Main Article Content
Abstract
Highlights:
1. This study analyzed the effects of using locally sourced pasak bumi extract and seluang fish on the parameters of neurogenesis in malnourished rat models.
2. It promotes further exploration into modified treatments for malnutrition, emphasizing nutritional strategies that harness locally available natural resources.
Abstract
Early developmental malnutrition exerts adverse effects on the structural, neurochemical, and neurophysiological maturation of cerebral cells by disrupting the process of neurogenesis. Pasak bumi (Eurycoma longifolia Jack) and seluang fish (Rasbora spp.), two indigenous natural resources of South Kalimantan, Indonesia, are believed to harbor nutritional components capable of mitigating these deleterious effects. We aimed to assess the impact of administering pasak bumi, seluang fish, and pure docosahexaenoic acid (DHA) on the neurogenesis process in malnourished rat models. The Rattus norvegicus specimens were partitioned into seven distinct cohorts, each consisting of five rats: healthy rats in the negative control group (KN), while malnourished rats in the positive control (KP) and treatment groups (P1, P2, P3, P4, and P5). Both the KP and KN groups received a placebo and a standard feed. The treatment groups received different interventions for five weeks: standard feed alongside pasak bumi extract for the P1 group, standard feed and DHA for the P2 group, standard feed in combination with pasak bumi extract and DHA for the P3 group, seluang fish for the P4 group, and pasak bumi extract and seluang fish for the P5 group. The doses determined for the pasak bumi extract and DHA were 15 and 1 mg/kg bw, respectively. The parameters evaluated consisted of the levels of brain-derived neurotrophic factor (BDNF), neural progenitor cell β-tubulin 3 (Tuj-1) expression, and peroxisome proliferator-activated receptor gamma (PPARγ). The data were subjected to analysis through the Kruskal-Wallis test and analysis of variance (ANOVA) at a 95% confidence level. A value of p<0.05 was considered significant. Statistically significant differences were observed in the BDNF levels (p=0.00) and Tuj-1 expressions (p=0.01) across all groups. In conclusion, the combined administration of pasak bumi and seluang fish demonstrates the capacity of enhancing neurogenesis in malnourished rats, as evidenced by elevated BDNF levels and Tuj-1 expressions.
Keywords
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References
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- Chen Y, Peng F, Xing Z, et al (2022). Beneficial effects of natural flavonoids on neuroinflammation. Frontiers in Immunology. doi: 10.3389/fimmu.2022.1006434.
- Cho YW, Kim DS, Suhito IR, et al (2019). Enhancing neurogenesis of neural stem cells using homogeneous nanohole pattern-modified conductive platform. International Journal of Molecular Sciences 21, 191. doi: 10.3390/ijms210 10191.
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- Gallo V, Deneen B (2014). Glial development: The crossroads of regeneration and repair in the CNS. Neuron 83, 283–308. doi: 10.1016/j.neuron.2014. 06.010.
- Georgieff MK, Ramel SE, Cusick SE (2018). Nutritional influences on brain development. Acta Paediatrica 107, 1310–1321. doi: 10.1111/apa.14 287.
- Gilmore JH, Knickmeyer RC, Gao W (2018). Imaging structural and functional brain development in early childhood. Nature Reviews Neuroscience 19, 123–137. doi: 10.1038/nrn.2018 .1.
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- de Guzman RM, Saulsbery AI, Workman JL (2018). High nursing demand reduces depression-like behavior despite increasing glucocorticoid concentrations and reducing hippocampal neurogenesis in late postpartum rats. Behavioural Brain Research 353, 143–153. doi: 10.1016/j.bbr.2018.07.012.
- Homem CCF, Repic M, Knoblich JA (2015). Proliferation control in neural stem and progenitor cells. Nature Reviews Neuroscience 16, 647–659. doi: 10.1038/nrn4021.
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- Krishna S, Cheng B, Sharma DR, et al (2021). PPAR-γ activation enhances myelination and neurological recovery in premature rabbits with intraventricular hemorrhage. Proceedings of the National Academy of Sciences. doi: 10.1073/pna s.2103084118.
- Liu Y, Yan Y, Inagaki Y, et al (2017). Insufficient astrocyte-derived brain-derived neurotrophic factor contributes to propofol-induced neuron death through Akt/Glycogen Synthase Kinase 3β/mitochondrial fission pathway. Anesthesia & Analgesia 125, 241–254. doi: 10.1213/ANE.0000 000000002137.
- Marwarha G, Claycombe-Larson K, Schommer J (2017). Maternal low-protein diet decreases brain-derived neurotrophic factor expression in the brains of the neonatal rat offspring. The Journal of Nutritional Biochemistry 45, 54-66. doi: 10.1016/j.jnutbio.2017.03.005.
- Matias I, Buosi AS, Gomes FCA (2016). Functions of flavonoids in the central nervous system: Astrocytes as targets for natural compounds. Neurochemistry International 95, 85–91. doi: 10.1016/j.neuint.2016.01.009.
- Minocha T, Birla H, Obaid AA, et al (2022). Flavonoids as promising neuroprotectants and their therapeutic potential against alzheimer’s disease ed. Aqib AI. Oxidative Medicine and Cellular Longevity 2022, 1–13. doi: 10.1155/2022 /6038996.
- Miranda M, Morici JF, Zanoni MB, et al (2019). Brain-derived neurotrophic factor: A key molecule for memory in the healthy and the pathological brain. Frontiers in Cellular Neuroscience. doi: 10.3389/fncel.2019.00363.
- Mudjihartini N (2021). Brain-derived neurotrophic factor (BDNF) and aging: A review. Jurnal Biomedika dan Kesehatan 4, 120–129. doi: 10.18051/JBiomedKes.2021.v4.120-129.
- Naik AA, Patro N, Seth P, et al (2017). Intra-generational protein malnutrition impairs temporal astrogenesis in rat brain. Biology Open. doi: 10.1242/bio.023432.
- Pérez-García G, Guzmán-Quevedo O, Da Silva Aragão R, et al (2016). Early malnutrition results in long-lasting impairments in pattern-separation for overlapping novel object and novel location memories and reduced hippocampal neurogenesis. Scientific Reports 6, 21275. doi: 10.1038/srep 21275.
- Phatnani H, Maniatis T (2015). Astrocytes in neurodegenerative disease: Table 1. Cold Spring Harbor Perspectives in Biology 7, a020628. doi: 10.1101/cshperspect.a020628.
- Rushmore RJ, McGaughy JA, Amaral AC, et al (2021). The neural basis of attentional alterations in prenatally protein malnourished rats. Cerebral Cortex 31, 497–512. doi: 10.1093/cercor/bhaa239.
- Sanyoto DD, Triawanti, Noor MS (2021). The effect of ethanol extract of pasak bumi (Eurycoma longifolia Jack.) on neurogenesis and neuroinflammation of rat post protein malnutrition. IOP Conference Series: Earth and Environmental Science 913, 012091. doi: 10.1088/1755-1315/913/1/012091.
- Sanyoto DD, Triawanti T, Airlangga DI (2022). Neuro progenitor cells (NPCS) and PPARΓ expression in the brain of protein-deficient rats after administration of pasak bumi (Eurycoma longifolia Jack) extract. Berkala Kedokteran 18, 19. doi: 10.20527/jbk.v18i1.12798.
- Schwarzenberg SJ, Georgieff MK, Daniels S, et al (2018). Advocacy for improving nutrition in the first 1000 days to support childhood development and adult health. Pediatrics. doi: 10.1542/peds.2017-3716.
- Sung PS, Lin PY, Liu CH, et al (2020). Neuroinflammation and neurogenesis in Alzheimer’s disease and potential therapeutic approaches. International Journal of Molecular Sciences 21, 701. doi: 10.3390/ijms21030701.
- Triawanti, Sanyoto DD, Noor MS (2020). The supplementation of pasak bumi (Eurycoma longifolia Jack.) in undernourished rats to increase spatial memory through antioxidant mechanism. Clinical Nutrition Experimental 33, 49–59. doi: 10.1016/j.yclnex.2020.08.002.
- Triawanti, Sanyoto DD, Yunanto A (2018). Kapita selekta malnutrisi. Sari Mulia, Banjarmasin. Available at: https://repo-dosen.ulm.ac.id/bitstr eam/handle/123456789/18024/2. Kapita Selekta Mal Nutrisi.pdf?sequence=1.
- Ullah A, Munir S, Badshah SL, et al (2020). Important flavonoids and their role as a therapeutic agent. Molecules 25, 5243. doi: 10.3390/molecules25225243.
- Urbán N, Guillemot F (2014). Neurogenesis in the embryonic and adult brain: Same regulators, different roles. Frontiers in Cellular Neuroscience. doi: 10.3389/fncel.2014.00396.
- Lo Van A, Hachem M, Lagarde M, et al (2019). Omega-3 docosahexaenoic acid is a mediator of fate-decision of adult neural stem cells. International Journal of Molecular Sciences 20, 4240. doi: 10.3390/ijms20174240.
- Villapol S (2018). Roles of peroxisome proliferator-activated receptor gamma on brain and peripheral inflammation. Cellular and Molecular Neurobiology 38, 121–132. doi: 10.1007/s10571-017-0554-5.
- Waber DP, Bryce CP, Fitzmaurice GM, et al (2014). Neuropsychological outcomes at midlife following moderate to severe malnutrition in infancy. Neuropsychology 28, 530–540. doi: 10.1037/neu0000058.
- Wang C, Wang D, Xu J, et al (2018). DHA enriched phospholipids with different polar groups (PC and PS) had different improvements on MPTP-induced mice with Parkinson’s disease. Journal of Functional Foods 45, 417–426. doi: 10.1016/j.jff.2018.04.017.
- Wang S, Awad KS, Elinoff JM, et al (2015). G protein-coupled receptor 40 (GPR40) and peroxisome proliferator-activated receptor γ (PPARγ). Journal of Biological Chemistry 290, 19544–19557. doi: 10.1074/jbc.M115.638924.
- Yunanto A, Sanyoto DD, Noor MS, et al (2015). The quality of rat brain spatial memory and expression of peroxisome proliferator activated receptor (PPAR) which fed with seluang (Rasbora spp.). Journal of Life Sciences and Technologies. doi: 10.18178/jolst.3.2.43-47.
References
Abbink MR, van Deijk AF, Heine VM, et al (2019). The involvement of astrocytes in early‐life adversity induced programming of the brain. Glia 67, 1637–1653. doi: 10.1002/glia.23625.
Bakoyiannis I, Daskalopoulou A, Pergialiotis V, et al (2019). Phytochemicals and cognitive health: Are flavonoids doing the trick? Biomedicine & Pharmacotherapy 109, 1488–1497. doi: 10.1016/j.biopha.2018.10.086.
Basak S, Mallick R, Duttaroy AK (2020). Maternal docosahexaenoic acid status during pregnancy and its impact on infant neurodevelopment. Nutrients 12, 3615. doi: 10.3390/nu12123615.
Beekmann K, Rubió L, de Haan LHJ, et al (2015). The effect of quercetin and kaempferol aglycones and glucuronides on peroxisome proliferator-activated receptor-gamma (PPAR-γ). Food & Function 6, 1098–1107. doi: 10.1039/C5FO0007 6A.
Chen Y, Peng F, Xing Z, et al (2022). Beneficial effects of natural flavonoids on neuroinflammation. Frontiers in Immunology. doi: 10.3389/fimmu.2022.1006434.
Cho YW, Kim DS, Suhito IR, et al (2019). Enhancing neurogenesis of neural stem cells using homogeneous nanohole pattern-modified conductive platform. International Journal of Molecular Sciences 21, 191. doi: 10.3390/ijms210 10191.
Cichon N, Saluk-Bijak J, Gorniak L, et al (2020). Flavonoids as a natural enhancer of neuroplasticity—An overview of the mechanism of neurorestorative action. Antioxidants 9, 1035. doi: 10.3390/antiox9111035.
Cleophas TJ, Zwinderman AH (2016). Non-parametric tests for three or more samples (Friedman and Kruskal-Wallis). In Clinical Data Analysis on a Pocket Calculator, 193–7. Springer International Publishing, Cham. Available at: http://link.springer.com/10.1007/978-3-319-27104-0_34.
Decara J, Rivera P, López-Gambero AJ, et al (2020). Peroxisome proliferator-activated receptors: Experimental targeting for the treatment of inflammatory bowel diseases. Frontiers in Pharmacology. doi: 10.3389/fphar.2020.00730.
Falomir-Lockhart LJ, Cavazzutti GF, Giménez E, et al (2019). Fatty acid signaling mechanisms in neural cells: Fatty acid receptors. Frontiers in Cellular Neuroscience. doi: 10.3389/fncel.2019.00 162.
Fang Q, Liu J, Chen L, et al (2021). Taurine improves the differentiation of neural stem cells in fetal rats with intrauterine growth restriction via activation of the PKA-CREB-BDNF signaling pathway. Metabolic Brain Disease 36, 969–981. doi: 10.1007/s11011-021-00672-0.
Ferreira FF, Ribeiro FF, Rodrigues RS, et al (2018). Brain-derived neurotrophic factor (BDNF) role in cannabinoid-mediated neurogenesis. Frontiers in Cellular Neuroscience. doi: 10.3389/fncel.2018.00 441.
Gallo V, Deneen B (2014). Glial development: The crossroads of regeneration and repair in the CNS. Neuron 83, 283–308. doi: 10.1016/j.neuron.2014. 06.010.
Georgieff MK, Ramel SE, Cusick SE (2018). Nutritional influences on brain development. Acta Paediatrica 107, 1310–1321. doi: 10.1111/apa.14 287.
Gilmore JH, Knickmeyer RC, Gao W (2018). Imaging structural and functional brain development in early childhood. Nature Reviews Neuroscience 19, 123–137. doi: 10.1038/nrn.2018 .1.
Gómez-Soler M, Cordobilla B, Morató X, et al (2018). Triglyceride form of docosahexaenoic acid mediates neuroprotection in experimental parkinsonism. Frontiers in Neuroscience. doi: 10.3389/fnins.2018.00604.
Gonçalves JT, Schafer ST, Gage FH (2016). Adult neurogenesis in the hippocampus: From stem cells to behavior. Cell 167, 897–914. doi: 10.1016/j.cell.2016.10.021.
de Guzman RM, Saulsbery AI, Workman JL (2018). High nursing demand reduces depression-like behavior despite increasing glucocorticoid concentrations and reducing hippocampal neurogenesis in late postpartum rats. Behavioural Brain Research 353, 143–153. doi: 10.1016/j.bbr.2018.07.012.
Homem CCF, Repic M, Knoblich JA (2015). Proliferation control in neural stem and progenitor cells. Nature Reviews Neuroscience 16, 647–659. doi: 10.1038/nrn4021.
IBM Corp. 2015. IBM SPSS Statistics for Windows, Version 23.0. Armonk, NY: IBM Corp. Available at: https://www.ibm.com/support/pages/spss-stati stics-230-now-available-download.
Kazi JA, Yaakob NA (2015). Eurycoma longifolia Jack (Tongkat Ali) induced c-Fos Expression in Sensory and Motor Neurons of the Rat Brain Nervous System. Advances in Environmental Biology 9, 24–31. Available at: https://www. aensiweb.net/AENSIWEB/aeb/aeb/2015/Special IPN Langkawi (August)/24-31.pdf.
Khasanah Y, Ratnayani, Ariani D, et al (2015). In vivo study on albumin and total protein in white rat (Rattus Norvegicus) after feeding of enteral formula from tempe and local food. Procedia Food Science 3, 274–279. doi: 10.1016/j.profoo.2015. 01.030.
Krishna S, Cheng B, Sharma DR, et al (2021). PPAR-γ activation enhances myelination and neurological recovery in premature rabbits with intraventricular hemorrhage. Proceedings of the National Academy of Sciences. doi: 10.1073/pna s.2103084118.
Liu Y, Yan Y, Inagaki Y, et al (2017). Insufficient astrocyte-derived brain-derived neurotrophic factor contributes to propofol-induced neuron death through Akt/Glycogen Synthase Kinase 3β/mitochondrial fission pathway. Anesthesia & Analgesia 125, 241–254. doi: 10.1213/ANE.0000 000000002137.
Marwarha G, Claycombe-Larson K, Schommer J (2017). Maternal low-protein diet decreases brain-derived neurotrophic factor expression in the brains of the neonatal rat offspring. The Journal of Nutritional Biochemistry 45, 54-66. doi: 10.1016/j.jnutbio.2017.03.005.
Matias I, Buosi AS, Gomes FCA (2016). Functions of flavonoids in the central nervous system: Astrocytes as targets for natural compounds. Neurochemistry International 95, 85–91. doi: 10.1016/j.neuint.2016.01.009.
Minocha T, Birla H, Obaid AA, et al (2022). Flavonoids as promising neuroprotectants and their therapeutic potential against alzheimer’s disease ed. Aqib AI. Oxidative Medicine and Cellular Longevity 2022, 1–13. doi: 10.1155/2022 /6038996.
Miranda M, Morici JF, Zanoni MB, et al (2019). Brain-derived neurotrophic factor: A key molecule for memory in the healthy and the pathological brain. Frontiers in Cellular Neuroscience. doi: 10.3389/fncel.2019.00363.
Mudjihartini N (2021). Brain-derived neurotrophic factor (BDNF) and aging: A review. Jurnal Biomedika dan Kesehatan 4, 120–129. doi: 10.18051/JBiomedKes.2021.v4.120-129.
Naik AA, Patro N, Seth P, et al (2017). Intra-generational protein malnutrition impairs temporal astrogenesis in rat brain. Biology Open. doi: 10.1242/bio.023432.
Pérez-García G, Guzmán-Quevedo O, Da Silva Aragão R, et al (2016). Early malnutrition results in long-lasting impairments in pattern-separation for overlapping novel object and novel location memories and reduced hippocampal neurogenesis. Scientific Reports 6, 21275. doi: 10.1038/srep 21275.
Phatnani H, Maniatis T (2015). Astrocytes in neurodegenerative disease: Table 1. Cold Spring Harbor Perspectives in Biology 7, a020628. doi: 10.1101/cshperspect.a020628.
Rushmore RJ, McGaughy JA, Amaral AC, et al (2021). The neural basis of attentional alterations in prenatally protein malnourished rats. Cerebral Cortex 31, 497–512. doi: 10.1093/cercor/bhaa239.
Sanyoto DD, Triawanti, Noor MS (2021). The effect of ethanol extract of pasak bumi (Eurycoma longifolia Jack.) on neurogenesis and neuroinflammation of rat post protein malnutrition. IOP Conference Series: Earth and Environmental Science 913, 012091. doi: 10.1088/1755-1315/913/1/012091.
Sanyoto DD, Triawanti T, Airlangga DI (2022). Neuro progenitor cells (NPCS) and PPARΓ expression in the brain of protein-deficient rats after administration of pasak bumi (Eurycoma longifolia Jack) extract. Berkala Kedokteran 18, 19. doi: 10.20527/jbk.v18i1.12798.
Schwarzenberg SJ, Georgieff MK, Daniels S, et al (2018). Advocacy for improving nutrition in the first 1000 days to support childhood development and adult health. Pediatrics. doi: 10.1542/peds.2017-3716.
Sung PS, Lin PY, Liu CH, et al (2020). Neuroinflammation and neurogenesis in Alzheimer’s disease and potential therapeutic approaches. International Journal of Molecular Sciences 21, 701. doi: 10.3390/ijms21030701.
Triawanti, Sanyoto DD, Noor MS (2020). The supplementation of pasak bumi (Eurycoma longifolia Jack.) in undernourished rats to increase spatial memory through antioxidant mechanism. Clinical Nutrition Experimental 33, 49–59. doi: 10.1016/j.yclnex.2020.08.002.
Triawanti, Sanyoto DD, Yunanto A (2018). Kapita selekta malnutrisi. Sari Mulia, Banjarmasin. Available at: https://repo-dosen.ulm.ac.id/bitstr eam/handle/123456789/18024/2. Kapita Selekta Mal Nutrisi.pdf?sequence=1.
Ullah A, Munir S, Badshah SL, et al (2020). Important flavonoids and their role as a therapeutic agent. Molecules 25, 5243. doi: 10.3390/molecules25225243.
Urbán N, Guillemot F (2014). Neurogenesis in the embryonic and adult brain: Same regulators, different roles. Frontiers in Cellular Neuroscience. doi: 10.3389/fncel.2014.00396.
Lo Van A, Hachem M, Lagarde M, et al (2019). Omega-3 docosahexaenoic acid is a mediator of fate-decision of adult neural stem cells. International Journal of Molecular Sciences 20, 4240. doi: 10.3390/ijms20174240.
Villapol S (2018). Roles of peroxisome proliferator-activated receptor gamma on brain and peripheral inflammation. Cellular and Molecular Neurobiology 38, 121–132. doi: 10.1007/s10571-017-0554-5.
Waber DP, Bryce CP, Fitzmaurice GM, et al (2014). Neuropsychological outcomes at midlife following moderate to severe malnutrition in infancy. Neuropsychology 28, 530–540. doi: 10.1037/neu0000058.
Wang C, Wang D, Xu J, et al (2018). DHA enriched phospholipids with different polar groups (PC and PS) had different improvements on MPTP-induced mice with Parkinson’s disease. Journal of Functional Foods 45, 417–426. doi: 10.1016/j.jff.2018.04.017.
Wang S, Awad KS, Elinoff JM, et al (2015). G protein-coupled receptor 40 (GPR40) and peroxisome proliferator-activated receptor γ (PPARγ). Journal of Biological Chemistry 290, 19544–19557. doi: 10.1074/jbc.M115.638924.
Yunanto A, Sanyoto DD, Noor MS, et al (2015). The quality of rat brain spatial memory and expression of peroxisome proliferator activated receptor (PPAR) which fed with seluang (Rasbora spp.). Journal of Life Sciences and Technologies. doi: 10.18178/jolst.3.2.43-47.