FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
PloS one2023; 18(9); e0290778; doi: 10.1371/journal.pone.0290778

Comparison of the broncoalveolar lavage fluid proteomics between foals and adult horses.

Abstract: Neonates have different cellular composition in their bronchoalveolar lavage fluid (BALF) when compared to foals and adult horses; however, little is known about the non-cellular components of BALF. The objective of this study was to determine the proteomic composition of BALF in neonatal horses and to compare it to that of foals and adult horses. Bronchoalveolar lavage fluid samples of seven neonates (< 1 week age), four 5 to 7-week-old foals, and six adult horses were collected. Quantitative proteomics of the fluid was performed using tandem mass tag labeling followed by high resolution liquid chromatography tandem mass spectrometry and protein relative abundances were compared between groups using exact text. A total of 704 proteins were identified with gene ontology terms and were classified. Of these, 332 proteins were related to the immune system in neonates, foals, and adult horses. The most frequent molecular functions identified were binding and catalytic activity and the most common biological processes were cellular process, metabolic process, and biological regulation. There was a significant difference in the proteome of neonates when compared to foals and to adult horses. Neonates had less relative expression (FDR < 0.01) of many immune-related proteins, including immunoglobulins, proteins involved in the complement cascade, ferritin, BPI fold-containing family B member 1, and macrophage receptor MARCO. This is the first report of equine neonate BALF proteomics and reveals differential abundance of proteins when compared to BALF from adult horses. The lower relative abundance of immune-related proteins in neonates could contribute to their susceptibility to pulmonary infections.
Copyright: © 2023 Rivolta et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Get Full Text
Publication Date: 2023-09-05 PubMed ID: 37669266PubMed Central: PMC10479908DOI: 10.1371/journal.pone.0290778Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't
  • Research Support
  • N.I.H.
  • Extramural

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 article is about a comparative study of the proteomic content of bronchoalveolar lavage fluid (BALF) between neonate horses, foals and adult horses. Significant differences in the proteomic composition were found between the groups with lower levels of immune-related proteins in neonates.

Objective of the Research

  • The main goal of this research was to determine the proteomic composition of BALF in newborn horses and compare it with foals (5 to 7-week-old) and adult horses.
  • This is driven by the recognition that while there are established differences in the cellular composition of BALF between different age groups, the non-cellular components, such as proteins, are not well understood.

Methodology

  • The researchers collected BALF samples from seven neonates (< 1 week old), four foals and six adult horses.
  • The proteomics of the fluid were quantified using tandem mass tag labeling, liquid chromatography tandem mass spectrometry, and relative abundances of proteins were compared using the exact test method.

Findings and Interpretation

  • The analysis identified 704 proteins, which were classified according to their gene ontology terms. Among these, 332 proteins were related to the immune system.
  • The predominant molecular functions identified were binding and catalytic activity and the most recurrent biological processes were cellular process, metabolic process, and biological regulation.
  • It was observed that the proteome of neonates was significantly different from that of both foals and adult horses. Notably, neonates expressed many immune-related proteins such as immunoglobulins, proteins involved in the complement cascade, ferritin, BPI fold-containing family B member 1, and macrophage receptor MARCO at a much lower level compared to the foals and adult horses.

Significance and Implications

  • This study is the first to report on equine neonate BALF proteomics and reveals a significant difference in protein abundance compared to BALF from adult horses.
  • The research is meaningful as it points out that the lower relative abundance of immune-related proteins in neonates could contribute to their susceptibility to pulmonary infections. This could inform targeted interventions in healthcare and management of neonate horses.

Cite This Article

APA
Rivolta AA, Bujold AR, Wilmarth PA, Phinney BS, Navelski JP, Horohov DW, Sanz MG. (2023). Comparison of the broncoalveolar lavage fluid proteomics between foals and adult horses. PLoS One, 18(9), e0290778. https://doi.org/10.1371/journal.pone.0290778

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 18
Issue: 9
Pages: e0290778
PII: e0290778

Researcher Affiliations

Rivolta, Alejandra A
  • Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, Washington, United States of America.
Bujold, Adina R
  • Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, Washington, United States of America.
  • Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada.
Wilmarth, Phillip A
  • Proteomic Shared Resource, Oregon Health & Science University, Portland, Oregon, United States of America.
Phinney, Brett S
  • Genome Center Proteomics Core Facility, UC Davis, Davis, California, United States of America.
Navelski, Joseph P
  • School of Economic Sciences, Washington State University, Pullman, Washington, United States of America.
Horohov, David W
  • Gluck Equine Research Center, University of Kentucky, Lexington, Kentucky, United States of America.
Sanz, Macarena G
  • Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, Washington, United States of America.

MeSH Terms

  • Horses
  • Animals
  • Proteomics
  • Therapeutic Irrigation
  • Body Fluids
  • Bronchoalveolar Lavage Fluid
  • Chromatography, Liquid

Grant Funding

  • P30 EY010572 / NEI NIH HHS
  • P30 CA069533 / NCI NIH HHS

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 69 references
  1. Giguère S, Polkes AC. Immunologic disorders in neonatal foals.. Vet Clin North Am Equine Pract 2005 Aug;21(2):241-72, v.
    doi: 10.1016/j.cveq.2005.04.004pubmed: 16051049google scholar: lookup
  2. Berghaus LJ, Giguère S, Sturgill TL. Effects of age and macrophage lineage on intracellular survival and cytokine induction after infection with Rhodococcus equi.. Vet Immunol Immunopathol 2014 Jul 15;160(1-2):41-50.
    doi: 10.1016/j.vetimm.2014.03.010pubmed: 24736188google scholar: lookup
  3. Sanz M, Loynachan A, Sun L, Oliveira A, Breheny P, Horohov DW. The effect of bacterial dose and foal age at challenge on Rhodococcus equi infection.. Vet Microbiol 2013 Dec 27;167(3-4):623-31.
    doi: 10.1016/j.vetmic.2013.09.018pubmed: 24139178google scholar: lookup
  4. Horowitz ML, Cohen ND, Takai S, Becu T, Chaffin MK, Chu KK, Magdesian KG, Martens RJ. Application of Sartwell's model (lognormal distribution of incubation periods) to age at onset and age at death of foals with Rhodococcus equi pneumonia as evidence of perinatal infection.. J Vet Intern Med 2001 May-Jun;15(3):171-5.
    doi: 10.1892/0891-6640(2001)015<0171:aosmld>2.3.co;2pubmed: 11380023google scholar: lookup
  5. Hines SA, Stone DM, Hines MT, Alperin DC, Knowles DP, Norton LK, Hamilton MJ, Davis WC, McGuire TC. Clearance of virulent but not avirulent Rhodococcus equi from the lungs of adult horses is associated with intracytoplasmic gamma interferon production by CD4+ and CD8+ T lymphocytes.. Clin Diagn Lab Immunol 2003 Mar;10(2):208-15.
    doi: 10.1128/cdli.10.2.208-215.2003pmc: PMC150533pubmed: 12626444google scholar: lookup
  6. Bordin AI, Cohen ND, Giguère S, Bray JM, Berghaus LJ, Scott B, Johnson R, Hook M. Host-directed therapy in foals can enhance functional innate immunity and reduce severity of Rhodococcus equi pneumonia.. Sci Rep 2021 Jan 28;11(1):2483.
    doi: 10.1038/s41598-021-82049-ypmc: PMC7844249pubmed: 33510265google scholar: lookup
  7. Hostetter SJ, Clark SK, Gilbertie JM, Wiechert SA, Jones DE, Sponseller BA. Age-related variation in the cellular composition of equine bronchoalveolar lavage fluid.. Vet Clin Pathol 2017 Jun;46(2):344-353.
    doi: 10.1111/vcp.12473pubmed: 28346682google scholar: lookup
  8. Balson GA, Smith GD, Yager JA. Immunophenotypic analysis of foal bronchoalveolar lavage lymphocytes.. Vet Microbiol 1997 Jun 16;56(3-4):237-46.
    doi: 10.1016/s0378-1135(97)00092-8pubmed: 9226838google scholar: lookup
  9. Bernoco M, Liu IK, Wuest-Ehlert CJ, Miller ME, Bowers J. Chemotactic and phagocytic function of peripheral blood polymorphonuclear leucocytes in newborn foals.. J Reprod Fertil Suppl 1987;35:599-605.
    pubmed: 3479614
  10. Leclere M, Lavoie-Lamoureux A, Lavoie JP. Heaves, an asthma-like disease of horses.. Respirology 2011 Oct;16(7):1027-46.
    doi: 10.1111/j.1440-1843.2011.02033.xpubmed: 21824219google scholar: lookup
  11. Breathnach CC, Sturgill-Wright T, Stiltner JL, Adams AA, Lunn DP, Horohov DW. Foals are interferon gamma-deficient at birth.. Vet Immunol Immunopathol 2006 Aug 15;112(3-4):199-209.
    doi: 10.1016/j.vetimm.2006.02.010pubmed: 16621024google scholar: lookup
  12. Sellon DC. Secondary immunodeficiencies of horses.. Vet Clin North Am Equine Pract 2000 Apr;16(1):117-30.
    doi: 10.1016/s0749-0739(17)30122-0pubmed: 10752142google scholar: lookup
  13. Rouse BT. The immunoglobulins of adult equine and foal sera: a quantitative study.. Br Vet J 1971 Jan;127(1):45-52.
    doi: 10.1016/s0007-1935(17)37788-6pubmed: 5541943google scholar: lookup
  14. Sheoran AS, Timoney JF, Holmes MA, Karzenski SS, Crisman MV. Immunoglobulin isotypes in sera and nasal mucosal secretions and their neonatal transfer and distribution in horses.. Am J Vet Res 2000 Sep;61(9):1099-105.
    doi: 10.2460/ajvr.2000.61.1099pubmed: 10976743google scholar: lookup
  15. Wright JR. Immunoregulatory functions of surfactant proteins.. Nat Rev Immunol 2005 Jan;5(1):58-68.
    doi: 10.1038/nri1528pubmed: 15630429google scholar: lookup
  16. Christmann U, Livesey LC, Taintor JS, Waldridge BM, Schumacher J, Grier BL, Hite RD. Lung surfactant function and composition in neonatal foals and adult horses.. J Vet Intern Med 2006 Nov-Dec;20(6):1402-7.
    doi: 10.1892/0891-6640(2006)20[1402:lsfaci]2.0.co;2pubmed: 17186857google scholar: lookup
  17. Bright LA, Mujahid N, Nanduri B, McCarthy FM, Costa LR, Burgess SC, Swiderski CE. Functional modelling of an equine bronchoalveolar lavage fluid proteome provides experimental confirmation and functional annotation of equine genome sequences.. Anim Genet 2011 Aug;42(4):395-405.
    doi: 10.1111/j.1365-2052.2010.02158.xpubmed: 21749422google scholar: lookup
  18. Feutz MM. Proteomic analysis of bronchoalveolar lavage fluid in an equine model of asthma during a natural antigen exposure trial. Journal of Integrated OMICS 2 (2)2012 p. 123–31.
  19. Sanz MG, Bradway DS, Horohov DW, Baszler TV. Rhodococcus equi-specific hyperimmune plasma administration decreases faecal shedding of pathogenic R. equi in foals.. Vet Rec 2019 Jul 6;185(1):19.
    doi: 10.1136/vr.105327pubmed: 30995996google scholar: lookup
  20. Hoffman AM. Bronchoalveolar lavage: sampling technique and guidelines for cytologic preparation and interpretation.. Vet Clin North Am Equine Pract 2008 Aug;24(2):423-35, vii-viii.
    doi: 10.1016/j.cveq.2008.04.003pubmed: 18652963google scholar: lookup
  21. Plubell DL, Wilmarth PA, Zhao Y, Fenton AM, Minnier J, Reddy AP, Klimek J, Yang X, David LL, Pamir N. Extended Multiplexing of Tandem Mass Tags (TMT) Labeling Reveals Age and High Fat Diet Specific Proteome Changes in Mouse Epididymal Adipose Tissue.. Mol Cell Proteomics 2017 May;16(5):873-890.
    doi: 10.1074/mcp.M116.065524pmc: PMC5417827pubmed: 28325852google scholar: lookup
  22. Tiwari S, Mishra M, Salemi MR, Phinney BS, Newens JL, Gomes AV. Gender-specific changes in energy metabolism and protein degradation as major pathways affected in livers of mice treated with ibuprofen.. Sci Rep 2020 Feb 25;10(1):3386.
    doi: 10.1038/s41598-020-60053-ypmc: PMC7042271pubmed: 32099006google scholar: lookup
  23. Eng JK, Jahan TA, Hoopmann MR. Comet: an open-source MS/MS sequence database search tool.. Proteomics 2013 Jan;13(1):22-4.
    doi: 10.1002/pmic.201200439pubmed: 23148064google scholar: lookup
  24. H D Sagawa C, de A B Assis R, Zaini PA, Wilmarth PA, Phinney BS, Moreira LM, Dandekar AM. Proteome Analysis of Walnut Bacterial Blight Disease.. Int J Mol Sci 2020 Oct 9;21(20).
    doi: 10.3390/ijms21207453pmc: PMC7593943pubmed: 33050347google scholar: lookup
  25. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.. Bioinformatics 2010 Jan 1;26(1):139-40.
    doi: 10.1093/bioinformatics/btp616pmc: PMC2796818pubmed: 19910308google scholar: lookup
  26. Robinson MD, Smyth GK. Moderated statistical tests for assessing differences in tag abundance.. Bioinformatics 2007 Nov 1;23(21):2881-7.
    doi: 10.1093/bioinformatics/btm453pubmed: 17881408google scholar: lookup
  27. Robinson MD, Smyth GK. Small-sample estimation of negative binomial dispersion, with applications to SAGE data.. Biostatistics 2008 Apr;9(2):321-32.
    doi: 10.1093/biostatistics/kxm030pubmed: 17728317google scholar: lookup
  28. Tesena P, Kingkaw A, Vongsangnak W, Pitikarn S, Phaonakrop N, Roytrakul S, Kovitvadhi A. Preliminary Study: Proteomic Profiling Uncovers Potential Proteins for Biomonitoring Equine Melanocytic Neoplasm.. Animals (Basel) 2021 Jun 27;11(7).
    doi: 10.3390/ani11071913pmc: PMC8300200pubmed: 34199079google scholar: lookup
  29. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data.. Genome Biol 2010;11(3):R25.
    doi: 10.1186/gb-2010-11-3-r25pmc: PMC2864565pubmed: 20196867google scholar: lookup
  30. Aguilan JT, Kulej K, Sidoli S. Guide for protein fold change and p-value calculation for non-experts in proteomics.. Mol Omics 2020 Dec 1;16(6):573-582.
    doi: 10.1039/d0mo00087fpubmed: 32968743google scholar: lookup
  31. Omenn GS, Lane L, Overall CM, Paik YK, Cristea IM, Corrales FJ, Lindskog C, Weintraub S, Roehrl MHA, Liu S, Bandeira N, Srivastava S, Chen YJ, Aebersold R, Moritz RL, Deutsch EW. Progress Identifying and Analyzing the Human Proteome: 2021 Metrics from the HUPO Human Proteome Project.. J Proteome Res 2021 Dec 3;20(12):5227-5240.
    doi: 10.1021/acs.jproteome.1c00590pmc: PMC9340669pubmed: 34670092google scholar: lookup
  32. Hood L, Campbell JH, Elgin SC. The organization, expression, and evolution of antibody genes and other multigene families.. Annu Rev Genet 1975;9:305-53.
    doi: 10.1146/annurev.ge.09.120175.001513pubmed: 813561google scholar: lookup
  33. Anoshchenko O, Prasad B, Neradugomma NK, Wang J, Mao Q, Unadkat JD. Gestational Age-Dependent Abundance of Human Placental Transporters as Determined by Quantitative Targeted Proteomics.. Drug Metab Dispos 2020 Sep;48(9):735-741.
    doi: 10.1124/dmd.120.000067pmc: PMC7469251pubmed: 32591415google scholar: lookup
  34. Umstead TM, Freeman WM, Chinchilli VM, Phelps DS. Age-related changes in the expression and oxidation of bronchoalveolar lavage proteins in the rat.. Am J Physiol Lung Cell Mol Physiol 2009 Jan;296(1):L14-29.
    doi: 10.1152/ajplung.90366.2008pubmed: 18931054google scholar: lookup
  35. Hollung K, Grove H, Færgestad EM, Sidhu MS, Berg P. Comparison of muscle proteome profiles in pure breeds of Norwegian Landrace and Duroc at three different ages.. Meat Sci 2009 Mar;81(3):487-92.
    doi: 10.1016/j.meatsci.2008.10.003pubmed: 20416601google scholar: lookup
  36. McGorum BC, Pirie RS, Eaton SL, Keen JA, Cumyn EM, Arnott DM, Chen W, Lamont DJ, Graham LC, Llavero Hurtado M, Pemberton A, Wishart TM. Proteomic Profiling of Cranial (Superior) Cervical Ganglia Reveals Beta-Amyloid and Ubiquitin Proteasome System Perturbations in an Equine Multiple System Neuropathy.. Mol Cell Proteomics 2015 Nov;14(11):3072-86.
    doi: 10.1074/mcp.M115.054635pmc: PMC4638047pubmed: 26364976google scholar: lookup
  37. Dong Z, Haines S, Coates D. Proteomic Profiling of Stem Cell Tissues during Regeneration of Deer Antler: A Model of Mammalian Organ Regeneration.. J Proteome Res 2020 Apr 3;19(4):1760-1775.
    doi: 10.1021/acs.jproteome.0c00026pubmed: 32155067google scholar: lookup
  38. Franzén K, Eriksson G, Olsson F, Asker L, Lidén P, Cöster J. Protein names and how to find them.. Int J Med Inform 2002 Dec 4;67(1-3):49-61.
    doi: 10.1016/s1386-5056(02)00052-7pubmed: 12460631google scholar: lookup
  39. Chen J, Ryu S, Gharib SA, Goodlett DR, Schnapp LM. Exploration of the normal human bronchoalveolar lavage fluid proteome.. Proteomics Clin Appl 2008 Apr;2(4):585-95.
    doi: 10.1002/prca.200780006pmc: PMC4432467pubmed: 21136857google scholar: lookup
  40. Guo Y, Ma SF, Grigoryev D, Van Eyk J, Garcia JG. 1-DE MS and 2-D LC-MS analysis of the mouse bronchoalveolar lavage proteome.. Proteomics 2005 Nov;5(17):4608-24.
    doi: 10.1002/pmic.200500052pubmed: 16240291google scholar: lookup
  41. Bartlett JA, Albertolle ME, Wohlford-Lenane C, Pezzulo AA, Zabner J, Niles RK, Fisher SJ, McCray PB Jr, Williams KE. Protein composition of bronchoalveolar lavage fluid and airway surface liquid from newborn pigs.. Am J Physiol Lung Cell Mol Physiol 2013 Aug 1;305(3):L256-66.
    doi: 10.1152/ajplung.00056.2013pmc: PMC3743012pubmed: 23709621google scholar: lookup
  42. Bernoco MM, Liu IK, Willits NH. Hemolytic complement activity and concentrations of its third component during maturation of the immune response in colostrum-deprived foals.. Am J Vet Res 1994 Jul;55(7):928-33.
    pubmed: 7978631
  43. Boyd NK, Cohen ND, Lim WS, Martens RJ, Chaffin MK, Ball JM. Temporal changes in cytokine expression of foals during the first month of life.. Vet Immunol Immunopathol 2003 Mar 20;92(1-2):75-85.
    doi: 10.1016/s0165-2427(03)00021-7pubmed: 12628765google scholar: lookup
  44. Noris M, Remuzzi G. Overview of complement activation and regulation.. Semin Nephrol 2013 Nov;33(6):479-92.
    doi: 10.1016/j.semnephrol.2013.08.001pmc: PMC3820029pubmed: 24161035google scholar: lookup
  45. Folmar CN, Cywes-Bentley C, Bordin AI, Rocha JN, Bray JM, Kahn SK, Schuckert AE, Pier GB, Cohen ND. In vitro evaluation of complement deposition and opsonophagocytic killing of Rhodococcus equi mediated by poly-N-acetyl glucosamine hyperimmune plasma compared to commercial plasma products.. J Vet Intern Med 2019 May;33(3):1493-1499.
    doi: 10.1111/jvim.15511pmc: PMC6524092pubmed: 31034109google scholar: lookup
  46. Kraal G, van der Laan LJ, Elomaa O, Tryggvason K. The macrophage receptor MARCO.. Microbes Infect 2000 Mar;2(3):313-6.
    doi: 10.1016/s1286-4579(00)00296-3pubmed: 10758408google scholar: lookup
  47. Kanno S, Hirano S, Sakamoto T, Furuyama A, Takase H, Kato H, Fukuta M, Aoki Y. Scavenger receptor MARCO contributes to cellular internalization of exosomes by dynamin-dependent endocytosis and macropinocytosis.. Sci Rep 2020 Dec 11;10(1):21795.
    doi: 10.1038/s41598-020-78464-2pmc: PMC7733512pubmed: 33311558google scholar: lookup
  48. Marra MN, Wilde CG, Griffith JE, Snable JL, Scott RW. Bactericidal/permeability-increasing protein has endotoxin-neutralizing activity.. J Immunol 1990 Jan 15;144(2):662-6.
    pubmed: 2295804
  49. Xu Y, Tao Z, Jiang Y, Liu T, Xiang Y. Overexpression of BPIFB1 promotes apoptosis and inhibits proliferation via the MEK/ERK signal pathway in nasopharyngeal carcinoma.. Int J Clin Exp Pathol 2019;12(1):356-364.
    pmc: PMC6944003pubmed: 31933752
  50. Theil EC. Ferritin: structure, gene regulation, and cellular function in animals, plants, and microorganisms.. Annu Rev Biochem 1987;56:289-315.
    doi: 10.1146/annurev.bi.56.070187.001445pubmed: 3304136google scholar: lookup
  51. Kawamata R, Yokoyama K, Sato M, Goto M, Nozaki Y, Takagi T, Kumagai H, Yamagata T. Utility of serum ferritin and lactate dehydrogenase as surrogate markers for steroid therapy for Mycoplasma pneumoniae pneumonia.. J Infect Chemother 2015 Nov;21(11):783-9.
    doi: 10.1016/j.jiac.2015.07.009pubmed: 26298038google scholar: lookup
  52. Guan WJ, Ni ZY, Hu Y, Liang WH, Ou CQ, He JX, Liu L, Shan H, Lei CL, Hui DSC, Du B, Li LJ, Zeng G, Yuen KY, Chen RC, Tang CL, Wang T, Chen PY, Xiang J, Li SY, Wang JL, Liang ZJ, Peng YX, Wei L, Liu Y, Hu YH, Peng P, Wang JM, Liu JY, Chen Z, Li G, Zheng ZJ, Qiu SQ, Luo J, Ye CJ, Zhu SY, Zhong NS. Clinical Characteristics of Coronavirus Disease 2019 in China.. N Engl J Med 2020 Apr 30;382(18):1708-1720.
    doi: 10.1056/NEJMoa2002032pmc: PMC7092819pubmed: 32109013google scholar: lookup
  53. Dondi F, Lukacs RM, Gentilini F, Rinnovati R, Spadari A, Romagnoli N. Serum amyloid A, haptoglobin, and ferritin in horses with colic: Association with common clinicopathological variables and short-term outcome.. Vet J 2015 Jul;205(1):50-5.
    doi: 10.1016/j.tvjl.2015.03.015pubmed: 25981935google scholar: lookup
  54. Knapp S, Florquin S, Golenbock DT, van der Poll T. Pulmonary lipopolysaccharide (LPS)-binding protein inhibits the LPS-induced lung inflammation in vivo.. J Immunol 2006 Mar 1;176(5):3189-95.
    doi: 10.4049/jimmunol.176.5.3189pubmed: 16493079google scholar: lookup
  55. Laoui D, Van Overmeire E, De Baetselier P, Van Ginderachter JA, Raes G. Functional Relationship between Tumor-Associated Macrophages and Macrophage Colony-Stimulating Factor as Contributors to Cancer Progression.. Front Immunol 2014;5:489.
    doi: 10.3389/fimmu.2014.00489pmc: PMC4188035pubmed: 25339957google scholar: lookup
  56. Kashyap B, Kullaa AM. Regulation of mucin 1 expression and its relationship with oral diseases.. Arch Oral Biol 2020 Sep;117:104791.
    doi: 10.1016/j.archoralbio.2020.104791pubmed: 32652493google scholar: lookup
  57. Dhar P, Ng GZ, Dunne EM, Sutton P. Mucin 1 protects against severe Streptococcus pneumoniae infection.. Virulence 2017 Nov 17;8(8):1631-1642.
    doi: 10.1080/21505594.2017.1341021pmc: PMC5810494pubmed: 28605238google scholar: lookup
  58. Kato K, Lillehoj EP, Lu W, Kim KC. MUC1: The First Respiratory Mucin with an Anti-Inflammatory Function.. J Clin Med 2017 Nov 29;6(12).
    doi: 10.3390/jcm6120110pmc: PMC5742799pubmed: 29186029google scholar: lookup
  59. Ferraboschi P, Ciceri S, Grisenti P. Applications of Lysozyme, an Innate Immune Defense Factor, as an Alternative Antibiotic.. Antibiotics (Basel) 2021 Dec 14;10(12).
    doi: 10.3390/antibiotics10121534pmc: PMC8698798pubmed: 34943746google scholar: lookup
  60. Mackie IA, Seal DV. Quantitative tear lysozyme assay in units of activity per microlitre.. Br J Ophthalmol 1976 Jan;60(1):70-4.
    doi: 10.1136/bjo.60.1.70pmc: PMC1017470pubmed: 1268164google scholar: lookup
  61. Ratjen F, Rehn B, Costabel U, Bruch J. Age-dependency of surfactant phospholipids and surfactant protein A in bronchoalveolar lavage fluid of children without bronchopulmonary disease.. Eur Respir J 1996 Feb;9(2):328-33.
    doi: 10.1183/09031936.96.09020328pubmed: 8777972google scholar: lookup
  62. Wattiez R, Hermans C, Bernard A, Lesur O, Falmagne P. Human bronchoalveolar lavage fluid: two-dimensional gel electrophoresis, amino acid microsequencing and identification of major proteins.. Electrophoresis 1999 Jun;20(7):1634-45.
    doi: 10.1002/(SICI)1522-2683(19990601)20:7<1634::AID-ELPS1634>3.0.CO;2-Jpubmed: 10424490google scholar: lookup
  63. Georgila K, Vyrla D, Drakos E. Apolipoprotein A-I (ApoA-I), Immunity, Inflammation and Cancer.. Cancers (Basel) 2019 Aug 1;11(8).
    doi: 10.3390/cancers11081097pmc: PMC6721368pubmed: 31374929google scholar: lookup
  64. Thompson A, Danesh J. Associations between apolipoprotein B, apolipoprotein AI, the apolipoprotein B/AI ratio and coronary heart disease: a literature-based meta-analysis of prospective studies.. J Intern Med 2006 May;259(5):481-92.
    doi: 10.1111/j.1365-2796.2006.01644.xpubmed: 16629854google scholar: lookup
  65. Arevalo JA, Vázquez-Medina JP. The Role of Peroxiredoxin 6 in Cell Signaling.. Antioxidants (Basel) 2018 Nov 24;7(12).
    doi: 10.3390/antiox7120172pmc: PMC6316032pubmed: 30477202google scholar: lookup
  66. Song Y, Fukuda N, Bai C, Ma T, Matthay MA, Verkman AS. Role of aquaporins in alveolar fluid clearance in neonatal and adult lung, and in oedema formation following acute lung injury: studies in transgenic aquaporin null mice.. J Physiol 2000 Jun 15;525 Pt 3(Pt 3):771-9.
    doi: 10.1111/j.1469-7793.2000.00771.xpmc: PMC2269974pubmed: 10856128google scholar: lookup
  67. Xie JJ, Zhang FR, Tao LH, Lü Z, Xu XE, Jian-Shen, Xu LY, Li EM. Expression of ezrin in human embryonic, fetal, and normal adult tissues.. J Histochem Cytochem 2011 Nov;59(11):1001-8.
    doi: 10.1369/0022155411418661pmc: PMC3261628pubmed: 21832146google scholar: lookup
  68. Halliwell RE, McGorum BC, Irving P, Dixon PM. Local and systemic antibody production in horses affected with chronic obstructive pulmonary disease.. Vet Immunol Immunopathol 1993 Oct;38(3-4):201-15.
    doi: 10.1016/0165-2427(93)90081-epubmed: 8291200google scholar: lookup
  69. Perkins GA, Wagner B. The development of equine immunity: Current knowledge on immunology in the young horse.. Equine Vet J 2015 May;47(3):267-74.
    doi: 10.1111/evj.12387pubmed: 25405920google scholar: lookup

Citations

This article has been cited 1 times.
  1. Rivolta AA, Bujold AR, Wilmarth PA, Phinney BS, Navelski JP, Horohov DW, Sanz MG. Correction: Comparison of the broncoalveolar lavage fluid proteomics between foals and adult horses. PLoS One 2024;19(6):e0306211.
    doi: 10.1371/journal.pone.0306211pubmed: 38905290google scholar: lookup
Subscribe to our newsletter
Join 99,911 horse owners like you who receive our email updates on horse health and nutrition.