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, Human mutation of CGI-58 is the cause of ChanarinDorfman syndrome, an orphan disease characterized by a systemic accumulation of TAG which engenders tissue disorders. The CGI-58 protein has also been shown to participate in neutral lipid metabolism in plants and, in this case, a mutation again provokes TAG accumulation. Although its roles as an ATGL coactivator and in lipid metabolism are quite clear, the catalytic activity of CGI-58 is still in question. The acyltransferase activities of CGI-58 have been speculated about, reported or even dismissed and experimental evidence that CGI-58 expressed in E. coli possesses an unambiguous catalytic activity is still lacking. To address this problem, we developed a new set of plasmids and site-directed mutants to elucidate the in vivo effects of CGI-58 expression on lipid metabolism in E. coli. By analyzing the lipid composition in selected E. coli strains expressing CGI-58 proteins, and by reinvestigating enzymatic tests with adequate controls, we show here that recombinant plant CGI58 has none of the proposed activities previously described. Recombinant plant and mouse CGI-58 both lack acyltransferase activity towards either lysophosphatidylglycerol or lysophosphatidic acid to form phosphatidylglycerol or phosphatidic acid and recombinant plant CGI-58 does not catalyze TAG or phospholipid hydrolysis. However, expression of recombinant plant CGI-58, but not mouse CGI-58, led to a decrease in phosphatidylglycerol in all strains of E. coli tested, and a mutation of the putative catalytic residues restored a wild-type phenotype. The potential activities of plant CGI-58 are subsequently discussed. Introduction The ?/? hydrolase-type protein Comparative Gene Identification-58 (CGI-58), also called ABDH5, is found in various organisms, LGSKEGMIPLEVWT 933 Reassessing the Potential Activities of Plant CGI-58 Protein Abdallah Khatib, Yani Arhab, Assia Bentebibel, Abdelkarim Abousalham, Alexandre Noiriel* Institut de Chimie et de Biochimie Moléculaires et Supramoléculaires UMR 5246 CNRS, Organisation et Dynamique des Membranes Biologiques, p.2, 20161-01-08.
, Reassessing the Potential Activities of Plant CGI-58 Protein, PLoS ONE, vol.11, issue.1, p.145806, 2016.
, Editor: Monika Oberer, 2015.
, This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: AK was supported by grant #2012-11 from the Lebanese Association for Scientific Research, www.laser-lb.org. The funders had no role in study design, data collection and analysis, 2016.
, Competing Interests: The authors have declared that no competing interests exist. Abbreviations: ABTS, 2,2'-azino-bis(3ethylbenzothiazoline-6-sulphonic acid)
, Adipose triglyceride lipase; CGI-58, Comparative Gene Identification-58, ATGL
, In these two clades of evolution, CGI-58 mutations provoke various neutral lipid disorders characterized, predominantly, by TAG accumulation in non-fat storing cells, such as the mesophyll cells of plants and the non-adipose tissues of mammals (skin, DOPC, vol.1, issue.2
, ICTI is a yeast protein identified by functional screening as being involved in tolerance to copper toxicity [6] and shown, by microarray analysis, CGI-58 was described as being closely related to ICT1
, In plants, a mutation in the gene for CGI-58 leads to an accumulation of TAG, with levels more than 10 times higher than in wild-type Arabidopsis leaves, a non-fat storing organ, vol.4
, In addition to its role as a lipid turnover regulator, it has been shown that CGI-58 also has an effect on polyamines, which have been described to be important molecules in growth and stress responses. In plants, CGI-58 regulates polyamine metabolism [10] by interacting with spermidine synthase 1 (SPDS1). Structurally, plant CGI-58 possesses at least two characteristic motifs. The first is a GXSXG motif found in lipases, CGI-58 co-regulates lipid homeostasis, too, by interacting with Peroxisomal ABC Transporter (PXA1)
, In mammals, the mutation of CGI-58 is responsible for the Chanarin-Dorfman syndrome, a neutral lipid storage disease with ichthyosis (NLSDI), characterized by TAG accumulation within the epidermis
, ATGL) activating, by a factor of 20, the lipolytic activity of ATGL
, In addition, the mammalian CGI-58 protein possesses an acyltransferase motif, HX 4 D, and harbors a mutated GXNXG lipase motif, whereby a suspected inactive asparagine replaces
, The contaminant was identified as plsC, the enzyme responsible for phosphatidic acid (PA) synthesis in E. coli through the transfer of the acyl group from acylCoA to LPA. It would be easy to imagine that the LPAAT activity, previously described in recombinant plant CGI-58 purified from E. coli, could originate from the same contaminant identified during the characterization of recombinant mouse CGI-58 purified from E. coli, raising reasonable doubts regarding the potential activity of recombinant plant CGI-58. More surprising results have emerged from a recent paper describing lysophosphatidylglycerol acylCoA acyltransferase (LPGAT) activity for human CGI-58, expressed in mammalian cells [19], questioning the putative activities and involvement of plant and mammalian CGI-58 in phospholipid synthesis. Although the role of CGI-58 as a regulator of lipid metabolism is quite clear, its catalytic activity is still elusive and questionable. In order to reassess the putative activities of plant CGI58, we tested the phenotype of several E. coli strains defective in lipid metabolism. We used new in vivo approaches to demonstrate that recombinant plant CGI-58 proteins are not able, 20162-01-08.
, DOPG, vol.1, issue.2
, DPPC, vol.1, issue.2
, DPPG, vol.1, issue.2
, Increased Copper Tolerance 1; IPTG, Isopropyl ?-D-1thiogalactopyranoside, ICT1
, Lysophosphatidic acid acylCoA acyltransferase; LPGAT, Lysophosphatidylglycerol acylCoA acyltransferase
,
, PLA 2 , Phospholipase A 2 ; PLD, Phospholipase D; plsC, 1acyl-sn-glycerol-3-phosphate acyltransferase
,
, Here, we report that the expression of plant CGI-58 in another E. coli strain deficient in phosphatidylglycerol (PG) synthesis could not restore the synthesis of PG in this genetic background, compared to an authentic PG synthase as prokaryotic pgsA. Also, more surprisingly, plant CGI-58 expression leads to a decrease in PG but not in phosphatidylethanolamine (PE) content, suggesting a role for CGI-58 in PG catabolism. Interestingly, a decrease in PG was also observed in all the tested E. coli strains expressing plant CGI-58 and we found that this effect was potentially due to the catalytic activity of CGI-58, via a mutation of the seryl residue within the GXSXG lipase motif at position 199. Using the decrease in PG as a phenotype, we tested the involvement of several residues, and we were able to show that only the histidyl, and not the aspartyl, residue belonging to the HX 4 D acyltransferase motif was implicated in the decrease of PG content. Materials and Methods Materials The lipids dioleoylphosphatidylcholine (DOPC), 1-palmitoyl, 2-oleoylphosphatidylglycerol (POPG), 1-palmitoyl, 2-oleoylphosphatidylethanolamine and 1-oleoyllysoPG were purchased from Avanti Polar, TLL, Thermomyces lanuginosus lipase. demonstrated has a toxic effect alleviated by moderate LPAAT activity. Likewise, these recombinant plant proteins did not show any detectable in vitro LPAAT activity, using purified protein obtained with an optimized protocol under native conditions, vol.18
, All strains were grown at 37°C except MN7 and SM2-1, which were kept at 30°C. When necessary, LB plates contained 250 ?M CuSO 4 , 1 mM ABTS and 1 ?M IPTG. Antibiotic concentrations were 0.1 ?g/?L for kanamycin, 0.02 ?g/?L for chloramphenicol, 0.05 ?g/?L for streptomycin, 0.1 ?g/ ?L for ampicillin and 0.01 ?g/?L for tetracycline. Pre-coated TLC-sheets ALUGRAM 1 Xtra SIL G/UV 254 (Macherey Nagel) were used for lipids analysis in E. coli, BL21(DE3) strain and plasmids pACYC184 and pACYC177 were obtained from New England Biolabs. Plasmid pAR1219 was from Sigma Aldrich Chimie. Mus musculus CGI-58 (MmCGI-58) was a gift of Dr Zechner (University of Graz, Austria), and pET28a-MmCGI-58-12His (referred to as MmCGI-58) was a gift from Prof. Brasaemle (Rutgers
, Basically, LPAAT activity was measured, in the presence of 50 ?M of lysoPA and 10 ?M oleoylCoA (13 000 dpm / test) in a 50 mM potassium phosphate buffer, at pH 7.0 for 10 minutes, and in a final volume of 100 ?L. Phospholipase activity was quantified for 40 minutes, in the presence of 100 ?M of dipalmitoylPC (20 000 dpm / test), in a 50 mM Tris HCl buffer, at pH 7.5, with 2 mM DTT and 1 ?g of Reassessing the Potential Activities of Plant, Enzymatic Activities LPAAT, phospholipase and triglyceride lipase activities were measured under the same conditions as described in [12], with some modifications, 2016.
, with the appropriate unlabeled substrates and expected unlabeled products as carriers using chloroform:methanol (2:1, v/v) and then separated by TLC on Silica Gel G & GF Preparative Uniplates with unlabeled, but identical products used as the reference
, Next, 7 ?g of purified AtCGI-58 Trc or 10 ?g of proteins from the cell extract were added and the reaction mixture was incubated, at 30°C, for 2 h for the purified fraction or 30 min for the cell extract. Reactions were terminated by adding 100 ?L of 0.1 N HCl. Lipids were extracted with chloroform:methanol (2:1, v/v) and separated, by TLC, using a chloroform:methanol:acetic acid (65:25:10, v/v/v) solution. The area containing free fatty acids was scraped and then quantified by scintillation counting. Cloning cDNAs coding for MmCGI-58 and for full-length (AtCGI-58 FL) or truncated AtCGI-58 (AtCGI-58 Trc) were amplified by PCR with primers 01 and 02, 03 and 04, 03 and 05, respectively. The primers are listed in Table 1. All constructs harbor an NdeI site and a sequence coding for a 6-Histidine tag at the 5' end, together with a NotI restriction site at the 3' end. PCR products were digested with NotI and NdeI, purified with the QIAquick PCR Purification Kit (QIagen, Courtaboeuf, France), and then ligated into the pET28b plasmid, dipalmitoylPC (DPPC) using phospholipase D (PLD) in the presence of glycerol. PC substrate, composed of 35.5 nmol of unlabeled DPPC and 4.5 nmol of [ 14 C]-DPPC, was sonicated for 10 min to form micelles in 150 ?L of buffer containing 0.83 mM SDS, 0.83 mM Triton X100, 20 mM CaCl 2 , 500 mM glycerol and 50 mM Tris-HCl, pH of chloroform:methanol, vol.65, 20164.
, allowing expression and purification of recombinant proteins in E. coli. A) Maps of vectors pYAT7 and pAKT7 containing T7 RNA polymerase cloned into plasmids harboring the p15A origin of replication. Left panel: pYAT7 plasmid with T7RP cloned into the BamHI site of the pACYC184 backbone, thus conferring resistance to chloramphenicol. Right panel: pAKT7 plasmid with T7RP cloned into the HindIII-SalI sites of the pACYC177 backbone, thus conferring resistance to ampicillin. Active and inactive antibiotic resistance genes are shown in green and in grey, respectively. Remarkable restriction sites Reassessing the Potential Activities of Plant, active LPAAT, such as plsC, can be detected in this expression system and that strains transformed with different CGI-58s behave as negative controls. CGI-58 was previously identified by its homology with yeast ICT1, 2016.
, Left panel: coloration due to ABTS oxidation in different E. coli genetic backgrounds necessitates both the presence of CotA and T7RP. MG1655 or BL21(DE3) strains were either transformed with void pET28b or with pET28b-CotA. Central and right panels: functional expression of CotA in MG1655 strain transformed with either pYAT7, pAKT7 plasmids or native pACYC184 or pACYC177 plasmids. LB plates contain 250 ?M CuSO 4 , 1 mM ABTS and 1 ?M IPTG. All pictures were taken 3 days after streaking. C) Functional expression of CotA cloned into pYAT7 and pAKT7 plasmids with analysis by SDS-PAGE of total proteins extracted from the recombinant strain. Extracts were analyzed before or after a 3 h induction with IPTG. Lane 1: strain BL21(DE3) transformed with pET28b-CotA. Lane 2 and 3: strain MG1655 transformed with pYAT7 and either void plasmid (lane 2) or pET28b-CotA (lane 3). Lane 4: strain MG1655 transformed with pAKT7 and pET28b-CotA. The expected size of CotA (58.5 kDa) is indicated. D) Analysis by SDS-PAGE of purified CGI-58, from plant or mouse, expressed either in BL21(DE3) strain or SM2-1 and transformed with pYAT7. 5 ?g of recombinant MmCGI-58 and 2 ?g of recombinant plant CGI-58 were loaded onto each lane. Lane 1: MmCGI-58 (42.0 kDa), Lane 2: truncated version of AtCGI-58 (44.5 kDa), Lane 3: full-length version of AtCGI-58 (47.8 kDa). The authenticity of purified recombinant MmCGI-58 was verified by mass spectrometry after tryptic digestion, and for recombinant plant CGI-58 a Western-blot with monoclonal Anti-polyHistidine antibody was performed, PA synthesis and copper sensitivity. are shown. B) Functional use of pYAT7 and pAKT7 plasmids for expressing the recombinant CotA protein in MG1655, a T7RP deficient E. coli strain, 201610-01-08.
, Our first attempts to measure the activity, as described previously [12], were unsuccessful. As detailed by Ghosh et al., recombinant plant CGI-58 was purified from inclusion bodies, under denaturing conditions with 6 M urea, and tested without any proper refolding step, but it is possible that the refolding was immediate when the protein was mixed in the reaction buffer. Consequently, we tried to measure LPAAT activity using recombinant plant CGI-58 purified under native conditions from BL21(DE3) [Fig 1D] and we were able to detect, by LC-MS, a weak PA synthesis over time. However, at the same time as we were performing this experiment, Since CGI-58 is described as being located in the cytosol [4] and plsC has been shown to be membrane-bound by the presence of a putative anchor in its N-terminal region, vol.36
, Phenotype of SM2-1 and SM105 strains, grown at 30 or 42°C in the presence or absence of 3 mM of copper sulfate after serial dilution. B) Serial dilutions of the SM2-1 strain containing the pYAT7 plasmid and transformed with CGI-58 constructs or controls: void pET28b vector, MmCG-58, AtCGI-58 Trc, plsC wt, or plsC*G39E. Liquid cultures were incubated for 4 hours with 100 ?M IPTG prior to dilution and plating. LB plates contained, in addition to antibiotics, 100 ?M IPTG. All pictures were taken 2 days after plating, Absence of lysphosphatidic acid acylCoA acyltransferase activity of plant CGI-58 protein shown by functional complementation. A), 201611-01-08.
, To test the hypothesis that PG could be a substrate for plant CGI-58, we synthesized labeled PG, from [ 14 C]-PC, using the phospholipase D-catalyzed transphosphatidylation reaction of [ 14 C]-PC and glycerol. However, under the conditions used, neither the incubation of crude extract from the BL21(DE3) strain expressing plant CGIfor CGI-58 showed that PG levels increased compared to the wild-type, whereas the amount of other major plant phospholipids (PC, PE, phosphatidylinositol and phosphatidylserine) was unchanged, by plant CGI-58 to form another undetected lipid or, alternatively, CGI-58 may have a regulatory role in phospholipid synthesis
, we designed primers to change these three residues by site-directed mutagenesis in plant CGI-58 and, hence, we created S199N, D384A and H379A versions of the truncated plant CGI-58. Mutated versions of plant CGI-58 were then expressed with the pYAT7 plasmids in MN7, SM2-1 and BL21(DE3) strains. Lipids were again extracted and separated by 2D-TLC
, demonstrating that S199 and H379 residues are involved in the decrease of PG seen in strains transformed with the wild-type construct. The amount of PG in mutant D384 is quite similar to that found in the corresponding wild-types, suggesting that this residue is not involved in the catalytic reaction. Consequently, we decided to quantify the amount of phospholipids, by LC/MS/MS, in SM2-1 transformants where we had previously observed the more dramatic effects, Mutations S199N and H379A led to a visual increase of the PG level in both strains
, Reassessing the Potential Activities of Plant CGI-58, Protein PLOS ONE, 201615-01-08.
, Alignment of plant CGI-58s. Sequences were retrieved from NCBI with the protein BLAST software, using AtCGI-58 as bait, from Mosses through to Eudicot proteins. Alignment was performed with BioEdit software and the shading threshold was set to 75% identity. Arabidopsis thaliana At4g24160 was retrieved from a sequenced RAFL19-16-I19 clone and the Physcomitrella patens sequence was reconstructed from a sequencing of ESTs BY990945
, Theobroma cacao XP_007017700.1, Nelumbo nucifera XP_010271460.1, Eucalyptus grandis XP_010061022.1, Musa acuminata subsp. malaccensis XP_009418733.1, Sesamum indicum XP_011083599.1, Solanum lycopersicum XP_004243145.1, Nicotiana sylvestris XP_009794253.1, Citrus sinensis XP_006473603.1, Ricinus communis XP_002510485.1, Phoenix dactylifera XP_008813831.1, Medicago truncatula XP_003603733.1, Glycine max XP_006577977.1, Fragaria vesca subsp. vesca XP_004291822.1, Malus domestica XP_008347352.1, Prunus persica XP_007222711.1, Picea glauca BT117776.1, Cucumis sativus XP_004152662.1, Amborella trichopoda XP_006854859.1, Beta vulgaris subsp. vulgaris XP_010670751.1, Zea mays ACF79200.1, Oryza sativa Japonica Group NP_001063697.2, Brachypodium distachyon XP_003578450, Accession numbers are as following: Camelina sativa XP_010439078.1, Brassica rapa XP_009137743.1, Populus trichocarpa XP_002307698, vol.2
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