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PMID: 9012816 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Membrane specific mapping and colocalization of malarial and host skeletal proteins in the Plasmodium falciparum infected erythrocyte by dual-color near-field scanning optical microscopy.

Enderle T, Ha T, Ogletree DF, Chemla DS, Magowan C, Weiss S

Abstract

Accurate localization of proteins within the substructure of cells and cellular organelles enables better understanding of structure-function relationships, including elucidation of protein-protein interactions. We describe the use of a near-field scanning optical microscope (NSOM) to simultaneously map and detect colocalized proteins within a cell, with superresolution. The system we elected to study was that of human red blood cells invaded by the human malaria parasite Plasmodium falciparum. During intraerythrocytic growth, the parasite expresses proteins that are transported to the erythrocyte cell membrane. Association of parasite proteins with host skeletal proteins leads to modification of the erythrocyte membrane. We report on colocalization studies of parasite proteins with an erythrocyte skeletal protein. Host and parasite proteins were selectively labeled in indirect immunofluorescence antibody assays. Simultaneous dual-color excitation and detection with NSOM provided fluorescence maps together with topography of the cell membrane with subwavelength (100 nm) resolution. Colocalization studies with laser scanning confocal microscopy provided lower resolution (310 nm) fluorescence maps of cross sections through the cell. Because the two excitation colors shared the exact same near-field aperture, the two fluorescence images were acquired in perfect, pixel-by-pixel registry, free from chromatic aberrations, which contaminate laser scanning confocal microscopy measurements. Colocalization studies of the protein pairs of mature parasite-infected erythrocyte surface antigen (MESA) (parasite)/protein4.1(host) and P. falciparum histidine rich protein (PfHRP1) (parasite)/protein4.1(host) showed good real-space correlation for the MESA/protein4.1 pair, but relatively poor correlation for the PfHRP1/protein4.1 pair. These data imply that NSOM provides high resolution information on in situ interactions between proteins in biological membranes. This method of detecting colocalization of proteins in cellular structures may have general applicability in many areas of current biological research.

MeSH Terms
Cells, Cultured Cytoskeletal Proteins Erythrocyte Membrane/metabolism Erythrocytes/parasitology,ultrastructure Fluorescent Antibody Technique, Indirect Humans Malaria, Falciparum/parasitology Membrane Proteins/metabolism Microscopy/methods Microscopy, Confocal/methods Microscopy, Fluorescence/methods Neuropeptides Proteins/metabolism Protozoan Proteins/metabolism
Chemicals
Cytoskeletal Proteins Membrane Proteins Neuropeptides Proteins Protozoan Proteins erythrocyte membrane band 4.1 protein erythrocyte membrane protein band 4.1-like 1 histidine-rich proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Enderle T
Molecular Design Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Ha T
Ogletree D F
Chemla D S
Magowan C
Weiss S
References (44)
44 references, click to expand
  1. Selective association of a fragment of the knob protein with spectrin, actin and the red cell membrane.
    Mol Biochem Parasitol. 1991 Feb;44(2):175-81 PMID: 2052019
  2. Plasmodium falciparum maturation abolishes physiologic red cell deformability.
    Science. 1984 Jan 27;223(4634):400-3 PMID: 6362007
  3. Abnormalities in the mechanical properties of red blood cells caused by Plasmodium falciparum.
    Blood. 1989 Aug 1;74(2):855-61 PMID: 2665857
  4. Variable antigen associated with the surface of erythrocytes infected with mature stages of Plasmodium falciparum.
    Mol Biochem Parasitol. 1986 Sep;20(3):265-77 PMID: 3531849
  5. The fine structure of Plasmodium falciparum and its host erythrocytes in natural malarial infections in man.
    Bull World Health Organ. 1966;35(6):883-5 PMID: 5338378
  6. An alternative to serum for cultivation of Plasmodium falciparum in vitro.
    Trans R Soc Trop Med Hyg. 1997 May-Jun;91(3):363-5 PMID: 9231219
  7. Plasmodium falciparum malaria. Ultrastructure of parasitized erythrocytes in cardiac vessels.
    Am J Trop Med Hyg. 1971 Sep;20(5):655-60 PMID: 4999241
  8. Variations in structure and function during the life cycle of malarial parasites.
    Bull World Health Organ. 1977;55(2-3):139-56 PMID: 338177
  9. Malarial proteins at the membrane of Plasmodium falciparum-infected erythrocytes and their involvement in cytoadherence to endothelial cells.
    Prog Allergy. 1988;41:98-147 PMID: 3043425
  10. Fluorescence resonance energy transfer reveals interleukin (IL)-1-dependent aggregation of IL-1 type I receptors that correlates with receptor activation.
    J Biol Chem. 1995 Nov 17;270(46):27562-8 PMID: 7499217
  11. Plasmodium falciparum and Plasmodium coatneyi: immunogenicity of "knob-like protrusions" on infected erythrocyte membranes.
    Exp Parasitol. 1977 Jun;42(1):157-64 PMID: 405234
  12. Human malaria parasites in continuous culture.
    Science. 1976 Aug 20;193(4254):673-5 PMID: 781840
  13. Libraries of peptides and proteins displayed on filamentous phage.
    Methods Enzymol. 1993;217:228-57 PMID: 7682645
  14. Characterization of a protein correlated with the production of knob-like protrusions on membranes of erythrocytes infected with Plasmodium falciparum.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4650-3 PMID: 388448
  15. Diminished red blood cell deformability in uncomplicated human malaria. A preliminary report.
    J Med. 1982;13(5-6):479-85 PMID: 6763070
  16. Localization of the ring-infected erythrocyte surface antigen (RESA) of Plasmodium falciparum in merozoites and ring-infected erythrocytes.
    J Exp Med. 1985 Aug 1;162(2):774-9 PMID: 3894564
  17. Isolation of skeleton-associated knobs from human red blood cells infected with malaria parasite Plasmodium falciparum.
    Mol Biochem Parasitol. 1992 Jun;52(2):283-7 PMID: 1620167
  18. Single molecules observed by near-field scanning optical microscopy.
    Science. 1993 Nov 26;262(5138):1422-5 PMID: 17736823
  19. The mature erythrocyte surface antigen of Plasmodium falciparum is not required for knobs or cytoadherence.
    Mol Biochem Parasitol. 1989 Aug;36(1):61-5 PMID: 2682238
  20. Cytoadherence by Plasmodium falciparum-infected erythrocytes is correlated with the expression of a family of variable proteins on infected erythrocytes.
    J Exp Med. 1988 Oct 1;168(4):1307-20 PMID: 3049911
  21. Antibodies in malarial sera to parasite antigens in the membrane of erythrocytes infected with early asexual stages of Plasmodium falciparum.
    J Exp Med. 1984 Jun 1;159(6):1686-704 PMID: 6374012
  22. Voltage sensing by fluorescence resonance energy transfer in single cells.
    Biophys J. 1995 Oct;69(4):1272-80 PMID: 8534797
  23. Separation of viable schizont-infected red cells of Plasmodium falciparum from human blood.
    Ann Trop Med Parasitol. 1978 Feb;72(1):87-8 PMID: 350172
  24. Scanning electron microscope-analysis of the protrusions (knobs) present on the surface of Plasmodium falciparum-infected erythrocytes.
    J Cell Biol. 1983 Sep;97(3):795-802 PMID: 6350320
  25. Transport of an Mr approximately 300,000 Plasmodium falciparum protein (Pf EMP 2) from the intraerythrocytic asexual parasite to the cytoplasmic face of the host cell membrane.
    J Cell Biol. 1987 May;104(5):1269-80 PMID: 2437128
  26. Plasmodium falciparum malaria: association of knobs on the surface of infected erythrocytes with a histidine-rich protein and the erythrocyte skeleton.
    J Cell Biol. 1984 Apr;98(4):1256-64 PMID: 6371019
  27. Localization of Plasmodium falciparum histidine-rich protein 1 in the erythrocyte skeleton under knobs.
    Mol Biochem Parasitol. 1987 Sep;25(2):165-74 PMID: 2444884
  28. Trafficking of malarial proteins to the host cell cytoplasm and erythrocyte surface membrane involves multiple pathways.
    J Cell Biol. 1992 Dec;119(6):1481-95 PMID: 1469045
  29. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes.
    Cell. 1995 Jul 14;82(1):77-87 PMID: 7541722
  30. Proximity relationships between the type I receptor for Fc epsilon (Fc epsilon RI) and the mast cell function-associated antigen (MAFA) studied by donor photobleaching fluorescence resonance energy transfer microscopy.
    Eur J Immunol. 1996 Jan;26(1):84-91 PMID: 8566088
  31. The mature-parasite-infected erythrocyte surface antigen (MESA) of Plasmodium falciparum associates with the erythrocyte membrane skeletal protein, band 4.1.
    Mol Biochem Parasitol. 1990 Jan 15;38(2):261-70 PMID: 2183050
  32. Mechanochemistry of protein 4.1's spectrin-actin-binding domain: ternary complex interactions, membrane binding, network integration, structural strengthening.
    J Cell Biol. 1995 Aug;130(4):897-907 PMID: 7642705
  33. Microspectroscopic imaging tracks the intracellular processing of a signal transduction protein: fluorescent-labeled protein kinase C beta I.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8407-12 PMID: 8710884
  34. Quantitation of fluorescence energy transfer between cell surface proteins via fluorescence donor photobleaching kinetics.
    Biophys J. 1994 Aug;67(2):881-8 PMID: 7948701
  35. Parasite-regulated membrane transport processes and metabolic control in malaria-infected erythrocytes.
    Biochem J. 1995 Jun 1;308 ( Pt 2):361-74 PMID: 7772015
  36. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes.
    Cell. 1995 Jul 14;82(1):89-100 PMID: 7606788
  37. Energy transfer: a spectroscopic ruler.
    Proc Natl Acad Sci U S A. 1967 Aug;58(2):719-26 PMID: 5233469
  38. Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes.
    J Exp Med. 1984 Jun 1;159(6):1567-75 PMID: 6374009
  39. Membrane rigidity of red blood cells parasitized by different strains of Plasmodium falciparum.
    J Lab Clin Med. 1993 Nov;122(5):581-9 PMID: 8228577
  40. Mapping of adherens junction components using microscopic resonance energy transfer imaging.
    J Cell Sci. 1995 Mar;108 ( Pt 3):1051-62 PMID: 7622593
  41. Role of the Plasmodium falciparum mature-parasite-infected erythrocyte surface antigen (MESA/PfEMP-2) in malarial infection of erythrocytes.
    Blood. 1995 Oct 15;86(8):3196-204 PMID: 7579415
  42. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes.
    Cell. 1995 Jul 14;82(1):101-10 PMID: 7606775
  43. Single Molecule Dynamics Studied by Polarization Modulation.
    Phys Rev Lett. 1996 Nov 4;77(19):3979-3982 PMID: 10062357
  44. Probing the interaction between two single molecules: fluorescence resonance energy transfer between a single donor and a single acceptor.
    Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6264-8 PMID: 8692803
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1997-01-21
Pages
520-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC19545
Subset
IM
Grants
NIDDK NIH HHS · P01 DK032094 · United States
NIDDK NIH HHS · DK 32094 · United States
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