Home LiteratureArticle Details
PMID: 7575411 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Ca2+ storage in Trypanosoma brucei: the influence of cytoplasmic pH and importance of vacuolar acidity.

The Biochemical journal ·Vol. 310 ( Pt 3) ·1995-09-15 ·Pages 789-94

Scott DA, Moreno SN, Docampo R

Abstract

The hypothesis that changes in cytosolic pH effect the release from intracellular compartments of stored calcium in Trypanosoma brucei was addressed by the use of procyclic and bloodstream trypomastigotes of T. brucei loaded with the fluorescent reagents 2',7'-bis-(2-carboxyethyl)-5(and 6)-carboxyfluorescein (BCECF) to measure intracellular pH (pHi), or fura 2 to measure intracellular free calcium ([Ca2+]i). Experiments were performed in EGTA-containing buffers, so increases in [Ca2+]i reflected release of stored calcium rather than Ca2+ entry. Nigericin reduced pHi and increased [Ca2+]i in loaded cells, whilst propionate reduced pHi, but did not affect [Ca2+]i, and NH4Cl increased both variables, so there appears to be no correlation between pHi and [Ca2+]i. Treatment of the cells with the calcium ionophore ionomycin under similar conditions (nominal absence of extracellular Ca2+) resulted in an increase of [Ca2+]i which was greatly increased by addition of either NH4Cl, nigericin or the vacuolar H(+)-ATPase inhibitor bafilomycin A1. Similar results were obtained when the order of additions was reversed or when digitonin-permeabilized cells were used with the Ca2+ indicator arsenazo III. The results suggest that more Ca2+ is stored in this acidic compartment in procyclic than in bloodstream forms. Taking into account the relative importance of the ionomycin-releasable and the ionomycin-plus-NH4Cl-releasable Ca2+ pools, it is apparent that a significant amount of the Ca2+ stored in T. brucei trypomastigotes is present in the acidic compartment thus identified.

MeSH Terms
Ammonium Chloride/pharmacology Animals Anti-Bacterial Agents/pharmacology Calcium/metabolism Cytosol/drug effects,metabolism Enzyme Inhibitors/pharmacology Fluoresceins Fluorescent Dyes Fura-2 Hydrogen-Ion Concentration Ionomycin/pharmacology Ionophores/pharmacology Kinetics Macrolides Nigericin/pharmacology Propionates/pharmacology Proton-Translocating ATPases/antagonists & inhibitors Trypanosoma brucei brucei/metabolism Vacuoles/metabolism
Chemicals
Anti-Bacterial Agents Enzyme Inhibitors Fluoresceins Fluorescent Dyes Ionophores Macrolides Propionates Ammonium Chloride Ionomycin 2',7'-bis(carboxyethyl)-5(6)-carboxyfluorescein bafilomycin A1 Proton-Translocating ATPases propionic acid Nigericin Calcium Fura-2
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Scott D A
Department of Veterinary Pathobiology, University of Illinois at Urbana-Champaign 61801, USA.
Moreno S N
Docampo R
References (38)
38 references, click to expand
  1. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):7972-6 PMID: 2973058
  2. A novel heterodimeric transferrin receptor encoded by a pair of VSG expression site-associated genes in T. brucei.
    Cell. 1994 Jul 15;78(1):75-86 PMID: 8033214
  3. Characterization of inositol 1,4,5-trisphosphate-sensitive (IsCaP) and -insensitive (IisCaP) nonmitochondrial Ca2+ pools in rat pancreatic acinar cells.
    J Membr Biol. 1989 Jul;109(2):173-86 PMID: 2527996
  4. Endocytosis by African trypanosomes. II. Occurrence in different life-cycle stages and intracellular sorting.
    Eur J Cell Biol. 1989 Aug;49(2):303-10 PMID: 2776776
  5. Intracellular ion activities and membrane transport in parietal cells measured with fluorescent dyes.
    Methods Enzymol. 1990;192:38-81 PMID: 2074799
  6. Endocytosis of gold-labeled proteins and LDL by Trypanosoma cruzi.
    Parasitol Res. 1991;77(6):461-8 PMID: 1656428
  7. Intracellular Ca2+ pools in PC12 cells. Three intracellular pools are distinguished by their turnover and mechanisms of Ca2+ accumulation, storage, and release.
    J Biol Chem. 1991 Oct 25;266(30):20159-67 PMID: 1939077
  8. Calcium homeostasis in Trypanosoma brucei. Identification of a pH-sensitive non-mitochondrial calcium pool.
    J Biol Chem. 1991 Dec 25;266(36):24351-8 PMID: 1722203
  9. Calcium homeostasis in procyclic and bloodstream forms of Trypanosoma brucei. Lack of inositol 1,4,5-trisphosphate-sensitive Ca2+ release.
    J Biol Chem. 1992 Mar 25;267(9):6020-6 PMID: 1556113
  10. Identification of a large pre-lysosomal compartment in the pathogenic protozoon Trypanosoma cruzi.
    J Cell Sci. 1992 May;102 ( Pt 1):157-67 PMID: 1500438
  11. Identification, purification and properties of clone-specific glycoprotein antigens constituting the surface coat of Trypanosoma brucei.
    Parasitology. 1975 Dec;71(3):393-417 PMID: 645
  12. Recent ultrastructural studies on trypanosomes.
    Ann Soc Belg Med Trop. 1977;57(4-5):441-57 PMID: 610620
  13. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents.
    Proc Natl Acad Sci U S A. 1978 Jul;75(7):3327-31 PMID: 28524
  14. Measurements of cation transport with metallochromic indicators.
    Methods Enzymol. 1979;56:301-38 PMID: 37412
  15. A novel model for fluid secretion by the trypanosomatid contractile vacuole apparatus.
    J Cell Biol. 1979 Nov;83(2 Pt 1):371-82 PMID: 500785
  16. Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication.
    Acta Trop. 1979 Sep;36(3):289-92 PMID: 43092
  17. Generation of free radical metabolites and superoxide anion by the calcium indicators arsenazo III, antipyrylazo III, and murexide in rat liver microsomes.
    J Biol Chem. 1983 Dec 25;258(24):14920-5 PMID: 6317679
  18. Effects of exogenous amines on mammalian cells, with particular reference to membrane flow.
    Biochem J. 1984 Jan 1;217(1):27-40 PMID: 6365083
  19. Ca2+ and Mg2+-enhanced reduction of arsenazo III to its anion free radical metabolite and generation of superoxide anion by an outer mitochondrial membrane azoreductase.
    J Biol Chem. 1984 Dec 10;259(23):14609-16 PMID: 6094566
  20. A new generation of Ca2+ indicators with greatly improved fluorescence properties.
    J Biol Chem. 1985 Mar 25;260(6):3440-50 PMID: 3838314
  21. Acidification of the endocytic and exocytic pathways.
    Annu Rev Biochem. 1986;55:663-700 PMID: 2874766
  22. Receptor-mediated endocytosis in the bloodstream form of Trypanosoma brucei.
    J Protozool. 1987 Nov;34(4):465-73 PMID: 2828605
  23. H+-dependent calcium uptake into an IP3-sensitive calcium pool from rat parotid gland.
    Am J Physiol. 1988 Oct;255(4 Pt 1):G429-40 PMID: 3263053
  24. ATP-driven Ca2+/H+ antiport in acid vesicles from Dictyostelium.
    Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8025-9 PMID: 1387710
  25. Endocytosed transferrin in African trypanosomes is delivered to lysosomes and may not be recycled.
    Eur J Cell Biol. 1992 Dec;59(2):398-404 PMID: 1493805
  26. Thapsigargin causes Ca2+ release and collapse of the membrane potential of Trypanosoma brucei mitochondria in situ and of isolated rat liver mitochondria.
    J Biol Chem. 1993 Apr 25;268(12):8564-8 PMID: 8473301
  27. Role of acidic compartments in Trypanosoma brucei, with special reference to low-density lipoprotein processing.
    Mol Biochem Parasitol. 1993 Apr;58(2):223-32 PMID: 8479447
  28. The transferrin receptor in African trypanosomes: identification, partial characterization and subcellular localization.
    Eur J Cell Biol. 1993 Oct;62(1):114-26 PMID: 8269969
  29. Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PMC1, a homolog of plasma membrane Ca2+ ATPases.
    J Cell Biol. 1994 Feb;124(3):351-63 PMID: 7507493
  30. Vacuolar H(+)-ATPase of Dictyostelium discoideum. A monoclonal antibody study.
    J Cell Sci. 1993 Dec;106 ( Pt 4):1103-13 PMID: 8126094
  31. Reconstitution of a surface transferrin binding complex in insect form Trypanosoma brucei.
    EMBO J. 1994 Jun 1;13(11):2565-73 PMID: 8013456
  32. Expression of a glycosylphosphatidylinositol-anchored Trypanosoma brucei transferrin-binding protein complex in insect cells.
    Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6443-7 PMID: 8022802
  33. An investigation on the role of vacuolar-type proton pumps and luminal acidity in calcium sequestration by nonmitochondrial and inositol-1,4,5-trisphosphate-sensitive intracellular calcium stores in clonal insulin-secreting cells.
    Eur J Biochem. 1994 Jun 15;222(3):869-77 PMID: 8026497
  34. Endocytosis of a cytotoxic human high density lipoprotein results in disruption of acidic intracellular vesicles and subsequent killing of African trypanosomes.
    J Cell Biol. 1994 Jul;126(1):155-67 PMID: 8027174
  35. Ca2+/H+ exchange in acidic vacuoles of Trypanosoma brucei.
    Biochem J. 1994 Nov 15;304 ( Pt 1):227-33 PMID: 7998937
  36. A Rab4-like GTPase in Dictyostelium discoideum colocalizes with V-H(+)-ATPases in reticular membranes of the contractile vacuole complex and in lysosomes.
    J Cell Sci. 1994 Oct;107 ( Pt 10):2801-12 PMID: 7876348
  37. Importance of acidic intracellular compartments in the lysis of Trypanosoma brucei brucei by normal human serum.
    Trans R Soc Trop Med Hyg. 1994 Jul-Aug;88(4):487-8 PMID: 7570851
  38. Characterization of a vacuolar proton ATPase in Dictyostelium discoideum.
    Biochim Biophys Acta. 1989 Jul 10;982(2):271-8 PMID: 2526657
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
1995-09-15
Pages
789-94
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1135967
Subset
IM
Grants
FIC NIH HHS · TW-00476 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]