New insights into the in situ microscopic visualization and quantification of inorganic polyphosphate stores by 4',6-diamidino-2-phenylindole (DAPI)-staining

European Journal of Histochemistry

Volumn 57, Issue 4, 2013, Pages 228-236

  Gomes, Fabio M ^a   Ramos, I B ^a   Wendt, C ^a   Girard Dias, W ^a   De Souza, W ^a,b   Machado, E A ^a,b   Miranda, Kildare ^a,b  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO NACIONAL DE METROLOGIA   (Brazil)

Author keywords

DAPI; Fluorescence; Fluorimetry; Polyphosphate

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; DIAGNOSTIC AGENT; FLUORESCENT DYE; INDOLE DERIVATIVE; POLYPHOSPHATE;

ANIMAL; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL ORGANELLE; CHEMISTRY; CHICKEN; EIMERIA; FLUORESCENCE; FLUOROMETRY; METHODOLOGY; STAINING; TRYPANOSOMA CRUZI;

ANIMALS; CELL MEMBRANE PERMEABILITY; CHICKENS; EIMERIA; FLUORESCENCE; FLUORESCENT DYES; FLUOROMETRY; INDOLES; ORGANELLES; POLYPHOSPHATES; STAINING AND LABELING; TRYPANOSOMA CRUZI;

EID: 84887149426     PISSN: 1121760X     EISSN: None     Source Type: Journal    
DOI: 10.4081/ejh.2013.e34     Document Type: Article

References (72)

1. Kulaev I, Keuslakovskaya T. Polyphosphate and phosphate pump. Annu Rev Microbiol 2000;54:709-34.
2. Rao NN, Gomez-Garcia MR, Kornberg A. Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem 2009;78:605-47.
3. van der Meijden P, Heemskerk J. Polyphosphates: a link between platelet activation, intrinsic coagulation and inflammation? Expert Rev Hematol 2010;3: 269-72.
4. Muller F, Mutch NJ, Schenk WA, Smith SA, Esterl L, Spronk HM, et al. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 2009;139: 1143-56.
5. Smith SA, Morrissey JH. Polyphosphate enhances fibrin clot structure. Blood 2008;112:2810-6.
6. Smith SA, Mutch NJ, Baskar D, Rohloff P, Docampo R, Morrissey JH. Polyphosphate modulates blood coagulation and fibrinolysis. Proc Natl Acad Sci USA 2006;103:903-8.
7. Wang L, Fraley CD, Faridi J, Kornberg A, Roth RA. Inorganic polyphosphate stimulates mammalian TOR, a kinase involved in the proliferation of mammary cancer cells. Proc Natl Acad Sci USA 2003;100:11249-54.
8. Han KY, Hong BS, Yoon YJ, Yoon CM, Kim YK, Kwon YG, et al. Polyphosphate blocks tumor metastasis via anti-angiogenic activity. Biochem J 2007;406:49-55.
9. Kawazoe Y, Katoh S, Onodera Y, Kohgo T, Shindoh M, Shiba T. Activation of the FGF signaling pathway and subsequent induction of mesenchymal stem cell differentiation by inorganic polyphosphate. Int J Biol Sci 2008;4:37-47.
10. Shiba T, Nishimura D, Kawazoe Y, Onodera Y, Tsutsumi K, Nakamura R, et al. Modulation of mitogenic activity of fibroblast growth factors by inorganic polyphosphate. J Biol Chem 2003;278:26788-92.
11. Docampo R, de Souza W, Miranda K, Rohloff P, Moreno SN. Acidocalcisomes-conserved from bacteria to man. Nat Rev Microbiol 2005;3:251-61.
12. Espiau B, Lemercier G, Ambit A, Bringaud F, Merlin G, Baltz T, et al. A soluble pyrophosphatase, a key enzyme for polyphosphate metabolism in Leishmania. J Biol Chem. 2006;281:1516-23.
13. Luo S, Ruiz FA, Moreno SNJ. The acidocalcisome Ca2+-ATPase (TgA1) of Toxoplasma gondii is required for polyphosphate storage, intracellular calcium homeostasis and virulence. Mol Microbiol 2005;55:1034-45.
14. Ruiz FA, Rodrigues CO, Docampo R. Rapid changes in polyphosphate content within acidocalcisomes in response to cell growth, differentiation, and environmental stress in Trypanosoma cruzi. J Biol Chem 2001;276:26114-21.
15. Docampo R, Scott DA, Vercesi AE, Moreno SN. Intracellular Ca2+ storage in acidocalcisomes of Trypanosoma cruzi. Biochem J 1995;310:1005-12.
16. Seufferheld MJ, Kim KM, Whitfield J, Valerio A, Caetano-Anolles G. Evolution of vacuolar proton pyrophosphatase domains and volutin granules: clues into the early evolutionary origin of the acidocalcisome. Biol Direct 2011;6:50.
17. Seufferheld M, Lea C, Vieira M, Oldfield E, Docampo R. The H+-pyrophosphatase of Rhodospirillum rubrum is predominantly located in polyphosphate-rich acidocalcisomes. J Biol Chem 2004;279:51193-202.
18. Motta LS, Ramos IB, Gomes FM, de Souza W, Champagne DE, Santiago MF, et al. Protonpyrophosphatase and polyphosphate in acidocalcisome-like vesicles from oocytes and eggs of Periplaneta americana. Insect Biochem Mol Biol 2009;39:198-206.
19. Ramos I, Gomes F, Koeller CM, Saito K, Heise N, Masuda H, et al. Acidocalcisomes as calcium-and polyphosphate-storage compartments during embryogenesis of the insect Rhodnius prolixus Stahl. PLOS One 2011;6:e27276.
20. Ramos IB, Miranda K, Pace DA, Verbist KC, Lin FY, Zhang Y, et al. Calcium-and polyphosphate-containing acidic granules of sea urchin eggs are similar to acidocalcisomes, but are not the targets for NAADP. Biochem J 2010;429:485-95.
21. Ramos IB, Miranda K, Ulrich P, Ingram P, LeFurgey A, Machado EA, et al. Calcium-and polyphosphate-containing acidocalcisomes in chicken egg yolk. Biol Cell 2010;102:421-34.
22. Kapuscinski J. DAPI: a DNA-specific fluorescent probe. Biotech Histochem 1995; 70:220-33.
23. Allan RA, Miller JJ. Influence of S-adenosylmethionine on DAPI-induced fluorescence of polyphosphate in the yeast vacuole. Can J Microbiol 1980;26:912-20.
24. Marchesini N, Ruiz FA, Vieira M, Docampo R. Acidocalcisomes are functionally linked to the contractile vacuole of Dictyostelium discoideum. J Biol Chem 2002;277:8146-53.
25. Ruiz FA, Marchesini N, Seufferheld M, Govindjee, Docampo R. The polyphosphate bodies of Chlamydomonas reinhardtii possess a proton-pumping pyrophosphatase and are similar to acidocalcisomes. J Biol Chem 2001;276:46196-203.
26. Gomes FM, Ramos IB, Motta LM, Miranda K, Santiago MF, de Souza W, et al. Polyphosphate polymers during early embryogenesis of Periplaneta americana. J Insect Physiol 2008;54:1459-66.
27. Gomes FM, Carvalho DB, Peron AC, Saito K, Miranda K, Machado EA. Inorganic polyphosphates are stored in spherites within the midgut of Anticarsia gemmatalis and play a role in copper detoxification. J Insect Physiol 2012;58:211-9.
28. Aschar-Sobbi R, Abramov AY, Diao C, Kargacin ME, Kargacin GJ, French RJ, et al. High sensitivity, quantitative measurements of polyphosphate using a new DAPIbased approach. J Fluoresc 2008;18:859-66.
29. Zink D, Sadoni N, Stelzer E. Visualizing chromatin and chromosomes in living cells. Methods 2003;29:42-50.
30. Diaz JM, Ingall ED. Fluorometric quantification of natural inorganic polyphosphate. Environ Sci Technol 2010;44:4665-71.
31. Camargo EP. Growth and differentiation in Trypanosoma cruzi. I. Origin of metacyclic Trypanosomes in Liquid media. Rev Inst Med Trop Sao Paulo 1964;6:93-100.
32. de Jesus TC, Tonelli RR, Nardelli SC, da Silva Augusto L, Motta MC, Girard-Dias W, et al. Target of rapamycin (TOR)-like 1 kinase is involved in the control of polyphosphate levels and acidocalcisome maintenance in Trypanosoma brucei. J Biol Chem 2010;285:24131-40.
33. Soares Medeiros LC, Gomes F, Maciel LR, Seabra SH, Docampo R, Moreno S, et al. Volutin granules of Eimeria parasites are acidic compartments and have physiological and structural characteristics similar to acidocalcisomes. J Eukaryot Microbiol 2011;58:416-23.
34. Einicker-Lamas M, Mezian A. Euglena gracilis as a model for the study of Cu2+ and Zn2+ toxicity and accumulation in eukaryotic cells. Environ Pollut 2002;120:779-86.
35. Garcia ES, Macarini JD, Garcia ML, Ubatuba FB. Feeding of Rhodnius prolixus in the laboratory. An Acad Bras Cienc 1975;47:537-45.
36. Gomes FM, Carvalho DB, Peron AC, Saito K, Miranda K, Machado EA. Inorganic polyphosphates are stored in spherites within the midgut of Anticarsia gemmatalis and play a role in copper detoxification. J Insect Physiol 2012;58:211-9.
37. Hoffmann-Campo C, Oliveira E, Moscardi F. Criação massal da lagarta da soja Anticarsia gemmatalis. Londrina, EMBRAPA-CNPSo, 1985.
38. Rohloff P, Miranda K, Rodrigues JC, Fang J, Galizzi M, Plattner H, et al. Calcium uptake and proton transport by acidocalcisomes of Toxoplasma gondii. PLOS One. 2011;6:e18390.
39. Ault-Riché D, Fraley CD, Tzeng CM, Kornberg A. Novel assay reveals multiple pathways regulating stress-induced accumulations of inorganic polyphosphate in Escherichia coli. J Bacteriol 1998;180: 1841-7.
40. Ruiz FA, Lea CR, Oldfield E, Docampo R. Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes. J Biol Chem 2004;279:44250-7.
41. Miranda K, Benchimol M, Docampo R, de Souza W. The fine structure of acidocalcisomes in Trypanosoma cruzi. Parasitol Res 2000;86:373-84.
42. Scott DA, Docampo R, Dvorak JA, Shi S, Leapman RD. In situ compositional analysis of acidocalcisomes in Trypanosoma cruzi. J Biol Chem 1997;272:28020-9.
43. Souza W, Carreiro I, Miranda K, Silva N. Two special organelles found in Trypanosoma cruzi. An Acad Bras Cienc 2000;72:421-32.
44. Miranda K, Docampo R, Grillo O, de Souza W. Acidocalcisomes of trypanosomatids have species-specific elemental composition. Protist 2004;155:395-405.
45. Lefort-Tran M, Bre MH, Ranck JL, Pouphile M. Euglena plasma membrane during normal and vitamin B12 starvation growth. J Cell Sci 1980;41:245-61.
46. Miranda K, Rodrigues CO, Hentchel J, Vercesi A, Plattner H, de Souza W, et al. Acidocalcisomes of Phytomonas francai possess distinct morphological characteristics and contain iron. Microscopy and Microanalysis 2004;10:647-55.
47. Miranda K, Docampo R, Grillo O, Franzen A, Attias M, Vercesi A, et al. Dynamics of polymorphism of acidocalcisomes in Leishmania parasites. Histochem Cell Biol 2004;121:407-18.
48. Scott DA, Docampo R. Characterization of Isolated Acidocalcisomes of Trypanosoma cruzi. J Biol Chem 2000;275:24215-21.
49. Gomes FM, Carvalho DB, Machado EA, Miranda K. Ultrastructural and functional analysis of secretory goblet cells in the midgut of the lepidopteran Anticarsia gemmatalis. Cell Tissue Res 2013;352:313-26.
50. Kulakova AN, Hobbs D, Smithen M, Pavlov E, Gilbert JA, Quinn JP, et al. Direct quantification of inorganic polyphosphate in microbial cells using 4'-6-diamidino-2-phenylindole (DAPI). Environ Sci Technol 2011;45:7799-803.
51. Omelon S, Omelon S, Georgiou J, Georgiou J, Henneman ZJ, Henneman ZJ, et al. Control of Vertebrate Skeletal Minera-lization by Polyphosphates. PLOS One. 2009;4:e5634.
52. Pavlov E, Aschar-Sobbi R, Campanella M, Turner RJ, Gomez-Garcia MR, Abramov AY. Inorganic polyphosphate and energy metabolism in mammalian cells. J Biol Chem 2010;285:9420-8.
53. Gomes FM, Oliveira DMP, Motta LS, Ramos IB, Miranda KM, Machado EA. Inorganic polyphosphate inhibits an aspartic proteaselike activity in the eggs of Rhodnius prolixus (Stahl) and impairs yolk mobilization in vitro. J Cell Physiol 2010;222:606-11.
54. Miranda K, de Souza W, Plattner H, Hentschel J, Kawazoe U, Fang J, et al. Acidocalcisomes in Apicomplexan parasites. Exp Parasitol 2008;118:2-9.
55. Tijssen JP, Beekes HW, Van Steveninck J. Localization of polyphosphates in Saccharomyces fragilis, as revealed by 4',6-diamidino-2-phenylindole fluorescence. Biochim Biophys Acta 1982;721:394-8.
56. Urech K, Drr M, Boller T, Wiemken A, Schwencke J. Localization of polyphosphate in vacuoles of Saccharomyces cerevisiae. Arch Microbiol 1978;116:275-8.
57. Ebel J. Recherches sur les polyphosphates contenus dans diverses cellules vivantes. IV. Localisation cytologique et role physiologique des polyphosphates dans la cellule vivante. Bull Soc Chim Biol (Paris) 1952; 34:498-505.
58. Wiame J. Remarque sur la metachromasie des cellules de levure. CR Soc Biol. 1946; 140:897-99.
59. Dmitrieva S, Bekker Z. Some data on the nature of the volutin granules in Penicillium chrysogenum. Tsitologiia 1961;4:691-95.
60. Voelz H, Voelz U, Ortigoza RO. The polyphosphate overplus phenomenon in Myxo coccus xanthus and its influence on the architecture of the cell. Arch Microbiol 1966;53:371-88.
61. Lopez Revilla R, Gomez Dominguez R. Incorporation and Toxicity of 32P Orthophosphate and Occurrence of Polyphosphate in Entamoeba Tropho zoites. J Eukaryot Microbiol 1985;32:353-5.
62. Suresh N, Warburg R, Timmerman M, Wells J, Coccia M, Roberts M, et al. New strategies for the isolation of microorganisms responsible for phosphate accumulation. Water Science & Technology 1985;17:99-111.
63. Kulaev IS, Vagabov V, Kulakovskaya T. The biochemistry of inorganic polyphosphates. Wiley Online Library, 1979.
64. Tanious FA, Veal JM, Buczak H, Ratmeyer LS, Wilson WD. DAPI (4', 6-diamidino-2-phenylindole) binds differently to DNA and RNA: minor-groove binding at AT sites and intercalation at AU sites. Biochemistry 1992;31:3103-12.
65. Gunther S, Trutnau M, Kleinsteuber S, Hause G, Bley T, Roske I, et al. Dynamics of polyphosphate-accumulating bacteria in wastewater treatment plant microbial communities detected via DAPI (4', 6'-diamidino-2-phenylindole) and tetracycline labeling. Appl Environ Microbiol 2009; 75:2111-21.
66. Saito K, Ohtomo R, Kuga-Uetake Y, Aono T, Saito M. direct labeling of polyphosphate at the ultrastructural level in Saccharomyces cerevisiae by Using the affinity of the poly-phosphate binding domain of Escherichia coli exopolyphosphatase. Appl Environ Microbiol 2005;71: 5692-701.
67. Kuga Y, Saito K, Nayuki K, Peterson RL, Saito M. Ultrastructure of rapidly frozen and freeze-substituted germ tubes of an arbuscular mycorrhizal fungus and localization of polyphosphate. New Phytologist 2008;178: 189-200.
68. Saito K, Kuga-Uetake Y, Saito M, Peterson RL. Vacuolar localization of phosphorus in hyphae of Phialocephala fortinii, a dark septate fungal root endophyte. Can J Microbiol 2006;52:643-50.
69. Chernysheva E, Kritskii M, Kulaev I. [The determination of the degree of polymerization of different inorganic polyphosphate fractions from mycelia of Neurospora crassa]. [Article in Russian]. Biokhimiia 1971;36:138-42.
70. Rao NN, Liu S, Kornberg A. Inorganic polyphosphate in Escherichia coli: the phosphate regulon and the stringent response. J Bacteriol 1998;180:2186-93.
71. Abramov AY, Fraley C, Diao CT, Winkfein R, Colicos MA, Duchen MR, et al. Targeted polyphosphatase expression alters mitochondrial metabolism and inhibits calciumdependent cell death. Proc Natl Acad Sci USA 2007;104:18091-6.
72. Martin P, Van Mooy BA. Fluorometric quantification of polyphosphate in environmental plankton samples: extraction protocols, matrix effects, and nucleic acid interference. Appl Environ Microbiol 2013;79:273-81.