ADAM17 cleaves CD16b (FcγRIIIb) in human neutrophils

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 3, 2013, Pages 680-685

  Wang, Yue ^a,b   Wu, Jianming ^a   Newton, Robert ^c   Bahaie, Nooshin S ^a   Long, Chunmei ^a   Walcheck, Bruce ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c Experimental Station   (United States)

Author keywords

ADAM17; Apoptosis; Fc receptor; Metalloprotease; Neutrophil

Indexed keywords

ADAM PROTEIN; ADAM10 ENDOPEPTIDASE; ADAM17 PROTEIN; ADERBASIB; CD16 ANTIGEN; CD16B ANTIGEN; DOCETAXEL; METALLOPROTEINASE INHIBITOR; MONOCLONAL ANTIBODY; TRASTUZUMAB; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG SELECTIVITY; DRUG TARGETING; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN VERSUS ANIMAL COMPARISON; LEUKOCYTE ACTIVATION; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CLEAVAGE; PROTEIN DOMAIN;

ADAM PROTEINS; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; FIBROBLASTS; FLOW CYTOMETRY; GPI-LINKED PROTEINS; HUMANS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; NEUTROPHIL ACTIVATION; NEUTROPHILS; PROTEASE INHIBITORS; RECEPTORS, IGG; SEQUENCE HOMOLOGY, AMINO ACID;

MUS;

EID: 84872044156     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.11.027     Document Type: Article

References (52)

1. Ravetch J.V., Perussia B. Alternative membrane forms of FctRIII (CD16) on human NK cells and neutrophils: cell-type specific expression of two genes which differ in single nucleotide substitutions. J. Exp. Med. 1989, 170:481-497.
2. Selvaraj P., Rosse W.F., Silber R., Springer T.A. The major Fc receptor in blood has a phosphatidylinositol anchor and is deficient in paroxysmal noctural hemoglobinuria. Nature 1988, 333:565-567.
3. Huizinga T.W.J., Kerst M., Nuyens J.H., Vlug A., Von dem Borne A.E.G.K., Roos D., Tetteroo P.A.T. Binding characteristics of dimeric IgG subclass complexes to human neutrophils. J. Immunol. 1989, 142:2359-2364.
4. Edwards S.W., Hallett M.B. Seeing the wood for the trees: the forgotten role of neutrophils in rheumatoid arthritis. Immunol. Today 1997, 18:320-324.
5. Tosi M.F., Zakem H. Surface expression of Fc gamma receptor III (CD16) on chemoattractant-stimulated neutrophils is determined by both surface shedding and translocation from intracellular storage compartments. J. Clin. Invest. 1992, 90:462-470.
6. Huizinga T.W., de Haas M., Kleijer M., Nuijens J.H., Roos D., von dem Borne A.E. Soluble Fc gamma receptor III in human plasma originates from release by neutrophils. J. Clin. Invest. 1990, 86:416-423.
7. Dransfield I., Buckle A.M., Savill J.S., McDowall A., Haslett C., Hogg N. Neutrophil apoptosis is associated with a reduction in CD16 (Fc gamma RIII) expression. J. Immunol. 1994, 153:1254-1263.
8. Middelhoven P.J., van Buul J.D., Hordijk P.L., Roos D. Different proteolytic mechanisms involved in Fc gamma RIIIb shedding from human neutrophils. Clin. Exp. Immunol. 2001, 125:169-175.
9. Bazil V., Strominger J.L. Metalloprotease and serine protease are involved in cleavage of CD43, CD44, and CD16 from stimulated granulocytes Induction of cleavage of L-selectin via CD16. J. Immunol. 1994, 152:1314-1322.
10. Moldovan I., Galon J., Maridonneau-Parini I., Roman-Roman S., Mathiot C., Fridman W.H., Sautes-Fridman C. Regulation of production of soluble Fc gamma receptors type III in normal and pathological conditions. Immunol. Lett. 1999, 68:125-134.
11. Reiss K., Saftig P. The "a disintegrin and metalloprotease" (ADAM) family of sheddases: physiological and cellular functions. Semin. Cell Dev. Biol. 2009, 20:126-137.
12. Walcheck B., Herrera A.H., Hill C.S., Mattila P.E., Whitney A.R., DeLeo F.R. ADAM17 activity during human neutrophil activation and apoptosis. Eur. J. Immunol. 2006, 36:968-976.
13. Horiuchi K., Kimura T., Miyamoto T., Takaishi H., Okada Y., Toyama Y., Blobel C.P. Cutting edge: TNF-alpha-converting enzyme (TACE/ADAM17) inactivation in mouse myeloid cells prevents lethality from endotoxin shock. J. Immunol. 2007, 179:2686-2689.
14. Wang Y., Herrera A.H., Li Y., Belani K.K., Walcheck B. Regulation of mature ADAM17 by redox agents for L-selectin shedding. J. Immunol. 2009, 182:2449-2457.
15. Wang Y., Robertson J.D., Walcheck B. Different signaling pathways stimulate a disintegrin and metalloprotease-17 (ADAM17) in neutrophils during apoptosis and activation. J. Biol. Chem. 2011, 286:38980-38988.
16. Long C., Wang Y., Herrera A.H., Horiuchi K., Walcheck B. In vivo role of leukocyte ADAM17 in the inflammatory and host responses during E coli-mediated peritonitis. J. Leukoc. Biol. 2010, 87:1097-1101.
17. Wang Y., Zhang A.C., Ni Z., Herrera A., Walcheck B. ADAM17 activity and other mechanisms of soluble L-selectin production during death receptor-induced leukocyte apoptosis. J. Immunol. 2010, 184:4447-4454.
18. Stringer R.E., Hart C.A., Edwards S.W. Sodium butyrate delays neutrophil apoptosis: role of protein biosynthesis in neutrophil survival. Br. J. Haematol. 1996, 92:169-175.
19. Whyte M.K., Savill J., Meagher L.C., Lee A., Haslett C. Coupling of neutrophil apoptosis to recognition by macrophages: coordinated acceleration by protein synthesis inhibitors. J. Leukoc. Biol. 1997, 62:195-202.
20. Ward C., Chilvers E.R., Lawson M.F., Pryde J.G., Fujihara S., Farrow S.N., Haslett C., Rossi A.G. NF-kappaB activation is a critical regulator of human granulocyte apoptosis in vitro. J. Biol. Chem. 1999, 274:4309-4318.
21. Zhang B. Elucidation of molecular events leading to neutrophil apoptosis following phagocytosis: cross-talk between caspase 8, reactive oxygen species, and MAPK/ERK activation. J. Biol. Chem. 2003, 278:28443-28454.
22. Mazzola R.D., Zhu Z., Sinning L., McKittrick B., Lavey B., Spitler J., Kozlowski J., Neng-Yang S., Zhou G., Guo Z., Orth P., Madison V., Sun J., Lundell D., Niu X. Discovery of novel hydroxamates as highly potent tumor necrosis factor-alpha converting enzyme inhibitors Part II: optimization of the S3' pocket. Bioorg. Med. Chem. Lett. 2008, 18:5809-5814.
23. Ott G.R., Asakawa N., Lu Z., Anand R., Liu R.-Q., Covington M.B., Vaddi K., Qian M., Newton R.C., Christ D.D., Trzaskos J.M., Duan J.J.-W. Potent, exceptionally selective, orally bioavailable inhibitors of TNF-alpha converting enzyme (TACE): novel 2-substituted-1H-benzo[d]imidazol-1-yl)methyl)benzamide P1' substituents. Bioorg. Med. Chem. Lett. 2008, 18:1577-1582.
24. Hundhausen C., Misztela D., Berkhout T.A., Broadway N., Saftig P., Reiss K., Hartmann D., Fahrenholz F., Postina R., Matthews V., Kallen K.J., Rose-John S., Ludwig A. The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood 2003, 102:1186-1195.
25. Reddy P., Slack J.L., Davis R., Cerretti D.P., Kozlosky C.J., Blanton R.A., Shows D., Peschon J.J., Black R.A. Functional analysis of the domain structure of tumor necrosis factor-alpha converting enzyme. J. Biol. Chem. 2000, 275:14608-14614.
26. Walcheck B., Alexander S.R., St Hill C.A., Matala E. ADAM-17-independent shedding of L-selectin. J. Leukoc. Biol. 2003, 74:389-394.
27. Verma A., Ngundi M.M., Meade B.D., De Pascalis R., Elkins K.L., Burns D.L. Analysis of the Fc gamma receptor-dependent component of neutralization measured by anthrax toxin neutralization assays. Clin. Vaccine Immunol. 2009, 16:1405-1412.
28. Tamm A., Schmidt R.E. The binding epitopes of human CD16 (Fc gamma RIII) monoclonal antibodies Implications for ligand binding. J. Immunol. 1996, 157:1576-1581.
29. Fridman J.S., Caulder E., Hansbury M., Liu X., Yang G., Wang Q., Lo Y., Zhou B.B., Pan M., Thomas S.M., Grandis J.R., Zhuo J., Yao W., Newton R.C., Friedman S.M., Scherle P.A., Vaddi K. Selective inhibition of ADAM metalloproteases as a novel approach for modulating ErbB pathways in cancer. Clin. Cancer Res. 2007, 13:1892-1902.
30. Zhou B.-B.S., Peyton M., He B., Liu C., Girard L., Caudler E., Lo Y., Baribaud F., Mikami I., Reguart N., Yang G., Li Y., Yao W., Vaddi K., Gazdar A.F., Friedman S.M., Jablons D.M., Newton R.C., Fridman J.S., Minna J.D., et al. Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer. Cancer Cell 2006, 10:39-50.
31. Witters L., Scherle P., Friedman S., Fridman J., Caulder E., Newton R., Lipton A. Synergistic inhibition with a dual epidermal growth factor receptor/HER-2/neu tyrosine kinase inhibitor and a disintegrin and metalloprotease inhibitor. Cancer Res. 2008, 68:7083-7089.
32. Newton R.C., Bradley E.C., Levy R.S., Doval D., Bondarde S., Sahoo T.P., Lokanatha D., Julka P.K., Nagarkar R., Friedman S.M. Clinical benefit of INCB7839, a potent and selective ADAM inhibitor, in combination with trastuzumab in patients with metastatic HER2+ breast cancer. J. Clin. Oncol. 2010, 28. (Abstract 3025).
33. Le Gall S.M., Bobé P., Reiss K., Horiuchi K., Niu X.-D., Lundell D., Gibb D.R., Conrad D., Saftig P., Blobel C.P. ADAMs 10 and 17 represent differentially regulated components of a general shedding machinery for membrane proteins such as transforming growth factor alpha, L-selectin, and tumor necrosis factor alpha. Mol. Biol. Cell 2009, 20:1785-1794.
34. Le Gall S.M., Maretzky T., Issuree P.D.A., Niu X.-D., Reiss K., Saftig P., Khokha R., Lundell D., Blobel C.P. ADAM17 is regulated by a rapid and reversible mechanism that controls access to its catalytic site. J. Cell Sci. 2010, 123:3913-3922.
35. Middelhoven P.J., Ager A., Roos D., Verhoeven A.J. Involvement of a metalloprotease in the shedding of human neutrophil Fc gammaRIIIB. FEBS Lett. 1997, 414:14-18.
36. Galon J., Moldovan I., Galinha A., Provost-Marloie M.A., Kaudewitz H., Roman-Roman S., Fridman W.H., Sautès C. Identification of the cleavage site involved in production of plasma soluble Fc gamma receptor type III (CD16). Eur. J. Immunol. 1998, 28:2101-2107.
37. Harrison D., Phillips J.H., Lanier L.L. Involvement of a metalloprotease in spontaneous and phorbol ester-induced release of natural killer cell-associated Fc gamma RIII (CD16-II). J. Immunol. 1991, 147:3459-3465.
38. Nimmerjahn F., Ravetch J.V. Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 2008, 8:34-47.
39. Athens J.W., Haab O.P., Raab S.O., Mauer A.M., Ashenbrucker H., Cartwright G.E., Wintrobe M.M. Leukokinetic studies. IV The total blood, circulating and marginal granulocyte pools and the granulocyte turnover rate in normal subjects. J. Clin. Invest. 1961, 40:989-995.
40. Kerst J.M., de Haas M., Van Der Schoot C.E., Slaper-Cortenbach I.C., Kleijer M., von dem Borne A.E., van Oers R.H. Recombinant granulocyte colony-stimulating factor administration to healthy volunteers: induction of immunophenotypically and functionally altered neutrophils via an effect on myeloid progenitor cells. Blood 1993, 82:3265-3272.
41. Huizinga T.W., de Haas M., van Oers M.H., Kleijer M., Vilé H., van der Wouw P.A., Moulijn A., van Weezel H., Roos D., von dem Borne A.E. The plasma concentration of soluble Fc-gamma RIII is related to production of neutrophils. Br. J. Haematol. 1994, 87:459-463.
42. Homburg C.H., de Haas M., von dem Borne A.E., Verhoeven A.J., Reutelingsperger C.P., Roos D. Human neutrophils lose their surface Fc gamma RIII and acquire Annexin V binding sites during apoptosis in vitro. Blood 1995, 85:532-540.
43. Tape C.J., Willems S.H., Dombernowsky S.L., Stanley P.L., Fogarasi M., Ouwehand W., McCafferty J., Murphy G. Cross-domain inhibition of TACE ectodomain. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5578-5583.
44. Ory P.A., Clark M.R., Kwoh E.E., Clarkson S.B., Goldstein I.M. Sequences of complementary DNAs that encode the NA1 and NA2 forms of Fc receptor III on human neutrophils. J. Clin. Invest. 1989, 84:1688-1691.
45. Condon T.P., Flournoy S., Sawyer G.J., Baker B.F., Kishimoto T.K., Bennett C.F. ADAM17 but not ADAM10 mediates tumor necrosis factor-alpha and L-selectin shedding from leukocyte membranes. Antisense Nucleic Acid Drug Dev. 2001, 11:107-116.
46. Li Y., Brazzell J., Herrera A., Walcheck B. ADAM17 deficiency by mature neutrophils has differential effects on L-selectin shedding. Blood 2006, 108:2275-2279.
47. Jang J.E., Hidalgo A., Frenette P.S. Intravenous immunoglobulins modulate neutrophil activation and vascular injury through FcgammaRIII and SHP-1. Circ. Res. 2012, 110:1057-1066.
48. Bell J.H., Herrera A.H., Li Y., Walcheck B. Role of ADAM17 in the ectodomain shedding of TNF-alpha and its receptors by neutrophils and macrophages. J. Leukoc. Biol. 2007, 82:173-176.
49. Chalaris A., Rabe B., Paliga K., Lange H., Laskay T., Fielding C.A., Jones S.A., Rose-John S., Scheller J. Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils. Blood 2007, 110:1748-1755.
50. Kurosaki T., Ravetch J.V. A single amino acid in the GPI attachment domain determines the membrane topology of Fc gamma RIII. Nature 1989, 342:805-807.
51. Hibbs M.L., Selvaraj P., Carpén O., Springer T.A., Kuster H., Jouvin M.H., Kinet J.P. Novel mechanisms for regulating expression of Fc gamma RIII (CD16) membrane isoforms. Science 1989, 246:1608-1611.
52. Mechetina L.V., Najakshin A.M., Alabyev B.Y., Chikaev N.A., Taranin A.V. Identification of CD16-2, a novel mouse receptor homologous to CD16/Fc gamma RIII. Immunogenetics 2002, 54:463-468.