Species-specific maturation profiles of human, chimpanzee and bonobo neural cells

Author:

Marchetto Maria C1ORCID,Hrvoj-Mihic Branka2,Kerman Bilal E3ORCID,Yu Diana X4,Vadodaria Krishna C1,Linker Sara B1,Narvaiza Iñigo1,Santos Renata15ORCID,Denli Ahmet M1,Mendes Ana PD1,Oefner Ruth1,Cook Jonathan1,McHenry Lauren1,Grasmick Jaeson M1,Heard Kelly1,Fredlender Callie1,Randolph-Moore Lynne1,Kshirsagar Rijul1,Xenitopoulos Rea1,Chou Grace1,Hah Nasun1,Muotri Alysson R67,Padmanabhan Krishnan8,Semendeferi Katerina29,Gage Fred H1ORCID

Affiliation:

1. Laboratory of Genetics, The Salk Institute for Biological Studies, La Jolla, United States

2. Department of Anthropology, University of California, San Diego, La Jolla, United States

3. Regenerative and Restorative Medicine Research Center (REMER), Istanbul Medipol University, Istanbul, Turkey

4. Department of Oncological Sciences, Huntsman Cancer Institute, Salt Lake City, United States

5. Laboratory of Dynamic of Neuronal Structure in Health and Disease, Institute of Psychiatry and Neuroscience of Paris (UMR S894 INSERM, University Paris Descartes), Paris, France

6. Department of Pediatrics, University of California, San Diego School of Medicine, La Jolla, United States

7. Department of Cellular & Molecular Medicine, Rady Children's Hospital San Diego, La Jolla, United States

8. Department of Neuroscience, University of Rochester School of Medicine and Dentistry, Rochester, United States

9. Neuroscience Graduate Program, University of California San Diego, La Jolla, United States

Abstract

Comparative analyses of neuronal phenotypes in closely related species can shed light on neuronal changes occurring during evolution. The study of post-mortem brains of nonhuman primates (NHPs) has been limited and often does not recapitulate important species-specific developmental hallmarks. We utilize induced pluripotent stem cell (iPSC) technology to investigate the development of cortical pyramidal neurons following migration and maturation of cells grafted in the developing mouse cortex. Our results show differential migration patterns in human neural progenitor cells compared to those of chimpanzees and bonobos both in vitro and in vivo, suggesting heterochronic changes in human neurons. The strategy proposed here lays the groundwork for further comparative analyses between humans and NHPs and opens new avenues for understanding the differences in the neural underpinnings of cognition and neurological disease susceptibility between species.

Funder

National Institutes of Health

California Institute for Regenerative Medicine

National Alliance for Research on Schizophrenia and Depression

Leona M. and Harry B. Helmsley Charitable Trust

Salk Cancer Center

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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