CC BY-NC-ND 4.0 · J Pediatr Infect Dis 2024; 19(02): 107-115
DOI: 10.1055/s-0044-1779519
Original Article

Periostin Modulating Mycoplasma pneumoniae Pneumonia in Children Related to Th17 Cell Function

1   Department of Respiration, Guangzhou Women and Children's Medical Center, Guangzhou Medical University, Guangzhou, Guangdong, China
,
Diyuan Yang
1   Department of Respiration, Guangzhou Women and Children's Medical Center, Guangzhou Medical University, Guangzhou, Guangdong, China
,
Tingting Shi
1   Department of Respiration, Guangzhou Women and Children's Medical Center, Guangzhou Medical University, Guangzhou, Guangdong, China
,
Dongwei Zhang
1   Department of Respiration, Guangzhou Women and Children's Medical Center, Guangzhou Medical University, Guangzhou, Guangdong, China
,
Gen Lu
1   Department of Respiration, Guangzhou Women and Children's Medical Center, Guangzhou Medical University, Guangzhou, Guangdong, China
› Author Affiliations
Funding The study was approved by Guangzhou Municipal Science and Technology Bureau, China (No. 202201010822) and Guangzhou Women and Children's Medical Center, Guangzhou, China (Nos. YIP-2018-011 and NKE-PRE-2019-013).

Abstract

ObjectiveMycoplasma pneumoniae pneumonia (MPP) is recognized as a significant respiratory tract infection in children. Periostin associates with airway remodeling, and the T helper 17 (Th17) cells play a crucial role against M. pneumoniae infection. This study investigates the effect of periostin in Th17 cells and the associated mechanism in MPP.

Methods The study investigated the role of periostin stimulated with pulmonary bronchoalveolar lavage fluid (BALF) from MPP. Levels of infection of M. pneumoniae were determined using quantitative real-time polymerase chain reaction. The periostin was cloned into vector, and siRNA fragment were synthesized. The Th17 cells were transfected with the vector and the fragment, and its expression and proinflammatory cytokines (interleukin [IL]-6, tumor necrosis factor [TNF]-α, and IL-1β) were determined using western blot. The cell apoptosis, migration, and proliferation were measured using flow cytometer, transwell migration, and cell counting kit-8 assay, respectively.

Results The results showed that periostin expression had a positive correlation with MPP severity. Fluorescence-activated cell sorting analysis showed that the periostin inhibited the apoptosis of Th17 cells. Moreover, transwell migration showed a significant increased migration in Th17 cell was detected treated with BALF, and selective knockdown of periostin by specific siRNA had negative effect on cell migration. Western blot analysis showed the periostin induced the expression of the proinflammatory cytokines (IL-6, TNF-α, and IL-1β), and downregulation of periostin could decrease the expression of cytokines in MPP group.

Conclusion The study suggested that periostin is required for Th17 cells migration, and it also has effect on Th17 apoptosis and proinflammatory cytokines expression in MPP.

Supplementary Material



Publication History

Received: 28 August 2023

Accepted: 29 December 2023

Article published online:
04 March 2024

© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Bajantri B, Venkatram S, Diaz-Fuentes G. Mycoplasma pneumoniae: a potentially severe infection. J Clin Med Res 2018; 10 (07) 535-544
  • 2 Wu HM, Wong KS, Huang YC. et al. Macrolide-resistant Mycoplasma pneumoniae in children in Taiwan. J Infect Chemother 2013; 19 (04) 782-786
  • 3 Hsieh YC, Tsao KC, Huang CG. et al. Life-threatening pneumonia caused by macrolide-resistant Mycoplasma pneumoniae . Pediatr Infect Dis J 2012; 31 (02) 208-209
  • 4 Zhao JL, Wang X, Wang YS. Relationships between Th1/Th2 cytokine profiles and chest radiographic manifestations in childhood Mycoplasma pneumoniae pneumonia. Ther Clin Risk Manag 2016; 12: 1683-1692
  • 5 Becker A, Kannan TR, Taylor AB. et al. Structure of CARDS toxin, a unique ADP-ribosylating and vacuolating cytotoxin from Mycoplasma pneumoniae . Proc Natl Acad Sci U S A 2015; 112 (16) 5165-5170
  • 6 Zhang Z, Wan R, Yuan Q. et al. Cell damage and neutrophils promote the infection of Mycoplasma pneumoniae and inflammatory response. Microb Pathog 2022; 169: 105647
  • 7 Medina JL, Coalson JJ, Brooks EG. et al. Mycoplasma pneumoniae CARDS toxin induces pulmonary eosinophilic and lymphocytic inflammation. Am J Respir Cell Mol Biol 2012; 46 (06) 815-822
  • 8 Medina JL, Coalson JJ, Brooks EG. et al. Mycoplasma pneumoniae CARDS toxin exacerbates ovalbumin-induced asthma-like inflammation in BALB/c mice. PLoS One 2014; 9 (07) e102613
  • 9 Takayama G, Arima K, Kanaji T. et al. Periostin: a novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals. J Allergy Clin Immunol 2006; 118 (01) 98-104
  • 10 Conway SJ, Izuhara K, Kudo Y. et al. The role of periostin in tissue remodeling across health and disease. Cell Mol Life Sci 2014; 71 (07) 1279-1288
  • 11 Izuhara K, Conway SJ, Moore BB. et al. Roles of periostin in respiratory disorders. Am J Respir Crit Care Med 2016; 193 (09) 949-956
  • 12 Halasz E, Townes-Anderson E, Wang W. LIM kinases in synaptic plasticity and their potential as therapeutic targets. Neural Regen Res 2020; 15 (08) 1471-1472
  • 13 Guo H, He Z, Li M, Wang T, Zhang L. Imbalance of peripheral blood Th17 and Treg responses in children with refractory Mycoplasma pneumoniae pneumonia. J Infect Chemother 2016; 22 (03) 162-166
  • 14 Wang X, Chen X, Tang H. et al. Increased frequency of Th17 cells in children with Mycoplasma pneumoniae pneumonia. J Clin Lab Anal 2016; 30 (06) 1214-1219
  • 15 Li QL, Wu YY, Sun HM. et al. The role of miR-29c/B7-H3/Th17 axis in children with Mycoplasma pneumoniae pneumonia. Ital J Pediatr 2019; 45 (01) 61
  • 16 Du F, Garg AV, Kosar K. et al. Inflammatory Th17 cells express integrin αvβ3 for pathogenic function. Cell Rep 2016; 16 (05) 1339-1351
  • 17 Butcher JT, Norris RA, Hoffman S, Mjaatvedt CH, Markwald RR. Periostin promotes atrioventricular mesenchyme matrix invasion and remodeling mediated by integrin signaling through Rho/PI 3-kinase. Dev Biol 2007; 302 (01) 256-266
  • 18 Bradley JS, Byington CL, Shah SS. et al; Pediatric Infectious Diseases Society and the Infectious Diseases Society of America. The management of community-acquired pneumonia in infants and children older than 3 months of age: clinical practice guidelines by the Pediatric Infectious Diseases Society and the Infectious Diseases Society of America. Clin Infect Dis 2011; 53 (07) e25-e76
  • 19 Shimizu T. Inflammation-inducing factors of Mycoplasma pneumoniae . Front Microbiol 2016; 7: 414
  • 20 Jiang Z, Li S, Zhu C, Zhou R, Leung PHM. Mycoplasma pneumoniae infections: pathogenesis and vaccine development. Pathogens 2021; 10 (02) 119
  • 21 Sonnenberg-Riethmacher E, Miehe M, Riethmacher D. Periostin in allergy and inflammation. Front Immunol 2021; 12: 722170
  • 22 Matsumoto H. Roles of periostin in asthma. Adv Exp Med Biol 2019; 1132: 145-159
  • 23 Uchida M, Shiraishi H, Ohta S. et al. Periostin, a matricellular protein, plays a role in the induction of chemokines in pulmonary fibrosis. Am J Respir Cell Mol Biol 2012; 46 (05) 677-686
  • 24 Luo Y, Li C, Zhou Z, Gong Z, Zhu C, Lei A. Biological functions of IL-17-producing cells in mycoplasma respiratory infection. Immunology 2021; 164 (02) 223-230
  • 25 Yu KW, Yao CC, Jeng JH, Shieh HY, Chen YJ. Periostin inhibits mechanical stretch-induced apoptosis in osteoblast-like MG-63 cells. J Formos Med Assoc 2018; 117 (04) 292-300
  • 26 Meng X, Zhu Y, Tao L, Zhao S, Qiu S. Periostin has a protective role in melatonin–induced cell apoptosis by inhibiting the eIF2α–ATF4 pathway in human osteoblasts. Int J Mol Med 2018; 41 (02) 1003-1012
  • 27 Liu HL, Chen Z. Periostin inhibits hypoxia-induced apoptosisin human periodontal ligament fibroblasts via the Akt/PKB signaling pathway. Int J Clin Exp Med 2017; 10: 9171-9179
  • 28 Lin JR, J Z Xu YW. Effects of losartan on immune function, t cell subsets and micro-inflammatory status in patients with chronic renal insufficiency. Acta Med Mediter 2020; 220 (02) 321-329
  • 29 Fang KN, Wang J, Ni JW. [Correlation between Mycoplasma pneumoniae DNA replication level and disease severity in children with severe Mycoplasma pneumoniae pneumonia]. Zhongguo Dang Dai Er Ke Za Zhi 2019; 21 (09) 876-880
  • 30 Shimizu T, Kida Y, Kuwano K. Cytoadherence-dependent induction of inflammatory responses by Mycoplasma pneumoniae . Immunology 2011; 133 (01) 51-61
  • 31 Li G, Fan L, Wang Y. et al. High co-expression of TNF-α and CARDS toxin is a good predictor for refractory Mycoplasma pneumoniae pneumonia. Mol Med 2019; 25 (01) 38
  • 32 Sun JH, Sun F, Yan B, Li JY, Xin L. Data mining and systematic pharmacology to reveal the mechanisms of traditional Chinese medicine in Mycoplasma pneumoniae pneumonia treatment. Biomed Pharmacother 2020; 125: 109900