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Cerebral Cortex Advance Access originally published online on December 20, 2006
Cerebral Cortex 2007 17(10):2312-2321; doi:10.1093/cercor/bhl140
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© The Author 2006. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Increased Cortical Expression of Two Synaptogenic Thrombospondins in Human Brain Evolution

Mario Cáceres1,2,4, Carolyn Suwyn1, Marcelia Maddox1, James W. Thomas2 and Todd M. Preuss1,3

1 Division of Neuroscience and Center for Behavioral Neuroscience, Yerkes National Primate Research Center, Emory University, 954 Gatewood Road, Atlanta, GA 30329, USA, 2 Department of Human Genetics, Emory University School of Medicine, 615 Michael Street, Atlanta, GA 30322, USA, 3 Department of Pathology and Laboratory Medicine, Emory University School of Medicine, 1364 Clifton Road, Atlanta, GA 30322, USA, 4 Present address: Genes and Disease Program, Center for Genomic Regulation (CRG-UPF), Barcelona Biomedical Research Park, Dr. Aiguader 88, 08003 Barcelona, Spain

Address correspondence to Mario Cáceres, Genes and Disease Program, Center for Genomic Regulation, Dr. Aiguader, 88 08003 Barcelona, Spain. Email: mario.caceres{at}crg.es.

Thrombospondins are extracellular-matrix glycoproteins implicated in the control of synaptogenesis and neurite growth. Previous microarray studies suggested that one gene of this family, thrombospondin 4 (THBS4), was upregulated during human brain evolution. Using independent techniques to examine thrombospondin expression patterns in adult brain samples, we report ~6-fold and ~2-fold greater expression of THBS4 and THBS2 messenger RNA (mRNA), respectively, in human cerebral cortex compared with chimpanzees and macaques, with corresponding differences in protein levels. In humans and chimpanzees, thrombospondin expression differences were observed in the forebrain (cortex and caudate), whereas the cerebellum and most nonbrain tissues exhibited similar levels of the 2 mRNAs. Histological examination revealed THBS4 mRNA and protein expression in numerous pyramidal and glial cells in the 3 species but humans also exhibited very prominent immunostaining of the synapse-rich cortical neuropil. In humans, additionally, THBS4 antibodies labeled ß-amyloid containing plaques in Alzheimer's cases and some control cases. This is the first detailed characterization of gene-expression changes in human evolution that involve specific brain regions, including portions of cerebral cortex. Increased expression of thrombospondins in human brain evolution could result in changes in synaptic organization and plasticity, and contribute to the distinctive cognitive abilities of humans, as well as to our unique vulnerability to neurodegenerative disease.

Key Words: gene expression • human evolution • neuroanatomy • plasticity • primates • synaptogenesis


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