Polyphosphate is a novel pro-inflammatory regulator of mast cells and is located in acidocalcisomes

Journal of Biological Chemistry

Volumn 287, Issue 34, 2012, Pages 28435-28444

  Moreno Sanchez, David ^a,b   Hernandez Ruiz, Laura ^a,b   Ruiz, Felix A ^a   Docampo, Roberto ^b  

^a HOSPITAL UNIVERSITARIO PUERTA DEL MAR   (Spain)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETOXYMETHYL ESTERS; ACIDOCALCISOMES; CALCIUM INDICATOR; CELL EXTRACTS; ELEMENTAL COMPOSITIONS; ENZYMATIC ASSAY; GEL ELECTROPHORESIS; HIGH DENSITY; MAST CELLS; POLYPHOSPHATES;

COAGULATION; CYTOLOGY; ELECTROPHORESIS; ESCHERICHIA COLI; GRANULATION; UREA;

CELLS;

BRADYKININ; IMMUNOGLOBULIN E; POLYPHOSPHATE;

ACIDOCALCISOME; ALKALINIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTICOAGULATION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CALCIUM CELL LEVEL; CELL ORGANELLE; CELL STIMULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ASSAY; ESCHERICHIA COLI; HUMAN; MAST CELL; MAST CELL DEGRANULATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RAT;

ANIMALS; BASOPHILS; BRADYKININ; CALCIUM; CELL LINE, TUMOR; FEMALE; HUMANS; INFLAMMATION MEDIATORS; LYSOSOMES; MALE; MAST CELLS; POLYPHOSPHATES; RATS; SEROTONIN;

EID: 84865240181     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.385823     Document Type: Article

References (50)

1. Morrissey, J. H., Choi, S. H., and Smith, S. A. (2012) Polyphosphate: an ancient molecule that links platelets, coagulation and inflammation. Blood 119, 5972-5979
2. Rao, N. N., Gómez-García, M. R., and Kornberg, A. (2009) Inorganic polyphosphate: essential for growth and survival. Annu. Rev. Biochem. 78, 605-647
3. Docampo, R., and Moreno, S. N. (2011) Acidocalcisomes. Cell Calcium 50, 113-119
4. Ruiz, F. A., Lea, C. R., Oldfield, E., and Docampo, R. (2004) Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes. J. Biol. Chem. 279, 44250-44257 (Pubitemid 39430828)
5. Müller, F., Mutch, N. J., Schenk, W. A., Smith, S. A., Esterl, L., Spronk, H. M., Schmidbauer, S., Gahl, W. A., Morrissey, J. H., and Renné, T. (2009) Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 139, 1143-1156
6. Smith, S. A., Mutch, N. J., Baskar, D., Rohloff, P., Docampo, R., and Morrissey, J.H.(2006)Polyphosphate modulates blood coagulation and fibrinolysis. Proc. Natl. Acad. Sci. U.S.A. 103, 903-908 (Pubitemid 43212194)
7. Smith, S. A., Choi, S. H., Davis-Harrison, R., Huyck, J., Boettcher, J., Rienstra, C. M., and Morrissey, J. H. (2010) Polyphosphate exerts differential effects on blood clotting, depending on polymer size. Blood 116, 4353-4359
8. Smith, S. A., and Morrissey, J. H. (2008) Polyphosphate enhances fibrin clot structure. Blood 112, 2810-2816
9. Mutch, N. J., Engel, R., Uitte de Willige, S., Philippou, H., and Ariëns, R. A. (2010) Polyphosphate modifies the fibrin network and down-regulates fibrinolysis by attenuating binding of tPA and plasminogen to fibrin. Blood 115, 3980-3988
10. Renné, T. (2012) The procoagulant and proinflammatory plasma contact system. Semin. Immunopathol. 34, 31-41
11. Huang, G., Fang, J., Sant'Anna, C., Li, Z. H., Wellems, D. L., Rohloff, P., and Docampo, R. (2011) Adaptor protein-3 (AP-3) complex mediates the biogenesis of acidocalcisomes and is essential for growth and virulence of Trypanosoma brucei. J. Biol. Chem. 286, 36619-36630
12. Cutler, D. F. (2002) Introduction: lysosome-related organelles. Semin. Cell Dev. Biol. 13, 261-262
13. Patel, S., and Docampo, R. (2010) Acidic calcium stores open for business: expanding the potential for intracellular Ca2+ signaling. Trends Cell Biol. 20, 277-286
14. Kendall, M. D., and Warley, A. (1986) Elemental content of mast cell granules measured by x-ray microanalysis of rat thymic tissue sections. J. Cell Sci. 83, 77-87 (Pubitemid 16100650)
15. Raison, S., Gillot, I., Choine, C., Pistone, P., Pagnotta, S., Laugier, J. P., and Nicaise, G. (1999) Ca increase in secretory granules of stimulated mast cells. Cell Calcium 26, 111-119 (Pubitemid 29516426)
16. Chodaczek, G., Bacsi, A., Dharajiya, N., Sur, S., Hazra, T. K., and Boldogh, I. (2009) Ragweed pollen-mediated IgE-independent release of biogenic amines from mast cells via induction of mitochondrial dysfunction. Mol. Immunol. 46, 2505-2514
17. Chakravarty, N., and Nielsen, E. H. (1980) Ca2+-Mg2+-activated adenosine triphosphatase in plasma and granule membranes in nonsecreting and secreting mast cells. Exp. Cell Res. 130, 175-184
18. Prussin, C., and Metcalfe, D. D. (2003) IgE, mast cells, basophils, and eosinophils. J. Allergy Clin. Immunol. 111, S486-494 (Pubitemid 36223287)
19. Abraham, S. N., and St John, A. L. (2010) Mast cell-orchestrated immunity to pathogens. Nat. Rev. Immunol. 10, 440-452
20. Meininger, C. J., and Zetter, B. R. (1992) Mast cells and angiogenesis. Semin. Cancer Biol. 3, 73-79
21. Kovanen, P. T. (2009) Mast cells in atherogenesis: actions and reactions. Curr. Atheroscler. Rep. 11, 214-219
22. Puri, N., and Roche, P. A. (2008) Mast cells possess distinct secretory granule subsets whose exocytosis is regulated by different SNARE isoforms. Proc. Natl. Acad. Sci. U.S.A. 105, 2580-2585 (Pubitemid 351520556)
23. Kanerva, K., Lappalainen, J., Mäkitie, L. T., Virolainen, S., Kovanen, P. T., and Andersson, L. C. (2009) Expression of antizyme inhibitor 2 in mast cells and role of polyamines as selective regulators of serotonin secretion. PLoS One 4, e6858
24. Muller, A. D., Lichtenbeld, H. H., Blijham, G. H., Vossen, R. C., and van Dam-Mieras, M. C. (1993) Mast cell lysate induces a procoagulant effect on endothelial cells. Thromb. Res. 72, 263-267 (Pubitemid 23309845)
25. Cugno, M., Marzano, A. V., Asero, R., and Tedeschi, A. (2010) Activation of blood coagulation in chronic urticaria: pathophysiological and clinical implications. Intern. Emerg. Med. 5, 97-101
26. Oschatz, C., Maas, C., Lecher, B., Jansen, T., Björkqvist, J., Tradler, T., Sedlmeier, R., Burfeind, P., Cichon, S., Hammerschmidt, S., Müller-Esterl, W., Wuillemin, W. A., Nilsson, G., and Renné, T. (2011) Mast cells increase vascular permeability by heparin-initiated bradykinin formation in vivo. Immunity 34, 258-268
27. Jimenez-Nunez, M. D., Moreno-Sanchez, D., Hernandez-Ruiz, L., Beni-tez- Rondan, A., Ramos-Amaya, A., Rodriguez-Bayona, B., Medina, F., Brieva, J. A., and Ruiz, F. A. (2012) Myeloma cells contain high inorganic polyphosphate levels that are associated with nucleolar transcription. Haematologica, in press
28. Saito, K., Ohtomo, R., Kuga-Uetake, Y., Aono, T., and Saito, M. (2005) Direct labeling of polyphosphate at the ultrastructural level in Saccharomyces cerevisiae by using the affinity of the polyphosphate binding domain of Escherichia coli exopolyphosphatase. Appl. Environ. Microbiol. 71, 5692-5701 (Pubitemid 41456857)
29. Medina, F., Segundo, C., Campos-Caro, A., González-García, I., and Brieva, J. A. (2002) The heterogeneity shown by human plasma cells from tonsil, blood, and bone marrow reveals graded stages of increasing maturity, but local profiles of adhesion molecule expression. Blood 99, 2154-2161 (Pubitemid 34525501)
30. Kumble, K. D., and Kornberg, A. (1995) Inorganic polyphosphate in mammalian cells and tissues. J. Biol. Chem. 270, 5818-5822
31. Ruiz, F. A., Rodrigues, C. O., and Docampo, R. (2001) Rapid changes in polyphosphate content within acidocalcisomes in response to cell growth, differentiation, and environmental stress in Trypanosoma cruzi. J. Biol. Chem. 276, 26114-26121
32. Smith, S. A., and Morrissey, J. H. (2007) Sensitive fluorescence detection of polyphosphate in polyacrylamide gels using 4',6-diamidino-2- phenylindol. Electrophoresis 28, 3461-3465 (Pubitemid 47604706)
33. Mizuno, K., Tolmachova, T., Ushakov, D. S., Romao, M., Abrink, M., Ferenczi, M. A., Raposo, G., and Seabra, M. C. (2007) Rab27b regulates mast cell granule dynamics and secretion. Traffic 8, 883-892 (Pubitemid 46971634)
34. Lindstedt, K. A., and Kovanen, P. T. (2006) Isolation of mast cell granules. Curr. Protoc. Cell Biol. Chapter 3, Unit 3.16
35. Docampo, R., Scott, D. A., Vercesi, A. E., and Moreno, S. N. (1995) Intracellular Ca2+ storage in acidocalcisomes of Trypanosoma cruzi. Biochem. J. 310, 1005-1012
36. Allan, R. A., and Miller, J. J. (1980) Influence of S-adenosylmethionine on DAPI-induced fluorescence of polyphosphate in the yeast vacuole. Can. J. Microbiol. 26, 912-920 (Pubitemid 11227091)
37. Nakano, N., Nakao, A., Uchida, T., Shirasaka, N., Yoshizumi, H., Okumura, K., Tsuboi, R., and Ogawa, H. (2005) Effects of arachidonic acid analogs on FcεRI-mediated activation of mast cells. Biochim. Biophys. Acta 1738, 19-28 (Pubitemid 43122127)
38. Teshima, R., Amano, F., Nakamura, R., Tanaka, Y., and Sawada, J. (2007) Effects of polyunsaturated fatty acids on calcium response and degranulation from RBL-2H3 cells. Int. Immunopharmacol. 7, 205-210 (Pubitemid 46037560)
39. Haller, T., Dietl, P., Deetjen, P., and Völkl, H. (1996) The lysosomal compartment as intracellular calcium store in MDCK cells: a possible involvement in InsP3-mediated Ca2+ release. Cell Calcium 19, 157-165
40. Lloyd-Evans, E., Morgan, A. J., He, X., Smith, D. A., Elliot-Smith, E., Sillence, D. J., Churchill, G. C., Schuchman, E. H., Galione, A., and Platt, F. M. (2008) Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 14, 1247-1255
41. Thastrup, O., Cullen, P. J., Drøbak, B. K., Hanley, M. R., and Dawson, A. P. (1990) Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2+-ATPase. Proc. Natl. Acad. Sci. U.S.A. 87, 2466-2470
42. Babes, V. (1895) Beoachtungen uber die methachromatischen Korperchen, Sporenbilidung, Verzweigung, Kolben- und Kapselbildung Pathogener Bakterien. Z. Hug. Infektionskr. 20, 412-420
43. Meyer, A. (1904) Orientirende Untersuchungen uber Verbreitung, Morphologie und chemie des volutins. Botansiche Zeitung 7, 113-152
44. Wiame, J. M. (1947) Etude d'une substance polyphosphoree, basophile et metachomatique chez les levures. Biochim. Biophys. Acta 1, 234-255
45. Seufferheld, M., Vieira, M. C., Ruiz, F. A., Rodrigues, C. O., Moreno, S. N., and Docampo, R. (2003) Identification of organelles in bacteria similar to acidocalcisomes of unicellular eukaryotes. J. Biol. Chem. 278, 29971-29978 (Pubitemid 36962386)
46. Foster, M. C., Leapman, R. D., Li, M. X., and Atwater, I. (1993) Elemental composition of secretory granules in pancreatic islets of Langerhans. Biophys. J. 64, 525-532 (Pubitemid 23093865)
47. Somlyo, A. V., Broderick, R., Shuman, H., Buhle, E. L., Jr., and Somlyo, A. P. (1988) Atrial-specific granules in situ have high calcium content, are acidic, and maintain anion gradients. Proc. Natl. Acad. Sci. U.S.A. 85, 6222-6226
48. Ornberg, R. L., Kuijpers, G. A., and Leapman, R. D. (1988) Electron probe microanalysis of the subcellular compartments of bovine adrenal chromaffin cells: comparison of chromaffin granules in situ and in vitro. J. Biol. Chem. 263, 1488-1493 (Pubitemid 18039957)
49. Ramos, I. B., Miranda, K., Pace, D. A., Verbist, K. C., Lin, F. Y., Zhang, Y., Oldfield, E., Machado, E. A., De Souza, W., and Docampo, R. (2010) Calcium- and polyphosphate-containing acidic granules of sea urchin eggs are similar to acidocalcisomes, but are not the targets for NAADP. Biochem. J. 429, 485-495
50. Ramos, I., Gomes, F., Koeller, C. M., Saito, K., Heise, N., Masuda, H., Docampo, R., de Souza, W., Machado, E. A., and Miranda, K. (2011) Acidocalcisomes as calcium- and polyphosphate-storage compartments during embryogenesis of the insect Rhodnius prolixus Stahl. PLoS One 6, e27276