Skip to main content

Advertisement

SpringerLink
Log in

Neuroprotection elicited by taurine in sporadic Alzheimer-like disease: benefits on memory and control of neuroinflammation in the hippocampus of rats

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

This study aimed to analyze whether taurine has a nootropic effect on short-term and long-term memory in a model of sporadic dementia of the Alzheimer’s type (SDAT). Moreover, we evaluated the immunoreactivity and insulin receptor (IR) distribution and markers for neurons and glial cells in the hippocampus of rats with SDAT and treated with taurine. For this, Male Wistar rats received STZ (ICV, 3 mg/kg, bilateral, 5ul per site, aCFS vehicle) and were treated with taurine (100 mg/kg orally, 1 time per day, saline vehicle) for 25 days. The animals were divided into 4 groups: vehicle (VE), taurine (TAU), ICV-STZ (STZ) and ICV-STZ plus taurine (STZ + TAU). At the end of taurine treatment, short- and long-term memory were assessed by performance on object recognition and Y-maze tasks. Insulin receptor (IR) was evaluated by immunoperoxidase while mature neurons (NeuN), astrocytes (GFAP, S100B, SOX9), and microglia (Iba-1) were evaluated by immunofluorescence. STZ induced worse spatial and recognition memory (INDEX) in YM and ORT tasks. Taurine protected against STZ-induced memory impairment. SDAT reduced the population of mature neurons as well as increased astrocytic and microglial reactivity, and taurine protected against these STZ-induced effects, mainly in the CA1 region of the hippocampus. Taurine increases IR expression in the hippocampus, and protects against the reduction in the density of this receptor in CA1 induced by STZ. In conclusion, these findings demonstrate that taurine is able to enhance memory, up-regulates IR in the hippocampus, protects the neuron population, and reduces the astrogliosis found in SDAT.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 7
Fig. 6
Fig. 8

Similar content being viewed by others

References

  1. Kim C, Cha YN (2014) Taurine chloramine produced from taurine under inflammation provides anti-inflammatory and cytoprotective effects. Amino Acids 46:89–100. https://doi.org/10.1007/s00726-013-1545-6

    Article  CAS  PubMed  Google Scholar 

  2. Wang GH, Jiang ZL, Fan XJ et al (2007) Neuroprotective effect of taurine against focal cerebral ischemia in rats possibly mediated by activation of both GABAA and glycine receptors. Neuropharmacology 52:1199–1209. https://doi.org/10.1016/j.neuropharm.2006.10.022

    Article  CAS  PubMed  Google Scholar 

  3. Sun M, Gu Y, Zhao Y, Xu C (2011) Protective functions of taurine against experimental stroke through depressing mitochondria-mediated cell death in rats. Amino Acids 40:1419–1429. https://doi.org/10.1007/s00726-010-0751-8

    Article  CAS  PubMed  Google Scholar 

  4. Sun M, Zhao Y, Gu Y, Xu C (2012) Anti-inflammatory mechanism of taurine against ischemic stroke is related to down-regulation of PARP and NF-jB. Amino Acids 42:1735–1747. https://doi.org/10.1007/s00726-011-0885-3

    Article  CAS  PubMed  Google Scholar 

  5. Silva SP, Zago AM, Carvalho FB et al (2021) Neuroprotective Effect of Taurine against Cell Death, Glial Changes, and Neuronal Loss in the Cerebellum of Rats Exposed to Chronic-Recurrent Neuroinflammation Induced by LPS. J Immunol Res 2021:. https://doi.org/10.1155/2021/7497185

  6. Rahmeier FL, Zavalhia LS, Tortorelli LS et al (2016) The effect of taurine and enriched environment on behaviour, memory and hippocampus of diabetic rats. Neurosci Lett 630:84–92. https://doi.org/10.1016/j.neulet.2016.07.032

    Article  CAS  PubMed  Google Scholar 

  7. Möller H-J, Graeber MB (1998) The case described by Alois Alzheimer in 1911. Eur Arch Psychiatry Clin Neurosci 248:111–122. https://doi.org/10.1007/s004060050027

    Article  PubMed  Google Scholar 

  8. Benilova I, Karran E, De Strooper B (2012) The toxic Aβ oligomer and Alzheimer’s disease: an emperor in need of clothes. Nat Neurosci 15:349–357. https://doi.org/10.1038/nn.3028

    Article  CAS  PubMed  Google Scholar 

  9. De Strooper B, Karran E (2016) The Cellular phase of Alzheimer’s Disease. Cell 164:603–615. https://doi.org/10.1016/j.cell.2015.12.056

    Article  CAS  PubMed  Google Scholar 

  10. Allen NJ (2014) Astrocyte regulation of synaptic behavior. Annu Rev Cell Dev Biol 30:439–463. https://doi.org/10.1146/annurev-cellbio-100913-013053

    Article  CAS  PubMed  Google Scholar 

  11. Sofroniew MV, Vinters HV (2010) Astrocytes: Biology and pathology. Acta Neuropathol 119:7–35. https://doi.org/10.1007/s00401-009-0619-8

    Article  PubMed  Google Scholar 

  12. Craft JM, Watterson DM, Marks A, Van Eldik LJ (2005) Enhanced susceptibility of S-100B transgenic mice to neuroinflammation and neuronal dysfunction induced by intracerebroventricular infusion of human β-amyloid. Glia 51:209–216. https://doi.org/10.1002/glia.20194

    Article  PubMed  Google Scholar 

  13. Sun W, Cornwell A, Li J et al (2017) SOX9 is an astrocyte-specific nuclear marker in the adult brain outside the neurogenic regions. J Neurosci 37:4493–4507. https://doi.org/10.1523/JNEUROSCI.3199-16.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Liu Y, Walter S, Stagi M et al (2005) LPS receptor (CD14): a receptor for phagocytosis of Alzheimer’s amyloid peptide. Brain 128:1778–1789. https://doi.org/10.1093/brain/awh531

    Article  PubMed  Google Scholar 

  15. Heneka MT, Carson MJ, Khoury J, El et al (2015) Neuroinflammation in Alzheimer’s disease. Lancet Neurol 14:388–405. https://doi.org/10.1016/S1474-4422(15)70016-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Furman JL, Sama DM, Gant JC et al (2012) Targeting astrocytes ameliorates neurologic changes in a mouse model of Alzheimer’s disease. J Neurosci 32:16129–16140. https://doi.org/10.1523/JNEUROSCI.2323-12.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Parkhurst CN, Yang G, Ninan I et al (2014) Microglia promote learning-dependent synapse formation through BDNF. 155:1596–1609. https://doi.org/10.1016/j.cell.2013.11.030.Microglia

  18. Chen Y, Liang Z, Tian Z et al (2014) Intracerebroventricular streptozotocin exacerbates alzheimer-like changes of 3xTg-AD mice. Mol Neurobiol 49:547–562. https://doi.org/10.1007/s12035-013-8539-y

    Article  CAS  PubMed  Google Scholar 

  19. Grünblatt E, Salkovic-Petrisic M, Osmanovic J et al (2007) Brain insulin system dysfunction in streptozotocin intracerebroventricularly treated rats generates hyperphosphorylated tau protein. J Neurochem 101:757–770. https://doi.org/10.1111/j.1471-4159.2006.04368.x

    Article  CAS  PubMed  Google Scholar 

  20. Kamat PK, Kalani A, Rai S et al (2016) Streptozotocin Intracerebroventricular-Induced neurotoxicity and brain insulin resistance: a therapeutic intervention for treatment of sporadic Alzheimer’s Disease (sAD)-Like Pathology. Mol Neurobiol 53:4548–4562. https://doi.org/10.1007/s12035-015-9384-y

    Article  CAS  PubMed  Google Scholar 

  21. Teixeira FC, Soares MSP, Blödorn EB et al (2022) Investigating the Effect of Inosine on Brain Purinergic receptors and neurotrophic and neuroinflammatory parameters in an experimental model of Alzheimer’s Disease. Mol Neurobiol 59:841–855. https://doi.org/10.1007/s12035-021-02627-z

    Article  CAS  PubMed  Google Scholar 

  22. Teixeira FC, Gutierres JM, Soares MSP et al (2020) Inosine protects against impairment of memory induced by experimental model of Alzheimer disease: a nucleoside with multitarget brain actions. Psychopharmacology 237:811–823. https://doi.org/10.1007/s00213-019-05419-5

    Article  CAS  PubMed  Google Scholar 

  23. Gutierres JM, Carvalho FB, Schetinger MRC et al (2014) Anthocyanins restore behavioral and biochemical changes caused by streptozotocin-induced sporadic dementia of Alzheimer’s type. Life Sci 96:7–17. https://doi.org/10.1016/j.lfs.2013.11.014

    Article  CAS  PubMed  Google Scholar 

  24. Pacheco SM, Soares MSP, Gutierres JM et al (2018) Anthocyanins as a potential pharmacological agent to manage memory deficit, oxidative stress and alterations in ion pump activity induced by experimental sporadic dementia of Alzheimer’s type. J Nutr Biochem 56:193–204. https://doi.org/10.1016/j.jnutbio.2018.02.014

    Article  CAS  PubMed  Google Scholar 

  25. Dodart JC, Mathis C, Ungerer A (1997) Scopolamine-induced deficits in a two-trial object recognition task in mice. NeuroReport 8:1173–1178. https://doi.org/10.1097/00001756-199703240-00023

    Article  CAS  PubMed  Google Scholar 

  26. Haider S, Sajid I, Batool Z, Madiha S, Sadir S, Kamil N et al (2020) Supplementation of Taurine insulates against oxidative stress, confers Neuroprotection and attenuates memory impairment in noise stress exposed male Wistar rats. Neurochem Res 45:2762–2774. https://doi.org/10.1007/s11064-020-03127-7

    Article  CAS  PubMed  Google Scholar 

  27. Javed H, Khan A, Vaibhav K et al (2013) Taurine ameliorates neurobehavioral, neurochemical and immunohistochemical changes in sporadic dementia of Alzheimer’s type (SDAT) caused by intracerebroventricular streptozotocin in rats. Neurol Sci 34:2181–2192. https://doi.org/10.1007/s10072-013-1444-3

    Article  PubMed  Google Scholar 

  28. Reeta KH, Singh D, Gupta YK (2017) Chronic treatment with taurine after intracerebroventricular streptozotocin injection improves cognitive dysfunction in rats by modulating oxidative stress, cholinergic functions and neuroinflammation. Neurochem Int 108:146–156. https://doi.org/10.1016/j.neuint.2017.03.006

    Article  CAS  PubMed  Google Scholar 

  29. Dou JT, Chen M, Dufour F et al (2005) Insulin receptor signaling in long-term memory consolidation following spatial learning. Learn Mem 12:646–655. https://doi.org/10.1101/lm.88005

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ronaghi A, Zibaii MI, Pandamooz S et al (2019) Entorhinal cortex stimulation induces dentate gyrus neurogenesis through insulin receptor signaling. Brain Res Bull 144:75–84. https://doi.org/10.1016/j.brainresbull.2018.11.011

    Article  CAS  PubMed  Google Scholar 

  31. Palmano K, Rowan A, Guillermo R et al (2015) The role of gangliosides in neurodevelopment. Nutrients 7:3891–3913. https://doi.org/10.3390/nu7053891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. El Idrissi A (2019) Taurine regulation of neuroendocrine function. Adv Exp Med Biol 1155:977–985. https://doi.org/10.1007/978-981-13-8023-5_81

    Article  CAS  PubMed  Google Scholar 

  33. Wang K, Shi Y, Liu W et al (2021) Taurine improves neuron injuries and cognitive impairment in a mouse Parkinson’s disease model through inhibition of microglial activation. Neurotoxicology 83:129–136. https://doi.org/10.1016/j.neuro.2021.01.002

    Article  CAS  PubMed  Google Scholar 

  34. Kowall NW, Beal MF (1991) Glutamate-, glutaminase‐, and taurine‐immunoreactive neurons develop neurofibrillary tangles in Alzheimer’s disease. Ann Neurol 29:162–167. https://doi.org/10.1002/ana.410290208

    Article  CAS  PubMed  Google Scholar 

  35. Du J, Lü W, Wu S et al (2015) Glycine receptor mechanism elucidated by electron cryo-microscopy. Nature 526:224–229. https://doi.org/10.1038/nature14853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Yu J, Zhu H, Lape R et al (2021) Mechanism of gating and partial agonist action in the glycine receptor. Cell 184:957–968e21. https://doi.org/10.1016/j.cell.2021.01.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Oh SJ, Lee HJ, Jeong YJ et al (2020) Evaluation of the neuroprotective effect of taurine in Alzheimer’s disease using functional molecular imaging. Sci Rep 10:1–9. https://doi.org/10.1038/s41598-020-72755-4

    Article  CAS  Google Scholar 

  38. Toma V, Al, Farcas AD, Parvu M et al (2017) CA3 hippocampal field: Cellular changes and its relation with blood nitro-oxidative stress reveal a balancing function of CA3 area in rats exposed to repetead restraint stress. Brain Res Bull 130:10–17. https://doi.org/10.1016/j.brainresbull.2016.12.012

    Article  CAS  PubMed  Google Scholar 

  39. Azevedo H, Khaled NA, Santos P et al (2018) Temporal analysis of hippocampal CA3 gene coexpression networks in a rat model of febrile seizures. DMM Dis Model Mech 11. https://doi.org/10.1242/dmm.029074

  40. Jha MK, Jo M, Kim JH, Suk K (2019) Microglia-Astrocyte Crosstalk: an intimate Molecular Conversation. Neuroscientist 25:227–240. https://doi.org/10.1177/1073858418783959

    Article  CAS  PubMed  Google Scholar 

  41. Farina C, Aloisi F, Meinl E (2007) Astrocytes are active players in cerebral innate immunity. Trends Immunol 28:138–145. https://doi.org/10.1016/j.it.2007.01.005

    Article  CAS  PubMed  Google Scholar 

  42. Heppner FL, Ransohoff RM, Becher B (2015) Immune attack: the role of inflammation in Alzheimer disease. Nat Rev Neurosci 16:358–372. https://doi.org/10.1038/nrn3880

    Article  CAS  PubMed  Google Scholar 

  43. Gupte R, Christian S, Keselman P et al (2019) Evaluation of taurine neuroprotection in aged rats with traumatic brain injury. Brain Imaging Behav 13:461–471. https://doi.org/10.1007/s11682-018-9865-5

    Article  PubMed  PubMed Central  Google Scholar 

  44. Vargas-Castro V, Gomez-Diaz R, Blanco-Alvarez VM et al (2021) Long-term taurine administration improves motor skills in a tubulinopathy rat model by decreasing oxidative stress and promoting myelination. Mol Cell Neurosci 115. https://doi.org/10.1016/j.mcn.2021.103643

  45. Wang K, Zhang B, Tian T et al (2022) Taurine protects dopaminergic neurons in paraquat-induced Parkinson’s disease mouse model through PI3K/Akt signaling pathways. Amino Acids 54:1–11. https://doi.org/10.1007/s00726-021-03104-6

    Article  CAS  PubMed  Google Scholar 

  46. Liu K, Zhu R, Jiang H et al (2022) Taurine inhibits KDM3a production and microglia activation in lipopolysaccharide-treated mice and BV-2 cells. Mol Cell Neurosci 122:103759. https://doi.org/10.1016/j.mcn.2022.103759

    Article  CAS  PubMed  Google Scholar 

  47. Quintas C, Vale N, Gonçalves J, Queiroz G (2018) Microglia P2Y13 receptors prevent astrocyte proliferation mediated by P2Y1 receptors. Front Pharmacol 9:1–12. https://doi.org/10.3389/fphar.2018.00418

    Article  CAS  Google Scholar 

  48. Park JS, Kam TI, Lee S et al (2021) Blocking microglial activation of reactive astrocytes is neuroprotective in models of Alzheimer’s disease. Acta Neuropathol Commun 9:1–15. https://doi.org/10.1186/s40478-021-01180-z

    Article  CAS  Google Scholar 

  49. Villarreal A, Vidos C, Monteverde Busso M et al (2021) Pathological Neuroinflammatory Conversion of reactive astrocytes is Induced by Microglia and involves chromatin remodeling. Front Pharmacol 12:1–15. https://doi.org/10.3389/fphar.2021.689346

    Article  CAS  Google Scholar 

  50. Zhang H, Wang D, Gong P et al (2019) Formyl peptide receptor 2 Deficiency improves cognition and attenuates tau hyperphosphorylation and astrogliosis in a mouse model of Alzheimer’s Disease. J Alzheimer’s Dis 67:169–179. https://doi.org/10.3233/JAD-180823

    Article  CAS  Google Scholar 

  51. Su Y, Fan W, Ma Z et al (2014) Taurine improves functional and histological outcomes and reduces inflammation in traumatic brain injury. Neuroscience 266:56–65. https://doi.org/10.1016/j.neuroscience.2014.02.006

    Article  CAS  PubMed  Google Scholar 

  52. Donato R, Sorci G, Riuzzi F et al (2009) S100B’s double life: intracellular regulator and extracellular signal. Biochim Biophys Acta - Mol Cell Res 1793:1008–1022. https://doi.org/10.1016/j.bbamcr.2008.11.009

    Article  CAS  Google Scholar 

  53. Wartchow KM, Rodrigues L, Swierzy I et al (2021) Amyloid-β processing in aged s100b transgenic mice is sex dependent. Int J Mol Sci 22. https://doi.org/10.3390/ijms221910823

  54. Huttunen HJ, Kuja-Panula J, Sorci G et al (2000) Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (RAGE) activation. J Biol Chem 275:40096–40105. https://doi.org/10.1074/jbc.M006993200

    Article  CAS  PubMed  Google Scholar 

  55. Ma Rhong, Zhang Y, Hong X, yue et al (2017) Role of microtubule-associated protein tau phosphorylation in Alzheimer’s disease. J Huazhong Univ Sci Technol - Med Sci 37:307–312. https://doi.org/10.1007/s11596-017-1732-x

    Article  CAS  Google Scholar 

  56. Langeh U, Singh S (2020) Targeting S100B protein as a surrogate biomarker and its role in various neurological Disorders. Curr Neuropharmacol 19:265–277. https://doi.org/10.2174/1570159x18666200729100427

    Article  CAS  Google Scholar 

  57. Michetti F, D’Ambrosi N, Toesca A et al (2019) The S100B story: from biomarker to active factor in neural injury. J Neurochem 148:168–187. https://doi.org/10.1111/jnc.14574

    Article  CAS  PubMed  Google Scholar 

  58. Shimamoto S, Tsuchiya M, Yamaguchi F et al (2014) Ca2+/S100 proteins inhibit the interaction of FKBP38 with Bcl-2 and Hsp90. Biochem J 458:141–152. https://doi.org/10.1042/BJ20130924

    Article  CAS  PubMed  Google Scholar 

  59. Li D, Li K, Chen G et al (2016) S100B suppresses the differentiation of C3H/10T1/2 murine embryonic mesenchymal cells into osteoblasts. Mol Med Rep 14:3878–3886. https://doi.org/10.3892/mmr.2016.5697

    Article  CAS  PubMed  Google Scholar 

  60. Tsoporis JN, Overgaard CB, Izhar S, Parker TG (2009) S100B modulates the hemodynamic response to norepinephrine stimulation. Am J Hypertens 22:1048–1053. https://doi.org/10.1038/ajh.2009.145

    Article  CAS  PubMed  Google Scholar 

  61. Wen XH, Duda T, Pertzev A et al (2012) S100B serves as a ca 2 + sensor for ROS-GC1 guanylate cyclase in cones but not in rods of the murine retina. Cell Physiol Biochem 29:417–430. https://doi.org/10.1159/000338496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Agam G, Almog O (2015) Calbindin D28k and S100B have a similar interaction site with the lithium-inhibitable enzyme inositol monophosphatase-1: a new drug target site. J Med Chem 58:2042–2044. https://doi.org/10.1021/jm5019324

    Article  CAS  PubMed  Google Scholar 

  63. Gógl G, Alexa A, Kiss B et al (2016) Structural basis of ribosomal S6 kinase 1 (RSK1) inhibition by S100B protein: modulation of the extracellular signal-regulated kinase (ERK) signaling cascade in a calcium-dependent way. J Biol Chem 291:11–27. https://doi.org/10.1074/jbc.M115.684928

    Article  CAS  PubMed  Google Scholar 

  64. Lee SG, Yoo DY, Jung HY et al (2015) Neurons in the hippocampal CA1 region, but not the dentate gyrus, are susceptible to oxidative stress in rats with streptozotocin-induced type 1 diabetes. Neural Regen Res 10:451–456. https://doi.org/10.4103/1673-5374.153695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Zhang Y, Chen K, Sloan SA et al (2014) An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci 34:11929–11947. https://doi.org/10.1523/JNEUROSCI.1860-14.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Farmer WT, Abrahamsson T, Chierzi S et al (2016) Neurons diversify astrocytes in the adult brain through sonic hedgehog signaling. Sci (80-) 351:849–854. https://doi.org/10.1126/science.aab3103

    Article  CAS  Google Scholar 

  67. Nagao M, Ogata T, Sawada Y, Gotoh Y (2016) Zbtb20 promotes astrocytogenesis during neocortical development. Nat Commun 7:1–14. https://doi.org/10.1038/ncomms11102

    Article  CAS  Google Scholar 

  68. Zhang Y, Sloan SA, Clarke LE et al (2016) Purification and characterization of progenitor and mature human astrocytes reveals transcriptional and functional differences with mouse. Neuron 89:37–53. https://doi.org/10.1016/j.neuron.2015.11.013.Purification

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful for all the support offered by the technician of the Pathology Research Laboratory, Teresinha Stein.

Author information

Authors and Affiliations

  1. Pathology Research Laboratory, Federal University of Health Sciences of Porto Alegre, Sarmento Leite, 245, Room 514 - Building 3, Porto Alegre, CEP 90050-170, RS, Brazil

    Fernanda Huf, Jessié Martins Gutierres, Gabrielle N. da Silva, Adriana M. Zago, Luiz Felipe C. Koenig & Marilda C. Fernandes

Authors
  1. Fernanda Huf
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jessié Martins Gutierres
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gabrielle N. da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adriana M. Zago
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luiz Felipe C. Koenig
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marilda C. Fernandes
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F.H, A.M.Z, G.N.S and J.M.G performed stereotactic surgery, drug preparation and animal care; G.N.S and F.H performed behavioral tests; F.H, A.M.Z and G.N.S performed immunofluorescence assays; M.C.F, F.H and L.F.K performed the optical density microscopic analysis; J.M.G, M.C.F and F.H wrote the main text of the manuscript and J.M.G and F.H prepared scheme 1 and Figs. 1, 2, 3, 4, 5, 6 and 7. All authors reviewed the manuscript.

Corresponding authors

Correspondence to Jessié Martins Gutierres or Marilda C. Fernandes.

Ethics declarations

Competing interests

The authors declare no competing interests.

Founding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript. The authors would like to thank the scholarships that allowed the execution of this project. These scholarships were funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) Finance Code 001. Fernanda Huf, Gabrielle N. da Silva, Luiz Felipe C. Koenig and Adriana M. Zago received PhD scholarships from the CAPES program, and Jessié M. Gutierres was supported by the National Postdoctoral Program (PNPD/CAPES).

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huf, F., Gutierres, J.M., da Silva, G.N. et al. Neuroprotection elicited by taurine in sporadic Alzheimer-like disease: benefits on memory and control of neuroinflammation in the hippocampus of rats. Mol Cell Biochem (2023). https://doi.org/10.1007/s11010-023-04872-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11010-023-04872-3

Keywords

Search

Navigation