Biosynthesis, processing and sorting of neutrophil proteins: Insight into neutrophil granule development

European Journal of Haematology

Volumn 58, Issue 3, 1997, Pages 137-153

  Gullberg, Urban ^a   Andersson, Elinor ^a   Garwicz, Daniel ^a   Lindmark, Anders ^a   Olsson, Inge ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Defensins; Myeloperoxidase; Serine proteases; Sorting

Indexed keywords

MYELOPEROXIDASE; SERINE PROTEINASE;

BIOSYNTHESIS; CELL GRANULE; HUMAN; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0030890357     PISSN: 09024441     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0609.1997.tb00940.x     Document Type: Review

References (134)

1. SACHS L, LOTEM J. The network of hematopoietic cytokines. Proc Soc Exp Biol Med 1994: 206: 170-175.
2. ORKIN SH. Transcription factors and hematopoietic development. J Biol Chem 1995: 270: 4955-4958.
3. COHN ZA, HIRSCH JG. The isolation and properties of the specific cytoplasmic granules of rabbit polymorphonuclear leukocytes. J Exp Med 1960: 112: 983-1004.
4. BAINTON DF, ULLYOT JL, FARQUHAR MG. The development of neutrophilic polymorphonuclear leukocytes in human bone marrow. J Exp Med 1971: 134: 907-934.
5. BAINTON DF. Developmental biology of neutrophils and eosinophils. In: GALLIN JI, GOLDSTEIN IM, SNYDERMAN R, eds. Inflammation, basic principles and clinical correlates. New York: Raven Press, 1992: 303-324.
6. BORREGAARD N, LOLLIKE K, KJELDSEN L, et al. Human neutrophil granules and secretory vesicles. Eur J Haematol 1993: 51: 187-198.
7. WEST BC, ROSENTHAL AS, GELB NA, KIMBALL HR. Separation and characterization of human neutrophil granules. Am J Pathol 1974: 77: 41-66.
8. BRETZ U, BAGGIOLINI M. Biochemical and morphological characterization of azurophil and specific granules of human neutrophilic polymorphonuclear leukocytes. J Cell Biol 1974: 63: 251-269.
9. LEFFELL MS, SPITZNAGEL JK. Association of lactoferrin with lysozyme in granules of human polymorphonuclear leukocytes. Infect Immun 1972: 6: 761-765.
10. SPITZNAGEL JK, DALLDORF FG, LEFFELL MS, et al. Character of azurophil and specific granules purified from human polymorphonuclear leukocytes. Lab Invest 1974: 30: 774-785.
11. MURPHY G, BRETZ U, BAGGIOLINI M, REYNOLDS JJ. The latent collagenase and gelatinase of human polymorphonuclear neutrophil leukocytes. Biochem J 1980: 192: 517-525.
12. DEWALD B, BRETZ U, BAGGIOLINI M. Release of gelatinase from a novel secretory compartment of human neutrophils. J Clin Invest 1982: 70: 518-525.
13. MOLLINEDO F, SCHNEIDER DL. Subcellular localization of cytochrome b and ubiquinone in a tertiary granule of resting neutrophils and evidence for a proton pump ATPase. J Biol Chem 1984: 259: 7143-7150.
14. SENGELØV H, NIELSEN MH, BORREGAARD N. Separation of human neutrophil plasma membrane from intracellular membranes containing alkaline phosphatase and NADPH-oxidase activity by free flow electrophoresis. J Biol Chem 1992: 267: 14912-14917.
15. BORREGAARD N, MILLER L, SPRINGER TA. Chemoattractant-regulated mobilization of a novel intracellular compartment in human neutrophils. Science 1987: 237: 1204-1206.
16. BORREGAARD N, KJELDSEN L, RYGAARD K, et al. Stimulus-dependent secretion of plasma proteins from human neutrophils. J Clin Invest 1992: 90: 86-96.
17. GRIFFITHS GM. Secretory lysosomes - a mechanism of regulated secretion in haemopoietic cells. Trends Cell Biol 1996: 6:329-332.
18. OWEN CA, CAMPBELL MA, SANNES PL, BOUKEDES SS, CAMPBELL EJ. Cell surface-bound elastase and cathepsin G on human neutrophils: a novel, non-oxidative mechanism by which neutrophils focus and preserve catalytic activity of serine proteases. J Cell Biol 1995: 131: 775-789.
19. WEERSINK AJL, VAN KESSEL KPM, VAN DEN TOL ME, et al. Human granulocytes express a 55-kDa lipopolysaccharide-binding protein on the cell surface that is identical to the bactericidal/permeability-increasing protein. J Immunol 1993: 150: 253-263.
20. WEINRAUCH Y, FOREMAN A, SHU C, et al. Extracellular accumulation of potently microbicidal bactericidal/ permeability-increasing protein and p15s in an evolving sterile rabbit peritoneal inflammatory exudate. J Clin Invest 1995: 95: 1916-1924.
21. BREDEROO P, VAN DER MEULEN J, MOMMAAS-KIENHUIS AM. Development of the granule population in neutrophil granulocytes from human bone marrow. Cell Tissue Res 1983: 234: 469-496.
22. BRETON-GORIUS J, REYES F. Ultrastructure of human bone marrow cell maturation. Int Rev Cytol 1976: 46: 251-321.
23. PRYZWANSKY KB, BRETON-GORIUS J. Identification of a subpopulation of primary granules in human neutrophils based upon maturation and distribution. Study by transmission electron microscopy cytochemistry and high voltage electron microscopy of whole cell preparations. Lab Invest 1985: 53: 664-671.
24. GANZ T, SELSTEDT ME, LEHRER RI. Defensins. Eur J Haematol 1990: 44: 1-8.
25. GANZ T, SELSTED ME, SZKLAREK D, et al. Defensins. Natural peptide antibiotics of human neutrophils. J Clin Invest 1985: 76: 1427-1435.
26. BERLINER N, HSING A, GRAUBERT T, et al. Granulocyte colony-stimulating factor induction of normal human bone marrow progenitors results in neutrophil-specific gene expression. Blood 1995: 85: 799-803.
27. RICE WG, GANZ T, KINKADE JR JM, SELSTED ME, LEHRER RI, PARMLEY RT. Defensin-rich dense granules of human neutrophils. Blood 1987: 70: 757-765.
28. EGESTEN A, BRETON-GORIUS J, GUICHARD J, GULLBERG U, OLSSON I. The heterogeneity of azurophil granules in neutrophil promyelocytes; immunogold localization of myeloperoxidase, cathepsin G, elastase, proteinase 3, and bactericidal/permeability increasing protein. Blood 1994: 83: 2985-2994.
29. WEISS J, ELSBACH P, OLSSON I, ODEBERG H. Purification and characterization of a potent bactericidal and membrane active protein from the granules of human polymorphonuclear leukocytes. J Biol Chem 1978: 253: 2664-2672.
30. ELSBACH P, WEISS J, FRANSON RC, BECKERDITE-QUAGLIATA S, SCHNEIDER A, HARRIS L. Separation and purification of a potent bactericidal/permeability increasing protein and a closely associated phospholipase A2 from rabbit polymorphonuclear leukocytes. Observations on their relationship. J Biol Chem 1979: 254: 11000-11009.
31. WEISS J, OLSSON I. Cellular and subcellular localization of the bactericidal/permeability-increasing protein of neutrophils. Blood 1987: 69: 652-659.
32. GRAY PW, FLAGGS G, LEONG SR, et al. Cloning of the cDNA of a human neutrophil bactericidal protein. Structural and functional correlations. J Biol Chem 1989: 264: 9505-9509.
33. FALK RJ, JENNETTE JC. Anti-neutrophil cytoplasmic autoantibodies with specificity for myeloperoxidase in patients with systemic vasculitis and idiopathic necrotizing and crescent glomerulonephritis. N Engl J Med 1988: 318: 1651-1657.
34. GROSS WL, CSERNOK E, HELMCHEN LJ. Antineutrophil cytoplasmic autoantibodies, autoantigens, and systemic vasculitis. APMIS 1995: 103: 81-97.
35. SINGER II, SCHOTT S, KAWKA DW, KAZAZIS DM. Adhesomes: specific granules containing receptors for laminin, C3bi/fibrinogen, and vitronectin in human polymorphonuclear leukocytes and monocytes. J Cell Biol 1989: 109: 3169-3182.
36. GALLIN JI. Neutrophil specific granules: a fuse that ignites the inflammatory response. Clin Res 1984: 32: 320-328.
37. LEVY O. Antibiotic proteins of polymorphonuclear leukocytes. Eur J Haematol 1996: 56: 263-277.
38. KJELDSEN L, JOHNSEN AH, SENGELØV H, BORREGAARD N. Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J Biol Chem 1993: 268: 10425-10432.
39. KJELDSEN L, BAINTON DF, SENGELØV H, BORREGAARD N. Identification of neutrophil gelatinase-associated lipocalin as a novel matrix protein of specific granules in human neutrophils. Blood 1994: 83: 799-807.
40. KJELDSEN L, BAINTON DF, SENGELØV H, BORREGAARD N. Structural and functional heterogeneity among peroxidase-negative granules in human neutrophils: Identification of a distinct gelatinase containing granule subset by combined immunocytochemistry and subcellular fractionation. Blood 1993: 82: 3183-3191.
41. KJELDSEN L, SENGELØV H, LOLLIKE K, NIELSEN MH, BORREGAARD N. Isolation and characterization of gelatinase granules from human neutrophils. Blood 1994: 83: 1640-1649.
42. SENGELØV H, KJELDSEN L, BORREGAARD N. Control of exocytosis in early neutrophil activation. J Immunol 1993: 150: 1535-1543.
43. NAUSEEF WM, OLSSON I, ARNLJOTS K. Biosynthesis and processing of myeloperoxidase - a marker for myeloid cell differentiation. Eur J Haematol 1988: 40: 97-110.
44. LUBBERT M, MILLER CW, KOEFFLER HP. Changes of DNA methylation and chromatin structure in the human myeloperoxidase gene during myeloid differentiation. Blood 1991: 78: 345-356.
45. HASHINAKA K, YAMADA M. Undermethylation and DNase I hypersensitivity of myeloperoxidase gene in HL-60 cells before and after differentiation. Arch Biochem Biophys 1992: 293: 40-45.
46. SUZOW J, FRIEDMAN AD. The murine myeloperoxidase promoter contains several functional elements, one of which binds a cell type-restricted transcription factor, myeloid nuclear factor 1 (MyNF1). Mol Cell Biol 1993: 13: 2141-2151.
47. NUCHPRAYOON I, MEYERS S, SCOTT LM, et al. PEBP2/CBF, the murine homolog of the human myeloid AML1 and PEBP2 beta/CBF beta proto-oncoproteins, regulates the murine myeloperoxidase and neutrophil elastase genes in immature myeloid cells. Mol Cell Biol 1994: 14: 5558-5568.
48. YAMADA M. Myeloperoxidase precursors in human myeloid leukemia HL-60 cells. J Biol Chem 1982: 257: 5980-5982.
49. YAMADA M, KURAHASHI K. Regulation of myeloperoxidase gene expression during differentiation of human myeloid leukemia HL-60 cells. J Biol Chem 1984: 259: 3021-3025.
50. OLSSON I, PERSSON A-M, STRÖMBERG K. Biosynthesis, transport and processing of myeloperoxidase in the human leukaemic promyelocytic cell line HL-60 and normal marrow cells. Biochem J 1984: 223: 911-920.
51. HASILIK A, POHLMANN R, OLSEN RL, VON FIGURA K. Myeloperoxidase is synthesized as larger phosphorylated precursor. EMBO J 1984: 3:2671-2676.
52. KOEFFLER HP, RANYARD J, PERTCHECK M. Myeloperoxidase: its structure and expression during myeloid differentiation. Blood 1985: 65: 484-491.
53. STRÖMBERG K, PERSSON A-M, OLSSON I. The processing and intracellular transport of myeloperoxidase. Modulation by lysosomotropic agents and monensin. Eur J Cell Biol 1985: 39: 424-431.
54. NAUSEEF WM. Myeloperoxidase biosynthesis by a human promyelocytic leukemia cell line: insight into myeloperoxidase deficiency. Blood 1986: 67: 865-872.
55. NAUSEEF WM. Posttranslational processing of a human myeloid lysosomal protein, myeloperoxidase. Blood 1987: 70: 1143-1150.
56. CHANG KS, TRUJILLO JM, COOK RG, STASS SA. Human myeloperoxidase gene: molecular cloning and expression in leukemic cells. Blood 1986: 68: 1411-1414.
57. JOHNSON KR, NAUSEEF WM, CARE A, et al. Characterization of cDNA clones for clones for human myeloperoxidase: predicted amino acid sequence and evidence for multiple mRNA species. Nucleic Acids Res 1987: 15: 2013-2028.
58. MORISHITA K, KUBOTA N, ASANO S, KAZIRO Y, NAGATA S. Molecular cloning and characterization of cDNA for human myeloperoxidase. J Biol Chem 1987: 262: 3844-3851.
59. WEIL SC, ROSNER GL, REID MS, et al. cDNA cloning of human myeloperoxidase: decrease in myeloperoxidase mRNA upon induction of HL-60 cells. Proc Natl Acad Sci 1987: 84: 2057-2061.
60. YAMADA M, HUR SJ, HASHINAKA K, et al. Isolation and characterization of a cDNA coding for human myeloperoxidase. Arch Biochem Biophys 1987: 255: 147-155.
61. HASHINAKA K, NISHIO C, HUR S-J, SAKIYAMA F, TSUNASAWA S, YAMADA M. Multiple species of myeloperoxidase messenger RNAs produced by alternative splicing and differential polyadenylation. Biochemistry 1988: 27: 5906-5914.
62. IKEDA-SAITO M, ARGADE PV, ROUSSEAU DL. Resonance Raman evidence of chloride binding to the heme iron in myeloperoxidase. FEBS Lett 1985: 184: 52-55.
63. ARNLJOTS K, OLSSON I. Myeloperoxidase precursors incorporate heme. J Biol Chem 1987: 262: 10430-10434.
64. NAUSEEF WM, MCCORMICK S, YI H. Roles of heme insertion and the mannose-6-phosphate receptor in processing of the human myeloid lysosomal enzyme, myeloperoxidase. Blood 1992: 80: 2622-2633.
65. NAUSEEF WM, MCCORMICK SJ, CLARK RA. Calreticulin functions as a molecular chaperone in the biosynthesis of myeloperoxidase. J Biol Chem 1995: 270: 4741-4747.
66. AKIN DT, KINKADE JR JM. Processing of a newly identificed intermediate of human myeloperoxidase in isolated granules occurs at neutral pH. J Biol Chem 1986: 261: 8370-8375.
67. ANDREWS PC, KRINSKY NI. The reductive cleavage of myeloperoxidase in half, producing enzymatically active hemi-myeloperoxidase. J Biol Chem 1981: 256: 4211-4218.
68. HARRISON JE, PABALAN S, SCHULTZ J. The subunit structure of crystalline canine myeloperoxidase. Biochem Biophys Acta 1977: 493: 247-259.
69. HASILIK A. The early and late processing of lysosomal enzymes: proteolysis and compartmentation. Experientia 1992: 48: 130-151.
70. GABAY JE, ALMEIDA RP. Antibiotic peptides and serine protease homologs in human polymorphonuclear leukocytes: defensins and azurocidin. Curr Opin Immunol 1993: 5:97-102.
71. ELSBACH P, WEISS J. Oxygen-independent antimicrobial systems of phagocytes. In: GALLIN JI, GOLDSTEIN IM, SNYDERMAN R, eds. Inflammation, basic principles and clinical correlates. New York: Raven Press, 1992: 603-636.
72. FLODGAARD H, ÖSTERGAARD E, BAYNE S, et al. Covalent structure of two novel neutrophil leucocyte-derived proteins of porcine and human origin. Neutrophil elastase homologues with strong monocyte and fibroblast chemotactic activities. Eur J Biochem 1991: 197: 535-547.
73. MORGAN JG, SUKIENNICKI T, PEREIRA HA, SPITZNAGEL JK, GUERRA ME, LARRICK JW. Cloning of the cDNA for the serine protease homolog CAP37/azurocidin, a microbicidal and chemotactic protein from human granulocytes. J Immunol 1991: 147: 3210-3214.
74. SMYTH MJ, TRAPANI JA. Granzymes: exogenous proteinases that induce target cell apoptosis. Immunol Today 1995: 16: 202-206.
75. GALLI SJ, HAMMEL I. Mast cell and basophil development. Curr Opin Hematol 1994: 1:33-39.
76. ZIMMER M, MEDCALF RL, FINK TM, MATTMANN C, LICHTER P, JENNE DE. Three human elastase-like genes coordinately expressed in the myelomonocyte lineage are organized as a single genetic locus on 19pter. Proc Natl Acad Sci USA 1992: 89: 8215-8219.
77. HANSON RD, HOHN PA, POPESCU NC, LEY TJ. A cluster of hematopoietic serine protease genes is found on the same chromosomal band as the human alpha/delta T-cell receptor locus. Proc Natl Acad Sci USA 1990: 87: 960-963.
78. HEUSEL JW, HANSON RD, SILVERMAN GA, LEY TJ. Structure and expression of a cluster of human hematopoietic serine protease genes found on chromosome 14q11.2. J Biol Chem 1991: 266: 6152-6158.
79. HAN J, UNLAP T, RADO TA. Expression of the human neutrophil elastase gene: positive and negative transcriptional elements in the 5′ flanking region. Biochem Biophys Res Commun 1991: 181: 1462-1468.
80. GRISOLANO JL, SCLAR GM, LEY TJ. Early myeloid cell-specific expression of the human cathepsin G gene in transgenic mice. Proc Natl Acad Sci USA 1994: 91: 8989-8993.
81. STURROCK AB, FRANKLIN KF, RAO G, et al. Structure, chromosomal assignment, and expression of the gene for proteinase-3. The Wegener's granulomatosis autoantigen. J Biol Chem 1992: 267: 21193-21199.
82. GARWICZ D, LINDMARK A, HELLMARK T, GLADH M, JÖGI J, GULLBERG U. Characterization of the processing and granular targeting of human proteinase 3 after transfection to the rat RBL or the murine 32D leukemic cell lines. J Leukocyte Biol, 1997: 61: 113-123.
83. SALVESEN G, ENGHILD JJ. An unusual specificity in the activation of neutrophil serine proteinase zymogens. Biochemistry 1990: 29: 5304-5308.
84. SALVESEN G ENGHILD JJ. Zymogen activation specificity and genomic structures of human neutrophil elastase and cathepsin G reveal a new branch of the chymotrypsinogen superfamily of serine proteinases. Biomed Biochim Acta 1991: 50: 665-671.
85. LINDMARK A, PERSSON A-M, OLSSON I. Biosynthesis and processing of cathepsin G and neutrophil elastase in the leukemic myeloid cell line U-937. Blood 1990: 76: 2374-2380.
86. LINDMARK A, GULLBERG U, OLSSON I. Processing and intracellular transport of cathepsin G and neutrophil elastase in the leukemic myeloid cell line U-937-modulation by brefeldin A, ammonium chloride, and monensin. J Leukocyte Biol 1994: 55: 50-57.
87. MCGUIRE MJ, LIPSKY PE, THIELE DL. Generation of active myeloid and lymphoid granule serine proteases requires processing by the granule thiol protease dipeptidyl peptidase I. J Biol Chem 1993: 268: 2458-2467.
88. RAO NV, RAO GV, MARSHALL BC, HOIDAL JR. Biosynthesis and processing of proteinase 3 in U937 cells. Processing pathwys are distinct from those of cathepsin G. J Biol Chem 1996: 271: 2972-2978.
89. MURAKAMI M, KARNIK SS, HUSAIN A. Human prochymase activation. A novel role for heparin in zymogen processing. J Biol Chem 1995: 270: 2218-23.
90. SELDIN DC, ADELMAN S, AUSTEN KF, et al. Homology of the rat basophilic leukemia cell and the rat mucosal mast cell. Proc Natl Acad Sci USA 1985: 82: 3871-3875.
91. GULLBERG U, LINDMARK A, NILSSON E, PERSSON A-M, OLSSON I. Processing of human cathepsin G after transfection to the rat basophilic/mast cell tumor line RBL. J Biol Chem 1994: 269: 25219-25225.
92. GULLBERG U, LINDMARK A, LINDGREN G, PERSSON A-M, NILSSON E, OLSSON I. Carboxyl-terminal prodomain-deleted human leukocyte elastase and cathepsin G are efficiently targeted to granules and enzymatically activated in the rat basophilic/mast cell line RBL. J Biol Chem 1995: 270: 12912-12918.
93. GARWICZ D, LINDMARK A, GULLBERG U. Human cathepsin G lacking functional glycosylation site is proteolytically processed and targeted for storage in granules after transfection to the rat basophilic/mast cell line RBL or the murine myeloid cell line 32D. J Biol Chem 1995: 270: 28413-28418.
94. 2: a Janus-faced proteinase with two opposite specifities. EMBO J 1996: 15: 5481-5491.
95. FUJINAGA M, CHERNAIA MM, HALENBECK R, KOTHS K, JAMES MNG. The crystal structure of PR3, a neutrophil serine proteinase antigen of Wegener's granulomatosis antibodies. J Mol Biol 1996: 261: 267-278.
96. GANZ T, LEHRER RI. Defensins. Curr Opin Immunol 1994: 6:584-589.
97. VALORE EV, GANZ T. Posttranslational processing of defensins in immature human myeloid cells. Blood 1992: 79: 1538-1544.
98. GANZ T, LIU L, VALORE EV, OREN A. Posttranslational processing and targeting of transgenic human defensin in murine granulocyte, macrophage, fibroblast, and pituitary adenoma cell lines. Blood 1993: 82: 641-650.
99. LIU L, GANZ T. The pro region of human neutrophil defensin contains a motif that is essential for normal subcellular sorting. Blood 1995: 85: 1095-1103.
100. RADO TA, BOLLEKENS J, LAURENT GST, PARKER L, BENZ JR EJ. Lactoferrin biosynthesis during granulopoiesis. Blood 1984: 64: 1103-1109.
101. OLSSON I, LANTZ M, PERSSON A-M, ARNLJOTS K. Biosynthesis and processing of lactoferrin in bone marrow cells, a comparison with processing of myeloperoxidase. Blood 1988: 71: 441-447.
102. GRAUBERT T, JOHNSTON J, BERLINER N. Cloning and expression of the cDNA encoding mouse neutrophil gelatinase: demonstration of coordinate secondary granule protein gene expression during terminal neutrophil maturation. Blood 1993: 82: 3192-3197.
103. BORREGAARD N, SEHESTED M, NIELSEN BS, SENGELØV H, KJELDSEN L. Biosynthesis of granule proteins in normal human bone marrow cells. Gelatinase is a marker of terminal myeloid maturation. Blood 1995: 85: 812-818.
104. KORNFELD S, MELLMAN I. The biogenesis of lysosomes. Ann Rev Cell Biol 1989: 5: 483-525.
105. VON FIGURA K, HASILIK A. Lysosomal enzymes and their receptors. Ann Rev Biochem 1986: 55: 167-193.
106. NEUFELD EF, LIM TW, SHAPIRA LJ. Inherited disorders of lysosomal metabolism. Ann Rev Biochem 1975: 44: 357-376.
107. AERTS JMFG, SCHRAM AW, STRIJLAND A, et al. Glucocerebrosidase, a lysosomal enzyme that does not undergo oligosaccharide phosphorylation. Biochim biophys Acta 1988: 964: 303-308.
108. GOTTSCHALK S, WAHEED A, VON FIGURA K. Targeting of lysosomal acid phosphatase with altered carbohydrate. Biol Chem Hoppe-Seyler 1989: 370: 75-80.
109. KRENTLER C, POHLMANN R, HASILIK A, VON FIGURA K. Lysosomal membrane proteins do not bind to mannose 6-phosphate-specific receptors. Biol Chem Hoppe-Seyler 1986: 367: 141-145.
110. CHIANG HL, TERLECKY SR, PLANT CP, DICE JF. A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 1989: 246: 382-385.
111. ROTHMAN JH, YAMASHIRO CT, KANE PM, STEVENS TH. Protein targeting to the yeast vacuole. Trends Biochem Sci 1989: 14: 347-350.
112. VALLS LA, WINTHER JR, STEVENS TH. Yeast carboxy-peptidase Y vacuolar targeting signal is defined by four propeptide amino acids. J Cell Biol 1990: 111: 361-368.
113. FITTSCHEN C, HENSON PM. Linkage of azurophil granule secretion in neutrophils to chloride ion transport and endosomal transcytosis. J Clin Invest 1994: 93: 247-255.
114. BERGER M, WETZLER, E, AUGUST JT, TARTAKOFF AM. Internalization of type 1 complement receptors and de novo multivesicular body formation during chemoattractant-induced endocytosis in human neutrophils. J Clin Invest 1994: 94: 1113-1125.
115. DAHLGREN C, CARLSSON SR, KARLSSON A, LUNDQVIST H, SJOLIN C. The lysosomal membrane glycoproteins Lamp-1 and Lamp-2 are present in mobilizable organelles, but are absent from the azurophil granules of human neutrophils. Biochem J 1995: 311: 667-674.
116. LE-CABEC V, COWLAND JB, CALAFAT J, BORREGAARD N. Targeting of proteins to granule subsets is determined by timing and not by sorting: the specific granule protein NGAL is localized to azurophil granules when expressed in HL-60 cells. Proc Natl Acad Sci USA 1996: 93: 6454-6457.
117. BAUERFEIND R, HUTTNER WB. Biogenesis of constitutive secretory vesicles, secretory granules and synaptic vesicles. Curr Opin Cell Biol 1993: 5:628-635.
118. CHANAT E, HUTTNER WB. Mileu-induced, selective aggregation of regulated secretory proteins in the trans-Golgi network. J Cell Biol 1991: 115: 1505-1519.
119. CHANAT E, WEIß U, HUTTNER WB, TOOZE SA. Reduction of the disulfide bond of chromogranin B (secretogranin I) in the trans-Golgi network causes its missorting to the constitutive secretory pathway. EMBO J 1993: 12: 2159-2168.
120. KOLSET SO, GALLAGHER JT. Proteoglycans in hematopoietic cells. Biochem Biophys Acta 1990: 1032: 191-211.
121. OLSSON I. The intracellular transport of glycosamino-glycans in human leukocytes. Exp Cell Res 1969: 54: 318-325.
122. SCHWARTZ LB, RIEDEL C, CAULFIELD JP, WASSERMAN SI, AUSTEN KF. Cell association of complexes of chymase, heparin proteoglycan, and protein after degranulation by rat mast cells. J Immunol 1981: 126: 2071-2078.
123. SERAFIN WE, KATZ HR, AUSTEN FK, STEVENS RL. Complexes of heparin proteoglycans, chondroitin sulfate E proteoglycans, and (3H)-diisopropyl fluorophosphate-binding proteins are exocytosed from activated mouse bone marrow-derived mast cells. J Biol Chem 1986: 261: 15017-15021.
124. SAYAMA S, IOZZO RV, LAZARUS GS, SCHECHTER NM. Human skin chymotrypsin-like proteinase chymase. Subcellular localization to mast cell granules and interaction with heparin and other glycosaminoglycans. J Biol Chem 1987: 262: 6808-6815.
125. LE TRONG H, NEURATH H, WOODBURY RG. Substrate specificity of the chymotrypsin-like protease in secretory granules isolated from rat mast cells. Proc Natl Acad Sci USA 1987: 84: 364-367.
126. MATSUMOTO R, SALI A, GHILDYAL N, KARPLUS M, STEVENS RL. Packaging of proteases and proteoglycans in the granules of mast cells and other hematopoietic cells. J Biol Chem 1995: 270: 19524-19531.
127. SCHMIDT RE, MACDERMOTT RP, BARTLEY, et al. Specific release of proteoglycans from human natural killer cells during target lysis. Nature 1985: 318: 289-291.
128. PODACK ER. Granule-mediated cytolosis of target cells. In: Current topics in microbiology and immunology v. 140. Berlin, Heidelberg: Springer-Verlag, 1988: 1-9.
129. KAMADA MM, MICHON J, RITZ J, et al. Identification of carboxypeptidase and tryptic esterase activities that are complexed to proteoglycans in the secretory granules of human cloned natural killer cells. J Immunol 1989: 142: 609-615.
130. BURGESS TL, KELLY RB. Sorting and secretion of adrenocorticotropin in a pituitary tumor cell line after perturbation of the level of a secretory granule-specific proteoglycan. J Cell Biol 1984: 99: 2223-2230.
131. MASSON D, PETERS PJ, GEUZE HJ, BORST J, TSCHOPP J. Interaction of chondroitin sulfate with perforin and granzymes of cytolytic T-cells is dependent on pH. Biochemistry 1990: 29: 11229-11235.
132. KULIAWAT R, ARVAN P. Protein targeting via the "constitutive-like" secretory pathway in isolated pancreatic islets: passive sorting in the immature granule compartment. J Cell Biol 1992: 118: 521-529.
133. BAETZ K, ISAAZ S, GRIFFITHS GM. Loss of cytotoxic T-lymphocyte function in Chediak-Higashi syndrome arises from a secretory defect that prevents lytic granule exocytosis. J Immunol 1995: 154: 6122-6131.
134. SCOCCHI M, SKERLAVAJ B, ROMEO D, GENNARO R. Proteolytic cleavage by neutrophil elastase converts inactive storage proforms to antibacterial bactenecins. Eur J Biochem 1992: 209: 589-595.