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Stress Induces the Danger-Associated Molecular Pattern HMGB-1 in the Hippocampus of Male Sprague Dawley Rats: A Priming Stimulus of Microglia and the NLRP3 Inflammasome
Open accessAbstract
Exposure to acute and chronic stressors sensitizes the proinflammatory response of microglia to a subsequent immune challenge. However, the proximal signal by which stressors prime microglia remains unclear. Here, high mobility group box-1 (HMGB-1) protein was explored as a potential mediator of stress-induced microglial priming and whether HMGB-1 does so via the nucleotide-binding domain, leucine-rich repeat, pyrin domain containing protein 3 (NLRP3) inflammasome. Exposure to 100 inescapable tail shocks (ISs) increased HMGB-1 and NLRP3 protein in the hippocampus and led isolated microglia to release HMGB-1 ex vivo. To determine whether HMGB-1 signaling is necessary for stress-induced sensitization of microglia, the HMGB-1 antagonist BoxA was injected into the cisterna magna before IS. Hippocampal microglia were isolated 24 h later and stimulated with LPS ex vivo to probe for stress-induced sensitization of proinflammatory responses. Previous IS potentiated gene expression of NLRP3 and proinflammatory cytokines to LPS, that is, microglia were sensitized. Treatment with BoxA abolished this effect. To determine whether HMGB-1 is sufficient to prime microglia, IS was replaced with intracerebral administration of disulfide or fully reduced HMGB-1. Intracerebral disulfide HMGB-1 mimicked the effect of the stressor, because microglia isolated from HMGB-1-treated rats expressed exaggerated NLRP3 and proinflammatory cytokine expression after LPS treatment, whereas fully reduced HMGB-1 had no effect. The present results suggest that the CNS innate immune system can respond to an acute stressor as if it were cellular damage, thereby releasing the danger signal HMGB-1 in the brain to prime microglia by acting on the NLRP3 inflammasome, in preparation for a later immune challenge.
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“We have also found that exposure to acute stress, in this case inescapable tailshock, increases NLRP3 protein in the hippocampus up to 24 h after stress treatment; however, microglial IL-1β was not increased at that time-point post stress (Weber et al, 2015).”
From Danger Signals and Inflammasomes: Stress-Evoked Sterile Inflammation in Mood Disorders (2017) · cites this paper as Weber et al, 2015
In the citing paper
“we found that intracisterna magna administration of an HMGB1 antagonist (box A) before stress exposure blocked the potentiated microglial proinflammatory response to an immune challenge ex vivo.”
From Danger Signals and Inflammasomes: Stress-Evoked Sterile Inflammation in Mood Disorders (2017) · cites this paper as Weber et al, 2015
In the citing paper
“We recently found that exposure to an acute stressor (inescapable tailshock) induces HMGB1 in the hippocampus concomitant with increased protein levels of active NF-κB and NLRP3 protein (Weber et al, 2015).”
From Danger Signals and Inflammasomes: Stress-Evoked Sterile Inflammation in Mood Disorders (2017) · cites this paper as Weber et al, 2015
In the citing paper
“treatment of hippocampal microglia with the TLR4 agonist LPS resulted in a potentiated IL-1β response in animals exposed to stress 24 h earlier, suggesting that the NLRP3 inflammasome was primed by initial stress exposure.”
From Danger Signals and Inflammasomes: Stress-Evoked Sterile Inflammation in Mood Disorders (2017) · cites this paper as Weber et al, 2015
In the citing paper
“Recently, HMGB-1 was found to be highly expressed in the CNS and was implicated in a variety of neuroinflammatory conditions (Kang et al, 2014), including stress (Weber et al, 2015).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Weber et al, 2015
In the citing paper
“For example, HMGB-1 protein is increased in the hippocampus following a series of repeated tail shock and persists for at least 24 h later (Weber et al, 2015).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Weber et al, 2015
In the citing paper
“Pharmacological antagonism of the receptor targets for HMGB-1 blocked the effect of stress to prime microglia (Weber et al, 2013(Weber et al, , 2015)).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Weber et al, 2015
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InfluentialPark, J. S., Svetkauskaite, D., He, Q., Kim, J., Strassheim, D., Ishizaka, A., & Abraham, E. H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m306793200 · Cited by 1,582
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“For example, repeated electric tail shocks increase the hippocampal release of high mobility group box-1 (HMGB1), a DAMP known to induce microglial activation (Weber et al., 2015).”
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Weber, M. D., Godbout, J. P., & Sheridan, J. F. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.102 · Cited by 283
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InfluentialSelf-citationPsychedelics in Psychiatry: Neuroplastic, Immunomodulatory, and Neurotransmitter Mechanisms
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“This is similar to previous reports that NLRP3 is primed in response to TLR4 activation by LPS, priming that includes increased levels of NLRP3 (Bauernfeind et al., 2009; Guo et al., 2015; Weber et al., 2015).”
InfluentialInflammasomes link vascular disease with neuroinflammation and brain disorders
Lénárt, N., Brough, D., & Dénes, Á. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16662043 · Cited by 170
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“For instance, stress-induced release of the DAMP, high mobility box group (HMGB)-1, caused microglia priming through inflammasome activation and increased pro-inflammatory gene expression (100).”
BackgroundInflammasomes in neurological diseases: emerging pathogenic and therapeutic concepts
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“Models such as shock-induced stress (foot shock and tail shock) are probably more accepted as models of inflammation in the periphery with emerging data to support a neuroinflammatory component in the pathology (Arakawa et al. 2009; Weber et al. 2015).”
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“Importantly, extranuclear HMGB1 does not necessarily induce a proinflammatory cytokine response in the brain; rather, HMGB1 can potentiate the effects of a subsequent neuroinflammatory challenge (Weber et al., 2015).”
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“Recently, we found that box A administered into the CNS blocks stress-induced sensitization of the microglial pro-inflammatory response to lipopolysaccharide (LPS) ex vivo, suggesting that stress induces the release of HMGB1 in the CNS, which then functions to sensitize neuroinflammatory processes (Weber et al., 2015).”
InfluentialSelf-citationChecks and balances: The glucocorticoid receptor and NFĸB in good times and bad
Bekhbat, M., Rowson, S. A., & Neigh, G. N. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.05.001 · Cited by 142
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“A recent study showed that the innate immune system in the CNS responds to acute stressors by releasing the hazard signal high-mobility group box-1 (HMGB-1) in primate brains, which activates microglia by acting on the NLRP3 inflammasome [80].”
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“Some examples of DAMPs include high mobility group box 1 (Weber et al., 2015) and heat shock proteins (Hsp), particularly Hsp72 (Johnson & Fleshner, 2006).”
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“In this context, it has been shown that activation of HMGB1 is associated with depression while blockage of HMGB1 attenuated the depressive-like behaviors (Weber et al., 2015; Wu et al., 2015).”
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“The finding of M2-type of microglia, however, is not inconsistent with innate immune induction via DAMPs eliciting primed microglia (Crews et al., 2013; Frank et al., 2016; Weber, Frank, Tracey, Watkins, & Maier, 2015).”
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Stress and aging act through common mechanisms to elicit neuroinflammatory priming
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Self-citationInnate Immune Signaling and Alcohol Use Disorders
Coleman, L. G., & Crews, F. T. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_92 · Cited by 97
Sterile Neuroinflammation and Strategies for Therapeutic Intervention
Banjara, M., & Ghosh, C. (2017) · International Journal of Inflammation · doi:10.1155/2017/8385961 · Cited by 92
“Elevation of HMGB1 in brain was measured in nondegenerative neuroinflammatory condition such as TBI [90], ethanol exposure [91], and stress-induced neuroinflammatory priming [92].”
Welcome, M. O. (2020) · Inflammopharmacology · doi:10.1007/s10787-020-00712-8 · Cited by 85
Effect of Systemic Inflammation in the CNS: A Silent History of Neuronal Damage
Solano, M. V. M., Lara, C. S., Sánchez-Garibay, C., Soto-Rojas, L. O., Escobedo-Ávila, I., Tena‐Suck, M. L., Ortiz-Butrón, R., Choreño-Parra, J. A., Romero‐López, J. P., & Meléndez-Camargo, M. E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241511902 · Cited by 78
“HMGB1 could be one of the causes of the damage since it can initiate and perpetuate neuroinflammation during sepsis without direct injury to the CNS [39,94] (Figure 2).”
InfluentialStress disinhibits microglia via down-regulation of CD200R: A mechanism of neuroinflammatory priming
Frank, M. G., Fonken, L. K., Annis, J. L., Watkins, L. R., & Maier, S. F. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.11.001 · Cited by 77
Self-citationVisentin, A. P. V., Colombo, R., Scotton, E., Fracasso, D. S., Rosa, A. R., Branco, C. S., & Salvador, M. M. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/2972968 · Cited by 77
“The increased release of DAMPs from the high mobility moiety (HMGB1) box 1 protein caused the activation of microglia and increased gene expression of proinflammatory cytokines [63].”
BackgroundAlcohol and Stress Activation of Microglia and Neurons: Brain Regional Effects
Walter, T. J., Vetreno, R. P., & Crews, F. T. (2017) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13511 · Cited by 71
“Acute stress also increases brain expression of cytokines such as TNF-a, IL1b, and Ccl2 (Knapp et al., 2016) and the danger signaling molecule, high mobility group box-1 protein (HMGB1) (Frank et al., 2015; Weber et al., 2015).”
BackgroundInfluentialRosciszewski, G., Cadena, V., Auzmendi, J., Cieri, M. B., Lukin, J., Rossi, A. R., Murta, V., Villarreal, A., Reinés, A. G., Gomes, F. C. A., et al. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00380 · Cited by 74
“High Mobility Group Box 1 (HMGB1) is an ubiquitous nuclear protein that is implicated in the maintenance of chromatin structure (Ellwood et al., 2000; Verrijdt et al., 2002) and that, following Central Nervous System (CNS) injury, is released as a DAMP (Qiu et al., 2008; Maroso et al., 2010).”
BackgroundInfluentialMarón, F. J. M., Ferder, L., Saraví, F. D., & Manucha, W. A. (2018) · Stress · doi:10.1080/10253890.2018.1542683 · Cited by 80
Stress-induced neuroinflammatory priming is time of day dependent
Fonken, L. K., Weber, M. D., Daut, R. A., Kitt, M. M., Frank, M. G., Watkins, L. R., & Maier, S. F. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.01.006 · Cited by 72
Self-citationFrank, M. G., Adhikary, S., Sobesky, J. L., Weber, M. D., Watkins, L. R., & Maier, S. F. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.08.001 · Cited by 70
“This dose of box A was selected because of its efficacy in blocking stress-induced neuroinflammatory priming (Weber et al., 2015) and as well as HMGB1 mediated seizure (Maroso et al.”
Self-citationZhang, H., Ding, L., Shen, T., & Peng, D. (2019) · General Psychiatry · doi:10.1136/gpsych-2019-100084 · Cited by 67
“16 Moreover, HMGB1 has been involving in several neuroinflammatory conditions, such as Alzheimer’s disease 17 and brain ischaemia injury.”
Prowse, N. A., & Hayley, S. P. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.018 · Cited by 72
“…found that HMGB1 activates microglia through the receptor for advanced glycation end products (RAGE) receptors (Franklin et al., 2018; Okuma et al., 2012; Weber et al., 2015; Zhang et al., 2020a) with stress-induced behavioural deficits ameliorated in RAGE-knockout mice (Franklin et al., 2018).”
BackgroundZhou, Z., Hou, J., Mo, Y., Ren, M., Yang, G., Qu, Z., & Hu, Y. (2019) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2019.172857 · Cited by 69
Frank, M. G., Fonken, L. K., Watkins, L. R., & Maier, S. F. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.05.063 · Cited by 70
“As noted, the NLRP3 inflammasome has been implicated in the neuroinflammatory effects of stress as well as the priming effects of stress (Alcocer-Gomez et al., 2015; Bharti et al., 2019; Feng et al., 2019; Iwata et al., 2015; Pan et al., 2014; Weber et al., 2015).”
BackgroundResultInfluentialSelf-citationSobesky, J. L., D’Angelo, H. M., Weber, M. D., Anderson, N. D., Frank, M. G., Watkins, L. R., Maier, S. F., & Barrientos, R. M. (2016) · eNeuro · doi:10.1523/eneuro.0113-16.2016 · Cited by 64
“These data are consistent with previous findings showing that levels of these molecules are elevated in response to increases in CORT levels (Busillo et al., 2011; Frank et al., 2014; Weber et al., 2015).”
ResultSelf-citationXie, J., Bi, B., Qin, Y., Dong, W., Zhong, J., Li, M., Cheng, Y., Xu, J., & Wang, H. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.11.029 · Cited by 62
Gut microbiota and neuropsychiatric disorders: Implications for neuroendocrine-immune regulation
Ge, T., Yao, X., Zhao, H., Yang, W., Zou, X., Peng, F., Li, B., & Cui, R. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105909 · Cited by 62
Lifestyle Shapes the Dialogue between Environment, Microglia, and Adult Neurogenesis
Valero, J., Paris, I., & Sierra, A. (2016) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.6b00009 · Cited by 64
Kim, I., Lee, H., Kim, S.-W., Lee, H., Choi, J., Han, P., & Lee, J.-K. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0438-8 · Cited by 61
Neuroimmune and Inflammatory Signals in Complex Disorders of the Central Nervous System
Liberman, A. C., Trías, E., Chagas, L. D. S., Trindade, P., Pereira, M. D. S., Refojo, D., Hedin‐Pereira, C., & Serfaty, C. A. (2018) · NeuroImmunoModulation · doi:10.1159/000494761 · Cited by 62
NOD-like Receptors in the Eye: Uncovering Its Role in Diabetic Retinopathy
Lim, R. R., Wieser, M. E., Ganga, R., Barathi, V. A., Lakshminarayanan, R., Mohan, R. R., Hainsworth, D. P., & Chaurasia, S. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21030899 · Cited by 59
“Similarly, high mobility group box-1 (HMGB-1) did not activate NLRP3 in THP-1 macrophages [64] but primed the inflammasome in the hippocampal microglial cells [65].”
BackgroundEspinosa‐García, C., Atif, F., Yousuf, S., Sayeed, I., Neigh, G. N., & Stein, D. G. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113740 · Cited by 59
AC-YVAD-CMK Inhibits Pyroptosis and Improves Functional Outcome after Intracerebral Hemorrhage
Lin, X., Ye, H., Siaw-Debrah, F., Pan, S., He, Z., Ni, H., Xu, Z., Jin, K., Zhuge, Q., & Huang, L. (2018) · BioMed Research International · doi:10.1155/2018/3706047 · Cited by 58
Horowitz, M. A., Cattaneo, A., Cattane, N., Lopizzo, N., Tojo, L. M., Bakunina, N., Musaelyan, K., Borsini, A., Zunszain, P. A., & Pariante, C. M. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.03.012 · Cited by 61
“Consistent with this, exposure to stress increases NLRP3 in hippocampal microglia that subsequently show potentiated inflammatory responses (Weber et al., 2015).”
BackgroundHow Stress Shapes Neuroimmune Function: Implications for the Neurobiology of Psychiatric Disorders
Koo, J. W., & Wohleb, E. S. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.11.007 · Cited by 60
The role of tryptophan metabolism in postpartum depression
Duan, K., Ma, J., Wang, S., Huang, Z., Zhou, Y., & Yu, H. (2018) · Metabolic Brain Disease · doi:10.1007/s11011-017-0178-y · Cited by 61
“Stress is closely associated with microglia activation, including via the induction of high-mobility group box 1 (HMGB1) and inflammasome activation, leading to increased IL-1 and IL-18, further activating IDO and the driving of tryptophan down the kynurenine pathway (Weber et al. 2015).”
BackgroundMicroglial Responses to Stress-Induced Depression: Causes and Consequences
Afridi, R., & Suk, K. (2023) · Cells · doi:10.3390/cells12111521 · Cited by 61
“Increased HMGB1 expression positively correlated with heightened NLRP3 inflammasome signaling [78].”
BackgroundLiu, L., Zhao, Z., Lu, L., Liu, J., Sun, J., & Dong, J. (2019) · International Immunopharmacology · doi:10.1016/j.intimp.2019.105799 · Cited by 53
Zhang, F. F., Morioka, N., Harano, S., Nakamura, Y., Liu, K., Nishibori, M., Hisaoka‐Nakashima, K., & Nakata, Y. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13434 · Cited by 52
Xu, E., Liu, J., Liu, H., Wang, X., & Xiong, H. (2018) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-018-9780-y · Cited by 52
“Taken together, the sensitization of proinflammatory responses by these endo- or exogenous danger signals are primarily achieved by priming the NLRP3 inflammasome for subsequent immune challenges (Weber et al. 2015).”
Neuroinflammation in Response to Intracerebral Injections of Different HMGB1 Redox Isoforms
Aucott, H., Lundberg, J., Salo, H., Klevenvall, L., Damberg, P., Ottosson, L., Andersson, U., Holmin, S., & Harris, H. E. (2018) · Journal of Innate Immunity · doi:10.1159/000487056 · Cited by 51
Molecular insights into the therapeutic promise of targeting HMGB1 in depression
Rana, T., Behl, T., Mehta, V., Uddin, M. S., & BUNGAU, S. G. (2020) · Pharmacological Reports · doi:10.1007/s43440-020-00163-6 · Cited by 49
Impact of Stress on Epilepsy: Focus on Neuroinflammation—A Mini Review
Espinosa‐García, C., Zeleke, H., & Rojas, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084061 · Cited by 56
The permissive role of glucocorticoids in neuroinflammatory priming
Frank, M. G., Watkins, L. R., & Maier, S. F. (2015) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0000000000000168 · Cited by 48
Self-citationXu, B., Zang, S., Li, S., Guo, J., Wang, J., Wang, D., Zhang, L.-P., Yang, H.-M., & Lian, S. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.11.313 · Cited by 47
Neuroinflammation and Mitochondrial Dysfunction Link Social Stress to Depression
Hollis, F., Pope, B. S., Gorman‐Sandler, E., & Wood, S. K. (2022) · Current topics in behavioral neurosciences · doi:10.1007/7854_2021_300 · Cited by 47
Vecchiarelli, H. A., Gandhi, C. P., Gray, J. M., Morena, M., Hassan, K. I., & Hill, M. N. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.07.026 · Cited by 44
“However, it has been shown that acute restraint stress, and specifically glucocorticoid signaling, can prime these regions, particularly the hippocampus, to respond to a second, inflammatory challenge with a more robust cytokine response than an inflammatory challenge alone (Frank et al., 2015, 2013, 2012; Weber et al…”
InfluentialRelevance of chronic stress and the two faces of microglia in Parkinson's disease
Herrera, A. J., Espinosa-Oliva, A. M., Carrillo-Jiménez, A., Oliva-Martín, M. J., García-Revilla, J., García-Quintanilla, A., de Pablos, R. M., & Venero, J. L. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00312 · Cited by 42
Mitochondrial DAMPs: Key mediators in neuroinflammation and neurodegenerative disease pathogenesis
Yu, H., Ren, K., Jin, Y., Zhang, L., Liu, H., Huang, Z., Zhang, Z., Chen, X., Yang, Y., & Wei, Z. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.110217 · Cited by 46
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An emerging role for microglia in stress‐effects on memory
Sanguino‐Gómez, J., Buurstede, J. C., Abiega, O., Fitzsimons, C. P., Lucassen, P. J., Eggen, B. J. L., Lesuis, S. L., Meijer, O. C., & Krugers, H. J. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15188 · Cited by 43
“Increased levels of the inflammasome have been reported after either acute (Iwata et al., 2016; Weber et al., 2015) or chronic (Alcocer-Gómez et al., 2016; Wang et al., 2018) exposure to stressors in adulthood.”
BackgroundAlarmins and central nervous system inflammation in HIV ‐associated neurological disorders
Gougeon, M. (2016) · Journal of Internal Medicine · doi:10.1111/joim.12570 · Cited by 41
Melbourne, J. K., Thompson, K. R., Peng, H., & Nixon, K. (2019) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2019.06.011 · Cited by 40
Medina‐Ceja, L., Salazar‐Sánchez, J. C., Ortega‐Ibarra, J., & Morales‐Villagrán, A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20235976 · Cited by 41
“The second signal is attributed to ATP [56–58] and glutamate via N-methyl-Daspartate (NMDA) receptors [59,60].”
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MicroRNA-574-5p Attenuates Acute Respiratory Distress Syndrome by Targeting HMGB1
He, B., Zhou, W., Rui, Y., Liu, L., Chen, B., & Su, X. (2020) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2020-0112oc · Cited by 41
Metadata
- Authors
- Weber, M. D., Frank, M. G., Tracey, K. J., Watkins, L. R., & Maier, S. F.
- Affiliations
- University of Colorado Boulder (US)
- Northwell Health (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2015-01-07
- Volume
- 35
- Issue
- 1
- Pages
- 316-324
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4287150
- OpenAlex
- W2087987871
- Cited by
- 215
- References
- 46
- Citations by year
- 2026: 10 · 2025: 10 · 2024: 12 · 2023: 11 · 2022: 20 · 2021: 21 · 2020: 25 · 2019: 19 · 2018: 24 · 2017: 25 · 2016: 21 · 2015: 16
- FWCI
- 15.29
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH096224, R21MH096224)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- HMGB1, NLRP3 inflammasome, microglial priming, hippocampus, inflammatory cytokines, lipopolysaccharide response, damage-associated molecular patterns
- MeSH terms
- NLR Family, Pyrin Domain-Containing 3 Protein, Animals, Carrier Proteins, Hippocampus, Male, Stress, Psychological, Rats, Sprague-Dawley, Microglia, Receptors, Cytoplasmic and Nuclear, HMGB1 Protein, Rats, Inflammasomes
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