Literature DB >> 25122892

Human and monkey striatal interneurons are derived from the medial ganglionic eminence but not from the adult subventricular zone.

Congmin Wang1, Yan You2, Dashi Qi3, Xing Zhou2, Lei Wang4, Song Wei2, Zhuangzhi Zhang2, Weixi Huang2, Zhidong Liu2, Fang Liu2, Lan Ma2, Zhengang Yang5.   

Abstract

In adult rodent and monkey brains, newly born neurons in the subventricular zone (SVZ) in the wall of the lateral ventricle migrate into the olfactory bulb (OB) via the rostral migratory stream (RMS). A recent study reported that interneurons are constantly generating in the adult human striatum from the SVZ. In contrast, by taking advantage of the continuous expression of Sp8 from the neuroblast stage through differentiation into mature interneurons, we found that the adult human SVZ does not generate new interneurons for the striatum. In the adult human SVZ and RMS, very few neuroblasts were observed, and most of them expressed the transcription factor Sp8. Neuroblasts in the adult rhesus monkey SVZ-RMS-OB pathway also expressed Sp8. In addition, we observed that Sp8 was expressed by most adult human and monkey OB interneurons. However, very few Sp8+ cells were in the adult human striatum. This suggests that neuroblasts in the adult human SVZ and RMS are likely destined for the OB, but not for the striatum. BrdU-labeling results also revealed few if any newly born neurons in the adult rhesus monkey striatum. Finally, on the basis of transcription factor expression, we provide strong evidence that the vast majority of interneurons in the human and monkey striatum are generated from the medial ganglionic eminence during embryonic developmental stages, as they are in rodents. We conclude that, although a small number of neuroblasts exist in the adult human SVZ, they do not migrate into the striatum and become mature striatal interneurons.
Copyright © 2014 the authors 0270-6474/14/3410906-18$15.00/0.

Entities:  

Keywords:  SVZ; Sp8; human; interneurons; neurogenesis; striatum

Mesh:

Year:  2014        PMID: 25122892      PMCID: PMC6705263          DOI: 10.1523/JNEUROSCI.1758-14.2014

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  58 in total

1.  Subventricular zone astrocytes are neural stem cells in the adult mammalian brain.

Authors:  F Doetsch; I Caillé; D A Lim; J M García-Verdugo; A Alvarez-Buylla
Journal:  Cell       Date:  1999-06-11       Impact factor: 41.582

2.  The generation, migration, and differentiation of olfactory neurons in the adult primate brain.

Authors:  D R Kornack; P Rakic
Journal:  Proc Natl Acad Sci U S A       Date:  2001-04-10       Impact factor: 11.205

3.  Genesis of the primate neostriatum: [3H]thymidine autoradiographic analysis of the time of neuron origin in the rhesus monkey.

Authors:  S Brand; P Rakic
Journal:  Neuroscience       Date:  1979       Impact factor: 3.590

4.  Origin and molecular specification of striatal interneurons.

Authors:  O Marin; S A Anderson; J L Rubenstein
Journal:  J Neurosci       Date:  2000-08-15       Impact factor: 6.167

5.  Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain.

Authors:  V Pencea; K D Bingaman; L J Freedman; M B Luskin
Journal:  Exp Neurol       Date:  2001-11       Impact factor: 5.330

6.  Cell proliferation without neurogenesis in adult primate neocortex.

Authors:  D R Kornack; P Rakic
Journal:  Science       Date:  2001-12-07       Impact factor: 47.728

7.  Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain.

Authors:  A Benraiss; E Chmielnicki; K Lerner; D Roh; S A Goldman
Journal:  J Neurosci       Date:  2001-09-01       Impact factor: 6.167

Review 8.  Chemical anatomy of striatal interneurons in normal individuals and in patients with Huntington's disease.

Authors:  F Cicchetti; L Prensa; Y Wu; A Parent
Journal:  Brain Res Brain Res Rev       Date:  2000-11

9.  Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum.

Authors:  L Sussel; O Marin; S Kimura; J L Rubenstein
Journal:  Development       Date:  1999-08       Impact factor: 6.868

10.  In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain.

Authors:  H Wichterle; D H Turnbull; S Nery; G Fishell; A Alvarez-Buylla
Journal:  Development       Date:  2001-10       Impact factor: 6.868

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  31 in total

Review 1.  New neurons in the adult striatum: from rodents to humans.

Authors:  Dragos Inta; Heather A Cameron; Peter Gass
Journal:  Trends Neurosci       Date:  2015-08-20       Impact factor: 13.837

2.  Characterization of the ventricular-subventricular stem cell niche during human brain development.

Authors:  Amanda M Coletti; Deepinder Singh; Saurabh Kumar; Tasnuva Nuhat Shafin; Patrick J Briody; Benjamin F Babbitt; Derek Pan; Emily S Norton; Eliot C Brown; Kristopher T Kahle; Marc R Del Bigio; Joanne C Conover
Journal:  Development       Date:  2018-10-26       Impact factor: 6.868

Review 3.  The Adult Ventricular-Subventricular Zone (V-SVZ) and Olfactory Bulb (OB) Neurogenesis.

Authors:  Daniel A Lim; Arturo Alvarez-Buylla
Journal:  Cold Spring Harb Perspect Biol       Date:  2016-05-02       Impact factor: 10.005

4.  Transcription Factors Sp8 and Sp9 Coordinately Regulate Olfactory Bulb Interneuron Development.

Authors:  Jiwen Li; Chunyang Wang; Zhuangzhi Zhang; Yan Wen; Lei An; Qifei Liang; Zhejun Xu; Song Wei; Weiwei Li; Teng Guo; Guoping Liu; Guangxu Tao; Yan You; Heng Du; Zhuoning Fu; Miao He; Bin Chen; Kenneth Campbell; Arturo Alvarez-Buylla; John L Rubenstein; Zhengang Yang
Journal:  Cereb Cortex       Date:  2018-09-01       Impact factor: 5.357

5.  Sp9 Regulates Medial Ganglionic Eminence-Derived Cortical Interneuron Development.

Authors:  Zhidong Liu; Zhuangzhi Zhang; Susan Lindtner; Zhenmeiyu Li; Zhejun Xu; Song Wei; Qifei Liang; Yan Wen; Guangxu Tao; Yan You; Bin Chen; Yanling Wang; John L Rubenstein; Zhengang Yang
Journal:  Cereb Cortex       Date:  2019-06-01       Impact factor: 5.357

6.  Positive Controls in Adults and Children Support That Very Few, If Any, New Neurons Are Born in the Adult Human Hippocampus.

Authors:  Shawn F Sorrells; Mercedes F Paredes; Zhuangzhi Zhang; Gugene Kang; Oier Pastor-Alonso; Sean Biagiotti; Chloe E Page; Kadellyn Sandoval; Anthony Knox; Andrew Connolly; Eric J Huang; Jose Manuel Garcia-Verdugo; Michael C Oldham; Zhengang Yang; Arturo Alvarez-Buylla
Journal:  J Neurosci       Date:  2021-03-24       Impact factor: 6.167

7.  The Zinc Finger Transcription Factor Sp9 Is Required for the Development of Striatopallidal Projection Neurons.

Authors:  Qiangqiang Zhang; Yue Zhang; Chunyang Wang; Zhejun Xu; Qifei Liang; Lei An; Jiwen Li; Zhidong Liu; Yan You; Miao He; Ying Mao; Bin Chen; Zhi-Qi Xiong; John L Rubenstein; Zhengang Yang
Journal:  Cell Rep       Date:  2016-07-21       Impact factor: 9.423

Review 8.  Brain size and limits to adult neurogenesis.

Authors:  Mercedes F Paredes; Shawn F Sorrells; Jose M Garcia-Verdugo; Arturo Alvarez-Buylla
Journal:  J Comp Neurol       Date:  2015-09-28       Impact factor: 3.215

9.  CTCF Governs the Identity and Migration of MGE-Derived Cortical Interneurons.

Authors:  Adrienne Elbert; Daniel Vogt; Ashley Watson; Michael Levy; Yan Jiang; Emilie Brûlé; Megan E Rowland; John Rubenstein; Nathalie G Bérubé
Journal:  J Neurosci       Date:  2018-10-30       Impact factor: 6.167

Review 10.  Adult neural stem cells stake their ground.

Authors:  Daniel A Lim; Arturo Alvarez-Buylla
Journal:  Trends Neurosci       Date:  2014-09-12       Impact factor: 13.837

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