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Plasmalogen loss caused by remodeling deficiency in mitochondria

View ORCID ProfileTomohiro Kimura  Correspondence email, Atsuko K Kimura, Mindong Ren, Vernon Monteiro, Yang Xu, Bob Berno, Michael Schlame, View ORCID ProfileRichard M Epand  Correspondence email
Tomohiro Kimura
1Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Canada
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  • For correspondence: kimurat@mcmaster.ca
Atsuko K Kimura
1Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Canada
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Mindong Ren
3Department of Cell Biology, New York University Langone Medical Center, New York, NY, USA
4Department of Anesthesiology, New York University Langone Medical Center, New York, NY, USA
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Vernon Monteiro
1Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Canada
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Yang Xu
4Department of Anesthesiology, New York University Langone Medical Center, New York, NY, USA
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Bob Berno
2Department of Chemistry and Chemical Biology, McMaster University, Hamilton, Canada
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Michael Schlame
3Department of Cell Biology, New York University Langone Medical Center, New York, NY, USA
4Department of Anesthesiology, New York University Langone Medical Center, New York, NY, USA
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Richard M Epand
1Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Canada
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  • For correspondence: epand@mcmaster.ca
Published 21 August 2019. DOI: 10.26508/lsa.201900348
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  • Figure 1.
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    Figure 1. 31P NMR observations of losses in the levels of plasmalogens in the tafazzin-deficient mouse organs and human lymphoblast cells compared with controls.

    (A) Structures of plasmenylcholine, plasmenylethanolamine, diacyl PC, and diacyl PE. Structures are drawn for the dominant acyl chain species in the mammalian heart regarding the choline glycerophospholipids (Schmid & Takahashi, 1968; Arthur et al, 1985; Kikuchi et al, 1999) and in the mammalian brain regarding the ethanolamine glycerophospholipids (O’Brien et al, 1964; O’Brien & Sampson, 1965; Sun & Horrocks, 1970; Choi et al, 2018). Dominant acyl chain species in the brain depend furthermore on a neuroanatomical location of a membrane. (B) 31P NMR spectra in the choline glycerophospholipid region of the mouse heart phospholipids and in the ethanolamine glycerophospholipid region of the mouse brain, liver, kidney, and the human lymphoblast phospholipids measured in a SDS micellar solution: WT or healthy individual control (blue trace) and the TAZ-KD or BTHS (red trace). The downfield part, marked with an arrow, of the overlapping signals corresponds to the plasmalogen signal, whereas the upfield part corresponds to the diacyl glycerophospholipid signal with a minor contribution from the plasmanyl glycerophospholipid signal (Diagne et al, 1984; May et al, 1988; Kikuchi et al, 1999; Kimura et al, 2018). Tafazzin deficiency causes a reduction of plasmalogen and a counterbalancing increase of the counterpart diacyl glycerophospholipid (see the main text). †Spectra of the heart phospholipids were based on data in Kimura et al (2018). *A shoulder peak from sphingomyelin. (C) Commonly present counterbalance of a decrease in the level of plasmalogen (1-O-alk-1′-enyl-2-acyl-GPE (plasmenylethanolamine) and 1-O-alk-1′-enyl-2-acyl-GPC (plasmenylcholine)) by an increase in the level of the counterpart diacyl glycerophospholipid (1,2-diacyl-GPE (diacyl PE) and 1,2-diacyl-GPC (diacyl PC), respectively) is explained by competition reactions of their precursors on the ethanolaminephosphotransferase (EPT) and cholinephosphotransferase (CPT) activities. (D) 31P NMR spectra of the BTHS (red) and control (blue) human lymphoblast phospholipids measured in a SDS micellar solution. A magnified region at the upper left shows a large decrease in the level of CL (0.751 ppm) along with increases in the levels of 2-MLCL (1.142 ppm) and 1-MLCL (1.014 ppm). An increase in the level of PG (0.851 ppm) is also seen. **A part of the CL decrease is masked by contributions from the resonance of a phosphate group in the diacyl half of MLCLs (Kimura et al, 2018).

  • Figure S1.
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    Figure S1. 31P NMR spectra of the mouse organ and human lymphoblast phospholipids in the chemical shift region corresponding to choline glycerophospholipids.

    31P NMR spectra in a SDS micellar solution show that the plasmenylcholine signal is not resolved as a minor component of the human lymphoblast and the mouse organs (brain, liver, and kidney) except the heart, which is a rare organ rich in plasmenylcholine (Diagne et al, 1984; May et al, 1988; Kikuchi et al, 1999; Kimura et al, 2018). The signal of plasmanylcholine as a minor component (Diagne et al, 1984; May et al, 1988; Kikuchi et al, 1999; Kimura et al, 2018) overlaps with that of diacyl PC (Kimura et al, 2018). The measured chemical shift value of a class or subclass of phospholipid extracted from those biological materials slightly depends on the organ and cell type as shown in Tables S1, S2, S3, and S4. This is due likely to some co-extracted materials that are present and depend on the organ/cell type, thus influencing differentially the molecular environment of the phosphate group of the same phospholipid class or subclass. The spectra are aligned with corrections for these minor chemical shift differences given in Tables S1, S2, S3, and S4.

  • Figure S2.
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    Figure S2. Biosynthesis pathway for plasmalogens [1-O-alk-1′-enyl-2-acyl-GPE (plasmenylethanolamine) and 1-O-alk-1′-enyl-2-acyl-GPC (plasmenylcholine)] in the cell (Lee, 1998; Nagan & Zoeller, 2001; Malheiro et al, 2015).

    Biosynthesis of plasmalogen initiates in peroxisomes, where dihydroxyacetone phosphate (DHAP) is acylated in its sn-1 position by glycerone phosphate O-acyltransferase (1: GNPAT), followed by formation of the characteristic ether linkage in the early precursor of plasmalogen via exchange of the sn-1 acyl group with an alkyl group by alkylglycerone phosphate synthase (2: AGPS). A fatty alcohol used for this introduction of the sn-1 alkyl ether group is derived from a fatty acid by the enzymatic action of fatty acyl-CoA reductase 1 (Far1) (Bishop & Hajra, 1981). Far1 is known as a rate-determining enzyme of the plasmalogen synthesis pathway, whose level is regulated by a feedback mechanism in response to the plasmalogen level (Honsho et al, 2010; Kimura et al, 2018). 1-O-alkyl-DHAP is reduced to 1-O-alkyl-2-hydroxy-glycero-3-phosphate (1-O-alkyl-2-hydroxy-G3P) by acyl/alkyl-DHAP reductase (3) located in both the peroxisomal and the ER membranes. Reaction proceeds in the ER to form 1-O-alkyl-2-acyl-G3P by alkyl/acyl-glycerophosphate acyltransferase (4) (Yamashita et al, 2014), 1-O-alkyl-2-acyl-G by PA phosphatase named lipin (5) (Zhang & Reue, 2017), 1-O-alkyl-2-acyl-GPE (GPC) by the ethanolaminephosphotransferase (EPT) or cholinephosphotransferase (CPT) activity (6), and 1-O-alk-1′-enyl-2-acyl-GPE, that is, plasmenylethanolamine by plasmanylethanolamine desaturase (7). Plasmenylcholine is formed from plasmenylethanolamine in pathways either with or without replacement of the sn-2 acyl chain. One pathway without the acyl chain replacement is via formation of 1-O-alk-1′-enyl-2-acyl-G, such as by phospholipase C among several possible routes (8), followed by the plasmenylcholine formation by the CPT activity (15). Another pathway including the acyl chain replacement is via formation of 1-O-alk-1′-enyl-2-hydroxy-GPE by phospholipase A2 (9), and 1-O-alk-1′-enyl-2-hydroxy-GP either upon cleavage of the ethanolamine headgroup by lysophospholipase D (10) or upon cleavage of the phosphoethanolamine headgroup by lysophospholipase C (11) with subsequent phosphorylation by phosphotransferase (12). 1-O-alk-1′-enyl-2-hydroxy-GP is acylated by acyl-CoA acyltransferase (13) to form 1-O-alk-1′-enyl-2-acyl-GP, whose phosphate is released by phosphohydrolase (14) to form 1-O-alk-1′-enyl-2-acyl-G.

  • Figure S3.
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    Figure S3. High-resolution 31P NMR shows that a plasmenylethanolamine loss and a diacyl PE gain observed on the whole cell lymphoblast derived from BTHS patients are attributed to those opposing changes observed in the crude mitochondria fraction. MALDI-TOF MS of ethanolamine glycerophospholipids on the crude mitochondria fraction evidences the opposing changes of individual species.

    (A) High-resolution 31P NMR spectra of healthy control (blue trace) and BTHS (red trace) lymphoblast phospholipids in the region showing ethanolamine glycerophospholipids and CLs. The spectra are shown for the whole cell, the crude mitochondria fraction, and the ER fraction. Measurements were conducted in aqueous solution of SDS micelles dissolving the lipids. The opposing trends in (i) the relative levels of plasmenylethanolamine and diacyl PE in mitochondria and (ii) those in the ER accord with data in a previous report (Arthur et al, 1985). These trends contribute to their comparable levels in the healthy whole cell (blue trace). The plasmenylethanolamine loss (14.4 ± 1.9 → 10.8 ± 1.1 mol % of total phospholipid) and the diacyl PE gain (13.6 ± 1.1 → 21.1 ± 1.4 mol %) in tafazzin deficiency observed in the whole cell (Table S4; N = 3) reflect the plasmenylethanolamine loss (11.2 ± 1.0 → 9.2 ± 0.7 mol %) and the diacyl PE gain (22.6 ± 1.7 → 28.5 ± 1.0 mol %) observed in the crude mitochondria fraction. Three independent subcellular fractionation experiments on three independent culture of lymphoblast cells were conducted (N = 3). No significant changes in their levels are seen in the ER fraction. The observation of the changes in the state of CL is also limited to the crude mitochondria fraction because of the predominant location of CL in the inner mitochondrial membrane of the cell (Daum, 1985; Horvath & Daum, 2013). *A part of the CL loss is masked in the spectra by contributions from the resonance of a phosphate group in the diacyl half of MLCLs (Kimura et al, 2018). (B) MALDI-TOF MS experiments were conducted to measure changes in the levels of individual ethanolamine glycerophospholipid species in the crude mitochondria fraction of BTHS lymphoblast compared with healthy control. Plots of molar ratios of plasmenylethanolamine/diacyl PE are shown on the dominant species in lymphoblast (18:0/18:1 [36:1] and 18:0/20:4 [38:4]) (Xu et al, 2005) and on the species of particular interest in transacylation by tafazzin (18:0/18:2 [36:2]) (Vreken et al, 2000; Schlame et al, 2002, 2003, 2005; Valianpour et al, 2005; Kiebish et al, 2013). The error is shown as the SD (N = 5). P values are from the t test. The measured plasmenylethanolamine/diacyl PE ratios <1 and the decreases in the ratios in BTHS compared with control are in accord with the NMR data showing the same result from the total amounts.

  • Figure 2.
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    Figure 2. Changes in the phospholipid composition of the mouse organs and human lymphoblast due to tafazzin deficiency.

    (A) Changes [TAZ-KD − WT, or BTHS − control (mol %)] in the compositions of phospholipids (PL: CL, choline [Cho], ethanolamine [Etn], and other classes) of the mouse heart, brain, liver, kidney, and human lymphoblast due to tafazzin deficiency. Values for these changes, and errors indicating the SDs (N = 3), are given in Tables S1, S2, S3, and S4. †Plot is based on numbers reported in Kimura et al (2018). *Not resolved in the 31P NMR spectrum as a minor component in these organs and blood cells (Fig S1). **Not detected in the 31P NMR spectrum of WT or TAZ-KD (or of control or BTHS). (B) Changes in the levels (mol %) of PLs (CL, Cho, and Etn classes) relative to the normal level (mol %) of CL [(TAZ-KDPL − WTPL)/WTCL, or (BTHSPL − controlPL)/controlCL], a known key player lipid in regulation of mitochondrial function. Values for these changes, and errors indicating the SDs (N = 3), are given in Table 1. †Plot is based on numbers reported in Kimura et al (2018).

  • Figure 3.
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    Figure 3. Quantitative Western blot of proteins in BTHS and control lymphoblast that are indicative of (i) the amount of peroxisomes (Pex19p and PMP70), (ii) a degree of feedback regulation of the plasmalogen level (Far1), and (iii) a degree of plasmalogen-selective lipid degradation (iPLA2β and iPLA2γ).

    (A) Ratios of the expression levels (BTHS/control) in lymphoblast on cytosolic Pex19p (N = 7) and peroxisomal membrane protein PMP70 (N = 6). Values for the ratios, and errors indicating the SDs, are given in Table S5. Measurements for determination of ratios were conducted on the PNS, whereas fractionation by ultracentrifugation (see Materials and Methods) results in detection of Pex19p exclusively in the supernatant fraction (S), and PMP70 exclusively in the membrane pellet fraction (P) that includes peroxisomes (Kimura et al, 2018). (B) Western blotting image showing no significant change in expression of Far1 in lymphoblast as a result of the plasmenylethanolamine loss observed by 31P NMR in BTHS. The fractionation experiment resulted in detection of Far1 dominantly in the S fraction. Incubation with the primary antibody in the presence of a blocking peptide (Table S6) resulted in disappearance of the immunodetection; plus (+) and minus (−) denote, respectively, the experiments with and without a blocking peptide, and capital M denotes a molecular weight marker. The ratio of BTHS/control measured on the PNS fraction (N = 7) is presented as a bar graph. Values for the ratio, and errors indicating the SD, are given in Table S5. †Shown together in the graph is greatly enhanced expression of Far1 in the TAZ-KD mouse heart, in response to the large loss of plasmenylcholine (Kimura et al, 2018). The ratio of TAZ-KD/WT was measured on the PNS (N = 10), and errors shown indicate the SD. (C) Western blotting images showing quantities of iPLA2β and iPLA2γ. The fractionation experiment resulted in detection of those proteins in both the S and P fractions. BTHS/control ratios determined from the PNS are shown in a bar graph (N = 6). Values for the ratios, and errors indicating the SDs, are given in Table S5.

  • Figure S4.
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    Figure S4. A 31P NMR measurement of PA content in the mouse brain.

    (A) PA, which is abundant in the mammalian brain, undergoes the characteristic second deprotonation of its phosphate located at the headgroup terminus with a pKa2 value of 7.9 (Kooijman et al, 2005). The molecular species shown is a representative species in the mammalian brain (Chan et al, 2012). (B) At pH 6.0, the PA signal appears in the spectral region where there is significant overlap with the 2-MLCL signal. The second deprotonation induced by increasing the pH to 8.5 shifts the PA signal largely downfield, so that both PA and 2-MLCL contents in the TAZ-KD mouse brain can be unambiguously quantified. (C) 31P NMR spectra of the WT (blue trace) and TAZ-KD (red trace) brain phospholipids measured at pH 8.5. *A part of the CL decrease is masked by contributions from the resonance of a phosphate group in the diacyl half of MLCLs (Kimura et al, 2018).

  • Figure S5.
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    Figure S5. Quantification of target proteins in human lymphoblast by the Western blot immunodetection.

    Measured expression levels of the target proteins were analyzed using Image Lab Software (Bio-Rad). In the analysis, normalization to the total protein content (Gürtler et al, 2013) was used rather than the conventional normalization using a particular internal control protein, such as a housekeeping protein whose level of expression may be significantly sensitive to tafazzin deficiency. A detailed procedure of the normalization method is given elsewhere (Kimura et al, 2018). Briefly, a fluorophore was introduced to a fraction of tryptophan residues in proteins in the gel after running the SDS–PAGE as described in Materials and Methods. This fluorophore introduction enables us to measure the total protein content and to determine the lane-dependent efficiency in the transfer from the gel to the membrane to correct for it. Adoption of the method of normalization to the total protein content also allows us to avoid usually more demanding empirical search for conditions where signals from a housekeeping protein and multiple target proteins of interest are all within the linear dynamic range (Taylor et al, 2013). The introduction of a fluorophore to proteins in the gel for measurements of the total protein content allows us to focus more on the search for conditions for quantitative detection of target proteins. (A) A linear response of the fluorescence to the total protein content was confirmed in the range of 0.2‒25 μg (N = 5) for our sample (human lymphoblast PNS) covering the three orders of magnitude. (B) Signal intensity in the immunodetection of each target protein (Pex19p, PMP70, Far1, catalase, iPLA2β, or iPLA2γ) was plotted as a function of the total protein content (μg) to evaluate the linear dynamic range for quantification on the human lymphoblast samples derived from BTHS patients and healthy individual controls (see the Materials and Methods section).

Tables

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    Table 1.

    Changes due to tafazzin deficiency in the contents (mol %) of the mouse organ and human lymphoblast phospholipids (PLs) relative to the normal content of CL (mol %) in the WT or healthy individual control ((TAZ-KDPL − WTPL)/WTCL or (BTHSPL − controlPL)/controlCL).a Numbers are shown for CL, choline (Cho), and ethanolamine (Etn) classes.

    PhospholipidMouseHuman lymphoblast
    HeartBrainLiverKidney
    CL−0.69 ± 0.06+0.18 ± 0.67−0.01 ± 0.21−0.14 ± 0.11−0.73 ± 0.05
    2-MLCL+0.38 ± 0.03+0.16 ± 0.02+0.17 ± 0.04+0.27 ± 0.02+0.64 ± 0.12
    1-MLCL+0.13 ± 0.06+0.05 ± 0.05+0.11 ± 0.03+0.12 ± 0.02+0.23 ± 0.08
    Diacyl PC (with plasmanylcholine)b+1.21 ± 0.54— c— c— c— c
    Plasmenylcholine−1.98 ± 0.65N.R.dN.R.dN.R.dN.R.d
    Diacyl PE (with plasmanylethanolamine)b+0.59 ± 0.25+1.22 ± 1.81+3.76 ± 1.45+0.60 ± 0.66+3.37 ± 0.79
    Plasmenylethanolamine+0.03 ± 0.08−4.56 ± 1.76−0.43 ± 0.24−0.32 ± 0.22−1.58 ± 0.96
    • ↵a The average and error, shown as the SD, are obtained from three independent sets of biological samples (N = 3) for each of the WT and TAZ-KD mice, or healthy individuals and BTHS patients (Tables S1, S2, S3, and S4).

    • ↵b The signal of plasmanyl glycerophospholipid as a minor component overlaps with the signal of the counterpart diacyl glycerophospholipid (Diagne et al, 1984; May et al, 1988; Kikuchi et al, 1999; Kimura et al, 2018).

    • ↵c Content change in combination with that of plasmenylcholine is not discussed here because of a minor content of plasmenylcholine in the organ or blood cells (Diagne et al, 1984; May et al, 1988; Kikuchi et al, 1999; Kimura et al, 2018).

    • ↵d Signal not resolved because of a minor content (Fig S1).

Supplementary Materials

  • Figures
  • Tables
  • Supplementary Text 1.

    Only plasmenylcholine but not plasmenylethanolamine is lost in the TAZ-KD mouse heart.[LSA-2019-00348_Supplementary_Text_1.doc]

  • Table S1 Contents and changes (mol %)1of the brain phospholipids of the WT versus TAZ-KD mice.

  • Table S2 Contents and changes (mol %)1 of the liver phospholipids of the WT versus TAZ-KD mice.

  • Table S3 Contents and changes (mol %)1 of the kidney phospholipids of the WT versus TAZ-KD mice.

  • Table S4 Contents and changes (mol %)1 of phospholipids of the lymphoblast cells derived from healthy individual controls and BTHS patients.

  • Supplementary Text 2.

    Mechanism of the counterbalance of a plasmalogen loss by a gain of the counterpart diacyl glycerophospholipid.[LSA-2019-00348_Supplementary_Text_2.doc]

  • Table S5 Ratios1 of the protein expression level BTHS/control in human lymphoblast, measured by the quantitative Western blotting.

  • Supplementary Text 3.

    Remodeling of CL acyl chain species by tafazzin: Is there any correlation with abundant species of plasmalogen and the observed plasmalogen loss?[LSA-2019-00348_Supplementary_Text_3.doc]

  • Supplementary Text 4.

    Influence of a loss of diacyl PE on expression, organization, and activity of the supercomplexes in yeast.[LSA-2019-00348_Supplementary_Text_4.doc]

  • Supplementary Text 5.

    A loss of plasmenylethanolamine–protein interactions in AD.[LSA-2019-00348_Supplementary_Text_5.doc]

  • Table S6 List of antibodies used in the quantitative Western blot experiments on the human lymphoblast derived from healthy individual controls and BTHS patients.

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Plasmalogen loss in remodeling deficiency
Tomohiro Kimura, Atsuko K Kimura, Mindong Ren, Vernon Monteiro, Yang Xu, Bob Berno, Michael Schlame, Richard M Epand
Life Science Alliance Aug 2019, 2 (4) e201900348; DOI: 10.26508/lsa.201900348

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Plasmalogen loss in remodeling deficiency
Tomohiro Kimura, Atsuko K Kimura, Mindong Ren, Vernon Monteiro, Yang Xu, Bob Berno, Michael Schlame, Richard M Epand
Life Science Alliance Aug 2019, 2 (4) e201900348; DOI: 10.26508/lsa.201900348
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