The Immunoglobulin Superfamily Member Basigin Is Required for Complex Dendrite Formation in Drosophila

Brikha R Shrestha,Wesley B Grueber,Anita Burgos

doi:10.3389/fncel.2021.739741

Abstract

Coordination of dendrite growth with changes in the surrounding substrate occurs widely in the nervous system and is vital for establishing and maintaining neural circuits. However, the molecular basis of this important developmental process remains poorly understood. To identify potential mediators of neuron-substrate interactions important for dendrite morphogenesis, we undertook an expression pattern-based screen in Drosophila larvae, which revealed many proteins with expression in dendritic arborization (da) sensory neurons and in neurons and their epidermal substrate. We found that reporters for Basigin, a cell surface molecule of the immunoglobulin (Ig) superfamily previously implicated in cell-cell and cell-substrate interactions, are expressed in da sensory neurons and epidermis. Loss of Basigin in da neurons led to defects in morphogenesis of the complex dendrites of class IV da neurons. Classes of sensory neurons with simpler branching patterns were unaffected by loss of Basigin. Structure-function analyses showed that a juxtamembrane KRR motif is critical for this function. Furthermore, knock down of Basigin in the epidermis led to defects in dendrite elaboration of class IV neurons, suggesting a non-autonomous role. Together, our findings support a role for Basigin in complex dendrite morphogenesis and interactions between dendrites and the adjacent epidermis.

Highlights

Morphogenesis of neuronal dendritic arbors influences neuronal connectivity and functional specialization and is a critical step in nervous system development
Following an expression pattern-based screen of publicly available proteintrap lines (Kelso et al, 2004; Buszczak et al, 2007), we focused on Basigin, an immunoglobulin (Ig) superfamily (IgSF) member and mediator of extracellular matrix (ECM) remodeling in vertebrates
To identify genes involved in dendrite morphogenesis, we examined the expression patterns of >250 genes in third instar Drosophila larvae using protein trap insertion lines generated previously (Morin et al, 2001; Buszczak et al, 2007; QuiñonesCoello et al, 2007)

Summary

Introduction

Morphogenesis of neuronal dendritic arbors influences neuronal connectivity and functional specialization and is a critical step in nervous system development. Neurons have complex cell-intrinsic molecular programs that regulate dendrite patterning and may be influenced by extrinsic factors (Corty et al, 2009; Dong et al, 2015). Basigin Regulates Dendrite Morphogenesis spaces between neurons house a complex mélange of molecules secreted by diverse cell types that provide physical support as well as important developmental cues to neurons. In a growing nervous system, this rich extracellular molecular environment and the cellular substrates with which neurons interact change continuously in physical size and molecular profiles. Proper formation and subsequent maintenance or refinement of dendritic arbors must involve precise coordination of arbor morphogenesis with such changes in the cellular/molecular substratum of neurons. Given the tremendous diversities of neuronal subtypes and their substrate environments across the nervous system, the mechanisms underlying such coordinative processes are likely very complex

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Conclusion