Glycobiology Advance Access originally published online on December 23, 2003
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Glycobiology vol 14 no 4 pp. 357-363, 2004
Glycobiology vol. 14 no. 4 © Oxford University Press 2004; all rights reserved.
Galectin-1 induces astrocyte differentiation, which leads to production of brain-derived neurotrophic factor
3 Glycobiology Research Group, Tokyo Metropolitan Institute of Gerontology, Foundation for Research on Aging and Promotion of Human Welfare, 35-2 Sakaecho, Itabashi-ku, Tokyo 173-0015, Japan; and 4 Department of Biological Chemistry, Faculty of Pharmaceutical Sciences, Teikyo University, Sagamiko, Kanagawa 199-0195, Japan
Received on November 12, 2003; revised on November 30, 2003; accepted on December 4, 2003
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Abstract |
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Brain-derived neurotrophic factor (BDNF) is a neuroprotective polypeptide that is thought to be responsible for neuron proliferation, differentiation, and survival. An agent that enhances production of BDNF is expected to be useful for the treatment of neurodegenerative diseases. Here we report that galectin-1, a member of the family of ß-galactoside binding proteins, induces astrocyte differentiation and strongly inhibits astrocyte proliferation, and then the differentiated astrocytes greatly enhance their production of BDNF. Induction of astrocyte differentiation and BDNF production by an endogenous mammalian lectin may be a new mechanism for preventing neuronal loss after injury.
Key words: astrocyte differentiation / brain-derived neurotrophic factor / galectin-1
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Introduction |
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Prevention of neuronal loss during central nervous system (CNS) injuries is important to maintain brain function. One protein in particular, brain-derived neurotrophic factor (BDNF), appears to play an important role in the survival, differentiation, and synaptic plasticity of neurons (Barde, 1989
; Ming et al., 2002; Thoenen, 1995). Finding an agent that enhances production of BDNF is expected to be useful and applicable to the treatment of neurodegenerative diseases. We report that galectin-1, a member of the family of ß-galactoside binding proteins, induces astrocyte differentiation, and then the differentiated astrocytes greatly enhance their production of BDNF.
Astrocytes are a major cell type in the CNS. They are believed to act in cooperation with neurons and other glial cells and to participate in the development and maintenance of functions of the CNS. Immature astrocytes possess a polygonal shape, have no processes, and continue to proliferate, whereas mature astrocytes have a stellate cell morphology, increased glial fibrillary acidic protein (GFAP) expression, and proliferate slowly (Bovolenta et al., 1984; Hatten, 1984). However, little is known about how astrocytes are induced to differentiate. Previously, we revealed that a lectin, Datura stramonium agglutinin (DSA), induced astrocyte differentiation from an immature polygonal shape to a matured stellate shape (Sasaki and Endo, 2000). DSA is known to bind the Galß1-4GlcNAcß1-6Man
1 branching multiantennary complex-type or two or more linear N-acetyllactosamine repeats (Cummings and Kornfeld, 1984; Yamashita et al., 1987). However, DSA is a plant agglutinin and has never been found in brain. We wanted to determine whether a similar molecule with the same carbohydrate-binding specificity and same ability to induce astrocyte differentiation is present in the brain in a more biological context.
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Results |
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Induction of astrocyte stellation by asialofetuin-bound fraction of rat brain
Previously, we revealed that DSA induced astrocyte differentiation from an immature polygonal shape to a matured stellate shape (Sasaki and Endo, 2000
). We wanted to determine whether a similar molecule with the same carbohydrate-binding specificity and differential activity of astrocytes is present in the brain. Because DSA can be purified from the seeds of D. stramonium by using an asialofetuin-affinity column (Cummings and Kornfeld, 1984; Yamashita et al., 1987), we applied whole rat brain homogenate to an asialofetuin column and obtained both the passed-through and bound fractions. Primary astrocytes were exclusively stained by anti-GFAP antibody and had a flat and polygonal shape (Figure 1A). Though most astrocytes bore more than three processes by 12 h after adding the asialofetuin-bound fraction (Figure 1B), the passed-through fraction did not induce any morphological change (Figure 1C). After adding the bound fraction, the staining intensity by anti-GFAP antibody clearly increased (Figure 1B). On the other hand, adding the passed-through fraction did not cause an increase in staining intensity (Figure 1C). These results indicate that astrocyte differentiation was induced by one or more molecules in rat brain that bound to the asialofetuin column.
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Identification of asialofetuin-binding proteins in brain
As shown by sodium dodecyl sulfate–polyacrylamide gel electrophoresis (SDS–PAGE) (Figure 1D), the asialofetuin-bound fraction contained a protein with a molecular weight of 14–15 kDa. These results suggested that this molecule is an endogenous lectin with a carbohydrate-binding specificity similar to that of DSA. DSA is known to bind to Galß1-4GlcNAcß1-6Man
1 branching multiantennary complex-type sugar chains or to two or more linear N-acetyllactosamine repeats (Cummings and Kornfeld, 1984; Yamashita et al., 1987). On the other hand, galectins, which are animal lectins that specifically bind to ß-galactosides, including linear N-acetyllactosamine repeats, are widely distributed in animals from lower invertebrates to higher vertebrates (Hirabayashi et al., 2002). Among them, the prototype of galectin (galectin-1) is comprised of small subunits (carbohydrate recognition domains) of about 14–16 kDa (Hirabayashi et al., 2002). This raised the possibility that the 14–16-kDa protein in Figure 1D is a kind of galectin. This was confirmed by its reacting with anti-galectin-1 antibody (Figure 1E). These results suggest that the 14–16 kDa protein is galectin-1.
Induction of morphological changes of astrocytes by galectin-1
To examine the ability of galectin-1 to induce astrocyte differentiation, recombinant human galectin-1 was added to an immature astrocyte culture. A dose-response analysis demonstrated that galectin-1 was able to induce morphological changes in astrocytes at a concentration of 10 µM (Figure 2A). This is similar to the concentration of galectin-1 needed for apoptosis of T cells (Perillo et al., 1995). Because the dimeric form of galectin-1 was required for induction of T-cell apoptosis (Perillo et al., 1995) and the Kd for the monomer-dimer of galectin-1 is 7 µM (Cho and Cummings, 1995), the results indicate that galectin-1 is also acting in a dimeric form in its induction of stellation. Addition of recombinant galectin-1–induced astrocyte morphological changes and an increase in the intensity of staining by anti-GFAP antibody (Figure 2B and 2C). No DNA fragmentation was observed (data not shown), indicating that galectin-1 did not induce apoptosis of astrocytes. GFAP is expressed exclusively in astrocytes, and the expression level increases during differentiation (Bovolenta et al., 1984). Expression of GFAP was increased 50-fold following the addition of galectin-1 (Figure 2F). Differentiated astrocytes are characterized by a stellate cell morphology, increased GFAP expression, and inhibited proliferation (Bovolenta et al., 1984; Hatten, 1984). The appearance of all of these characteristics after the addition of galectin-1 strongly indicates that galectin-1 induced astrocyte differentiation.
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The stellate astrocytes appeared about 10 h after the addition of galectin-1. Astrocyte stellation was inhibited by lactose (Figure 2E) but not by maltose, suggesting that astrocyte stellation was induced by galectin-1 in a sugar-specific manner.
Galectin-1 loses its carbohydrate-binding activity after oxidation (Tracey et al., 1992). The ability of lactose to specifically inhibit the morphological changes of astrocytes suggested that the carbohydrate-binding activity of galectin-1 was involved in astrocyte stellation. This hypothesis was confirmed by the use of an oxidation-resistant galectin-1, C2S, in which the second cysteine residue is changed to serine. C2S is considerably more stable than wild-type galectin-1 under nonreducing conditions (Hirabayashi and Kasai, 1991). Although C2S induced astrocyte differentiation (Figure 2D), wild-type galectin-1 left for a day did not show any activity. These results indicated that the carbohydrate-binding activity of galectin-1 was essential for induction of astrocyte differentiation. It should be noted that induction of astrocyte stellation by galectin-1 was irreversible. After 1 h exposure to galectin-1, replacing the medium with galectin-1-free medium did not cause the cells to revert to their former polygonal state.
Effect of galectin-1 on the proliferation of cultured astrocytes
Recombinant human galectin-1 inhibited astrocyte proliferation (Figure 2G). The doubling time of astrocytes in culture was around 4.5 days. After the addition of recombinant galectin-1 or C2S, however, astrocyte proliferation was almost completely arrested.
Effect of various inhibitors of signal transduction on astrocyte stellation induced by galectin-1
To elucidate the signal transduction events that occur after galectin-1 binding, we examined the effects of various signal transduction inhibitors (Table I). PKA (protein kinase A) is thought to be involved in astrocyte stellation (Goldman and Chiu, 1984), but KT5720, an inhibitor of PKA, did not inhibit galectin-1-induced stellation, indicating that PKA is not involved in astrocyte stellation induced by galectin-1. In addition, genistein, a tyrosine kinase inhibitor, was not effective at inhibiting galectin-1-induced astrocyte stellation. However, orthovanadate, an inhibitor of protein tyrosine phosphatase (PTP) almost completely inhibited the stellation of astrocytes. These results indicate that PTP is involved in the induction of astrocyte differentiation by galectin-1. On the contrary, in the case of apoptosis of activated T cells by galectin-1, the PTP activity is down-regulated (Hernandez and Baum, 2002; Lowe, 2001). These observations suggest that galectin-1 binding modulates PTP activity positively or negatively depending on the cell type.
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Detection of dephosphorylated proteins by anti-phosphotyrosine antibody
To investigate which protein is dephosphorylated by PTP during astrocyte differentiation induced by galectin-1, the reactivity of galectin-1-treated cells with anti-phosphotyrosine antibody was examined (Figure 3). As early as 1 min after treatment, the phosphorylation level of several proteins was decreased. A band around 38 kDa and several bands around 85 kDa were immediately dephosphorylated after the addition of galectin-1. A band around 65 kDa was dephosphorylated gradually and disappeared 540 min later. On the other hand, a band around 75 kDa showed immediate enhanced tyrosine phosphorylation, and then the phosphorylation level was decreased gradually. These results suggest that differentiation of astrocytes induced by galectin-1 involves tyrosine dephosphorylation of several unidentified proteins. It will be important to determine these substrates of PTP involved in the signal transduction after galectin-1 binding to understand the mechanisms of astrocyte differentiation.
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Increased production of BDNF after the addition of galectin-1
BDNF is necessary for neuron proliferation, differentiation, and survival in brain (Barde, 1989
; Poo, 2001). Stellate astrocytes, which immediately appear at the site of brain lesion by ischemia or other brain injury (Isackson et al., 1991; Rocamora et al., 1992), are thought to produce several neurotrophic factors to protect neurons from delayed postlesion death (Bresjanac and Antauer, 2000; Dougherty et al., 2000; Miyazaki et al., 2001; Stadelmann et al., 2002). The production of BDNF greatly increased about 1 day after the addition of galectin-1 (Figure 4A), after the change to the stellate form. C2S also enhanced BDNF production. BDNF production remained high for at least 5 days. A densitometric evaluation of the blot indicated that the amount of BDNF after the addition of galectin-1 or C2S increased more than several thousand-fold relative to the amount in the control cells. Because the expression of BDNF mRNA was increased in differentiated astrocytes (Figure 4B), production of BDNF during astrocyte differentiation may be regulated at the transcriptional level. These results conclusively demonstrate that the expression of BDNF is augmented in galectin-1-activated astrocytes.
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Discussion |
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BDNF was released acutely from astrocytes following activation by galectin-1. Astrocytes such as these might be the source of BDNF in injured brain. Considered together, these results indicate that galectin-1 induced up-regulation of BDNF and suggest that galectin-1-induced astrocyte differentiation has a crucial role in the brain. Although galectin-1 induced production of BDNF, it did not induce production of nerve growth factor, neurotrophin-3, ciliary neurotrophic factor, or glial cell line–derived neurotrophic factor (Sasaki and Endo, unpublished data). CNS injury stimulates the expression of several neurotrophic factors to protect neurons from delayed postlesion death (Aliaga et al., 2000
; Isackson et al., 1991; Rocamora et al., 1992; Yurek and Fletcher-Turner, 2001), and reactive astrocytes were revealed to produce those factors (Bresjanac and Antauer, 2000; Dougherty et al., 2000; Miyazaki et al., 2001; Stadelmann et al., 2002). Our results seem to indicate that astrocytes that differentiate in response to galectin-1 produce only BDNF. However, the possibility that such astrocytes produce very small amounts of other neurotrophic cannot be ruled out.
Induction of astrocyte differentiation is a new function of galectin-1. Galectin-1 has previously been associated with many cellular functions, including development, differentiation, immunity, and apoptosis (Cooper, 2002; Hirabayashi et al., 2002; Lowe, 2001). Galectin-1 is present in the CNS (Caron et al., 1987; Hynes et al., 1990; Joubert et al., 1989; Kuchler et al., 1989). Immunochemistry showed that galectin-1 was expressed in both neuronal cells and nonneuronal cells, including astrocytes in rat brain (Joubert et al., 1989; Kuchler et al., 1989). Those cells might be the source of galectin-1 when the brain was injured. In galectin-1-null mice, neurite outgrowth and targeting of olfactory neurons was altered, demonstrating a role for galectin-1 in neural development (Puche et al., 1996). However, the effect of brain injury in galectin-1-null mice was not studied. On the other hand, in the peripheral nervous system, only the oxidized form of galectin-1 promoted axonal regeneration (Horie et al., 1999). Because the reduced form did not show such activity, the carbohydrate-binding activity of galectin-1 was not necessary for axonal regeneration. On the contrary, as shown in this study, the carbohydrate-binding activity of galectin-1 was essential for astrocyte differentiation and BDNF production. Together these results indicate that galectin-1 is a bifunctional protein and plays different roles depending on whether it is in the oxidized or reduced form.
Probable substrates of PTP that are believed to be involved in the signal transduction after stimulation by galectin-1 remain to be determined. Immunoblotting with anti-phosphotyrosine antibody revealed that the staining intensity of several protein bands was markedly decreased after the addition of galectin-1 (Figure 3). Especially, the band around 38 kDa and several bands around 85 kDa were immediately dephosphorylated after the addition of galectin-1. These proteins remain to be identified. Tyrosine residues of proteins are phosphorylated and dephosphorylated by the action of tyrosine kinase and PTP, respectively. Galectin-1-induced astrocyte stellation was not affected by genistein but significantly blocked by the tyrosine phosphatase inhibitor orthovanadate (Table I). These results suggest that PTP activity is necessary for the induction of astrocyte stellation by galectin-1 and that galectin-1-triggered astrocyte differentiation is predominantly through a tyrosine dephosphorylation pathway.
Our results show that galectin-1 triggers differentiation, and then the differentiated astrocytes greatly increase their production of BDNF. Galectin-1 induces these phenomena through its carbohydrate-binding activity. This novel role of galectin-1 in brain raises the possibility that it might eventually have applications in the prevention of neuronal loss, such as what occurs in CNS injuries.
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Materials and methods |
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Materials
Rabbit anti-BDNF polyclonal antibody and sodium orthovanadate were obtained from Sigma (St. Louis, MO). Kanamycin sulfate, Dulbecco's modified Eagle's medium (DMEM), and fetal bovine serum (FBS) were obtained from Gibco BRL (Grand Island, NY). Phenylmethylsulfonyl fluoride, leupeptin hemisulfate, aprotinin, bovine serum albumin, 3,3'-diaminobenzidine, and pepstatin A were obtained from Nacalai Tesque (Kyoto, Japan). Peroxidase-conjugated avidin (Vectastain ABC kit) was purchased from Vector Laboratories (Burlingame, CA). Polyclonal rabbit antiserum raised against galectin-1 from human placenta was prepared as described previously (Hirabayashi et al., 1987
). Anti-GFAP antibody and anti-phosphotyrosine monoclonal antibody (clone 4G10) were obtained from Dako (Carpinteria, CA) and Upstate Biotechnology (Lake Placid, NY). The peroxidase-linked F(ab')2 fragment of anti-rabbit IgG was obtained from Amersham Biosciences (Piscataway, NJ). Anti-mouse IgG antibody conjugated with peroxidase-labeled dextran were obtained from Dako. KT5720 and genistein were obtained from Calbiochem-Novabiochem (La Jolla, CA).
Asialofetuin-binding proteins from rat brain
Asialofetuin was coupled to an AF-Tresyl-Toyopearl gel according to the instructions of the manufacturer (Tosoh, Tokyo) using 50 mg asialofetuin and 1 g AF-Tresyl-Toyopearl gel resin, and more than 90% of the protein had coupled to the gel.
Adult rat brains were homogenized with 10 ml/g wet tissue of cold 4 mM 2-mercaptoethanol and 0.1 M phosphate buffered saline (pH 7.4) containing 2 mM ethylenediaminetetraacetic acid (EDTA) (buffer A) in a Potter homogenizer. The homogenate was centrifuged at 100,000 x g for 1 h at 4°C. The obtained precipitate was moved to buffer A with 100 mM lactose and stirred at 4°C for 12 h. The solution was centrifuged at 100,000 x g for 1 h at 4°C, and the supernatant was dialyzed against buffer A to remove lactose completely. Then the solution (2.2 mg protein) was applied to an asialofetuin immobilized column (5 ml volume). After extensive washing of the column with buffer A, the bound proteins were eluted with buffer A containing 100 mM lactose. Asialofetuin-nonbinding fraction (2.1 mg protein) and asialofetuin-binding fraction (5 µg protein) were obtained. Both asialofetuin-binding and -nonbinding fractions were concentrated to 4 ml. Forty microliters and 4 µl each were applied to SDS–polyacrylamide gel with silver staining and immunoblot stained with anti-galectin-1, respectively. Buffer of remaining both fractions was changed to DMEM with an Ultrafree-4 Centrifugal Filter Unit having a Biomax-10 filter (Millipore, Billerica, MA), and each fraction was added to cultured astrocytes.
Recombinant galectin-1 and mutant protein, C2S
Recombinant galectin-1 and its mutant galectin-1 (termed C2S), in which the second cysteine residue was changed to serine, were produced as described by Hirabayashi and Kasai (1991). C2S is substantially resistant to oxidative inactivation while preserving carbohydrate-binding activity.
Cell cultures of astrocytes
Pregnant Fischer rats (F344/N Slc) were obtained from Japan SLC (Shizuoka). Astrocytes were prepared from the cerebellums of postnatal day 5 rats as described previously (Sasaki and Endo, 2000). None of the cells were labeled by anti-neurofilament antibody, a specific marker of neurons, and most were labeled by the anti-GFAP antibody, a specific astrocyte marker. Cells were subcultured at a 1:4 ratio every 8 days to obtain a highly homogenous astrocyte preparation.
Changes in cell morphology were assessed under a microscope (TE300, Nikon, Tokyo) with a Hoffman Modulation Contrast module (Nikon). Cells were seeded in 12-well plates (Asahi Techno glass, Tokyo) at a density of 5x 103 cells per cm2. The cells were cultured with media containing 10% FBS. Three days before the experiments, the medium was changed to FBS-free medium. Cells having three or more processes at least twice as long as the diameter of the cell body were defined as stellate. Results are expressed as the percentages of stellate cells relative to the total cell count. A cell proliferation assay and immunostaining with anti-GFAP were performed as described (Sasaki and Endo, 2000).
SDS–PAGE and immunoblotting
The cells in the culture dish were washed three times with ice-cold phosphate buffered saline, and detached and homogenized with 1% SDS in 10 mM Tris–HCl buffer, pH 7.4, containing 1 mM phenylmethylsulfonyl fluoride, 10 µM leupeptin, 1 µM aprotinin, 1 µM pepstatin A. and 1 mM EDTA for the anti-GFAP blotting. To homogenize the cells for the anti-phosphotyrosine blotting, 2 mM sodium orthovanadate and 10 mM sodium fluoride were added to the buffer. Conditioned media were 40 times concentrated with a Biomax-10 filter. Ten-microliter samples were also subjected to SDS–PAGE. Proteins were separated by 15% SDS–PAGE according to Laemmli (1970) and then electroblotted onto a polyvinyl difluoride (PVDF) membrane (Millipore) as described (Sasaki and Endo, 2000). Protein concentration was determined with a BCA protein assay kit (Pierce, Rockford, IL). GFAP, galectin-1, phosphotyrosine, or BDNF was detected with anti-GFAP antibody, anti-galectin-1 antiserum, anti-phosphotyrosine antibody, or anti-BDNF antibody, respectively, with an ECL kit (Amersham Biosciences). Band intensities were measured by densitometric scanning using a densitometer and NIH Image 1.61/ppc software.
Reverse transcription polymerase chain reaction
Cultured immature astrocytes were incubated with or without 10 µM recombinant galectin-1 for 24 h. Total RNA was isolated from cells using Isogen (Nippon Gene, Toyama). First-strand cDNA was synthesized using SuperScript III RNase H–, Reverse Transcriptase (Invitrogen, Carlsbad, CA) and polymerase chain reaction (PCR) was performed with KOD DNA polymerase (KOD plus, Toyobo, Osaka) according to the manufacture's instruction. The following primers were used (forward and backward, respectively): BDNF, 5'-cactccgaccctgcccgccg-3' and 5'-tccactatcttcccctttta-3' (Guo et al., 2002) and glyceraldehyde 3-phosphate dehydrogenase (G3PDH), 5'-tgaaggtcggtgtcaacggatttggc-3' and 5'-catgtaggccatgaggtccaccac-3' (Tso et al., 1985). Cycling was preceded by 2 min at 94°C and followed by 10 min at 72°C and performed as follows: 15 s at 94°C, 30 s at annealing temperature, 1 min at 72°C. Annealing temperature was 61°C for G3PDH and 54°C for BDNF. PCR products were calculated to a length of 983 bp (G3PDH) and 364 bp (BDNF). Five microliters of each amplification reaction were resolved on a 1% agarose gel.
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Acknowledgements |
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This study was supported by a Grant-in-Aid for Scientific Research on Priority Area (14082209) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.
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Footnotes |
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1 To whom correspondence should be addressed; e-mail: endo{at}tmig.or.jp
2 Present address: Glycostructure Analysis Team, Research Center for Glycoscience, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba Central 6, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8566, Japan 
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Abbreviations |
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CNS, central nervous system; BDNF, brain-derived neurotrophic factor; DMEM, Dulbecco's modified Eagle's medium; DSA, Datura stramonium agglutinin; EDTA, ethylenediaminetetraacetic acid; FBS, fetal bovine serum; G3PDH, glyceraldehyde 3-phosphate dehydrogenase; GFAP, glial fibrillary acidic protein; PCR, polymeras chain reaction; PTP, protein tyrosine phosphatase; PVDF, polyvinylidene difluoride; SDS–PAGE, sodium dodecyl sulfate–polyacrylamide gel electrophoresis
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