Cortical Interlaminar Astrocytes Are Generated Prenatally, Mature Postnatally, and Express Unique Markers in Human and Nonhuman Primates

Author:

Falcone Carmen12ORCID,Penna Elisa34ORCID,Hong Tiffany12,Tarantal Alice F5,Hof Patrick R6,Hopkins William D7,Sherwood Chet C8,Noctor Stephen C34,Martínez-Cerdeño Verónica123

Affiliation:

1. Department of Pathology and Laboratory Medicine, UC Davis School of Medicine, Sacramento, CA 95817, USA

2. Institute for Pediatric Regenerative Medicine, and Shriners Hospitals, Sacramento, CA 95817, USA

3. MIND Institute, UC Davis School of Medicine, Sacramento, CA 95817, USA

4. Department of Psychiatry and Behavioral Sciences, UC Davis School of Medicine, Sacramento, CA 95817, USA

5. Departments of Pediatrics and Cell Biology and Human Anatomy, and California National Primate Research Center, University of California, Davis, CA 95616, USA

6. Nash Family Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA

7. Department of Comparative Medicine, Keeling Center for Comparative Medicine and Research, The University of Texas MD Anderson Cancer Center, Bastrop, TX 78602, USA

8. Department of Anthropology and Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC 20052, USA

Abstract

Abstract Interlaminar astrocytes (ILAs) are a subset of cortical astrocytes that reside in layer I, express GFAP, have a soma contacting the pia, and contain long interlaminar processes that extend through several cortical layers. We studied the prenatal and postnatal development of ILAs in three species of primates (rhesus macaque, chimpanzee, and human). We found that ILAs are generated prenatally likely from radial glial (RG) cells, that ILAs proliferate locally during gestation, and that ILAs extend interlaminar processes during postnatal stages of development. We showed that the density and morphological complexity of ILAs increase with age, and that ILAs express multiple markers that are expressed by RG cells (Pax6, Sox2, and Nestin), specific to inner and outer RG cells (Cryab and Hopx), and astrocyte markers (S100β, Aqp4, and GLAST) in prenatal stages and in adult. Finally, we demonstrated that rudimentary ILAs in mouse also express the RG markers Pax6, Sox2, and Nestin, but do not express S100β, Cryab, or Hopx, and that the density and morphological complexity of ILAs differ between primate species and mouse. Together these findings contribute new information on astrogenesis of this unique class of cells and suggest a lineal relationship between RG cells and ILAs.

Funder

National Science Foundation

National Institute of Mental Health

National Institutes of Health

National Heart, Lung, and Blood Institute

California National Primate Research Center

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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