#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

PTP1B negatively regulates nitric oxide-mediated Pseudomonas aeruginosa killing by neutrophils


Autoři: Lei Yue aff001;  Min Yan aff002;  Michel L. Tremblay aff003;  Tong-Jun Lin aff004;  Hua Li aff001;  Ting Yang aff001;  Xia Song aff001;  Tianhong Xie aff001;  Zhongping Xie aff001
Působiště autorů: The Institute of Medical Biology, Chinese Academy of Medical Sciences and Peking Union Medical College, Kunming, Yunnan, China aff001;  Department of Microbiology and Immunology, Kunming Medical University, Kunming, Yunnan, China aff002;  Rosalind and Morris Goodman Cancer Research Centre, Department of Biochemistry, McGill University, Montréal, Quebec, Canada aff003;  Department of Microbiology and Immunology, Dalhousie University, Halifax, Nova Scotia, Canada aff004;  Department of Pediatrics, Dalhousie University, Halifax, Nova Scotia, Canada aff005
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222753

Souhrn

Neutrophils play a critical role in host defense against Pseudomonas aeruginosa infection. Mechanisms underlying the negative regulation of neutrophil function in bacterial clearance remain incompletely defined. Here, we demonstrate that protein tyrosine phosphatase-1B (PTP1B) is a negative regulator of P. aeruginosa clearance by neutrophils. PTP1B-deficient neutrophils display greatly enhanced bacterial phagocytosis and killing, which are accompanied by increased Toll-like receptor 4 (TLR4) signaling activation and nitric oxide (NO) production following P. aeruginosa infection. Interestingly, PTP1B deficiency mainly upregulates the production of IL-6 and IFN-β, leads to enhanced TLR4-dependent STAT1 activation and iNOS expression by neutrophils following P. aeruginosa infection. Further studies reveal that PTP1B and STAT1 are physically associated. These findings demonstrate a negative regulatory mechanism in neutrophil underlying the elimination of P. aeruginosa infection though a PTP1B-STAT1 interaction.

Klíčová slova:

Biology and life sciences – Cell biology – Cellular types – Animal cells – Blood cells – White blood cells – Neutrophils – Immune cells – Cell processes – Phagocytosis – Signal transduction – Cell signaling – Membrane receptor signaling – Immune receptor signaling – STAT signaling – Microbiology – Medical microbiology – Microbial pathogens – Bacterial pathogens – Pseudomonas aeruginosa – Organisms – Bacteria – Pseudomonas – Biochemistry – Neurochemistry – Neurochemicals – Nitric oxide – Neuroscience – Molecular biology – Molecular biology techniques – Artificial gene amplification and extension – Polymerase chain reaction – Physiology – Developmental biology – Molecular development – Medicine and health sciences – Immunology – Immune system – Innate immune system – Cytokines – Pathology and laboratory medicine – Pathogens – Immune physiology – Research and analysis methods


Zdroje

1. Choi J, Oh JY, Lee YS, Hur GY, Lee SY, Shim JJ, et al. Pseudomonas aeruginosa infection increases the readmission rate of COPD patients. Int J Chron Obstruct Pulmon Dis. 2018;13:3077–83. doi: 10.2147/COPD.S173759 30323578

2. Cilloniz C, Gabarrus A, Ferrer M, Puig de la Bellacasa J, Rinaudo M, Mensa J, et al. Community-Acquired Pneumonia Due to Multidrug- and Non-Multidrug-Resistant Pseudomonas aeruginosa. Chest. 2016;150(2):415–25. doi: 10.1016/j.chest.2016.03.042 27060725.

3. Cripps AW, Dunkley ML, Clancy RL, Kyd J. Pulmonary immunity to Pseudomonas aeruginosa. Immunol Cell Biol. 1995;73(5):418–24. doi: 10.1038/icb.1995.65 8595919.

4. Bhagirath AY, Li Y, Somayajula D, Dadashi M, Badr S, Duan K. Cystic fibrosis lung environment and Pseudomonas aeruginosa infection. BMC Pulm Med. 2016;16(1):174. doi: 10.1186/s12890-016-0339-5 27919253

5. Lavoie EG, Wangdi T, Kazmierczak BI. Innate immune responses to Pseudomonas aeruginosa infection. Microbes Infect. 2011;13(14–15):1133–45. doi: 10.1016/j.micinf.2011.07.011 21839853

6. Cigana C, Lore NI, Riva C, De Fino I, Spagnuolo L, Sipione B, et al. Tracking the immunopathological response to Pseudomonas aeruginosa during respiratory infections. Sci Rep. 2016;6:21465. doi: 10.1038/srep21465 26883959

7. Parker D, Ahn D, Cohen T, Prince A. Innate Immune Signaling Activated by MDR Bacteria in the Airway. Physiol Rev. 2016;96(1):19–53. doi: 10.1152/physrev.00009.2015 26582515

8. Berger M. Inflammation in the lung in cystic fibrosis. A vicious cycle that does more harm than good? Clin Rev Allergy. 1991;9(1–2):119–42. 1884321.

9. Heeckeren A, Walenga R, Konstan MW, Bonfield T, Davis PB, Ferkol T. Excessive inflammatory response of cystic fibrosis mice to bronchopulmonary infection with Pseudomonas aeruginosa. J Clin Invest. 1997;100(11):2810–5. doi: 10.1172/JCI119828 9389746

10. Koh AY, Priebe GP, Ray C, Van Rooijen N, Pier GB. Inescapable need for neutrophils as mediators of cellular innate immunity to acute Pseudomonas aeruginosa pneumonia. Infect Immun. 2009;77(12):5300–10. doi: 10.1128/IAI.00501-09 19805527

11. Futosi K, Fodor S, Mocsai A. Neutrophil cell surface receptors and their intracellular signal transduction pathways. Int Immunopharmacol. 2013;17(3):638–50. doi: 10.1016/j.intimp.2013.06.034 23994464

12. Manda-Handzlik A, Demkow U. Neutrophils: The Role of Oxidative and Nitrosative Stress in Health and Disease. Adv Exp Med Biol. 2015;857:51–60. doi: 10.1007/5584_2015_117 25904001.

13. Vareechon C, Zmina SE, Karmakar M, Pearlman E, Rietsch A. Pseudomonas aeruginosa Effector ExoS Inhibits ROS Production in Human Neutrophils. Cell Host Microbe. 2017;21(5):611–8 e5. doi: 10.1016/j.chom.2017.04.001 28494242

14. Miller CC, Hergott CA, Rohan M, Arsenault-Mehta K, Doring G, Mehta S. Inhaled nitric oxide decreases the bacterial load in a rat model of Pseudomonas aeruginosa pneumonia. J Cyst Fibros. 2013;12(6):817–20. doi: 10.1016/j.jcf.2013.01.008 23481089.

15. Lewis RS, Kolesnik TB, Kuang Z, D’Cruz AA, Blewitt ME, Masters SL, et al. TLR regulation of SPSB1 controls inducible nitric oxide synthase induction. J Immunol. 2011;187(7):3798–805. doi: 10.4049/jimmunol.1002993 21876038.

16. Ji DB, Xu B, Liu JT, Ran FX, Cui JR. beta-Escin sodium inhibits inducible nitric oxide synthase expression via downregulation of the JAK/STAT pathway in A549 cells. Mol Carcinog. 2011;50(12):945–60. doi: 10.1002/mc.20762 21400616.

17. Aktan F. iNOS-mediated nitric oxide production and its regulation. Life Sci. 2004;75(6):639–53. doi: 10.1016/j.lfs.2003.10.042 15172174.

18. Atherton-Fessler S, Hannig G, Piwnica-Worms H. Reversible tyrosine phosphorylation and cell cycle control. Semin Cell Biol. 1993;4(6):433–42. 8305682.

19. Bourdeau A, Dube N, Tremblay ML. Cytoplasmic protein tyrosine phosphatases, regulation and function: the roles of PTP1B and TC-PTP. Curr Opin Cell Biol. 2005;17(2):203–9. doi: 10.1016/j.ceb.2005.02.001 15780598.

20. Xu H, An H, Hou J, Han C, Wang P, Yu Y, et al. Phosphatase PTP1B negatively regulates MyD88- and TRIF-dependent proinflammatory cytokine and type I interferon production in TLR-triggered macrophages. Mol Immunol. 2008;45(13):3545–52. doi: 10.1016/j.molimm.2008.05.006 18571728.

21. Myers MP, Andersen JN, Cheng A, Tremblay ML, Horvath CM, Parisien JP, et al. TYK2 and JAK2 are substrates of protein-tyrosine phosphatase 1B. J Biol Chem. 2001;276(51):47771–4. doi: 10.1074/jbc.C100583200 11694501.

22. Lund IK, Hansen JA, Andersen HS, Moller NP, Billestrup N. Mechanism of protein tyrosine phosphatase 1B-mediated inhibition of leptin signalling. J Mol Endocrinol. 2005;34(2):339–51. doi: 10.1677/jme.1.01694 15821101.

23. Yue L, Xie Z, Li H, Pang Z, Junkins RD, Tremblay ML, et al. Protein Tyrosine Phosphatase-1B Negatively Impacts Host Defense against Pseudomonas aeruginosa Infection. Am J Pathol. 2016;186(5):1234–44. doi: 10.1016/j.ajpath.2016.01.005 27105736.

24. Yue L, Pang Z, Li H, Yang T, Guo L, Liu L, et al. CXCL4 contributes to host defense against acute Pseudomonas aeruginosa lung infection. PLoS One. 2018;13(10):e0205521. doi: 10.1371/journal.pone.0205521 30296305

25. Jin YH, Li ZT, Chen H, Jiang XQ, Zhang YY, Wu F. Effect of dexmedetomidine on kidney injury in sepsis rats through TLR4/MyD88/NF-kappaB/iNOS signaling pathway. Eur Rev Med Pharmacol Sci. 2019;23(11):5020–5. doi: 10.26355/eurrev_201906_18094 31210339.

26. Kim HY, Baik JE, Ahn KB, Seo HS, Yun CH, Han SH. Streptococcus gordonii induces nitric oxide production through its lipoproteins stimulating Toll-like receptor 2 in murine macrophages. Mol Immunol. 2017;82:75–83. doi: 10.1016/j.molimm.2016.12.016 28038357.

27. Ryu JC, Kim MJ, Kwon Y, Oh JH, Yoon SS, Shin SJ, et al. Neutrophil pyroptosis mediates pathology of P. aeruginosa lung infection in the absence of the NADPH oxidase NOX2. Mucosal Immunol. 2017;10(3):757–74. doi: 10.1038/mi.2016.73 27554297.

28. Mustelin T, Vang T, Bottini N. Protein tyrosine phosphatases and the immune response. Nat Rev Immunol. 2005;5(1):43–57. doi: 10.1038/nri1530 15630428.

29. Liang X, Gupta K, Quintero JR, Cernadas M, Kobzik L, Christou H, et al. Macrophage FABP4 is required for neutrophil recruitment and bacterial clearance in Pseudomonas aeruginosa pneumonia. FASEB J. 2019;33(3):3562–74. doi: 10.1096/fj.201802002R 30462529.

30. Kim YI, Park SW, Kang IJ, Shin MK, Lee MH. Activin suppresses LPS-induced Toll-like receptor, cytokine and inducible nitric oxide synthase expression in normal human melanocytes by inhibiting NF-kappaB and MAPK pathway activation. Int J Mol Med. 2015;36(4):1165–72. doi: 10.3892/ijmm.2015.2308 26259928.

31. Junkins RD, MacNeil AJ, Wu Z, McCormick C, Lin TJ. Regulator of calcineurin 1 suppresses inflammation during respiratory tract infections. J Immunol. 2013;190(10):5178–86. doi: 10.4049/jimmunol.1203196 23589609.

32. Junkins RD, Carrigan SO, Wu Z, Stadnyk AW, Cowley E, Issekutz T, et al. Mast cells protect against Pseudomonas aeruginosa-induced lung injury. Am J Pathol. 2014;184(8):2310–21. doi: 10.1016/j.ajpath.2014.05.009 25043620.

33. Villarino AV, Kanno Y, O’Shea JJ. Mechanisms and consequences of Jak-STAT signaling in the immune system. Nat Immunol. 2017;18(4):374–84. doi: 10.1038/ni.3691 28323260.

34. Heinonen KM, Bourdeau A, Doody KM, Tremblay ML. Protein tyrosine phosphatases PTP-1B and TC-PTP play nonredundant roles in macrophage development and IFN-gamma signaling. Proc Natl Acad Sci U S A. 2009;106(23):9368–72. doi: 10.1073/pnas.0812109106 19474293

35. Lesina M, Wormann SM, Neuhofer P, Song L, Algul H. Interleukin-6 in inflammatory and malignant diseases of the pancreas. Semin Immunol. 2014;26(1):80–7. doi: 10.1016/j.smim.2014.01.002 24572992.

36. Walford HH, Doherty TA. STAT6 and lung inflammation. JAKSTAT. 2013;2(4):e25301. doi: 10.4161/jkst.25301 24416647

37. O’Sullivan R, Carrigan SO, Marshall JS, Lin TJ. Signal transducer and activator of transcription 4 (STAT4), but not IL-12 contributes to Pseudomonas aeruginosa-induced lung inflammation in mice. Immunobiology. 2008;213(6):469–79. doi: 10.1016/j.imbio.2007.11.007 18514749.

38. Pike KA, Hutchins AP, Vinette V, Theberge JF, Sabbagh L, Tremblay ML, et al. Protein tyrosine phosphatase 1B is a regulator of the interleukin-10-induced transcriptional program in macrophages. Sci Signal. 2014;7(324):ra43. doi: 10.1126/scisignal.2005020 24803538.

39. Roger T, David J, Glauser MP, Calandra T. MIF regulates innate immune responses through modulation of Toll-like receptor 4. Nature. 2001;414(6866):920–4. doi: 10.1038/414920a 11780066.

40. van Heeckeren AM, Tscheikuna J, Walenga RW, Konstan MW, Davis PB, Erokwu B, et al. Effect of Pseudomonas infection on weight loss, lung mechanics, and cytokines in mice. Am J Respir Crit Care Med. 2000;161(1):271–9. doi: 10.1164/ajrccm.161.1.9903019 10619831.

41. Luu K, Greenhill CJ, Majoros A, Decker T, Jenkins BJ, Mansell A. STAT1 plays a role in TLR signal transduction and inflammatory responses. Immunol Cell Biol. 2014;92(9):761–9. doi: 10.1038/icb.2014.51 25027037.

42. Ivashkiv LB, Donlin LT. Regulation of type I interferon responses. Nat Rev Immunol. 2014;14(1):36–49. doi: 10.1038/nri3581 24362405

43. Zhang S, Zhang ZY. PTP1B as a drug target: recent developments in PTP1B inhibitor discovery. Drug Discov Today. 2007;12(9–10):373–81. doi: 10.1016/j.drudis.2007.03.011 17467573.

44. Wiese J, Aldemir H, Schmaljohann R, Gulder TAM, Imhoff JF. Asperentin B, a New Inhibitor of the Protein Tyrosine Phosphatase 1B. Mar Drugs. 2017;15(6). doi: 10.3390/md15060191 28635658


Článek vyšel v časopise

PLOS One


2019 Číslo 9
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Svět praktické medicíny 1/2024 (znalostní test z časopisu)
nový kurz

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Význam metforminu pro „udržitelnou“ terapii diabetu
Autoři: prof. MUDr. Milan Kvapil, CSc., MBA

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#