Abstract
Increasing evidence during the past two decades shows that cells interconnect and communicate through cytonemes. These cytoskeleton-driven extensions of specialized membrane territories are involved in cell–cell signaling in development, patterning, and differentiation, but also in the maintenance of adult tissue homeostasis, tissue regeneration, and cancer. Brain tumor cells in glioblastoma extend ultralong membrane protrusions (named tumor microtubes, TMs), which contribute to invasion, proliferation, radioresistance, and tumor progression. Here we review the mechanisms underlying cytoneme formation, regulation, and their roles in cell signaling and communication in epithelial cells and other cell types. Furthermore, we discuss the recent discovery of glial cytonemes in the Drosophila glial cells that alter Wingless (Wg)/Frizzled (Fz) signaling between glia and neurons. Research on cytoneme formation, maintenance, and cell signaling mechanisms will help to better understand not only physiological developmental processes and tissue homeostasis but also cancer progression.
Highlights
Filopodia are long, thin, finger-like, actin-rich plasma-membrane protrusions that function as tentacles for cells to explore their local environment
Filopodia sense the extracellular environment at their tips using cell surface receptors, and they have been given different names usually according to their size or functions: microspikes [3], thin filopodia [4], thick filopodia [5], gliopodia [6], myopodia [7], growth cone filopodia, and dendritic spines involved in synapse formation [8] and in neuronal targeting and pathfinding [9], invadopodia [10], podosomes [11,12], antigen presentation by dendritic cells of the immune system [13], telopodes [14], pseudopods, tunneling nanotubes [15], and cytonemes [16]
This study showed that Hh gradient correlates with cytonemes formation, and mutations affecting cytoneme formation disrupt the Hh gradient [23]
Summary
Thin, finger-like, actin-rich plasma-membrane protrusions that function as tentacles for cells to explore their local environment. Drosophila melanogaster, cytonemes were initially found in wing and eye imaginal discs [16] and later in ovaries [28], trachea [29,30], and lymph glands [31] They have been described in other organisms, such as earthworms [32], earwig ovaries [33], spider embryos [34], in Rhodnius and Calpodes [35], and in several mammalian cell types including retroviral-infected cells [36], mast cells [37], B-lymphocytes [38], and neutrophils [39]. We will review the physiological role of cytonemes during development in different tissues and the role of cytonemes in tumorigenesis, focusing mainly on the Drosophila model organism
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