A Metalloprotease Inhibitor Blocks Shedding of the 80-kD TNF Receptor and TNF Processing in T Lymphocytes

Overview

Journal J Exp Med

Specialties Allergy & Immunology
General Medicine

Date 1995 Mar 1

PMID 7869036

Citations 54

Authors

P D Crowe

B N Walter

K M Mohler

R A Black

C F Ware

Affiliations

Soon will be listed here.

Abstract

TNF is synthesized as a 26-kD membrane-anchored precursor and is proteolytically processed at the cell surface to yield the mature secreted 17-kD polypeptide. The 80-kD tumor necrosis factor (TNF) receptor (TNFR80) is also proteolytically cleaved at the cell surface (shed), releasing a soluble ligand-binding receptor fragment. Since processing of TNF and TNFR80 occurs concurrently in activated T cells, we asked whether a common protease may be involved. Here, we present evidence that a recently described inhibitor of TNF processing N-(D,L-[2-(hydroxyaminocarbonyl)methyl]-4-methylpentanoyl)L- 3-(2'naphthyl)- alanyl-L-alanine, 2-aminoethyl amide (TAPI) also blocks shedding of TNFR80, suggesting that these processes may be coordinately regulated during T cell activation. In addition, studies of murine fibroblasts transfected with human TNFR80, or a cytoplasmic deletion form of TNFR80, reveal that inhibition of TNFR80 shedding by TAPI is independent of receptor phosphorylation and does not require the receptor cytoplasmic domain.

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References

Perez C, Albert I, DeFay K, Zachariades N, Gooding L, Kriegler M . A nonsecretable cell surface mutant of tumor necrosis factor (TNF) kills by cell-to-cell contact. Cell. 1990; 63(2):251-8. DOI: 10.1016/0092-8674(90)90158-b. View

Heller R, Song K, Onasch M, Fischer W, Chang D, Ringold G . Complementary DNA cloning of a receptor for tumor necrosis factor and demonstration of a shed form of the receptor. Proc Natl Acad Sci U S A. 1990; 87(16):6151-5. PMC: 54490. DOI: 10.1073/pnas.87.16.6151. View

Gatanaga T, Hwang C, Kohr W, Cappuccini F, Lucci 3rd J, Jeffes E . Purification and characterization of an inhibitor (soluble tumor necrosis factor receptor) for tumor necrosis factor and lymphotoxin obtained from the serum ultrafiltrates of human cancer patients. Proc Natl Acad Sci U S A. 1990; 87(22):8781-4. PMC: 55043. DOI: 10.1073/pnas.87.22.8781. View

Aderka D, Englemann H, Hornik V, Skornick Y, Levo Y, Wallach D . Increased serum levels of soluble receptors for tumor necrosis factor in cancer patients. Cancer Res. 1991; 51(20):5602-7. View

Ware C, Crowe P, VanArsdale T, Andrews J, Grayson M, Jerzy R . Tumor necrosis factor (TNF) receptor expression in T lymphocytes. Differential regulation of the type I TNF receptor during activation of resting and effector T cells. J Immunol. 1991; 147(12):4229-38. View

Aderka D, Engelmann H, Maor Y, Brakebusch C, Wallach D . Stabilization of the bioactivity of tumor necrosis factor by its soluble receptors. J Exp Med. 1992; 175(2):323-9. PMC: 2119112. DOI: 10.1084/jem.175.2.323. View

Van Zee K, Kohno T, FISCHER E, Rock C, Moldawer L, Lowry S . Tumor necrosis factor soluble receptors circulate during experimental and clinical inflammation and can protect against excessive tumor necrosis factor alpha in vitro and in vivo. Proc Natl Acad Sci U S A. 1992; 89(11):4845-9. PMC: 49184. DOI: 10.1073/pnas.89.11.4845. View

Brockhaus M, BAR-KHAYIM Y, Gurwicz S, FRENSDORFF A, HARAN N . Plasma tumor necrosis factor soluble receptors in chronic renal failure. Kidney Int. 1992; 42(3):663-7. DOI: 10.1038/ki.1992.332. View

Cope A, Aderka D, Doherty M, Engelmann H, Gibbons D, Jones A . Increased levels of soluble tumor necrosis factor receptors in the sera and synovial fluid of patients with rheumatic diseases. Arthritis Rheum. 1992; 35(10):1160-9. DOI: 10.1002/art.1780351008. View

10.

Deleuran B, Chu C, Field M, Brennan F, Mitchell T, Feldmann M . Localization of tumor necrosis factor receptors in the synovial tissue and cartilage-pannus junction in patients with rheumatoid arthritis. Implications for local actions of tumor necrosis factor alpha. Arthritis Rheum. 1992; 35(10):1170-8. DOI: 10.1002/art.1780351009. View

11.

Gullberg U, Lantz M, Lindvall L, Olsson I, Himmler A . Involvement of an Asn/Val cleavage site in the production of a soluble form of a human tumor necrosis factor (TNF) receptor. Site-directed mutagenesis of a putative cleavage site in the p55 TNF receptor chain. Eur J Cell Biol. 1992; 58(2):307-12. View

12.

Godfried M, van der Poll T, Jansen J, Romijin J, Schattenkerk J, Endert E . Soluble receptors for tumour necrosis factor: a putative marker of disease progression in HIV infection. AIDS. 1993; 7(1):33-6. View

13.

Armitage R, Macduff B, Ziegler S, Grabstein K . Multiple cytokine secretion by IL-7-stimulated human T cells. Cytokine. 1992; 4(6):461-9. DOI: 10.1016/1043-4666(92)90006-d. View

14.

Aderka D, Wysenbeek A, Engelmann H, Cope A, Brennan F, Molad Y . Correlation between serum levels of soluble tumor necrosis factor receptor and disease activity in systemic lupus erythematosus. Arthritis Rheum. 1993; 36(8):1111-20. DOI: 10.1002/art.1780360812. View

15.

Crowe P, VanArsdale T, Goodwin R, Ware C . Specific induction of 80-kDa tumor necrosis factor receptor shedding in T lymphocytes involves the cytoplasmic domain and phosphorylation. J Immunol. 1993; 151(12):6882-90. View

16.

Tracey K, Cerami A . Tumor necrosis factor, other cytokines and disease. Annu Rev Cell Biol. 1993; 9:317-43. DOI: 10.1146/annurev.cb.09.110193.001533. View

17.

Mohler K, Sleath P, Fitzner J, Cerretti D, Alderson M, Kerwar S . Protection against a lethal dose of endotoxin by an inhibitor of tumour necrosis factor processing. Nature. 1994; 370(6486):218-20. DOI: 10.1038/370218a0. View

18.

Gearing A, Beckett P, Christodoulou M, Churchill M, Clements J, Davidson A . Processing of tumour necrosis factor-alpha precursor by metalloproteinases. Nature. 1994; 370(6490):555-7. DOI: 10.1038/370555a0. View

19.

McGeehan G, Becherer J, Bast Jr R, Boyer C, Champion B, Connolly K . Regulation of tumour necrosis factor-alpha processing by a metalloproteinase inhibitor. Nature. 1994; 370(6490):558-61. DOI: 10.1038/370558a0. View

20.

Hoxie J, Matthews D, Callahan K, Cassel D, Cooper R . Transient modulation and internalization of T4 antigen induced by phorbol esters. J Immunol. 1986; 137(4):1194-201. View