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Review Article | Open Access

Crosstalk between Sensory Neurons and Local Immunity during Peripheral Inflammation

Department of Anesthesiology and Perioperative Medicine, the Second Affiliated Hospital of Anhui Medical University; Key Laboratory of Anesthesiology and Perioperative Medicine of Anhui Higher Education Institutes, Anhui Medical University, Hefei 230032, China
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Abstract

Sensory neurons, also known as afferent neurons, perceive noxious stimuli from internal as well as external environments through nociceptive receptors and then transmit these signals to the central nervous system. Similarly, the innate immune system also recognizes external and internal danger signals from invading microbes or tissue injuries. The immune system and sensory neurons share mechanisms to respond to pathogen/damage-associated molecular patterns (PAMPs/DAMPs) through pattern recognition receptors. Recent studies have identified an inseparable bidirectional connection between sensory neurons and the immune system that is important for maintaining tissue homeostasis and regulating inflammatory states, as well as affecting the progression of inflammatory diseases. This review summarizes the recent findings on the crosstalk between sensory neurons and local immunity in peripheral tissues, including the skin, respiratory system, gastrointestinal tract, cornea, and joints. Understanding the mechanisms of this interaction can help in the development of therapeutic strategies to treat peripheral inflammatory diseases.

References

[1]
Chiu I M, Hehn C A v, Woolf C J. Neurogenic inflammation and the peripheral nervous system in host defense and immunopathology. Nat Neurosci, 2012, 15(8): 10631067.
[2]
Veiga-Fernandes H, Pachnis V. Neuroimmune regulation during intestinal development and homeostasis. Nat Immunol, 2017, 18(2): 116122.
[3]
Godinho-Silva C, Cardoso F, Veiga-Fernandes H. Neuro-Immune Cell Units: A New Paradigm in Physiology. Annu Rev Immunol, 2019, 37: 1946.
[4]
Cai Y, Shen X, Ding C, et al. Pivotal role of dermal IL-17-producing gammadelta T cells in skin inflammation. Immunity, 2011, 35(4): 596610.
[5]
Riol-Blanco L, Ordovas-Montanes J, Perro M, et al. Nociceptive sensory neurons drive interleukin-23-mediated psoriasiform skin inflammation. Nature, 2014, 510(7503): 157161.
[6]
Cohen J A, Edwards T N, Liu A W, et al. Cutaneous TRPV1(+) Neurons Trigger Protective Innate Type 17 Anticipatory Immunity. Cell, 2019, 178(4): 919-932 e914.
[7]
Steinhoff M, Neisius U, Ikoma A, et al. Proteinase-Activated Receptor-2 Mediates Itch: A Novel Pathway for Pruritus in Human Skin. J Neurosci, 2003, 23(15): 61766180.
[8]
Chen W, Shu Q, Fan J. Neural Regulation of Interactions Between Group 2 Innate Lymphoid Cells and Pulmonary Immune Cells. Front Immunol, 2020, 11: 576929.
[9]
Moriyama M, Furue H, Katafuchi T, et al. Presynaptic modulation by neuromedin U of sensory synaptic transmission in rat spinal dorsal horn neurones. J Physiol, 2004, 559(Pt 3): 707713.
[10]
Hedrick J A, Morse K, Shan L, et al. Identification of a Human Gastrointestinal Tract and Immune System Receptor for the Peptide Neuromedin U. Mol Pharmacol, 2000, 58(4): 870875.
[11]
Wallrapp A, Riesenfeld S J, Burkett P R, et al. The neuropeptide NMU amplifies ILC2-driven allergic lung inflammation. Nature, 2017, 549(7672): 351356.
[12]
Chen W, Lai D, Li Y, et al. Neuronal-Activated ILC2s Promote IL-17A Production in Lung gammadelta T Cells During Sepsis. Front Immunol, 2021, 12: 670676.
[13]
Omar S, Clarke R, Abdullah H, et al. Respiratory virus infection up-regulates TRPV1, TRPA1 and ASICS3 receptors on airway cells. PLoS One, 2017, 12(2): e0171681.
[14]
Baral P, Umans B D, Wei Y, et al. Nociceptor sensory neurons suppress neutrophil and γδ T cell responses in bacterial lung infections and lethal pneumonia. nature medicine, 2018, 24(4): 417426.
[15]
Khalil M, Zhang Z, Engel M A. Neuro-Immune Networks in Gastrointestinal Disorders. Visc Med, 2019, 35(1): 5260.
[16]
Barbara G, Wang B, Stanghellini V, et al. Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology, 2007, 132(1): 2637.
[17]
Hughes P A, Harrington A M, Castro J, et al. Sensory neuro-immune interactions differ between irritable bowel syndrome subtypes. Gut, 2013, 62(10): 14561465.
[18]
Korzenik J R, Podolsky D K. Evolving knowledge and therapy of inflammatory bowel disease. Nat Rev Drug Discov, 2006, 5(3): 197209.
[19]
Engel M A, Leffler A, Niedermirtl F, et al. TRPA1 and substance P mediate colitis in mice. Gastroenterology, 2011, 141(4): 13461358.
[20]
Margolis K G, Gershon M D. Neuropeptides and inflammatory bowel disease. Curr Opin Gastroenterol, 2009, 25(6): 503511.
[21]
Koon H W, Zhao D, Na X, et al. Metalloproteinases and transforming growth factor-alpha mediate substance P-induced mitogen-activated protein kinase activation and proliferation in human colonocytes. J Biol Chem, 2004, 279(44): 4551945527.
[22]
Populin L, Stebbing M J, Furness J B. Neuronal regulation of the gut immune system and neuromodulation for treating inflammatory bowel disease. FASEB Bioadv, 2021, 3(11): 953966.
[23]
de Jong P R, Takahashi N, Peiris M, et al. TRPM8 on mucosal sensory nerves regulates colitogenic responses by innate immune cells via CGRP. Mucosal Immunol, 2015, 8(3): 491504.
[24]
Di Giovangiulio M, Verheijden S, Bosmans G, et al. The Neuromodulation of the Intestinal Immune System and Its Relevance in Inflammatory Bowel Disease. Front Immunol, 2015 6: 590.
[25]
Delgado M, Gonzalez-Rey E, Ganea D. The Neuropeptide Vasoactive Intestinal Peptide Generates Tolerogenic Dendritic Cells. J Immunol, 2005, 175(11): 73117324.
[26]
Stakenborg N, Viola M F, Boeckxstaens G E. Intestinal neuro-immune interactions: focus on macrophages, mast cells and innate lymphoid cells. Curr Opin Neurobiol, 2020, 62: 6875.
[27]
Salzer I, Gantumur E, Yousuf A, et al. Control of sensory neuron excitability by serotonin involves 5HT2C receptors and Ca(2+)-activated chloride channels. Neuropharmacology, 2016, 110(Pt A): 277286.
[28]
Seillet C, Luong K, Tellier J, et al. The neuropeptide VIP confers anticipatory mucosal immunity by regulating ILC3 activity. Nat Immunol, 2020, 21(2): 168177.
[29]
Klose C S N, Mahlakoiv T, Moeller J B, et al. The neuropeptide neuromedin U stimulates innate lymphoid cells and type 2 inflammation. Nature, 2017, 549(7671): 282286.
[30]
Hori J, Vega J L, Masli S. Review of ocular immune privilege in the year 2010: modifying the immune privilege of the eye. Ocul Immunol Inflamm, 2010, 18(5): 325333.
[31]
Liu J, Li Z. Resident Innate Immune Cells in the Cornea. Frontiers in Immunology, 2021, 12:620284.
[32]
Al-Aqaba M A, Dhillon V K, Mohammed I, et al. Corneal nerves in health and disease. Prog Retin Eye Res, 2019, 73: 100762.
[33]
Belmonte C, Aracil A, Acosta M C, et al. Nerves and sensations from the eye surface. Ocul Surf, 2004, 2(4): 248-253.
[34]
Parra A, Madrid R, Echevarria D, et al. Ocular surface wetness is regulated by TRPM8-dependent cold thermoreceptors of the cornea. Nat Med, 2010, 16(12): 13961399.
[35]
Lasagni Vitar R M, Rama P, Ferrari G. The two-faced effects of nerves and neuropeptides in corneal diseases. Prog Retin Eye Res, 2022, 86: 100974.
[36]
Yuan K, Zheng J, Shen X, et al. Sensory nerves promote corneal inflammation resolution via CGRP mediated transformation of macrophages to the M2 phenotype through the PI3K/AKT signaling pathway. Int Immunopharmacol, 2022, 102: 108426.
[37]
Fukui S, Iwamoto N, Takatani A, et al. M1 and M2 Monocytes in Rheumatoid Arthritis: A Contribution of Imbalance of M1/M2 Monocytes to Osteoclastogenesis. Frontiers in Immunology, 2018, 8: 1958
[38]
Liu J, Huang S, Yu R, et al. TRPV1(+) sensory nerves modulate corneal inflammation after epithelial abrasion via RAMP1 and SSTR5 signaling. Mucosal Immunol, 2022, 15(5): 867881.
[39]
Liu L, Dana R, Yin J. Sensory neurons directly promote angiogenesis in response to inflammation via substance P signaling. The FASEB Journal, 2020, 34(5): 62296243.
[40]
Borbely E, Botz B, Bolcskei K, et al. Capsaicin-sensitive sensory nerves exert complex regulatory functions in the serum-transfer mouse model of autoimmune arthritis. Brain Behav Immun, 2015, 45: 5059.
[41]
Uematsu T, Sakai A, Ito H, et al. Intra-articular administration of tachykinin NK(1) receptor antagonists reduces hyperalgesia and cartilage destruction in the inflammatory joint in rats with adjuvant-induced arthritis. Eur J Pharmacol, 2011, 668(1-2): 163168.
[42]
Walsh DA, Mapp PI, Kelly S. Calcitonin gene-related peptide in the joint: contributions to pain and inflammation. Br J Clin Pharmacol, 2015, 80(5): 96578.
[43]
Mei J, Zhou F, Qiao H, et al. Nerve modulation therapy in gouty arthritis: targeting increased sFRP2 expression in dorsal root ganglion regulates macrophage polarization and alleviates endothelial damage. Theranostics, 2019, 9(13): 37073722.
[44]
Gao D, Gao X, Yang F, et al. Neuroimmune Crosstalk in Rheumatoid Arthritis. International Journal of Molecular Sciences, 2022, 23(15) : 8158.
[45]
Ebbinghaus M, Uhlig B, Richter F, et al. The role of interleukin-1beta in arthritic pain: main involvement in thermal, but not mechanical, hyperalgesia in rat antigen-induced arthritis. Arthritis Rheum, 2012, 64(12): 38973907.
[46]
Silverman HA, Chen A, Kravatz NL, et al. Involvement of Neural Transient Receptor Potential Channels in Peripheral Inflammation. Front Immunol, 2020, 11: 590261.
[47]
Zhang W, Lyu M, Bessman NJ, et al. Gut-innervating nociceptors regulate the intestinal microbiota to promote tissue protection. Cell, 2022, 185(22): 41704189 e20.
[48]
Yu M, Lee SM, Lee H, et al. Neurokinin-1 Receptor Antagonism Ameliorates Dry Eye Disease by Inhibiting Antigen-Presenting Cell Maturation and T Helper 17 Cell Activation. Am J Pathol, 2020, 190(1): 125133.
[49]
Johnson MB, Suptela SR, Sipprell SE, et al. Substance P Exacerbates the Inflammatory and Pro-osteoclastogenic Responses of Murine Osteoclasts and Osteoblasts to Staphylococcus aureus. Inflammation, 2023, 46(1): 256269.
[50]
Benschop RJ, Collins EC, Darling RJ, et al. Development of a novel antibody to calcitonin gene-related peptide for the treatment of osteoarthritis-related pain. Osteoarthritis Cartilage, 2014, 22(4): 57885.
[51]
Bonaz B, Sinniger V, Pellissier S. Anti-inflammatory properties of the vagus nerve: potential therapeutic implications of vagus nerve stimulation. J Physiol, 2016, 594(20): 57815790.
[52]
Bonaz B, Sinniger V, Pellissier S. Therapeutic Potential of Vagus Nerve Stimulation for Inflammatory Bowel Diseases. Front Neurosci, 2021, 15: 650971.
Stress and Brain
Pages 69-79
Cite this article:
Qile M, He S. Crosstalk between Sensory Neurons and Local Immunity during Peripheral Inflammation. Stress and Brain, 2023, 3(2): 69-79. https://doi.org/10.26599/SAB.2022.9060001

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Received: 27 June 2023
Accepted: 14 August 2023
Published: 05 October 2023
© The Author(s) 2023

Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attributtion-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission.

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