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      Repeatability and reproducibility of apparent exchange rate measurements in yeast cell phantoms using filter-exchange imaging

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          Abstract

          Objectives

          Development of a protocol for validation and quality assurance of filter-exchange imaging (FEXI) pulse sequences with well-defined and reproducible phantoms.

          Materials and methods

          A FEXI pulse sequence was implemented on a 7 T preclinical MRI scanner. Six experiments in three different test categories were established for sequence validation, demonstration of the reproducibility of phantoms and the measurement of induced changes in the apparent exchange rate (AXR). First, an ice–water phantom was used to investigate the consistency of apparent diffusion coefficient (ADC) measurements with different diffusion filters. Second, yeast cell phantoms were utilized to validate the determination of the AXR in terms of repeatability (same phantom and session), reproducibility (separate but comparable phantoms in different sessions) and directionality of diffusion encodings. Third, the yeast cell phantoms were, furthermore, used to assess potential AXR bias because of altered cell density and temperature. In addition, a treatment experiment with aquaporin inhibitors was performed to evaluate the influence of these compounds on the cell membrane permeability in yeast cells.

          Results

          FEXI-based ADC measurements of an ice–water phantom were performed for three different filter strengths, showed good agreement with the literature value of 1.099 × 10 –3 mm 2/s and had a maximum coefficient of variation (CV) of 0.55% within the individual filter strengths. AXR estimation in a single yeast cell phantom and imaging session with five repetitions resulted in an overall mean value of (1.49 ± 0.05) s −1 and a CV of 3.4% between the chosen regions of interest. For three separately prepared phantoms, AXR measurements resulted in a mean value of (1.50 ± 0.04) s −1 and a CV of 2.7% across the three phantoms, demonstrating high reproducibility. Across three orthogonal diffusion directions, a mean value of (1.57 ± 0.03) s −1 with a CV of 1.9% was detected, consistent with isotropy of AXR in yeast cells. Temperature and AXR were linearly correlated ( R 2 = 0.99) and an activation energy E A of 37.7 kJ/mol was determined by Arrhenius plot. Furthermore, a negative correlation was found between cell density (as determined by the reference ADC/ f e) and AXR ( R 2 = 0.95). The treatment experiment resulted in significantly decreased AXR values at different temperatures in the treated sample compared to the untreated control indicating an inhibiting effect.

          Conclusions

          Using ice–water and yeast cell-based phantoms, a protocol for the validation of FEXI pulse sequences was established for the assessment of stability, repeatability, reproducibility and directionality. In addition, a strong dependence of AXR on cell density and temperature was shown. As AXR is an emerging novel imaging biomarker, the suggested protocol will be useful for quality assurance of AXR measurements within a study and potentially across multiple sites.

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          Most cited references52

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          Temperature-dependent self-diffusion coefficients of water and six selected molecular liquids for calibration in accurate 1H NMR PFG measurements

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            Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein.

            Water rapidly crosses the plasma membrane of red blood cells (RBCs) and renal tubules through specialized channels. Although selective for water, the molecular structure of these channels is unknown. The CHIP28 protein is an abundant integral membrane protein in mammalian RBCs and renal proximal tubules and belongs to a family of membrane proteins with unknown functions. Oocytes from Xenopus laevis microinjected with in vitro-transcribed CHIP28 RNA exhibited increased osmotic water permeability; this was reversibly inhibited by mercuric chloride, a known inhibitor of water channels. Therefore it is likely that CHIP28 is a functional unit of membrane water channels.
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              Aquaporins are multifunctional water and solute transporters highly divergent in living organisms.

              Aquaporins (AQPs) are ubiquitous membrane proteins whose identification, pioneered by Peter Agre's team in the early nineties, provided a molecular basis for transmembrane water transport, which was previously thought to occur only by free diffusion. AQPs are members of the Major Intrinsic Protein (MIP) family and often referred to as water channels. In mammals and plants they are present in almost all organs and tissues and their function is mostly associated to water molecule movement. However, recent studies have pointed out a wider range of substrates for these proteins as well as complex regulation levels and pathways. Although their relative abundance in plants and mammals makes it difficult to investigate the role of a particular AQP, the use of knock-out and mutagenesis techniques is now bringing important clues regarding the direct implication of specific AQPs in animal pathologies or plant deficiencies. The present paper gives an overview about AQP structure, function and regulation in a broad range of living organisms. Emphasis will be given on plant AQPs where the high number and diversity of these transport proteins, together with some emerging aspects of their functionalities, make them behave more like multifunctional, highly adapted channels rather than simple water pores.
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                Author and article information

                Contributors
                rbraren@tum.de
                schilling@tum.de
                Journal
                MAGMA
                MAGMA
                Magma (New York, N.y.)
                Springer International Publishing (Cham )
                0968-5243
                1352-8661
                12 July 2023
                12 July 2023
                2023
                : 36
                : 6
                : 957-974
                Affiliations
                [1 ]GRID grid.6936.a, ISNI 0000000123222966, Department of Nuclear Medicine, School of Medicine, Klinikum rechts der Isar, , Technical University of Munich, ; 81675 Munich, Germany
                [2 ]GRID grid.6936.a, ISNI 0000000123222966, Diagnostic and Interventional Radiology, School of Medicine, Klinikum rechts der Isar, , Technical University of Munich, ; 81675 Munich, Germany
                [3 ]GRID grid.7497.d, ISNI 0000 0004 0492 0584, German Cancer Consortium (DKTK), , Partner Site Munich and German Cancer Research Center (DKFZ), ; Heidelberg, Germany
                Author information
                http://orcid.org/0000-0001-5239-4628
                Article
                1107
                10.1007/s10334-023-01107-w
                10667135
                37436611
                23949127-bd87-46ef-8eef-8405e434942c
                © The Author(s) 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 14 October 2022
                : 21 June 2023
                : 22 June 2023
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: 391523415
                Award Recipient :
                Funded by: Technische Universität München (1025)
                Categories
                Research Article
                Custom metadata
                © European Society for Magnetic Resonance in Medicine and Biology (ESMRMB) 2023

                Radiology & Imaging
                magnetic resonance imaging,diffusion-weighted imaging,filter-exchange imaging,apparent exchange rate,transmembrane permeability,validation phantom,yeast

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