Ginseng total saponins rescue susceptibility to adult depression-like behaviors in mice induced by early-life stress via regulating CREB/BDNF/TrkB signaling

References

• Advani, T., Koek, W., & Hensler, J. G. (2009). Gender differences in the enhanced vulnerability of BDNF+/− mice to mild stress. The International Journal of Neuropsychopharmacology / Official Scientific Journal of the Collegium Internationale Neuropsychopharmacologicum (CINP), 12(5), 583–588. https://doi.org/10.1017/S1461145709000248
   PubMed Web of Science ®Google Scholar
• Anda, R. F., Felitti, V. J., Bremner, J. D., Walker, J. D., Whitfield, C., Perry, B. D., Dube, S. R., & Giles, W. H. (2006). The enduring effects of abuse and related adverse experiences in childhood: A convergence of evidence from neurobiology and epidemiology. European Archives of Psychiatry and Clinical Neuroscience, 256(3), 174–186. https://doi.org/10.1007/s00406-005-0624-4
   PubMed Web of Science ®Google Scholar
• Baugher, B. J., & Sachs, B. D. (2022). Early life maternal separation induces sex-specific antidepressant-like responses but has minimal effects on adult stress susceptibility in mice. Frontiers in Behavioral Neuroscience, 16, 1–10. https://doi.org/10.3389/fnbeh.2022.941884
   Web of Science ®Google Scholar
• Bian, Y., Yang, L., Wang, Z., Wang, Q., Zeng, L., & Xu, G. (2015). Repeated three-hour maternal separation induces depression-like behavior and affects the expression of hippocampal plasticity-related proteins in C57BL/6N mice. Neural Plasticity, 2015, 5–11. https://doi.org/10.1155/2015/627837
   Web of Science ®Google Scholar
• Bian, Y., Yang, L., Zhao, M., Li, Z., Xu, Y., Zhou, G., Li, W., & Zeng, L. (2019). Identification of key genes and pathways in post-traumatic stress disorder using microarray analysis. Frontiers in Psychology, 10. https://doi.org/10.3389/fpsyg.2019.00302
   Web of Science ®Google Scholar
• Caetano, S. C., Hatch, J. P., Brambilla, P., Sassi, R. B., Nicoletti, M., Mallinger, A. G., Frank, E., Kupfer, D. J., Keshavan, M. S., & Soares, J. C. (2004). Anatomical MRI study of hippocampus and amygdala in patients with current and remitted major depression. Psychiatry Research: Neuroimaging, 132(2), 141–147. https://doi.org/10.1016/j.pscychresns.2004.08.002
   Web of Science ®Google Scholar
• Chen, L., Dai, J., Wang, Z., Zhang, H., Huang, Y., & Zhao, Y. (2014). The antidepressant effects of ginseng total saponins in male C57BL/6N mice by enhancing hippocampal inhibitory phosphorylation of GSK-3β. Phytotherapy Research, 28(7), 1102–1106. https://doi.org/10.1002/ptr.5103
   PubMed Web of Science ®Google Scholar
• Chen, L., Wang, X., Lin, Z. X., Dai, J. G., Huang, Y. F., & Zhao, Y. N. (2017). Preventive effects of ginseng total saponins on chronic corticosterone-induced impairment in astrocyte structural plasticity and hippocampal atrophy. Phytotherapy Research, 31(9), 1341–1348. https://doi.org/10.1002/ptr.5859
   PubMed Web of Science ®Google Scholar
• Cipriani, A., Furukawa, T. A., Salanti, G., Chaimani, A., Atkinson, L. Z., Ogawa, Y., Leucht, S., Ruhe, H. G., Turner, E. H., Higgins, J. P. T., Egger, M., Takeshima, N., Hayasaka, Y., Imai, H., Shinohara, K., Tajika, A., Ioannidis, J. P. A., & Geddes, J. R. (2018). Comparative efficacy and acceptability of 21 antidepressant drugs for the acute treatment of adults with major depressive disorder: A systematic review and network meta-analysis. The Lancet, 391(10128), 1357–1366. https://doi.org/10.1016/S0140-6736(17)32802-7
   PubMed Web of Science ®Google Scholar
• Dandekar, M. P., Palepu, M. S. K., Satti, S., Jaiswal, Y., Singh, A. A., Dash, S. P., Gajula, S. N. R., & Sonti, R. (2022). Multi-strain probiotic formulation reverses maternal separation and chronic unpredictable mild stress-generated anxiety- and depression-like phenotypes by modulating gut microbiome–brain activity in rats. ACS Chemical Neuroscience, 13(13), 1948–1965. https://doi.org/10.1021/acschemneuro.2c00143
   PubMedGoogle Scholar
• Dang, H., Chen, Y., Liu, X., Wang, Q., Wang, L., Jia, W., & Wang, Y. (2009). Antidepressant effects of ginseng total saponins in the forced swimming test and chronic mild stress models of depression. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 33(8), 1417–1424. https://doi.org/10.1016/j.pnpbp.2009.07.020
   PubMed Web of Science ®Google Scholar
• Du, L., Wang, J., Meng, B., Yong, N., Yang, X., Huang, Q., Zhang, Y., Yang, L., Qu, Y., Chen, Z., Li, Y., Lv, F., & Hu, H. (2016). Early life stress affects limited regional brain activity in depression. Scientific Reports, 6(1), 6. https://doi.org/10.1038/srep25338
   PubMedGoogle Scholar
• Finkbeiner, S., Tavazoie, S. F., Maloratsky, A., Jacobs, K. M., Harris, K. M., & Greenberg, M. E. (1997). CREB: A major mediator of neuronal neurotrophin responses. Neuron, 19(5), 1031–1047. https://doi.org/10.1016/S0896-6273(00)80395-5
   PubMed Web of Science ®Google Scholar
• Goodwill, H. L., Manzano-Nieves, G., Gallo, M., Lee, H. I., Oyerinde, E., Serre, T., & Bath, K. G. (2019). Early life stress leads to sex differences in development of depressive-like outcomes in a mouse model. Neuropsychopharmacology, 44(4), 711–720. https://doi.org/10.1038/s41386-018-0195-5
   PubMed Web of Science ®Google Scholar
• Hanson, J. L., Nacewicz, B. M., Sutterer, M. J., Cayo, A. A., Schaefer, S. M., Rudolph, K. D., Shirtcliff, E. A., Pollak, S. D., & Davidson, R. J. (2015). Behavioral problems after early life stress: Contributions of the hippocampus and amygdala. Biological Psychiatry, 77(4), 314–323. https://doi.org/10.1016/j.biopsych.2014.04.020
   PubMed Web of Science ®Google Scholar
• Henriksson, B. G., Söderström, S., Gower, A. J., Ebendal, T., Winblad, B., & Mohammed, A. H. (1992). Hippocampal nerve growth factor levels are related to spatial learning ability in aged rats. Behavioural Brain Research, 48(1), 15–20. https://doi.org/10.1016/S0166-4328(05)80134-2
   PubMed Web of Science ®Google Scholar
• Hoshaw, B. A., Malberg, J. E., & Lucki, I. (2005). Central administration of IGF-I and BDNF leads to long-lasting antidepressant-like effects. Brain Research, 1037(1–2), 204–208. https://doi.org/10.1016/j.brainres.2005.01.007
   PubMed Web of Science ®Google Scholar
• Jeong, H. G., Ko, Y. H., Oh, S. Y., Han, C., Kim, T., & Joe, S. H. (2015). Effect of Korean red ginseng as an adjuvant treatment for women with residual symptoms of major depression. Asia-Pacific Psychiatry, 7(3), 330–336. https://doi.org/10.1111/appy.12169
   PubMed Web of Science ®Google Scholar
• Jiang, B., Xiong, Z., Yang, J., Wang, W., Wang, Y., Hu, Z. L., Wang, F., & Chen, J. G. (2012). Antidepressant-like effects of ginsenoside Rg1 are due to activation of the BDNF signalling pathway and neurogenesis in the hippocampus. British Journal of Pharmacology, 166(6), 1872–1887. https://doi.org/10.1111/j.1476-5381.2012.01902.x
   PubMed Web of Science ®Google Scholar
• Jiang, Z., Zhu, Z., Zhao, M., Wang, W., Li, H., Liu, D., & Pan, F. (2021). H3K9me2 regulation of BDNF expression in the hippocampus and medial prefrontal cortex is involved in the depressive-like phenotype induced by maternal separation in male rats. Psychopharmacology (Berl), 238(10), 2801–2813. https://doi.org/10.1007/s00213-021-05896-7
   PubMed Web of Science ®Google Scholar
• Jin, Y., Cui, R., Zhao, L., Fan, J., & Li, B. (2019). Mechanisms of panax ginseng action as an antidepressant. Cell Proliferation, 52(6). https://doi.org/10.1111/cpr.12696
   Web of Science ®Google Scholar
• Juruena, M. F. (2014). Early-life stress and HPA axis trigger recurrent adulthood depression. Epilepsy & Behavior: E&B, 38, 148–159. https://doi.org/10.1016/j.yebeh.2013.10.020
   PubMed Web of Science ®Google Scholar
• Karege, F., Vaudan, G., Schwald, M., Perroud, N., & La Harpe, R. (2005). Neurotrophin levels in postmortem brains of suicide victims and the effects of antemortem diagnosis and psychotropic drugs. Molecular Brain Research, 136(1–2), 29–37. https://doi.org/10.1016/j.molbrainres.2004.12.020
   PubMedGoogle Scholar
• Lee, K. H., Bahk, W. M., Lee, S. J., & Pae, C. U. (2020). Effectiveness and tolerability of Korean red ginseng augmentation in major depressive disorder patients with difficult-to-treat in routine practice. Clinical Psychopharmacology and Neuroscience: The Official Scientific Journal of the Korean College of Neuropsychopharmacology, 18(4), 621–626. https://doi.org/10.9758/CPN.2020.18.4.621
   PubMed Web of Science ®Google Scholar
• Lee, Y., & Han, P. L. (2019). Early-life stress in D2 heterozygous mice promotes autistic-like behaviors through the downregulation of the BDNF-TrkB pathway in the dorsal striatum. Experimental Neurobiology, 28(3), 337–351. https://doi.org/10.5607/en.2019.28.3.337
   PubMed Web of Science ®Google Scholar
• Liu, H., Atrooz, F., Salvi, A., & Salim, S. (2017). Behavioral and cognitive impact of early life stress: Insights from an animal model. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 78, 88–95. https://doi.org/10.1016/j.pnpbp.2017.05.015
   PubMed Web of Science ®Google Scholar
• Liu, H., Patki, G., Salvi, A., Kelly, M., & Salim, S. (2018). Behavioral effects of early life maternal trauma witness in rats. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 81, 80–87. https://doi.org/10.1016/j.pnpbp.2017.10.013
   PubMed Web of Science ®Google Scholar
• Lu, G., Liu, Z., Wang, X., & Wang, C. (2021). Recent advances in panax ginseng C.A. Meyer as a herb for anti-fatigue: An effects and mechanisms review. Foods, 10(5), 1030. https://doi.org/10.3390/foods10051030
   PubMed Web of Science ®Google Scholar
• Lu, J., Wang, X., Wu, A., Cao, Y., Dai, X., Liang, Y., & Li, X. (2022). Ginsenosides in central nervous system diseases: Pharmacological actions, mechanisms, and therapeutics. Phytotherapy Research, 36(4), 1523–1544. https://doi.org/10.1002/ptr.7395
   PubMed Web of Science ®Google Scholar
• Macrì, S., Zoratto, F., & Laviola, G. (2011). Early-stress regulates resilience, vulnerability and experimental validity in laboratory rodents through mother–offspring hormonal transfer. Neuroscience & Biobehavioral Reviews, 35(7), 1534–1543. https://doi.org/10.1016/j.neubiorev.2010.12.014
   PubMed Web of Science ®Google Scholar
• Malki, K., Keers, R., Tosto, M. G., Lourdusamy, A., Carboni, L., Domenici, E., Uher, R., McGuffin, P., & Schalkwyk, L. C. (2014). The endogenous and reactive depression subtypes revisited: Integrative animal and human studies implicate multiple distinct molecular mechanisms underlying major depressive disorder. BMC Medicine, 12(1), 1–14. https://doi.org/10.1186/1741-7015-12-73
   Google Scholar
• Mental, G. B. D., & Collaborators, D. (2022). Global, regional, and national burden of 12 mental disorders in 204 countries and territories, 1990–2019: A systematic analysis for the Global burden of disease study 2019. The Lancet Psychiatry, 9, 137–150. https://doi.org/10.1016/S2215-0366(21)00395-3
   PubMed Web of Science ®Google Scholar
• Nishinaka, T., Kinoshita, M., Nakamoto, K., & Tokuyama, S. (2015). Sex differences in depression-like behavior after nerve injury are associated with differential changes in brain-derived neurotrophic factor levels in mice subjected to early life stress. Neuroscience Letters, 592, 32–36. https://doi.org/10.1016/j.neulet.2015.02.053
   PubMed Web of Science ®Google Scholar
• Peña, C. J., Kronman, H. G., Walker, D. M., Cates, H. M., Bagot, R. C., Purushothaman, I., Issler, O., Eddie Loh, Y. H., Leong, T., Kiraly, D. D., Goodman, E., Neve, R. L., Shen, L., & Nestler, E. J. (2017). Early life stress confers lifelong stress susceptibility in mice via ventral tegmental area OTX2. Science, 356(80), 1185–1188. https://doi.org/10.1126/science.aan4491
   PubMedGoogle Scholar
• Pryce, C. R., & Feldon, J. (2003). Long-term neurobehavioural impact of the postnatal environment in rats: Manipulations, effects and mediating mechanisms. Neuroscience & Biobehavioral Reviews, 27(1–2), 57–71. https://doi.org/10.1016/s0149-7634(03)00009-5
   PubMed Web of Science ®Google Scholar
• Renard, G. M., Rivarola, M. A., & Suárez, M. M. (2007). Sexual dimorphism in rats: Effects of early maternal separation and variable chronic stress on pituitary-adrenal axis and behavior. International Journal of Developmental Neuroscience: The Official Journal of the International Society for Developmental Neuroscience, 25(6), 373–379. https://doi.org/10.1016/j.ijdevneu.2007.07.001
   PubMed Web of Science ®Google Scholar
• Renard, G. M., Rivarola, M. A., & Suárez, M. M. (2010). Gender-dependent effects of early maternal separation and variable chronic stress on vasopressinergic activity and glucocorticoid receptor expression in adult rats. Developmental Neuroscience, 32(1), 71–80. https://doi.org/10.1159/000280102
   PubMed Web of Science ®Google Scholar
• Rüedi-Bettschen, D., Feldon, J., & Pryce, C. R. (2004). Circadian- and temperature-specific effects of early deprivation on rat maternal care and pup development: Short-term markers for long-term effects. Developmental Psychobiology, 45(2), 59–71. https://doi.org/10.1002/dev.20014
   PubMed Web of Science ®Google Scholar
• Russo, S. J., & Nestler, E. J. (2013). The brain reward circuitry in mood disorders. Nature Reviews Neuroscience, 14(10), 736–736. https://doi.org/10.1038/nrn3381
   Web of Science ®Google Scholar
• Saleh, A., Potter, G. G., McQuoid, D. R., Boyd, B., Turner, R., MacFall, J. R., & Taylor, W. D. (2017). Effects of early life stress on depression, cognitive performance and brain morphology. Psychological Medicine, 47(1), 171–181. https://doi.org/10.1017/S0033291716002403
   PubMed Web of Science ®Google Scholar
• Schmidt, H. D., & Duman, R. S. (2010). Peripheral BDNF produces antidepressant-like effects in cellular and behavioral models. Neuropsychopharmacology, 35(12), 2378–2391. https://doi.org/10.1038/npp.2010.114
   PubMed Web of Science ®Google Scholar
• Seo, M. K., Ly, N. N., Lee, C. H., Cho, H. Y., Choi, C. M., Nhu, L. H., Lee, J. G., Lee, B. J., Kim, G. M., Yoon, B. J., Park, S. W., & Kim, Y. H. (2016). Early life stress increases stress vulnerability through BDNF gene epigenetic changes in the rat hippocampus. Neuropharmacology, 105, 388–397. https://doi.org/10.1016/j.neuropharm.2016.02.009
   PubMed Web of Science ®Google Scholar
• Torres-Berrío, A., Issler, O., Parise, E. M., & Nestler, E. J. (2019). Unraveling the epigenetic landscape of depression: Focus on early life stress. Dialogues in Clinical Neuroscience, 21(4), 341–357. https://doi.org/10.31887/DCNS.2019.21.4/enestler
   PubMed Web of Science ®Google Scholar
• Tractenberg, S. G., Levandowski, M. L., de Azeredo, L. A., Orso, R., Roithmann, L. G., Hoffmann, E. S., Brenhouse, H., & Grassi-Oliveira, R. (2016). An overview of maternal separation effects on behavioural outcomes in mice: Evidence from a four-stage methodological systematic review. Neuroscience & Biobehavioral Reviews, 68, 489–503. https://doi.org/10.1016/j.neubiorev.2016.06.021
   PubMed Web of Science ®Google Scholar
• Vetulani, J. (2013). Early maternal separation: A rodent model of depression and a prevailing human condition. Pharmacological Reports, 65(6), 1451–1461. https://doi.org/10.1016/S1734-1140(13)71505-6
   PubMed Web of Science ®Google Scholar
• Wang, Z., Dai, J., Chen, L., Huang, Y., & Zhao, Y. (2011). Preventive action of panax ginseng roots in hypercortisolism-induced impairment of hippocampal neurons in male C57BL/6N mice. Phytotherapy Research, 25(8), 1242–1245. https://doi.org/10.1002/ptr.3389
   PubMed Web of Science ®Google Scholar
• Wang, G., Lei, C., Tian, Y., Wang, Y., Zhang, L., & Zhang, R. (2019). Rb1, the primary active ingredient in panax ginseng C.A. Meyer, exerts antidepressant-like effects via the BDNF-TrkB-CREB pathway. Frontiers in Pharmacology, 10, 1–12. https://doi.org/10.3389/fphar.2019.01034
   PubMed Web of Science ®Google Scholar
• Wang, W., Wang, G. J., Xie, H. T., Sun, J. G., Zhao, S., Jiang, X. L., Li, H., Lv, H., Xu, M. J., & Wang, R. (2007). Determination of ginsenoside Rd in dog plasma by liquid chromatography–mass spectrometry after solid-phase extraction and its application in dog pharmacokinetics studies. Journal of Chromatography B Analytical Technologies in the Biomedical & Life Sciences, 852(1–2), 8–14. https://doi.org/10.1016/j.jchromb.2006.12.046
   PubMed Web of Science ®Google Scholar
• Wang, R., Wang, W., Xu, J., Liu, D., Jiang, H., & Pan, F. (2018). Dynamic effects of early adolescent stress on depressive-like behaviors and expression of cytokines and JMJD3 in the prefrontal cortex and hippocampus of rats. Frontiers in Psychiatry / Frontiers Research Foundation, 9. https://doi.org/10.3389/fpsyt.2018.00471
   Google Scholar
• Wang, W. K., Zhou, Y., Fan, L., Sun, Y., Ge, F., & Xue, M. (2021). The antidepressant-like effects of danggui buxue decoction in GK rats by activating CREB/BDNF/TrkB signaling pathway. Phytomedicine, 89, 153600. https://doi.org/10.1016/j.phymed.2021.153600
   PubMed Web of Science ®Google Scholar
• Williams, L. M., Debattista, C., Duchemin, A. M., Schatzberg, A. F., & Nemeroff, C. B. (2016). Childhood trauma predicts antidepressant response in adults with major depression: Data from the randomized international study to predict optimized treatment for depression. Translational Psychiatry, 6(5), e799. https://doi.org/10.1038/tp.2016.61
   PubMed Web of Science ®Google Scholar
• Ye, Y. L., Zhong, K., Liu, D. D., Xu, J., Pan, B. B., Li, X., Yu, Y. P., & Zhang, Q. (2017). Huanglian-jie-Du-tang extract ameliorates depression-like behaviors through BDNF-TrkB-CREB pathway in rats with chronic unpredictable stress. Evidence-Based Complementary and Alternative Medicine, 2017, 1–13. https://doi.org/10.1155/2017/7903918
   Web of Science ®Google Scholar
• Zhang, H., Chen, Z., Zhong, Z., Gong, W., & Li, J. (2018). Total saponins from the leaves of panax notoginseng inhibit depression on mouse chronic unpredictable mild stress model by regulating circRNA expression. Brain and Behavior, 8(11), 1–10. https://doi.org/10.1002/brb3.1127
   Web of Science ®Google Scholar
• Zhao, Y., Wang, Z., Dai, J., Chen, L., Huang, Y., & Zhan, Z. (2012). Beneficial effects of benzodiazepine diazepam on chronic stress-induced impairment of hippocampal structural plasticity and depression-like behavior in mice. Behavioural Brain Research, 228(2), 339–350. https://doi.org/10.1016/j.bbr.2011.12.013
   PubMed Web of Science ®Google Scholar
• Zhu, S., Shi, R., Wang, J., Wang, J. F., & Li, X. M. (2014). Unpredictable chronic mild stress not chronic restraint stress induces depressive behaviours in mice. Neuroreport, 25(14), 1151–1155. https://doi.org/10.1097/WNR.0000000000000243
   PubMed Web of Science ®Google Scholar
• Zhu, S., Wang, J., Zhang, Y., Li, V., Kong, J., He, J., & Li, X. M. (2014). Unpredictable chronic mild stress induces anxiety and depression-like behaviors and inactivates AMP-activated protein kinase in mice. Brain Research, 1576, 81–90. https://doi.org/10.1016/j.brainres.2014.06.002
   PubMed Web of Science ®Google Scholar