sadaba; Mirian Fernández-Alonso The effect of early treatment with ivermectin on viral load, symptoms and humoral response in patients with non-severe COVID-19: A pilot, double-blind, placebo-controlled, randomized clinical trial, EClinicalMedicine, Volume 32 (2021), p. 100720 | DOI:10.1016/j.eclinm.2020.100720
  • Guilherme Dias de Melo; Françoise Lazarini; Florence Larrous; Lena Feige; Etienne Kornobis; Sylvain Levallois; Agnès Marchio; Lauriane Kergoat; David Hardy; Thomas Cokelaer; Pascal Pineau; Marc Lecuit; Pierre‐Marie Lledo; Jean‐Pierre Changeux; Hervé Bourhy Attenuation of clinical and immunological outcomes during SARS‐CoV‐2 infection by ivermectin, EMBO Molecular Medicine, Volume 13 (2021) no. 8 | DOI:10.15252/emmm.202114122
  • Fabrizio Maggi; Alfredo Rosellini; Pietro Giorgio Spezia; Daniele Focosi; Lisa Macera; Michele Lai; Mauro Pistello; Antonio de Iure; Carlo Tomino; Stefano Bonassi; Patrizia Russo Nicotine upregulates ACE2 expression and increases competence for SARS-CoV-2 in human pneumocytes, ERJ Open Research, Volume 7 (2021) no. 2, p. 00713-2020 | DOI:10.1183/23120541.00713-2020
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  • Xiuxiu Fu; Tingyu Zong; Panyu Yang; Lin Li; Shizhong Wang; Zhibin Wang; Min Li; Xiaolu Li; Yulin Zou; Ying Zhang; Lynn Htet Htet Aung; Yanyan Yang; Tao Yu Nicotine: Regulatory roles and mechanisms in atherosclerosis progression, Food and Chemical Toxicology, Volume 151 (2021), p. 112154 | DOI:10.1016/j.fct.2021.112154
  • Ifeoluwa O. Awogbindin; Benneth Ben-Azu; Babatunde A. Olusola; Elizabeth T. Akinluyi; Philip A. Adeniyi; Therese Di Paolo; Marie-Ève Tremblay Microglial Implications in SARS-CoV-2 Infection and COVID-19: Lessons From Viral RNA Neurotropism and Possible Relevance to Parkinson’s Disease, Frontiers in Cellular Neuroscience, Volume 15 (2021) | DOI:10.3389/fncel.2021.670298
  • Florin Dumitru Mihaltan; Armand-Gabriel Rajnoveanu; Ruxandra-Mioara Rajnoveanu Impact of Smoking on Women During the Covid-19 Pandemic, Frontiers in Medicine, Volume 8 (2021) | DOI:10.3389/fmed.2021.584061
  • Massimo Caruso; Alfio Distefano; Rosalia Emma; Michelino Di Rosa; Giuseppe Carota; Sonja Rust; Riccardo Polosa; Pietro Zuccarello; Margherita Ferrante; Giuseppina Raciti; Giovanni Li Volti Role of Cigarette Smoke on Angiotensin-Converting Enzyme-2 Protein Membrane Expression in Bronchial Epithelial Cells Using an Air-Liquid Interface Model, Frontiers in Pharmacology, Volume 12 (2021) | DOI:10.3389/fphar.2021.652102
  • Martina Di Maro; Mauro Cataldi; Mariarosaria Santillo; Martina Chiurazzi; Simona Damiano; Barbara De Conno; Antonio Colantuoni; Bruna Guida The Cholinergic and ACE-2-Dependent Anti-Inflammatory Systems in the Lung: New Scenarios Emerging From COVID-19, Frontiers in Physiology, Volume 12 (2021) | DOI:10.3389/fphys.2021.653985
  • Sinu Rose Mathachan; Kabir Sardana; Ananta Khurana Current Use of Ivermectin in Dermatology, Tropical Medicine, and COVID-19, Indian Dermatology Online Journal, Volume 12 (2021) no. 4, p. 500 | DOI:10.4103/idoj.idoj_298_21
  • Yajie Li; Tzu Tsun Luk; Yongda Wu; Derek Yee Tak Cheung; William Ho Cheung Li; Henry Sau Chai Tong; Vienna Wai Yin Lai; Sai Yin Ho; Tai Hing Lam; Man Ping Wang High Perceived Susceptibility to and Severity of COVID-19 in Smokers Are Associated with Quitting-Related Behaviors, International Journal of Environmental Research and Public Health, Volume 18 (2021) no. 20, p. 10894 | DOI:10.3390/ijerph182010894
  • Lola Rueda Ruzafa; José Luis Cedillo; Arik J. Hone Nicotinic Acetylcholine Receptor Involvement in Inflammatory Bowel Disease and Interactions with Gut Microbiota, International Journal of Environmental Research and Public Health, Volume 18 (2021) no. 3, p. 1189 | DOI:10.3390/ijerph18031189
  • Chunliang Tao; Destiny Diaz; Zidian Xie; Long Chen; Dongmei Li; Richard O’Connor Potential Impact of a Paper About COVID-19 and Smoking on Twitter Users’ Attitudes Toward Smoking: Observational Study, JMIR Formative Research, Volume 5 (2021) no. 6, p. e25010 | DOI:10.2196/25010
  • Elif BARIŞ; Mualla ARICI Possible Therapeutic Role of Cholinergic Agonists on COVID-19 related inflammatory response, Journal of Basic and Clinical Health Sciences, Volume 5 (2021) no. 1, p. 102 | DOI:10.30621/jbachs.869857
  • Alex G. Gauthier; Mosi Lin; Jiaqi Wu; Thomas P. Kennedy; Lee-Anne Daley; Charles R. Ashby; Lin L. Mantell From nicotine to the cholinergic anti-inflammatory reflex – Can nicotine alleviate the dysregulated inflammation in COVID-19?, Journal of Immunotoxicology, Volume 18 (2021) no. 1, p. 23 | DOI:10.1080/1547691x.2021.1875085
  • Anant Mohan; Pawan Tiwari; Tejas Menon Suri; Saurabh Mittal; Ankit Patel; Avinash Jain; Thirumurthy Velpandian; Ujjalkumar Subhash Das; Tarun Krishna Boppana; Ravindra Mohan Pandey; Sushil Suresh Shelke; Angel Rajan Singh; Sushma Bhatnagar; Shet Masih; Shelly Mahajan; Tanima Dwivedi; Biswajeet Sahoo; Anuja Pandit; Shweta Bhopale; Saurabh Vig; Ritu Gupta; Karan Madan; Vijay Hadda; Nishkarsh Gupta; Rakesh Garg; Ved Prakash Meena; Randeep Guleria Single-dose oral ivermectin in mild and moderate COVID-19 (RIVET-COV): A single-centre randomized, placebo-controlled trial, Journal of Infection and Chemotherapy, Volume 27 (2021) no. 12, p. 1743 | DOI:10.1016/j.jiac.2021.08.021
  • Sushma Bommanavar; V C Patil; Alexander Maniangat Luke; Mohamed Jaber; Jagadish Hosmani Study of ABO Blood Group Susceptibility to Coronavirus Disease - COVID-19, Journal of Oral and Maxillofacial Pathology, Volume 25 (2021) no. 3, p. 396 | DOI:10.4103/jomfp.jomfp_21_21
  • S. D Bruyakin; D. A Makarevich STRUCTURAL PROTEINS OF THE SARS-COV-2 CORONAVIRUS: ROLE, IMMUNOGENICITY, SUPERANTIGENIC PROPERTIES AND POTENTIAL USE FOR THERAPEUTIC PURPOSES, Journal of Volgograd State Medical University, Volume 18 (2021) no. 2, p. 18 | DOI:10.19163/1994-9480-2021-2(78)-18-27
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