Differential Responses of Retinal Neurons and Glia Revealed via Proteomic Analysis on Primary and Secondary Retinal Ganglion Cell Degeneration
<p>Workflow diagram for SWATH and bioinformatics analysis. Four biological samples of temporal and nasal quadrants at three time points (1 wk, 4 wk, and 8 wk) were pooled to form six representative samples. Technical duplicates were included. Two micrograms of digested peptides were identified via ProteinPilot (PP) and quantified via the OneOmics Cloud platform. Subsequent bioinformatics analysis was performed using iPathwayGuide.</p> "> Figure 2
<p>Volcano plot of retinal proteins quantified using SWATH-MS (shown in gene names) in samples at 1 wk (<b>A</b>), 4 wk (<b>B</b>), and 8 wk (<b>C</b>) after pONT. The horizontal axis is the log<sub>2</sub>(Fold Change), and the vertical axis is the negative log10 value of the <span class="html-italic">p</span>-value. The dashed lines represent the threshold (0.43 and −0.43 for the <span class="html-italic">x</span>-axis and 1.30 for the <span class="html-italic">y</span>-axis). The upregulated proteins (log<sub>2</sub>FC ≥ 0.43 and <span class="html-italic">p</span> < 0.05) are shown in red, while the downregulated proteins (log<sub>2</sub>FC ≤ −0.43 and <span class="html-italic">p</span> < 0.05) are in blue. Names of regulated proteins shared by 2 time points are shown. Fold changes in all groups are calculated by comparing temporal compared to nasal quadrants (T/N).</p> "> Figure 3
<p>Comparison of differentially expressed proteins among three time points (1 wk, 4 wk, and 8 wk) after pONT. Venn diagram showed that one common protein was shared by 1 wk and 4 wk while seven common proteins were shared by 4 wk and 8 wk. The different colors indicate different time points: 1-week (blue); 4-week (red); 8-week (green). Significantly expressed proteins were considered if the following criteria were met: <span class="html-italic">p</span>-value < 0.05, log<sub>2</sub>FC ≥ 0.43 or ≤−0.43, and confidence ≥ 0.70.</p> "> Figure 4
<p>Expression levels of eight proteins that were differentially expressed when compared temporal retinal quadrant to nasal retinal quadrant using the SWATH-MS approach for at least 2 time points among 1 wk, 4 wk, and 8 wk after pONT. The proteins with log<sub>2</sub>FC > 0 are shown in red, while the proteins with log<sub>2</sub>FC < 0 are in blue. The dashed lines represented the <span class="html-italic">y</span>-axis as 0.43 or −0.43. * <span class="html-italic">p</span> < 0.05, ** <span class="html-italic">p</span> < 0.01.</p> "> Figure 5
<p>Immunohistochemistry of gamma-synuclein (SNCG) after pONT. Loss of gamma-synuclein immuno-positive nerve fiber (arrowhead) was noted in the temporal retina as early as 1 week up to 8 weeks, while mild loss was observed in the nasal retina at 4 weeks. After pONT, the remaining fibers (red) appeared to be thinner compared to the control. Red = gamma-synuclein; blue = DAPI. RGCL = retinal ganglion cell layer; IPL = inner plexiform layer; INL = inner nuclear layer; OPL = outer plexiform layer; ONL = outer nuclear layer.</p> "> Figure 6
<p>Localization of gamma-synuclein (SNCG) at 8 weeks after pONT. In control retina, gamma–synuclein was expressed by the nerve fibers (red) but not RBPMS-positive RGC bodies (green). After pONT, loss of gamma-synuclein immunolabeling (arrowheads) and dropout of RBPMS-positive cells was more apparent in the temporal retina. Red = gamma–synuclein; green = RBPMS; blue = DAPI. NFL = nerve fiber layer; RGCL = retinal ganglion cell layer.</p> "> Figure 7
<p>Immunohistochemistry of glial fibrillary acidic protein (GFAP) after pONT. Expression of GFAP was noted in the inner limiting membrane of the control retina. GFAP expression levels were progressively increased, and the processes extended to the inner plexiform layer (*), inner nuclear layer (#) and outer nuclear layer (<span>$</span>) in the temporal retina at 8 weeks. GFAP labeled processes extended up to INL of the nasal retina at 8 weeks. Red = GFAP; Blue = DAPI. RGCL = retinal ganglion cell layer; IPL = inner plexiform layer; INL = inner nuclear layer; OPL = outer plexiform layer; ONL = outer nuclear layer.</p> "> Figure 8
<p>Double labeling of GFAP and S100 at 8 weeks after pONT. Colocalization of GFAP and S100 was found in the inner limiting membrane of the control retina (arrowheads) but some processes were not labeled by S100 (*). At 8 weeks after pONT, there was colocalization of GFAP and S100 at Muller cell processes in the ONL of temporal retinal quadrant (arrows) and a few processes in the INL of nasal quadrant (arrows). Red = GFAP; Green = S100; Blue = DAPI. RGCL = retinal ganglion cell layer; IPL = inner plexiform layer; INL = inner nuclear layer; OPL = outer plexiform layer; ONL = outer nuclear layer.</p> "> Figure 9
<p>Change in ALDH1A1 expression pattern after pONT. Decreased immunoreactivity was noted in NFL (arrowheads) of both temporal and nasal retina after pONT. More ALDH1A1 labeled cell bodies in INL and processes in ONL (arrows) were found in the temporal retina. Green = ALDH1A1; Blue = DAPI. RGCL = retinal ganglion cell layer; IPL = inner plexiform layer; INL = inner nuclear layer; OPL = outer plexiform layer; ONL = outer nuclear layer.</p> ">
Abstract
:1. Introduction
2. Results
3. Discussion
4. Materials and Methods
4.1. Animals and Partial Optic Nerve Transection (pONT)
4.2. Rat Retinal Harvest and Protein Extraction
4.3. Protein Reduction, Alkylation, and Digestion
4.4. Data Dependent Acquisition (DDA) and SWATH-MS Acquisition
4.5. SWATH-MS and Statistical Analysis
4.6. Bioinformatics Analysis
4.7. Tissue Processing and Immunohistochemistry
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Groups | Protein | Peptide | Differentially Expressed Proteins ** |
---|---|---|---|
Individual search-1 wk | 2023 | 12,543 | 10/2208 (8 upregulated and 2 downregulated) |
Individual search-4 wk | 2173 | 13,715 | 25/2208 (16 upregulated and 9 downregulated) |
Individual search-8 wk | 2185 | 13,951 | 61/2208 (47 upregulated and 14 downregulated) |
Combined search (1, 4, and 8 wk) * | 2531 | 18,871 | N/A |
Uniprot ID | Gene Name | Protein Name | FC (T/N) | log2FC | Confidence | p |
---|---|---|---|---|---|---|
Upregulation | ||||||
D4A8G0 | Lsm12 | LSM12 homolog | 9.12 | 3.19 | 0.84 | 0.01 |
Q1W1V7 | N/A | Liver cancer-related protein | 6.33 | 2.66 | 0.88 | 0.01 |
A0A0H2UHP1 | Aldh1a1 | Aldehyde dehydrogenase 1A1 | 5.60 | 2.49 | 0.84 | 0.01 |
B2GV57 | Cars2 | cysteine-tRNA ligase | 5.03 | 2.33 | 0.80 | 0.04 |
A0A8I5ZSA8 | ENSRNOG00000069233 | Histone H2B | 3.34 | 1.74 | 0.91 | 0.03 |
P69897 | Tubb5 | Tubulin beta-5 chain | 2.60 | 1.38 | 0.82 | 0.00 |
Q6PED0 | Rps27a | Ubiquitin-40S ribosomal protein S27a | 1.78 | 0.83 | 0.93 | 0.03 |
A0A0G2K2S2 | Slc2a1 | Solute carrier family 2, facilitated glucose transporter member 1member 1 | 1.48 | 0.57 | 0.77 | 0.03 |
Downregulation | ||||||
A0A0H2UHU0 | Rps25 | 40S ribosomal protein S25 | 0.38 | −1.41 | 0.72 | 0.02 |
Q91XU7 | Cdhr1 | Cadherin-related family member 1 | 0.11 | −3.20 | 0.79 | 0.03 |
Uniprot ID | Gene Name | Protein Name | FC (T/N) | log2FC | Confidence | p |
---|---|---|---|---|---|---|
Upregulation | ||||||
B5DEZ3 | Ccdc126 | Ccdc126 protein | 17.25 | 4.11 | 0.71 | 0.04 |
Q91ZE7 | N/A | Anion exchange protein | 8.58 | 3.10 | 0.70 | 0.00 |
Q5M842 | IgG-2a | IgG-2a protein | 8.13 | 3.02 | 0.70 | 0.03 |
Q05175 | Basp1 | Brain acid-soluble protein 1 | 3.36 | 1.75 | 0.80 | 0.04 |
A0A0H2UHP1 | Aldh1a1 | Aldehyde dehydrogenase 1A1 | 2.49 | 1.32 | 0.89 | 0.00 |
P18437 | Hmgn2 | Non-histone chromosomal protein HMG-17 | 2.19 | 1.13 | 0.72 | 0.01 |
Q499T3 | Sirpa | Sirpa protein | 1.89 | 0.92 | 0.72 | 0.04 |
W4VSR7 | Try10 | RCG64520 | 1.74 | 0.80 | 0.85 | 0.04 |
A0A0G2K2V6 | Krt10 | Keratin, type I cytoskeletal 10 | 1.71 | 0.77 | 0.75 | 0.01 |
A0A0G2JSY7 | Rho | Rhodopsin | 1.70 | 0.77 | 0.84 | 0.00 |
A0A0H2UHW4 | Pcnp | PEST proteolytic signal-containing nuclear protein | 1.66 | 0.73 | 0.70 | 0.04 |
D4A3K5 | H1-1 | Histone H1.1 | 1.59 | 0.67 | 0.88 | 0.01 |
P47819 | Gfap | Glial fibrillary acidic protein | 1.57 | 0.65 | 0.87 | 0.03 |
A0A0G2JSH5 | Alb | Albumin | 1.57 | 0.65 | 0.82 | 0.02 |
Q6PDU6 | Hbb-b1 | Beta-glo | 1.50 | 0.59 | 0.82 | 0.03 |
K7S2S2 | Hist2h2aa3 | Histone H2A | 1.43 | 0.52 | 0.79 | 0.01 |
Downregulation | ||||||
Q6P3E1 | Rps16 | Rps16 protein | 0.74 | −0.43 | 0.70 | 0.03 |
D3ZK97 | H3f3c | Histone H3 | 0.74 | −0.43 | 0.99 | 0.01 |
P47728 | Calb2 | Calretinin | 0.67 | −0.58 | 0.75 | 0.00 |
Q8CFN2 | Cdc42 | Cell division control protein 42 homolog | 0.58 | −0.79 | 0.75 | 0.04 |
A0A0G2K0T6 | Sncg | Gamma-synuclein | 0.37 | −1.44 | 0.87 | 0.04 |
P19527 | Nefl | Neurofilament light polypeptide | 0.34 | −1.56 | 0.81 | 0.00 |
Q5XI38 | Lcp1 | Lymphocyte cytosolic protein 1 | 0.13 | −2.92 | 0.81 | 0.03 |
Q3B7U9 | Fkbp8 | Peptidyl-prolyl cis-trans isomerase FKBP8 | 0.13 | −2.98 | 0.70 | 0.03 |
G3V9E4 | Apeh | Acylamino-acid-releasing enzyme | 0.08 | −3.59 | 0.71 | 0.04 |
Uniprot ID | Gene Name | Protein Name | FC (T/N) | log2FC | Confidence | p |
---|---|---|---|---|---|---|
Upregulation | ||||||
Q5M8C3 | Serpina4 | Serine (Or cysteine) proteinase inhibitor, clade A (Alpha-1 antiproteinase, antitrypsin), member 4 | 13.76 | 3.78 | 0.70 | 0.00 |
Q6YDN7 | Cdc26 | Anaphase-promoting complex subunit CDC26 | 7.80 | 2.96 | 0.81 | 0.03 |
Q5EB90 | Polr2c | Polymerase (RNA) II | 7.73 | 2.95 | 0.80 | 0.02 |
P23928 | Cryab | Alpha-crystallin B chain | 2.42 | 1.27 | 0.89 | 0.00 |
P10068 | Crygf | Gamma-crystallin F | 2.20 | 1.14 | 0.98 | 0.00 |
A0A0H2UHM3 | Hp | Haptoglobin | 2.17 | 1.12 | 0.89 | 0.00 |
P62697 | Crybb2 | Beta-crystallin B2 | 2.17 | 1.12 | 0.95 | 0.00 |
A0JN13 | Cryaa | Alpha-crystallin A chain | 2.14 | 1.10 | 0.86 | 0.00 |
Q8CGQ0 | Cryba2 | BetaA2-crystallin | 2.12 | 1.08 | 0.96 | 0.04 |
P02767 | Ttr | Transthyretin | 2.11 | 1.08 | 0.86 | 0.01 |
P62329 | Tmsb4x | Thymosin beta-4 | 2.07 | 1.05 | 0.78 | 0.00 |
P02524 | Crybb3 | Beta-crystallin B3 | 1.95 | 0.97 | 0.88 | 0.02 |
P02523 | Crybb1 | Beta-crystallin B1 | 1.94 | 0.96 | 0.87 | 0.02 |
Q8CHN7 | Pcp4 | Calmodulin regulator protein PCP4 | 1.92 | 0.94 | 0.86 | 0.00 |
P63249 | Pkia | cAMP-dependent protein kinase inhibitor alpha | 1.89 | 0.92 | 0.89 | 0.03 |
Q62785 | Pdap1 | 28 kDa heat- and acid-stable phosphoprotein | 1.86 | 0.90 | 0.77 | 0.02 |
P14881-2 | Cryba1 | Beta-crystallin A3 | 1.83 | 0.87 | 0.88 | 0.00 |
P02770 | Alb | Albumin | 1.81 | 0.86 | 0.85 | 0.02 |
B0K010 | Txndc17 | Thioredoxin domain-containing protein 17 | 1.81 | 0.86 | 0.70 | 0.02 |
A0A0G2JZ73 | Serpina1 | Alpha-1-antiproteinase | 1.78 | 0.83 | 0.82 | 0.01 |
A0A0G2K376 | Fip1l1 | Pre-mRNA 3′-end-processing factor FIP1 | 1.75 | 0.80 | 0.70 | 0.01 |
Q6PDU6 | Hbb-b1 | Beta-glo | 1.70 | 0.77 | 0.80 | 0.04 |
A0A1K0FUA6 | LOC100134871 | Globin a2 | 1.69 | 0.76 | 0.83 | 0.03 |
P14046 | A1i3 | Alpha-1-inhibitor 3 | 1.68 | 0.75 | 0.84 | 0.01 |
P20059 | Hpx | Hemopexin | 1.66 | 0.73 | 0.85 | 0.03 |
Q923W4 | Hdgfl3 | Hepatoma-derived growth factor-related protein 3 | 1.63 | 0.71 | 0.84 | 0.02 |
D3ZXP8 | Pcp2 | Purkinje cell protein 2 | 1.61 | 0.69 | 0.87 | 0.00 |
W4VSR7 | Try10 | RCG64520 | 1.59 | 0.67 | 0.84 | 0.01 |
P14841 | Cst3 | Cystatin-C | 1.58 | 0.66 | 0.99 | 0.01 |
B4F758 | Hmgb1 | High mobility group protein B1 | 1.57 | 0.65 | 0.78 | 0.02 |
D4A9Z8 | Chmp4bl1 | Chromatin-modifying protein 4B-like 1 | 1.57 | 0.65 | 0.73 | 0.02 |
A0A0G2K6H5 | Cfdp1 | Craniofacial development protein 1 | 1.55 | 0.64 | 0.80 | 0.01 |
P47819 | Gfap | Glial fibrillary acidic protein | 1.55 | 0.63 | 0.85 | 0.01 |
Q05175 | Basp1 | Brain acid soluble protein 1 | 1.53 | 0.61 | 0.72 | 0.04 |
P26772 | Hspe1 | 10 kDa heat shock protein, mitochondrial | 1.51 | 0.59 | 0.79 | 0.00 |
A0A0G2JSW3 | Hbb | Hemoglobin subunit beta-1 | 1.46 | 0.55 | 0.78 | 0.01 |
P11030 | Dbi | Acyl-CoA-binding protein | 1.46 | 0.54 | 0.86 | 0.04 |
Q4KLJ1 | Sfrs7 | RCG61762, isoform CRA_a | 1.42 | 0.51 | 0.88 | 0.01 |
P31044 | Pebp1 | Phosphatidylethanolamine-binding protein 1 | 1.41 | 0.49 | 0.82 | 0.04 |
D4A6E3 | Mug1 | Murinoglobulin-1 | 1.38 | 0.47 | 0.78 | 0.02 |
F1LNF1 | Hnrnpa2b1 | Heterogeneous nuclear ribonucleoproteins A2/B1 | 1.38 | 0.47 | 0.84 | 0.03 |
D3ZM85 | Cplx4 | Complexin 4 | 1.38 | 0.46 | 0.71 | 0.02 |
P55053 | Fabp5 | Fatty acid-binding protein 5 | 1.37 | 0.45 | 0.73 | 0.01 |
Q6P6G9 | Hnrnpa1 | Heterogeneous nuclear ribonucleoprotein A1 | 1.36 | 0.45 | 0.77 | 0.01 |
D4ABK7 | Hnrnph3 | Heterogeneous nuclear ribonucleoprotein H3 | 1.36 | 0.45 | 0.78 | 0.02 |
P11240 | Cox5a | Cytochrome c oxidase subunit 5A | 1.36 | 0.45 | 0.79 | 0.02 |
B1WBQ0 | Cdc5l | CDC5 cell division cycle 5-like | 1.35 | 0.43 | 0.80 | 0.02 |
Downregulation | ||||||
P68370 | Tuba1a | Tubulin alpha-1A chain | 0.74 | −0.43 | 0.99 | 0.02 |
D3ZC55 | Hspa12a | Heat shock 70kDa protein 12A (Predicted), isoform CRA_a | 0.73 | −0.46 | 0.73 | 0.03 |
Q8CJD2 | N/A | Guanylate cyclase | 0.72 | −0.47 | 0.81 | 0.03 |
F1M779 | Cltc | Clathrin heavy chain | 0.71 | −0.49 | 0.87 | 0.00 |
C7C5T2 | Pfkp | ATP-dependent 6-phosphofructokinase | 0.69 | −0.53 | 0.76 | 0.00 |
P01830 | Thy1 | Thy-1 membrane glycoprotein | 0.67 | −0.58 | 0.74 | 0.00 |
A0A0G2K0T6 | Sncg | Gamma-synuclein | 0.58 | −0.78 | 0.74 | 0.01 |
D4AE00 | “Obsolete” | “Obsolete” | 0.55 | −0.87 | 0.74 | 0.01 |
Q8K4V4 | Snx27 | Sorting nexin-27 | 0.53 | −0.90 | 0.81 | 0.04 |
P12007 | Ivd | Isovaleryl-CoA dehydrogenase, mitochondrial | 0.50 | −0.99 | 0.77 | 0.03 |
Q8CFN2 | Cdc42 | Cell division control protein 42 homolog | 0.42 | −1.25 | 0.80 | 0.01 |
P19527 | Nefl | Neurofilament light polypeptide | 0.38 | −1.41 | 0.81 | 0.04 |
Q6EV70 | Pofut1 | GDP-fucose protein O-fucosyltransferase 1 | 0.22 | −2.19 | 0.74 | 0.04 |
B1H267 | Snx5 | Sorting nexin-5 | 0.06 | −3.95 | 0.78 | 0.00 |
GO ID | T/N-1 wk | T/N-4 wk | T/N-8 wk | ||||
---|---|---|---|---|---|---|---|
Genes (DE/All) | p | Genes (DE/All) | p | Genes (DE/All) | p | ||
GO term-Biological process | |||||||
lens development in camera-type eye | GO:0002088 | N/A | N/A | 1/14 | 0.364 | 8/14 | 2.4 × 10−6 |
neuron projection regeneration | GO:0031102 | N/A | N/A | 2/16 | 0.089 | 8/16 | 9.1 × 10−6 |
response to wounding | GO:0009611 | 1/78 | 0.915 | 6/79 | 0.036 | 18/79 | 2.0 × 10−5 |
visual system development | GO:0150063 | 1/65 | 0.871 | 7/67 | 0.004 | 15/67 | 1.3 × 10−4 |
sensory system development | GO:0048880 | 1/65 | 0.871 | 7/67 | 0.004 | 15/67 | 1.3 × 10−4 |
eye development | GO:0001654 | 1/65 | 0.871 | 7/67 | 0.004 | 15/67 | 1.3 × 10−4 |
lipid biosynthetic process | GO:0008610 | 1/68 | 0.883 | 1/68 | 0.893 | 15/68 | 1.5 × 10−4 |
negative regulation of endopeptidase activity | GO:0010951 | 4/40 | 0.031 | 3/40 | 0.131 | 11/40 | 1.5 × 10−4 |
negative regulation of peptidase activity | GO:0010466 | 4/41 | 0.034 | 3/41 | 0.139 | 11/41 | 2.0 × 10−4 |
negative regulation of hydrolase activity | GO:0051346 | 4/54 | 0.079 | 4/55 | 0.094 | 13/55 | 2.1 × 10−4 |
GO terms-molecular function | |||||||
structural constituent of eye lens | GO:0005212 | N/A | N/A | 1/12 | 0.325 | 8/12 | 2.9 × 10−7 |
structural molecule activity | GO:0005198 | 7/111 | 0.054 | 6/112 | 0.145 | 23/112 | 2.7 × 10−6 |
serine-type endopeptidase inhibitor activity | GO:0004867 | 2/13 | 0.060 | 3/13 | 0.007 | 6/13 | 1.6 × 10−4 |
endopeptidase inhibitor activity | GO:0004866 | 4/25 | 0.007 | 3/25 | 0.044 | 8/25 | 2.7 × 10−4 |
peptidase inhibitor activity | GO:0030414 | 4/25 | 0.007 | 3/25 | 0.044 | 8/25 | 2.7 × 10−4 |
endopeptidase regulator activity | GO:0061135 | 4/28 | 0.010 | 3/28 | 0.058 | 8/28 | 6.4 × 10−4 |
signaling receptor regulator activity | GO:0030545 | N/A | N/A | 1/18 | 0.445 | 6/18 | 0.001 |
peptidase regulator activity | GO:0061134 | 4/31 | 0.014 | 3/31 | 0.075 | 8/31 | 0.001 |
monosaccharide binding | GO:0048029 | 1/20 | 0.472 | 1/20 | 0.481 | 6/20 | 0.002 |
receptor ligand activity | GO:0048018 | N/A | N/A | N/A | N/A | 5/15 | 0.003 |
GO terms-cellular component | |||||||
extracellular space | GO:0005615 | 7/125 | 0.079 | 9/127 | 0.014 | 28/127 | 1.1 × 10−7 |
extracellular region | GO:0005576 | 9/163 | 0.052 | 12/165 | 0.004 | 30/165 | 3.1 × 10−6 |
hemoglobin complex | GO:0005833 | N/A | N/A | 1/4 | 0.118 | 3/4 | 0.002 |
haptoglobin-hemoglobin complex | GO:0031838 | N/A | N/A | N/A | N/A | 3/4 | 0.002 |
neurofilament | GO:0005883 | N/A | N/A | 1/5 | 0.146 | 3/5 | 0.004 |
presynaptic intermediate filament cytoskeleton | GO:0099182 | N/A | N/A | 1/2 | 0.061 | 2/2 | 0.006 |
intermediate filament | GO:0005882 | 1/19 | 0.444 | 4/19 | 0.002 | 5/19 | 0.013 |
axon | GO:0030424 | 7/209 | 0.449 | 7/211 | 0.486 | 25/211 | 0.017 |
postsynaptic intermediate filament cytoskeleton | GO:0099160 | N/A | N/A | 1/3 | 0.090 | 2/3 | 0.017 |
growth cone membrane | GO:0032584 | N/A | N/A | N/A | N/A | 2/3 | 0.017 |
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Kwong, J.M.K.; Caprioli, J.; Lee, J.C.Y.; Song, Y.; Yu, F.-J.; Bian, J.; Sze, Y.-H.; Li, K.-K.; Do, C.-W.; To, C.-H.; et al. Differential Responses of Retinal Neurons and Glia Revealed via Proteomic Analysis on Primary and Secondary Retinal Ganglion Cell Degeneration. Int. J. Mol. Sci. 2023, 24, 12109. https://doi.org/10.3390/ijms241512109
Kwong JMK, Caprioli J, Lee JCY, Song Y, Yu F-J, Bian J, Sze Y-H, Li K-K, Do C-W, To C-H, et al. Differential Responses of Retinal Neurons and Glia Revealed via Proteomic Analysis on Primary and Secondary Retinal Ganglion Cell Degeneration. International Journal of Molecular Sciences. 2023; 24(15):12109. https://doi.org/10.3390/ijms241512109
Chicago/Turabian StyleKwong, Jacky M. K., Joseph Caprioli, Joanne C. Y. Lee, Yifan Song, Feng-Juan Yu, Jingfang Bian, Ying-Hon Sze, King-Kit Li, Chi-Wai Do, Chi-Ho To, and et al. 2023. "Differential Responses of Retinal Neurons and Glia Revealed via Proteomic Analysis on Primary and Secondary Retinal Ganglion Cell Degeneration" International Journal of Molecular Sciences 24, no. 15: 12109. https://doi.org/10.3390/ijms241512109