Characterizing progenitor cells in developing and injured spinal cord: Insights from single-nucleus transcriptomics and lineage tracing

Q Qi Zhang X Xianming Wu (State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) Y Yongheng Fan (State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) H Haipeng Zhang (State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) M Man Yin (State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) X Xiaoyu Xue Y Yanyun Yin (State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) C Chen Jin (State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) R Rui Quan (State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) P Peipei Jiang (Department of Obstetrics and Gynecology, The Affiliated Drum Tower Hospital of Nanjing University Medical School) Y Yongguang Liu (Department of Organ Transplantation, Zhujiang Hospital, Southern Medical University) C Cheng Yu (Department of Spinal Surgery, Zhujiang Hospital, Southern Medical University) W Wenhao Kuang (Department of Spinal Surgery, Zhujiang Hospital, Southern Medical University) B Bing Chen J Jiayin Li (State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) Z Zhong Chen Y Yali Hu (Department of Obstetrics and Gynecology, The Affiliated Drum Tower Hospital of Nanjing University Medical School) Z Zhifeng Xiao (State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) Y Yannan Zhao (State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) J Jianwu Dai (State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences)

Abstract

Various mature tissue-resident cells exhibit progenitor characteristics following injury. However, the existence of endogenous stem cells with multiple lineage potentials in the adult spinal cord remains a compelling area of research. In this study, we present a cross-species investigation that extends from development to injury. We used single-nucleus transcriptomic sequencing and genetic lineage tracing to characterize neural cells in the spinal cord. Our findings show that ciliated ependymal cells lose neural progenitor gene signatures and proliferation ability following the differentiation of NPCs within the ventricular zone. By combining single-nucleus transcriptome datasets from the rhesus macaque spinal cord injury (SCI) model with developmental human spinal cord datasets, we revealed that ciliated ependymal cells respond minimally to injury and cannot revert to a developmental progenitor state. Intriguingly, we observed astrocytes transdifferentiating into mature oligodendrocytes postinjury through lineage tracing experiments. Further analysis identifies an intermediate-state glial cell population expressing both astrocyte and oligodendrocyte feature genes in adult spinal cords. The transition ratio from astrocytes into oligodendrocytes increased after remodeling injury microenvironment by functional scaffolds. Overall, our results highlight the remarkable multilineage potential of astrocytes in the adult spinal cord.

Article Details

Volume / Issue Vol. 122, Issue 2
Published January 14, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (20)

Q

Qi Zhang

X

Xianming Wu

State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

Y

Yongheng Fan

State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

H

Haipeng Zhang

State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

M

Man Yin

State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

X

Xiaoyu Xue

Y

Yanyun Yin

State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

C

Chen Jin

State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

R

Rui Quan

State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

P

Peipei Jiang

Department of Obstetrics and Gynecology, The Affiliated Drum Tower Hospital of Nanjing University Medical School

Y

Yongguang Liu

Department of Organ Transplantation, Zhujiang Hospital, Southern Medical University

C

Cheng Yu

Department of Spinal Surgery, Zhujiang Hospital, Southern Medical University

W

Wenhao Kuang

Department of Spinal Surgery, Zhujiang Hospital, Southern Medical University

B

Bing Chen

J

Jiayin Li

State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

Z

Zhong Chen

Y

Yali Hu

Department of Obstetrics and Gynecology, The Affiliated Drum Tower Hospital of Nanjing University Medical School

Z

Zhifeng Xiao

State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

Y

Yannan Zhao

State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

J

Jianwu Dai

State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences