Reviews

Exploration of a new strategy for the treatment of allergic rhinitis based on the circadian clock

  • WEI Shitong ,
  • BAI Weiliang ,
  • CHANG Ziwen ,
  • GAO Zhao ,
  • LIU Tiancong
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  • Department of Otorhinolaryngology, Shengjing Hospital of China Medical University, Shenyang 110022, China

Received date: 2023-03-08

  Revised date: 2023-06-11

  Online published: 2023-09-28

Abstract

Allergic rhinitis (AR) is a type I allergic reaction mediated by specific immunoglobulin E after exposure to allergens in atopic individuals. The main symptoms of AR are nasal congestion, nasal itching, sneezing and rhinorrhea, which are worse at night or early in the morning. The circadian clock is an endogenous timing system in the organism that produces an approximate 24-hour circadian rhythm. The temporal characteristics of the changes in the symptoms of AR coincide with the circadian clock, indicating a close relationship with the biological clock. Taking the biological clock into account during the treatment can be effective in improving symptoms and the quality of life. Intrinsic biological clock molecules in mast cell (MC) regulate its activation through both IgE-dependent and non-IgE-dependent pathways, leading to exacerbation of AR at night or in the early morning. Based on the understanding of the circadian clock, three treatment strategies have been proposed. Chronotherapy reduces side effects and increases efficacy by optimizing the dosing time. Combining chronotherapy with immunotherapy is expected to shorten the duration of treatment. Targeting specific biological clock molecules is expected to be a new option. Disruption of clock genes not only affects changes in the timing of the circadian clock, but can also enhances the severity of allergic reactions and even increases susceptibility to allergic diseases, therefore, lifestyle interventions to maintain intrinsic biological clock homeostasis are critical.

Cite this article

WEI Shitong , BAI Weiliang , CHANG Ziwen , GAO Zhao , LIU Tiancong . Exploration of a new strategy for the treatment of allergic rhinitis based on the circadian clock[J]. Science & Technology Review, 2023 , 41(18) : 84 -91 . DOI: 10.3981/j.issn.1000-7857.2023.18.011

References

[1] Vandevyver S, Dejager L, Libert C. Comprehensive overview of the structure and regulation of the glucocorticoid receptor[J]. Endocrine Reviews, 2014, 35(4): 671-693.
[2] Menz G, Akdis C A, Blaser K, et al. Glucocorticoids upregulate FOXP3 expression and regulatory T cells in asthma[J]. Journal of Allergy and Clinical Immunology, 2004, 114(6): 1425-1433.
[3] 孟娟, 徐睿, 叶菁, 等. 变应性鼻炎的分类和诊断专家共识(2022, 成都)[J]. 中国眼耳鼻喉科杂志, 2022, 22(3): 215-224.
[4] Storms W. Pharmacologic approaches to daytime and nighttime symptoms of allergic rhinitis[J]. Journal of Allergy and Clinical Immunology, 2004, 114: 146-153.
[5] Smolensky M H, Lemmer B, Reinberg A E. Chronobiology and chronotherapy of allergic rhinitis and bronchial asthma[J]. Advanced Drug Delivery Reviews, 2007, 59(9-10): 852-882.
[6] Zhang Y, Lan F, Zhang L. Update on pathomechanisms and treatments in allergic rhinitis[J]. Allergy, 2022, 77(11): 3309-3319.
[7] Nakamura Y, Harama D, Shimokawa N, et al. Circadian clock gene Period2 regulates a time-of-day-dependent variation in cutaneous anaphylactic reaction[J]. Journal of Allergy and Clinical Immunology, 2011, 127(4): 1038-1045.
[8] Vandenberghe A, Lefranc M, Furlan A. An overview of the circadian clock in the frame of chronotherapy: From bench to bedside[J]. Pharmaceutics, 2022, 14(7): 14-24.
[9] Patke A, Young M W, Axelrod S. Molecular mechanisms and physiological importance of circadian rhythms[J]. Nature Reviews Molecular Cell Biology, 2020, 21(2): 67-84.
[10] Fagiani F, Di Marino D, Romagnoli A, et al. Molecular regulations of circadian rhythm and implications for physiology and diseases[J]. Signal Transduction and Targeted Therapy, 2022, 7(1): 41.
[11] Lu D, Zhao M, Chen M, et al. Circadian clock-controlled drug metabolism: Implications for chronotherapeutics[J]. Drug Metabolism and Disposition, 2020, 48(5): 395-406.
[12] Dibner C, Schibler U, Albrecht U. The mammalian circadian timing system: Organization and coordination of central and peripheral clocks[J]. Annual Review of Physiology, 2010, 72(1): 517-549.
[13] Turek F W. Circadian clocks: Not your grandfather's clock[J]. Science, 2016, 354(6315): 992-993.
[14] Mohawk J A, Green C B, Takahashi J S. Central and peripheral circadian clocks in mammals[J]. Annual Review of Neuroscience, 2012, 35: 445-462.
[15] Ruan W, Yuan X, Eltzschig H K. Circadian rhythm as a therapeutic target[J]. Nature Reviews Drug Discovery, 2021, 20(4): 287-307.
[16] Green C B. Circadian posttranscriptional regulatory mechanisms in mammals[J]. Cold Spring Harbor Perspectives in Biology, 2018, 10(6): a030692.
[17] Lee H, Chen R, Lee Y, et al. Essential roles of CKI delta and CKI epsilon in the mammalian circadian clock[J]. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(50): 21359-21364.
[18] Nakamura Y, Nakano N, Ishimaru K, et al. Inhibition of IgE-mediated allergic reactions by pharmacologically targeting the circadian clock[J]. Journal of Allergy and Clinical Immunology, 2016, 137(4): 1226-1235.
[19] Schibler U. BMAL1 dephosphorylation determines the pace of the circadian clock[J]. Genes & Development, 2021, 35(15-16): 1076-1078.
[20] Smolensky M H, Reinberg A, Labrecque G. Twenty-four hour pattern in symptom intensity of viral and allergic rhinitis: treatment implications[J]. The Journal of Allergy and Clinical Immunology, 1995, 95(5): 1084-1096.
[21] Kim H K, Kim H J, Kim J H, et al. Asymmetric expression level of clock genes in left vs. right nasal mucosa in humans with and without allergies and in rats: Circa⁃dian characteristics and possible contribution to nasal cycle[J]. PloS One, 2018, 13(3): e0194018.
[22] Ando N, Nakamura Y, Ishimaru K, et al. Allergen-specific basophil reactivity exhibits daily variations in seasonal allergic rhinitis[J]. Allergy, 2015, 70(3): 319-322.
[23] Leaker B R, Malkov V A, Mogg R, et al. The nasal mucosal late allergic reaction to grass pollen involves type 2 inflammation (IL-5 and IL-13), the inflammasome(IL-1β), and complement[J]. Mucosal Immunology, 2017, 10(2): 408-420.
[24] Wang X, Reece S P, Van Scott M R, et al. A circadian clock in murine bone marrow-derived mast cells modulates IgE-dependent activation in vitro[J]. Brain, Behavior, and Immunity, 2011, 25(1): 127-134.
[25] Nakamura Y, Nakano N, Ishimaru K, et al. Circadian regulation of allergic reactions by the mast cell clock in mice[J]. Journal of Allergy and Clinical Immunology, 2014, 133(2): 568-575.
[26] 刘果, 刘锋 . IL-33/ST2信号通路在变应性鼻炎中的研究进展[J]. 临床耳鼻咽喉头颈外科杂志, 2020, 34(6): 565-568.
[27] Nian J B, Zeng M, Zheng J, et al. Epithelial cells expressed IL-33 to promote degranulation of mast cells through inhibition on ST2/PI3K/mTOR-mediated autophagy in allergic rhinitis[J]. Cell Cycle, 2020, 19(10): 1132-1142.
[28] Kawauchi T, Ishimaru K, Nakamura Y, et al. Clock-dependent temporal regulation of IL-33/ST2-mediated mast cell response[J]. Allergology International: Official Journal of the Japanese Society of Allergology, 2017, 66(3): 472-478.
[29] Sulli G, Manoogian E N C, Taub P R, et al. Training the circadian clock, clocking the drugs, and drugging the clock to prevent, manage, and treat chronic diseases[J]. Trends in Pharmacological Sciences, 2018, 39(9): 812-827.
[30] Cardinali D P, Brown G M, Pandi-Perumal S R. Chronotherapy[J]. Handbook of Clinical Neurology, 2021, 179: 357-370.
[31] Dong D, Yang D, Lin L, et al. Circadian rhythm in pharmacokinetics and its relevance to chronotherapy[J]. Biochemical Pharmacology, 2020, 178: 114045.
[32] Urdaneta E R, Patel M K, Franklin K B, et al. Assessment of different cetirizine dosing strategies on seasonal allergic rhinitis symptoms: Findings of two randomized trials[J]. Allergy & Rhinology, 2018, 9: 1-11.
[33] Marmouz F, Giralt J, Izquierdo I. Morning and evening efficacy evaluation of rupatadine (10 and 20 mg), compared with cetirizine 10 mg in perennial allergic rhinitis: A randomized, double-blind, placebo-controlled trial[J]. Journal of Asthma and Allergy, 2011, 4: 27-35.
[34] Benninger M S, Ahmad N, Marple B F. The safety of intranasal steroids[J]. Otolaryngology-Head and Neck Surgery: Official Journal of American Academy of Otolaryngology-Head and Neck Surgery, 2003, 129(6): 739-750.
[35] Honma A, Yamada Y, Nakamaru Y, et al. Glucocorticoids reset the nasal circadian clock in mice[J]. Endocrinology, 2015, 156(11): 4302-4311.
[36] Pfaar O, Lou H, Zhang Y, et al. Recent developments and highlights in allergen immunotherapy[J]. Allergy, 2018, 73(12): 2274-2289.
[37] 顾瑜蓉, 李华斌 .《中国变应性鼻炎诊断和治疗指南(2022 年, 修订版)》解读[J]. 中国眼耳鼻喉科杂志, 2022, 22(2): 209-211.
[38] McMurray J C, Waters A M, Macomb C V, et al. Circadian and seasonal variations in subcutaneous allergen immunotherapy reactions[J]. Annals of Allergy, Asthma & Immunology, 2021, 127(5): 595-596.
[39] Bavishi A A, Grammer L C, Pongracic J, et al. Diurnal variations in subcutaneous allergen immunotherapy reactions[J]. Annals of Allergy, Asthma & Immunology, 2017, 118(1): 103-107.
[40] Aryan Z, Rezaei N. Toll-like receptors as targets for allergen immunotherapy[J]. Current Opinion in Allergy & Clinical Immunology, 2015, 15(6): 568-574.
[41] Silver A C, Arjona A, Walker W E, et al. The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity[J]. Immunity, 2012, 36(2): 251-261.
[42] Orihara K, Saito H. Controlling the peripheral clock might be a new treatment strategy in allergy and immunology[J]. Journal of Allergy and Clinical Immunology, 2016, 137(4): 1236-1237.
[43] Fan Y, Piao C H, Hyeon E, et al. Gallic acid alleviates nasal inflammation via activation of Th1 and inhibition of Th2 and Th17 in a mouse model of allergic rhinitis[J]. International Immunopharmacology, 2019, 70: 512-519.
[44] Cheng F L, An Y F, Han Z Q, et al. Period2 gene regulates diurnal changes of nasal symptoms in an allergic rhinitis mouse model[J]. International Forum of Allergy & Rhinology, 2020, 10(11): 1236-1248.
[45] Yang H, Yang L T, Liu J, et al. Circadian protein CLK suppresses transforming growth factor- β expression in peripheral B cells of nurses with day-night shift rotation[J]. American Journal of Translational Research, 2018, 10(12): 4331-4337.
[46] Wang Q, Li L, Li C, et al. Circadian protein CLOCK modulates regulatory B cell functions of nurses engaging day-night shift rotation[J]. Cellular Signalling, 2022, 96: 110362.
[47] Nakamura Y, Ishimaru K, Shibata S, et al. Regulation of plasma histamine levels by the mast cell clock and its modulation by stress[J]. Scientific Reports, 2017, 7: 39934.
[48] Kolarski D, Miró-Vinyals C, Sugiyama A, et al. Reversible modulation of circadian time with chronophotopharmacology[J]. Nature Communications, 2021, 12(1): 3164.
[49] 张艳廷, 曹济民, 赵长青. 生物钟原理及其对变应性鼻炎的调控[J]. 临床耳鼻咽喉头颈外科杂志, 2019, 33(1): 1-4.
[50] LeGates T A, Altimus C M, Wang H, et al. Aberrant light directly impairs mood and learning through melanopsin-expressing neurons[J]. Nature, 2012, 491(7425): 594-598.
[51] G Y, H Z, Y L, et al. Alternation of circadian clock modulates forkhead box protein-3 gene transcription in CD4+ T cells in the intestine[J]. The Journal of Allergy and Clinical Immunology, 2016, 138(5): 1446-1449.
[52] Palomares O, Akdis M, Martín-Fontecha M, et al. Mechanisms of immune regulation in allergic diseases: The role of regulatory T and B cells[J]. Immunological Reviews, 2017, 278(1): 219-236.
[53] M X, M P, Y D, et al. C-MAF-dependent regulatory T cells mediate immunological tolerance to a gut pathobiont[J]. Nature, 2018, 554(7692): 373-377.
[54] Cheng F L, An Y F, Xue J M, et al. Circadian rhythm disruption exacerbates Th2-like immune response in murine allergic airway inflammation[J]. International Forum of Allergy & Rhinology, 2022, 12(5): 757-770.
[55] Hesse J, Malhan D, Yalçin M, et al. An optimal time for treatment-predicting circadian time by machine learning and mathematical modelling[J]. Cancers, 2020, 12(11): 3103.
[56] Liu L P, Li M H, Zheng Y W. Hair follicles as a critical model for monitoring the circadian clock[J]. International Journal of Molecular Sciences, 2023, 24(3): 2407.
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