Nanofocused Scanning X-ray Fluorescence Microscopy Revealing an Effect of Heterozygous Hemoglobin S and C on Biochemical Activities in Plasmodium falciparum-Infected Erythrocytes

Fröhlich, Benjamin; Yang, Yang; Thoma, Judith; Czajor, Julian; Lansche, Christine; Sanchez, Cecilia; Lanzer, Michael; Cloetens, Peter; Tanaka, Motomu

doi:10.1021/acs.analchem.9b05111

Title: Nanofocused Scanning X-ray Fluorescence Microscopy Revealing an Effect of Heterozygous Hemoglobin S and C on Biochemical Activities in Plasmodium falciparum-Infected Erythrocytes

Journal Article · Mon Mar 23 00:00:00 EDT 2020 · Analytical Chemistry

DOI:https://doi.org/10.1021/acs.analchem.9b05111· OSTI ID:1646582

Fröhlich, Benjamin ^[1];

^[2]; Thoma, Judith ^[1]; Czajor, Julian ^[1]; Lansche, Christine ^[3]; Sanchez, Cecilia ^[3]; Lanzer, Michael ^[3];

^[4];

^[5]

Heidelberg Univ. (Germany)
European Synchrotron Radiation Facility (ESRF), Grenoble (France); Brookhaven National Lab. (BNL), Upton, NY (United States). National Synchrotron Light Source II (NSLS-II)
Universitätsklinikum Heidelberg (Germany)
The European Synchrotron Radiation Facility (ESRF), 38043 Grenoble, France
Heidelberg Univ. (Germany); Kyoto Univ. (Japan)

While there is ample evidence suggesting that carriers of heterozygous hemoglobin S and C are protected from life-threatening malaria, little is known about the underlying biochemical mechanisms at the single cell level. In this work, using nanofocused scanning X-ray fluorescence microscopy, we quantify the spatial distribution of individual elements in subcellular compartments, including Fe, S, P, Zn, and Cu, in Plasmodium falciparum-infected (P. falciparum-infected) erythrocytes carrying the wild type or variant hemoglobins. Our data indicate that heterozygous hemoglobin S and C significantly modulate biochemical reactions in parasitized erythrocytes, such as aberrant hemozoin mineralization and a delay in hemoglobin degradation. The label-free scanning X-ray fluorescence imaging has great potential to quantify the spatial distribution of elements in subcellular compartments of P. falciparum-infected erythrocytes and unravel the biochemical mechanisms underpinning disease and protective traits.

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Research Organization:: Brookhaven National Lab. (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); German Research Foundation (DFG); Germany’s Excellence Strategy; Japan Society for the Promotion of Science (JSPS); Nakatani Foundation

Grant/Contract Number:: SC0012704; SFB1129 P3; 2082/1-390761711

OSTI ID:: 1646582

Report Number(s):: BNL-216237-2020-JAAM

Journal Information:: Analytical Chemistry, Vol. 92, Issue 8; ISSN 0003-2700

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 1 work

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References (32)

Is Hemoglobin an Essential Structural Component of Human Erythrocyte Membranes?* Weed, Robert I.; Reed, Claude F.; Berg, George Journal of Clinical Investigation, Vol. 42, Issue 4 https://doi.org/10.1172/JCI104747	journal	April 1963
Hemoglobin degradation in malaria‐infected erythrocytes determined from live cell magnetophoresis Moore, Lee R.; Fujioka, Hisashi; Williams, P. Stephen The FASEB Journal, Vol. 20, Issue 6 https://doi.org/10.1096/fj.05-5122fje	journal	February 2006
Global distribution of the sickle cell gene and geographical confirmation of the malaria hypothesis Piel, Frédéric B.; Patil, Anand P.; Howes, Rosalind E. Nature Communications, Vol. 1, Issue 1 https://doi.org/10.1038/ncomms1104	journal	November 2010
Iron Storage within Dopamine Neurovesicles Revealed by Chemical Nano-Imaging Ortega, Richard; Cloetens, Peter; Devès, Guillaume PLoS ONE, Vol. 2, Issue 9 https://doi.org/10.1371/journal.pone.0000925	journal	September 2007
Trace element mapping of a single cell using a hard x-ray nanobeam focused by a Kirkpatrick-Baez mirror system Matsuyama, S.; Shimura, M.; Mimura, H. X-Ray Spectrometry, Vol. 38, Issue 2 https://doi.org/10.1002/xrs.1123	journal	March 2009
Hard X-ray nanoprobe at beamline P06 at PETRA III Schroer, Christian G.; Boye, Pit; Feldkamp, Jan M. Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 616, Issue 2-3 https://doi.org/10.1016/j.nima.2009.10.094	journal	May 2010
Two dimensional hard x-ray nanofocusing with crossed multilayer Laue lenses Yan, Hanfei; Rose, Volker; Shu, Deming Optics Express, Vol. 19, Issue 16 https://doi.org/10.1364/OE.19.015069	journal	January 2011
Efficient concentration of high-energy x-rays for diffraction-limited imaging resolution Cesar da Silva, Julio; Pacureanu, Alexandra; Yang, Yang Optica, Vol. 4, Issue 5 https://doi.org/10.1364/OPTICA.4.000492	journal	January 2017
Three-Dimensional Correlative Imaging of a Malaria-Infected Cell with a Hard X-ray Nanoprobe Yang, Y.; Fus, F.; Pacureanu, A. Analytical Chemistry https://doi.org/10.1021/acs.analchem.8b05957	journal	May 2019
Synchrotron X-Ray Fluorescence Nanoprobe Reveals Target Sites for Organo-Osmium Complex in Human Ovarian Cancer Cells Sanchez-Cano, Carlos; Romero-Canelón, Isolda; Yang, Yang Chemistry - A European Journal, Vol. 23, Issue 11 https://doi.org/10.1002/chem.201605911	journal	January 2017
Holotomography: Quantitative phase tomography with micrometer resolution using hard synchrotron radiation x rays Cloetens, P.; Ludwig, W.; Baruchel, J. Applied Physics Letters, Vol. 75, Issue 19 https://doi.org/10.1063/1.125225	journal	November 1999
A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra Solé, V. A.; Papillon, E.; Cotte, M. Spectrochimica Acta Part B: Atomic Spectroscopy, Vol. 62, Issue 1 https://doi.org/10.1016/j.sab.2006.12.002	journal	January 2007
Fate of haem iron in the malaria parasite Plasmodium falciparum Egan, Timothy J.; Combrinck, Jill M.; Egan, Joanne Biochemical Journal, Vol. 365, Issue 2 https://doi.org/10.1042/bj20020793	journal	July 2002
The Structure of Human Hemoglobin Konigsberg, William; Hill, Robert J. Journal of Biological Chemistry, Vol. 237, Issue 8 https://doi.org/10.1016/S0021-9258(19)73787-9	journal	August 1962
l -Cysteine influx and efflux: A possible role for red blood cells in regulation of redox status of the plasma Yildiz, Deniz; Uslu, Ceylan; Cakir, Yeliz Free Radical Research, Vol. 40, Issue 5 https://doi.org/10.1080/10715760600602902	journal	January 2006
Erythocyte phosphate content in Huntington's disease Sarpel, G.; Barp, A. N.; Lubansky, H. J. Neuroscience Letters, Vol. 31, Issue 1 https://doi.org/10.1016/0304-3940(82)90060-X	journal	July 1982
The effect of phosphate loading on erythrocyte 2,3-bisphosphoglycerate levels Bremner, Kyla; Bubb, William A.; Kemp, Graham J. Clinica Chimica Acta, Vol. 323, Issue 1-2 https://doi.org/10.1016/S0009-8981(02)00165-1	journal	September 2002
Fluxes in “Free” and Total Zinc Are Essential for Progression of Intraerythrocytic Stages of Plasmodium falciparum Marvin, Rebecca G.; Wolford, Janet L.; Kidd, Matthew J. Chemistry & Biology, Vol. 19, Issue 6 https://doi.org/10.1016/j.chembiol.2012.04.013	journal	June 2012
Copper pathways in Plasmodium falciparum infected erythrocytes indicate an efflux role for the copper P-ATPase Rasoloson, Dominique; Shi, Lirong; Chong, Curtis R. Biochemical Journal, Vol. 381, Issue 3 https://doi.org/10.1042/BJ20040335	journal	July 2004
Intraerythrocytic Plasmodium falciparum utilizes only a fraction of the amino acids derived from the digestion of host cell cytosol for the biosynthesis of its proteins Krugliak, Miriam; Zhang, Jianmin; Ginsburg, Hagai Molecular and Biochemical Parasitology, Vol. 119, Issue 2 https://doi.org/10.1016/S0166-6851(01)00427-3	journal	February 2002
Excess hemoglobin digestion and the osmotic stability ofPlasmodium falciparum–infected red blood cells Lew, Virgilio L.; Tiffert, Teresa; Ginsburg, Hagai Blood, Vol. 101, Issue 10 https://doi.org/10.1182/blood-2002-08-2654	journal	May 2003
Differential time-dependent volumetric and surface area changes and delayed induction of new permeation pathways in P. falciparum -infected hemoglobinopathic erythrocytes: Volumeric and surface area changes in P. falciparum -infected erythrocytes Waldecker, Mailin; Dasanna, Anil K.; Lansche, Christine Cellular Microbiology, Vol. 19, Issue 2 https://doi.org/10.1111/cmi.12650	journal	August 2016
Beyond hemoglobin polymerization: the red blood cell membrane and sickle disease pathophysiology Hebbel, Rp Blood, Vol. 77, Issue 2 https://doi.org/10.1182/blood.V77.2.214.214	journal	January 1991
Hemoglobin S and C affect protein export in Plasmodium falciparum-infected erythrocytes Kilian, N.; Srismith, S.; Dittmer, M. Biology Open, Vol. 4, Issue 3 https://doi.org/10.1242/bio.201410942	journal	February 2015
The sickle cell trait affects contact dynamics and endothelial cell activation in Plasmodium falciparum-infected erythrocytes Lansche, Christine; Dasanna, Anil K.; Quadt, Katharina Communications Biology, Vol. 1, Issue 1 https://doi.org/10.1038/s42003-018-0223-3	journal	November 2018
Hemoglobinopathies: Slicing the Gordian Knot of Plasmodium falciparum Malaria Pathogenesis Taylor, Steve M.; Cerami, Carla; Fairhurst, Rick M. PLoS Pathogens, Vol. 9, Issue 5 https://doi.org/10.1371/journal.ppat.1003327	journal	May 2013
Abnormal PfEMP1/knob display on Plasmodium falciparum-infected erythrocytes containing hemoglobin variants: fresh insights into malaria pathogenesis and protection Fairhurst, Rick M.; Bess, Cameron D.; Krause, Michael A. Microbes and Infection, Vol. 14, Issue 10 https://doi.org/10.1016/j.micinf.2012.05.006	journal	August 2012
Haemoglobin C protects against clinical Plasmodium falciparum malaria Modiano, David; Luoni, Gaia; Sirima, Bienvenu Sodiomon Nature, Vol. 414, Issue 6861 https://doi.org/10.1038/35104556	journal	November 2001
Human malaria parasites in continuous culture Trager, W.; Jensen, J. Science, Vol. 193, Issue 4254 https://doi.org/10.1126/science.781840	journal	August 1976
Trans Stimulation Provides Evidence for a Drug Efflux Carrier as the Mechanism of Chloroquine Resistance in Plasmodium falciparum ^† Sanchez, Cecilia P.; Stein, Wilfred; Lanzer, Michael Biochemistry, Vol. 42, Issue 31 https://doi.org/10.1021/bi034269h	journal	August 2003
Synchronization of Plasmodium falciparum Erythrocytic Stages in Culture Lambros, Chris; Vanderberg, Jerome P. The Journal of Parasitology, Vol. 65, Issue 3 https://doi.org/10.2307/3280287	journal	June 1979
Lensless Tomographic Imaging of Near Surface Structures of Frozen Hydrated Malaria-Infected Human Erythrocytes by Coherent X-Ray Diffraction Microscopy Frank, Viktoria; Chushkin, Yuriy; Fröhlich, Benjamin Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-14586-4	journal	October 2017

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59 BASIC BIOLOGICAL SCIENCES
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Title: Nanofocused Scanning X-ray Fluorescence Microscopy Revealing an Effect of Heterozygous Hemoglobin S and C on Biochemical Activities in Plasmodium falciparum-Infected Erythrocytes

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