ACS Publications. Most Trusted. Most Cited. Most Read

OR SEARCH CITATIONS

My Activity
Publications
CONTENT TYPES

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:ACS Chem. Neurosci. 2016, 7, 4, 464-469
RETURN TO ISSUEPREVReviewNEXT

The Olfactory Bulb: An Immunosensory Effector Organ during Neurotropic Viral Infections

View Author Information
† Biological Sciences Department, California State Polytechnic University, 3801 West Temple Ave., Pomona, California 91768, United States
‡ § ∥ ‡Department of Medicine, §Department of Pathology & Immunology, and ∥Department of Neuroscience, Washington University School of Medicine, 660 S. Euclid Ave., St Louis, Missouri 63110, United States
*Mailing address: Washington University School of Medicine, Departments of Internal Medicine, Neurobiology, Pathology & Immunology, Campus Box 8051, 660 S. Euclid Ave., St. Louis, MO 63110. Phone: 314-286-2140. Fax: 314-362-9230. E-mail: [email protected]
Cite this: ACS Chem. Neurosci. 2016, 7, 4, 464–469
Publication Date (Web):April 8, 2016
https://doi.org/10.1021/acschemneuro.6b00043
Copyright © 2016 American Chemical Society
Request reuse permissions

    Article Views

    1118

    Altmetric

    -

    Citations

    77
    LEARN ABOUT THESE METRICS
    Read OnlinePDF (474 KB)
    Get e-Alerts
    SUBJECTS:

    Abstract

    Abstract Image

    In 1935, the olfactory route was hypothesized to be a portal for virus entry into the central nervous system (CNS). This hypothesis was based on experiments in which nasophayngeal infection with poliovirus in monkeys was prevented from spreading to their CNS via transection of olfactory tracts between the olfactory neuroepithelium (ONE) of the nasal cavity and the olfactory bulb (OB). Since then, numerous neurotropic viruses have been observed to enter the CNS via retrograde transport along axons of olfactory sensory neurons whose cell bodies reside in the ONE. Importantly, this route of infection can occur even after subcutaneous inoculation of arboviruses that can cause encephalitis in humans. While the olfactory route is now accepted as an important pathway for viral entry into the CNS, it is unclear whether it provides a way for infection to spread to other brain regions. More recently, studies of antiviral innate and adaptive immune responses within the olfactory bulb suggest it provides early virologic control. Here we will review the data demonstrating that neurotropic viruses gain access to the CNS initially via the olfactory route with emphasis on findings that suggest the OB is a critical immunosensory effector organ that effectively clears virus.

    KEYWORDS:

    Cited By

    This article is cited by 77 publications.

    1. Daniela Brunert, Renata Medinaceli Quintela, Markus Rothermel. The anterior olfactory nucleus revisited – An emerging role for neuropathological conditions?. Progress in Neurobiology 2023, 228 , 102486. https://doi.org/10.1016/j.pneurobio.2023.102486
    2. Maggie Jing Ouyang, Zhujun Ao, Titus A. Olukitibi, Peter Lawrynuik, Christopher Shieh, Sam K. P. Kung, Keith R. Fowke, Darwyn Kobasa, Xiaojian Yao. Oral Immunization with rVSV Bivalent Vaccine Elicits Protective Immune Responses, Including ADCC, against Both SARS-CoV-2 and Influenza A Viruses. Vaccines 2023, 11 (9) , 1404. https://doi.org/10.3390/vaccines11091404
    3. Zhen Yu Liu, Luigi Angelo Vaira, Paolo Boscolo-Rizzo, Abigail Walker, Claire Hopkins. Post-viral olfactory loss and parosmia. BMJ Medicine 2023, 2 (1) , e000382. https://doi.org/10.1136/bmjmed-2022-000382
    4. Wentao Zhu, Meihua Qiao, Meidi Hu, Xingchen Huo, Yongan Zhang, Jianguo Su. Type II Grass Carp Reovirus Rapidly Invades Grass Carp (Ctenopharyngodon idella) via Nostril–Olfactory System–Brain Axis, Gill, and Skin on Head. Viruses 2023, 15 (7) , 1614. https://doi.org/10.3390/v15071614
    5. Aki Morikawa, Jinju Li, Peter Ulintz, Xu Cheng, Athena Apfel, Dan Robinson, Alex Hopkins, Chandan Kumar-Sinha, Yi-Mi Wu, Habib Serhan, Kait Verbal, Dafydd Thomas, Daniel F. Hayes, Arul M. Chinnaiyan, Veerabhadran Baladandayuthapani, Jason Heth, Matthew B. Soellner, Sofia D. Merajver, Nathan Merrill. Optimizing Precision Medicine for Breast Cancer Brain Metastases with Functional Drug Response Assessment. Cancer Research Communications 2023, 3 (6) , 1093-1103. https://doi.org/10.1158/2767-9764.CRC-22-0492
    6. Amanda L. Phelps, Francisco J. Salguero, Laura Hunter, Alexander L. Stoll, Dominic C. Jenner, Lyn M. O’Brien, E. Diane Williamson, M. Stephen Lever, Thomas R. Laws. Tumour Necrosis Factor-α, Chemokines, and Leukocyte Infiltrate Are Biomarkers for Pathology in the Brains of Venezuelan Equine Encephalitis (VEEV)-Infected Mice. Viruses 2023, 15 (6) , 1307. https://doi.org/10.3390/v15061307
    7. Lisa A. Beltz. Introduction. 2023, 1-52. https://doi.org/10.1016/B978-0-323-98809-4.00005-X
    8. Zhuang-Yao D. Wei, Ketty Liang, Ashok K. Shetty. Complications of COVID-19 on the Central Nervous System: Mechanisms and Potential Treatment for Easing Long COVID. Aging and disease 2023, , 0. https://doi.org/10.14336/AD.2023.0312
    9. Ryoji Kagoya, Makiko Toma-Hirano, Junya Yamagishi, Naoyuki Matsumoto, Kenji Kondo, Ken Ito. Immunological status of the olfactory bulb in a murine model of Toll-like receptor 3-mediated upper respiratory tract inflammation. Journal of Neuroinflammation 2022, 19 (1) https://doi.org/10.1186/s12974-022-02378-1
    10. Yuto Hasegawa, Minghong Ma, Akira Sawa, Andrew P. Lane, Atsushi Kamiya. Olfactory impairment in psychiatric disorders: Does nasal inflammation impact disease psychophysiology?. Translational Psychiatry 2022, 12 (1) https://doi.org/10.1038/s41398-022-02081-y
    11. E. Thunell, M.G. Peter, V. Lenoir, P. Andersson, B.N. Landis, M. Becker, J.N. Lundström. Effects of COVID-19 on the Human Central Olfactory System: A Natural Pre-Post Experiment. American Journal of Neuroradiology 2022, 43 (12) , 1777-1783. https://doi.org/10.3174/ajnr.A7713
    12. Eleanor Marshall, Marion Koopmans, Barry Rockx. A Journey to the Central Nervous System: Routes of Flaviviral Neuroinvasion in Human Disease. Viruses 2022, 14 (10) , 2096. https://doi.org/10.3390/v14102096
    13. Mercedes Lachén-Montes, Naroa Mendizuri, Karina Ausín, Miriam Echaide, Ester Blanco, Luisa Chocarro, María de Toro, David Escors, Joaquín Fernández-Irigoyen, Grazyna Kochan, Enrique Santamaría. Metabolic dyshomeostasis induced by SARS-CoV-2 structural proteins reveals immunological insights into viral olfactory interactions. Frontiers in Immunology 2022, 13 https://doi.org/10.3389/fimmu.2022.866564
    14. Richard L. Doty. Olfactory dysfunction in COVID-19: pathology and long-term implications for brain health. Trends in Molecular Medicine 2022, 28 (9) , 781-794. https://doi.org/10.1016/j.molmed.2022.06.005
    15. Leslie M. Kay. COVID-19 and olfactory dysfunction: a looming wave of dementia?. Journal of Neurophysiology 2022, 128 (2) , 436-444. https://doi.org/10.1152/jn.00255.2022
    16. Piotr Rzymski, Barbara Poniedziałek, Joanna Rosińska, Magdalena Rogalska, Dorota Zarębska-Michaluk, Marta Rorat, Anna Moniuszko-Malinowska, Beata Lorenc, Dorota Kozielewicz, Anna Piekarska, Katarzyna Sikorska, Anna Dworzańska, Beata Bolewska, Grzegorz Angielski, Justyna Kowalska, Regina Podlasin, Barbara Oczko-Grzesik, Włodzimierz Mazur, Aleksandra Szymczak, Robert Flisiak. The association of airborne particulate matter and benzo[a]pyrene with the clinical course of COVID-19 in patients hospitalized in Poland. Environmental Pollution 2022, 306 , 119469. https://doi.org/10.1016/j.envpol.2022.119469
    17. Yudibeth Sixto-López, José Correa-Basurto. HDAC Inhibition as Neuroprotection in COVID-19 Infection. Current Topics in Medicinal Chemistry 2022, 22 (16) , 1369-1378. https://doi.org/10.2174/1568026622666220303113445
    18. Giulia Moreni, Ikrame Aknouch, Morris Ras, Lieke Brouwer, René Spijker, Carlemi Calitz, Koert J. Stittelaar, Adithya Sridhar, Katja C. Wolthers, Dasja Pajkrt. Bridging the gap between emerging models and humans by learning from polio animal studies: A systematic review. Clinical and Translational Discovery 2022, 2 (2) https://doi.org/10.1002/ctd2.42
    19. Christopher Käufer, Cara S. Schreiber, Anna-Sophia Hartke, Ivo Denden, Stephanie Stanelle-Bertram, Sebastian Beck, Nancy Mounogou Kouassi, Georg Beythien, Kathrin Becker, Tom Schreiner, Berfin Schaumburg, Andreas Beineke, Wolfgang Baumgärtner, Gülsah Gabriel, Franziska Richter. Microgliosis and neuronal proteinopathy in brain persist beyond viral clearance in SARS-CoV-2 hamster model. eBioMedicine 2022, 79 , 103999. https://doi.org/10.1016/j.ebiom.2022.103999
    20. Amaan Javed. Neurological Associations of SARS-CoV-2 Infection: A Systematic Review. CNS & Neurological Disorders - Drug Targets 2022, 21 (3) , 246-258. https://doi.org/10.2174/1871527320666210216121211
    21. Kah-Whye Peng, Timothy Carey, Patrycja Lech, Rianna Vandergaast, Miguel Á. Muñoz-Alía, Nandakumar Packiriswamy, Clement Gnanadurai, Karina Krotova, Mulu Tesfay, Christopher Ziegler, Michelle Haselton, Kara Sevola, Chase Lathrum, Samantha Reiter, Riya Narjari, Baskar Balakrishnan, Lukkana Suksanpaisan, Toshie Sakuma, Jordan Recker, Lianwen Zhang, Scott Waniger, Luke Russell, Christopher D. Petro, Christos A. Kyratsous, Alina Baum, Jody L. Janecek, Rachael M. Lee, Sabarinathan Ramachandran, Melanie L. Graham, Stephen J. Russell. Boosting of SARS-CoV-2 immunity in nonhuman primates using an oral rhabdoviral vaccine. Vaccine 2022, 40 (15) , 2342-2351. https://doi.org/10.1016/j.vaccine.2021.12.063
    22. Min‐Wen Ku, Pierre Authié, Maryline Bourgine, François Anna, Amandine Noirat, Fanny Moncoq, Benjamin Vesin, Fabien Nevo, Jodie Lopez, Philippe Souque, Catherine Blanc, Ingrid Fert, Sébastien Chardenoux, llta Lafosse, Delphine Cussigh, David Hardy, Kirill Nemirov, Françoise Guinet, Francina Langa Vives, Laleh Majlessi, Pierre Charneau. Brain cross‐protection against SARS‐CoV‐2 variants by a lentiviral vaccine in new transgenic mice. EMBO Molecular Medicine 2021, 13 (12) https://doi.org/10.15252/emmm.202114459
    23. Fan Yang, Hai Zhao, Hongtao Liu, Xiuying Wu, Yongnan Li. Manifestations and mechanisms of central nervous system damage caused by SARS-CoV-2. Brain Research Bulletin 2021, 177 , 155-163. https://doi.org/10.1016/j.brainresbull.2021.09.015
    24. Haiyue Xu, Lucy Cai, Stephanie Hufnagel, Zhengrong Cui. Intranasal vaccine: Factors to consider in research and development. International Journal of Pharmaceutics 2021, 609 , 121180. https://doi.org/10.1016/j.ijpharm.2021.121180
    25. Yichen Guo, Dawei Wu, Zhifu Sun, Linyin Yao, Jia Liu, Yongxiang Wei. Prognostic value of olfactory evoked potentials in patients with post-infectious olfactory dysfunction. European Archives of Oto-Rhino-Laryngology 2021, 278 (10) , 3839-3846. https://doi.org/10.1007/s00405-021-06683-y
    26. Michael S Xydakis, Mark W Albers, Eric H Holbrook, Dina M Lyon, Robert Y Shih, Johannes A Frasnelli, Axel Pagenstecher, Alexandra Kupke, Lynn W Enquist, Stanley Perlman. Post-viral effects of COVID-19 in the olfactory system and their implications. The Lancet Neurology 2021, 20 (9) , 753-761. https://doi.org/10.1016/S1474-4422(21)00182-4
    27. M. Obolenskaya, V. Dotsenko, O. Martsenyuk, S. Ralchenko, O. Krupko, A. Pastukhov, N. Filimonova, D. Starosila, S. Chernykh, T. Borisova. A new insight into mechanisms of interferon alpha neurotoxicity: Expression of GRIN3A subunit of NMDA receptors and NMDA-evoked exocytosis. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2021, 110 , 110317. https://doi.org/10.1016/j.pnpbp.2021.110317
    28. Harald Brüssow, Kenneth Timmis. COVID ‐19: long covid and its societal consequences. Environmental Microbiology 2021, 23 (8) , 4077-4091. https://doi.org/10.1111/1462-2920.15634
    29. Wei Han, Mingxing Gao, Changqing Xie, Jinhua Zhang, Zikai Zhao, Xueying Hu, Wanpo Zhang, Xiaoli Liu, Shengbo Cao, Guofu Cheng, Changqin Gu, . Precise localization and dynamic distribution of Japanese encephalitis virus in the rain nuclei of infected mice. PLOS Neglected Tropical Diseases 2021, 15 (6) , e0008442. https://doi.org/10.1371/journal.pntd.0008442
    30. Luca Ghita, Julia Spanier, Chintan Chhatbar, Felix Mulenge, Andreas Pavlou, Pia-Katharina Larsen, Inken Waltl, Yvonne Lueder, Moritz Kohls, Klaus Jung, Sonja M. Best, Reinhold Förster, Martin Stangel, Dietmar Schreiner, Ulrich Kalinke. MyD88 signaling by neurons induces chemokines that recruit protective leukocytes to the virus-infected CNS. Science Immunology 2021, 6 (60) https://doi.org/10.1126/sciimmunol.abc9165
    31. Guilherme Dias de Melo, Françoise Lazarini, Sylvain Levallois, Charlotte Hautefort, Vincent Michel, Florence Larrous, Benjamin Verillaud, Caroline Aparicio, Sebastien Wagner, Gilles Gheusi, Lauriane Kergoat, Etienne Kornobis, Flora Donati, Thomas Cokelaer, Rémi Hervochon, Yoann Madec, Emmanuel Roze, Dominique Salmon, Hervé Bourhy, Marc Lecuit, Pierre-Marie Lledo. COVID-19–related anosmia is associated with viral persistence and inflammation in human olfactory epithelium and brain infection in hamsters. Science Translational Medicine 2021, 13 (596) https://doi.org/10.1126/scitranslmed.abf8396
    32. Igor Santana de Melo, Robinson Sabino-Silva, Thúlio Marquez Cunha, Luiz Ricardo Goulart, Wagner Luis Reis, Ana Carolina Gomes Jardim, Ashok K. Shetty, Olagide Wagner de Castro. Hydroelectrolytic Disorder in COVID-19 patients: Evidence Supporting the Involvement of Subfornical Organ and Paraventricular Nucleus of the Hypothalamus. Neuroscience & Biobehavioral Reviews 2021, 124 , 216-223. https://doi.org/10.1016/j.neubiorev.2021.02.008
    33. Liang Huo, Kai-Li Xu, Hua Wang. Clinical features of SARS-CoV-2-associated encephalitis and meningitis amid COVID-19 pandemic. World Journal of Clinical Cases 2021, 9 (5) , 1058-1078. https://doi.org/10.12998/wjcc.v9.i5.1058
    34. Pratima Kumari, Hussin A. Rothan, Janhavi P. Natekar, Shannon Stone, Heather Pathak, Philip G. Strate, Komal Arora, Margo A. Brinton, Mukesh Kumar. Neuroinvasion and Encephalitis Following Intranasal Inoculation of SARS-CoV-2 in K18-hACE2 Mice. Viruses 2021, 13 (1) , 132. https://doi.org/10.3390/v13010132
    35. Isabelle Pastor Bandeira, Marco Antônio Machado Schlindwein, Leticia Caroline Breis, Jean Pierre Schatzmann Peron, Marcus Vinícius Magno Gonçalves. Neurological Complications of the COVID-19 Pandemic: What Have We Got So Far?. 2021, 21-31. https://doi.org/10.1007/978-3-030-59261-5_2
    36. Morteza Mousavi-Hasanzadeh, Hossein Sarmadian, Fatemeh Safi, Mohammad Jamalian, Amir Almasi-Hashiani. Epidemiological and Clinical Characteristics of Patients with COVID-19 in Arak, Iran. The Open Public Health Journal 2020, 13 (1) , 712-717. https://doi.org/10.2174/1874944502013010712
    37. Haiyang Yu, Tong Sun, Juan Feng. Complications and Pathophysiology of COVID-19 in the Nervous System. Frontiers in Neurology 2020, 11 https://doi.org/10.3389/fneur.2020.573421
    38. Jingman Hu, Jukka Jolkkonen, Chuansheng Zhao. Neurotropism of SARS-CoV-2 and its neuropathological alterations: Similarities with other coronaviruses. Neuroscience & Biobehavioral Reviews 2020, 119 , 184-193. https://doi.org/10.1016/j.neubiorev.2020.10.012
    39. Mazigh Fares, Marielle Cochet-Bernoin, Gaëlle Gonzalez, Claudia N. Montero-Menei, Odile Blanchet, Alexandra Benchoua, Claire Boissart, Sylvie Lecollinet, Jennifer Richardson, Nadia Haddad, Muriel Coulpier. Pathological modeling of TBEV infection reveals differential innate immune responses in human neurons and astrocytes that correlate with their susceptibility to infection. Journal of Neuroinflammation 2020, 17 (1) https://doi.org/10.1186/s12974-020-01756-x
    40. Waqas Ahmed, Adeel Khan, Wish Hal Sundar, Humaira Naseem, Wanghao Chen, Jia Feng, Samran Durrani, Lukui Chen. Neurological diseases caused by coronavirus infection of the respiratory airways. Brain Science Advances 2020, 6 (4) , 324-343. https://doi.org/10.26599/BSA.2020.9050022
    41. Leon Fodoulian, Joël Tuberosa, Daniel Rossier, Madlaina Boillat, Chenda Kan, Véronique Pauli, Kristof Egervari, Johannes A. Lobrinus, Basile N. Landis, Alan Carleton, Ivan Rodriguez. SARS-CoV-2 Receptors and Entry Genes Are Expressed in the Human Olfactory Neuroepithelium and Brain. iScience 2020, 23 (12) , 101839. https://doi.org/10.1016/j.isci.2020.101839
    42. Souhel Najjar, Amanda Najjar, Derek J. Chong, Bidyut K. Pramanik, Claudia Kirsch, Ruben I. Kuzniecky, Steven V. Pacia, Salman Azhar. Central nervous system complications associated with SARS-CoV-2 infection: integrative concepts of pathophysiology and case reports. Journal of Neuroinflammation 2020, 17 (1) https://doi.org/10.1186/s12974-020-01896-0
    43. Simon Pan, Willam C. Chen, Joe D. Baal, Leo P. Sugrue. Neuroradiological Features of Mild and Severe SARS-CoV-2 Infection. Academic Radiology 2020, 27 (11) , 1507-1514. https://doi.org/10.1016/j.acra.2020.08.026
    44. Shweta Jakhmola, Omkar Indari, Sayantani Chatterjee, Hem Chandra Jha. SARS-CoV-2, an Underestimated Pathogen of the Nervous System. SN Comprehensive Clinical Medicine 2020, 2 (11) , 2137-2146. https://doi.org/10.1007/s42399-020-00522-7
    45. Niloufar Yazdanpanah, Amene Saghazadeh, Nima Rezaei. Anosmia: a missing link in the neuroimmunology of coronavirus disease 2019 (COVID-19). Reviews in the Neurosciences 2020, 31 (7) , 691-701. https://doi.org/10.1515/revneuro-2020-0039
    46. S.D. Le Bon, M. Horoi. Is anosmia the price to pay in an immune-induced scorched-earth policy against COVID-19?. Medical Hypotheses 2020, 143 , 109881. https://doi.org/10.1016/j.mehy.2020.109881
    47. Debasmita Mukhopadhyay, Bashair M. Mussa. Identification of Novel Hypothalamic MicroRNAs as Promising Therapeutics for SARS-CoV-2 by Regulating ACE2 and TMPRSS2 Expression: An In Silico Analysis. Brain Sciences 2020, 10 (10) , 666. https://doi.org/10.3390/brainsci10100666
    48. A. Giorli, F. Ferretti, C. Biagini, L. Salerni, I. Bindi, S. Dasgupta, A. Pozza, G. Gualtieri, R. Gusinu, A. Coluccia, Marco Mandalà. A Literature Systematic Review with Meta-Analysis of Symptoms Prevalence in Covid-19: the Relevance of Olfactory Symptoms in Infection Not Requiring Hospitalization. Current Treatment Options in Neurology 2020, 22 (10) https://doi.org/10.1007/s11940-020-00641-5
    49. Bertrand Bryche, Maxence Frétaud, Audrey Saint‐Albin Deliot, Marie Galloux, Laura Sedano, Christelle Langevin, Delphyne Descamps, Marie‐Anne Rameix‐Welti, Jean‐François Eléouët, Ronan Le Goffic, Nicolas Meunier. Respiratory syncytial virus tropism for olfactory sensory neurons in mice. Journal of Neurochemistry 2020, 155 (2) , 137-153. https://doi.org/10.1111/jnc.14936
    50. Giuseppe Chiarella, Raffaella Pizzolato, Donatella Malanga, Davide Pisani, Ludovico Abenavoli, Pasquale Viola. Prevention of COVID-19 Infection in the Medical Population: Possible Help from Anosmia?. Reviews on Recent Clinical Trials 2020, 15 (3) , 244-245. https://doi.org/10.2174/1574887115666200603152637
    51. Alessandra Gori, Fabrizio Leone, Lorenzo Loffredo, Bianca Laura Cinicola, Giulia Brindisi, Giovanna De Castro, Alberto Spalice, Marzia Duse, Anna Maria Zicari. COVID-19-Related Anosmia: The Olfactory Pathway Hypothesis and Early Intervention. Frontiers in Neurology 2020, 11 https://doi.org/10.3389/fneur.2020.00956
    52. Daniele Armocida, Mauro Palmieri, Alessandro Frati, Antonio Santoro, Alessandro Pesce. How SARS-Cov-2 can involve the central nervous system. A systematic analysis of literature of the department of human neurosciences of Sapienza University, Italy. Journal of Clinical Neuroscience 2020, 79 , 231-236. https://doi.org/10.1016/j.jocn.2020.07.007
    53. Pankoj Kumar Das, Irene Salinas. Fish nasal immunity: From mucosal vaccines to neuroimmunology. Fish & Shellfish Immunology 2020, 104 , 165-171. https://doi.org/10.1016/j.fsi.2020.05.076
    54. Albert Y Han, Laith Mukdad, Jennifer L Long, Ivan A Lopez. Anosmia in COVID-19: Mechanisms and Significance. Chemical Senses 2020, 45 (6) , 423-428. https://doi.org/10.1093/chemse/bjaa040
    55. Anna von Mikecz, Tamara Schikowski. Effects of Airborne Nanoparticles on the Nervous System: Amyloid Protein Aggregation, Neurodegeneration and Neurodegenerative Diseases. Nanomaterials 2020, 10 (7) , 1349. https://doi.org/10.3390/nano10071349
    56. Antonino Giordano, Ghil Schwarz, Laura Cacciaguerra, Federica Esposito, Massimo Filippi. COVID-19: can we learn from encephalitis lethargica?. The Lancet Neurology 2020, 19 (7) , 570. https://doi.org/10.1016/S1474-4422(20)30189-7
    57. Keiland W. Cooper, David H. Brann, Michael C. Farruggia, Surabhi Bhutani, Robert Pellegrino, Tatsuya Tsukahara, Caleb Weinreb, Paule V. Joseph, Eric D. Larson, Valentina Parma, Mark W. Albers, Linda A. Barlow, Sandeep Robert Datta, Antonella Di Pizio. COVID-19 and the Chemical Senses: Supporting Players Take Center Stage. Neuron 2020, 107 (2) , 219-233. https://doi.org/10.1016/j.neuron.2020.06.032
    58. Matteo Briguglio, Alberto Bona, Mauro Porta, Bernardo Dell'Osso, Fabrizio Ernesto Pregliasco, Giuseppe Banfi. Disentangling the Hypothesis of Host Dysosmia and SARS-CoV-2: The Bait Symptom That Hides Neglected Neurophysiological Routes. Frontiers in Physiology 2020, 11 https://doi.org/10.3389/fphys.2020.00671
    59. Mehmet Hakan Ozdener, Martina Donadoni, Stephanie Cicalese, Andrew I. Spielman, Alvaro Garcia-Blanco, Jennifer Gordon, Ilker Kudret Sariyer. Zika virus infection in chemosensory cells. Journal of NeuroVirology 2020, 26 (3) , 371-381. https://doi.org/10.1007/s13365-020-00835-2
    60. Joy D. Iroegbu, Chibuzor W. Ifenatuoha, Omamuyovwi M. Ijomone. Potential neurological impact of coronaviruses: implications for the novel SARS-CoV-2. Neurological Sciences 2020, 41 (6) , 1329-1337. https://doi.org/10.1007/s10072-020-04469-4
    61. Nobuyuki Kobayashi, Naomi Oka, Mayumi Takahashi, Kazuya Shimada, Azusa Ishii, Yoshitaka Tatebayashi, Masahiro Shigeta, Hiroyuki Yanagisawa, Kazuhiro Kondo. Human Herpesvirus 6B Greatly Increases Risk of Depression by Activating Hypothalamic-Pituitary -Adrenal Axis during Latent Phase of Infection. iScience 2020, 23 (6) , 101187. https://doi.org/10.1016/j.isci.2020.101187
    62. Xingliang Feng, Meng Zhang, Jialin Meng, Yongqiang Wang, Yi Liu, Chaozhao Liang, Song Fan. Correlating Transcriptional Networks to Papillary Renal Cell Carcinoma Survival: A Large-Scale Coexpression Analysis and Clinical Validation. Oncology Research Featuring Preclinical and Clinical Cancer Therapeutics 2020, 28 (3) , 285-297. https://doi.org/10.3727/096504020X15791676105394
    63. Valerie B. Duffy. Causes of Smell, Taste, and Oral Somatosensory Disorders Affecting Eating and Drinking. 2020, 1281-1320. https://doi.org/10.1007/978-3-030-14504-0_182
    64. Valerie B. Duffy. Causes of Smell, Taste, and Oral Somatosensory Disorders Affecting Eating and Drinking. 2020, 1-40. https://doi.org/10.1007/978-3-319-75388-1_182-1
    65. Valerie B. Duffy. Causes of Smell, Taste, and Oral Somatosensory Disorders Affecting Eating and Drinking. 2020, 1-40. https://doi.org/10.1007/978-3-319-75388-1_182-2
    66. Marc Desforges, Alain Le Coupanec, Philippe Dubeau, Andréanne Bourgouin, Louise Lajoie, Mathieu Dubé, Pierre J. Talbot. Human Coronaviruses and Other Respiratory Viruses: Underestimated Opportunistic Pathogens of the Central Nervous System?. Viruses 2020, 12 (1) , 14. https://doi.org/10.3390/v12010014
    67. Brian P. Daniels, Andrew Oberst. Outcomes of RIP Kinase Signaling During Neuroinvasive Viral Infection. 2020https://doi.org/10.1007/82_2020_204
    68. Bertrand Bryche, Aurélie Dewaele, Audrey Saint-Albin, Claire Le Poupon Schlegel, Patrice Congar, Nicolas Meunier. IL-17c is involved in olfactory mucosa responses to Poly(I:C) mimicking virus presence. Brain, Behavior, and Immunity 2019, 79 , 274-283. https://doi.org/10.1016/j.bbi.2019.02.012
    69. Taekyun Shin, Jeongtae Kim, Meejung Ahn, Changjong Moon. Olfactory Dysfunction in CNS Neuroimmunological Disorders: a Review. Molecular Neurobiology 2019, 56 (5) , 3714-3721. https://doi.org/10.1007/s12035-018-1341-0
    70. Elisa Casadei, Irene Salinas. Comparative models for human nasal infections and immunity. Developmental & Comparative Immunology 2019, 92 , 212-222. https://doi.org/10.1016/j.dci.2018.11.022
    71. Forrest Keck, Stephanie Kortchak, Allison Bakovic, Brian Roberts, Nitin Agrawal, Aarthi Narayanan. Direct and indirect pro-inflammatory cytokine response resulting from TC-83 infection of glial cells. Virulence 2018, 9 (1) , 1403-1421. https://doi.org/10.1080/21505594.2018.1509668
    72. Rebecca Johnson, Mary Tachedjian, Brenton Rowe, Bronwyn Clayton, Rachel Layton, Jemma Bergfeld, Lin-Fa Wang, Ina Smith, Glenn Marsh. Alston Virus, a Novel Paramyxovirus Isolated from Bats Causes Upper Respiratory Tract Infection in Experimentally Challenged Ferrets. Viruses 2018, 10 (12) , 675. https://doi.org/10.3390/v10120675
    73. Forrest Keck, Daud Khan, Brian Roberts, Nitin Agrawal, Nishank Bhalla, Aarthi Narayanan. Mitochondrial-Directed Antioxidant Reduces Microglial-Induced Inflammation in Murine In Vitro Model of TC-83 Infection. Viruses 2018, 10 (11) , 606. https://doi.org/10.3390/v10110606
    74. Olga A. Maximova, Alexander G. Pletnev. Flaviviruses and the Central Nervous System: Revisiting Neuropathological Concepts. Annual Review of Virology 2018, 5 (1) , 255-272. https://doi.org/10.1146/annurev-virology-092917-043439
    75. María E. Rivarola, Soledad de Olmos, Guillermo Albrieu-Llinás, Laura B. Tauro, Melisa Gorosito-Serrán, Brenda S. Konigheim, Marta S. Contigiani, Adriana Gruppi. Neuronal Degeneration in Mice Induced by an Epidemic Strain of Saint Louis Encephalitis Virus Isolated in Argentina. Frontiers in Microbiology 2018, 9 https://doi.org/10.3389/fmicb.2018.01181
    76. Monica Manglani, Dorian B McGavern. New advances in CNS immunity against viral infection. Current Opinion in Virology 2018, 28 , 116-126. https://doi.org/10.1016/j.coviro.2017.12.003
    77. Marco Tullio Liuzza, Torun Lindholm, Caitlin Hawley, Marie Gustafsson Sendén, Ingrid Ekström, Mats J. Olsson, Maria Larsson, Jonas K. Olofsson. The Body Odor Disgust Scale (BODS): Development and Validation of a Novel Olfactory Disgust Assessment. Chemical Senses 2016, 22 , bjw107. https://doi.org/10.1093/chemse/bjw107
    Download PDF

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect