Leukocyte invasion of the brain after peripheral trauma in zebrafish (Danio rerio)
0
조회
0
다운로드
0
인용
0
참고문헌
초록
Despite well-known systemic immune reactions in peripheral trauma, little is known about their roles in posttraumatic neurological disorders, such as anxiety, sickness, and cognitive impairment. Leukocyte invasion of the brain, a common denominator of systemic inflammation, is involved in neurological disorders that occur in peripheral inflammatory diseases, whereas the influences of peripheral leukocytes on the brain after peripheral trauma remain largely unclear. In this study, we found that leukocytes, largely macrophages, transiently invaded the brain of zebrafish larvae after peripheral trauma through vasculature-independent migration, which was a part of the systemic inflammation and was mediated by interleukin-1b (il1b). Notably, myeloid cells in the brain that consist of microglia and invading macrophages were implicated in posttraumatic anxiety-like behaviors, such as hyperactivity (restlessness) and thigmotaxis (avoidance), while a reduction in systemic inflammation or myeloid cells can rescue these behaviors. In addition, invading leukocytes together with microglia were found to be responsible for the clearance of apoptotic cells in the brain; however, they also removed the nonapoptotic cells, which suggested that phagocytes have dual roles in the brain after peripheral trauma. More importantly, a category of conserved proteins between zebrafish and humans or rodents that has been featured in systemic inflammation and neurological disorders was determined in the zebrafish brain after peripheral trauma, which supported that zebrafish is a translational model of posttraumatic neurological disorders. These findings depicted leukocyte invasion of the brain during systemic inflammation after peripheral trauma and its influences on the brain through il1b-dependent mechanisms.
Abstract
Despite well-known systemic immune reactions in peripheral trauma, little is known about their roles in posttraumatic neurological disorders, such as anxiety, sickness, and cognitive impairment. Leukocyte invasion of the brain, a common denominator of systemic inflammation, is involved in neurological disorders that occur in peripheral inflammatory diseases, whereas the influences of peripheral leukocytes on the brain after peripheral trauma remain largely unclear. In this study, we found that leukocytes, largely macrophages, transiently invaded the brain of zebrafish larvae after peripheral trauma through vasculature-independent migration, which was a part of the systemic inflammation and was mediated by interleukin-1b (il1b). Notably, myeloid cells in the brain that consist of microglia and invading macrophages were implicated in posttraumatic anxiety-like behaviors, such as hyperactivity (restlessness) and thigmotaxis (avoidance), while a reduction in systemic inflammation or myeloid cells can rescue these behaviors. In addition, invading leukocytes together with microglia were found to be responsible for the clearance of apoptotic cells in the brain; however, they also removed the nonapoptotic cells, which suggested that phagocytes have dual roles in the brain after peripheral trauma. More importantly, a category of conserved proteins between zebrafish and humans or rodents that has been featured in systemic inflammation and neurological disorders was determined in the zebrafish brain after peripheral trauma, which supported that zebrafish is a translational model of posttraumatic neurological disorders. These findings depicted leukocyte invasion of the brain during systemic inflammation after peripheral trauma and its influences on the brain through il1b-dependent mechanisms.
참고문헌 (57)
- Prinz, M., "The role of peripheral immune cells in the CNS in steady state and disease", Nat. Neurosci, 20, pp.136~144 (2017)
- Baruch, K., "Cerebral nitric oxide represses choroid plexus NFκB-dependent gateway activity for leukocyte trafficking", EMBO J, 34, pp.1816~1828 (2015)
- Möhle, L., "Ly6C(hi)monocytes provide a link between antibiotic-induced changes in gut microbiota and adult hippocampal neurogenesis", Cell Rep, 15, pp.1945~1956 (2016)
- Prinz, M., "Heterogeneity of CNS myeloid cells and their roles in neurodegeneration", Nat. Neurosci, 14, pp.1227~1235 (2011)
- Greenhalgh, A. D., "Peripherally derived macrophages modulate microglial function to reduce inflammation after CNS injury", PLoS Biol, 16, pp.e2005264~ (2018)
- Wohleb, E. S., "Integrating neuroimmune systems in the neurobiology of depression", Nat. Rev. Neurosci, 17, pp.497~511 (2016)
- Cao, W., "Peripheral immune system in aging and Alzheimer’s disease", Mol. Neurodegener, 13, pp.51~ (2018)
- D’Mello, C., "Cerebral microglia recruit monocytes into the brain in response to tumor necrosis factoralpha signaling during peripheral organ inflammation", J. Neurosci, 29, pp.2089~2102 (2009)
- Buckman, L. B., "Obesity induced by a high-fat diet is associated with increased immune cell entry into the central nervous system", Brain. Behav. Immun, 35, pp.33~42 (2014)
- Garré, J. M., "CX3CR1(+)monocytes modulate learning and learning-dependent dendritic spine remodeling via TNF-α", Nat. Med, 23, pp.714~722 (2017)
- Zhu, H., "Inflammation caused by peripheral immune cells across into injured mouse blood brain barrier can worsen postoperative cognitive dysfunction induced by isoflurane", BMC Cell Biol, 19, pp.23~ (2018)
- MacKenzie, E. J., "Epidemiology of injuries : current trends and future challenges", Epidemiol. Rev, 22, pp.112~119 (2000)
- Kilpatrick, D. G., "National estimates of exposure to traumatic events and PTSD prevalence using DSM-IV and DSM-5 criteria", J. Trauma. Stress, 26, pp.537~547 (2013)
- Lord, J. M., "The systemic immune response to trauma: an overview of pathophysiology and treatment", Lancet, 384, pp.1455~1465 (2014)
- Alam, A., "Surgery, neuroinflammation and cognitive impairment", EBioMedicine, 37, pp.547~556 (2018)
- Das, M., "New perspectives on central and peripheral immune responses to acute traumatic brain injury", J. Neuroinflammation, 9, pp.236~ (2012)
- Brøchner, A. C., "Pathophysiology of the systemic inflammatory response after major accidental trauma", Scand. J. Trauma Resusc. Emerg. Med, 17, pp.43~ (2009)
- Nourshargh, S., "Leukocyte migration into inflamed tissues", Immunity, 41, pp.694~707 (2014)
- Lee, J. W., "Neuro-inflammation induced by lipopolysaccharide causes cognitive impairment through enhancement of beta-amyloid generation", J. Neuroinflammation, 5, pp.37~ (2008)
- Huang, C., "Evidence of the impact of systemic inflammation on neuroinflammation from a non-bacterial endotoxin animal model", J. Neuroinflammation, 15, pp.147~ (2018)
- Skelly, D. T., "Acute transient cognitive dysfunction and acute brain injury induced by systemic inflammation occur by dissociable IL-1-dependent mechanisms", Mol. Psychiatry, 24, pp.1533~1548 (2019)
- Fidalgo, A. R., "Systemic inflammation enhances surgery-induced cognitive dysfunction in mice", Neurosci. Lett, 498, pp.63~66 (2011)
- Yan, B., "IL-1β and reactive oxygen species differentially regulate neutrophil directional migration and Basal random motility in a zebrafish injury-induced inflammation model", J. Immunol, 192, pp.5998~6008 (2014)
- Fontana, B. D., "The developing utility of zebrafish models of neurological and neuropsychiatric disorders : a critical review", Exp. Neurol, 299, pp.157~171 (2018)
- Kimmel, C. B., "Stages of embryonic development of the zebrafish", Dev. Dyn, 203, pp.253~310 (1995)
- Pei, W., "Extracellular HSP60 triggers tissue regeneration and wound healing by regulating inflammation and cell proliferation", NPJ Regen. Med, 1, pp.16013~ (2016)
- Chen, X. K., "1-phenyl 2-thiourea (PTU) activates autophagy in zebrafish embryos", Autophagy, 17, pp.1~10 (2020)
- Sztal, T. E., "Using touchevoked response and locomotion assays to assess muscle performance and function in zebrafish", J. Vis. Exp, 116, pp.e54431~ (2016)
- Kedra, M., "TrkB hyperactivity contributes to brain dysconnectivity, epileptogenesis, and anxiety in zebrafish model of Tuberous Sclerosis Complex", Proc. Natl Acad. Sci. USA, 117, pp.2170~2179 (2020)
- Casano, A. M., "Developmental apoptosis mediates entry and positioning of microglia in the zebrafish brain", Cell Rep, 16, pp.897~906 (2016)
- Ma, A. C., "FusX: a rapid one-step transcription activator-like effector assembly system for genome science", Hum. Gene. Ther, 27, pp.451~463 (2016)
- Ma, A. C., "The role of jak2a in zebrafish hematopoiesis", Blood, 110, pp.1824~1830 (2007)
- Ogryzko, N. V., "Zebrafish tissue injury causes upregulation of interleukin-1and caspase-dependent amplification of the inflammatory response", Dis. Model. Mech, 7, pp.259~264 (2014)
- Bill, B. R., "A primer for morpholino use in zebrafish", Zebrafish, 6, pp.69~77 (2009)
- Taylor, J. C., "A novel zebrafish-based model of nociception", Physiol. Behav, 174, pp.83~88 (2017)
- Xu, J., "Microglia colonization of developing zebrafish midbrain is promoted by apoptotic neuron and lysophosphatidylcholine", Dev. Cell, 38, pp.214~222 (2016)
- Wang, X. -W., "Plasma levels of high mobility group box 1 increase in patients with posttraumatic stress disorder after severe blunt chest trauma : a prospective cohort study", J. Surg. Res, 193, pp.308~315 (2015)
- Wingo, A. P., "Expression of the PPM1F gene is regulated by stress and associated with anxiety and depression", Biol. Psychiatry, 83, pp.284~295 (2018)
- Wu, F., "Complement component C3a plays a critical role in endothelial activation and leukocyte recruitment into the brain", J. Neuroinflammation, 13, pp.23~ (2016)
- Wang, R. P. -H., "Systemic inflammation linking chronic periodontitis to cognitive decline", Brain. Behav. Immun, 81, pp.63~73 (2019)
- Huang, C., "Differential effects of propofol and dexmedetomidine on neuroinflammation induced by systemic endotoxin lipopolysaccharides in adult mice", Neurosci. Lett, 707, pp.134309~ (2019)
- Wohleb, E. S., "Re-establishment of anxiety in stress-sensitized mice is caused by monocyte trafficking from the spleen to the brain", Biol. Psychiatry, 75, pp.970~981 (2014)
- Wohleb, E. S., "Monocyte trafficking to the brain with stress and inflammation : a novel axis of immune-to-brain communication that influences mood and behavior", Front. Neurosci, 8, pp.447~ (2014)
- Wohleb, E. S., "Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxietylike behavior", J. Neurosci, 33, pp.13820~13833 (2013)
- Cusick, M. F., "Infiltrating macrophages are key to the development of seizures following virus infection", J. Virol, 87, pp.1849~1860 (2013)
- Yong, V. W., "Taking advantage of the systemic immune system to cure brain diseases", Neuron, 64, pp.55~60 (2009)
- Bremner, J. D., "Traumatic stress: effects on the brain", Dialogues Clin. Neurosci, 8, pp.445~461 (2006)
- Rea, V., "Using zebrafish to model autism spectrum disorder: a comparison of ASD risk genes between zebrafish and their mammalian counterparts", Front. Mol. Neurosci, 13, pp.575575~ (2020)
- Paouri, E., "Peripheral tumor necrosis factor-alpha (TNF-α) modulates amyloid pathology by regulating bloodderived immune cells and glial response in the brain of AD", TNF transgenic mice, 2017, pp.37, 5155~5171
- Varvel, N. H., "Infiltrating monocytes promote brain inflammation and exacerbate neuronal damage after status epilepticus", Proc. Natl Acad. Sci. USA, 113, pp.E5665~E5674 (2016)
- Li, S., "Microglial deletion and inhibition alleviate behavior of post-traumatic stress disorder in mice", J. Neuroinflammation, 18, pp.7~ (2021)
- McMahon, E. J., "Peripheral macrophage recruitment in cuprizone-induced CNS demyelination despite an intact blood-brain barrier", J. Neuroimmunol, 130, pp.32~45 (2002)
- Ransohoff, R. M., "Three or more routes for leukocyte migration into the central nervous system", Nat. Rev. Immunol, 3, pp.569~581 (2003)
- Jeong, J. -Y., "Functional and developmental analysis of the blood-brain barrier in zebrafish", Brain Res. Bull, 75, pp.619~628 (2008)
- Levy, R. M., "Systemic inflammation and remote organ injury following trauma require HMGB1", Am. J. Physiol. Regul. Integr. Comp. Physiol, 293, pp.R1538~R1544 (2007)
- Alam, A., "Cellular infiltration in traumatic brain injury", J. Neuroinflammation, 17, pp.328~ (2020)
- Huber-Lang, M., "Innate immune responses to trauma", Nat. Immunol, 19, pp.327~341 (2018)