Skip to main content
SpringerLink
Log in

Augmented Mitochondrial Transfer Involved in Astrocytic PSPH Attenuates Cognitive Dysfunction in db/db Mice

  • Original Article
  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Diabetes-associated cognitive dysfunction (DACD) has ascended to become the second leading cause of mortality among diabetic patients. Phosphoserine phosphatase (PSPH), a pivotal rate-limiting enzyme in L-serine biosynthesis, has been documented to instigate the insulin signaling pathway through dephosphorylation. Concomitantly, CD38, acting as a mediator in mitochondrial transfer, is activated by the insulin pathway. Given that we have demonstrated the beneficial effects of exogenous mitochondrial supplementation on DACD, we further hypothesized whether astrocytic PSPH could contribute to improving DACD by promoting astrocytic mitochondrial transfer into neurons. In the Morris Water Maze (MWM) test, our results demonstrated that overexpression of PSPH in astrocytes alleviated DACD in db/db mice. Astrocyte specific-stimulated by PSPH lentivirus/ adenovirus promoted the spine density both in vivo and in vitro. Mechanistically, astrocytic PSPH amplified the expression of CD38 via initiation of the insulin signaling pathway, thereby promoting astrocytic mitochondria transfer into neurons. In summation, this comprehensive study delineated the pivotal role of astrocytic PSPH in alleviating DACD and expounded upon its intricate cellular mechanism involving mitochondrial transfer. These findings propose that the specific up-regulation of astrocytic PSPH holds promise as a discerning therapeutic modality for DACD.

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. 6
Scheme 1

Similar content being viewed by others

Data Availability

All data that support the fundings of this study are available from corresponding author upon reasonable request.

Abbreviations

AAV:

Adeno-Associated Viruses

ACM:

Astrocyte-Conditioned Media

AKT:

Protein Kinase B

ATP:

Adenosine Triphosphate

cADPR:

cyclic ADP-Ribose

CD38:

Cluster of Differentiation 38

CO-IP:

Co-Immunoprecipitation

DACD:

Diabetes-Associated Cognitive Dysfunction

DMEM:

Dulbecco?s Modified Eagle Medium

EDTA:

Ethylenediaminetetraacetic Acid

GFAP:

Glial Fibrillary Acidic Protein

GSK3?:

Glycogen Synthase Kinase-3?

HE:

Haematoxylin and Eosin

IF:

Immunofluorescent Staining

IRS-1:

Insulin Receptor Substrate 1

LV:

Lentivirus

MAPK:

Mitogen-Activated Protein Kinase

MWM:

Morris Water Maze

PSPH:

Phosphoserine Phosphatase

SDS-PAGE:

Sodium Dodecyl Sulfate Polyacrylamide Gel Electrophoresis

TUNEL:

TdT-Mediated dUTP Nick-End Labeling

T2DM:

Type 2 Diabetes Mellitus

References

  1. Valencia WM, Florez H (2017) How to prevent the microvascular complications of type 2 diabetes beyond glucose control. BMJ 356:i6505. https://doi.org/10.1136/bmj.i6505

    Article  PubMed  Google Scholar 

  2. Xue M, Xu W, Ou YN, Cao XP, Tan MS, Tan L, Yu JT (2019) Diabetes mellitus and risks of cognitive impairment and dementia: a systematic review and meta-analysis of 144 prospective studies. Ageing Res Rev 55:100944. https://doi.org/10.1016/j.arr.2019.100944

    Article  CAS  PubMed  Google Scholar 

  3. Biessels GJ, Whitmer RA (2020) Cognitive dysfunction in diabetes: how to implement emerging guidelines. Diabetologia 63(1):3–9. https://doi.org/10.1007/s00125-019-04977-9

    Article  PubMed  Google Scholar 

  4. Pearson-Stuttard J, Bennett J, Cheng YJ, Vamos EP, Cross AJ, Ezzati M, Gregg EW (2021) Trends in predominant causes of death in individuals with and without diabetes in England from 2001 to 2018: an epidemiological analysis of linked primary care records. Lancet Diabetes Endocrinol 9(3):165–173. https://doi.org/10.1016/S2213-8587(20)30431-9

    Article  PubMed  PubMed Central  Google Scholar 

  5. de Galan BE, Zoungas S, Chalmers J, Anderson C, Dufouil C, Pillai A, Cooper M, Grobbee DE, Hackett M, Hamet P, Heller SR, Lisheng L, MacMahon S, Mancia G, Neal B, Pan CY, Patel A, Poulter N, Travert F, Woodward M (2009) group AC Cognitive function and risks of cardiovascular disease and hypoglycaemia in patients with type 2 diabetes: the Action in Diabetes and Vascular Disease: Preterax and Diamicron Modified Release Controlled Evaluation (ADVANCE) trial. Diabetologia 52 (11):2328–2336. https://doi.org/10.1007/s00125-009-1484-7

  6. Holm LJ, Buschard K (2019) L-serine: a neglected amino acid with a potential therapeutic role in diabetes. APMIS 127(10):655–659. https://doi.org/10.1111/apm.12987

    Article  PubMed  PubMed Central  Google Scholar 

  7. Park SM, Seo EH, Bae DH, Kim SS, Kim J, Lin W, Kim KH, Park JB, Kim YS, Yin J, Kim SY (2019) Phosphoserine Phosphatase promotes Lung Cancer Progression through the dephosphorylation of IRS-1 and a noncanonical L-Serine-independent pathway. Mol Cells 42(8):604–616. https://doi.org/10.14348/molcells.2019.0160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kampen KR, Fancello L, Girardi T, Rinaldi G, Planque M, Sulima SO, Loayza-Puch F, Verbelen B, Vereecke S, Verbeeck J, Op de Beeck J, Royaert J, Vermeersch P, Cassiman D, Cools J, Agami R, Fiers M, Fendt SM, De Keersmaecker K (2019) Translatome analysis reveals altered serine and glycine metabolism in T-cell acute lymphoblastic leukemia cells. Nat Commun 10(1):2542. https://doi.org/10.1038/s41467-019-10508-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Vincent JB, Jamil T, Rafiq MA, Anwar Z, Ayaz M, Hameed A, Nasr T, Naeem F, Khattak NA, Carter M, Ahmed I, John P, Wiame E, Andrade DM, Schaftingen EV, Mir A, Ayub M (2015) Phosphoserine phosphatase (PSPH) gene mutation in an intellectual disability family from Pakistan. Clin Genet 87(3):296–298. https://doi.org/10.1111/cge.12445

    Article  CAS  PubMed  Google Scholar 

  10. Begum N, Sussman KE, Draznin B (1992) Calcium-induced inhibition of phosphoserine phosphatase in insulin target cells is mediated by the phosphorylation and activation of inhibitor 1. J Biol Chem 267(9):5959–5963

    Article  CAS  PubMed  Google Scholar 

  11. Giovannoni F, Quintana FJ (2020) The role of astrocytes in CNS inflammation. Trends Immunol 41(9):805–819. https://doi.org/10.1016/j.it.2020.07.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Sofroniew MV (2015) Astrocyte barriers to neurotoxic inflammation. Nat Rev Neurosci 16(5):249–263. https://doi.org/10.1038/nrn3898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Chung WS, Clarke LE, Wang GX, Stafford BK, Sher A, Chakraborty C, Joung J, Foo LC, Thompson A, Chen C, Smith SJ, Barres BA (2013) Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature 504(7480):394–400. https://doi.org/10.1038/nature12776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kreft M, Bak LK, Waagepetersen HS, Schousboe A (2012) Aspects of astrocyte energy metabolism, amino acid neurotransmitter homoeostasis and metabolic compartmentation. ASN Neuro 4(3). https://doi.org/10.1042/AN20120007

  15. Mills WA 3rd, Woo AM, Jiang S, Martin J, Surendran D, Bergstresser M, Kimbrough IF, Eyo UB, Sofroniew MV, Sontheimer H (2022) Astrocyte plasticity in mice ensures continued endfoot coverage of cerebral blood vessels following injury and declines with age. Nat Commun 13(1):1794. https://doi.org/10.1038/s41467-022-29475-2

  16. Rahman MH, Bhusal A, Kim JH, Jha MK, Song GJ, Go Y, Jang IS, Lee IK, Suk K (2020) Astrocytic pyruvate dehydrogenase kinase-2 is involved in hypothalamic inflammation in mouse models of diabetes. Nat Commun 11(1):5906. https://doi.org/10.1038/s41467-020-19576-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Gundersen V, Storm-Mathisen J, Bergersen LH (2015) Neuroglial Transmission. Physiol Rev 95(3):695–726. https://doi.org/10.1152/physrev.00024.2014

    Article  CAS  PubMed  Google Scholar 

  18. Tan Z, Liu Y, Xi W, Lou HF, Zhu L, Guo Z, Mei L, Duan S (2017) Glia-derived ATP inversely regulates excitability of pyramidal and CCK-positive neurons. Nat Commun 8:13772. https://doi.org/10.1038/ncomms13772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Koh W, Park M, Chun YE, Lee J, Shim HS, Park MG, Kim S, Sa M, Joo J, Kang H, Oh SJ, Woo J, Chun H, Lee SE, Hong J, Feng J, Li Y, Ryu H, Cho J, Lee CJ (2022) Astrocytes render memory flexible by releasing D-Serine and regulating NMDA receptor tone in the Hippocampus. Biol Psychiatry 91(8):740–752. https://doi.org/10.1016/j.biopsych.2021.10.012

    Article  CAS  PubMed  Google Scholar 

  20. Cheung G, Bataveljic D, Visser J, Kumar N, Moulard J, Dallerac G, Mozheiko D, Rollenhagen A, Ezan P, Mongin C, Chever O, Bemelmans AP, Lubke J, Leray I, Rouach N (2022) Physiological synaptic activity and recognition memory require astroglial glutamine. Nat Commun 13(1):753. https://doi.org/10.1038/s41467-022-28331-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hayakawa K, Esposito E, Wang X, Terasaki Y, Liu Y, Xing C, Ji X, Lo EH (2016) Transfer of mitochondria from astrocytes to neurons after stroke. Nature 535(7613):551–555. https://doi.org/10.1038/nature18928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Amin SN (2021) Platelets: the peripheral donor of mitochondria for diabetes-induced cognitive impairment. Clin Sci (Lond) 135(4):593–595. https://doi.org/10.1042/CS20201297

    Article  PubMed  Google Scholar 

  23. Cobley JN, Fiorello ML, Bailey DM (2018) 13 reasons why the brain is susceptible to oxidative stress. Redox Biol 15:490–503. https://doi.org/10.1016/j.redox.2018.01.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ma H, Jiang T, Tang W, Ma Z, Pu K, Xu F, Chang H, Zhao G, Gao W, Li Y, Wang Q (2020) Transplantation of platelet-derived mitochondria alleviates cognitive impairment and mitochondrial dysfunction in db/db mice. Clin Sci (Lond) 134(16):2161–2175. https://doi.org/10.1042/CS20200530

    Article  CAS  PubMed  Google Scholar 

  25. Ramos-Rodriguez JJ, Ortiz O, Jimenez-Palomares M, Kay KR, Berrocoso E, Murillo-Carretero MI, Perdomo G, Spires-Jones T, Cozar-Castellano I, Lechuga-Sancho AM, Garcia-Alloza M (2013) Differential central pathology and cognitive impairment in pre-diabetic and diabetic mice. Psychoneuroendocrinology 38(11):2462–2475. https://doi.org/10.1016/j.psyneuen.2013.05.010

    Article  PubMed  Google Scholar 

  26. Luo Q, Xian P, Wang T, Wu S, Sun T, Wang W, Wang B, Yang H, Yang Y, Wang H, Liu W, Long Q (2021) Antioxidant activity of mesenchymal stem cell-derived extracellular vesicles restores hippocampal neurons following seizure damage. Theranostics 11(12):5986–6005. https://doi.org/10.7150/thno.58632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Yamasaki M, Yamada K, Furuya S, Mitoma J, Hirabayashi Y, Watanabe M (2001) 3-Phosphoglycerate dehydrogenase, a key enzyme for l-serine biosynthesis, is preferentially expressed in the radial glia/astrocyte lineage and olfactory ensheathing glia in the mouse brain. J Neurosci 21(19):7691–7704. https://doi.org/10.1523/JNEUROSCI.21-19-07691.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Wolosker H, Radzishevsky I (2013) The serine shuttle between glia and neurons: implications for neurotransmission and neurodegeneration. Biochem Soc Trans 41(6):1546–1550. https://doi.org/10.1042/BST20130220

    Article  CAS  PubMed  Google Scholar 

  29. Akhtar MW, Sanz-Blasco S, Dolatabadi N, Parker J, Chon K, Lee MS, Soussou W, McKercher SR, Ambasudhan R, Nakamura T, Lipton SA (2016) Elevated glucose and oligomeric beta-amyloid disrupt synapses via a common pathway of aberrant protein S-nitrosylation. Nat Commun 7:10242. https://doi.org/10.1038/ncomms10242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Stranahan AM, Lee K, Martin B, Maudsley S, Golden E, Cutler RG, Mattson MP (2009) Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice. Hippocampus 19(10):951–961. https://doi.org/10.1002/hipo.20577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. von Bohlen Und Halbach O (2009) Structure and function of dendritic spines within the hippocampus. Ann Anat 191(6):518–531. https://doi.org/10.1016/j.aanat.2009.08.006

    Article  CAS  PubMed  Google Scholar 

  32. Shawl AI, Park KH, Kim UH (2009) Insulin receptor signaling for the proliferation of pancreatic beta-cells: involvement of Ca2 + second messengers, IP3, NAADP and cADPR. Islets 1(3):216–223. https://doi.org/10.4161/isl.1.3.9646

    Article  PubMed  Google Scholar 

  33. Horike N, Takemori H, Katoh Y, Doi J, Min L, Asano T, Sun XJ, Yamamoto H, Kasayama S, Muraoka M, Nonaka Y, Okamoto M (2003) Adipose-specific expression, phosphorylation of Ser794 in insulin receptor substrate-1, and activation in diabetic animals of salt-inducible kinase-2. J Biol Chem 278(20):18440–18447. https://doi.org/10.1074/jbc.M211770200

    Article  CAS  PubMed  Google Scholar 

  34. Tzatsos A, Tsichlis PN (2007) Energy depletion inhibits phosphatidylinositol 3-kinase/Akt signaling and induces apoptosis via AMP-activated protein kinase-dependent phosphorylation of IRS-1 at Ser-794. J Biol Chem 282(25):18069–18082. https://doi.org/10.1074/jbc.M610101200

    Article  CAS  PubMed  Google Scholar 

  35. Bervoets L, Massa G, Guedens W, Louis E, Noben JP, Adriaensens P (2017) Metabolic profiling of type 1 diabetes mellitus in children and adolescents: a case-control study. Diabetol Metab Syndr 9:48. https://doi.org/10.1186/s13098-017-0246-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bertea M, Rutti MF, Othman A, Marti-Jaun J, Hersberger M, von Eckardstein A, Hornemann T (2010) Deoxysphingoid bases as plasma markers in diabetes mellitus. Lipids Health Dis 9:84. https://doi.org/10.1186/1476-511X-9-84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Suzuki M, Sasabe J, Furuya S, Mita M, Hamase K, Aiso S (2012) Type 1 diabetes mellitus in mice increases hippocampal D-serine in the acute phase after streptozotocin injection. Brain Res 1466:167–176. https://doi.org/10.1016/j.brainres.2012.05.042

    Article  CAS  PubMed  Google Scholar 

  38. Wang Y, Ni J, Gao T, Gao C, Guo L, Yin X (2020) Activation of astrocytic sigma-1 receptor exerts antidepressant-like effect via facilitating CD38-driven mitochondria transfer. Glia 68(11):2415–2426. https://doi.org/10.1002/glia.23850

    Article  PubMed  Google Scholar 

  39. Holscher C (2020) Brain insulin resistance: role in neurodegenerative disease and potential for targeting. Expert Opin Investig Drugs 29(4):333–348. https://doi.org/10.1080/13543784.2020.1738383

    Article  CAS  PubMed  Google Scholar 

  40. Kellar D, Craft S (2020) Brain insulin resistance in Alzheimer’s disease and related disorders: mechanisms and therapeutic approaches. Lancet Neurol 19(9):758–766. https://doi.org/10.1016/S1474-4422(20)30231-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Xu J, Gao H, Zhang L, Rong S, Yang W, Ma C, Chen M, Huang Q, Deng Q, Huang F (2019) Melatonin alleviates cognition impairment by antagonizing brain insulin resistance in aged rats fed a high-fat diet. J Pineal Res 67(2):e12584. https://doi.org/10.1111/jpi.12584

    Article  CAS  PubMed  Google Scholar 

  42. Cai W, Xue C, Sakaguchi M, Konishi M, Shirazian A, Ferris HA, Li ME, Yu R, Kleinridders A, Pothos EN, Kahn CR (2018) Insulin regulates astrocyte gliotransmission and modulates behavior. J Clin Invest 128(7):2914–2926. https://doi.org/10.1172/JCI99366

    Article  PubMed  PubMed Central  Google Scholar 

  43. Yamamoto N, Matsubara T, Sobue K, Tanida M, Kasahara R, Naruse K, Taniura H, Sato T, Suzuki K (2012) Brain insulin resistance accelerates Abeta fibrillogenesis by inducing GM1 ganglioside clustering in the presynaptic membranes. J Neurochem 121(4):619–628. https://doi.org/10.1111/j.1471-4159.2012.07668.x

    Article  CAS  PubMed  Google Scholar 

  44. Girault FM, Sonnay S, Gruetter R, Duarte JMN (2019) Alterations of Brain Energy metabolism in type 2 Diabetic Goto-Kakizaki rats measured in vivo by (13)C magnetic resonance spectroscopy. Neurotox Res 36(2):268–278. https://doi.org/10.1007/s12640-017-9821-y

    Article  CAS  PubMed  Google Scholar 

  45. Durkee CA, Araque A (2019) Diversity and specificity of astrocyte-neuron communication. Neuroscience 396:73–78. https://doi.org/10.1016/j.neuroscience.2018.11.010

    Article  CAS  PubMed  Google Scholar 

  46. Herrera Moro Chao D, Kirchner MK, Pham C, Foppen E, Denis RGP, Castel J, Morel C, Montalban E, Hassouna R, Bui LC, Renault J, Mouffle C, Garcia-Caceres C, Tschop MH, Li D, Martin C, Stern JE, Luquet SH (2022) Hypothalamic astrocytes control systemic glucose metabolism and energy balance. Cell Metab 34(10):1532–1547e1536. https://doi.org/10.1016/j.cmet.2022.09.002

    Article  CAS  PubMed  Google Scholar 

  47. Shima T, Jesmin S, Matsui T, Soya M, Soya H (2018) Differential effects of type 2 diabetes on brain glycometabolism in rats: focus on glycogen and monocarboxylate transporter 2. J Physiol Sci 68(1):69–75. https://doi.org/10.1007/s12576-016-0508-6

    Article  CAS  PubMed  Google Scholar 

  48. Sickmann HM, Waagepetersen HS, Schousboe A, Benie AJ, Bouman SD (2010) Obesity and type 2 diabetes in rats are associated with altered brain glycogen and amino-acid homeostasis. J Cereb Blood Flow Metab 30(8):1527–1537. https://doi.org/10.1038/jcbfm.2010.61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

National Natural Science Foundation of China (Grants Nos. 81974540, 81801899), the Key Research & Development Program of Shaanxi (Program No. 2022ZDLSF02-09) and Innovation Capability Support Program of Shaanxi (Program No. 2021TD-58), Basic Research Program of Natural Sciences of Shaanxi Province (Grant No. 2022JQ-850).

Author information

Author notes

  1. Hongli Ma and Shuxuan He contributed equally to this work.

Authors and Affiliations

  1. Department of Anesthesiology & Center for Brain Science, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, Shaanxi, 710061, China

    Hongli Ma, Shuxuan He, Yansong Li, Xin Zhang, Haiqing Chang, Mengyu Du, Chaoying Yan, Shiqiu Jiang, Jing Zhao & Qiang Wang

  2. Department of Anesthesiology, China-Japan Friendship Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100029, China

    Hongli Ma, Jing Zhao & Qiang Wang

  3. Department of Anesthesiology, Yan’an University Affiliated Hospital, Yan’an, Shaanxi, 716000, China

    Hui Gao

Authors
  1. Hongli Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shuxuan He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yansong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haiqing Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mengyu Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chaoying Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shiqiu Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hui Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jing Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Qiang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Q.W., J.Z., H.M., and Y.L. contributed to the conceptualization and study design. Development of methodology, investigation, and original draft preparation was done by H.M., S.H., Y.L., X.Z., H.C., M.D., S.J., H.G., and C.Y. assisted in experimental procedures. Manuscript review and editing was done by H.M., S.H., S.J., H.G., Q.W., J.Z. All the authors read and approved the final manuscript. H.M. and S.H. contributed equally to this study.

Corresponding authors

Correspondence to Jing Zhao or Qiang Wang.

Ethics declarations

Ethical Approval

All experiments involving animals have obtained approval from the Institutional Animal Care and Use Committees of Xi’an Jiaotong University (NO. 2019-060).

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary Material 1

Supplementary Material 2

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

Ma, H., He, S., Li, Y. et al. Augmented Mitochondrial Transfer Involved in Astrocytic PSPH Attenuates Cognitive Dysfunction in db/db Mice. Mol Neurobiol (2024). https://doi.org/10.1007/s12035-024-04064-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12035-024-04064-0

Keywords

Search

Navigation