title: In vivo time-lapse imaging reveals extensive neural crest and endothelial cell interactions during neural crest migration and formation of the dorsal root and sympathetic ganglia.
abstract: During amniote embryogenesis the nervous and vascular systems interact in a process that significantly affects the respective morphogenesis of each network by forming a "neurovascular" link. The importance of neurovascular cross-talk in the central nervous system has recently come into focus with the growing awareness that these two systems interact extensively both during development, in the stem-cell niche, and in neurodegenerative conditions such as Alzheimer's Disease and Amyotrophic Lateral Sclerosis. With respect to the peripheral nervous system, however, there have been no live, real-time investigations of the potential relationship between these two developing systems. To address this deficit, we used multispectral 4D time-lapse imaging in a transgenic quail model in which endothelial cells (ECs) express a yellow fluorescent marker, while neural crest cells (NCCs) express an electroporated red fluorescent marker. We monitored EC and NCC migration in real-time during formation of the peripheral nervous system. Our time-lapse recordings indicate that NCCs and ECs are physically juxtaposed and dynamically interact at multiple locations along their trajectories. These interactions are stereotypical and occur at precise anatomical locations along the NCC migratory pathway. NCCs migrate alongside the posterior surface of developing intersomitic vessels, but fail to cross these continuous streams of motile ECs. NCCs change their morphology and migration trajectory when they encounter gaps in the developing vasculature. Within the nascent dorsal root ganglion, proximity to ECs causes filopodial retraction which curtails forward persistence of NCC motility. Overall, our time-lapse recordings support the conclusion that primary vascular networks substantially influence the distribution and migratory behavior of NCCs and the patterned formation of dorsal root and sympathetic ganglia.
authors.affiliation: Department of Cell Biology and Neuroscience, Montana State University, Bozeman, MT 59717, United States; Department of Biological and Physical Sciences, Montana State University Billings, Billings, MT 59101, United States. Electronic address: lynn.george@msubillings.edu.
authors.forename: Lynn
authors.initials: L
authors.lastname: George
authors.affiliation: Department of Cell Biology and Neuroscience, Montana State University, Bozeman, MT 59717, United States.
authors.forename: Haley
authors.initials: H
authors.lastname: Dunkel
authors.affiliation: Department of Cell Biology and Neuroscience, Montana State University, Bozeman, MT 59717, United States.
authors.forename: Barbara J
authors.initials: BJ
authors.lastname: Hunnicutt
authors.affiliation: University of Kansas Medical Center, Kansas City, KS 66160, United States.
authors.forename: Michael
authors.initials: M
authors.lastname: Filla
authors.affiliation: University of Kansas Medical Center, Kansas City, KS 66160, United States.
authors.forename: Charles
authors.initials: C
authors.lastname: Little
authors.affiliation: Department of Radiology and Developmental Neuroscience Program, Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, United States; Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, United States.
authors.forename: Rusty
authors.initials: R
authors.lastname: Lansford
authors.affiliation: Department of Cell Biology and Neuroscience, Montana State University, Bozeman, MT 59717, United States.
authors.forename: Frances
authors.initials: F
authors.lastname: Lefcort
mesh_terms: D000544:Alzheimer Disease / Q000378:metabolism; D000690:Amyotrophic Lateral Sclerosis / Q000378:metabolism; D000818:Animals; D030801:Animals, Genetically Modified; D001426:Bacterial Proteins / Q000378:metabolism; D019521:Body Patterning; D002450:Cell Communication; D002465:Cell Movement; D003370:Coturnix; D042783:Endothelial Cells / Q000166:cytology*; D005727:Ganglia, Spinal / Q000166:cytology / Q000196:embryology*; D018507:Gene Expression Regulation, Developmental; D007150:Immunohistochemistry; D008164:Luminescent Proteins / Q000378:metabolism; D008853:Microscopy / Q000379:methods*; D009432:Neural Crest / Q000166:cytology / Q000196:embryology*; D017933:Peripheral Nervous System / Q000196:embryology*; D013234:Stem Cells / Q000166:cytology; D013564:Sympathetic Nervous System / Q000196:embryology*; D059008:Time-Lapse Imaging / Q000379:methods*
chemical_list: D001426:Bacterial Proteins; D008164:Luminescent Proteins; C054562:yellow fluorescent protein, Bacteria
keywords: Endothelial cells; Neural crest migration; Neurovascular; Peripheral nervous system