An essential role for Rab27a GTPase in eosinophil exocytosis

Journal of Leukocyte Biology

Volumn 94, Issue 6, 2013, Pages 1265-1274

  Kim, John Dongil ^a   Willetts, Lian ^a   Ochkur, Sergei ^b   Srivastava, Nutan ^a   Hamburg, Rudolf ^a   Shayeganpour, Anooshirvan ^a   Seabra, Miguel C ^c   Lee, James J ^b   Moqbel, Redwan ^d   Lacy, Paige ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b MAYO GRADUATE SCHOOL   (United States)

^c NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^d UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Allergic asthma; Ashen mice; Degranulation; hE2 transgenic mice; IL 5 transgenic mice; Subcellular fractionation

Indexed keywords

CD63 ANTIGEN; RAB27A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; DEGRANULATION; EOSINOPHIL; EXOCYTOSIS; IMMUNOFLUORESCENCE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; WESTERN BLOTTING;

ALLERGIC ASTHMA; ASHEN MICE; DEGRANULATION; HE2 TRANSGENIC MICE; IL-5 TRANSGENIC MICE; SUBCELLULAR FRACTIONATION;

ANIMALS; ANTIGENS, CD63; ASTHMA; CELL DEGRANULATION; DISEASE MODELS, ANIMAL; EOSINOPHILS; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HL-60 CELLS; HUMANS; MALE; MICE; MICE, KNOCKOUT; RAB GTP-BINDING PROTEINS;

EID: 84888802805     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0812431     Document Type: Article

References (57)

1. Lacy, P., Moqbel, R. (2001) Immune effector functions of eosinophils in allergic airway inflammation. Curr. Opin. Allergy Clin. Immunol. 1, 79-84.
2. Adamko, D., Lacy, P., Moqbel, R. (2004) Eosinophil function in allergic inflammation: from bone marrow to tissue response. Curr. Allergy Asthma Rep. 4, 149-158.
3. Rothenberg, M. E., Hogan, S. P. (2006) The eosinophil. Annu. Rev. Immunol. 24, 147-174.
4. Hogan, S. P., Rosenberg, H. F., Moqbel, R., Phipps, S., Foster, P. S., Lacy, P., Kay, A. B., Rothenberg, M. E. (2008) Eosinophils: biological properties and role in health and disease. Clin. Exp. Allergy 38, 709-750.
5. Jacobsen, E. A., Taranova, A. G., Lee, N. A., Lee, J. J. (2007) Eosinophils: singularly destructive effector cells or purveyors of immunoregulation? J. Allergy Clin. Immunol.
6. Leckie, M. J., ten Brinke, A., Khan, J., Diamant, Z., O'Connor, B. J., Walls, C. M., Mathur, A. K., Cowley, H. C., Chung, K. F., Djukanovic, R., Hansel, T. T., Holgate, S. T., Sterk, P. J., Barnes, P. J. (2000) Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyper-responsiveness, and the late asthmatic response. Lancet 356, 2144-2148.
7. Flood-Page, P. T., Menzies-Gow, A. N., Kay, A. B., Robinson, D. S. (2003) Eosinophil's role remains uncertain as anti-interleukin-5 only partially depletes numbers in asthmatic airway. Am. J. Respir. Crit. Care Med. 167, 199-204.
8. Kips, J. C., O'Connor, B. J., Langley, S. J., Woodcock, A., Kerstjens, H. A., Postma, D. S., Danzig, M., Cuss, F., Pauwels, R. A. (2003) Effect of SCH55700, a humanized anti-human interleukin-5 antibody, in severe persistent asthma: a pilot study. Am. J. Respir. Crit. Care Med. 167, 1655-1659.
9. Nair, P., Pizzichini, M. M., Kjarsgaard, M., Inman, M. D., Efthimiadis, A., Pizzichini, E., Hargreave, F. E., O'Byrne, P. M. (2009) Mepolizumab for prednisone-dependent asthma with sputum eosinophilia. N. Engl. J. Med. 360, 985-993.
10. Haldar, P., Brightling, C. E., Hargadon, B., Gupta, S., Monteiro, W., Sousa, A., Marshall, R. P., Bradding, P., Green, R. H., Wardlaw, A. J., Pavord, I. D. (2009) Mepolizumab and exacerbations of refractory eosinophilic asthma. N. Engl. J. Med. 360, 973-984.
11. Lee, J. J., Dimina, D., Macias, M. P., Ochkur, S. I., McGarry, M. P., O'Neill, K. R., Protheroe, C., Pero, R., Nguyen, T., Cormier, S. A., Lenkiewicz, E., Colbert, D., Rinaldi, L., Ackerman, S. J., Irvin, C. G., Lee, N. A. (2004) Defining a link with asthma in mice congenitally deficient in eosinophils. Science 305, 1773-1776.
12. Humbles, A. A., Lloyd, C. M., McMillan, S. J., Friend, D. S., Xanthou, G., McKenna, E. E., Ghiran, S., Gerard, N. P., Yu, C., Orkin, S. H., Gerard, C. (2004) A critical role for eosinophils in allergic airways remodeling. Science 305, 1776-1779.
13. Coughlin, J. J., Odemuyiwa, S. O., Davidson, C. E., Moqbel, R. (2008) Differential expression and activation of Rab27A in human eosinophils: relationship to blood eosinophilia. Biochem. Biophys. Res. Commun. 373, 382-386.
14. Seabra, M. C., Mules, E. H., Hume, A. N. (2002) Rab GTPases, intracellular traffic and disease. Trends. Mol. Med. 8, 23-30.
15. Seabra, M. C., Coudrier, E. (2004) Rab GTPases and myosin motors in organelle motility. Traffic 5, 393-399.
16. Wood, S. M., Meeths, M., Chiang, S. C., Bechensteen, A. G., Boelens, J. J., Heilmann, C., Horiuchi, H., Rosthoj, S., Rutynowska, O., Winiarski, J., Stow, J. L., Nordenskjold, M., Henter, J. I., Ljunggren, H. G., Bryceson, Y. T. (2009) Different NK cell-activating receptors preferentially recruit Rab27a or Munc13-4 to perforin-containing granules for cytotoxicity. Blood 114, 4117-4127.
17. Arico, M., Zecca, M., Santoro, N., Caselli, D., Maccario, R., Danesino, C., de Saint Basile, G., Locatelli, F. (2002) Successful treatment of Griscelli syndrome with unrelated donor allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant. 29, 995-998.
18. Wilson, S. M., Yip, R., Swing, D. A., O'Sullivan, T. N., Zhang, Y., Novak, E. K., Swank, R. T., Russell, L. B., Copeland, N. G., Jenkins, N. A. (2000) A mutation in Rab27a causes the vesicle transport defects observed in ashen mice. Proc. Natl. Acad. Sci. U. S. A. 97, 7933-7938.
19. Barral, D. C., Ramalho, J. S., Anders, R., Hume, A. N., Knapton, H. J., Tolmachova, T., Collinson, L. M., Goulding, D., Authi, K. S., Seabra, M. C. (2002) Functional redundancy of Rab27 proteins and the pathogenesis of Griscelli syndrome. J. Clin. Invest. 110, 247-257.
20. Haddad, E. K., Wu, X., Hammer, J. A., 3rd, Henkart, P. A. (2001) Defective granule exocytosis in Rab27a-deficient lymphocytes from Ashen mice. J. Cell Biol. 152, 835-842.
21. Stinchcombe, J. C., Barral, D. C., Mules, E. H., Booth, S., Hume, A. N., Machesky, L. M., Seabra, M. C., Griffiths, G. M. (2001) Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J. Cell Biol. 152, 825-834.
22. Ochkur, S. I., Jacobsen, E. A., Protheroe, C. A., Biechele, T. L., Pero, R. S., McGarry, M. P., Wang, H., O'Neill, K. R., Colbert, D. C., Colby, T. V., Shen, H., Blackburn, M. R., Irvin, C. C., Lee, J. J., Lee, N. A. (2007) Coexpression of IL-5 and eotaxin-2 in mice creates an eosinophil-dependent model of respiratory inflammation with characteristics of severe asthma. J. Immunol. 178, 7879-7889.
23. Lee, N. A., McGarry, M. P., Larson, K. A., Horton, M. A., Kristensen, A. B., Lee, J. J. (1997) Expression of IL-5 in thymocytes/T cells leads to the development of a massive eosinophilia, extramedullary eosinophilopoiesis, and unique histopathologies. J. Immunol. 158, 1332-1344.
24. Garcia-Zepeda, E. A., Rothenberg, M. E., Ownbey, R. T., Celestin, J., Leder, P., Luster, A. D. (1996) Human eotaxin is a specific chemoattractant for eosinophil cells and provides a new mechanism to explain tissue eosinophilia. Nat. Med. 2, 449-456.
25. Denzler, K. L., Borchers, M. T., Crosby, J. R., Cieslewicz, G., Hines, E. M., Justice, J. P., Cormier, S. A., Lindenberger, K. A., Song, W., Wu, W., Hazen, S. L., Gleich, G. J., Lee, J. J., Lee, N. A. (2001) Extensive eosinophil degranulation and peroxidase-mediated oxidation of airway proteins do not occur in a mouse ovalbumin-challenge model of pulmonary inflammation. J. Immunol. 167, 1672-1682.
26. Ishihara, K., Hong, J., Zee, O., Ohuchi, K. (2005) Mechanism of the eosinophilic differentiation of HL-60 clone 15 cells induced by n-butyrate. Int. Arch. Allergy Immunol. 137(Suppl. 1), 77-82.
27. Lacy, P., Abdel-Latif, D., Steward, M., Musat-Marcu, S., Man, S. F., Moqbel, R. (2003) Divergence of mechanisms regulating respiratory burst in blood and sputum eosinophils and neutrophils from atopic subjects. J. Immunol. 170, 2670-2679.
28. Levi-Schaffer, F., Lacy, P., Severs, N. J., Newman, T. M., North, J., Gomperts, B., Kay, A. B., Moqbel, R. (1995) Association of granulocyte-macrophage colony-stimulating factor with the crystalloid granules of human eosinophils. Blood 85, 2579-2586.
29. Lacy, P., Mahmudi-Azer, S., Bablitz, B., Hagen, S. C., Velazquez, J. R., Man, S. F., Moqbel, R. (1999) Rapid mobilization of intracellularly stored RANTES in response to interferonin human eosinophils. Blood 94, 23-32.
30. Rothenberg, M. E., Luster, A. D., Leder, P. (1995) Murine eotaxin: an eosinophil chemoattractant inducible in endothelial cells and in interleukin 4-induced tumor suppression. Proc. Natl. Acad. Sci. U. S. A. 92, 8960-8964.
31. Lacy, P., Willetts, L., Kim, J. D., Lo, A., Lam, B., MacLean, E. I., Moqbel, R., Rothenberg, M. E., Zimmermann, N. (2011) Agonist activation of F-actin-mediated eosinophil shape change and mediator release is dependent on Rac2. Int Arch Allergy Immunol. 156, 137-147.
32. Dyer, K. D., Moser, J. M., Czapiga, M., Siegel, S. J., Percopo, C. M., Rosenberg, H. F. (2008) Functionally competent eosinophils differentiated ex vivo in high purity from normal mouse bone marrow. J. Immunol. 181, 4004-4009.
33. Lacy, P., Levi-Schaffer, F., Mahmudi-Azer, S., Bablitz, B., Hagen, S. C., Velazquez, J., Kay, A. B., Moqbel, R. (1998) Intracellular localization of interleukin-6 in eosinophils from atopic asthmatics and effects of interferon. Blood 91, 2508-2516.
34. Lacy, P., Willetts, L., Kim, J. D., Lo, A. N., Lam, B., Maclean, E. I., Moqbel, R., Rothenberg, M. E., Zimmermann, N. (2011) Agonist activation of f-actin-mediated eosinophil shape change and mediator release is dependent on Rac2. Int. Arch. Allergy Immunol. 156, 137-147.
35. Mahmudi-Azer, S., Lacy, P., Bablitz, B., Moqbel, R. (1998) Inhibition of nonspecific binding of fluorescent-labelled antibodies to human eosinophils. J. Immunol. Methods 217, 113-119.
36. Hume, A. N., Collinson, L. M., Rapak, A., Gomes, A. Q., Hopkins, C. R., Seabra, M. C. (2001) Rab27a regulates the peripheral distribution of melanosomes in melanocytes. J. Cell Biol. 152, 795-808.
37. Ochkur, S. I., Kim, J. D., Protheroe, C. A., Colbert, D., Moqbel, R., Lacy, P., Lee, J. J., Lee, N. A. (2012) The development of a sensitive and specific ELISA for mouse eosinophil peroxidase: assessment of eosinophil degranulation ex vivo and in models of human disease. J. Immunol. Methods 375, 138-147.
38. Dyer, K. D., Percopo, C. M., Xie, Z., Yang, Z., Kim, J. D., Davoine, F., Lacy, P., Druey, K. M., Moqbel, R., Rosenberg, H. F. (2010) Mouse and human eosinophils degranulate in response to platelet-activating factor (PAF) and lysoPAF via a PAF-receptor-independent mechanism: evidence for a novel receptor. J. Immunol. 184, 6327-6334.
39. Mahmudi-Azer, S., Downey, G. P., Moqbel, R. (2002) Translocation of the tetraspanin CD63 in association with human eosinophil mediator release. Blood 99, 4039-4047.
40. Bahadoran, P., Aberdam, E., Mantoux, F., Busca, R., Bille, K., Yalman, N., de Saint-Basile, G., Casaroli-Marano, R., Ortonne, J. P., Ballotti, R. (2001) Rab27a: a key to melanosome transport in human melanocytes. J. Cell Biol. 152, 843-850.
41. Casey, T. M., Meade, J. L., Hewitt, E. W. (2007) Organelle proteomics: identification of the exocytic machinery associated with the natural killer cell secretory lysosome. Mol. Cell. Proteomics
42. Munafo, D. B., Johnson, J. L., Ellis, B. A., Rutschmann, S., Beutler, B., Catz, S. D. (2007) Rab27a is a key component of the secretory machinery of azurophilic granules in granulocytes. Biochem. J. 402, 229-239.
43. Mizuno, K., Tolmachova, T., Ushakov, D. S., Romao, M., Abrink, M., Ferenczi, M. A., Raposo, G., Seabra, M. C. (2007) Rab27b regulates mast cell granule dynamics and secretion. Traffic 8, 883-892.
44. Fukuda, M. (2008) Regulation of secretory vesicle traffic by Rab small GTPases. Cell. Mol. Life Sci. 65, 2801-2813.
45. McAdara Berkowitz, J. K., Catz, S. D., Johnson, J. L., Ruedi, J. M., Thon, V., Babior, B. M. (2001) JFC1, a novel tandem C2 domain-containing protein associated with the leukocyte NADPH oxidase. J. Biol. Chem. 276, 18855-18862.
46. Lacy, P., Logan, M. R., Bablitz, B., Moqbel, R. (2001) Fusion protein vesicle-associated membrane protein 2 is implicated in IFN -induced piecemeal degranulation in human eosinophils from atopic individuals. J. Allergy Clin. Immunol. 107, 671-678.
47. Logan, M. R., Lacy, P., Bablitz, B., Moqbel, R. (2002) Expression of eosinophil target SNAREs as potential cognate receptors for vesicle-associated membrane protein-2 in exocytosis. J. Allergy Clin. Immunol. 109, 299-306.
48. Logan, M. R., Lacy, P., Odemuyiwa, S. O., Steward, M., Davoine, F., Kita, H., Moqbel, R. (2006) A critical role for vesicle-associated membrane protein-7 in exocytosis from human eosinophils and neutrophils. Allergy 61, 777-784.
49. Logan, M. R., Odemuyiwa, S. O., Moqbel, R. (2003) Understanding exocytosis in immune and inflammatory cells: the molecular basis of mediator secretion. J. Allergy Clin. Immunol. 111, 923-932.
50. Shirakawa, R., Higashi, T., Tabuchi, A., Yoshioka, A., Nishioka, H., Fukuda, M., Kita, T., Horiuchi, H. (2004) Munc13-4 is a GTP-Rab27-binding protein regulating dense core granule secretion in platelets. J. Biol. Chem. 279, 10730-10737.
51. Neeft, M., Wieffer, M., de Jong, A. S., Negroiu, G., Metz, C. H., van Loon, A., Griffith, J., Krijgsveld, J., Wulffraat, N., Koch, H., Heck, A. J., Brose, N., Kleijmeer, M., van der Sluijs, P. (2005) Munc13-4 is an effector of rab27a and controls secretion of lysosomes in hematopoietic cells. Mol. Biol. Cell 16, 731-741.
52. Menager, M. M., Menasche, G., Romao, M., Knapnougel, P., Ho, C. H., Garfa, M., Raposo, G., Feldmann, J., Fischer, A., de Saint Basile, G. (2007) Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat. Immunol.
53. Herrero-Turrion, M. J., Calafat, J., Janssen, H., Fukuda, M., Mollinedo, F. (2008) Rab27a regulates exocytosis of tertiary and specific granules in human neutrophils. J. Immunol. 181, 3793-3803.
54. Spencer, L. A., Melo, R. C., Perez, S. A., Bafford, S. P., Dvorak, A. M., Weller, P. F. (2006) Cytokine receptor-mediated trafficking of preformed IL-4 in eosinophils identifies an innate immune mechanism of cytokine secretion. Proc. Natl. Acad. Sci. U. S. A. 103, 3333-3338.
55. Adamko, D. J., Wu, Y., Gleich, G. J., Lacy, P., Moqbel, R. (2004) The induction of eosinophil peroxidase release: improved methods of measurement and stimulation. J. Immunol. Methods 291, 101-108.
56. Erjefalt, J. S., Greiff, L., Andersson, M., Adelroth, E., Jeffery, P. K., Persson, C. G. (2001) Degranulation patterns of eosinophil granulocytes as determinants of eosinophil driven disease. Thorax 56, 341-344.
57. Stelts, D., Egan, R. W., Falcone, A., Garlisi, C. G., Gleich, G. J., Kreutner, W., Kung, T. T., Nahrebne, D. K., Chapman, R. W., Minnicozzi, M. (1998) Eosinophils retain their granule major basic protein in a murine model of allergic pulmonary inflammation. Am. J. Respir. Cell Mol. Biol. 18, 463-470.