Proteome profiling of human neutrophil granule subsets, secretory vesicles, and cell membrane: Correlation with transcriptome profiling of neutrophil precursors

Journal of Leukocyte Biology

Volumn 94, Issue 4, 2013, Pages 711-721

  Rørvig, Sara ^a   Østergaard, Ole ^b   Heegaard, Niels H H ^b   Borregaard, Niels ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b STATENS SERUM INSTITUT   (Denmark)

Author keywords

Azurophil; Ficolin 1; Gelatinase; Mass spectrometry

Indexed keywords

MESSENGER RNA; TRYPSIN;

ARTICLE; CELL FRACTIONATION; CELL MEMBRANE; CENTRIFUGATION; CONTROLLED STUDY; CORRELATIONAL STUDY; DENSITY GRADIENT CENTRIFUGATION; GENE EXPRESSION; HUMAN; HUMAN CELL; MASS SPECTROMETRY; NEUTROPHIL GRANULE; NEUTROPHIL STEM CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEOMICS; SECRETORY VESICLE; STEM CELL; TRANSCRIPTOMICS;

AZUROPHIL; FICOLIN-1; GELATINASE; MASS SPECTROMETRY;

CELL FRACTIONATION; CELL MEMBRANE; CENTRIFUGATION; CLUSTER ANALYSIS; CYTOPLASMIC GRANULES; GENE EXPRESSION PROFILING; HUMANS; NEUTROPHILS; PROTEOME; PROTEOMICS; RNA, MESSENGER; SECRETORY VESICLES; TIME FACTORS;

EID: 84883167789     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1212619     Document Type: Article

References (44)

1. Borregaard, N. (2010) Neutrophils, from marrow to microbes. Immunity 33, 657-670.
2. Borregaard, N., Cowland, J. B. (1997) Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89, 3503-3521.
3. Le Cabec, V., Cowland, J. B., Calafat, J., Borregaard, N. (1996) Targeting of proteins to granule subsets determined by timing not by sorting: the specific granule protein NGAL is localized to azurophil granules when expressed in HL-60 cells. Proc. Natl. Acad. Sci. USA 93, 6454-6457.
4. Borregaard, N., Sehested, M., Nielsen, B. S., Sengeløv, H., Kjeldsen, L. (1995) Biosynthesis of granule proteins in normal human bone marrow cells. Gelatinase is a marker of terminal neutrophil differentiation. Blood 85, 812-817.
5. Sengeløv, H., Kjeldsen, L., Borregaard, N. (1993) Control of exocytosis in early neutrophil activation. J. Immunol. 150, 1535-1543.
6. Sengeløv, H., Follin, P., Kjeldsen, L., Lollike, K., Dahlgren, C., Borregaard, N. (1995) Mobilization of granules and secretory vesicles during in vivo exudation of human neutrophils. J. Immunol. 154, 4157-4165.
7. Brumell, J. H., Volchuk, A., Sengeløv, H., Borregaard, N., Cieutat, A. M., Bainton, D. F., Grinstein, S., Klip, A. (1995) Subcellular distribution of docking/fusion proteins in neutrophils, secretory cells with multiple exocytic compartments. J. Immunol. 155, 5750-5759.
8. Fittschen, C., Henson, P. M. (1994) Linkage of azurophil granule secretion in neutrophils to chloride ion transport and endosomal transcytosis. J. Clin. Invest. 93, 247-255.
9. N'Diaye, E. N., Darzacq, X., Astarie-Dequeker, C., Daffe, M., Calafat, J., Maridonneau-Parini, I. (1998) Fusion of azurophil granules with phagosomes and activation of the tyrosine kinase Hck are specifically inhibited during phagocytosis of mycobacteria by human neutrophils. J. Immunol. 161, 4983-4991.
10. Rorvig, S., Honore, C., Larsson, L. I., Ohlsson, S., Pedersen, C. C., Jacobsen, L. C., Cowland, J. B., Garred, P., Borregaard, N. (2009) Ficolin-1 is present in a highly mobilizable subset of human neutrophil granules and associates with the cell surface after stimulation with fMLP. J. Leukoc. Biol. 86, 1439-1449.
11. Borregaard, N., Kjeldsen, L., Rygaard, K., Bastholm, L., Nielsen, M. H., Sengeløv, H., Bjerrum, O. W., Johnsen, A. H. (1992) Stimulus-dependent secretion of plasma proteins from human neutrophils. J. Clin. Invest. 90, 86-96.
12. Borregaard, N., Miller, L., Springer, T. A. (1987) Chemoattractant-regulated mobilization of a novel intracellular compartment in human neutrophils. Science 237, 1204-1206.
13. 2) in human neutrophils. J. Clin. Invest. 92, 1467-1476.
14. Sengeløv, H., Boulay, F., Kjeldsen, L., Borregaard, N. (1994) Subcellular localization and translocation of the receptor for N-formyl-methionylleucyl-phenylalanine in human neutrophils. Biochem. J. 299, 473-479.
15. Theilgaard-Monch, K., Jacobsen, L. C., Borup, R., Rasmussen, T., Bjerregaard, M. D., Nielsen, F. C., Cowland, J. B., Borregaard, N. (2005) The transcriptional program of terminal granulocytic differentiation. Blood 105, 1785-1796.
16. Udby, L., Borregaard, N. (2007) Subcellular fractionation of human neutrophils and analysis of subcellular markers. In Methods in Molecular Biology Series #412: Neutrophil Methods and Protocols (Quinn, M. T. Deleo, F. R. Bokoch, eds.), G. Humana, Springer-Verlag, New York, NY, USA, 35-56
17. Lominadze, G., Powell, D. W., Luerman, G. C., Link, A. J., Ward, R. A., McLeish, K. R. (2005) Proteomic analysis of human neutrophil granules. Mol. Cell. Proteomics 4, 1503-1521.
18. Uriarte, S. M., Powell, D. W., Luerman, G. C., Merchant, M. L., Cummins, T. D., Jog, N. R., Ward, R. A., McLeish, K. R. (2008) Comparison of proteins expressed on secretory vesicle membranes and plasma membranes of human neutrophils. J. Immunol. 180, 5575-5581.
19. Borregaard, N., Heiple, J. M., Simons, E. R., Clark, R. A. (1983) Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: translocation during activation. J. Cell Biol. 97, 52-61.
20. Bjerregaard, M. D., Jurlander, J., Klausen, P., Borregaard, N., Cowland, J. B. (2003) The in vivo profile of transcription factors during neutrophil differentiation in human bone marrow. Blood 101, 4322-4332.
21. Clemmensen, S. N., Jacobsen, L. C., Rorvig, S., Askaa, B., Christenson, K., Iversen, M., Jorgensen, M. H., Larsen, M. T., van, D. B., Ostergaard, O., et al. (2011) α-1-Antitrypsin is produced by human neutrophil granulocytes and their precursors and liberated during granule exocytosis. Eur. J. Haematol. 86, 517-530.
22. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V., Mann, M. (2006) Ingel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860.
23. Cox, J., Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p. p. b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372.
24. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., Mann, M. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805.
25. Kumar, L., Futschik, M. (2007) Mfuzz: a software package for soft clustering of microarray data. Bioinformation 2, 5-7.
26. Schwammle, V., Jensen, O. N. (2010) A simple and fast method to determine the parameters for fuzzy c-means cluster analysis. Bioinformatics 26, 2841-2848.
27. Zhao, L., Furebring, M., Xu, S., Venge, P. (2004) Subcellular localization and mobilization of carcinoembryonic antigen-related cell adhesion molecule 8 in human neutrophils. Br. J. Haematol. 125, 666-673.
28. Yam, L. T., Janckila, A. J., Li, C. Y., Lam, W. K. (1981) Presence of "prostatic" acid phosphatase in human neutrophils. Invest. Urol. 19, 34-38.
29. Dahlgren, C., Carlsson, S. R., Karlsson, A., Lundqvist, H., Sjölin, C. (1995) 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. 311, 667-674.
30. Cieutat, A. M., Lobel, P., August, J. T., Kjeldsen, L., Sengeløv, H., Borregaard, N., Bainton, D. F. (1998) Azurophilic granules of human neutrophilic leukocytes are deficient in lysosome-associated membrane proteins but retain the mannose 6-phosphate recognition marker. Blood 91, 1044-1058.
31. Plesner, T., Ploug, M., Ellis, V., Ronne, E., Hoyerhansen, G., Wittrup, M., Pedersen, T. L., Tscherning, T., Dano, K., Hansen, N. E. (1994) The receptor for urokinase-type plasminogen activator and urokinase is translocated from two distinct intracellular compartments to the plasma membrane on stimulation of human neutrophils. Blood 83, 808-815.
32. Pedersen, T. L., Yong, K., Pedersen, J. O., Hansen, N. E., Dano, K., Plesner, T. (1996) Impaired migration in vitro of neutrophils from patients with paroxysmal nocturnal haemoglobinuria. Br. J. Haematol. 95, 45-51.
33. Sengeløv, H., Kjeldsen, L., Kroeze, W., Berger, M., Borregaard, N. (1994) Secretory vesicles are the intracellular reservoir of complement receptor 1 in human neutrophils. J. Immunol. 153, 804-810.
34. Dahlgren, C., Karlsson, A., Sendo, F. (2001) Neutrophil secretory vesicles are the intracellular reservoir for GPI-80, a protein with adhesionregulating potential. J. Leukoc. Biol. 69, 57-62.
35. Lee, S. M., Shin, H., Jang, S. W., Shim, J. J., Song, I. S., Son, K. N., Hwang, J., Shin, Y. H., Kim, H. H., Lee, C. K., et al. (2004) PLP2/A4 interacts with CCR1 and stimulates migration of CCR1-expressing HOS cells. Biochem. Biophys. Res. Commun. 324, 768-772.
36. Mollinedo, F., Calafat, J., Janssen, H., Martin-Martin, B., Canchado, J., Nabokina, S. M., Gajate, C. (2006) Combinatorial SNARE complexes modulate the secretion of cytoplasmic granules in human neutrophils. J. Immunol. 177, 2831-2841.
37. Ostermann, G., Weber, K. S., Zernecke, A., Schroder, A., Weber, C. (2002) JAM-1 is a ligand of the β(2) integrin LFA-1 involved in transendothelial migration of leukocytes. Nat. Immunol. 3, 151-158.
38. Muller, W. A., Weigl, S. A., Deng, X., Phillips, D. M. (1993) PECAM-1 is required for transendothelial migration of leukocytes. J. Exp. Med. 178, 449-460.
39. Tomazella, G. G., daSilva, I., Thome, C. H., Greene, L. J., Koehler, C. J., Thiede, B., Wiker, H. G., de Souza, G. A. (2010) Analysis of detergentinsoluble and whole cell lysate fractions of resting neutrophils using high-resolution mass spectrometry. J. Proteome Res. 9, 2030-2036.
40. Luerman, G. C., Powell, D. W., Uriarte, S. M., Cummins, T. D., Merchant, M. L., Ward, R. A., McLeish, K. R. (2011) Identification of phosphoproteins associated with human neutrophil granules following chemotactic peptide stimulation. Mol. Cell. Proteomics 10, M110.
41. Hu, Q., Noll, R. J., Li, H., Makarov, A., Hardman, M., Graham, C. R. (2005) The Orbitrap: a new mass spectrometer. J. Mass. Spectrom. 40, 430-443.
42. Jog, N. R., Rane, M. J., Lominadze, G., Luerman, G. C., Ward, R. A., McLeish, K. R. (2007) The actin cytoskeleton regulates exocytosis of all neutrophil granule subsets. Am. J. Physiol. Cell. Physiol. 292, C1690-C1700.
43. McEver, R. P. (2002) Selectins: lectins that initiate cell adhesion under flow. Curr. Opin. Cell Biol. 14, 581-586.
44. Arnljots, K., Sorensen, O., Lollike, K., Borregaard, N. (1998) Timing targeting and sorting of azurophil granule proteins in human myeloid cells. Leukemia 12, 1789-1795.