Targeting ADAM17 in leukocytes increases neutrophil recruitment and reduces bacterial spread during polymicrobial sepsis

Journal of Leukocyte Biology

Volumn 100, Issue 5, 2016, Pages 999-1004

  Mishra, Hemant K ^a   Johnson, Timothy J ^a   Seelig, Davis M ^a   Walcheck, Bruce ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Inflammation; Microbiota; TACE

Indexed keywords

A DISINTEGRIN AND METALLOPROTEASE 17 PROTEIN; ADAM PROTEIN; BIOLOGICAL MARKER; CXCL1 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 23P19; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ADAM17 PROTEIN, MOUSE; CYTOKINE; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEREMIA; BACTERIAL LOAD; BACTERIAL VIRULENCE; CECAL LIGATION AND PUNCTURE-INDUCED SEPSIS; CECUM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DISEASE SEVERITY; INFLAMMATION; INTESTINE FLORA; KNOCKOUT MOUSE; LEUKOCYTE FUNCTION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PERITONEUM; PRIORITY JOURNAL; PROGNOSIS; PROTEIN FUNCTION; SURVIVAL RATE; ANIMAL; BLOOD; DEFICIENCY; DISEASE MODEL; ENZYMOLOGY; GENETICS; GERMFREE ANIMAL; IMMUNOLOGY; LEUKOCYTE; LEUKOCYTE COUNT; MICROBIOLOGY; MIXED INFECTION; NEUTROPHIL; PHYSIOLOGY; SEPSIS;

ADAM17 PROTEIN; ANIMALS; BACTERIAL LOAD; CECUM; CHEMOTAXIS, LEUKOCYTE; COINFECTION; CYTOKINES; DISEASE MODELS, ANIMAL; GASTROINTESTINAL MICROBIOME; LEUKOCYTE COUNT; LEUKOCYTES; MICE; MICE, KNOCKOUT; NEUTROPHILS; SEPSIS; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 84994115633     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3VMAB1115-496RR     Document Type: Article

References (53)

1. Mayadas, T. N., Cullere, X., Lowell, C. A. (2014) The multifaceted functions of neutrophils. Annu. Rev. Pathol. 9, 181-218.
2. Quaid, G. A., Cave, C., Robinson, C., Williams, M. A., Solomkin, J. S. (1999) Preferential loss of CXCR-2 receptor expression and function in patients who have undergone trauma. Arch. Surg. 134, 1367-1371, discussion 1371-1372.
3. Kordonowy, L. L., Burg, E., Lenox, C. C., Gauthier, L. M., Petty, J. M., Antkowiak, M., Palvinskaya, T., Ubags, N., Rincón, M., Dixon, A. E., Vernooy, J. H., Fessler, M. B., Poynter, M. E., Suratt, B. T. (2012) Obesity is associated with neutrophil dysfunction and attenuation of murine acute lung injury. Am. J. Respir. Cell Mol. Biol. 47, 120-127.
4. Sˆonego, F., Alves-Filho, J. C., Cunha, F. Q. (2014) Targeting neutrophils in sepsis. Expert Rev. Clin. Immunol. 10, 1019-1028.
5. Lerman, Y. V., Kim, M. (2015) Neutrophil migration under normal and sepsis conditions. Cardiovasc. Hematol. Disord. Drug Targets 15, 19-28.
6. Alves-Filho, J. C., Freitas, A., Souto, F. O., Spiller, F., Paula-Neto, H., Silva, J. S., Gazzinelli, R. T., Teixeira, M. M., Ferreira, S. H., Cunha, F. Q. (2009) Regulation of chemokine receptor by Toll-like receptor 2 is critical to neutrophil migration and resistance to polymicrobial sepsis. Proc. Natl. Acad. Sci. USA 106, 4018-4023.
7. Alves-Filho, J. C., Sˆonego, F., Souto, F. O., Freitas, A., Verri, Jr., W. A., Auxiliadora-Martins, M., Basile-Filho, A., McKenzie, A. N., Xu, D., Cunha, F. Q., Liew, F. Y. (2010) Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat. Med. 16, 708-712.
8. Spiller, F., Orrico, M. I., Nascimento, D. C., Czaikoski, P. G., Souto, F. O., Alves-Filho, J. C., Freitas, A., Carlos, D., Montenegro, M. F., Neto, A. F., Ferreira, S. H., Rossi, M. A., Hothersall, J. S., Assreuy, J., Cunha, F. Q. (2010) Hydrogen sulfide improves neutrophil migration and survival in sepsis via K +ATP channel activation. Am. J. Respir. Crit. Care Med. 182, 360-368.
9. Zonneveld, R., Martinelli, R., Shapiro, N. I., Kuijpers, T. W., Plötz, F. B., Carman, C. V. (2014) Soluble adhesion molecules as markers for sepsis and the potential pathophysiological discrepancy in neonates, children and adults. Crit. Care 18, 204.
10. Gooz, M. (2010) ADAM-17: the enzyme that does it all. Crit. Rev. Biochem. Mol. Biol. 45, 146-169.
11. Black, R. A., Rauch, C. T., Kozlosky, C. J., Peschon, J. J., Slack, J. L., Wolfson, M. F., Castner, B. J., Stocking, K. L., Reddy, P., Srinivasan, S., Nelson, N., Boiani, N., Schooley, K. A., Gerhart, M., Davis, R., Fitzner, J. N., Johnson, R. S., Paxton, R. J., March, C. J., Cerretti, D. P. (1997) A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385, 729-733.
12. Wang, Y., Herrera, A. H., Li, Y., Belani, K. K., Walcheck, B. (2009) Regulation of mature ADAM17 by redox agents for L-selectin shedding. J. Immunol. 182, 2449-2457.
13. Wang, Y., Robertson, J. D., Walcheck, B. (2011) Different signaling pathways stimulate a disintegrin and metalloprotease-17 (ADAM17) in neutrophils during apoptosis and activation. J. Biol. Chem. 286, 38980-38988.
14. Maretzky, T., McIlwain, D. R., Issuree, P. D., Li, X., Malapeira, J., Amin, S., Lang, P. A., Mak, T. W., Blobel, C. P. (2013) iRhom2 controls the substrate selectivity of stimulated ADAM17-dependent ectodomain shedding. Proc. Natl. Acad. Sci. USA 110, 11433-11438.
15. Lamour, N. F., Wijesinghe, D. S., Mietla, J. A., Ward, K. E., Stahelin, R. V., Chalfant, C. E. (2011) Ceramide kinase regulates the production of tumor necrosis factor a (TNFa) via inhibition of TNFa-converting enzyme. J. Biol. Chem. 286, 42808-42817.
16. Xu, P., Liu, J., Sakaki-Yumoto, M., Derynck, R. (2012) TACE activation by MAPK-mediated regulation of cell surface dimerization and TIMP3 association. Sci. Signal. 5, ra34.
17. Scheller, J., Chalaris, A., Garbers, C., Rose-John, S. (2011) ADAM17: a molecular switch to control inflammation and tissue regeneration. Trends Immunol. 32, 380-387.
18. Li, Y., Brazzell, J., Herrera, A., Walcheck, B. (2006) ADAM17 deficiency by mature neutrophils has differential effects on L-selectin shedding. Blood 108, 2275-2279.
19. Bell, J. H., Herrera, A. H., Li, Y., Walcheck, B. (2007) Role of ADAM17 in the ectodomain shedding of TNF-alpha and its receptors by neutrophils and macrophages. J. Leukoc. Biol. 82, 173-176.
20. Weskamp, G., Mendelson, K., Swendeman, S., Le Gall, S., Ma, Y., Lyman, S., Hinoki, A., Eguchi, S., Guaiquil, V., Horiuchi, K., Blobel, C. P. (2010) Pathological neovascularization is reduced by inactivation of ADAM17 in endothelial cells but not in pericytes. Circ. Res. 106, 932-940.
21. Dreymueller, D., Martin, C., Kogel, T., Pruessmeyer, J., Hess, F.M., Horiuchi, K., Uhlig, S., Ludwig, A. (2012) Lung endothelial ADAM17 regulates the acute inflammatory response to lipopolysaccharide. EMBO Mol. Med. 4, 412-423.
22. Wang, Y., Wu, J., Newton, R., Bahaie, N. S., Long, C., Walcheck, B. (2013) ADAM17 cleaves CD16b (FcgRIIIb) in human neutrophils. Biochim. Biophys. Acta 1833, 680-685.
23. Mishra, H. K., Long, C., Bahaie, N. S., Walcheck, B. (2015) Regulation of CXCR2 expression and function by a disintegrin and metalloprotease-17 (ADAM17). J. Leukoc. Biol. 97, 447-454.
24. Tsuboi, N., Asano, K., Lauterbach, M., Mayadas, T. N. (2008) Human neutrophil Fcgamma receptors initiate and play specialized nonredundant roles in antibody-mediated inflammatory diseases. Immunity 28, 833-846.
25. Kolaczkowska, E., Kubes, P. (2013) Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13, 159-175.
26. Arndt, P. G., Strahan, B., Wang, Y., Long, C., Horiuchi, K., Walcheck, B. (2011) Leukocyte ADAM17 regulates acute pulmonary inflammation. PLoS One 6, e19938.
27. Long, C., Hosseinkhani, M. R., Wang, Y., Sriramarao, P., Walcheck, B. (2012) ADAM17 activation in circulating neutrophils following bacterial challenge impairs their recruitment. J. Leukoc. Biol. 92, 667-672.
28. Tang, J., Zarbock, A., Gomez, I., Wilson, C. L., Lefort, C. T., Stadtmann, A., Bell, B., Huang, L.-C., Ley, K., Raines, E. W. (2011) Adam17-dependent shedding limits early neutrophil influx but does not alter early monocyte recruitment to inflammatory sites. Blood 118, 786-794.
29. Peschon, J. J., Slack, J. L., Reddy, P., Stocking, K. L., Sunnarborg, S. W., Lee, D. C., Russell, W. E., Castner, B. J., Johnson, R. S., Fitzner, J. N., Boyce, R. W., Nelson, N., Kozlosky, C. J., Wolfson, M. F., Rauch, C. T., Cerretti, D. P., Paxton, R. J., March, C. J., Black, R. A. (1998) An essential role for ectodomain shedding in mammalian development. Science 282, 1281-1284.
30. Long, C., Wang, Y., Herrera, A. H., Horiuchi, K., Walcheck, B. (2010) In vivo role of leukocyte ADAM17 in the inflammatory and host responses during E. coli-mediated peritonitis. J. Leukoc. Biol. 87, 1097-1101.
31. Wen, H. (2013) Sepsis induced by cecal ligation and puncture. Methods Mol. Biol. 1031, 117-124.
32. Shrum, B., Anantha, R. V., Xu, S. X., Donnelly, M., Haeryfar, S. M., McCormick, J. K., Mele, T. (2014) A robust scoring system to evaluate sepsis severity in an animal model. BMC Res. Notes 7, 233.
33. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J., Weber, C. F. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541.
34. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., Reeder, J., Sevinsky, J. R., Turnbaugh, P. J., Walters, W. A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R. (2010) QIIME allows analysis of highthroughput community sequencing data. Nat. Methods 7, 335-336.
35. Edgar, R. C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461.
36. Cole, J. R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., Kulam-Syed-Mohideen, A. S., McGarrell, D. M., Marsh, T., Garrity, G. M., Tiedje, J. M. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37, D141-D145.
37. Livak, K. J., Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(2Delta Delta C(T)) method. Methods 25, 402-408.
38. Roth, D. M., Swaney, J. S., Dalton, N. D., Gilpin, E. A., Ross, J. Jr. (2002) Impact of anesthesia on cardiac function during echocardiography in mice. Am. J. Physiol. Heart Circ. Physiol. 282, H2134-H2140.
39. Schulte, W., Bernhagen, J., Bucala, R. (2013) Cytokines in sepsis: potent immunoregulators and potential therapeutic targets—an updated view. Mediators Inflamm. 2013, 165974.
40. Haro, H., Crawford, H. C., Fingleton, B., Shinomiya, K., Spengler, D. M., Matrisian, L. M. (2000) Matrix metalloproteinase-7-dependent release of tumor necrosis factor-alpha in a model of herniated disc resorption. J. Clin. Invest. 105, 143-150.
41. Zheng, Y., Saftig, P., Hartmann, D., Blobel, C. (2004) Evaluation of the contribution of different ADAMs to tumor necrosis factor alpha (TNFalpha) shedding and of the function of the TNFalpha ectodomain in ensuring selective stimulated shedding by the TNFalpha convertase (TACE/ADAM17). J. Biol. Chem. 279, 42898-42906.
42. Vandenbroucke, R. E., Dejonckheere, E., Van Hauwermeiren, F., Lodens, S., De Rycke, R., Van Wonterghem, E., Staes, A., Gevaert, K., López-Otin, C., Libert, C. (2013) Matrix metalloproteinase 13 modulates intestinal epithelial barrier integrity in inflammatory diseases by activating TNF. EMBO Mol. Med. 5, 932-948.
43. Yamashiro, S., Kamohara, H., Yoshimura, T. (2000) Alteration in the responsiveness to tumour necrosis factor-alpha is crucial for maximal expression of monocyte chemoattractant protein-1 in human neutrophils. Immunology 101, 97-103.
44. Delano, M. J., Kelly-Scumpia, K. M., Thayer, T. C., Winfield, R. D., Scumpia, P. O., Cuenca, A. G., Harrington, P. B., O’Malley, K. A., Warner, E., Gabrilovich, S., Mathews, C. E., Laface, D., Heyworth, P. G., Ramphal, R., Strieter, R. M., Moldawer, L. L., Efron, P. A. (2011) Neutrophil mobilization from the bone marrow during polymicrobial sepsis is dependent on CXCL12 signaling. J. Immunol. 187, 911-918.
45. Echtenacher, B., Falk, W., Männel, D. N., Krammer, P. H. (1990) Requirement of endogenous tumor necrosis factor/cachectin for recovery from experimental peritonitis. J. Immunol. 145, 3762-3766.
46. Eskandari, M. K., Bolgos, G., Miller, C., Nguyen, D. T., DeForge, L. E., Remick, D. G. (1992) Anti-tumor necrosis factor antibody therapy fails to prevent lethality after cecal ligation and puncture or endotoxemia. J. Immunol. 148, 2724-2730.
47. Zeni, F., Freeman, B., Natanson, C. (1997) Anti-inflammatory therapies to treat sepsis and septic shock: a reassessment. Crit. Care Med. 25, 1095-1100.
48. Echtenacher, B., Weigl, K., Lehn, N., Männel, D. N. (2001) Tumor necrosis factor-dependent adhesions as a major protective mechanism early in septic peritonitis in mice. Infect. Immun. 69, 3550-3555.
49. Olleros, M. L., Guler, R., Vesin, D., Parapanov, R., Marchal, G., Martinez-Soria, E., Corazza, N., Pache, J. C., Mueller, C., Garcia, I. (2005) Contribution of transmembrane tumor necrosis factor to host defense against Mycobacterium bovis bacillus Calmette-Guerin and Mycobacterium tuberculosis infections. Am. J. Pathol. 166, 1109-1120.
50. Torres, D., Janot, L., Quesniaux, V. F., Grivennikov, S. I., Maillet, I., Sedgwick, J. D., Ryffel, B., Erard, F. (2005) Membrane tumor necrosis factor confers partial protection to Listeria infection. Am. J. Pathol. 167, 1677-1687.
51. Blaydon, D. C., Biancheri, P., Di, W. L., Plagnol, V., Cabral, R. M., Brooke, M. A., van Heel, D. A., Ruschendorf, F., Toynbee, M., Walne, A., O’Toole, E. A., Martin, J. E., Lindley, K., Vulliamy, T., Abrams, D. J., MacDonald, T. T., Harper, J. I., Kelsell, D. P. (2011) Inflammatory skin and bowel disease linked to ADAM17 deletion. N. Engl. J. Med. 365, 1502-1508.
52. Duffy, M. J., Mullooly, M., O’Donovan, N., Sukor, S., Crown, J., Pierce, A., McGowan, P. M. (2011) The ADAMs family of proteases: new biomarkers and therapeutic targets for cancer? Clin. Proteomics 8, 9.
53. Friedman, S., Levy, R., Garrett, W., Doval, D., Bondarde, S., Sahoo, T., Lokanatha, D., Julka, P., Shenoy, K., Nagarkar, R., Bhattacharyya, G., Kumar, K., Nag, S., Mohan, P., Narang, N., Raghunadharao, D., Walia, M., Yao, W., Li, J., Emm, T., Yeleswaram, S., Scherle, P., Newton, R. (2009) Clinical benefit of INCB7839, a potent and selective inhibitor of ADAM10 and ADAM17, in combination with trastuzumab in metastatic HER2 positive breast cancer patients. Cancer Res. 69, 5056 (abs.).