International Review of Cell and Molecular Biology (eBook)

Kwang W. Jeon (Herausgeber)

eBook Download: PDF | EPUB

2015 | 1. Auflage
318 Seiten
Elsevier Science (Verlag)
978-0-12-802477-5 (ISBN)

Infos

International Review of Cell and Molecular Biology presents comprehensive reviews and current advances in cell and molecular biology, with articles addressing structure and control of gene expression, nucleocytoplasmic interactions, control of cell development and differentiation, and cell transformation and growth. The series has a worldwide readership, maintaining a high standard by publishing invited articles on important and timely topics authored by prominent cell and molecular biologists. - Authored by some of the foremost scientists in the field - Provides comprehensive reviews and current advances - Brings a fresh perspective to those conducting research in cell biology, molecular biology, biochemistry, biotechnology, plant biology, physiology, and microbiology, among others - Includes a wide range of perspectives on specific subjects - Valuable reference material for advanced undergraduates, graduate students, and professional scientists

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Chapter One

Dendritic Remodeling

Lessons from Invertebrate Model Systems

Takahiro Kanamori1,2, Kazuya Togashi1,2, Hiroyuki Koizumi1,2 and Kazuo Emoto1,2,∗     1Department of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo, Japan     2Department of Cell Biology, Osaka Bioscience Institute, Osaka, Japan
∗ Corresponding author: E-mail: [e-mail] 

Abstract

Dendrites are the entry site of neural signals into neurons. Once formed, dendrites are not just the same in structure but rather are dynamically remodeled in vivo: some dendrites are pruned away, while others lengthen and branch out. Dendritic remodeling occurs not only during neural development, but also in mature dendrites under both physiological and pathological conditions, suggesting its contribution to neural plasticity. The underlying cellular and molecular mechanisms remained poorly understood until recently, but they are just beginning to be elucidated from recent studies on invertebrate model systems. Here, we review recent advances in our understanding of how dendrites are remodeled by focusing particularly on insights obtained from Drosophila sensory neurons.

Keywords

Dendrites; Dendritic remodeling; Drosophila; Metamorphosis; Neuron

1. Introduction

Dendrites are the entry site of neural signals. In most types of neurons, neural signals, such as external stimuli for sensory neurons and synaptic inputs for postsynaptic neurons, are processed and converted to electrical signals in dendritic branches. The early anatomical studies, pioneered by Ramón y Cajal, have revealed that dendritic structure can vary considerably between neurons (Cajal, 1911). This has led the researchers to believe that the dendritic divergence might explain, at least in part, why neurons show distinct functional properties in the brain. The fact that functional properties of neurons can often change in a plastic manner in vivo raises an intriguing question: do neurons remodel their dendrites structurally?

It has become increasingly clear that dendrites are remodeled in developmental, physiological, and pathological contexts. During neural development, neurons eliminate selectively exuberant dendritic branches to refine neural circuits. For example, in the developing olfactory system of rats, mitral cells initially form multiple primary dendrites that contact adjacent glomeruli; however, they eventually prune all but one dendritic branch that remains in contact with a single glomerulus (Malun and Brunjes, 1996). Developmental refinement of dendritic branches is also observed in other types of neurons, including retinal ganglion cells (Wang et al., 2001), spiny stellate cells in layer 4 of the primary somatosensory cortex (Mizuno et al., 2014), and the cerebellar Purkinje cells (Kaneko et al., 2011). In a physiological condition, the superficial layer 2/3 interneurons in cerebral cortex dynamically add and eliminate dendritic branches, and the fraction of dynamic dendrites increases by threefold after sensory deprivation, suggesting that neural activity influences the dynamics of dendritic remodeling (Chen et al., 2011; Lee et al., 2006). Pathologically, chronic stress and drug exposure can induce dendritic remodeling in a wide range of cerebral neurons in rodents (Ehlinger et al., 2012; Gourley et al., 2013; Li et al., 2012; Liston et al., 2006). Thus, increasing evidence indicates that both developing and mature neurons have the ability to remodel their dendritic branches. However, due to the lack of an appropriate model system, the cellular and molecular mechanisms of dendritic remodeling have remained poorly understood.

Structural remodeling of dendrites has been reported to occur also in invertebrate nervous systems. In Drosophila, a variety of neurons in both the central nervous system (CNS) and peripheral nervous system (PNS) remodel their dendritic branches during metamorphosis from larva to pupa and adult (Consoulas, 2002; Kuo et al., 2005; Scott et al., 2011; Watts et al., 2003; Williams and Truman, 2005). By taking advantage of the genetic tools available in Drosophila, a decade of extensive research has opened up new avenues for addressing the molecular and cellular basis of dendritic remodeling. In this review, we summarize recent progress in understanding the cellular and molecular mechanisms of dendritic remodeling by mainly focusing on a class of Drosophila PNS neurons, where major advances in knowledge have been made. The article begins with a brief overview of PNS circuit remodeling during Drosophila metamorphosis. This is followed by a detailed account of genetic dissection of dendritic remodeling in the Drosophila PNS neurons. We also mention recent investigations using another invertebrate model system, Caenorhabditis elegans sensory neurons. We suggest that genetic studies using invertebrate model systems better enable us to gain molecular insights into dendrite remodeling. Because of space limitations, we do not review the extensive work that has been done on structural remodeling of Drosophila CNS neurons and dendritic spines in the mammalian brain, but readers are referred to recent excellent reviews in these areas (Alvarez and Sabatini, 2007; Chen and Nedivi, 2010; Emoto, 2011; Luo and O'Leary, 2005; Yu and Schuldiner, 2014; Yu and Zuo, 2011).

2. Dendritic Changes during Transition from Larval to Adult Circuits in Fly Peripheral Nervous System

The PNS neurons of Drosophila larvae are an excellent model to study dendrites (Emoto, 2012; Parrish et al., 2007). In each hemisegment, 15 dendritic arborization (da) neurons elaborate stereotypic dendritic branches underneath the epidermal tissue. The da neurons are classified into four classes, class I, II, III, and IV, according to the complexity of dendritic morphology. Each class of da neurons, expressing different sets of genes including those of ion channels, can sense different external stimuli: for example, class III da (C3da) neurons express a transient receptor potential (TRP) channel NompC, which confers the ability to sense gentle touch (Yan et al., 2013); and class IV da (C4da) neurons sense noxious mechanical, heat, and light stimuli, which are converted into neural signals by the degenerin/epithelial sodium channel (DEG/ENaC) family Pickpocket (for mechanical), the newly discovered mechanosensory ion channel Piezo (for mechanical), and the TRP channel TrpA1(for heat and light) (Kim et al., 2012; Zhong et al., 2010, 2012). By taking advantage of the class-specific gene expression, several transgenic reporter lines were developed to label a specific class of da neurons with single dendrite resolution in vivo.

Live imaging studies using the reporter lines have revealed that during metamorphosis from larva to pupa and adult, dendrites of larval da neurons remodel dynamically to develop the adult PNS. The remodeling process of da neuron dendrites can be divided into three phases: destructive, latent, and regenerating phases (Figure 1). The first destructive phase is within 16–20 h after puparium formation (APF). During this phase, ddaB class II da (C2da) and ddaA C3da neurons undergo programmed cell death within ∼10 h APF. In contrast, ddaD/ddaE class I da (C1da) and ddaC C4da neurons remain alive and prune their dendritic arbor completely away, while their axons and cell bodies remain intact (Williams and Truman, 2005). Dendrite pruning of both classes of da neurons is mediated by local degeneration rather than retraction of branches (Williams and Truman, 2004, 2005). After the completion of dendrite pruning, da neurons stay “dormant” without net regrowth of dendritic branches (the latent phase). The length of this phase differs between da neurons: until ∼42 and ∼72 h APF for ddaE C1da and ddaC C4da neurons, respectively (Lyons et al., 2014; Williams and Truman, 2004). Finally, during the regenerating phase, da neurons regenerate their dendritic branches through the rest of metamorphosis and are incorporated into the adult PNS circuits (Kuo et al., 2005; Lyons et al., 2014; Satoh et al., 2012; Shimono et al., 2009; Williams and Truman, 2004). Hereafter, we mainly focus on dendritic remodeling of ddaC C4da neurons, whose dendrites undergo pruning and regeneration during metamorphosis (Figure 1), and review recently revealed molecular mechanisms underlying these processes.

Figure 1 Dendritic remodeling of Drosophila C4da sensory neurons.

Dendritic branches of larval neurons (upper left) remodel during metamorphosis to form adult specific dendrites (upper right). Dendrite remodeling is divided into three phases: destructive, latent, and regenerating phases (bottom). During the destructive phase, dendritic branches are pruned away by local degeneration while axons and soma remain intact (green (gray in print versions)). After a latency of ∼72 h, pupal neurons start to regenerate dendritic branches.

3. Pruning of Larval...

Produkt-Details

• Erscheint lt. Verlag: 25.8.2015
• Sprache: englisch
• Themenwelt: Naturwissenschaften ► Biologie ► Genetik / Molekularbiologie
• Themenwelt: Naturwissenschaften ► Biologie ► Zellbiologie
• Themenwelt: Technik
• ISBN-10: 0-12-802477-1 / 0128024771
• ISBN-13: 978-0-12-802477-5 / 9780128024775