Matrikines are key regulators in modulating the amplitude of lung inflammation in acute pulmonary infection

Nature Communications

Volumn 6, Issue , 2015, Pages

  Akthar, Samia ^a   Patel, Dhiren F ^a   Beale, Rebecca C ^a   Peiró, Teresa ^a   Xu, Xin ^b   Gaggar, Amit ^b,c,d   Jackson, Patricia L ^b   Blalock, J Edwin ^b,d   Lloyd, Clare M ^a   Snelgrove, Robert J ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPOXIDE HYDROLASE; GELATINASE B; HYDROLASE; INTERLEUKIN 8; LACTATE DEHYDROGENASE; LEUKOTRIENE A4; LEUKOTRIENE B4; MACROPHAGE ELASTASE; MATRIKINE; PROTEINASE; REGULATOR PROTEIN; UNCLASSIFIED DRUG; LEUKOCYTE ELASTASE; LEUKOTRIENE A4 HYDROLASE; LEUKOTRIENE B4 RECEPTOR; LTB4R1 PROTEIN, MOUSE; MATRIX METALLOPEPTIDASE 12, MOUSE; MMP9 PROTEIN, MOUSE; OLIGOPEPTIDE; PROLINE; PROLYL-GLYCYL-PROLINE;

AMPLITUDE; BIOACTIVITY; ENZYME ACTIVITY; INHIBITOR; PHYSIOLOGICAL RESPONSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL CLEARANCE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; HAEMOPHILUS INFLUENZAE TYPE B; INFLUENZA B; LUNG INFECTION; LUNG LAVAGE; MOUSE; NONHUMAN; PNEUMONIA; ANALOGS AND DERIVATIVES; ANIMAL; BACTERIAL PNEUMONIA; FLOW CYTOMETRY; GENETICS; HAEMOPHILUS INFECTION; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; LUNG; LUNG ALVEOLUS MACROPHAGE; METABOLISM; NEUTROPHIL; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; EPOXIDE HYDROLASES; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE TYPE B; INFLAMMATION; LEUKOCYTE ELASTASE; LEUKOTRIENE B4; LUNG; MACROPHAGES, ALVEOLAR; MATRIX METALLOPROTEINASE 12; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; NEUTROPHILS; OLIGOPEPTIDES; PNEUMONIA, BACTERIAL; PNEUMONIA, PNEUMOCOCCAL; PROLINE; RECEPTORS, LEUKOTRIENE B4; STREPTOCOCCUS PNEUMONIAE;

EID: 84942134776     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9423     Document Type: Article

References (70)

1. Reeves, E. P. et al. Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416, 291-297 (2002).
2. Stuart, L. M. & Ezekowitz, R. A. Phagocytosis: elegant complexity. Immunity 22, 539-550 (2005).
3. Rot, A. & von Andrian, U. H. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 22, 891-928 (2004).
4. Nathan, C. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6, 173-182 (2006).
5. Mantovani, A., Cassatella, M. A., Costantini, C. & Jaillon, S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11, 519-531 (2011).
6. ODonnell, R., Breen, D., Wilson, S. & Djukanovic, R. Inflammatory cells in the airways in COPD. Thorax 61, 448-454 (2006).
7. Rowe, S. M., Miller, S. & Sorscher, E. J. Cystic fibrosis. N. Engl. J. Med. 352, 1992-2001 (2005).
8. Djekic, U. V., Gaggar, A. & Weathington, N. M. Attacking the multi-Tiered proteolytic pathology of COPD: new insights from basic and translational studies. Pharmacol. Ther. 121, 132-146 (2009).
9. Shapiro, S. D. et al. Neutrophil elastase contributes to cigarette smoke-induced emphysema in mice. Am. J. Pathol. 163, 2329-2335 (2003).
10. Churg, A. et al. Acute cigarette smoke-induced connective tissue breakdown requires both neutrophils and macrophage metalloelastase in mice. Am. J. Respir. Cell Mol. Biol. 27, 368-374 (2002).
11. Houghton, A. M. et al. Elastin fragments drive disease progression in a murine model of emphysema. J. Clin. Invest. 116, 753-759 (2006).
12. Hautamaki, R. D., Kobayashi, D. K., Senior, R. M. & Shapiro, S. D. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 277, 2002-2004 (1997).
13. Weathington, N. M. et al. A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat. Med. 12, 317-323 (2006).
14. Gaggar, A. et al. A novel proteolytic cascade generates an extracellular matrixderived chemoattractant in chronic neutrophilic inflammation. J. Immunol. 180, 5662-5669 (2008).
15. Hardison, M. T. et al. The presence of a matrix-derived neutrophil chemoattractant in bronchiolitis obliterans syndrome after lung transplantation. J. Immunol. 182, 4423-4431 (2009).
16. OReilly, P. et al. N-Alpha-PGP and PGP, potential biomarkers and therapeutic targets for COPD. Respir. Res. 10, 38 (2009).
17. OReilly, P. J. et al. Sputum PGP is reduced by azithromycin treatment in patients with COPD and correlates with exacerbations. BMJ Open 3, e004140 (2013).
18. Wells, J. M. et al. An aberrant leukotriene A4 hydrolase-proline-glycine-proline pathway in the pathogenesis of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 190, 51-61 (2014).
19. Snelgrove, R. J. et al. A critical role for LTA4H in limiting chronic pulmonary neutrophilic inflammation. Science 330, 90-94 (2010).
20. Haeggstrom, J. Z., Tholander, F. & Wetterholm, A. Structure and catalytic mechanisms of leukotriene A4 hydrolase. Prostaglandins Other Lipid Mediat. 83, 198-202 (2007).
21. Funk, C. D. Prostaglandins and leukotrienes: Advances in eicosanoid biology. Science 294, 1871-1875 (2001).
22. Tager, A. M. & Luster, A. D. BLT1 and BLT2: The leukotriene B(4) receptors. Prostaglandins Leukot. Essent. Fatty Acids 69, 123-134 (2003).
23. Di Gennaro, A. & Haeggstrom, J. Z. The leukotrienes: immune-modulating lipid mediators of disease. Adv. Immunol. 116, 51-92 (2012).
24. Whittle, B. J. et al. Attenuation of inflammation and cytokine production in rat colitis by a novel selective inhibitor of leukotriene A4 hydrolase. Br. J. Pharmacol. 153, 983-991 (2008).
25. Griffiths, R. J. et al. Leukotriene B4 plays a critical role in the progression of collagen-induced arthritis. Proc. Natl Acad. Sci. USA 92, 517-521 (1995).
26. Bailie, M. B. et al. Leukotriene-deficient mice manifest enhanced lethality from Klebsiella pneumonia in association with decreased alveolar macrophage phagocytic and bactericidal activities. J. Immunol. 157, 5221-5224 (1996).
27. Chen, X. S., Sheller, J. R., Johnson, E. N. & Funk, C. D. Role of leukotrienes revealed by targeted disruption of the 5-lipoxygenase gene. Nature 372, 179-182 (1994).
28. Snelgrove, R. J. Leukotriene A4 hydrolase: An anti-inflammatory role for a proinflammatory enzyme. Thorax 66, 550-551 (2011).
29. Fourie, A. M. Modulation of inflammatory disease by inhibitors of leukotriene A4 hydrolase. Curr. Opin. Investig. Drugs 10, 1173-1182 (2009).
30. Barchuk, W. et al. Effects of JNJ-40929837, a leukotriene A4 hydrolase inhibitor, in a bronchial allergen challenge model of asthma. Pulm. Pharmacol. Ther. 29, 15-23 (2014).
31. Ulanova, M. & Tsang, R. S. Invasive Haemophilus influenzae disease: changing epidemiology and host-parasite interactions in the 21st century. Infect. Genet. Evol. 9, 594-605 (2009).
32. Ulanova, M. & Tsang, R. S. Haemophilus influenzae serotype a as a cause of serious invasive infections. Lancet Infect. Dis. 14, 70-82 (2014).
33. Kelly, D. F., Moxon, E. R. & Pollard, A. J. Haemophilus influenzae type b conjugate vaccines. Immunology 113, 163-174 (2004).
34. OReilly, P. J. et al. Neutrophils contain prolyl endopeptidase and generate the chemotactic peptide, PGP, from collagen. J. Neuroimmunol. 217, 51-54 (2009).
35. Overbeek, S. A. et al. Cigarette smoke-induced collagen destruction; key to chronic neutrophilic airway inflammation? PLoS ONE 8, e55612 (2013).
36. Braber, S. et al. Cigarette smoke-induced lung emphysema in mice is associated with prolyl endopeptidase, an enzyme involved in collagen breakdown. Am. J. Physiol. Lung Cell. Mol. Physiol. 300, L255-L265 (2010).
37. Serezani, C. H., Aronoff, D. M., Jancar, S., Mancuso, P. & Peters-Golden, M. Leukotrienes enhance the bactericidal activity of alveolar macrophages against Klebsiella pneumoniae through the activation of NADPH oxidase. Blood 106, 1067-1075 (2005).
38. Soares, E. M. et al. Leukotriene B4 enhances innate immune defense against the puerperal sepsis agent Streptococcus pyogenes. J. Immunol. 190, 1614-1622 (2013).
39. Mancuso, P., Nana-Sinkam, P. & Peters-Golden, M. Leukotriene B4 augments neutrophil phagocytosis of Klebsiella pneumoniae. Infect. Immun. 69, 2011-2016 (2001).
40. Mancuso, P., Lewis, C., Serezani, C. H., Goel, D. & Peters-Golden, M. Intrapulmonary administration of leukotriene B4 enhances pulmonary host defense against pneumococcal pneumonia. Infect. Immun. 78, 2264-2271 (2010).
41. Serezani, C. H., Perrela, J. H., Russo, M., Peters-Golden, M. & Jancar, S. Leukotrienes are essential for the control of Leishmania amazonensis infection and contribute to strain variation in susceptibility. J. Immunol. 177, 3201-3208 (2006).
42. Peres, C. M. et al. Inhibition of leukotriene biosynthesis abrogates the host control of Mycobacterium tuberculosis. Microbes Infect. 9, 483-489 (2007).
43. Wirth, J. J. & Kierszenbaum, F. Stimulatory effects of leukotriene B4 on macrophage association with and intracellular destruction of Trypanosoma cruzi. J. Immunol. 134, 1989-1993 (1985).
44. Mancuso, P., Standiford, T. J., Marshall, T. & Peters-Golden, M. 5-Lipoxygenase reaction products modulate alveolar macrophage phagocytosis of Klebsiella pneumoniae. Infect. Immun. 66, 5140-5146 (1998).
45. Mancuso, P. & Peters-Golden, M. Modulation of alveolar macrophage phagocytosis by leukotrienes is Fc receptor-mediated and protein kinase C-dependent. Am. J. Respir. Cell Mol. Biol. 23, 727-733 (2000).
46. Demitsu, T., Katayama, H., Saito-Taki, T., Yaoita, H. & Nakano, M. Phagocytosis and bactericidal action of mouse peritoneal macrophages treated with leukotriene B4. Int. J. Immunopharmacol. 11, 801-808 (1989).
47. Talvani, A. et al. Leukotriene B(4) induces nitric oxide synthesis in Trypanosoma cruzi-infected murine macrophages and mediates resistance to infection. Infect. Immun. 70, 4247-4253 (2002).
48. Coffey, M. J., Phare, S. M. & Peters-Golden, M. Role of leukotrienes in killing of Mycobacterium bovis by neutrophils. Prostaglandins Leukot. Essent. Fatty Acids 71, 185-190 (2004).
49. Larfars, G., Lantoine, F., Devynck, M. A., Palmblad, J. & Gyllenhammar, H. Activation of nitric oxide release and oxidative metabolism by leukotrienes B4, C4, and D4 in human polymorphonuclear leukocytes. Blood 93, 1399-1405 (1999).
50. Ito, N. et al. Requirement of phosphatidylinositol 3-kinase activation and calcium influx for leukotriene B4-induced enzyme release. J. Biol. Chem. 277, 44898-44904 (2002).
51. van Houwelingen, A. H. et al. Induction of lung emphysema is prevented by L-Arginine-Threonine-Arginine. FASEB J. 22, 3403-3408 (2008).
52. Pfister, R. R. et al. Synthetic complementary peptides inhibit a neutrophil chemoattractant found in the alkali-injured cornea. Cornea 19, 384-389 (2000).
53. Rao, N. L. et al. Anti-inflammatory activity of a potent, selective leukotriene A4 hydrolase inhibitor in comparison with the 5-lipoxygenase inhibitor zileuton. J. Pharmacol. Exp. Ther. 321, 1154-1160 (2007).
54. He, J., Turino, G. M. & Lin, Y. Y. Characterization of peptide fragments from lung elastin degradation in chronic obstructive pulmonary disease. Exp. Lung Res. 36, 548-557 (2013).
55. Blanchevoye, C. et al. Interaction between the elastin peptide VGVAPG and human elastin binding protein. J. Biol. Chem. 288, 1317-1328 (2013).
56. Haeggstrom, J. Z. Structure, function, and regulation of leukotriene A4 hydrolase. Am. J. Respir. Crit. Care Med. 161, S25-S31 (2000).
57. Goulet, J. L., Snouwaert, J. N., Latour, A. M., Coffman, T. M. & Koller, B. H. Altered inflammatory responses in leukotriene-deficient mice. Proc. Natl Acad. Sci. USA 91, 12852-12856 (1994).
58. Kim, S. D. et al. Activation of CXCR2 by extracellular matrix degradation product acetylated-Pro-Gly-Pro has therapeutic effects against sepsis. Am. J. Respir. Crit. Care Med. 184, 243-251 (2011).
59. Xu, X. et al. A self-propagating matrix metalloprotease-9 (MMP-9) dependent cycle of chronic neutrophilic inflammation. PLoS ONE 6, e15781 (2011).
60. Senior, R. M., Griffin, G. L. & Mecham, R. P. Chemotactic activity of elastin-derived peptides. J. Clin. Invest. 66, 859-862 (1980).
61. Senior, R. M. et al. Val-Gly-Val-Ala-Pro-Gly, a repeating peptide in elastin, is chemotactic for fibroblasts and monocytes. J. Cell Biol. 99, 870-874 (1984).
62. Hunninghake, G. W. et al. Elastin fragments attract macrophage precursors to diseased sites in pulmonary emphysema. Science 212, 925-927 (1981).
63. Byrum, R. S., Goulet, J. L., Snouwaert, J. N., Griffiths, R. J. & Koller, B. H. Determination of the contribution of cysteinyl leukotrienes and leukotriene B4 in acute inflammatory responses using 5-lipoxygenase-And leukotriene A4 hydrolase-deficient mice. J. Immunol. 163, 6810-6819 (1999).
64. Shim, Y. M. et al. Role of LTB(4) in the pathogenesis of elastase-induced murine pulmonary emphysema. Am. J. Physiol. Lung Cell. Mol. Physiol. 299, L749-L759 (2010).
65. Hardison, M. T., Brown, M. D., Snelgrove, R. J., Blalock, J. E. & Jackson, P. Cigarette smoke enhances chemotaxis via acetylation of proline-glycineproline. Front. Biosci. (Elite Ed). 4, 2402-2409 (2012).
66. Wedzicha, J. A., Brill, S. E., Allinson, J. P. & Donaldson, G. C. Mechanisms and impact of the frequent exacerbator phenotype in chronic obstructive pulmonary disease. BMC Med. 11, 181 (2013).
67. Mercer, P. F. et al. MMP-9, TIMP-1 and inflammatory cells in sputum from COPD patients during exacerbation. Respir. Res. 6, 151 (2005).
68. Snelgrove, R. J. Targeting of a common receptor shared by CXCL8 and N-Ac-PGP as a therapeutic strategy to alleviate chronic neutrophilic lung diseases. Eur. J. Pharmacol. 667, 1-5 (2011).
69. De Oliveira, E. O. et al. Effect of the leukotriene A4 hydrolase aminopeptidase augmentor 4-methoxydiphenylmethane in a pre-clinical model of pulmonary emphysema. Bioorg. Med. Chem. Lett. 21, 6746-6750 (2011).
70. Paige, M. et al. Role of leukotriene A4 Hydrolase aminopeptidase in the pathogenesis of emphysema. J. Immunol. 192, 5059-5068 (2014).