Conversion of proepithelin to epithelins: Roles of SLPI and elastase in host defense and wound repair

Cell

Volumn 111, Issue 6, 2002, Pages 867-878

  Zhu, Jing ^a,b   Nathan, Carl ^a,b   Jin, Wenwen ^c   Sim, Davis ^c   Ashcroft, Gillian S ^c   Wahl, Sharon M ^c   Lacomis, Lynne ^d   Erdjument Bromage, Hediye ^d   Tempst, Paul ^b,d   Wright, Clifford D ^e   Ding, Aihao ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITHELIN; GROWTH FACTOR; INTERLEUKIN 8; LEUKOCYTE ELASTASE; OXIDIZING AGENT; PROGRANULIN; PROTEIN; PROTEINASE; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CELL GROWTH; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME RELEASE; EPITHELIUM CELL; FEMALE; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNITY; LEUKOCYTE ACTIVATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; WOUND HEALING;

ANIMALIA;

EID: 0037074016     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(02)01141-8     Document Type: Article

References (70)

1. Abe T., Kobayashi N., Yoshimura K., Trapnell B.C., Kim H., Hubbard R.C., Brewer M.T., Thompson R.C., Crystal R.G. Expression of the secretory leukoprotease inhibitor gene in epithelial cells. J. Clin. Invest. 87:1991;2207-2215.
2. Ashcroft G.S., Yang X., Glick A.B., Weinstein M., Letterio J.J., Mizel D.E., Anzano M., Greenwell-Wild T., Wahl S.M., Deng C., Roberts A.B. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat. Cell Biol. 1:1999;260-266.
3. Ashcroft G.S., Lei K., Jin W., Longenecker G., Kulkarni A.B., Greenwell-Wild T., Hale-Donze H., McGrady G., Song X.Y., Wahl S.M. Secretory leukocyte protease inhibitor mediates non-redundant functions necessary for normal wound healing. Nat. Med. 6:2000;1147-1153.
4. Avrova A.O., Stewart H.E., De Jong W.D., Heilbronn J., Lyon G.D., Birch P.R. A cysteine protease gene is expressed early in resistant potato interactions with Phytophthora infestans. Mol. Plant Microbe Interact. 12:1999;1114-1119.
5. Baba T., Hoff H.B. 3rd, Nemoto H., Lee H., Orth J., Arai Y., Gerton G.L. Acrogranin, an acrosomal cysteine-rich glycoprotein, is the precursor of the growth-modulating peptides, granulins, and epithelins, and is expressed in somatic as well as male germ cells. Mol. Reprod. Dev. 34:1993;233-243.
6. Baggiolini M., Clark-Lewis I. Interleukin-8, a chemotactic and inflammatory cytokine. FEBS Lett. 307:1992;97-101.
7. Bateman A., Bennett H.P. Granulins. the structure and function of an emerging family of growth factors J. Endocrinol. 158:1998;145-151.
8. Bateman A., Belcourt D., Bennett H., Lazure C., Solomon S. Granulins, a novel class of peptide from leukocytes. Biochem. Biophys. Res. Commun. 173:1990;1161-1168.
9. Belaaouaj A., McCarthy R., Baumann M., Gao Z., Ley T.J., Abraham S.N., Shapiro S.D. Mice lacking neutrophil elastase reveal impaired host defense against gram negative bacterial sepsis. Nat. Med. 4:1998;615-618.
10. Belcourt D.R., Lazure C., Bennett H.P. Isolation and primary structure of the three major forms of granulin-like peptides from hematopoietic tissues of a teleost fish (Cyprinus carpio). J. Biol. Chem. 268:1993;9230-9237.
11. Bhandari V., Palfree R.G., Bateman A. Isolation and sequence of the granulin precursor cDNA from human bone marrow reveals tandem cysteine-rich granulin domains. Proc. Natl. Acad. Sci. USA. 89:1992;1715-1719.
12. Carp H., Janoff A. Inactivation of bronchial mucous proteinase inhibitor by cigarette smoke and phagocyte-derived oxidants. Exp. Lung Res. 1:1980;225-237.
13. Caughey G.H. Serine proteinases of mast cell and leukocyte granules. A league of their own. Am. J. Respir. Crit. Care Med. 150:1994;S138-S142.
14. Chien C.T., Bartel P.L., Sternglanz R., Fields S. The two-hybrid system. a method to identify and clone genes for proteins that interact with a protein of interest Proc. Natl. Acad. Sci. USA. 88:1991;9578-9582.
15. Couto M.A., Harwig S.S., Cullor J.S., Hughes J.P., Lehrer R.I. Identification of eNAP-1, an antimicrobial peptide from equine neutrophils. Infect. Immun. 60:1992;3065-3071.
16. Daniel R., He Z., Carmichael K.P., Halper J., Bateman A. Cellular localization of gene expression for progranulin. J. Histochem. Cytochem. 48:2000;999-1009.
17. DelMar E.G., Largman C., Brodrick J.W., Geokas M.C. A sensitive new substrate for chymotrypsin. Anal. Biochem. 99:1979;316-320.
18. Diaz-Cueto L., Stein P., Jacobs A., Schultz R.M., Gerton G.L. Modulation of mouse preimplantation embryo development by acrogranin (epithelin/granulin precursor). Dev. Biol. 217:2000;406-418.
19. Drew A.F., Liu H., Davidson J.M., Daugherty C.C., Degen J.L. Wound-healing defects in mice lacking fibrinogen. Blood. 97:2001;3691-3698.
20. Eisenberg S.P., Hale K.K., Heimdal P., Thompson R.C. Location of the protease-inhibitory region of secretory leukocyte protease inhibitor. J. Biol. Chem. 265:1990;7976-7981.
21. Fuortes M., Jin W.W., Nathan C. Adhesion-dependent protein tyrosine phosphorylation in neutrophils treated with tumor necrosis factor. J. Cell Biol. 120:1993;777-784.
22. Fuortes M., Melchior M., Han H., Lyon G., Nathan C. Role of the tyrosine kinase pyk2 in the integrin-dependent activation of human neutrophils by TNF. J. Clin. Invest. 104:1999;327-335.
23. Grobmyer S.R., Barie P.S., Nathan C.F., Fuortes M., Lin E., Lowry S.F., Wright C.D., Weyant M.J., Hydo L., Reeves F.et al. Secretory leukocyte protease inhibitor, an inhibitor of neutrophil activation, is elevated in serum in human sepsis and experimental endotoxemia. Crit. Care Med. 28:2000;1276-1282.
24. Grutter M.G., Fendrich G., Huber R., Bode W. The 2.5 A X-ray crystal structure of the acid-stable proteinase inhibitor from human mucous secretions analysed in its complex with bovine alpha-chymotrypsin. EMBO J. 7:1988;345-351.
25. He Z., Bateman A. Progranulin gene expression regulates epithelial cell growth and promotes tumor growth in vivo. Cancer Res. 59:1999;3222-3229.
26. Helmig R., Uldbjerg N., Ohlsson K. Secretory leukocyte protease inhibitor in the cervical mucus and in the fetal membranes. Eur. J. Obstet. Gynecol. Reprod. Biol. 59:1995;95-101.
27. Hong S.J., Kang K.W. Purification of granulin-like polypeptide from the blood-sucking leech, Hirudo nipponia. Protein Expr. Purif. 16:1999;340-346.
28. Hrabal R., Chen Z., James S., Bennett H.P., Ni F. The hairpin stack fold, a novel protein architecture for a new family of protein growth factors. Nat. Struct. Biol. 3:1996;747-752.
29. Hunt T.K. Basic principles of wound healing. J. Trauma. 30:1990;S122-S128.
30. Hutchison D.C. The role of proteases and antiproteases in bronchial secretions. Eur. J. Respir. Dis. Suppl. 153:1987;78-85.
31. Jin F.Y., Nathan C., Radzioch D., Ding A. Secretory leukocyte protease inhibitor. a macrophage product induced by and antagonistic to bacterial lipopolysaccharide Cell. 88:1997;417-426.
32. Jin F., Nathan C.F., Radzioch D., Ding A. Lipopolysaccharide-related stimuli induce expression of the secretory leukocyte protease inhibitor, a macrophage-derived lipopolysaccharide inhibitor. Infect. Immun. 66:1998;2447-2452.
33. Kramps J.A., van Twisk C., van der Linden A.C. L-Pyroglutamyl-L-prolyl-L-valine-p-nitroanilide, a highly specific substrate for granulocyte elastase. Scand. J. Clin. Lab. Invest. 43:1983;427-432.
34. Lee C.H., Igarashi Y., Hohman R.J., Kaulbach H., White M.V., Kaliner M.A. Distribution of secretory leukoprotease inhibitor in the human nasal airway. Am. Rev. Respir. Dis. 147:1993;710-716.
35. Martin P. Wound healing - aiming for perfect skin regeneration. Science. 276:1997;75-81.
36. Mashimo H., Wu D.C., Podolsky D.K., Fishman M.C. Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor. Science. 274:1996;262-265.
37. McElvaney N.G., Nakamura H., Birrer P., Hebert C.A., Wong W.L., Alphonso M., Baker J.B., Catalano M.A., Crystal R.G. Modulation of airway inflammation in cystic fibrosis. In vivo suppression of interleukin-8 levels on the respiratory epithelial surface by aerosolization of recombinant secretory leukoprotease inhibitor. J. Clin. Invest. 90:1992;1296-1301.
38. McQuibban G.A., Gong J.H., Tam E.M., McCulloch C.A., Clark-Lewis I., Overall C.M. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science. 289:2000;1202-1206.
39. Mellet P., Ermolieff J., Bieth J.G. Mapping the heparin-binding site of mucus proteinase inhibitor. Biochemistry. 34:1995;2645-2652.
40. Nathan C.F. Neutrophil activation on biological surfaces. Massive secretion of hydrogen peroxide in response to products of macrophages and lymphocytes. J. Clin. Invest. 80:1987;1550-1560.
41. Nathan C., Srimal S., Farber C., Sanchez E., Kabbash L., Asch A., Gailit J., Wright S.D. Cytokine-induced respiratory burst of human neutrophils. dependence on extracellular matrix proteins and CD11/CD18 integrins J. Cell Biol. 109:1989;1341-1349.
42. Ohlsson K., Bjartell A., Lilja H. Secretory leucocyte protease inhibitor in the male genital tract. PSA-induced proteolytic processing in human semen and tissue localization J. Androl. 16:1995;64-74.
43. Park P.W., Reizes O., Bernfield M. Cell surface heparan sulfate proteoglycans. selective regulators of ligand-receptor encounters J. Biol. Chem. 275:2000;29923-29926.
44. Plowman G.D., Green J.M., Neubauer M.G., Buckley S.D., McDonald V.L., Todaro G.J., Shoyab M. The epithelin precursor encodes two proteins with opposing activities on epithelial cell growth. J. Biol. Chem. 267:1992;13073-13078.
45. Rappolee D.A., Werb Z. Secretory products of phagocytes. Curr. Opin. Immunol. 1:1988;47-55.
46. Rehault S., Brillard-Bourdet M., Juliano M.A., Juliano L., Gauthier F., Moreau T. New, sensitive fluorogenic substrates for human cathepsin G based on the sequence of serpin-reactive site loops. J. Biol. Chem. 274:1999;13810-13817.
47. Romer J., Bugge T.H., Pyke C., Lund L.R., Flick M.J., Degen J.L., Dano K. Impaired wound healing in mice with a disrupted plasminogen gene. Nat. Med. 2:1996;287-292.
48. Sallenave J.M., Si-Ta har M., Cox G., Chignard M., Gauldie J. Secretory leukocyte proteinase inhibitor is a major leukocyte elastase inhibitor in human neutrophils. J. Leukoc. Biol. 61:1997;695-702.
49. Shoyab M., McDonald V.L., Byles C., Todaro G.J., Plowman G.D. Epithelins 1 and 2. isolation and characterization of two cysteine-rich growth-modulating proteins Proc. Natl. Acad. Sci. USA. 87:1990;7912-7916.
50. Singer A.J., Clark R.A. Cutaneous wound healing. N. Engl. J. Med. 341:1999;738-746.
51. Somorin O., Tokura S., Nishi N., Noguchi J. The action of trypsin on synthetic chromogenic arginine substrates. J. Biochem. (Tokyo). 85:1979;157-162.
52. Song X., Jin W., Thompson J., Mizel D.E., Lei K., Billinghurst R.C., Poole A.R., Whal S. Secretory leukocyte protease inhibitor suppresses the inflammation and joint damage of bacterial cell wall-induced arthritis. J. Exp. Med. 190:1999;535-542.
53. Sparro G., Galdenzi G., Eleuteri A.M., Angeletti M., Schroeder W., Fioretti E. Isolation and N-terminal sequence of multiple forms of granulins in human urine. Protein Expr. Purif. 10:1997;169-174.
54. Taggart C., Coakley R.J., Greally P., Canny G., O'Neill S.J., McElvaney N.G. Increased elastase release by CF neutrophils is mediated by tumor necrosis factor-alpha and interleukin-8. Am. J. Physiol. Lung Cell. Mol. Physiol. 278:2000;L33-L41.
55. Tempst P., Geromanos S., Elicone C., Erdjument-Bromage H. Improvements in microsequencer performance for low picomole sequence analysis. Methods. 6:1994;248-261.
56. Thompson R.C., Ohlsson K. Isolation, properties, and complete amino acid sequence of human secretory leukocyte protease inhibitor, a potent inhibitor of leukocyte elastase. Proc. Natl. Acad. Sci. USA. 83:1986;6692-6696.
57. van Wetering S., van der Linden A.C., van Sterkenburg M.A., de Boer W.I., Kuijpers A.L., Schalkwijk J., Hiemstra P.S. Regulation of SLPI and elafin release from bronchial epithelial cells by neutrophil defensins. Am. J. Physiol. Lung Cell. Mol. Physiol. 278:2000;L51-L58.
58. Wahl S.M., Worley P., Jin W., McNeely T.B., Eisenberg S., Fasching C., Orenstein J.M., Janoff E.N. Anatomic dissociation between HIV-1 and its endogenous inhibitor in mucosal tissues. Am. J. Pathol. 150:1997;1275-1284.
59. Weinzimer S.A., Gibson T.B., Collett-Solberg P.F., Khare A., Liu B., Cohen P. Transferrin is an insulin-like growth factor-binding protein-3 binding protein. J. Clin. Endocrinol. Metab. 86:2001;1806-1813.
60. Witte M.B., Barbul A. General principles of wound healing. Surg. Clin. North Am. 77:1997;509-528.
61. Wright C.D., Kennedy J.A., Zitnik R.J., Kashem M.A. Inhibition of murine neutrophil serine proteinases by human and murine secretory leukocyte protease inhibitor. Biochem. Biophys. Res. Commun. 254:1999;614-617.
62. Xu S.Q., Tang D., Chamberlain S., Pronk G., Masiarz F.R., Kaur S., Prisco M., Zanocco-Marani T., Baserga R. The granulin/epithelin precursor abrogates the requirement for the insulin-like growth factor 1 receptor for growth in vitro. J. Biol. Chem. 273:1998;20078-20083.
63. Ying Q.L., Kemme M., Simon S.R. Functions of the N-terminal domain of secretory leukoprotease inhibitor. Biochemistry. 33:1994;5445-5450.
64. Zanocco-Marani T., Bateman A., Romano G., Valentinis B., He Z.H., Baserga R. Biological activities and signaling pathways of the granulin/epithelin precursor. Cancer Res. 59:1999;5331-5340.
65. Zhang H., Serrero G. Inhibition of tumorigenicity of the teratoma PC cell line by transfection with antisense cDNA for PC cell-derived growth factor (PCDGF, epithelin/granulin precursor). Proc. Natl. Acad. Sci. USA. 95:1998;14202-14207.
66. Zhang Y., DeWitt D.L., McNeely T.B., Wahl S.M., Wahl L.M. Secretory leukocyte protease inhibitor suppresses the production of monocyte prostaglandin H synthase-2, prostaglandin E2, and matrix metalloproteinases. J. Clin. Invest. 99:1997;894-900.
67. Zhou J., Gao G., Crabb J.W., Serrero G. Purification of an autocrine growth factor homologous with mouse epithelin precursor from a highly tumorigenic cell line. J. Biol. Chem. 268:1993;10863-10869.
68. Zhu J., Kahn C.R. Analysis of a peptide hormone-receptor interaction in the yeast two-hybrid system. Proc. Natl. Acad. Sci. USA. 94:1997;13063-13068.
69. Zhu J., Nathan C., Ding A. Suppression of macrophage responses to bacterial lipopolysaccharide by a non-secretory form of secretory leukocyte protease inhibitor. Biochim. Biophys. Acta. 1451:1999;219-223.
70. Zitnik R.J., Zhang J., Kashem M.A., Kohno T., Lyons D.E., Wright C.D., Rosen E., Goldberg I., Hayday A.C. The cloning and characterization of a murine secretory leukocyte protease inhibitor cDNA. Biochem. Biophys. Res. Commun. 232:1997;687-697.