Journal of Southern Medical University ›› 2026, Vol. 46 ›› Issue (10): 2357-2371.doi: 10.12122/j.issn.1673-4254.2026.10.06
Qian XU(
), Erqi LIU, Qiaofeng ZHANG, Haixin LIU, Xinpei LIN, Yao LIN()
Received:2025-12-23
Online:2026-10-20
Published:2026-10-26
Contact:
Yao LIN
E-mail:xmuxuqian@163.com;55380098@qq.com
Qian XU, Erqi LIU, Qiaofeng ZHANG, Haixin LIU, Xinpei LIN, Yao LIN. Role of Ddx56 gene associated with early-onset Parkinson disease in maintaining neural development and protecting against dopaminergic neuron apoptosis in zebrafish[J]. Journal of Southern Medical University, 2026, 46(10): 2357-2371.
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URL: https://www.j-smu.com/EN/10.12122/j.issn.1673-4254.2026.10.06
| Gene | Primer (5'-3') |
|---|---|
| Ddx56 | F:TCATCAGCCAGTTCAATCAAGG |
| Galnt13 | F:GTGATTCCCAAAGAAGAGCAGG |
Tab.1 Probe and primer sequences for Ddx56 and Galnt13
| Gene | Primer (5'-3') |
|---|---|
| Ddx56 | F:TCATCAGCCAGTTCAATCAAGG |
| Galnt13 | F:GTGATTCCCAAAGAAGAGCAGG |
| Gene | Primer (5'-3') | Fragment length (bp) |
|---|---|---|
| Galnt13 | F:GTCTTCCTTGCTATACTTCAG GTCTTGGGTCTTCCTCTTGCTATACTTCAG | 259 |
| R:TCGTCTTACAGCCATCCAGC | ||
| Ddx56 | F:AAGGCTCTGGCGGATTTAGG | 181 |
| R:CCTGCTCTCGTACAGTCTGTTT | ||
| F: | 358 | |
| R: | ||
| Sncga | F:GCAGCCGCCAAAACCAAAGA | 134 |
| R:CCAGCCACAGCAGTATCACT | ||
| Sncgb | F:TCCAGAAGACCACCGACCAG | 152 |
| R:TTCCATACCACCATGAGAGA | ||
| Syn2b | F:AGTCATCCCATCCTCTCTTG | 104 |
| R:CTCTGCCTTTGCTTCGTCCT | ||
| Polg | F:GCTCTGGTTTTTGATGTGGA | 182 |
| R:CTGGAGTTTGCGAGGGTTTC | ||
| Dj-1 | F:TGTGAAAGAGGTGTTGAAGG | 120 |
| R:GGATGAGTAGTAACTGTGCT | ||
| Pink1 | F:GTACCTGGAGGTGTGTGTGC | 104 |
| R:CTCTGTGAGCGATGTTTTGT | ||
| Parkin | F:CCATCACCAAAACCACTCAC | 110 |
| R:GCACCACTCGAACTTACACT | ||
| Lrrk2 | F:TATTCGTTCGGTCTGCTGCT | 196 |
| R:TGTCCTGGGGGTTTTCTCTC | ||
| Gba | F:ACCAGGAGGCAAAGAACACA | 198 |
| R:GGACCTAGATCCAGGGCAAT | ||
| β-Synucleins (Sncb) | F:CAGCAAGACCAAAGACAGCG | 170 |
| R:TGGCTTCCTGACCAAACTCC |
Tab.2 Primer sequences for real-time quantitative PCR for Parkinson disease (PD)-associated genes
| Gene | Primer (5'-3') | Fragment length (bp) |
|---|---|---|
| Galnt13 | F:GTCTTCCTTGCTATACTTCAG GTCTTGGGTCTTCCTCTTGCTATACTTCAG | 259 |
| R:TCGTCTTACAGCCATCCAGC | ||
| Ddx56 | F:AAGGCTCTGGCGGATTTAGG | 181 |
| R:CCTGCTCTCGTACAGTCTGTTT | ||
| F: | 358 | |
| R: | ||
| Sncga | F:GCAGCCGCCAAAACCAAAGA | 134 |
| R:CCAGCCACAGCAGTATCACT | ||
| Sncgb | F:TCCAGAAGACCACCGACCAG | 152 |
| R:TTCCATACCACCATGAGAGA | ||
| Syn2b | F:AGTCATCCCATCCTCTCTTG | 104 |
| R:CTCTGCCTTTGCTTCGTCCT | ||
| Polg | F:GCTCTGGTTTTTGATGTGGA | 182 |
| R:CTGGAGTTTGCGAGGGTTTC | ||
| Dj-1 | F:TGTGAAAGAGGTGTTGAAGG | 120 |
| R:GGATGAGTAGTAACTGTGCT | ||
| Pink1 | F:GTACCTGGAGGTGTGTGTGC | 104 |
| R:CTCTGTGAGCGATGTTTTGT | ||
| Parkin | F:CCATCACCAAAACCACTCAC | 110 |
| R:GCACCACTCGAACTTACACT | ||
| Lrrk2 | F:TATTCGTTCGGTCTGCTGCT | 196 |
| R:TGTCCTGGGGGTTTTCTCTC | ||
| Gba | F:ACCAGGAGGCAAAGAACACA | 198 |
| R:GGACCTAGATCCAGGGCAAT | ||
| β-Synucleins (Sncb) | F:CAGCAAGACCAAAGACAGCG | 170 |
| R:TGGCTTCCTGACCAAACTCC |
| Gene | Primer (5'-3') | Fragment length (bp) |
|---|---|---|
| Th1 | F:TCAGAAGTTTGTTGGGAGG | 237 |
| R:CTGGTTTCAAGATGGTGGA | ||
| Th2 | F:GTCTCGCTTGGAGCATCAG | 155 |
| R:TTAGAAAGGGCATACAACA | ||
| Vat2 | F:GTGTCGGTGTATGGAAGTG | 164 |
| R:AAGAAACAAAGAGGAGCAA | ||
| Ddc | F:TTCCCACTGCCCACTCTTA | 151 |
| R:TCCGGTAGTTTCAGCATCTTT | ||
| Mao | F:TGCTGAAGAATGGGACAAG | 141 |
| R:AGAAACCACAAAGCCGAAA | ||
| Dat | F:AGACTCCATCCCTCCCATAGC | 115 |
| R:CATCATTTACCCAGAAGCCATT | ||
| Comta | F:GAATGTGGGCGACGAGAAA | 114 |
| R:CGAGCGATGCGAACAGTAG | ||
| Drd1a | F:ATTTGGGTCGCATTTGATA | 126 |
| R:CACCCTGGGAGTCATCTTC | ||
| Drd2a | F:ATCACAAACCGAAACCCTT | 195 |
| R:GACCTGGATCTCAAATGCT | ||
| Drd2b | F:TTTTGTTGTCTACTCCTCCAT | 144 |
| R:GCATCAGCGTCTGTCTTCT | ||
| Drd3 | F:TGGGCAGTTTATTTGGAAG | 177 |
| R:GCTGTGGGTGGTGTTGTAT | ||
| Drd4a | F:ACCACCACCAACTACTTCAT | 135 |
| R:CAGTCCATCACATACGGTCA | ||
| Drd4b | F:TCAAGACGACGACAAACTA | 121 |
| R:ACATTCAAGGACCAAACAC | ||
| Drd5a | F:CTGCGTCAGCGACACCACCT | 108 |
| R:GAGAAGCCCTTGCGGAACT |
Tab.3 Primer sequences for real-time quantitative PCR for dopamine （DA） neuron-related genes
| Gene | Primer (5'-3') | Fragment length (bp) |
|---|---|---|
| Th1 | F:TCAGAAGTTTGTTGGGAGG | 237 |
| R:CTGGTTTCAAGATGGTGGA | ||
| Th2 | F:GTCTCGCTTGGAGCATCAG | 155 |
| R:TTAGAAAGGGCATACAACA | ||
| Vat2 | F:GTGTCGGTGTATGGAAGTG | 164 |
| R:AAGAAACAAAGAGGAGCAA | ||
| Ddc | F:TTCCCACTGCCCACTCTTA | 151 |
| R:TCCGGTAGTTTCAGCATCTTT | ||
| Mao | F:TGCTGAAGAATGGGACAAG | 141 |
| R:AGAAACCACAAAGCCGAAA | ||
| Dat | F:AGACTCCATCCCTCCCATAGC | 115 |
| R:CATCATTTACCCAGAAGCCATT | ||
| Comta | F:GAATGTGGGCGACGAGAAA | 114 |
| R:CGAGCGATGCGAACAGTAG | ||
| Drd1a | F:ATTTGGGTCGCATTTGATA | 126 |
| R:CACCCTGGGAGTCATCTTC | ||
| Drd2a | F:ATCACAAACCGAAACCCTT | 195 |
| R:GACCTGGATCTCAAATGCT | ||
| Drd2b | F:TTTTGTTGTCTACTCCTCCAT | 144 |
| R:GCATCAGCGTCTGTCTTCT | ||
| Drd3 | F:TGGGCAGTTTATTTGGAAG | 177 |
| R:GCTGTGGGTGGTGTTGTAT | ||
| Drd4a | F:ACCACCACCAACTACTTCAT | 135 |
| R:CAGTCCATCACATACGGTCA | ||
| Drd4b | F:TCAAGACGACGACAAACTA | 121 |
| R:ACATTCAAGGACCAAACAC | ||
| Drd5a | F:CTGCGTCAGCGACACCACCT | 108 |
| R:GAGAAGCCCTTGCGGAACT |
Fig.1 Detection of Ddx56 and Galnt13 gene probes by gel electrophoresis. Marker is the 2000 bp DNA Ladder; the Ddx56 probe is approximately 550 bp, and the Galnt13 probe is approximately 600 bp.
Fig.2 Expression of Ddx56 during early embryonic development of zebrafish. LV: Lateral view; AV : Anterior view; DV: Dorsal view.
Fig.3 Expression of Galnt13 during early embryonic development of zebrafish.
Fig.4 Expression of Ddx56 (A) and Galnt13 (B) in various organs of zebrafish (n=3). *P<0.05 vs other organs.
Fig.5 qRT-PCR analysis of Ddx56 and Galnt13 knockdown efficiency (n=3). *P<0.05 vs CasRx.
Fig.6 Expression of PD- and DA neuron-associated genes in zebrafish after Ddx56 or Galnt13 knockdown (n=3). A: Expression of PD-related genes following Ddx56 knockdown. B: Expression of PD-related genes following Galnt13 knockdown. C: Expression of DA-related genes following Ddx56 knockdown. D: Expression of DA-related genes following Galnt13 knockdown. *P<0.05, **P<0.01, ***P<0.001 vs CasRx control group.
Fig.7 Infection efficiency of SH-SY5Y-ZsGreen-PURO cells and efficiency of Ddx56 overexpression or knockdown (n=3). A: Bright-field image of SH-SY5Y-ZsGreen-PURO cells (Original magnification: ×400). B: Fluorescence image of SH-SY5Y-ZsGreen-PURO cells (×400). C: Electrophoresis gel of Ddx56 overexpression. D: Statistical graph of Ddx56 overexpression. E: Electrophoresis gel of Ddx56 knockdown. F: Statistical graph of Ddx56 knockdown. *P<0.05.
Fig.8 Detection of Ddx56 protein overexpression and knockdown efficiency.
| Item | Blank | Ddx56-con-OE | Ddx56-con-sh | Ddx56-OE | Ddx56-sh |
|---|---|---|---|---|---|
| GAPDH | 140.25 | 183.60 | 179.49 | 137.24 | 163.96 |
| Ddx56 | 178.12 | 199.04 | 218.13 | 194.95 | 142.65 |
| Ddx56/GAPDH | 1.27 | 1.08 | 1.22 | 1.42 | 0.87 |
Tab.4 Gray-scale analysis results of Ddx56 protein overexpression and knockdown (n=3)
| Item | Blank | Ddx56-con-OE | Ddx56-con-sh | Ddx56-OE | Ddx56-sh |
|---|---|---|---|---|---|
| GAPDH | 140.25 | 183.60 | 179.49 | 137.24 | 163.96 |
| Ddx56 | 178.12 | 199.04 | 218.13 | 194.95 | 142.65 |
| Ddx56/GAPDH | 1.27 | 1.08 | 1.22 | 1.42 | 0.87 |
Fig.9 Effect of Ddx56 knockdown or overexpression on apoptosis in SH-SY5Y cells (n=3). A: Blank. B: Blank+Vector. C: Ddx56-con-sh (knockdown control). D: Ddx56-sh (knockdown). E: Ddx56-con-OE (overexpression control). F: Ddx56-OE (overexpression). G: Apoptosis rates. *P<0.05 vs Ddx56-con-sh.
Fig.10 KEGG functional clustering (A) and pathway enrichment (B) of transcriptomic changes induced by Ddx56 knockdown.
| Pathway | Gene count | Differentially expressed genes (DEGs) |
|---|---|---|
| TNF pathway | 3 | Casp3, Creb1, Mmp9 |
| Hippo pathway | 2 | Ppp1cb, Mob1b |
| VEGF pathway | 1 | Pla2g4a |
| Wnt pathway | 3 | Cxxc4, Prkacb, Gpc4 |
| cGMP-PKG pathway | 3 | Ppp1cb, Creb1, Kcnma1 |
| TGF-beta pathway | 2 | Rbl1, Acvr2a |
| HIF-1pathway | 2 | Tfrc, Cul2 |
| cAMP pathway | 5 | Sucnr1, Ppp1cb, Creb1, Oxtr, Abcc4 |
| AMPK pathway | 3 | Creb1, Cptic, Lepr |
| NF-kappa B pathway | 1 | Bcl2a1 |
| PI3K-Akt pathway | 4 | Gng11, Creb1, Hsp90aa1, Itgb1 |
| Jak-STAT pathway | 1 | Lepr |
| Ras pathway | 4 | Gng11, Prkacb, Pla2g4a, Tbk1 |
| Calcium pathway | 3 | Prkacb, Avpr1a, Oxtr |
| MAPK pathway | 3 | Casp3, Prkacb, Pla2g4a |
| Rap1 pathway | 2 | Cnr1, Itgb1 |
| Hedgehog pathway | 2 | Csnk1g3, Prkacb |
| Sphingolipid pathway | 1 | Fcer1a |
| mRNA pathway | 2 | Ppp1cb, Rnmt |
| Ribosome biogenesis pathway | 3 | Rmrp, Sbds, Nmd3 |
| RNA transport pathway | 5 | Eif1ax, Thoc7, Strap, Eif3e, Nmd3 |
| Aminoacyl-tRNA biosynthesis pathway | 1 | Rars |
| Ribosome pathway | 20 | Rps7, Rps17, Rps3a, Rps15a, Rps21, Rpl6, Rsl24d1, Rpl27, Rpl30, Rpl26, Mrpl13, Rpl23, Rpl7, Rpl31,Mrpl1, Rpl39, Rpl34, Rpl41, Rpl11, Rpl17 |
| Metabolic pathway | 26 | Cox7c, Tusc3, Cox6c, Ndufb3, Minpp1, Hprt1, Atp5c1, Ndufa4, Atp5j, Mocs2, Pla2g4a, Cox7b, Atp5e, Galnt1, Polr2k, Uqcrb, Idi1, Dpm1, Atp5i, Aoc1, Ndufs4, Galnt5, Apip, Fpgt, Cmpk1, Pole2 |
| Fatty acid metabolism pathway | 1 | Cpt1c |
Tab.5 KEGG functional clustering of transcriptomic changes induced by Ddx56 knockdown
| Pathway | Gene count | Differentially expressed genes (DEGs) |
|---|---|---|
| TNF pathway | 3 | Casp3, Creb1, Mmp9 |
| Hippo pathway | 2 | Ppp1cb, Mob1b |
| VEGF pathway | 1 | Pla2g4a |
| Wnt pathway | 3 | Cxxc4, Prkacb, Gpc4 |
| cGMP-PKG pathway | 3 | Ppp1cb, Creb1, Kcnma1 |
| TGF-beta pathway | 2 | Rbl1, Acvr2a |
| HIF-1pathway | 2 | Tfrc, Cul2 |
| cAMP pathway | 5 | Sucnr1, Ppp1cb, Creb1, Oxtr, Abcc4 |
| AMPK pathway | 3 | Creb1, Cptic, Lepr |
| NF-kappa B pathway | 1 | Bcl2a1 |
| PI3K-Akt pathway | 4 | Gng11, Creb1, Hsp90aa1, Itgb1 |
| Jak-STAT pathway | 1 | Lepr |
| Ras pathway | 4 | Gng11, Prkacb, Pla2g4a, Tbk1 |
| Calcium pathway | 3 | Prkacb, Avpr1a, Oxtr |
| MAPK pathway | 3 | Casp3, Prkacb, Pla2g4a |
| Rap1 pathway | 2 | Cnr1, Itgb1 |
| Hedgehog pathway | 2 | Csnk1g3, Prkacb |
| Sphingolipid pathway | 1 | Fcer1a |
| mRNA pathway | 2 | Ppp1cb, Rnmt |
| Ribosome biogenesis pathway | 3 | Rmrp, Sbds, Nmd3 |
| RNA transport pathway | 5 | Eif1ax, Thoc7, Strap, Eif3e, Nmd3 |
| Aminoacyl-tRNA biosynthesis pathway | 1 | Rars |
| Ribosome pathway | 20 | Rps7, Rps17, Rps3a, Rps15a, Rps21, Rpl6, Rsl24d1, Rpl27, Rpl30, Rpl26, Mrpl13, Rpl23, Rpl7, Rpl31,Mrpl1, Rpl39, Rpl34, Rpl41, Rpl11, Rpl17 |
| Metabolic pathway | 26 | Cox7c, Tusc3, Cox6c, Ndufb3, Minpp1, Hprt1, Atp5c1, Ndufa4, Atp5j, Mocs2, Pla2g4a, Cox7b, Atp5e, Galnt1, Polr2k, Uqcrb, Idi1, Dpm1, Atp5i, Aoc1, Ndufs4, Galnt5, Apip, Fpgt, Cmpk1, Pole2 |
| Fatty acid metabolism pathway | 1 | Cpt1c |
| The pathway function | The number of DEGs | Q values (adjusted P-values) |
|---|---|---|
| Ribosome | 20 | 1.28E-09 |
| Parkinson disease | 12 | 0.006253826 |
| Oxidative phosphorylation | 11 | 0.009234468 |
| Huntington disease | 13 | 0.017892934 |
| Alzheimer disease | 11 | 0.043900536 |
| Fanconi anemia | 5 | 0.089089127 |
Tab.6 KEGG pathway enrichment of transcriptomic changes induced by Ddx56 knockdown
| The pathway function | The number of DEGs | Q values (adjusted P-values) |
|---|---|---|
| Ribosome | 20 | 1.28E-09 |
| Parkinson disease | 12 | 0.006253826 |
| Oxidative phosphorylation | 11 | 0.009234468 |
| Huntington disease | 13 | 0.017892934 |
| Alzheimer disease | 11 | 0.043900536 |
| Fanconi anemia | 5 | 0.089089127 |
Fig.11 Expression of Ddx56 and Galnt13 during human whole-brain development and in different tissues. A: Expression of Ddx56 and Galnt13 during human whole-brain development, based on RNA-seq data from the Genotype-Tissue Expression (GTEx) database. B: Expression of Ddx56 in various tissues based on GTEx database (red indicates different brain regions, and blue indicates other tissues).
Fig.12 Functional analysis of Ddx56 in human single-cell transcriptomic data. A: Rho (Spearman's correlation coefficient) of Ddx56 with PD-related genes across human brain cell populations. B: Rho of Ddx56 with apoptosis-related genes across human brain cell populations. C: DA-related differentially expressed genes between Ddx56+ and Ddx56- cells. D: Correlation strength (average Rho) of Ddx56 with ribosomal genes across different human brain cell populations. *P<0.05, **P<0.01, ***P<0.001.
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