The Administration of Heat Shock Protein-70 Bacterial Homolog (DnaK) Improves the Cumulative Survival and the Expression of Immune-Related Genes in Gnotobiotic Full-Sibling Sea Bass Larvae Challenged with Vibrio anguillarum
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Bacterial Strain and Culture Conditions
2.2. Induction and Synthesis of DnaK
2.3. Protein Extraction, SDS-PAGE, and Western Blot to Verify DnaK Synthesis
2.4. Gnotobiotic Full-Sibling Sea Bass Larvae
2.5. Full-Sibling Sea Bass Larvae Incubated with E. coli Overexpressing DnaK
2.6. Full-Sibling Sea Bass Larvae Incubated with E. coli Overexpressing DnaK and Challenged with Vibrio anguillarum
2.7. Ethics Statement
2.8. RNA Extraction and cDNA Synthesis of Single Full-Sibling Sea Bass Larvae
2.9. Gene Expression Analysis by Real-Time PCR
2.10. Statistical Analysis
3. Results
3.1. DnaK Induction and Synthesis
3.2. Cumulative Survival in Gnotobiotic Full-Sibling European Sea Bass Larvae Incubated with DnaK
3.3. Innate Immune-Related Gene Expression Profile in Gnotobiotic Full-Sibling European Sea Bass Larvae Incubated with DnaK
3.4. Innate Immune-Related Gene Expression Profile in Gnotobiotic Full-Sibling European Sea Bass Larvae Incubated with DnaK and Challenged with V. anguillarum
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Appendix A
Genes | Time (hpc) | NB-MI | YS0-MI | YS1-MI | YS2-MI | ||||
---|---|---|---|---|---|---|---|---|---|
Mean | SD | Mean | SD | Mean | SD | Mean | SD | ||
pentraxin | 0 | 0.94 | 0.48 | 1.31 | 0.53 | 1.10 | 0.51 | 0.87 | 0.25 |
18 | 0.57 | 0.16 | 0.76 | 0.35 | 0.64 | 0.24 | 0.77 | 0.35 | |
24 | 0.93 | 0.42 | 0.82 | 0.24 | 0.93 | 0.34 | 1.01 | 0.33 | |
36 | 0.93 | 0.30 | 0.89 | 0.31 | 0.59 | 0.43 | 0.78 | 0.31 | |
120 | 0.67 | 0.50 | 1.13 | 0.68 | 0.94 | 0.36 | 0.97 | 0.34 | |
lysozyme | 0 | 0.71 | 0.26 | 1.27 | 0.90 | 1.48 | 1.17 | 1.90 | 1.24 |
18 | 1.02 | 0.74 | 1.34 | 0.63 | 0.82 | 0.46 | 1.16 | 0.67 | |
24 | 1.05 | 0.66 | 0.89 | 0.41 | 1.18 | 0.64 | 0.84 | 0.35 | |
36 | 1.16 | 0.46 | 1.06 | 0.59 | 0.75 | 0.40 | 0.77 | 0.45 | |
120 | 0.55 | 0.29 | 0.71 | 0.26 | 0.98 | 0.64 | 1.10 | 0.46 | |
trasnsferrin | 0 | 1.03 | 0.41 | 1.74 | 0.97 | 1.30 | 0.54 | 1.10 | 0.65 |
18 | 0.96 | 0.50 | 1.79 | 1.00 | 0.88 | 0.38 | 1.46 | 0.47 | |
24 | 1.83 | 0.64 | 1.51 | 0.50 | 1.57 | 0.89 | 1.89 | 0.93 | |
36 | 1.85 | 0.75 | 1.34 | 0.79 | 0.89 | 0.54 | 1.57 | 0.63 | |
120 | 1.47 | 0.63 | 2.60 | 1.26 | 1.51 | 0.55 | 2.36 | 1.15 | |
hepcidin | 0 | 0.43 | 0.14 | 2.82 | 2.52 | 0.99 | 0.61 | 1.37 | 1.73 |
18 | 0.69 | 0.34 | 1.39 | 1.02 | 0.95 | 0.48 | 0.68 | 0.19 | |
24 | 0.48 | 0.40 | 1.68 | 1.45 | 1.13 | 1.54 | 1.01 | 0.21 | |
36 | 0.45 | 0.26 | 0.89 | 0.42 | 0.71 | 0.25 | 0.67 | 0.35 | |
120 | 0.48 | 0.17 | 0.72 | 0.45 | 0.69 | 0.36 | 0.57 | 0.24 | |
il-1β | 0 | 0.75 | 0.51 | 1.36 | 1.05 | 1.50 | 1.69 | 1.51 | 1.80 |
18 | 1.38 | 0.86 | 1.07 | 0.68 | 0.73 | 0.35 | 1.35 | 1.03 | |
24 | 0.57 | 0.24 | 0.70 | 0.41 | 0.77 | 0.54 | 1.30 | 0.75 | |
36 | 0.81 | 0.69 | 0.71 | 0.37 | 1.02 | 0.47 | 1.10 | 0.47 | |
120 | 2.08 | 0.89 | 1.48 | 0.88 | 1.37 | 0.68 | 1.46 | 0.96 | |
il-8 | 0 | 0.76 | 0.77 | 0.61 | 0.20 | 0.79 | 0.57 | 0.69 | 0.38 |
18 | 0.85 | 0.33 | 0.67 | 0.46 | 0.56 | 0.42 | 0.79 | 0.62 | |
24 | 0.38 | 0.08 | 0.49 | 0.25 | 0.64 | 0.50 | 0.82 | 0.29 | |
36 | 0.57 | 0.30 | 0.54 | 0.31 | 0.65 | 0.29 | 0.64 | 0.22 | |
120 | 1.23 | 0.58 | 0.99 | 0.68 | 1.12 | 0.53 | 1.39 | 0.98 | |
ccl4 | 0 | 0.98 | 0.49 | 1.11 | 0.31 | 1.42 | 1.00 | 0.97 | 0.32 |
18 | 0.94 | 0.51 | 1.20 | 0.45 | 0.90 | 0.35 | 1.23 | 0.64 | |
24 | 0.83 | 0.25 | 0.89 | 0.24 | 1.11 | 0.38 | 1.65 | 0.48 | |
36 | 1.07 | 0.57 | 1.06 | 0.40 | 1.22 | 0.51 | 1.40 | 0.39 | |
120 | 0.95 | 0.32 | 1.38 | 0.64 | 1.53 | 0.83 | 0.89 | 0.37 | |
il-10 | 0 | 1.00 | 0.42 | 1.17 | 0.40 | 1.00 | 0.25 | 1.22 | 0.46 |
18 | 0.89 | 0.30 | 0.92 | 0.40 | 1.11 | 0.34 | 1.12 | 0.41 | |
24 | 1.15 | 0.45 | 1.29 | 0.54 | 1.17 | 0.37 | 1.21 | 0.57 | |
36 | 1.29 | 0.38 | 0.96 | 0.20 | 0.92 | 0.25 | 1.24 | 0.31 | |
120 | 1.57 | 0.31 | 1.59 | 0.24 | 1.92 | 0.38 | 1.48 | 0.33 | |
hsp70 | 0 | 1.14 | 0.08 | 0.99 | 0.14 | 0.99 | 0.15 | 0.97 | 0.13 |
18 | 0.96 | 0.30 | 0.92 | 0.26 | 0.81 | 0.21 | 0.93 | 0.22 | |
24 | 1.12 | 0.27 | 1.02 | 0.38 | 0.97 | 0.18 | 0.96 | 0.08 | |
36 | 0.89 | 0.11 | 0.85 | 0.11 | 0.77 | 0.19 | 0.80 | 0.16 | |
120 | 0.87 | 0.18 | 0.95 | 0.20 | 0.81 | 0.20 | 0.93 | 0.18 |
Genes | Group Comparison | Hours Post Administration of DnaK | ||||
---|---|---|---|---|---|---|
0 | 18 | 24 | 36 | 120 | ||
pentraxin | NB-MI vs. YS0-MI | 0.2129 | 0.7074 | 0.9298 | 0.996 | 0.0506 |
NB-MI vs. YS1-MI | 0.8373 | 0.9732 | >0.9999 | 0.2203 | 0.4512 | |
NB-MI vs. YS2-MI | 0.9816 | 0.6739 | 0.9636 | 0.8262 | 0.3233 | |
YS0-MI vs. YS1-MI | 0.6127 | 0.9144 | 0.9286 | 0.3008 | 0.7478 | |
YS0-MI vs. YS2-MI | 0.0633 | >0.9999 | 0.6987 | 0.9146 | 0.7897 | |
YS1-MI vs. YS2-MI | 0.5575 | 0.894 | 0.9644 | 0.6908 | 0.9992 | |
lysozyme | NB-MI vs. YS0-MI | 0.29 | 0.6633 | 0.9493 | 0.9864 | 0.9529 |
NB-MI vs. YS1-MI | 0.0751 | 0.903 | 0.9741 | 0.5091 | 0.4884 | |
NB-MI vs. YS2-MI | 0.0018 | 0.959 | 0.9051 | 0.561 | 0.2287 | |
YS0-MI vs. YS1-MI | 0.8867 | 0.2641 | 0.736 | 0.705 | 0.81 | |
YS0-MI vs. YS2-MI | 0.1457 | 0.9278 | 0.9988 | 0.7548 | 0.5441 | |
YS1-MI vs. YS2-MI | 0.4821 | 0.6493 | 0.646 | 0.9998 | 0.9815 | |
transferrin | NB-MI vs. YS0-MI | 0.2237 | 0.0818 | 0.7765 | 0.4656 | 0.0074 |
NB-MI vs. YS1-MI | 0.8907 | 0.9952 | 0.8722 | 0.0327 | 0.9996 | |
NB-MI vs. YS2-MI | 0.9977 | 0.4819 | 0.9978 | 0.8574 | 0.0458 | |
YS0-MI vs. YS1-MI | 0.5808 | 0.0459 | 0.9975 | 0.5429 | 0.0174 | |
YS0-MI vs. YS2-MI | 0.2523 | 0.7831 | 0.668 | 0.9177 | 0.8982 | |
YS1-MI vs. YS2-MI | 0.9423 | 0.3465 | 0.7815 | 0.2148 | 0.086 | |
hepcidin | NB-MI vs. YS0-MI | <0.0001 | 0.358 | 0.0289 | 0.7354 | 0.943 |
NB-MI vs. YS1-MI | 0.6525 | 0.9251 | 0.4246 | 0.9286 | 0.963 | |
NB-MI vs. YS2-MI | 0.1929 | >0.9999 | 0.5981 | 0.9567 | 0.9958 | |
YS0-MI vs. YS1-MI | 0.0003 | 0.7279 | 0.5578 | 0.9741 | >0.9999 | |
YS0-MI vs. YS2-MI | 0.0047 | 0.3662 | 0.3834 | 0.952 | 0.9864 | |
YS1-MI vs. YS2-MI | 0.8373 | 0.9215 | 0.9918 | 0.9996 | 0.9934 | |
il-1β | NB-MI vs. YS0-MI | 0.4449 | 0.8649 | 0.9901 | 0.9953 | 0.4291 |
NB-MI vs. YS1-MI | 0.2986 | 0.3479 | 0.9613 | 0.9532 | 0.2998 | |
NB-MI vs. YS2-MI | 0.2632 | 0.9999 | 0.2538 | 0.8965 | 0.3791 | |
YS0-MI vs. YS1-MI | 0.9841 | 0.8235 | 0.9981 | 0.8582 | 0.9926 | |
YS0-MI vs. YS2-MI | 0.979 | 0.8928 | 0.4181 | 0.7685 | >0.9999 | |
YS1-MI vs. YS2-MI | >0.9999 | 0.3856 | 0.5025 | 0.9971 | 0.9951 | |
il-8 | NB-MI vs. YS0-MI | 0.9271 | 0.8564 | 0.9605 | 0.9995 | 0.6896 |
NB-MI vs. YS1-MI | 0.9988 | 0.5566 | 0.6531 | 0.9833 | 0.9597 | |
NB-MI vs. YS2-MI | 0.9925 | 0.9936 | 0.1957 | 0.9866 | 0.8876 | |
YS0-MI vs. YS1-MI | 0.8659 | 0.9599 | 0.9029 | 0.9618 | 0.9448 | |
YS0-MI vs. YS2-MI | 0.9862 | 0.9509 | 0.417 | 0.9675 | 0.2748 | |
YS1-MI vs. YS2-MI | 0.9728 | 0.7245 | 0.8285 | >0.9999 | 0.6411 | |
ccl4 | NB-MI vs. YS0-MI | 0.9366 | 0.6931 | 0.9942 | >0.9999 | 0.2572 |
NB-MI vs. YS1-MI | 0.2473 | 0.9985 | 0.6058 | 0.9154 | 0.0809 | |
NB-MI vs. YS2-MI | >0.9999 | 0.6155 | 0.0019 | 0.4821 | 0.9932 | |
YS0-MI vs. YS1-MI | 0.5279 | 0.5916 | 0.7607 | 0.9016 | 0.9317 | |
YS0-MI vs. YS2-MI | 0.9252 | 0.9993 | 0.0047 | 0.446 | 0.1559 | |
YS1-MI vs. YS2-MI | 0.2144 | 0.5129 | 0.0776 | 0.8535 | 0.0429 | |
il-10 | NB-MI vs. YS0-MI | 0.7923 | 0.9984 | 0.8448 | 0.2293 | 0.9995 |
NB-MI vs. YS1-MI | >0.9999 | 0.5506 | 0.9998 | 0.1309 | 0.199 | |
NB-MI vs. YS2-MI | 0.6378 | 0.5435 | 0.9834 | 0.9901 | 0.9423 | |
YS0-MI vs. YS1-MI | 0.7655 | 0.677 | 0.8742 | 0.9916 | 0.2638 | |
YS0-MI vs. YS2-MI | 0.9924 | 0.6665 | 0.9658 | 0.3563 | 0.9111 | |
YS1-MI vs. YS2-MI | 0.5956 | >0.9999 | 0.9917 | 0.2178 | 0.0613 | |
hsp70 | NB-MI vs. YS0-MI | 0.4408 | 0.9584 | 0.6403 | 0.9663 | 0.8582 |
NB-MI vs. YS1-MI | 0.4316 | 0.3345 | 0.3182 | 0.5489 | 0.9171 | |
NB-MI vs. YS2-MI | 0.3211 | 0.9805 | 0.2748 | 0.8029 | 0.9326 | |
YS0-MI vs. YS1-MI | >0.9999 | 0.6666 | 0.95 | 0.8145 | 0.5146 | |
YS0-MI vs. YS2-MI | 0.9936 | 0.9995 | 0.9241 | 0.9697 | 0.9967 | |
YS1-MI vs. YS2-MI | 0.9947 | 0.5926 | 0.9998 | 0.9729 | 0.622 |
Genes | Time (hpc) | NB-Ch | YS0-Ch | YS1-Ch | YS2-Ch | ||||
---|---|---|---|---|---|---|---|---|---|
Mean | SD | Mean | SD | Mean | SD | Mean | SD | ||
pentraxin | 0 | 1.13 | 0.69 | 1.31 | 0.53 | 1.10 | 0.51 | 0.87 | 0.25 |
18 | 0.74 | 0.16 | 0.55 | 0.10 | 0.66 | 0.32 | 0.55 | 0.21 | |
24 | 1.22 | 0.64 | 1.21 | 0.52 | 1.32 | 0.55 | 0.78 | 0.28 | |
36 | 1.06 | 0.55 | 0.78 | 0.35 | 1.07 | 0.69 | 0.72 | 0.44 | |
120 | 0.63 | 0.32 | 0.63 | 0.41 | 1.17 | 1.09 | 1.00 | 0.89 | |
lysozyme | 0 | 1.08 | 1.08 | 1.27 | 0.90 | 1.48 | 1.17 | 1.90 | 1.24 |
18 | 0.85 | 0.47 | 0.43 | 0.34 | 1.51 | 0.90 | 0.69 | 0.29 | |
24 | 1.12 | 0.75 | 0.91 | 0.59 | 1.51 | 0.99 | 1.26 | 0.62 | |
36 | 1.03 | 0.62 | 0.92 | 0.39 | 1.35 | 1.10 | 1.06 | 0.74 | |
120 | 2.35 | 2.33 | 2.67 | 1.77 | 2.17 | 3.59 | 2.61 | 3.26 | |
trasnferrin | 0 | 1.14 | 0.50 | 1.74 | 0.97 | 1.46 | 0.73 | 1.10 | 0.65 |
18 | 1.72 | 0.69 | 1.04 | 0.66 | 1.50 | 0.61 | 0.99 | 0.37 | |
24 | 1.89 | 0.98 | 1.23 | 0.73 | 1.76 | 1.14 | 1.40 | 0.47 | |
36 | 1.56 | 0.70 | 1.03 | 0.36 | 1.86 | 1.16 | 1.20 | 0.49 | |
120 | 9.89 | 8.92 | 10.81 | 7.48 | 10.76 | 11.12 | 21.92 | 10.50 | |
hepcidin | 0 | 0.92 | 1.40 | 2.82 | 2.52 | 1.40 | 1.21 | 1.37 | 1.73 |
18 | 1.02 | 1.12 | 2.12 | 2.89 | 0.82 | 0.31 | 0.55 | 0.23 | |
24 | 1.50 | 2.59 | 1.70 | 1.71 | 2.35 | 2.40 | 0.96 | 0.43 | |
36 | 1.31 | 1.22 | 1.43 | 0.88 | 4.67 | 11.64 | 0.67 | 0.54 | |
120 | 1320.33 | 1673.60 | 917.26 | 699.12 | 659.76 | 355.95 | 1564.23 | 1757.90 | |
il-1β | 0 | 1.77 | 3.08 | 1.36 | 1.05 | 1.50 | 1.69 | 1.51 | 1.80 |
18 | 2.65 | 4.09 | 1.84 | 2.88 | 1.14 | 0.83 | 0.73 | 0.49 | |
24 | 1.12 | 0.81 | 0.65 | 0.41 | 1.77 | 1.67 | 1.03 | 0.29 | |
36 | 1.40 | 1.49 | 1.02 | 0.48 | 1.22 | 0.98 | 0.73 | 0.49 | |
120 | 43.22 | 39.27 | 20.67 | 16.47 | 22.23 | 17.56 | 64.18 | 52.47 | |
il-8 | 0 | 0.76 | 0.77 | 0.61 | 0.20 | 1.55 | 1.67 | 0.69 | 0.38 |
18 | 1.04 | 1.04 | 0.96 | 1.13 | 0.67 | 0.36 | 0.45 | 0.17 | |
24 | 0.73 | 0.63 | 0.69 | 0.65 | 1.58 | 1.48 | 0.81 | 0.54 | |
36 | 1.31 | 1.54 | 0.58 | 0.25 | 0.99 | 0.68 | 0.64 | 0.56 | |
120 | 21.33 | 14.37 | 11.18 | 8.94 | 12.34 | 12.47 | 28.56 | 21.35 | |
ccl4 | 0 | 0.98 | 0.49 | 1.11 | 0.31 | 1.42 | 1.00 | 0.97 | 0.32 |
18 | 1.67 | 1.71 | 1.64 | 2.11 | 1.25 | 0.71 | 1.21 | 0.66 | |
24 | 1.52 | 0.89 | 0.95 | 0.66 | 1.73 | 1.01 | 1.08 | 0.33 | |
36 | 1.15 | 0.53 | 1.19 | 0.28 | 1.63 | 0.79 | 1.11 | 0.70 | |
120 | 2.56 | 1.83 | 3.10 | 2.17 | 4.17 | 3.69 | 4.17 | 1.66 | |
il-10 | 0 | 1.22 | 0.74 | 1.17 | 0.40 | 1.00 | 0.25 | 1.22 | 0.46 |
18 | 1.21 | 0.36 | 1.24 | 0.44 | 1.09 | 0.58 | 1.02 | 0.22 | |
24 | 1.44 | 0.45 | 1.26 | 0.76 | 1.04 | 0.26 | 1.13 | 0.25 | |
36 | 1.10 | 0.46 | 1.06 | 0.43 | 1.46 | 0.90 | 0.89 | 0.29 | |
120 | 7.42 | 7.60 | 3.85 | 3.13 | 3.26 | 2.10 | 5.58 | 5.39 | |
hsp70 | 0 | 1.14 | 0.08 | 0.99 | 0.14 | 0.99 | 0.15 | 0.97 | 0.13 |
18 | 0.85 | 0.12 | 0.89 | 0.23 | 0.93 | 0.16 | 0.97 | 0.17 | |
24 | 1.02 | 0.34 | 0.78 | 0.15 | 0.90 | 0.12 | 0.84 | 0.10 | |
36 | 0.97 | 0.25 | 0.87 | 0.09 | 0.94 | 0.70 | 0.69 | 0.09 | |
120 | 0.95 | 0.20 | 1.07 | 0.13 | 1.36 | 1.06 | 1.40 | 0.94 |
Genes | Group Comparison | Hours Post Challenge | ||||
---|---|---|---|---|---|---|
0 | 18 | 24 | 36 | 120 | ||
pentraxin | NB-MI vs. NB-Ch | 0.9483 | 0.95 | 0.7373 | 0.984 | 0.9998 |
NB-MI vs. YS0-Ch | 0.5548 | >0.9999 | 0.7564 | 0.968 | >0.9999 | |
NB-MI vs. YS1-Ch | 0.9665 | 0.9958 | 0.401 | 0.9748 | 0.2522 | |
NB-MI vs. YS2-Ch | 0.9984 | >0.9999 | 0.9666 | 0.8925 | 0.5979 | |
NB-Ch vs. YS0-Ch | 0.9384 | 0.9382 | >0.9999 | 0.771 | >0.9999 | |
NB-Ch vs. YS1-Ch | >0.9999 | 0.997 | 0.9926 | >0.9999 | 0.2062 | |
NB-Ch vs. YS2-Ch | 0.8134 | 0.93 | 0.3555 | 0.6113 | 0.5171 | |
YS0-Ch vs. YS1-Ch | 0.8761 | 0.9923 | 0.9902 | 0.7058 | 0.3046 | |
YS0-Ch vs. YS2-Ch | 0.2969 | >0.9999 | 0.3744 | 0.9987 | 0.6318 | |
YS1-Ch vs. YS2-Ch | 0.8463 | 0.991 | 0.1174 | 0.529 | 0.9621 | |
lysozyme | NB-MI vs. NB-Ch | 0.9816 | 0.9988 | >0.9999 | 0.9996 | 0.0249 |
NB-MI vs. YS0-Ch | 0.9057 | 0.8752 | 0.9996 | 0.9942 | 0.0157 | |
NB-MI vs. YS1-Ch | 0.7512 | 0.9204 | 0.9469 | 0.9979 | 0.0695 | |
NB-MI vs. YS2-Ch | 0.3662 | 0.9833 | 0.997 | 0.9998 | 0.0063 | |
NB-Ch vs. YS0-Ch | 0.998 | 0.9614 | 0.9977 | 0.9997 | 0.9895 | |
NB-Ch vs. YS1-Ch | 0.9674 | 0.8196 | 0.9714 | 0.9866 | 0.9987 | |
NB-Ch vs. YS2-Ch | 0.693 | 0.999 | 0.9994 | >0.9999 | 0.9932 | |
YS0-Ch vs. YS1-Ch | 0.9965 | 0.4253 | 0.8727 | 0.947 | 0.9537 | |
YS0-Ch vs. YS2-Ch | 0.8291 | 0.9933 | 0.9803 | 0.9993 | >0.9999 | |
YS1-Ch vs. YS2-Ch | 0.9549 | 0.6697 | 0.9933 | 0.9874 | 0.9589 | |
transferrin | NB-MI vs. NB-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 |
NB-MI vs. YS0-Ch | >0.99 | >0.99 | >0.99 | 0.99 | <0.001 | |
NB-MI vs. YS1-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
NB-MI vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
NB-Ch vs. YS0-Ch | >0.99 | >0.99 | >0.99 | >0.99 | 0.99 | |
NB-Ch vs. YS1-Ch | >0.99 | >0.99 | >0.99 | >0.99 | 0.99 | |
NB-Ch vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
YS0-Ch vs. YS1-Ch | >0.99 | >0.99 | >0.99 | 0.99 | >0.99 | |
YS0-Ch vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
YS1-Ch vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
hepcidin | NB-MI vs. NB-Ch | >0.9999 | >0.9999 | >0.9999 | >0.9999 | <0.0001 |
NB-MI vs. YS0-Ch | >0.9999 | >0.9999 | >0.9999 | >0.9999 | 0.0039 | |
NB-MI vs. YS1-Ch | >0.9999 | >0.9999 | >0.9999 | >0.9999 | 0.0368 | |
NB-MI vs. YS2-Ch | >0.9999 | >0.9999 | >0.9999 | >0.9999 | <0.0001 | |
NB-Ch vs. YS0-Ch | >0.9999 | >0.9999 | >0.9999 | >0.9999 | 0.5799 | |
NB-Ch vs. YS1-Ch | >0.9999 | >0.9999 | >0.9999 | >0.9999 | 0.0659 | |
NB-Ch vs. YS2-Ch | >0.9999 | >0.9999 | >0.9999 | >0.9999 | 0.8506 | |
YS0-Ch vs. YS1-Ch | >0.9999 | >0.9999 | >0.9999 | >0.9999 | 0.8799 | |
YS0-Ch vs. YS2-Ch | >0.9999 | >0.9999 | >0.9999 | >0.9999 | 0.1113 | |
YS1-Ch vs. YS2-Ch | >0.9999 | >0.9999 | >0.9999 | >0.9999 | 0.0022 | |
il-1β | NB-MI vs. NB-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 |
NB-MI vs. YS0-Ch | >0.99 | >0.99 | >0.99 | >0.99 | 0.05 | |
NB-MI vs. YS1-Ch | >0.99 | >0.99 | >0.99 | >0.99 | 0.02 | |
NB-MI vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
NB-Ch vs. YS0-Ch | >0.99 | >0.99 | >0.99 | >0.99 | 0.01 | |
NB-Ch vs. YS1-Ch | >0.99 | >0.99 | >0.99 | >0.99 | 0.02 | |
NB-Ch vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | 0.02 | |
YS0-Ch vs. YS1-Ch | >0.99 | >0.99 | >0.99 | >0.99 | >0.99 | |
YS0-Ch vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
YS1-Ch vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
il-8 | NB-MI vs. NB-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 |
NB-MI vs. YS0-Ch | >0.99 | >0.99 | >0.99 | >0.99 | 0.01 | |
NB-MI vs. YS1-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
NB-MI vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
NB-Ch vs. YS0-Ch | >0.99 | >0.99 | >0.99 | >0.99 | 0.01 | |
NB-Ch vs. YS1-Ch | >0.99 | >0.99 | >0.99 | >0.99 | 0.02 | |
NB-Ch vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | 0.08 | |
YS0-Ch vs. YS1-Ch | >0.99 | >0.99 | >0.99 | >0.99 | >0.99 | |
YS0-Ch vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
YS1-Ch vs. YS2-Ch | >0.99 | >0.99 | >0.99 | >0.99 | <0.001 | |
ccl4 | NB-MI vs. NB-Ch | >0.9999 | 0.6909 | 0.7139 | 0.9999 | 0.031 |
NB-MI vs. YS0-Ch | 0.9992 | 0.7504 | 0.9997 | 0.9994 | 0.0054 | |
NB-MI vs. YS1-Ch | 0.9346 | 0.9821 | 0.4441 | 0.8471 | <0.0001 | |
NB-MI vs. YS2-Ch | >0.9999 | 0.989 | 0.9917 | >0.9999 | <0.0001 | |
NB-Ch vs. YS0-Ch | 0.9992 | >0.9999 | 0.8898 | >0.9999 | 0.9099 | |
NB-Ch vs. YS1-Ch | 0.9346 | 0.9434 | 0.9956 | 0.9198 | 0.0481 | |
NB-Ch vs. YS2-Ch | >0.9999 | 0.9243 | 0.9315 | >0.9999 | 0.0369 | |
YS0-Ch vs. YS1-Ch | 0.979 | 0.9625 | 0.7075 | 0.9258 | 0.4689 | |
YS0-Ch vs. YS2-Ch | 0.999 | 0.9481 | 0.9996 | 0.9999 | 0.437 | |
YS1-Ch vs. YS2-Ch | 0.9248 | >0.9999 | 0.7538 | 0.8713 | >0.9999 | |
il-10 | NB-MI vs. NB-Ch | 0.9995 | 0.9969 | 0.9982 | 0.9997 | <0.0001 |
NB-MI vs. YS0-Ch | 0.9998 | 0.9964 | >0.9999 | 0.9991 | 0.1938 | |
NB-MI vs. YS1-Ch | >0.9999 | 0.9995 | >0.9999 | 0.9998 | 0.4035 | |
NB-MI vs. YS2-Ch | 0.9995 | >0.9999 | >0.9999 | 0.993 | 0.0003 | |
NB-Ch vs. YS0-Ch | >0.9999 | >0.9999 | 0.9998 | >0.9999 | 0.009 | |
NB-Ch vs. YS1-Ch | 0.9994 | >0.9999 | 0.9929 | 0.996 | 0.0004 | |
NB-Ch vs. YS2-Ch | >0.9999 | 0.9996 | 0.9974 | 0.9995 | 0.3103 | |
YS0-Ch vs. YS1-Ch | 0.9998 | 0.9999 | 0.9995 | 0.9923 | 0.9832 | |
YS0-Ch vs. YS2-Ch | >0.9999 | 0.9995 | >0.9999 | 0.9997 | 0.4897 | |
YS1-Ch vs. YS2-Ch | 0.9994 | >0.9999 | >0.9999 | 0.9715 | 0.1339 | |
hsp70 | NB-MI vs. NB-Ch | >0.9999 | 0.9556 | 0.9703 | 0.9901 | 0.9902 |
NB-MI vs. YS0-Ch | 0.9112 | 0.9921 | 0.2385 | >0.9999 | 0.814 | |
NB-MI vs. YS1-Ch | 0.9081 | 0.9996 | 0.6239 | 0.9972 | 0.0352 | |
NB-MI vs. YS2-Ch | 0.8633 | >0.9999 | 0.3933 | 0.7379 | 0.0124 | |
NB-Ch vs. YS0-Ch | 0.9112 | 0.9993 | 0.651 | 0.9745 | 0.9652 | |
NB-Ch vs. YS1-Ch | 0.9081 | 0.9889 | 0.9568 | 0.9999 | 0.1275 | |
NB-Ch vs. YS2-Ch | 0.8633 | 0.9543 | 0.8359 | 0.4585 | 0.0582 | |
YS0-Ch vs. YS1-Ch | >0.9999 | 0.9993 | 0.9467 | 0.9894 | 0.5684 | |
YS0-Ch vs. YS2-Ch | 0.9999 | 0.9912 | 0.9947 | 0.7928 | 0.4038 | |
YS1-Ch vs. YS2-Ch | >0.9999 | 0.9994 | 0.9962 | 0.4974 | 0.9992 |
References
- Sung, Y.Y.; Pineda, C.; MacRae, T.H.; Sorgeloos, P.; Bossier, P. Exposure of Gnotobiotic Artemia franciscana Larvae to Abiotic Stress Promotes Heat Shock Protein 70 Synthesis and Enhances Resistance to Pathogenic Vibrio campbellii. Cell Stress. Chaperones 2008, 13, 59–66. [Google Scholar] [CrossRef] [PubMed]
- Tort, L. Stress and Immune Modulation in Fish. Dev. Comp. Immunol. 2011, 35, 1366–1375. [Google Scholar] [CrossRef]
- Khansari, A.R.; Balasch, J.C.; Vallejos-Vidal, E.; Teles, M.; Fierro-Castro, C.; Tort, L.; Reyes-López, F.E. Comparative Study of Stress and Immune-Related Transcript Outcomes Triggered by Vibrio anguillarum Bacterin and Air Exposure Stress in Liver and Spleen of Gilthead Seabream (Sparus aurata), Zebrafish (Danio rerio) and Rainbow Trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 2019, 86, 436–448. [Google Scholar] [CrossRef] [PubMed]
- Lindquist, S. The Heat-Shock Response. Annu. Rev. Biochem. 1986, 55, 1151–1191. [Google Scholar] [CrossRef]
- Steinert, S.A.; Pickwell, G.V. Induction of HSP70 Proteins in Mussels by Ingestion of Tributyltin. Mar. Environ. Res. 1993, 35, 89–93. [Google Scholar] [CrossRef]
- Sørensen, J.G.; Loeschcke, V. Larval Crowding in Drosophila Melanogaster Induces Hsp70 Expression, and Leads to Increased Adult Longevity and Adult Thermal Stress Resistance. J. Insect Physiol. 2001, 47, 1301–1307. [Google Scholar] [CrossRef]
- Dang, W.; Hu, Y.H.; Zhang, M.; Sun, L. Identification and Molecular Analysis of a Stress-Inducible Hsp70 from Sciaenops Ocellatus. Fish Shellfish Immunol. 2010, 29, 600–607. [Google Scholar] [CrossRef]
- Athman, R.; Philpott, D. Innate Immunity via Toll-like Receptors and Nod Proteins. Curr. Opin. Microbiol. 2004, 7, 25–32. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Liu, S.; Wang, Y.; Lu, W.; Zhang, Q.; Cheng, J. Genomic and Transcriptomic Landscape and Evolutionary Dynamics of Heat Shock Proteins in Spotted Sea Bass (Lateolabrax maculatus) under Salinity Change and Alkalinity Stress. Biology 2022, 11, 353. [Google Scholar] [CrossRef]
- Li, Z.H.; Zhong, L.Q.; Wu, Y.H.; Mu, W.N. Alteration of Cytochrome P450 1 Regulation and HSP 70 Level in Brain of Juvenile Common Carp (Cyprinus carpio) after Chronic Exposure to Tributyltin. Fish. Physiol. Biochem. 2016, 42, 287–294. [Google Scholar] [CrossRef]
- Wieten, L.; Broere, F.; van der Zee, R.; Koerkamp, E.K.; Wagenaar, J.; van Eden, W. Cell Stress Induced HSP Are Targets of Regulatory T Cells: A Role for HSP Inducing Compounds as Anti-Inflammatory Immuno-Modulators? FEBS Lett. 2007, 581, 3716–3722. [Google Scholar] [CrossRef] [PubMed]
- Wilhelm, V.; Soza, C.; Martínez, R.; Rosemblatt, M.; Burzio, L.O.; Valenzuela, P.D.T. Production and Immune Response of Recombinant Hsp60 and Hsp70 from the Salmon Pathogen Piscirickettsia Salmonis. Biol. Res. 2005, 38, 69–82. [Google Scholar] [CrossRef] [PubMed]
- Josepriya, T.A.; Chien, K.H.; Lin, H.Y.; Huang, H.N.; Wu, C.J.; Song, Y.L. Immobilization Antigen Vaccine Adjuvanted by Parasitic Heat Shock Protein 70C Confers High Protection in Fish against Cryptocaryonosis. Fish Shellfish Immunol. 2015, 45, 517–527. [Google Scholar] [CrossRef]
- Pederzoli, A.; Mola, L. The Early Stress Responses in Fish Larvae. Acta Histochem. 2016, 118, 443–449. [Google Scholar] [CrossRef]
- Yang, Q.; Guo, L.; Liu, B.S.; Guo, H.Y.; Zhu, K.C.; Zhang, N.; Jiang, S.G.; Zhang, D.C. Effects of Stocking Density on the Growth Performance, Serum Biochemistry, Muscle Composition and HSP70 Gene Expression of Juvenile Golden Pompano Trachinotus Ovatus (Linnaeus, 1758). Aquaculture 2020, 518, 734841. [Google Scholar] [CrossRef]
- Choi, J.H.; Lee, J.H.; Jo, A.H.; Choi, Y.J.; Choi, C.Y.; Kang, J.C.; Kim, J.H. Microplastic Polyamide Toxicity: Neurotoxicity, Stress Indicators and Immune Responses in Crucian Carp, Carassius carassius. Ecotoxicol. Environ. Saf. 2023, 265, 115469. [Google Scholar] [CrossRef]
- Ahani, S.; Ahani, S.; Taheri, A.; Morteza, S.; Pagheh, E.; Arghideh, M.; Yousefi, M. Probiotic, Fructooligosaccharide and Yeast Extract Mixture Improves Gut Health in Rainbow Trout, Oncorhynchus mykiss. J. Anim. Physiol. Anim. Nutr. 2025, 109, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Huang, K.C.; Lee, J.W.; Hu, Y.F.; Ballantyne, R.; Liu, C.H. Effects of Aspergillus-Meal Prebiotic Diet on the Growth Performance, Health Status and Gut Microbiota of Asian Seabass, Lates calcarifer. Fish Shellfish Immunol. 2023, 136, 108696. [Google Scholar] [CrossRef]
- Reyes-López, F.E.; Romeo, J.S.; Vallejos-Vidal, E.; Reyes-Cerpa, S.; Sandino, A.M.; Tort, L.; Mackenzie, S.; Imarai, M. Differential Immune Gene Expression Profiles in Susceptible and Resistant Full-Sibling Families of Atlantic Salmon (Salmo salar) Challenged with Infectious Pancreatic Necrosis Virus (IPNV). Dev. Comp. Immunol. 2015, 53, 210–221. [Google Scholar] [CrossRef]
- Yaacob, E.N.; Norouzitallab, P.; De Geest, B.G.; Bajek, A.; Dierckens, K.; Bossier, P.; Vanrompay, D. Recombinant DnaK Orally Administered Protects Axenic European Sea Bass Against Vibriosis. Front. Immunol. 2020, 10, 492419. [Google Scholar] [CrossRef]
- Sinnasamy, S.; Mat Noordin, N.; Macrae, T.H.; Ikhwanuddin bin Abdullah, M.; Bossier, P.; bin Abdul Wahid, M.E.; Noriaki, A.; Sung, Y.Y. Ingestion of Food Pellets Containing Escherichia Coli Overexpressing the Heat-Shock Protein DnaK Protects Penaeus vannamei (Boone) against Vibrio harveyi (Baumann) Infection. J. Fish Dis. 2016, 39, 577–584. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Wang, W.; Hou, S.; Fu, W.; Cai, J.; Xia, L.; Lu, Y. Comparison of Protective Efficacy between Two DNA Vaccines Encoding DnaK and GroEL against Fish Nocardiosis. Fish Shellfish Immunol. 2019, 95, 128–139. [Google Scholar] [CrossRef] [PubMed]
- Paliwal, P.K.; Bansal, A.; Sagi, S.S.K.; Sairam, M. Intraperitoneal Immunization of Recombinant HSP70 (DnaK) of Salmonella Typhi Induces a Predominant Th2 Response and Protective Immunity in Mice against Lethal Salmonella infection. Vaccine 2011, 29, 6532–6539. [Google Scholar] [CrossRef]
- Hu, B.; Phuoc, L.H.; Sorgeloos, P.; Bossier, P. Bacterial HSP70 (DnaK) Is an Efficient Immune Stimulator in Litopenaeus vannamei. Aquaculture 2014, 418–419, 87–93. [Google Scholar] [CrossRef]
- Deane, E.E.; Woo, N.Y.S. Advances and Perspectives on the Regulation and Expression of Piscine Heat Shock Proteins. Rev. Fish Biol. Fish. 2010, 21, 153–185. [Google Scholar] [CrossRef]
- Engelsma, M.Y.; Huising, M.O.; Van Muiswinkel, W.B.; Flik, G.; Kwang, J.; Savelkoul, H.F.J.; Verburg-Van Kemenade, B.M.L. Neuroendocrine-Immune Interactions in Fish: A Role for Interleukin-1. Vet. Immunol. Immunopathol. 2002, 87, 467–479. [Google Scholar] [CrossRef]
- Nardocci, G.; Navarro, C.; Cortés, P.P.; Imarai, M.; Montoya, M.; Valenzuela, B.; Jara, P.; Acuña-Castillo, C.; Fernández, R. Neuroendocrine Mechanisms for Immune System Regulation during Stress in Fish. Fish Shellfish Immunol. 2014, 40, 531–538. [Google Scholar] [CrossRef]
- Engelsma, M.Y.; Stet, R.J.M.; Saeij, J.P.; Verburg-Van Kemenade, B.M.L. Differential Expression and Haplotypic Variation of Two Interleukin-1β Genes in the Common Carp (Cyprinus carpio L.). Cytokine 2003, 22, 21–32. [Google Scholar] [CrossRef]
- Monzón-Atienza, L.; Bravo, J.; Fernández-Montero, Á.; Charlie-Silva, I.; Montero, D.; Ramos-Vivas, J.; Galindo-Villegas, J.; Acosta, F. Dietary Supplementation of Bacillus Velezensis Improves Vibrio anguillarum Clearance in European Sea Bass by Activating Essential Innate Immune Mechanisms. Fish Shellfish Immunol. 2022, 124, 244–253. [Google Scholar] [CrossRef]
- Hickey, M.E.; Lee, J.L. A Comprehensive Review of Vibrio (Listonella) Anguillarum: Ecology, Pathology and Prevention. Rev. Aquac. 2018, 10, 585–610. [Google Scholar] [CrossRef]
- Sung, Y.; Ashame, M.; Chen, S.; MacRae, T.; Sorgeloos, P.; Bossier, P. Feeding Artemia franciscana (Kellogg) Larvae with Bacterial Heat Shock Protein, Protects from Vibrio campbellii Infection. J. Fish Dis. 2009, 32, 675–685. [Google Scholar] [CrossRef] [PubMed]
- Baruah, K.; Ranjan, J.; Sorgeloos, P.; MacRae, T.H.; Bossier, P. Priming the Prophenoloxidase System of Artemia franciscana by Heat Shock Proteins Protects against Vibrio campbellii Challenge. Fish Shellfish Immunol. 2011, 31, 134–141. [Google Scholar] [CrossRef] [PubMed]
- Dierckens, K.; Rekecki, A.; Laureau, S.; Sorgeloos, P.; Boon, N.; Van den Broeck, W.; Bossier, P. Development of a Bacterial Challenge Test for Gnotobiotic Sea Bass (Dicentrarchus labrax) Larvae. Environ. Microbiol. 2009, 11, 526–533. [Google Scholar] [CrossRef]
- Reyes-López, F.E.; Aerts, J.; Vallejos-Vidal, E.; Ampe, B.; Dierckens, K.; Tort, L.; Bossier, P. Modulation of Innate Immune-Related Genes and Glucocorticoid Synthesis in Gnotobiotic Full-Sibling European Sea Bass (Dicentrarchus labrax) Larvae Challenged with Vibrio anguillarum. Front. Immunol. 2018, 9, 914. [Google Scholar] [CrossRef] [PubMed]
- Pfaffl, M.W.; Tichopad, A.; Prgomet, C.; Neuvians, T.P. Determination of Stable Housekeeping Genes, Differentially Regulated Target Genes and Sample Integrity: BestKeeper--Excel-Based Tool Using Pair-Wise Correlations. Biotechnol. Lett. 2004, 26, 509–515. [Google Scholar] [CrossRef]
- Mitter, K.; Kotoulas, G.; Magoulas, A.; Mulero, V.; Sepulcre, P.; Figueras, A.; Novoa, B.; Sarropoulou, E. Evaluation of Candidate Reference Genes for QPCR during Ontogenesis and of Immune-Relevant Tissues of European Seabass (Dicentrarchus labrax). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2009, 153, 340–347. [Google Scholar] [CrossRef]
- Pfaffl, M.W. A New Mathematical Model for Relative Quantification in Real-Time RT-PCR. Nucleic Acids Res. 2001, 29, e45. [Google Scholar] [CrossRef]
- Ma, F.; Luo, L.T.; Wang, Q. Hsp60/10 and SHsp Families of Heat Shock Protein Genes in Rainbow Trout (Oncorhynchus mykiss) and Their Expression under Heat Stress. Aquac. Int. 2022, 30, 1–18. [Google Scholar] [CrossRef]
- Lange, M.D.; Beck, B.H.; Brown, J.D.; Farmer, B.D.; Barnett, L.M.; Webster, C.D. Missing the Target: DNAk Is a Dominant Epitope in the Humoral Immune Response of Channel Catfish (Ictalurus punctatus) to Flavobacterium Columnare. Fish Shellfish Immunol. 2016, 51, 170–179. [Google Scholar] [CrossRef]
- Camberg, J.L.; Doyle, S.M.; Jhonston, D.M.; Wickner, S. Molecular Chaperones. In Brenner’s Encyclopedia of Genetics; Elsevier: Amsterdam, The Netherlands, 2013; pp. 456–460. [Google Scholar]
- Sung, Y.; MacRae, T. Heat Shock Proteins and Disease Control in Aquatic Organisms. J. Aquac. Res. Dev. 2011, S2, 006. [Google Scholar] [CrossRef]
- Frans, I.; Michiels, C.W.; Bossier, P.; Willems, K.A.; Lievens, B.; Rediers, H. Vibrio anguillarum as a Fish Pathogen: Virulence Factors, Diagnosis and Prevention. J. Fish Dis. 2011, 34, 643–661. [Google Scholar] [CrossRef] [PubMed]
- Rekecki, A.; Gunasekara, R.A.Y.S.A.; Dierckens, K.; Laureau, S.; Boon, N.; Favoreel, H.; Cornelissen, M.; Sorgeloos, P.; Ducatelle, R.; Bossier, P.; et al. Bacterial Host Interaction of GFP-Labelled Vibrio anguillarum HI-610 with Gnotobiotic Sea Bass, Dicentrarchus labrax (L.), Larvae. J. Fish Dis. 2012, 35, 265–273. [Google Scholar] [CrossRef] [PubMed]
- Basu, N.; Nakano, T.; Grau, E.G.; Iwama, G.K. The Effects of Cortisol on Heat Shock Protein 70 Levels in Two Fish Species. Gen. Comp. Endocrinol. 2001, 124, 97–105. [Google Scholar] [CrossRef] [PubMed]
- Stolte, E.H.; Chadzinska, M.; Przybylska, D.; Flik, G.; Savelkoul, H.; Verburg-van Kemenade, B.L. The Immune Response Differentially Regulates Hsp70 and Glucocorticoid Receptor Expression in Vitro and in Vivo in Common Carp (Cyprinus carpio L.). Fish Shellfish Immunol. 2009, 27, 9–16. [Google Scholar] [CrossRef]
- Valero, Y.; Arizcun, M.; Cortés, J.; Ramírez-Cepeda, F.; Guzmán, F.; Mercado, L.; Esteban, M.Á.; Chaves-Pozo, E.; Cuesta, A. NK-Lysin, Dicentracin and Hepcidin Antimicrobial Peptides in European Sea Bass. Ontogenetic Development and Modulation in Juveniles by Nodavirus. Dev. Comp. Immunol. 2020, 103, 103516. [Google Scholar] [CrossRef]
- Buchmann, K.; Secombes, C.J. Principles of Fish Immunology, 1st ed.; Buchmann, K., Secombes, C.J., Eds.; Springer International Publishing: Cham, Switzerland, 2022. [Google Scholar]
- Talbot, A.T.; Pottinger, T.G.; Smith, T.J.; Cairns, M.T. Acute Phase Gene Expression in Rainbow Trout (Oncorhynchus mykiss) after Exposure to a Confinement Stressor: A Comparison of Pooled and Individual Data. Fish Shellfish Immunol. 2009, 27, 309–317. [Google Scholar] [CrossRef]
- Shi, Y.H.; Chen, K.; Ma, W.J.; Chen, J. Ayu C-Reactive Protein/Serum Amyloid P Agglutinates Bacteria and Inhibits Complement-Mediated Opsonophagocytosis by Monocytes/Macrophages. Fish Shellfish Immunol. 2018, 76, 58–67. [Google Scholar] [CrossRef]
- Magnadottir, B.; Gudmundsdottir, B.K.; Groman, D. Immuno-Histochemical Determination of Humoral Immune Markers within Bacterial Induced Granuloma Formation in Atlantic Cod (Gadus morhua L.). Fish Shellfish Immunol. 2013, 34, 1372–1375. [Google Scholar] [CrossRef]
- Cecchini, S.; Terova, G.; Caricato, G.; Saroglia, M. Lysozyme Activity in Embryos and Larvae of Sea Bass (Dicentrarchus labrax L.), Spawned by Broodstock Fed with Vitamin C Enriched Diets. Bull.-Eur. Assoc. Fish Pathol. 2000, 20, 120–124. [Google Scholar]
- Álvarez, C.A.; Acosta, F.; Montero, D.; Guzmán, F.; Torres, E.; Vega, B.; Mercado, L. Synthetic Hepcidin from Fish: Uptake and Protection against Vibrio anguillarum in Sea Bass (Dicentrarchus labrax). Fish Shellfish Immunol. 2016, 55, 662–670. [Google Scholar] [CrossRef]
- Wang, X.; Li, L.; Yuan, G.; Zhu, L.; Pei, C.; Hou, L.; Li, C.; Jiang, X.; Kong, X. Interleukin (IL)-22 in Common Carp (Cyprinus carpio L.): Immune Modulation, Antibacterial Defense, and Activation of the JAK-STAT Signaling Pathway. Fish Shellfish Immunol. 2022, 131, 796–808. [Google Scholar] [CrossRef] [PubMed]
- Liyanage, D.S.; Omeka, W.K.M.; Yang, H.; Lim, C.; Choi, C.Y.; Lee, J. Molecular Characterization of Fish Cytokine IL-17C from Amphiprion Clarkii and Its Immunomodulatory Effects on the Responses to Pathogen-Associated Molecular Patterns and Bacterial Challenges. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2022, 257, 110669. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.H.; Lin, H.T.; Foung, Y.F.; Han-You Lin, J. The Bioactivity of Teleost IL-6: IL-6 Protein in Orange-Spotted Grouper (Epinephelus coioides) Induces Th2 Cell Differentiation Pathway and Antibody Production. Dev. Comp. Immunol. 2012, 38, 285–294. [Google Scholar] [CrossRef] [PubMed]
- Galindo-Villegas, J.; Mulero, I.; García-Alcazar, A.; Muñoz, I.; Peñalver-Mellado, M.; Streitenberger, S.; Scapigliati, G.; Meseguer, J.; Mulero, V. Recombinant TNFα as Oral Vaccine Adjuvant Protects European Sea Bass against Vibriosis: Insights into the Role of the CCL25/CCR9 Axis. Fish Shellfish Immunol. 2013, 35, 1260–1271. [Google Scholar] [CrossRef]
- Guo, M.; Tang, X.; Sheng, X.; Xing, J.; Zhan, W. The Effects of IL-1β, IL-8, G-CSF and TNF-α as Molecular Adjuvant on the Immune Response to an E. Tarda Subunit Vaccine in Flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 2018, 77, 374–384. [Google Scholar] [CrossRef]
- Huang, Y.; Chen, Z.; Zhang, J.; Amoah, K.; Asiedu, B.; Cai, J.; Wang, B.; Jian, J. Novel C-Type Lectin Mediated Non-Specific Cytotoxic Cells Killing Activity through NCCRP-1 in Nile Tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 2024, 149, 109594. [Google Scholar] [CrossRef]
- Li, J.H.; Yu, Z.L.; Xue, N.N.; Zou, P.F.; Hu, J.Y.; Nie, P.; Chang, M.X. Molecular Cloning and Functional Characterization of Peptidoglycan Recognition Protein 6 in Grass Carp Ctenopharyngodon Idella. Dev. Comp. Immunol. 2014, 42, 244–255. [Google Scholar] [CrossRef]
- Sun, Y.; Cao, Z.; Zhang, P.; Wei, C.; Li, J.; Wu, Y.; Zhou, Y. IFN Regulatory Factor 3 of Golden Pompano and Its NLS Domain Are Involved in Antibacterial Innate Immunity and Regulate the Expression of Type I Interferon (IFNa3). Front. Immunol. 2023, 14, 1128196. [Google Scholar] [CrossRef]
- Chistiakov, D.A.; Kabanov, F.V.; Troepolskaya, O.D.; Tischenko, M.M. A Variant of the Interleukin-1β Gene in European Sea Bass, Dicentrarchus labrax L., Is Associated with Increased Resistance against Vibrio anguillarum. J. Fish Dis. 2010, 33, 759–767. [Google Scholar] [CrossRef]
- Reyes-Cerpa, S.; Vallejos-Vidal, E.; Gonzalez-Bown, M.J.; Morales-Reyes, J.; Pérez-Stuardo, D.; Vargas, D.; Imarai, M.; Cifuentes, V.; Spencer, E.; Sandino, A.M.; et al. Effect of Yeast (Xanthophyllomyces dendrorhous) and Plant (Saint John’s Wort, Lemon Balm, and Rosemary) Extract Based Functional Diets on Antioxidant and Immune Status of Atlantic Salmon (Salmo salar) Subjected to Crowding Stress. Fish Shellfish Immunol. 2018, 74, 250–259. [Google Scholar] [CrossRef]
- Sepulcre, M.P.; Sarropoulou, E.; Kotoulas, G.; Meseguer, J.; Mulero, V. Vibrio anguillarum Evades the Immune Response of the Bony Fish Sea Bass (Dicentrarchus labrax L.) through the Inhibition of Leukocyte Respiratory Burst and down-Regulation of Apoptotic Caspases. Mol. Immunol. 2007, 44, 3751–3757. [Google Scholar] [CrossRef] [PubMed]
- Meloni, M.; Candusso, S.; Galeotti, M.; Volpatti, D. Preliminary Study on Expression of Antimicrobial Peptides in European Sea Bass (Dicentrarchus labrax) Following in Vivo Infection with Vibrio anguillarum. A Time Course Experiment. Fish Shellfish Immunol. 2015, 43, 82–90. [Google Scholar] [CrossRef] [PubMed]
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Vallejos-Vidal, E.; Fierro-Castro, C.; Santillán-Araneda, M.J.; Goldstein, M.; Reyes-Cerpa, S.; Balasch, J.C.; Khansari, A.R.; Dierckens, K.; Bossier, P.; Tort, L.; et al. The Administration of Heat Shock Protein-70 Bacterial Homolog (DnaK) Improves the Cumulative Survival and the Expression of Immune-Related Genes in Gnotobiotic Full-Sibling Sea Bass Larvae Challenged with Vibrio anguillarum. Animals 2025, 15, 1655. https://doi.org/10.3390/ani15111655
Vallejos-Vidal E, Fierro-Castro C, Santillán-Araneda MJ, Goldstein M, Reyes-Cerpa S, Balasch JC, Khansari AR, Dierckens K, Bossier P, Tort L, et al. The Administration of Heat Shock Protein-70 Bacterial Homolog (DnaK) Improves the Cumulative Survival and the Expression of Immune-Related Genes in Gnotobiotic Full-Sibling Sea Bass Larvae Challenged with Vibrio anguillarum. Animals. 2025; 15(11):1655. https://doi.org/10.3390/ani15111655
Chicago/Turabian StyleVallejos-Vidal, Eva, Camino Fierro-Castro, María Jesús Santillán-Araneda, Merari Goldstein, Sebastián Reyes-Cerpa, Joan Carles Balasch, Ali Reza Khansari, Kristof Dierckens, Peter Bossier, Lluis Tort, and et al. 2025. "The Administration of Heat Shock Protein-70 Bacterial Homolog (DnaK) Improves the Cumulative Survival and the Expression of Immune-Related Genes in Gnotobiotic Full-Sibling Sea Bass Larvae Challenged with Vibrio anguillarum" Animals 15, no. 11: 1655. https://doi.org/10.3390/ani15111655
APA StyleVallejos-Vidal, E., Fierro-Castro, C., Santillán-Araneda, M. J., Goldstein, M., Reyes-Cerpa, S., Balasch, J. C., Khansari, A. R., Dierckens, K., Bossier, P., Tort, L., & Reyes-López, F. E. (2025). The Administration of Heat Shock Protein-70 Bacterial Homolog (DnaK) Improves the Cumulative Survival and the Expression of Immune-Related Genes in Gnotobiotic Full-Sibling Sea Bass Larvae Challenged with Vibrio anguillarum. Animals, 15(11), 1655. https://doi.org/10.3390/ani15111655