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Home / Equine Research Bank / PLoS One / Secretoglobin 1A1 and 1A1A differentially regulate neutrophi...
PloS one2014; 9(4); e96217; doi: 10.1371/journal.pone.0096217

Secretoglobin 1A1 and 1A1A differentially regulate neutrophil reactive oxygen species production, phagocytosis and extracellular trap formation.

Abstract: Secretoglobin family 1A member 1 (SCGB 1A1) is a small protein mainly secreted by mucosal epithelial cells of the lungs and uterus. SCGB 1A1, also known as club (Clara) cell secretory protein, represents a major constituent of airway surface fluid. The protein has anti-inflammatory properties, and its concentration is reduced in equine recurrent airway obstruction (RAO) and human asthma. RAO is characterized by reversible airway obstruction, bronchoconstriction and neutrophilic inflammation. Direct effects of SCGB 1A1 on neutrophil functions are unknown. We have recently identified that the SCGB1A1 gene is triplicated in equids and gives rise to two distinct proteins. In this study we produced the endogenously expressed forms of SCGBs (SCGB 1A1 and 1A1A) as recombinant proteins, and analyzed their effects on reactive oxygen species production, phagocytosis, chemotaxis and neutrophil extracellular trap (NET) formation ex vivo. We further evaluated whether NETs are present in vivo in control and inflamed lungs. Our data show that SCGB 1A1A but not SCGB 1A1 increase neutrophil oxidative burst and phagocytosis; and that both proteins markedly reduce neutrophil chemotaxis. SCGB 1A1A reduced chemotaxis significantly more than SCGB 1A1. NET formation was significantly reduced in a time- and concentration-dependent manner by SCGB 1A1 and 1A1A. SCGB mRNA in bronchial biopsies, and protein concentration in bronchoalveolar lavage fluid, was lower in horses with RAO. NETs were present in bronchoalveolar lavage fluid from horses with exacerbated RAO, but not in fluid from horses with RAO in remission or in challenged healthy horses. These findings indicate that SCGB 1A1 and 1A1A have overlapping and diverging functions. Considering disparities in the relative abundance of SCGB 1A1 and 1A1A in airway secretions of animals with RAO suggests that these functional differences may contribute to the pathogenesis of RAO and other neutrophilic inflammatory lung diseases.
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Publication Date: 2014-04-28 PubMed ID: 24777050PubMed Central: PMC4002474DOI: 10.1371/journal.pone.0096217Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research examines the role of two proteins, Secretoglobin 1A1 and 1A1A, in regulating the production of reactive oxygen species, phagocytosis, and neutrophil extracellular trap (NET) formation in case of lung diseases. The study found disparities in the relative abundance of these proteins in lung secretions, suggesting that these differences contribute to the progression of lung diseases characterized by neutrophilic inflammation, like equine recurrent airway obstruction and asthma.

Examining Secretoglobin Variants

  • The researchers looked at Secretoglobin family 1A member 1 (SCGB 1A1), a small protein majorly secreted by mucosal epithelial cells in lungs and uterus, which is associated with anti-inflammatory properties.
  • SCGB 1A1’s concentration has been found to be reduced in cases of equine recurrent airway obstruction (RAO) and human asthma.
  • Through this study, the researchers explored the direct effects of SCGB 1A1 on neutrophil functions (neutrophils being a type of white blood cell responsible for immune responses).
  • The researchers detected that SCGB1A1 gene is triplicated in equids, producing two distinct proteins: SCGB 1A1 and 1A1A.

Experiment and Findings

  • Through this study, both forms of the proteins (SCGB 1A1 and 1A1A) were produced as recombinant proteins and their effects on certain neutrophil functions, including reactive oxygen species production, phagocytosis, chemotaxis, and neutrophil extracellular trap (NET) formation were tested.
  • Findings revealed that SCGB 1A1A influence increased neutrophil oxidative burst and phagocytosis, while both SCGB 1A1 and 1A1A significantly reduced chemotaxis, with SCGB 1A1A reducing it more.
  • NET formation was seen to be reduced by both SCGB 1A1 and 1A1A in a time- and concentration-dependent manner.
  • It was found that horses with RAO had lower concentrations of SCGB in their bronchial biopsies and bronchoalveolar lavage fluid, while NETs were present in fluid from horses with exacerbated RAO but not in those where RAO was in remission or healthy horses.

Implications

  • The study deduces that SCGB 1A1 and 1A1A have both overlapping and diverging functions.
  • The differences in the relative abundance of these proteins in airway secretions in animals with RAO prompt the understanding that these functional disparities might contribute to the pathogenesis of RAO and other lung diseases characterized by neutrophilic inflammation.
  • Understanding the function of these proteins and their impact on the immune response could provide critical insights into potential therapeutic strategies for related lung diseases.

Cite This Article

APA
Côté O, Clark ME, Viel L, Labbé G, Seah SY, Khan MA, Douda DN, Palaniyar N, Bienzle D. (2014). Secretoglobin 1A1 and 1A1A differentially regulate neutrophil reactive oxygen species production, phagocytosis and extracellular trap formation. PLoS One, 9(4), e96217. https://doi.org/10.1371/journal.pone.0096217

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 9
Issue: 4
Pages: e96217
PII: e96217

Researcher Affiliations

Côté, Olivier
  • Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada.
Clark, Mary Ellen
  • Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada.
Viel, Laurent
  • Department of Clinical Studies, University of Guelph, Guelph, Ontario, Canada.
Labbé, Geneviève
  • Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada.
Seah, Stephen Y K
  • Department of Molecular and Cellular Biology, University of Guelph, Guelph, Ontario, Canada.
Khan, Meraj A
  • Program in Physiology and Experimental Medicine, Lung Innate Immunity Research Laboratory, Hospital for Sick Children, Toronto, Ontario, Canada.
Douda, David N
  • Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada; Program in Physiology and Experimental Medicine, Lung Innate Immunity Research Laboratory, Hospital for Sick Children, Toronto, Ontario, Canada.
Palaniyar, Nades
  • Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada; Institute of Medical Sciences, University of Toronto, Toronto, Ontario, Canada; Program in Physiology and Experimental Medicine, Lung Innate Immunity Research Laboratory, Hospital for Sick Children, Toronto, Ontario, Canada.
Bienzle, Dorothee
  • Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada.

MeSH Terms

  • Airway Obstruction / genetics
  • Airway Obstruction / metabolism
  • Animals
  • Base Sequence
  • Bronchoalveolar Lavage Fluid / chemistry
  • Chemotaxis / drug effects
  • Dose-Response Relationship, Drug
  • Extracellular Traps / drug effects
  • Extracellular Traps / metabolism
  • Horses
  • Humans
  • Interleukin-8 / pharmacology
  • Molecular Sequence Data
  • Neutrophils / cytology
  • Neutrophils / drug effects
  • Neutrophils / metabolism
  • Phagocytosis / drug effects
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Reactive Oxygen Species / metabolism
  • Recurrence
  • Respiratory Burst / drug effects
  • Secretoglobins / genetics
  • Secretoglobins / metabolism
  • Secretoglobins / pharmacology
  • Time Factors

Conflict of Interest Statement

Dr Nades Palaniyar is an Academic Editor for PLOS ONE. This does not alter the authors' adherence to PLOS ONE Editorial policies and criteria.

References

This article includes 49 references
  1. Klug J, Beier HM, Bernard A, Chilton BS, Fleming TP, Lehrer RI, Miele L, Pattabiraman N, Singh G. Uteroglobin/Clara cell 10-kDa family of proteins: nomenclature committee report.. Ann N Y Acad Sci 2000;923:348-54.
    pubmed: 11193777doi: 10.1111/j.1749-6632.2000.tb05549.xgoogle scholar: lookup
  2. Callebaut I, Poupon A, Bally R, Demaret JP, Housset D, Delettré J, Hossenlopp P, Mornon JP. The uteroglobin fold.. Ann N Y Acad Sci 2000;923:90-112.
    pubmed: 11193783doi: 10.1111/j.1749-6632.2000.tb05522.xgoogle scholar: lookup
  3. Beato M. Binding of steroids to uteroglobin.. J Steroid Biochem 1976 May;7(5):327-34.
    pubmed: 933532doi: 10.1016/0022-4731(76)90091-1google scholar: lookup
  4. López de Haro MS, Pérez Martínez M, García C, Nieto A. Binding of retinoids to uteroglobin.. FEBS Lett 1994 Aug 1;349(2):249-51.
    pubmed: 8050575doi: 10.1016/0014-5793(94)00678-4google scholar: lookup
  5. Stripp BR, Lund J, Mango GW, Doyen KC, Johnston C, Hultenby K, Nord M, Whitsett JA. Clara cell secretory protein: a determinant of PCB bioaccumulation in mammals.. Am J Physiol 1996 Oct;271(4 Pt 1):L656-64.
    pubmed: 8897914doi: 10.1152/ajplung.1996.271.4.L656google scholar: lookup
  6. Mandal AK, Zhang Z, Ray R, Choi MS, Chowdhury B, Pattabiraman N, Mukherjee AB. Uteroglobin represses allergen-induced inflammatory response by blocking PGD2 receptor-mediated functions.. J Exp Med 2004 May 17;199(10):1317-30.
    pmc: PMC2211805pubmed: 15148333doi: 10.1084/jem.20031666google scholar: lookup
  7. Andersson O, Nordlund-Möller L, Barnes HJ, Lund J. Heterologous expression of human uteroglobin/polychlorinated biphenyl-binding protein. Determination of ligand binding parameters and mechanism of phospholipase A2 inhibition in vitro.. J Biol Chem 1994 Jul 22;269(29):19081-7.
    pubmed: 7518449
  8. Umland TC, Swaminathan S, Singh G, Warty V, Furey W, Pletcher J, Sax M. Structure of a human Clara cell phospholipid-binding protein-ligand complex at 1.9 A resolution.. Nat Struct Biol 1994 Aug;1(8):538-45.
    pubmed: 7664082doi: 10.1038/nsb0894-538google scholar: lookup
  9. Pilon AL. Rationale for the development of recombinant human CC10 as a therapeutic for inflammatory and fibrotic disease.. Ann N Y Acad Sci 2000;923:280-99.
    pubmed: 11193764doi: 10.1111/j.1749-6632.2000.tb05536.xgoogle scholar: lookup
  10. Johnston CJ, Mango GW, Finkelstein JN, Stripp BR. Altered pulmonary response to hyperoxia in Clara cell secretory protein deficient mice.. Am J Respir Cell Mol Biol 1997 Aug;17(2):147-55.
    pubmed: 9271302doi: 10.1165/ajrcmb.17.2.2676google scholar: lookup
  11. Nie W, Xue C, Chen J, Xiu Q. Secretoglobin 1A member 1 (SCGB1A1) +38A/G polymorphism is associated with asthma risk: a meta-analysis.. Gene 2013 Oct 10;528(2):304-8.
    pubmed: 23820082doi: 10.1016/j.gene.2013.06.049google scholar: lookup
  12. Moreno JJ. Antiflammins: endogenous nonapeptides with regulatory effect on inflammation.. Gen Pharmacol 1997 Jan;28(1):23-6.
    pubmed: 9112072doi: 10.1016/s0306-3623(96)00151-6google scholar: lookup
  13. Levine CR, Gewolb IH, Allen K, Welch RW, Melby JM, Pollack S, Shaffer T, Pilon AL, Davis JM. The safety, pharmacokinetics, and anti-inflammatory effects of intratracheal recombinant human Clara cell protein in premature infants with respiratory distress syndrome.. Pediatr Res 2005 Jul;58(1):15-21.
    pubmed: 15774846doi: 10.1203/01.PDR.0000156371.89952.35google scholar: lookup
  14. Welty SE. CC10 administration to premature infants: in search of the "silver bullet" to prevent lung inflammation.. Pediatr Res 2005 Jul;58(1):7-9.
    pubmed: 15879298doi: 10.1203/01.PDR.0000163373.65809.F5google scholar: lookup
  15. Léguillette R. Recurrent airway obstruction--heaves.. Vet Clin North Am Equine Pract 2003 Apr;19(1):63-86, vi.
    pubmed: 12747662doi: 10.1016/s0749-0739(02)00067-6google scholar: lookup
  16. Robinson NE. International Workshop on Equine Chronic Airway Disease. Michigan State University 16-18 June 2000.. Equine Vet J 2001 Jan;33(1):5-19.
    pubmed: 11191611doi: 10.2746/042516401776767412google scholar: lookup
  17. Katavolos P, Ackerley CA, Viel L, Clark ME, Wen X, Bienzle D. Clara cell secretory protein is reduced in equine recurrent airway obstruction.. Vet Pathol 2009 Jul;46(4):604-13.
    pubmed: 19276063doi: 10.1354/vp.08-VP-0255-B-FLgoogle scholar: lookup
  18. Côté O, Lillie BN, Hayes MA, Clark ME, van den Bosch L, Katavolos P, Viel L, Bienzle D. Multiple secretoglobin 1A1 genes are differentially expressed in horses.. BMC Genomics 2012 Dec 19;13:712.
    pmc: PMC3556144pubmed: 23253434doi: 10.1186/1471-2164-13-712google scholar: lookup
  19. Côté O, Viel L, Bienzle D. Phylogenetic relationships among Perissodactyla: secretoglobin 1A1 gene duplication and triplication in the Equidae family.. Mol Phylogenet Evol 2013 Dec;69(3):430-6.
    pubmed: 23988306doi: 10.1016/j.ympev.2013.08.012google scholar: lookup
  20. Zeilhofer HU, Schorr W. Role of interleukin-8 in neutrophil signaling.. Curr Opin Hematol 2000 May;7(3):178-82.
    pubmed: 10786656doi: 10.1097/00062752-200005000-00009google scholar: lookup
  21. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation.. Nat Rev Immunol 2013 Mar;13(3):159-75.
    pubmed: 23435331doi: 10.1038/nri3399google scholar: lookup
  22. Hurst JK. What really happens in the neutrophil phagosome?. Free Radic Biol Med 2012 Aug 1;53(3):508-20.
    pmc: PMC4382085pubmed: 22609248doi: 10.1016/j.freeradbiomed.2012.05.008google scholar: lookup
  23. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. Neutrophil extracellular traps kill bacteria.. Science 2004 Mar 5;303(5663):1532-5.
    pubmed: 15001782doi: 10.1126/science.1092385google scholar: lookup
  24. Brinkmann V, Zychlinsky A. Neutrophil extracellular traps: is immunity the second function of chromatin?. J Cell Biol 2012 Sep 3;198(5):773-83.
    pmc: PMC3432757pubmed: 22945932doi: 10.1083/jcb.201203170google scholar: lookup
  25. Cheng OZ, Palaniyar N. NET balancing: a problem in inflammatory lung diseases.. Front Immunol 2013;4:1.
    pmc: PMC3553399pubmed: 23355837doi: 10.3389/fimmu.2013.00001google scholar: lookup
  26. Johansson S, Andersson K, Wennergren G, Wennerås C, Rudin A. CC16 inhibits the migration of eosinophils towards the formyl peptide fMLF but not towards PGD2.. Inflammation 2009 Apr;32(2):65-9.
    pubmed: 19132521doi: 10.1007/s10753-008-9103-1google scholar: lookup
  27. Katavolos P, Ackerley CA, Clark ME, Bienzle D. Clara cell secretory protein increases phagocytic and decreases oxidative activity of neutrophils.. Vet Immunol Immunopathol 2011 Jan;139(1):1-9.
    pubmed: 20728946doi: 10.1016/j.vetimm.2010.07.021google scholar: lookup
  28. Parker H, Dragunow M, Hampton MB, Kettle AJ, Winterbourn CC. Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus.. J Leukoc Biol 2012 Oct;92(4):841-9.
    pubmed: 22802447doi: 10.1189/jlb.1211601google scholar: lookup
  29. Douda DN, Jackson R, Grasemann H, Palaniyar N. Innate immune collectin surfactant protein D simultaneously binds both neutrophil extracellular traps and carbohydrate ligands and promotes bacterial trapping.. J Immunol 2011 Aug 15;187(4):1856-65.
    pubmed: 21724991doi: 10.4049/jimmunol.1004201google scholar: lookup
  30. Levin SW, Butler JD, Schumacher UK, Wightman PD, Mukherjee AB. Uteroglobin inhibits phospholipase A2 activity.. Life Sci 1986 May 19;38(20):1813-9.
    pubmed: 3084897doi: 10.1016/0024-3205(86)90135-9google scholar: lookup
  31. Lesur O, Bernard A, Arsalane K, Lauwerys R, Bégin R, Cantin A, Lane D. Clara cell protein (CC-16) induces a phospholipase A2-mediated inhibition of fibroblast migration in vitro.. Am J Respir Crit Care Med 1995 Jul;152(1):290-7.
    pubmed: 7541278doi: 10.1164/ajrccm.152.1.7541278google scholar: lookup
  32. Geerts L, Jorens PG, Willems J, De Ley M, Slegers H. Natural inhibitors of neutrophil function in acute respiratory distress syndrome.. Crit Care Med 2001 Oct;29(10):1920-4.
    pubmed: 11588452doi: 10.1097/00003246-200110000-00012google scholar: lookup
  33. Shijubo N, Itoh Y, Yamaguchi T, Imada A, Hirasawa M, Yamada T, Kawai T, Abe S. Clara cell protein-positive epithelial cells are reduced in small airways of asthmatics.. Am J Respir Crit Care Med 1999 Sep;160(3):930-3.
    pubmed: 10471621doi: 10.1164/ajrccm.160.3.9803113google scholar: lookup
  34. Lensmar C, Nord M, Gudmundsson GH, Roquet A, Andersson O, Jörnvall H, Eklund A, Grunewald J, Agerberth B. Decreased pulmonary levels of the anti-inflammatory Clara cell 16 kDa protein after induction of airway inflammation in asthmatics.. Cell Mol Life Sci 2000 Jun;57(6):976-81.
    pubmed: 10950311doi: 10.1007/PL00000738google scholar: lookup
  35. Burmeister R, Boe IM, Nykjaer A, Jacobsen C, Moestrup SK, Verroust P, Christensen EI, Lund J, Willnow TE. A two-receptor pathway for catabolism of Clara cell secretory protein in the kidney.. J Biol Chem 2001 Apr 20;276(16):13295-301.
    pubmed: 11278724doi: 10.1074/jbc.M010679200google scholar: lookup
  36. Bin LH, Nielson LD, Liu X, Mason RJ, Shu HB. Identification of uteroglobin-related protein 1 and macrophage scavenger receptor with collagenous structure as a lung-specific ligand-receptor pair.. J Immunol 2003 Jul 15;171(2):924-30.
    pubmed: 12847263doi: 10.4049/jimmunol.171.2.924google scholar: lookup
  37. Lee DS, Yang SH, Kim HL, Joo KW, Lim CS, Chae DW, Kim S, Lee JS, Kim YS. Recombinant uteroglobin prevents the experimental crescentic glomerulonephritis.. Kidney Int 2004 Sep;66(3):1061-7.
    pubmed: 15327399doi: 10.1111/j.1523-1755.2004.00855.xgoogle scholar: lookup
  38. Zheng F, Kundu GC, Zhang Z, Ward J, DeMayo F, Mukherjee AB. Uteroglobin is essential in preventing immunoglobulin A nephropathy in mice.. Nat Med 1999 Sep;5(9):1018-25.
    pubmed: 10470078doi: 10.1038/12458google scholar: lookup
  39. Bohdanowicz M, Grinstein S. Role of phospholipids in endocytosis, phagocytosis, and macropinocytosis.. Physiol Rev 2013 Jan;93(1):69-106.
    pubmed: 23303906doi: 10.1152/physrev.00002.2012google scholar: lookup
  40. Vasanthakumar G, Manjunath R, Mukherjee AB, Warabi H, Schiffmann E. Inhibition of phagocyte chemotaxis by uteroglobin, an inhibitor of blastocyst rejection.. Biochem Pharmacol 1988 Feb 1;37(3):389-94.
    pubmed: 3337740doi: 10.1016/0006-2952(88)90204-3google scholar: lookup
  41. Ray R, Zhang Z, Lee YC, Gao JL, Mukherjee AB. Uteroglobin suppresses allergen-induced TH2 differentiation by down-regulating the expression of serum amyloid A and SOCS-3 genes.. FEBS Lett 2006 Oct 30;580(25):6022-6.
    pmc: PMC1859844pubmed: 17046755doi: 10.1016/j.febslet.2006.09.059google scholar: lookup
  42. Leyton J, Manyak MJ, Mukherjee AB, Miele L, Mantile G, Patierno SR. Recombinant human uteroglobin inhibits the in vitro invasiveness of human metastatic prostate tumor cells and the release of arachidonic acid stimulated by fibroblast-conditioned medium.. Cancer Res 1994 Jul 15;54(14):3696-9.
    pubmed: 8033085
  43. Wei Y, Xu YD, Yin LM, Wang Y, Ran J, Liu Q, Ma ZF, Liu YY, Yang YQ. Recombinant rat CC10 protein inhibits PDGF-induced airway smooth muscle cells proliferation and migration.. Biomed Res Int 2013;2013:690937.
    pmc: PMC3784082pubmed: 24106713doi: 10.1155/2013/690937google scholar: lookup
  44. Hall JA, Hoyt D, Zuver C, Skinner MM, Schlipf JW Jr. Rapid, multiwell colorimetric assay for measuring neutrophil chemoattractant activity in bronchoalveolar lavage fluid of horses with recurrent airway obstruction.. J Vet Diagn Invest 2006 May;18(3):257-63.
    pubmed: 16789713doi: 10.1177/104063870601800304google scholar: lookup
  45. Saffarzadeh M, Juenemann C, Queisser MA, Lochnit G, Barreto G, Galuska SP, Lohmeyer J, Preissner KT. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones.. PLoS One 2012;7(2):e32366.
    pmc: PMC3289648pubmed: 22389696doi: 10.1371/journal.pone.0032366google scholar: lookup
  46. Alghamdi AS, Foster DN. Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps.. Biol Reprod 2005 Dec;73(6):1174-81.
    pubmed: 16107606doi: 10.1095/biolreprod.105.045666google scholar: lookup
  47. Dworski R, Simon HU, Hoskins A, Yousefi S. Eosinophil and neutrophil extracellular DNA traps in human allergic asthmatic airways.. J Allergy Clin Immunol 2011 May;127(5):1260-6.
    pmc: PMC3085562pubmed: 21315435doi: 10.1016/j.jaci.2010.12.1103google scholar: lookup
  48. Beeler-Marfisi J, Clark ME, Wen X, Sears W, Huber L, Ackerley C, Viel L, Bienzle D. Experimental induction of recurrent airway obstruction with inhaled fungal spores, lipopolysaccharide, and silica microspheres in horses.. Am J Vet Res 2010 Jun;71(6):682-9.
    pubmed: 20513185doi: 10.2460/ajvr.71.6.682google scholar: lookup
  49. Ainsworth DM, Wagner B, Franchini M, Grünig G, Erb HN, Tan JY. Time-dependent alterations in gene expression of interleukin-8 in the bronchial epithelium of horses with recurrent airway obstruction.. Am J Vet Res 2006 Apr;67(4):669-77.
    pubmed: 16579761doi: 10.2460/ajvr.67.4.669google scholar: lookup

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  1. Rojas-Quintero J, Laucho-Contreras ME, Wang X, Fucci QA, Burkett PR, Kim SJ, Zhang D, Tesfaigzi Y, Li Y, Bhashyam AR, Li Z, Khamas H, Celli B, Pilon AL, Polverino F, Owen CA. CC16 augmentation reduces exaggerated COPD-like disease in Cc16-deficient mice.. JCI Insight 2023 Mar 22;8(6).
    doi: 10.1172/jci.insight.130771pubmed: 36787195google scholar: lookup
  2. Salinas C, Barriga K, Albornoz A, Alarcon P, Quiroga J, Uberti B, Sarmiento J, Henriquez C, Ehrenfeld P, Burgos RA, Moran G. Tamoxifen triggers the in vitro release of neutrophil extracellular traps in healthy horses.. Front Vet Sci 2022;9:1025249.
    doi: 10.3389/fvets.2022.1025249pubmed: 36686170google scholar: lookup
  3. Janssen P, Tosi I, Hego A, Maréchal P, Marichal T, Radermecker C. Neutrophil Extracellular Traps Are Found in Bronchoalveolar Lavage Fluids of Horses With Severe Asthma and Correlate With Asthma Severity.. Front Immunol 2022;13:921077.
    doi: 10.3389/fimmu.2022.921077pubmed: 35911691google scholar: lookup
  4. Simões J, Batista M, Tilley P. The Immune Mechanisms of Severe Equine Asthma-Current Understanding and What Is Missing.. Animals (Basel) 2022 Mar 16;12(6).
    doi: 10.3390/ani12060744pubmed: 35327141google scholar: lookup
  5. Theuerkauf K, Obach-Schröck C, Staszyk C, Moritz A, Roscher KA. Activated platelets and platelet-leukocyte aggregates in the equine systemic inflammatory response syndrome.. J Vet Diagn Invest 2022 May;34(3):448-457.
    doi: 10.1177/10406387221077969pubmed: 35168432google scholar: lookup
  6. Becker N, Störmann P, Janicova A, Köhler K, Horst K, Dunay IR, Neunaber C, Marzi I, Vollrath JT, Relja B. Club Cell Protein 16 Attenuates CD16(bright)CD62(dim) Immunosuppressive Neutrophils in Damaged Tissue upon Posttraumatic Sepsis-Induced Lung Injury.. J Immunol Res 2021;2021:6647753.
    doi: 10.1155/2021/6647753pubmed: 33575362google scholar: lookup
  7. Couetil L, Cardwell JM, Leguillette R, Mazan M, Richard E, Bienzle D, Bullone M, Gerber V, Ivester K, Lavoie JP, Martin J, Moran G, Niedźwiedź A, Pusterla N, Swiderski C. Equine Asthma: Current Understanding and Future Directions.. Front Vet Sci 2020;7:450.
    doi: 10.3389/fvets.2020.00450pubmed: 32903600google scholar: lookup
  8. Neumann A, Brogden G, von Köckritz-Blickwede M. Extracellular Traps: An Ancient Weapon of Multiple Kingdoms.. Biology (Basel) 2020 Feb 18;9(2).
    doi: 10.3390/biology9020034pubmed: 32085405google scholar: lookup
  9. Xu B, Janicova A, Vollrath JT, Störmann P, Martin L, Marzi I, Wutzler S, Hildebrand F, Ehnert S, Relja B. Club cell protein 16 in sera from trauma patients modulates neutrophil migration and functionality via CXCR1 and CXCR2.. Mol Med 2019 Oct 30;25(1):45.
    doi: 10.1186/s10020-019-0115-0pubmed: 31666007google scholar: lookup
  10. Gy C, Leclere M, Vargas A, Grimes C, Lavoie JP. Investigation of blood biomarkers for the diagnosis of mild to moderate asthma in horses.. J Vet Intern Med 2019 Jul;33(4):1789-1795.
    doi: 10.1111/jvim.15505pubmed: 31099114google scholar: lookup
  11. Sheats MK. A Comparative Review of Equine SIRS, Sepsis, and Neutrophils.. Front Vet Sci 2019;6:69.
    doi: 10.3389/fvets.2019.00069pubmed: 30931316google scholar: lookup
  12. Li RHL, Tablin F. A Comparative Review of Neutrophil Extracellular Traps in Sepsis.. Front Vet Sci 2018;5:291.
    doi: 10.3389/fvets.2018.00291pubmed: 30547040google scholar: lookup
  13. Mainguy-Seers S, Picotte K, Lavoie JP. Efficacy of tamoxifen for the treatment of severe equine asthma.. J Vet Intern Med 2018 Sep;32(5):1748-1753.
    doi: 10.1111/jvim.15289pubmed: 30084157google scholar: lookup
  14. Manfredi AA, Ramirez GA, Rovere-Querini P, Maugeri N. The Neutrophil's Choice: Phagocytose vs Make Neutrophil Extracellular Traps.. Front Immunol 2018;9:288.
    doi: 10.3389/fimmu.2018.00288pubmed: 29515586google scholar: lookup
  15. Vargas A, Boivin R, Cano P, Murcia Y, Bazin I, Lavoie JP. Neutrophil extracellular traps are downregulated by glucocorticosteroids in lungs in an equine model of asthma.. Respir Res 2017 Dec 12;18(1):207.
    doi: 10.1186/s12931-017-0689-4pubmed: 29233147google scholar: lookup
  16. Riedl M, Noone DG, Khan MA, Pluthero FG, Kahr WHA, Palaniyar N, Licht C. Complement Activation Induces Neutrophil Adhesion and Neutrophil-Platelet Aggregate Formation on Vascular Endothelial Cells.. Kidney Int Rep 2017 Jan;2(1):66-75.
    doi: 10.1016/j.ekir.2016.08.015pubmed: 29142942google scholar: lookup
  17. Tessier L, Côté O, Clark ME, Viel L, Diaz-Méndez A, Anders S, Bienzle D. Impaired response of the bronchial epithelium to inflammation characterizes severe equine asthma.. BMC Genomics 2017 Sep 8;18(1):708.
    doi: 10.1186/s12864-017-4107-6pubmed: 28886691google scholar: lookup
  18. Herteman N, Vargas A, Lavoie JP. Characterization of Circulating Low-Density Neutrophils Intrinsic Properties in Healthy and Asthmatic Horses.. Sci Rep 2017 Aug 10;7(1):7743.
    doi: 10.1038/s41598-017-08089-5pubmed: 28798364google scholar: lookup
  19. Liu J, Pang Z, Wang G, Guan X, Fang K, Wang Z, Wang F. Advanced Role of Neutrophils in Common Respiratory Diseases.. J Immunol Res 2017;2017:6710278.
    doi: 10.1155/2017/6710278pubmed: 28589151google scholar: lookup
  20. Liu T, Wang FP, Wang G, Mao H. Role of Neutrophil Extracellular Traps in Asthma and Chronic Obstructive Pulmonary Disease.. Chin Med J (Engl) 2017 Mar 20;130(6):730-736.
    doi: 10.4103/0366-6999.201608pubmed: 28303858google scholar: lookup
  21. Khan MA, Palaniyar N. Transcriptional firing helps to drive NETosis.. Sci Rep 2017 Feb 8;7:41749.
    doi: 10.1038/srep41749pubmed: 28176807google scholar: lookup
  22. Yuen J, Pluthero FG, Douda DN, Riedl M, Cherry A, Ulanova M, Kahr WH, Palaniyar N, Licht C. NETosing Neutrophils Activate Complement Both on Their Own NETs and Bacteria via Alternative and Non-alternative Pathways.. Front Immunol 2016;7:137.
    doi: 10.3389/fimmu.2016.00137pubmed: 27148258google scholar: lookup
  23. Laucho-Contreras ME, Polverino F, Tesfaigzi Y, Pilon A, Celli BR, Owen CA. Club Cell Protein 16 (CC16) Augmentation: A Potential Disease-modifying Approach for Chronic Obstructive Pulmonary Disease (COPD).. Expert Opin Ther Targets 2016 Jul;20(7):869-83.
    doi: 10.1517/14728222.2016.1139084pubmed: 26781659google scholar: lookup
  24. Miskovic Feutz M, Couetil LL, Riley CP, Zhang X, Adamec J, Raskin RE. Secretoglobin and Transferrin Expression in Bronchoalveolar Lavage Fluid of Horses with Chronic Respiratory Disease.. J Vet Intern Med 2015 Nov-Dec;29(6):1692-9.
    doi: 10.1111/jvim.13604pubmed: 26332291google scholar: lookup
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