Top

Published in:

Open Access 01-12-2021 | Research

Differential hippocampal protein expression between normal mice and mice with the perioperative neurocognitive disorder: a proteomic analysis

Authors: Chuan Li, Jingzhu Li, He Tao, Jinghua Shan, Fanghao Liu, Xiyuan Deng, Yanan Lin, Xu Lin, Li Fu, Bin Wang, Yanlin Bi

Published in: European Journal of Medical Research | Issue 1/2021

Abstract

Objectives

To compare differential expression protein in hippocampal tissues from mice of perioperative neurocognitive disorder (PND) and normal control mice and to explore the possible mechanism of PND.

Methods

Mice were randomly divided into a PND group (n = 9) and a control group (n = 9).The mice in the PND group were treated with open tibial fracture with intramedullary fixation under isoflurane anesthesia, while the mice in the control group received pure oxygen without surgery. The cognitive functions of the two groups were examined using Morris water maze experiment, Open field test and Fear conditioning test. The protein expression of the hippocampus of mice was analyzed by high-performance liquid chromatography–mass spectrometry (HPLC–MS/MS). Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses were performed to explore the principal functions of dysregulated proteins.

Results

A total of 21 proteins were differentially expressed between PND and control mice on days 1, 3, and 7 after the operation. These proteins were involved in many pathological processes, such as neuroinflammatory responses, mitochondrial oxidative stress, impaired synaptic plasticity, and neuronal cell apoptosis. Also, the dysregulated proteins were involved in MAPK, AMPK, and ErbB signaling pathways.

Conclusion

The occurrence of PND could be attributed to multiple mechanisms.

He X, Long G, Quan C, et al. Insulin resistance predicts postoperative cognitive dysfunction in elderly gastrointestinal patients. Front Aging Neurosci. 2019;11:197. https://doi.org/10.3389/fnagi.2019.00197.CrossRefPubMedPubMedCentral

Joseph DJ, Liu C, Peng J, et al. Isoflurane mediated neuropathological and cognitive impairments in the triple transgenic Alzheimer’s mouse model are associated with hippocampal synaptic deficits in an age-dependent manner. PLoS ONE. 2019;14(10): e0223509. https://doi.org/10.1371/journal.pone.0223509.CrossRefPubMedPubMedCentral

Hou R, Wang H, Chen L, et al. POCD in patients receiving total knee replacement under deep vs light anesthesia: a randomized controlled trial. Brain Behav. 2018;8(2): e00910. https://doi.org/10.1002/brb3.910.CrossRefPubMedPubMedCentral

Gerlach RM, Chaney MA. Postoperative cognitive dysfunction related to Alzheimer disease? J Thorac Cardiovasc Surg. 2018;155(3):968–9. https://doi.org/10.1016/j.jtcvs.2017.10.113.CrossRefPubMed

Evered L, Scott DA, Silbert B, et al. Postoperative cognitive dysfunction is independent of type of surgery and anesthetic. Anesth Analg. 2011;112(5):1179–85. https://doi.org/10.1213/ANE.0b013e318215217e.CrossRefPubMed

Szwed K, Bieliński M, Drozdz W, et al. Cognitive dysfunction after cardiac surgery. Psychiatr Pol. 2012;46(3):473–82.PubMed

Geromanos SJ, Vissers JP, Silva JC, et al. The detection, correlation, and comparison of peptide precursor and product ions from data independent LC-MS with data dependant LC-MS/MS. Proteomics. 2009;9(6):1683–95. https://doi.org/10.1002/pmic.200800562.CrossRefPubMed

Zeidman P, Maguire EA. Anterior hippocampus: the anatomy of perception, imagination and episodic memory. Nat Rev Neurosci. 2016;17(3):173–82. https://doi.org/10.1038/nrn.2015.24.CrossRefPubMedPubMedCentral

Bartsch T, Wulff P. The hippocampus in aging and disease: from plasticity to vulnerability. Neuroscience. 2015;309:1–16. https://doi.org/10.1016/j.neuroscience.2015.07.084.CrossRefPubMed

10.

Arushanyan EB, Beier EV. The hippocampus and cognitive impairments. Neurosci Behav Physiol. 2008;38(8):751–8. https://doi.org/10.1007/s11055-008-9043-0.CrossRefPubMed

11.

Wisniewski JR, Zougman A, Nagaraj N, et al. Universal sample preparation method for proteome analysis. Nat Methods. 2009;6:359–62.CrossRef

12.

Vizcaychipi MP, Xu L, Barreto GE, et al. Heat shock protein 72 over expression prevents early postoperative memory decline after orthopedic surgery under general anesthesia in mice. Anesthesiology. 2011;114(4):891–900. https://doi.org/10.1097/ALN.0b013e318-20ad3ce.CrossRefPubMed

13.

Greenfield EA. Administering anesthesia to mice, rats, and hamsters. Cold Spring Harb Protoc. 2019. https://doi.org/10.1101/pdb.prot100198.CrossRefPubMed

14.

Vorhees CV, Williams MT. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc. 2006;1(2):848–58. https://doi.org/10.1038/nprot.2006.116.CrossRefPubMedPubMedCentral

15.

Spires-Jones TL, Hyman BT. The intersection of amyloid beta and tau at synapses in Alzheimer’s disease. Neuron. 2014;82(4):756–71. https://doi.org/10.1016/j.neuron.2014.05.004.CrossRefPubMedPubMedCentral

16.

Rengel KF, Pandharipande PP, Hughes CG. Special considerations for the aging brain and perioperative neurocognitive dysfunction. Anesthesiol Clin. 2019;37(3):521–36. https://doi.org/10.1016/j.anclin.2019.04.010.CrossRefPubMed

17.

Bagge A, Dahmcke CM, Dalgaard LT. Syntaxin-1a is a direct target of miR-29a in insulin-producing β-cells. Horm Metab Res. 2013;45(6):463–6. https://doi.org/10.1055/s-0032-1333238.CrossRefPubMed

18.

Toonen RF, Verhage M. Munc18–1 in secretion: lonely Munc joins SNARE team and takes control. Trends Neurosci. 2007;30:564–72.CrossRef

19.

Shi VH, Craig TJ, Bishop P, et al. Phosphorylation of Syntaxin-1a by casein kinase 2α regulates pre-synaptic vesicle exocytosis from the reserve pool. J Neurochem. 2020. https://doi.org/10.1111/jnc.15161.CrossRefPubMed

20.

Bennett MK, Calakos N, Scheller RH. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science. 1992;257:255–9.CrossRef

21.

Mishima T, Fujiwara T, Kofuji T, et al. Impairment of catecholamine systems during induction of long-term potentiation at hippocampal CA1 synapses in HPC-1/syntaxin 1A knockout mice. J Neurosci. 2012;32(1):381–9. https://doi.org/10.1523/JNEUROSCI.2911-11.2012.CrossRefPubMedPubMedCentral

22.

Fujiwara T, Mishima T, Kofuji T, et al. Analysis of knockout mice to determine the role of HPC-1/syntaxin 1A in expressing synaptic plasticity. J Neurosci. 2006;26:5767–76.CrossRef

23.

Minger SL, Honer WG, Esiri MM, et al. Synaptic pathology in prefrontal cortex is present only with severe dementia in Alzheimer disease. J Neuropathol Exp Neurol. 2001;60(10):929–36. https://doi.org/10.1093/jnen/60.10.929.CrossRefPubMed

24.

Popugaeva E, Pchitskaya E, Bezprozvanny I, et al. Dysregulation of neuronal calcium homeostasis in Alzheimer’s disease—a therapeutic opportunity? Biochem Biophys Res Commun. 2017;483:998–1004.CrossRef

25.

Nicholson RM, Kusne Y, Nowak LA, et al. Regional cerebral glucose uptake in the 3xTG model of Alzheimer’s disease highlights common regional vulnerability across AD mouse models. Brain Res. 2010;1347:179–85.CrossRef

26.

Berridge MJ. Calcium regulation of neural rhythms, memory and Alzheimer’s disease. J Physiol. 2014;592:281–93.CrossRef

27.

Whitworth AJ, Pallanck LJ. PINK1/Parkin mitophagy and neurodegeneration-what do we really know in vivo? Curr Opin Genet Dev. 2017;44:47–53. https://doi.org/10.1016/j.gde.2017.01.016.CrossRefPubMed

28.

Santos R, Bulteau AL, Gomes CM, et al. Neurodegeneration, neurogenesis, and oxidative stress. Oxid Med Cell Longev. 2013;2013: 730581. https://doi.org/10.1155/2013/730581.CrossRefPubMedPubMedCentral

29.

Bargiela D, Chinnery PF. Mitochondria in neuroinflammation—multiple sclerosis (MS), leber hereditary optic neuropathy (LHON) and LHON-MS. Neurosci Lett. 2019;25(710): 132932. https://doi.org/10.1016/j.neulet.2017.06.051.CrossRef

30.

Yan MH, Wang X, Zhu X. Mitochondrial defects and oxidative stress in Alzheimer disease and Parkinson disease. Free Radic Biol Med. 2013;62:90–101. https://doi.org/10.1016/j.freeradbiomed.2012.11.014.CrossRefPubMed

31.

Carteri RB, Kopczynski A, Rodolphi MS, et al. Testosterone administration after traumatic brain injury reduces mitochondrial dysfunction and neurodegeneration. J Neurotrauma. 2019;36(14):2246–59. https://doi.org/10.1089/neu.2018.6266.CrossRefPubMedPubMedCentral

32.

Iurlaro R, Muñoz-Pinedo C. Cell death induced by endoplasmic reticulum stress. FEBS J. 2016;283(14):2640–52. https://doi.org/10.1111/febs.13598.CrossRefPubMed

33.

Noack R, Frede S, Albrecht P, et al. Charcot–Marie–Tooth disease CMT4A: GDAP1 increases cellular glutathione and the mitochondrial membrane potential. Hum Mol Genet. 2012;21:150–62.CrossRef

34.

Niemann A, Huber N, Wagner KM, et al. The Gdap1 knockout mouse mechanistically links redox control to Charcot–Marie–Tooth disease. Brain. 2014;137:668–82.CrossRef

35.

Chen G, Gong M, Yan M, Zhang X. Sevoflurane induces endoplasmic reticulum stress mediated apoptosis in hippocampal neurons of aging rats. PLoS ONE. 2013;8(2): e57870. https://doi.org/10.1371/journal.pone.0057870.CrossRefPubMedPubMedCentral

36.

Segal M, Korkotian E. Roles of calcium stores and store-operated channels in plasticity of dendritic spines. Neuroscientist. 2016;22:477–85.CrossRef

37.

Emptage NJ, Reid CA, Fine A. Calcium stores in hippocampal synaptic boutons mediate short-term plasticity, store-operated Ca2+entry, and spontaneous transmitter release. Neuron. 2001;29:197–208.CrossRef

38.

De Juan-Sanz J, Holt GT, Schreiter ER, et al. Axonal endoplasmic reticulum Ca2+ content controls release probability in CNS nerve terminals. Neuron. 2017;93:867-881.e6.CrossRef

39.

Hartmann J, Karl RM, Alexander RP, et al. STIM1 controls neuronal Ca2+ signaling, mGluR1-dependent synaptic transmission, and cerebellar motor behavior. Neuron. 2014;82:635–44.CrossRef

40.

Kho AR, Choi BY, Lee SH, et al. The effects of sodium dichloroacetate on mitochondrial dysfunction and neuronal death following hypoglycemia-induced injury. Cells. 2019;8(5):405. https://doi.org/10.3390/cells8050405.CrossRefPubMedCentral

41.

Jha MK, Rahman MH, Park DH, et al. Pyruvate dehydrogenase kinase 2 and 4 gene deficiency attenuates nociceptive behaviors in a mouse model of acute inflammatory pain. J Neurosci Res. 2016;94(9):837–49. https://doi.org/10.1002/jnr.23727.CrossRefPubMed

42.

Nakai N, Obayashi M, Nagasaki M, et al. The abundance of mRNAs for pyruvate dehydrogenase kinase isoenzymes in brain regions of young and aged rats. Life Sci. 2000;68(5):497–503.CrossRef

43.

Wei H, Xie Z. Anesthesia, calcium homeostasis and Alzheimer’s disease. Curr Alzheimer Res. 2009;6(1):30–5. https://doi.org/10.2174/156720509787313934.CrossRefPubMedPubMedCentral

44.

Kaenmaki M, Tammimaki A, Myohanen T, et al. Quantitative role of COMT in dopamine clearance in the prefrontal cortex of freely moving mice. J Neurochem. 2010;114:1745–55.CrossRef

45.

Xu H, Wang R, Zhang YW, et al. Estrogen, beta-amyloid metabolism/trafficking, and Alzheimer’s disease. Ann NY Acad Sci. 2006;1089:324–42.CrossRef

46.

Martorana A, Mori F, Esposito Z, et al. Dopamine modulates cholinergic cortical excitability in Alzheimer’s disease patients. Neuropsychopharmacology. 2011;34:2323–8.CrossRef

47.

Di Giovanni S, Eleuteri S, Paleologou KE, et al. Entacapone and tolcapone, two catechol O-methyltransferase inhibitors, block fibril formation of alpha-synuclein and beta-amyloid and protect against amyloid-induced toxicity. J Biol Chem. 2010;285(20):14941–54. https://doi.org/10.1074/jbc.M109.080390.CrossRefPubMedPubMedCentral

48.

Serretti A, Olgiati P. Catechol-o-methyltransferase and Alzheimer’s disease: a review of biological and genetic findings. CNS Neurol Disord Drug Targets. 2012;11(3):299–305. https://doi.org/10.2174/187152712800672472.CrossRefPubMed

49.

Gaczynska M, Osmulski PA. Targeting protein–protein interactions in the ubiquitin-proteasome pathway. Adv Protein Chem Struct Biol. 2018;110:123–65. https://doi.org/10.1016/bs.apcsb.2017.09.001.CrossRefPubMed

50.

Budenholzer L, Cheng CL, Li Y, et al. Proteasome structure and assembly. J Mol Biol. 2017;429(22):3500–24. https://doi.org/10.1016/j.jmb.2017.05.027.CrossRefPubMedPubMedCentral

51.

Nandi D, Tahiliani P, Kumar A, et al. The ubiquitin–proteasome system. J Biosci. 2006;31(1):137–55. https://doi.org/10.1007/BF02705243.CrossRefPubMed

52.

Gu ZC, Enenkel C. Proteasome assembly. Cell Mol Life Sci. 2014;71(24):4729–45. https://doi.org/10.1007/s00018-014-1699-8.CrossRefPubMed

53.

McKinnon C, Tabrizi SJ. The ubiquitin-proteasome system in neurodegeneration. Antioxid Redox Signal. 2014;21(17):2302–21. https://doi.org/10.1089/ars.2013.5802.CrossRefPubMed

54.

Ghavami S, Shojaei S, Yeganeh B, et al. Autophagy and apoptosis dysfunction in neurodegenerative disorders. Prog Neurobiol. 2014;112:24–49. https://doi.org/10.1016/j.pneurobio.2013.10.004.CrossRefPubMed

55.

Deshmukh RR, Dou QP. Proteasome inhibitors induce AMPK activation via CaMKKβ in human breast cancer cells. Breast Cancer Res Treat. 2015;153(1):79–88. https://doi.org/10.1007/s10549-015-3512-2.CrossRefPubMed

56.

Wen Z, Zhang J, Tang P, et al. Overexpression of miR-185 inhibits autophagy and apoptosis of dopaminergic neurons by regulating the AMPK/mTOR signaling pathway in Parkinson’s disease. Mol Med Rep. 2018;17(1):131–7. https://doi.org/10.3892/mmr.2017.7897.CrossRefPubMed

57.

Sokolova V, Li F, Polovin G, et al. Proteasome activation is mediated via a functional switch of the Rpt6 C-terminal tail following chaperone-dependent assembly. Sci Rep. 2015;9(5):14909. https://doi.org/10.1038/srep14909.CrossRef

58.

Kong G, Zhou L, Serger E, et al. AMPK controls the axonal regenerative ability of dorsal root ganglia sensory neurons after spinal cord injury. Nat Metab. 2020;2(9):918–33. https://doi.org/10.1038/s42255-020-0252-3.CrossRefPubMed

59.

Liu X, Wang P, Zhang C, et al. Epidermal growth factor receptor (EGFR): a rising star in the era of precision medicine of lung cancer. Oncotarget. 2017;8(30):50209–20. https://doi.org/10.18632/oncotarget.16854.CrossRefPubMedPubMedCentral

60.

Wang Z. ErbB receptors and cancer. Methods Mol Biol. 2017;1652:3–35. https://doi.org/10.1007/978-1-4939-7219-7_1.CrossRefPubMed

61.

Lupo G, Gioia R, Nisi PS, et al. Molecular mechanisms of neurogenic aging in the adult mouse subventricular zone. J Exp Neurosci. 2019;13:1179069519829040.CrossRef

62.

Wang BJ, Her GM, Hu MK, et al. ErbB2 regulates autophagic flux to modulate the proteostasis of APP-CTFs in Alzheimer’s disease. Proc Natl Acad Sci. 2017;114(15):E3129–38.CrossRef

63.

Wang L, Chiang HC, Wu W, et al. Epidermal growth factor receptor is a preferred target for treating amyloid-β-induced memory loss. Proc Natl Acad Sci. 2012;109(41):16743–8.CrossRef

64.

Armstrong R, Xu F, Arora A, et al. General anesthetics and cytotoxicity: possible implications for brain health. Drug Chem Toxicol. 2017;40(2):241–9. https://doi.org/10.1080/01480545.2016.1188306.CrossRefPubMed

65.

Bi Y, Liu S, Yu X, et al. Adaptive and regulatory mechanisms in aged rats with postoperative cognitive dysfunction. Neural Regen Res. 2014;9(5):534–9. https://doi.org/10.4103/1673-5374.130084.CrossRefPubMedPubMedCentral

66.

Liu X, Yu Y, Zhu S. Inflammatory markers in postoperative delirium (POD) and cognitive dysfunction (POCD): a meta-analysis of observational studies. PLoS ONE. 2018;13(4): e0195659. https://doi.org/10.1371/journal.pone.0195659.CrossRefPubMedPubMedCentral

67.

Skvarc DR, Berk M, Byrne LK, et al. Post-operative cognitive dysfunction: an exploration of the inflammatory hypothesis and novel therapies. Neurosci Biobehav Rev. 2018;84:116–33. https://doi.org/10.1016/j.neubiorev.2017.11.011.CrossRefPubMed

68.

Zhang S, Ju P, Tjandra E, et al. Inhibition of epidermal growth factor receptor improves myelination and attenuates tissue damage of spinal cord injury. Cell Mol Neurobiol. 2016;36(7):1169–78.CrossRef

69.

Qu WS, Tian DS, Guo ZB, et al. Inhibition of EGFR/MAPK signaling reduces microglial inflammatory response and the associated secondary damage in rats after spinal cord injury. J Neuroinflam. 2012;9(1):178.CrossRef

70.

Esseltine JL, Ribeiro FM, Ferguson SS. Rab8 modulates metabotropic glutamate receptor subtype 1 intracellular trafficking and signaling in a protein kinase C-dependent manner. J Neurosci. 2012;32(47):16933–42. https://doi.org/10.1523/JNEUROSCI.0625-12.2012.CrossRefPubMedPubMedCentral

71.

Kim JH, Yoon MS, Chen J. Signal transducer and activator of transcription 3 (STAT3) mediates amino acid inhibition of insulin signalling through Serine 727 phosphorylation. J Biol Chem. 2009;284:35425–32.CrossRef

72.

Weichhart T, et al. The TSC-mTOR signalling pathway regulates the innate inflammatory response. Immunity. 2008;29:565–77.CrossRef

73.

D’Arcy MS. Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biol Int. 2019;43(6):582–92. https://doi.org/10.1002/cbin.11137.CrossRefPubMed

74.

Zhang X, Dong H, Li N, et al. Activated brain mast cells contribute to postoperative cognitive dysfunction by evoking microglia activation and neuronal apoptosis. J Neuroinflammation. 2016;13(1):127. https://doi.org/10.1186/s12974-016-0592-9.CrossRefPubMedPubMedCentral

75.

Xu X, Shi YC, Gao W, et al. The novel presenilin-1-associated protein is a proapoptotic mitochondrial protein. J Biol Chem. 2002;277(50):48913–22. https://doi.org/10.1074/jbc.M209613200.CrossRefPubMed

76.

Nelo-Bazán MA, Latorre P, Bolado-Carrancio A, et al. Early growth response 1 (EGR-1) is a transcriptional regulator of mitochondrial carrier homolog 1 (MTCH 1)/presenilin 1-associated protein (PSAP). Gene. 2016;578(1):52–62. https://doi.org/10.1016/j.gene.2015.12.014.CrossRefPubMed

Title: Differential hippocampal protein expression between normal mice and mice with the perioperative neurocognitive disorder: a proteomic analysis
Authors: Chuan Li
Jingzhu Li
He Tao
Jinghua Shan
Fanghao Liu
Xiyuan Deng
Yanan Lin
Xu Lin
Li Fu
Bin Wang
Yanlin Bi
Publication date: 01-12-2021
Publisher: BioMed Central
Published in: European Journal of Medical Research / Issue 1/2021
Electronic ISSN: 2047-783X
DOI: https://doi.org/10.1186/s40001-021-00599-3

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Differential hippocampal protein expression between normal mice and mice with the perioperative neurocognitive disorder: a proteomic analysis

Abstract

Objectives

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objectives

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2021

A first case report of nasopharyngeal Mycobacterium abscessus subspecies massiliense infection

Differentiating brucella spondylitis from tuberculous spondylitis by the conventional MRI and MR T2 mapping: a prospective study

A case report of brain abscess caused by Nocardia farcinica

Ultrasonic evaluation of muscle functional recovery following free functioning gracilis transfer, a preliminary study

Correction to: Epiphyseal enchondroma masking as osteoid osteoma: a case report

Application study of 3D LAVA-Flex on lumbar intervertebral disc degeneration