The synergistic effect of cold stress plus particulate matter 2.5 co-exposure on the occurrence of respiratory inflammation and the post-transcriptional mechanism of cold inducible RNA-binding protein_Chinese Journal of Respiratory and Critical Care Medicine

Authors：

ZENG Man ¹ , LI Qi ^1,2,3 ,  ZHOU Xiangdong ^1,2,3 , Victor P. Kolosov ⁴ , Juliy M. Perelman ⁴ , Andrei I. Shpakou ⁵

1. First Affiliated Hospital, Hainan Medical University, Haikou, Hainan 570102, P. R. China;
2. Key Laboratory Emergency and Trauma of Ministry, Hainan Medical University, Haikou, Hainan 570102, P. R. China;
3. Innovative Unit of Island Emergency Medicine, Chinese Academy of Medical Sciences, Haikou, Hainan 570102, P. R. China;
4. Far Eastern Scientific Center of Physiology and Pathology of Respiration, Siberian Branch, Russian Academy of Medical Sciences,Blagoveschensk 675000, Russia;
5. Department of Sport and Rehabilitation Medicine, Yanka Kupala State University of Grodno, Grodno 230023, Belarus;

Corresponding author：

ZHOU Xiangdong, Email: zxd999@263.net

Keywords：

Cold inducible RNA-binding protein; Airway inflammation; Particulate matter 2.5; Cold stress

DOI：

10.7507/1671-6205.202001023

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Objective To investigate the synergistic effect of cold stress plus particulate matter 2.5 (PM2.5) co-exposure on the occurrence of respiratory inflammation and the possible post-transcriptional regulation mechanism of cold inducible RNA-binding protein (CIRP).Methods In vivo and in vitro experiments were carried out, and the lung tissue specimens from human surgical resection were observed. The rat model and cultured airway epithelial cells 16HBE were respectively divided into four groups (n=8), namely blank control group, 5 °C/18 °C group, PM2.5 group and 5 °C/18 °C+PM2.5 group. The expression of mRNA and protein of representative inflammatory cytokines and CIRP of cultured airway epithelial cells and rat bronchial/pulmonary tissues were respectively detected by ELISA, qPCR, and Western blot. Furthermore, the temporal dynamics of CIRP distribution were observed by cellular immunofluorescence. Finally, immunohistochemical method was used to observe the localization and expression of CIRP in rat and human bronchial/pulmonary tissues at the same time.Results In vivo experiments, the mRNA and protein expression levels of CIRP, interleukin-6, and tumor necrosis factor-α in 5 °C group and PM2.5 group were significantly higher than those in the control group (all P<0.05), while the expression level of mRNA and protein in 5 °C+PM2.5 group were increased most obviously (all P<0.01). The same rule also appeared in the experimental results of each group in the vitro experiment. In addition, CIRP was mainly located in the cell nucleus; compared with the control group, the intracellular shift of CIRP appeared in 18 °C group and PM2.5 group, while the migration phenomenon was most obvious in the 18 °C+PM2.5 group. In the immunohistochemistry of rat bronchus/pulmonary tissue, the expressions of CIRP in the 5 °C group and in the PM2.5 group were significantly higher than those in the control group, and the CIRP expression in 5 °C+PM2.5 group was increased most evidently. Moreover, CIRP was expressed in the bronchial epithelial mucosa of normal people and patients with chronic obstructive respiratory disease (COPD), and it is mainly located in the nucleus of airway mucosal epithelial cells. The CIRP expression of COPD patients was significantly higher than that in the normal population.Conclusion Cold stress has a sensitizing effect on airway epithelial inflammatory response induced by PM2.5, and post-transcriptional regulation of CIRP translocation from nucleus to cytoplasm may be an important mechanism.

Citation： ZENG Man, LI Qi, ZHOU Xiangdong, Victor P. Kolosov, Juliy M. Perelman, Andrei I. Shpakou. The synergistic effect of cold stress plus particulate matter 2.5 co-exposure on the occurrence of respiratory inflammation and the post-transcriptional mechanism of cold inducible RNA-binding protein. Chinese Journal of Respiratory and Critical Care Medicine, 2021, 20(3): 195-202. doi: 10.7507/1671-6205.202001023 Copy

1.	Seys SF, Daenen M, Dilissen E, et al. Effects of high altitude and cold air exposure on airway inflammation in patients with asthma. Thorax, 2013, 68(10): 906-913.
2.	Ogino K, Nagaoka K, Okuda T, et al. PM2.5-induced airway inflammation and hyperresponsiveness in NC/Nga mice. Environ Toxicol, 2017, 32(3): 1047-1054.
3.	Huang SL, Hsu MK, Chan CC. Effects of submicrometer particle compositions on cytokine production and lipid peroxidation of human bronchial epithelial cells. Environ Health Perspect, 2003, 111(4): 478-482.
4.	Yang J, Wu HQ, Zhou XD, et al. Cold-inducible RNA-binding protein mediates airway inflammation and mucus hypersecretion through a post-transcriptional regulatory mechanism under cold stress. Int J Biochem Cell Biol, 2016, 78(4): 335-348.
5.	De Leeuw F, Zhang T, Wauquier C, et al. The cold-inducible RNA-binding protein migrates from the nucleus to cytoplasmic stress granules by a methylation-dependent mechanism and acts as a translational repressor. Exp Cell Res, 2007, 313(20): 4130-4144.
6.	Qiang X, Yang WL, Wu R, et al. Cold-inducible RNA-binding protein (CIRP) triggers inflammatory responses in hemorrhagic shock and sepsis. Nat Med, 2013, 19(11): 1489-1495.
7.	刘美花, 周向东, 李琪, 等. 苦味类中药成份藉苦味受体途径对气道炎症过程的遏制效应. 中国免疫学杂志, 2017, 33(9): 1331-1335.
8.	Wiesmiller K, Keck T, Leiacker R, et al. Simultaneous in vivo measurements of intranasal air and mucosal temperature. Eur Arch Otorhinolaryngol, 2007, 264(6): 615-619.
9.	Lindemann J, Leiacker R, Stehmer V, et al. Intranasal temperature and humidity profile in patients with nasal septal perforation before and after surgical closure. Clin Otolaryngol Allied Sci, 2001, 26(5): 433-437.
10.	Lindemann J, Keck T, Scheithauer MO, et al. Nasal mucosal temperature in relation to nasal air-flow as measured by rhinomanometry. Am J Rhinol, 2007, 21(1): 46-49.
11.	刘峰, 周向东, 余红梅, 等. Elafin对气道上皮细胞黏蛋白5AC的调节作用. 中国呼吸与危重监护杂志, 2018, 17(3): 296-300.
12.	Donaldson GC, Wedzicha JA. The causes and consequences of seasonal variation in COPD exacerbations. Int J Chron Obstruct Pulmon Dis, 2014, 9(1): 1101-1110.
13.	Davis MS, Freed AN. Repeated hyperventilation causes peripheral airways inflammation, hyperreactivity, and impaired bronchodilation in dogs. Am J Respir Crit Care Med, 2001, 164(5): 785-789.
14.	Niu H, Hu W, Zhang D, et al. Variations of fine particle physiochemical properties during a heavy haze episode in the winter of Beijing. Sci Total Environ, 2016, 571(2): 103-109.
15.	Zanobetti A, Franklin M, Koutrakis P, et al. Fine particulate air pollution and its components in association with cause-specific emergency admissions. Environ. Health Glob. Access Sci Source, 2009, 8(1): 58.
16.	Lleonart ME. A new generation of proto-oncogenes: cold-inducible RNA binding proteins. Biochim Biophys Acta, 2010, 1805(1): 43-52.
17.	Wellmann S, Bührer C, Moderegger E, et al. Oxygen-regulated expression of the RNA-binding proteins RBM3 and CIRP by a HIF-1-independent mechanism. J Cell Sci, 2004, 117(Pt 9): 1785-1794.
18.	Yang C, Carrier F. The UV-inducible RNA-binding protein A18 (A18 hnRNP) plays a protective role in the genotoxic stress response. J Biol Chem, 2001, 276(50): 47277-47284.
19.	Sheikh MS, Carrier F, Papathanasiou MA, et al. Identification of several human homologs of hamster DNA damage-inducible transcripts. Cloning and characterization of a novel UV-inducible cDNA that codes for a putative RNA-binding protein. J Biol Chem, 1997, 272(42): 26720-26726.
20.	Pichon X, Wilson LA, Stoneley M, et al. RNA binding protein/RNA element interactions and the control of translation. Curr Protein Pept Sci, 2012, 13(4): 294-304.
21.	Liu J, Xue J, Zhang H, et al. Cloning, expression, and purification of cold inducible RNA-binding protein and its neuroprotective mechanism of action. Brain Res, 2015, 1597(3): 189-195.

1. Seys SF, Daenen M, Dilissen E, et al. Effects of high altitude and cold air exposure on airway inflammation in patients with asthma. Thorax, 2013, 68(10): 906-913.
2. Ogino K, Nagaoka K, Okuda T, et al. PM2.5-induced airway inflammation and hyperresponsiveness in NC/Nga mice. Environ Toxicol, 2017, 32(3): 1047-1054.
3. Huang SL, Hsu MK, Chan CC. Effects of submicrometer particle compositions on cytokine production and lipid peroxidation of human bronchial epithelial cells. Environ Health Perspect, 2003, 111(4): 478-482.
4. Yang J, Wu HQ, Zhou XD, et al. Cold-inducible RNA-binding protein mediates airway inflammation and mucus hypersecretion through a post-transcriptional regulatory mechanism under cold stress. Int J Biochem Cell Biol, 2016, 78(4): 335-348.
5. De Leeuw F, Zhang T, Wauquier C, et al. The cold-inducible RNA-binding protein migrates from the nucleus to cytoplasmic stress granules by a methylation-dependent mechanism and acts as a translational repressor. Exp Cell Res, 2007, 313(20): 4130-4144.
6. Qiang X, Yang WL, Wu R, et al. Cold-inducible RNA-binding protein (CIRP) triggers inflammatory responses in hemorrhagic shock and sepsis. Nat Med, 2013, 19(11): 1489-1495.
7. 刘美花, 周向东, 李琪, 等. 苦味类中药成份藉苦味受体途径对气道炎症过程的遏制效应. 中国免疫学杂志, 2017, 33(9): 1331-1335.
8. Wiesmiller K, Keck T, Leiacker R, et al. Simultaneous in vivo measurements of intranasal air and mucosal temperature. Eur Arch Otorhinolaryngol, 2007, 264(6): 615-619.
9. Lindemann J, Leiacker R, Stehmer V, et al. Intranasal temperature and humidity profile in patients with nasal septal perforation before and after surgical closure. Clin Otolaryngol Allied Sci, 2001, 26(5): 433-437.
10. Lindemann J, Keck T, Scheithauer MO, et al. Nasal mucosal temperature in relation to nasal air-flow as measured by rhinomanometry. Am J Rhinol, 2007, 21(1): 46-49.
11. 刘峰, 周向东, 余红梅, 等. Elafin对气道上皮细胞黏蛋白5AC的调节作用. 中国呼吸与危重监护杂志, 2018, 17(3): 296-300.
12. Donaldson GC, Wedzicha JA. The causes and consequences of seasonal variation in COPD exacerbations. Int J Chron Obstruct Pulmon Dis, 2014, 9(1): 1101-1110.
13. Davis MS, Freed AN. Repeated hyperventilation causes peripheral airways inflammation, hyperreactivity, and impaired bronchodilation in dogs. Am J Respir Crit Care Med, 2001, 164(5): 785-789.
14. Niu H, Hu W, Zhang D, et al. Variations of fine particle physiochemical properties during a heavy haze episode in the winter of Beijing. Sci Total Environ, 2016, 571(2): 103-109.
15. Zanobetti A, Franklin M, Koutrakis P, et al. Fine particulate air pollution and its components in association with cause-specific emergency admissions. Environ. Health Glob. Access Sci Source, 2009, 8(1): 58.
16. Lleonart ME. A new generation of proto-oncogenes: cold-inducible RNA binding proteins. Biochim Biophys Acta, 2010, 1805(1): 43-52.
17. Wellmann S, Bührer C, Moderegger E, et al. Oxygen-regulated expression of the RNA-binding proteins RBM3 and CIRP by a HIF-1-independent mechanism. J Cell Sci, 2004, 117(Pt 9): 1785-1794.
18. Yang C, Carrier F. The UV-inducible RNA-binding protein A18 (A18 hnRNP) plays a protective role in the genotoxic stress response. J Biol Chem, 2001, 276(50): 47277-47284.
19. Sheikh MS, Carrier F, Papathanasiou MA, et al. Identification of several human homologs of hamster DNA damage-inducible transcripts. Cloning and characterization of a novel UV-inducible cDNA that codes for a putative RNA-binding protein. J Biol Chem, 1997, 272(42): 26720-26726.
20. Pichon X, Wilson LA, Stoneley M, et al. RNA binding protein/RNA element interactions and the control of translation. Curr Protein Pept Sci, 2012, 13(4): 294-304.
21. Liu J, Xue J, Zhang H, et al. Cloning, expression, and purification of cold inducible RNA-binding protein and its neuroprotective mechanism of action. Brain Res, 2015, 1597(3): 189-195.

Chinese Journal of Respiratory and Critical Care Medicine

The synergistic effect of cold stress plus particulate matter 2.5 co-exposure on the occurrence of respiratory inflammation and the post-transcriptional mechanism of cold inducible RNA-binding protein

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