Minocycline Activates the Nucleus of the Solitary Tract-Associated Network to Alleviate Lipopolysaccharide-Induced Neuroinflammation

Xiu Jianbo; Li Lanlan; Xu Qi

doi:10.24920/003954

Your Location：

Home >

Browse articles >

Minocycline Activates the Nucleus of the Solitary Tract-Associated Network to Alleviate Lipopolysaccharide-Induced Neuroinflammation

Chinese Medical Sciences Journal Vol. 37, Issue 1, Pages: 1-14(2022)

Original Article | Updated：2024-04-10

- Minocycline Activates the Nucleus of the Solitary Tract-Associated Network to Alleviate Lipopolysaccharide-Induced Neuroinflammation
- Affiliations：
  
  1. 1State Key Laboratory of Medical Molecular Biology, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, School of Basic Medicine Peking Union Medical College, Beijing 100005, China
  2. 2Neuroscience Center, Chinese Academy of Medical Sciences, Beijing 100005, China
- Author bio：
  
  *E-mail: xuqi@pumc.edu.cn
- Funds：
- DOI：10.24920/003954
  CLC：
- Received：10 June 2021，
  
  Accepted：2021-6-29，
  
  Published Online：30 June 2021，
  
  Published：31 March 2022
- Accepted：
Scan QR Code
Xiu Jianbo, Li Lanlan, Xu Qi. Minocycline Activates the Nucleus of the Solitary Tract-Associated Network to Alleviate Lipopolysaccharide-Induced Neuroinflammation[J]. Chinese medical sciences journal, 2022, 37(1): 1-14.
DOI：

Xiu Jianbo, Li Lanlan, Xu Qi. Minocycline Activates the Nucleus of the Solitary Tract-Associated Network to Alleviate Lipopolysaccharide-Induced Neuroinflammation[J]. Chinese medical sciences journal, 2022, 37(1): 1-14. DOI： 10.24920/003954.

摘要

目的

研究米诺环素减轻脂多糖（LPS）诱导的神经炎症的神经解剖基础。

方法

将40只C57BL/6雄性小鼠随机分为8组。连续三天

四组小鼠服用生理盐水

其他四组服用米诺环素。在第三天服用生理盐水或米诺环素后

两组小鼠立即额外注射生理盐水

另外两组小鼠注射LPS。最后一次注射后6或24小时

处死小鼠

取出大脑。对整个大脑进行免疫组织化学染色

通过Iba1检测小胶质细胞激活情况

通过c-Fos检测神经元的活化。通过Image Pro Premier 3D分析小胶质细胞的形态和c-Fos阳性神经元的数量。采用单因素方差分析和Fisher最小显著性差异进行统计分析。

结果

米诺环素可减轻LPS诱导的神经炎症

其表现为多个脑区小胶质细胞的激活减少

包括伏隔核的壳亚区、下丘脑室旁核（PVN）、中央杏仁核、蓝斑（LC）和孤束核（NTS）。米诺环素显著增加LPS注射后NTS和极后区中c-Fos阳性神经元的数量。此外

在NTS相关的脑区

包括LC、臂旁外侧核、中脑导水管周围灰质、中缝背核、杏仁核、PVN和终纹床核

米诺环素也显著增加了LPS注射后c-Fos阳性神经元的数量。

结论

米诺环素可减轻脂多糖诱导的多个脑区神经炎症

这种效应可能是由于孤束核相关网络中神经元的激活增加所致。

Abstract

Objective

To examine the neuroanatomical substrates underlying the effects of minocycline in alleviating lipopolysaccharide (LPS)-induced neuroinflammation.

Methods

Forty C57BL/6 male mice were randomly and equally divided into eight groups. Over three conse-cutive days

saline was administered to four groups of mice and minocycline to the other four groups. Immediately after the administration of saline or minocycline on the third day

two groups of mice were additionally injected with saline and the other two groups were injected with LPS. Six or 24 hours after the last injection

mice were sacrificed and the brains were removed. Immunohistochemical staining across the whole brain was performed to detect microglia activation via Iba1 and neuronal activation via c-Fos. Morphology of microglia and the number of c-Fo-positive neurons were analyzed by Image-Pro Premier 3D. One-way ANOVA and Fisher’s least-significant differences were employed for statistical analyses.

Results

Minocycline alleviated LPS-induced neuroinflammation as evidenced by reduced activation of microglia in multiple brain regions

including the shell part of the nucleus accumbens (Acbs)

paraventricular nucleus (PVN) of the hypothalamus

central nucleus of the amygdala (CeA)

locus coeruleus (LC)

and nucleus tractus solitarius (NTS). Minocycline significantly increased the number of c-Fo-positive neurons in NTS and area postrema (AP) after LPS treatment. Furthermore

in NTS-associated brain areas

including LC

lateral parabrachial nucleus (LPB)

periaqueductal gray (PAG)

dorsal raphe nucleus (DR)

amygdala

PVN

and bed nucleus of the stria terminali (BNST)

minocycline also significantly increased the number of c-Fo-positive neurons after LPS administration.

Conclusion

Minocycline alleviates LPS-induced neuroinflammation in multiple brain regions

possibly due to increased activation of neurons in the NTS-associated network.

关键词

Keywords

references

Wohleb ES , Franklin T , Iwata M , et al . Integrating neuroimmune systems in the neurobiology of depression . Nat Rev Neurosci 2016 ; 17 ( 8 ): 497 - 511 . doi: 10.1038/nrn.2016.69 https://dx.doi.org/10.1038/nrn.2016.69 . DOI: 10.1038/nrn.2016.69 http://doi.org/10.1038/nrn.2016.69

Miller AH , Raison CL . The role of inflammation in depression: from evolutionary imperative to modern treatment target . Nat Rev Immunol 2016 ( 1 ): 16 , 22 - 34 . doi: 10.1038/nri.2015.5 https://dx.doi.org/10.1038/nri.2015.5 . DOI: 10.1038/nri.2015.5 http://doi.org/10.1038/nri.2015.5 https://doi.org/10.1038/nri.2015.5 https://doi.org/10.1038/nri.2015.5

Dantzer R , O’Connor JC , Freund GG , et al . From inflammation to sickness and depression: when the immune system subjugates the brain . Nat Rev Neurosci 2008 ; 9 ( 1 ): 46 - 56 . doi: 10.1038/nrn2297 https://dx.doi.org/10.1038/nrn2297 . DOI: 10.1038/nrn2297 http://doi.org/10.1038/nrn2297

Hodes GE , Kana V , Menard C , et al . Neuroimmune mechanisms of depression . Nat neurosci 2015 ; 18 ( 10 ): 1386 - 93 . doi: 10.1038/nn.4113 https://dx.doi.org/10.1038/nn.4113 . DOI: 10.1038/nn.4113 http://doi.org/10.1038/nn.4113

Beurel E , Toups M , Nemeroff CB . The Bidirectional Relationship of Depression and Inflammation: Double Trouble . Neuron 2020 ; 107 ( 2 ): 234 - 56 . doi: 10.1016/j.neuron.2020.06.002 https://dx.doi.org/10.1016/j.neuron.2020.06.002 . DOI: 10.1016/j.neuron.2020.06.002 http://doi.org/10.1016/j.neuron.2020.06.002 https://linkinghub.elsevier.com/retrieve/pii/S0896627320304311 https://linkinghub.elsevier.com/retrieve/pii/S0896627320304311

Zhan L , Krabbe G , Du F , et al . Proximal recolonization by self-renewing microglia re-establishes microglial homeostasis in the adult mouse brain . PLoS biology 2019 ; 17 ( 2 ): e3000134 . doi: 10.1371/journal.pbio.3000134 https://dx.doi.org/10.1371/journal.pbio.3000134 . DOI: 10.1371/journal.pbio.3000134 http://doi.org/10.1371/journal.pbio.3000134 https://dx.plos.org/10.1371/journal.pbio.3000134 https://dx.plos.org/10.1371/journal.pbio.3000134

Lawson LJ , Perry VH , Dri P , et al . Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain . Neurosci 1990 ; 39 ( 1 ): 151 - 70 . doi: 10.1016/0306-4522(90)90229-w https://dx.doi.org/10.1016/0306-4522(90)90229-w . DOI: 10.1016/0306-4522(90)90229-w http://doi.org/10.1016/0306-4522(90)90229-w

Prinz M , Jung S , Priller J . Microglia Biology: One Century of Evolving Concepts . Cell 2019 ; 179 ( 2 ): 292 - 311 . doi: 10.1016/j.cell.2019.08.053 https://dx.doi.org/10.1016/j.cell.2019.08.053 . DOI: 10.1016/j.cell.2019.08.053 http://doi.org/10.1016/j.cell.2019.08.053 https://linkinghub.elsevier.com/retrieve/pii/S0092867419310049 https://linkinghub.elsevier.com/retrieve/pii/S0092867419310049

Deng SL , Chen JG , Wang F . Microglia: A central player in depression . Curr Med Sci 2020 ; 40 ( 3 ): 391 - 400 . doi: 10.1007/s11596-020-2193-1 https://dx.doi.org/10.1007/s11596-020-2193-1 . DOI: 10.1007/s11596-020-2193-1 http://doi.org/10.1007/s11596-020-2193-1 https://doi.org/10.1007/s11596-020-2193-1 https://doi.org/10.1007/s11596-020-2193-1

Jia X , Gao Z , Hu H . Microglia in depression: current perspectives . Sci China Life Sci 2021 ; 64 ( 6 ): 911 - 25 . doi: 10.1007/s11427-020-1815-6 https://dx.doi.org/10.1007/s11427-020-1815-6 . DOI: 10.1007/s11427-020-1815-6 http://doi.org/10.1007/s11427-020-1815-6 https://doi.org/10.1007/s11427-020-1815-6 https://doi.org/10.1007/s11427-020-1815-6

Yirmiya R , Rimmerman N , Reshef R . Depression as a microglial disease . Trends Neurosci 2015 ; 38 ( 10 ): 637 - 58 . doi: 10.1016/j.tins.2015.08.001 https://dx.doi.org/10.1016/j.tins.2015.08.001 . DOI: S0166-2236(15)00176-9 http://doi.org/S0166-2236(15)00176-9

Dantzer R . Cytokine-induced sickness behavior: Mechanisms and implications . Ann Ny Acad Sci 2001 ; 933 , 222 - 34 . doi: 10.1111/j.1749-6632.2001.tb05827.x https://dx.doi.org/10.1111/j.1749-6632.2001.tb05827.x . DOI: 10.1111/j.1749-6632.2001.tb05827.x http://doi.org/10.1111/j.1749-6632.2001.tb05827.x

Quan N , Banks WA . Brain-immune communication pathways . Brain Behav Immun 2007 ; 21 ( 6 ): 727 - 35 . doi: 10.1016/j.bbi.2007.05.005 https://dx.doi.org/10.1016/j.bbi.2007.05.005 . DOI: 10.1016/j.bbi.2007.05.005 http://doi.org/10.1016/j.bbi.2007.05.005 https://linkinghub.elsevier.com/retrieve/pii/S0889159107001158 https://linkinghub.elsevier.com/retrieve/pii/S0889159107001158

Henry CJ , Huang Y , Wynne A , et al . Minocycline attenuates lipopolysaccharide (LPS)-induced neuroinflammation, sickness behavior, and anhedonia . J Neuroinflammation 2008 ; 5 : 15 . doi: 10.1186/1742-2094-5-15 https://dx.doi.org/10.1186/1742-2094-5-15 . DOI: 10.1186/1742-2094-5-15 http://doi.org/10.1186/1742-2094-5-15 https://doi.org/10.1186/1742-2094-5-15 https://doi.org/10.1186/1742-2094-5-15

Soczynska JK , Mansur RB , Brietzke E , et al . Novel therapeutic targets in depression: Minocycline as a candidate treatment . Behav Brain Res 2012 ; 235 ( 2 ): 302 - 17 . doi: 10.1016/j.bbr.2012.07.026 https://dx.doi.org/10.1016/j.bbr.2012.07.026 . DOI: 10.1016/j.bbr.2012.07.026 http://doi.org/10.1016/j.bbr.2012.07.026

Zhu FR , Zheng YJ , Ding YQ , et al . Minocycline and Risperidone Prevent microglia activation and rescue behavioral deficits induced by neonatal intrahippocampal injection of lipopolysaccharide in rats . Plos One 2014 ; 9 ( 4 ): e93966 . doi: 10.1371/journal.pone.0093966 https://dx.doi.org/10.1371/journal.pone.0093966 . DOI: 10.1371/journal.pone.0093966 http://doi.org/10.1371/journal.pone.0093966 https://dx.plos.org/10.1371/journal.pone.0093966 https://dx.plos.org/10.1371/journal.pone.0093966

Zheng LS , Kaneko N , Sawamoto K . Minocycline treatment ameliorates interferon-alpha-induced neurogenic defects and depression-like behaviors in mice . Front Cell Neurosci 2015 ; 9 : 5 . doi: 10.3389/fncel.2015.00005 https://dx.doi.org/10.3389/fncel.2015.00005 . DOI: 10.3389/fncel.2015.00005 http://doi.org/10.3389/fncel.2015.00005

Majidi J , Kosari-Nasab M , Salari AA . Developmental minocycline treatment reverses the effects of neonatal immune activation on anxiety- and depression-like behaviors, hippocampal inflammation, and HPA axis activity in adult mice . Brain Res Bull 2016 ; 120 : 1 - 13 . doi: 10.1016/j.brainresbull.2015.10.009 https://dx.doi.org/10.1016/j.brainresbull.2015.10.009 . DOI: 10.1016/j.brainresbull.2015.10.009 http://doi.org/10.1016/j.brainresbull.2015.10.009

Husain MI , Chaudhry IB , Husain N , et al . Minocycline as an adjunct for treatment-resistant depressive symptoms: A pilot randomised placebo-controlled trial . J Psychopharmacol 2017 ; 31 ( 9 ): 1166 - 75 . doi: 10.1177/0269881117724352 https://dx.doi.org/10.1177/0269881117724352 . DOI: 10.1177/0269881117724352 http://doi.org/10.1177/0269881117724352 http://journals.sagepub.com/doi/10.1177/0269881117724352 http://journals.sagepub.com/doi/10.1177/0269881117724352

Han Y , Zhang LJ , Wang QZ , et al . Minocycline inhibits microglial activation and alleviates depressive-like behaviors in male adolescent mice subjected to maternal separation . Psychoneuroendocrinology 2019 ; 107 : 37 - 45 . doi: 10.1016/j.psyneuen.2019.04.021 https://dx.doi.org/10.1016/j.psyneuen.2019.04.021 . DOI: 10.1016/j.psyneuen.2019.04.021 http://doi.org/10.1016/j.psyneuen.2019.04.021

Zhang C , Zhang YP , Li YY , et al . Minocycline ameliorates depressive behaviors and neuro-immune dysfunction induced by chronic unpredictable mild stress in the rat . Behav Brain Res 2019 ; 356 : 348 - 57 . doi: 10.1016/j.bbr.2018.07.001 https://dx.doi.org/10.1016/j.bbr.2018.07.001 . DOI: S0166-4328(18)30395-4 http://doi.org/S0166-4328(18)30395-4

Wang B , Huang X , Pan X , et al . Minocycline prevents the depressive-like behavior through inhibiting the release of HMGB1 from microglia and neurons . Brain Behav Immun 2020 ; 88 : 132 - 43 . doi: 10.1016/j.bbi.2020.06.019 https://dx.doi.org/10.1016/j.bbi.2020.06.019 . DOI: S0889-1591(20)30334-2 http://doi.org/S0889-1591(20)30334-2

Yang Q , Luo L , Sun T , et al . Chronic minocycline treatment exerts antidepressant effect, inhibits neuroinflammation, and modulates gut microbiota in mice . Psychopharmacology 2020 ; 237 : 3201 - 13 . doi: 10.1007/s00213-020-05604-x https://dx.doi.org/10.1007/s00213-020-05604-x . DOI: 10.1007/s00213-020-05604-x http://doi.org/10.1007/s00213-020-05604-x

Nettis MA , Lombardo G , Hastings C , et al . Augmentation therapy with minocycline in treatment-resistant depression patients with low-grade peripheral inflammation: results from a double-blind randomised clinical trial . Neuropsychopharmacology 2021 ; 46 ( 5 ): 939 - 48 . doi: 10.1038/s41386-020-00948-6 https://dx.doi.org/10.1038/s41386-020-00948-6 . DOI: 10.1038/s41386-020-00948-6 http://doi.org/10.1038/s41386-020-00948-6 https://doi.org/10.1038/s41386-020-00948-6 https://doi.org/10.1038/s41386-020-00948-6

Bassett B , Subramaniyam S , Fan Y , et al . Minocycline alleviates depression-like symptoms by rescuing decrease in neurogenesis in dorsal hippocampus via blocking microglia activation/phagocytosis . Brain Behav Immun 2021 ; 91 : 519 - 30 . doi: 10.1016/j.bbi.2020.11.009 https://dx.doi.org/10.1016/j.bbi.2020.11.009 . DOI: 10.1016/j.bbi.2020.11.009 http://doi.org/10.1016/j.bbi.2020.11.009

Rosenblat JD , McIntyre RS . Efficacy and tolerability of minocycline for depression: a systematic review and meta-analysis of clinical trials . J Affect Disorders 2018 ; 227 : 219 - 25 . doi: 10.1016/j.jad.2017.10.042 https://dx.doi.org/10.1016/j.jad.2017.10.042 . DOI: S0165-0327(17)31998-5 http://doi.org/S0165-0327(17)31998-5

Reis DJ , Casteen EJ , Ilardi SS . The antidepressant impact of minocycline in rodents: a systematic review and meta-analysis . Sci Rep 2019 ; 9 ( 1 ): 261 . doi: 10.1038/s41598-018-36507-9 https://dx.doi.org/10.1038/s41598-018-36507-9 . DOI: 10.1038/s41598-018-36507-9 http://doi.org/10.1038/s41598-018-36507-9 https://doi.org/10.1038/s41598-018-36507-9 https://doi.org/10.1038/s41598-018-36507-9

Burke NN , Kerr DM , Moriarty O , et al . Minocycline modulates neuropathic pain behaviour and cortical M1-M2 microglial gene expression in a rat model of depression . Brain Behav Immun 2014 ; 42 : 147 - 56 . doi: 10.1016/j.bbi.2014.06.015 https://dx.doi.org/10.1016/j.bbi.2014.06.015 . DOI: 10.1016/j.bbi.2014.06.015 http://doi.org/10.1016/j.bbi.2014.06.015 https://linkinghub.elsevier.com/retrieve/pii/S0889159114001809 https://linkinghub.elsevier.com/retrieve/pii/S0889159114001809

Yrjanheikki J , Keinanen R , Pellikka M , et al . Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia . P Natl Acad Sci U S A 1998 ; 95 ( 26 ): 15769 - 74 . doi: 10.1073/pnas.95.26.15769 https://dx.doi.org/10.1073/pnas.95.26.15769 . DOI: 10.1073/pnas.95.26.15769 http://doi.org/10.1073/pnas.95.26.15769 https://pnas.org/doi/full/10.1073/pnas.95.26.15769 https://pnas.org/doi/full/10.1073/pnas.95.26.15769

Tikka T , Fiebich BL , Goldsteins G , et al . Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia . J Neurosci 2001 ; 21 ( 8 ): 2580 - 8 . doi: 10.1523/Jneurosci.21-08-02580.2001 https://dx.doi.org/10.1523/Jneurosci.21-08-02580.2001 . DOI: 10.1523/Jneurosci.21-08-02580.2001 http://doi.org/10.1523/Jneurosci.21-08-02580.2001

Ekdahl CT , Claasen JH , Bonde S , et al . Inflammation is detrimental for neurogenesis in adult brain . P Natl Acad Sci U S A 2003 ; 100 ( 23 ): 13632 - 7 . doi: 10.1073/pnas.2234031100 https://dx.doi.org/10.1073/pnas.2234031100 . DOI: 10.1073/pnas.2234031100 http://doi.org/10.1073/pnas.2234031100 https://pnas.org/doi/full/10.1073/pnas.2234031100 https://pnas.org/doi/full/10.1073/pnas.2234031100

O’Connor JC , Lawson MA , Andre C , et al . Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice . Mol Psychiatry 2009 ; 14 ( 5 ): 511 - 22 . doi: 10.1038/sj.mp.4002148 https://dx.doi.org/10.1038/sj.mp.4002148 . DOI: 10.1038/sj.mp.4002148 http://doi.org/10.1038/sj.mp.4002148 https://doi.org/10.1038/sj.mp.4002148 https://doi.org/10.1038/sj.mp.4002148

Frenois F , Moreau M , O’Connor J , et al . Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior . Psychoneuroendocrinology 2007 ; 32 ( 5 ): 516 - 31 . doi: 10.1016/j.psyneuen.2007.03.005 https://dx.doi.org/10.1016/j.psyneuen.2007.03.005 . DOI: 10.1016/j.psyneuen.2007.03.005 http://doi.org/10.1016/j.psyneuen.2007.03.005 https://linkinghub.elsevier.com/retrieve/pii/S0306453007000637 https://linkinghub.elsevier.com/retrieve/pii/S0306453007000637

Tynan RJ , Naicker S , Hinwood M , et al . Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions . Brain Behav Immun 2010 ; 24 : 1058 - 68 . doi: 10.1016/j.bbi.2010.02.001 https://dx.doi.org/10.1016/j.bbi.2010.02.001 . DOI: 10.1016/j.bbi.2010.02.001 http://doi.org/10.1016/j.bbi.2010.02.001

Han RR , Liu ZY , Sun NN , et al . BDNF alleviates neuroinflammation in the hippocampus of type 1 diabetic mice via blocking the aberrant HMGB1/RAGE/NF-kappa B pathway . Aging Dis 2019 ; 10 ( 3 ): 611 - 25 . doi: 10.14336/Ad.2018.0707 https://dx.doi.org/10.14336/Ad.2018.0707 . DOI: 10.14336/Ad.2018.0707 http://doi.org/10.14336/Ad.2018.0707 http://www.aginganddisease.org/EN/10.14336/AD.2018.0707 http://www.aginganddisease.org/EN/10.14336/AD.2018.0707

Ransohoff RM , Perry VH . Microglial physiology: unique stimuli, specialized responses . Annu Rev Immunol 2009 ; 27 : 119 - 45 . doi: 10.1146/annurev.immunol.021908.132528 https://dx.doi.org/10.1146/annurev.immunol.021908.132528 . DOI: 10.1146/annurev.immunol.021908.132528 http://doi.org/10.1146/annurev.immunol.021908.132528

Kettenmann H , Hanisch UK , Noda M , et al . Physiology of microglia . Physiol Rev 2001 ; 91 ( 2 ): 461 - 553 . doi: 10.1152/physrev.00011.2010 https://dx.doi.org/10.1152/physrev.00011.2010 . DOI: 10.1152/physrev.00011.2010 http://doi.org/10.1152/physrev.00011.2010 https://www.physiology.org/doi/10.1152/physrev.00011.2010 https://www.physiology.org/doi/10.1152/physrev.00011.2010

Konsman JP , Kelley K , Dantzer R . Temporal and spatial relationships between lipopolysaccharide-induced expression of fos, interleukin-1 beta and inducible nitric oxide synthase in rat brain . Neuroscience 1999 ; 89 ( 2 ): 535 - 548 . doi: 10.1016/S0306-4522(98)00368-6 https://dx.doi.org/10.1016/S0306-4522(98)00368-6 . DOI: 10.1016/S0306-4522(98)00368-6 http://doi.org/10.1016/S0306-4522(98)00368-6

Rinaman L . Ascending projections from the caudal visceral nucleus of the solitary tract to brain regions involved in food intake and energy expenditure . Brain Res 2010 ; 1350 : 18 - 34 . doi: 10.1016/j.brainres.2010.03.059 https://dx.doi.org/10.1016/j.brainres.2010.03.059 . DOI: 10.1016/j.brainres.2010.03.059 http://doi.org/10.1016/j.brainres.2010.03.059

Kawai Y . Differential ascending projections from the male rat caudal nucleus of the tractus solitarius: an interface between local microcircuits and global macrocircuits . Front Neuroanat 2018 ; 12 : 63 . doi: 10.3389/Fnana.2018.00063 https://dx.doi.org/10.3389/Fnana.2018.00063 . DOI: 10.3389/Fnana.2018.00063 http://doi.org/10.3389/Fnana.2018.00063 https://www.frontiersin.org/article/10.3389/fnana.2018.00063/full https://www.frontiersin.org/article/10.3389/fnana.2018.00063/full

Ulrich-Lai YM , Herman JP . Neural regulation of endocrine and autonomic stress responses . Nat RevNeurosci 2009 ; 10 ( 6 ): 397 - 409 . doi: 10.1038/nrn2647 https://dx.doi.org/10.1038/nrn2647 . DOI: 10.1038/nrn2647 http://doi.org/10.1038/nrn2647

Russo SJ , Nestler EJ . The brain reward circuitry in mood disorders . Nat Rev Neurosci 2013 ; 14 ( 9 ): 609 - 25 . doi: 10.1038/nrn3381 https://dx.doi.org/10.1038/nrn3381 . DOI: 10.1038/nrn3381 http://doi.org/10.1038/nrn3381

Michelsen KA , Schmitz C , Steinbusch HWM . The dorsal raphe nucleus: from silver stainings to a role in depression . Brain Res Rev 2007 ; 55 ( 2 ): 329 - 342 . doi: 10.1016/j.brainresrev.2007.01.002 https://dx.doi.org/10.1016/j.brainresrev.2007.01.002 . DOI: 10.1016/j.brainresrev.2007.01.002 http://doi.org/10.1016/j.brainresrev.2007.01.002

George DT , Ameli R , Koob GF . Periaqueductal gray sheds light on dark areas of psychopathology . Trends Neurosci 2019 ; 42 ( 5 ): 349 - 60 . doi: 10.1016/j.tins.2019.03.004 https://dx.doi.org/10.1016/j.tins.2019.03.004 . DOI: S0166-2236(19)30038-4 http://doi.org/S0166-2236(19)30038-4

Schwarz LA , Luo LQ . Organization of the locus coeruleus-norepinephrine system . Curr Biol 2015 ; 25 ( 21 ): R1051 - R1056 , doi: 10.1016/j.cub.2015.09.039 https://dx.doi.org/10.1016/j.cub.2015.09.039 . DOI: 10.1016/j.cub.2015.09.039 http://doi.org/10.1016/j.cub.2015.09.039 https://linkinghub.elsevier.com/retrieve/pii/S0960982215011501 https://linkinghub.elsevier.com/retrieve/pii/S0960982215011501

Zahm DS . An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens . Neurosci Biobehav Rev 2000 ; 24 ( 1 ): 85 - 105 . doi: 10.1016/S0149-7634(99)00065-2 https://dx.doi.org/10.1016/S0149-7634(99)00065-2 . DOI: 10.1016/S0149-7634(99)00065-2 http://doi.org/10.1016/S0149-7634(99)00065-2

Konsman JP , Luheshi GN , Bluthe RM , et al . The vagus nerve mediates behavioural depression, but not fever, in response to peripheral immune signals: a functional anatomical analysis . Eur J Neurosci 2000 ; 12 : 4434 - 46 . doi: 10.1046/j.0953-816X.2000.01319.x https://dx.doi.org/10.1046/j.0953-816X.2000.01319.x . DOI: 10.1046/j.0953-816X.2000.01319.x http://doi.org/10.1046/j.0953-816X.2000.01319.x

Sarhan M , Freund-Mercier MJ , Veinante P . Branching patterns of parabrachial neurons projecting to the central extended amgydala: Single axonal reconstructions . J Comp Neurol 2005 ; 491 ( 4 ): 418 - 42 . doi: 10.1002/cne.20697 https://dx.doi.org/10.1002/cne.20697 . DOI: 10.1002/cne.20697 http://doi.org/10.1002/cne.20697

Gaykema RPA , Chen CC , Goehler LE . Organization of immune-responsive medullary projections to the bed nucleus of the stria terminalis, central amygdala, and paraventricular nucleus of the hypothalamus: evidence for parallel viscerosensory pathways in the rat brain . Brain Res 2007 ; 1130 ( 1 ): 130 - 45 . doi: 10.1016/j.brainres.2006.10.084 https://dx.doi.org/10.1016/j.brainres.2006.10.084 . DOI: 10.1016/j.brainres.2006.10.084 http://doi.org/10.1016/j.brainres.2006.10.084

Marvel FA , Chen CC , Badr N , et al . Reversible inactivation of the dorsal vagal complex blocks lipopolysaccharide-induced social withdrawal and c-Fos expression in central autonomic nuclei . Brain Behav Immun 2004 ; 18 : 123 - 34 . doi: 10.1016/j.bbi.2003.09.004 https://dx.doi.org/10.1016/j.bbi.2003.09.004 . DOI: 10.1016/j.bbi.2003.09.004 http://doi.org/10.1016/j.bbi.2003.09.004 https://linkinghub.elsevier.com/retrieve/pii/S0889159103001429 https://linkinghub.elsevier.com/retrieve/pii/S0889159103001429

Ericsson A , Kovacs KJ , Sawchenko PE . A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons . J Neurosci 1994 ; 14 ( 2 ): 897 - 913 . doi: 10.1523/JNEUROSCI.14-02-00897.1994 https://dx.doi.org/10.1523/JNEUROSCI.14-02-00897.1994 . DOI: 10.1523/JNEUROSCI.14-02-00897.1994 http://doi.org/10.1523/JNEUROSCI.14-02-00897.1994

Van Bockstaele EJ , Peoples J , Telegan P . Efferent projections of the nucleus of the solitary tract to peri-locus coeruleus dendrites in rat brain: evidence for a monosynaptic pathway . J Comp Neurol 1999 ; 412 ( 3 ): 410 - 28 . doi: 10.1002/(Sici)1096-9861(19990927)412:3<410::Aid-Cne3>3.0.Co https://dx.doi.org/10.1002/(Sici)1096-9861(19990927)412:3<410::Aid-Cne3>3.0.Co ;2-F. DOI: 10.1002/(Sici)1096-9861(19990927)412:3<410::Aid-Cne3>3.0.Co http://doi.org/10.1002/(Sici)1096-9861(19990927)412:3<410::Aid-Cne3>3.0.Co

Borsody MK , Weiss JM . The effects of endogenous interleukin-1 bioactivity on locus coeruleus neurons in response to bacterial and viral substances . Brain Res 2004 ; 1007 ( 1-2 ): 39 - 56 . doi: 10.1016/j.brainres.2004.02.011 https://dx.doi.org/10.1016/j.brainres.2004.02.011 . DOI: 10.1016/j.brainres.2004.02.011 http://doi.org/10.1016/j.brainres.2004.02.011

Borsody MK , Weiss JM . The subdiaphragmatic vagus nerves mediate activation of locus coeruleus neurons by peripherally administered microbial substances . Neuroscience 2005 ; 131 ( 1 ): 235 - 45 . doi: 10.1016/j.neuroscience.2004.09.061 https://dx.doi.org/10.1016/j.neuroscience.2004.09.061 . DOI: 10.1016/j.neuroscience.2004.09.061 http://doi.org/10.1016/j.neuroscience.2004.09.061

Chen LW , Rao ZR , Shi JW . Catecholaminergic neurons in the nucleus-tractus-solitarii which send their axons to the midbrain periaqueductal gray express fos protein after noxious-stimulation of the stomach: a triple labeling study in the rat . Neurosci Lett 1995 ; 189 ( 3 ): 179 - 81 . doi: 10.1016/0304-3940(95)11475-C https://dx.doi.org/10.1016/0304-3940(95)11475-C . DOI: 10.1016/0304-3940(95)11475-C http://doi.org/10.1016/0304-3940(95)11475-C

Bhatt S , Bhatt RS , Zalcman SS , et al . Peripheral and central mediators of lipopolysaccharide induced suppression of defensive rage behavior in the cat . Neuroscience 2009 ; 163 ( 4 ): 1002 - 11 . doi: 10.1016/j.neuroscience.2009.07.050 https://dx.doi.org/10.1016/j.neuroscience.2009.07.050 . DOI: 10.1016/j.neuroscience.2009.07.050 http://doi.org/10.1016/j.neuroscience.2009.07.050

Floyd NS , Keay KA , Arias CM , et al . Projections from the ventrolateral periaqueductal gray to endocrine regulatory subdivisions of the paraventricular nucleus of the hypothalamus in the rat . Neurosci Lett 1996 ; 220 ( 2 ): 105 - 8 . doi: 10.1016/S0304-3940(96)13240-7 https://dx.doi.org/10.1016/S0304-3940(96)13240-7 . DOI: 10.1016/S0304-3940(96)13240-7 http://doi.org/10.1016/S0304-3940(96)13240-7

Sawchenko PE , Swanson LW . The organization of noradrenergic pathways from the brain-stem to the paraventricular and supraoptic nuclei in the rat . Brain Res Rev 1982 ; 257 ( 3 ): 275 - 325 . doi: 10.1016/0165-0173(82)90010-8 https://dx.doi.org/10.1016/0165-0173(82)90010-8 . DOI: 10.1016/0165-0173(82)90010-8 http://doi.org/10.1016/0165-0173(82)90010-8

Bienkowski MS , Rinaman L . Noradrenergic inputs to the paraventricular hypothalamus contribute to hypothalamic-pituitary-adrenal axis and central fos activation in rats after acute systemic endotoxin exposure . Neuroscience 2008 ; 156 ( 4 ): 1093 - 2 . doi: 10.1016/j.neuroscience.2008.08.011 https://dx.doi.org/10.1016/j.neuroscience.2008.08.011 . DOI: 10.1016/j.neuroscience.2008.08.011 http://doi.org/10.1016/j.neuroscience.2008.08.011

Herman JP . Regulation of hypothalamo-pituitary-adrenocortical responses to stressors by the nucleus of the solitary tract/dorsal vagal complex . Cell Mol Neurobiol 2018 ; 38 ( 1 ): 25 - 35 . doi: 10.1007/s10571-017-0543-8 https://dx.doi.org/10.1007/s10571-017-0543-8 . DOI: 10.1007/s10571-017-0543-8 http://doi.org/10.1007/s10571-017-0543-8

Watkins LR , Maier SF , Goehler LE . Cytokine-to-brain communication: a review and analysis of alternative mechanisms . Life Sci 1995 ; 57 ( 11 ): 1011 - 26 . doi: 10.1016/0024-3205(95)02047-M https://dx.doi.org/10.1016/0024-3205(95)02047-M . DOI: 10.1016/0024-3205(95)02047-m http://doi.org/10.1016/0024-3205(95)02047-m

Buller KM . Role of circumventricular organs in pro-inflammatory cytokine-induced activation of the hypothalamic-pituitary-adrenal axis . Clin Exp Pharmacol Physiol 2001 ; 28 ( 7 ): 581 - 9 . doi: 10.1046/j.1440-1681.2001.03490.x https://dx.doi.org/10.1046/j.1440-1681.2001.03490.x . DOI: 10.1046/j.1440-1681.2001.03490.x http://doi.org/10.1046/j.1440-1681.2001.03490.x http://doi.wiley.com/10.1046/j.1440-1681.2001.03490.x http://doi.wiley.com/10.1046/j.1440-1681.2001.03490.x

Shapiro RE , Miselis RR . The central neural connections of the area postrema of the rat . J Comp Neurol 1985 ; 234 ( 3 ): 344 - 64 . doi: 10.1002/cne.902340306 https://dx.doi.org/10.1002/cne.902340306 . DOI: 10.1002/cne.902340306 http://doi.org/10.1002/cne.902340306

Views

1065

Downloads

CSCD

Alert me when the article has been cited

Submit

Publicity Resources

Effects of TYROBP Deficiency on Neuroinflammation of a Alzheimer’s Disease Mouse Model Carrying a PSEN1 p.G378E Mutation

Related Author

Ran Li

Zhanyun Lv

Yanxin Li

Wei Li

Yanlei Hao

Related Institution

School of Basic Medical Sciences, Shandong University

Zhejiang University Medical Center

Department of Neurology, Pingdu People’s Hospital

Department of Neurology, Affiliated Hospital of Jining Medical College

⁰