Regeneration of the central nervous system-principles from brain regeneration in adult zebrafish

Zambusi, Alessandro; Ninkovic, Jovica

doi:10.4252/wjsc.v12.i1.8

Cited by 48 publications

(54 citation statements)

References 123 publications

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“…A key difference between mouse models and the zebrafish model is that zebrafish possess many constitutively active neurogenic niches in the adult CNS [ 79 , 80 , 81 ], particularly in the olfactory system with its diverse plasticity mechanisms [ 82 , 83 , 84 ]. The regenerative nature of the zebrafish is useful for examining the potential of multi-organ regeneration after damage from injury or disease, including the brain, spinal cord, retina, fin, and heart [ 85 ].…”

Section: Overview Of Physiological Functions Of Macrophages and MImentioning

confidence: 99%

“…For example, injury in the zebrafish is followed quickly by a microglial inflammatory response, characterized by morphological modification and leukocyte accumulation at the injury site [ 112 , 120 , 122 , 148 ]. There is also an increase in proliferation of ependymal glial cells that produces intermediate neural progenitors [ 85 , 149 ] that aid in replacing damaged neurons. Microglial cells abandon the injury site once sigma-1 receptors switch off [ 150 ], leading to a quickly resolved inflammatory response in the zebrafish telencephalon.…”

Section: Macrophages and Microglia In Tissue Regeneration In Fishmentioning

confidence: 99%

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Role of Macrophages and Microglia in Zebrafish Regeneration

Var

Byrd-Jacobs

2020

IJMS

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Currently, there is no treatment for recovery of human nerve function after damage to the central nervous system (CNS), and there are limited regenerative capabilities in the peripheral nervous system. Since fish are known for their regenerative abilities, understanding how these species modulate inflammatory processes following injury has potential translational importance for recovery from damage and disease. Many diseases and injuries involve the activation of innate immune cells to clear damaged cells. The resident immune cells of the CNS are microglia, the primary cells that respond to infection and injury, and their peripheral counterparts, macrophages. These cells serve as key modulators of development and plasticity and have been shown to be important in the repair and regeneration of structure and function after injury. Zebrafish are an emerging model for studying macrophages in regeneration after injury and microglia in neurodegenerative disorders such as Parkinson’s disease and Alzheimer’s disease. These fish possess a high degree of neuroanatomical, neurochemical, and emotional/social behavioral resemblance with humans, serving as an ideal simulator for many pathologies. This review explores literature on macrophage and microglial involvement in facilitating regeneration. Understanding innate immune cell behavior following damage may help to develop novel methods for treating toxic and chronic inflammatory processes that are seen in trauma and disease.

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Section: Overview Of Physiological Functions Of Macrophages and MImentioning

confidence: 99%

Section: Macrophages and Microglia In Tissue Regeneration In Fishmentioning

confidence: 99%

Role of Macrophages and Microglia in Zebrafish Regeneration

Var

Byrd-Jacobs

2020

IJMS

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“…These zones are detected along the entire rostro-caudal axis of the zebrafish brain and contain ventricularly positioned self-renewing neural progenitors ( Grandel et al, 2006 ; Kaslin et al, 2008 ; Kizil et al, 2012b ; Grandel and Brand, 2013 ). Zebrafish CNS regenerates via the proliferation and differentiation of the radial glial cells (RGCs), also referred to as ependymoglia due to their functional orthology to the mammalian ependymal cells, and the neuroepithelial-like progenitor cells ( Grandel et al, 2006 ; Ganz et al, 2010 ; Fleisch et al, 2011 ; Kizil et al, 2012b ; Kaslin et al, 2017 ; Lindsey et al, 2017 ; Zambusi and Ninkovic, 2020 ). The permissive environment, which is necessary for these progenitors—upon injury—to become activated and differentiate into functional neurons, results most likely from the fact that zebrafish does not form any obvious scar tissue after injury in the CNS, thus granting zebrafish a regeneration potential higher than that of mammals ( Becker and Becker, 2002 ; Kroehne et al, 2011 ).…”

Section: Introductionmentioning

confidence: 99%

“…Being one of the best-characterized regions of the adult zebrafish brain, the telencephalon harbors at least two distinct neurogenic zones, the dorsal and the medio-ventral neurogenic niches, with ependymoglial cells that differ in their proliferation and progeny characteristics ( Marz et al, 2010 ; Zambusi and Ninkovic, 2020 ). Accordingly, these cells express different markers including glial fibrillary acidic protein (Gfap), S100β, nestin, brain lipid-binding protein (Blbp), aromatase, and SRY-box 2 (Sox2), confirming their radial glia-like nature ( Adolf et al, 2006 ; Pellegrini et al, 2007 ; Lam et al, 2009 ; Ganz et al, 2010 ; Marz et al, 2010 ; Kroehne et al, 2011 ).…”

Section: Introductionmentioning

confidence: 99%

Comparative Transcriptome Analysis of the Regenerating Zebrafish Telencephalon Unravels a Resource With Key Pathways During Two Early Stages and Activation of Wnt/β-Catenin Signaling at the Early Wound Healing Stage

Demırcı

Cucun

Poyraz

et al. 2020

Front. Cell Dev. Biol.

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Owing to its pronounced regenerative capacity in many tissues and organs, the zebrafish brain represents an ideal platform to understand the endogenous regeneration mechanisms that restore tissue integrity and function upon injury or disease. Although radial glial and neuronal cell populations have been characterized with respect to specific marker genes, comprehensive transcriptomic profiling of the regenerating telencephalon has not been conducted so far. Here, by processing the lesioned and unlesioned hemispheres of the telencephalon separately, we reveal the differentially expressed genes (DEGs) at the early wound healing and early proliferative stages of regeneration, i.e., 20 h post-lesion (hpl) and 3 days post-lesion (dpl), respectively. At 20 hpl, we detect a far higher number of DEGs in the lesioned hemisphere than in the unlesioned half and only 7% of all DEGs in both halves. However, this difference disappears at 3 dpl, where the lesioned and unlesioned hemispheres share 40% of all DEGs. By performing an extensive comparison of the gene expression profiles in these stages, we unravel that the lesioned hemispheres at 20 hpl and 3 dpl exhibit distinct transcriptional profiles. We further unveil a prominent activation of Wnt/β-catenin signaling at 20 hpl, returning to control level in the lesioned site at 3 dpl. Wnt/β-catenin signaling indeed appears to control a large number of genes associated primarily with the p53, apoptosis, forkhead box O (FoxO), mitogen-activated protein kinase (MAPK), and mammalian target of rapamycin (mTOR) signaling pathways specifically at 20 hpl. Based on these results, we propose that the lesioned and unlesioned hemispheres react to injury dynamically during telencephalon regeneration and that the activation of Wnt/β-catenin signaling at the early wound healing stage plays a key role in the regulation of cellular and molecular events.

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“…The fundamental importance of NSCs stimulated an explosive research field during the last 20-years, and, more recently, the development of a new study model: the zebrafish adult brain. The large amount of adult NSCs in this system, their widespread distribution and varied properties, and their reactivity toward regeneration, all propelled the zebrafish model to the forefront of adult NSC research, as a complementary and synergistic model to rodents (Anand and Mondal, 2017;Lindsey et al, 2018;Zambusi and Ninkovic, 2020). The time to reach sexual maturity in zebrafish (3 months) and the adult lifespan also approximate those of mouse, allowing to draw direct temporal parallels.…”

mentioning

confidence: 99%

Conserved and Divergent Features of Adult Neurogenesis in Zebrafish

Labusch

Mancini

Morizet

et al. 2020

Front. Cell Dev. Biol.

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Adult neurogenesis, i.e., the generation of neurons from neural stem cells (NSCs) in the adult brain, contributes to brain plasticity in all vertebrates. It varies, however, greatly in extent, location and physiological characteristics between species. During the last decade, the teleost zebrafish (D. rerio) was increasingly used to study the molecular and cellular properties of adult NSCs, in particular as a prominent NSC population was discovered at the ventricular surface of the dorsal telencephalon (pallium), in territories homologous to the adult neurogenic niches of rodents. This model, for its specific features (large NSC population, amenability to intravital imaging, high regenerative capacity) allowed rapid progress in the characterization of basic adult NSC features. We review here these findings, with specific comparisons with the situation in rodents. We specifically discuss the cellular nature of NSCs (astroglial or neuroepithelial cells), their heterogeneities and their neurogenic lineages, and the mechanisms controlling NSC quiescence and fate choices, which all impact the neurogenic output. We further discuss the regulation of NSC activity in response to physiological triggers and non-physiological conditions such as regenerative contexts.

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Regeneration of the central nervous system-principles from brain regeneration in adult zebrafish

Cited by 48 publications

References 123 publications

Role of Macrophages and Microglia in Zebrafish Regeneration

Role of Macrophages and Microglia in Zebrafish Regeneration

Comparative Transcriptome Analysis of the Regenerating Zebrafish Telencephalon Unravels a Resource With Key Pathways During Two Early Stages and Activation of Wnt/β-Catenin Signaling at the Early Wound Healing Stage

Conserved and Divergent Features of Adult Neurogenesis in Zebrafish

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