Host brain environmental influences on transplanted medial ganglionic eminence progenitors.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
13 Feb 2024
13 Feb 2024
Historique:
received:
06
07
2023
accepted:
19
01
2024
medline:
14
2
2024
pubmed:
14
2
2024
entrez:
13
2
2024
Statut:
epublish
Résumé
Interneuron progenitor transplantation can ameliorate disease symptoms in a variety of neurological disorders. The strategy is based on transplantation of embryonic medial ganglionic eminence (MGE) progenitors. Elucidating how host brain environment influences the integration of interneuron progenitors is critical for optimizing this strategy across different disease states. Here, we systematically evaluated the influence of age and brain region on survival, migration, and differentiation of transplant-derived cells. We find that early postnatal MGE transplantation yields superior survival and more extensive migratory capabilities compared to transplantation during the juvenile or adult stages. MGE progenitors migrate more widely in the cortex compared to the hippocampus. Maturation to interneuron subtypes is regulated by age and brain region. MGE progenitors transplanted into the dentate gyrus sub-region of the early postnatal hippocampus can differentiate into astrocytes. Our results suggest that the host brain environment critically regulates survival, spatial distribution, and maturation of MGE-derived interneurons following transplantation. These findings inform and enable optimal conditions for interneuron transplant therapies.
Identifiants
pubmed: 38351191
doi: 10.1038/s41598-024-52478-6
pii: 10.1038/s41598-024-52478-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3610Subventions
Organisme : NIH/NINDS
ID : R01NS-071785-14
Informations de copyright
© 2024. The Author(s).
Références
Sohal, V. S. & Rubenstein, J. L. R. Excitation-inhibition balance as a framework for investigating mechanisms in neuropsychiatric disorders. Mol. Psychiatry 24, 1248–1257 (2019).
pubmed: 31089192
pmcid: 6742424
doi: 10.1038/s41380-019-0426-0
Dienel, S. J. & Lewis, D. A. Alterations in cortical interneurons and cognitive function in schizophrenia. Neurobiol. Dis. 131, 104208 (2019).
pubmed: 29936230
doi: 10.1016/j.nbd.2018.06.020
Paterno, R., Casalia, M. & Baraban, S. C. Interneuron deficits in neurodevelopmental disorders: Implications for disease pathology and interneuron-based therapies. Eur. J. Paediatr. Neurol. 24, 81–88 (2020).
pubmed: 31870698
doi: 10.1016/j.ejpn.2019.12.015
Xu, Y., Zhao, M., Han, Y. & Zhang, H. GABAergic inhibitory interneuron deficits in Alzheimer’s disease: Implications for treatment. Front. Neurosci. 14, 660 (2020).
pubmed: 32714136
pmcid: 7344222
doi: 10.3389/fnins.2020.00660
Marafiga, J. R., Pasquetti, M. V. & Calcagnotto, M. E. GABAergic interneurons in epilepsy: More than a simple change in inhibition. Epilepsy Behav. 121, 106935 (2021).
doi: 10.1016/j.yebeh.2020.106935
Kato, M. & Dobyns, W. B. X-linked lissencephaly with abnormal genitalia as a tangential migration disorder causing intractable epilepsy: Proposal for a new term, “interneuronopathy”. J. Child Neurol. 20, 392–397 (2005).
pubmed: 15921244
doi: 10.1177/08830738050200042001
Thomas, G. P. & Jobst, B. C. Critical review of the responsive neurostimulator system for epilepsy. Med. Dev. Evid. Res. 8, 405-411 (2015).
Chiken, S. & Nambu, A. Mechanism of deep brain stimulation: Inhibition, excitation, or disruption?. The Neurosci. 22, 313–322 (2016).
Hunt, R. F. & Baraban, S. C. Interneuron transplantation as a treatment for epilepsy. Cold Spring Harb. Perspect. Med. 5, (2015).
Hunt, R. F., Girskis, K. M., Rubenstein, J. L., Alvarez-Buylla, A. & Baraban, S. C. GABA progenitors grafted into the adult epileptic brain control seizures and abnormal behavior. Nat. Neurosci. 16, 692–697 (2013).
pubmed: 23644485
pmcid: 3665733
doi: 10.1038/nn.3392
Martinez-Losa, M. et al. Nav1.1-overexpressing interneuron transplants restore brain rhythms and cognition in a mouse model of Alzheimer’s disease. Neuron 98, 75-89 (2018).
pubmed: 29551491
pmcid: 5886814
doi: 10.1016/j.neuron.2018.02.029
Zhu, B., Eom, J. & Hunt, R. F. Transplanted interneurons improve memory precision after traumatic brain injury. Nat. Commun. 10, 5156 (2019).
pubmed: 31727894
pmcid: 6856380
doi: 10.1038/s41467-019-13170-w
Tong, L. M. et al. Inhibitory interneuron progenitor transplantation restores normal learning and memory in ApoE4 knock-in mice without or with Aβ accumulation. J. Neurosci. 34, 9506–9515 (2014).
pubmed: 25031394
pmcid: 4099537
doi: 10.1523/JNEUROSCI.0693-14.2014
Wichterle, H., Garcia-Verdugo, J. M., Herrera, D. G. & Alvarez-Buylla, A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat. Neurosci. 2, 461–466 (1999).
pubmed: 10321251
doi: 10.1038/8131
Xu, Q., Cobos, I., De La Cruz, E., Rubenstein, J. L. & Anderson, S. A. Origins of cortical interneuron subtypes. J. Neurosci. 24, 2612–2622 (2004).
pubmed: 15028753
pmcid: 6729522
doi: 10.1523/JNEUROSCI.5667-03.2004
Lim, L., Mi, D., Llorca, A. & Marín, O. Development and functional diversification of cortical interneurons. Neuron 100, 294–313 (2018).
pubmed: 30359598
pmcid: 6290988
doi: 10.1016/j.neuron.2018.10.009
Williams, R. H. & Riedemann, T. Development, diversity, and death of MGE-derived cortical interneurons. Int. J. Mol. Sci. 22, 9297 (2021).
pubmed: 34502208
pmcid: 8430628
doi: 10.3390/ijms22179297
Alvarez-Dolado, M. et al.. Cortical inhibition modified by embryonic neural precursors grafted into the postnatal brain. J. Neurosci. 26, 7380–7389 (2006).
pubmed: 16837585
pmcid: 1550786
doi: 10.1523/JNEUROSCI.1540-06.2006
Howard, M. A. & Baraban, S. C. Synaptic integration of transplanted interneuron progenitor cells into native cortical networks. J. Neurophysiol. 116, 472–478 (2016).
pubmed: 27226453
pmcid: 4978788
doi: 10.1152/jn.00321.2016
Hsieh, J.-Y. & Baraban, S. C. Medial ganglionic eminence progenitors transplanted into hippocampus integrate in a functional and subtype-appropriate manner. eneuro 4 (2017).
Baraban, S. C. et al.. Reduction of seizures by transplantation of cortical GABAergic interneuron precursors into Kv1.1 mutant mice. Proc. Natl. Acad. Sci. 106, 15472–15477 (2009).
pubmed: 19706400
pmcid: 2741275
doi: 10.1073/pnas.0900141106
Martínez-Cerdeño, V. et al. Embryonic MGE precursor cells grafted into adult rat striatum integrate and ameliorate motor symptoms in 6-OHDA-lesioned rats. Cell Stem Cell 6, 238–250 (2010).
pubmed: 20207227
pmcid: 4075336
doi: 10.1016/j.stem.2010.01.004
Casalia, M. L., Howard, M. A. & Baraban, S. C. Persistent seizure control in epileptic mice transplanted with gamma-aminobutyric acid progenitors. Ann. Neurol. 82, 530–542 (2017).
pubmed: 28833459
pmcid: 5771437
doi: 10.1002/ana.25021
Bráz, J. M., Wang, X., Guan, Z. & Basbaum, A. I. Transplant-mediated enhancement of spinal cord GABAergic inhibition reverses paclitaxel-induced mechanical and heat hypersensitivity. Pain 156, 1084–1091 (2015).
pubmed: 25760475
pmcid: 4431911
doi: 10.1097/j.pain.0000000000000152
Perez, S. M. & Lodge, D. J. Hippocampal interneuron transplants reverse aberrant dopamine system function and behavior in a rodent model of schizophrenia. Mol. Psychiatry 18, 1193–1198 (2013).
pubmed: 23979606
pmcid: 4028118
doi: 10.1038/mp.2013.111
Southwell, D. G. et al. Interneuron transplantation rescues social behavior deficits without restoring wild-type physiology in a mouse model of autism with excessive synaptic inhibition. J. Neurosci. 40, 2215–2227 (2020).
pubmed: 31988060
pmcid: 7083289
doi: 10.1523/JNEUROSCI.1063-19.2019
Tanaka, D. H., Toriumi, K., Kubo, K., Nabeshima, T. & Nakajima, K. GABAergic precursor transplantation into the prefrontal cortex prevents phencyclidine-induced cognitive deficits. J. Neurosci. 31, 14116–14125 (2011).
pubmed: 21976496
pmcid: 6623672
doi: 10.1523/JNEUROSCI.2786-11.2011
Rosell-Valle, C. et al.. GABAergic deficits in absence of LPA1 receptor, associated anxiety-like and coping behaviors, and amelioration by interneuron precursor transplants into the dorsal hippocampus. Brain Struct. Funct. 226, 1479–1495 (2021).
pubmed: 33792787
doi: 10.1007/s00429-021-02261-4
Jaiswal, M. K. et al.. Reduction in focal ictal activity following transplantation of MGE interneurons requires expression of the GABA
pubmed: 25914623
pmcid: 4391265
doi: 10.3389/fncel.2015.00127
Sebe, J. Y., Looke-Stewart, E., Dinday, M. T., Alvarez-Buylla, A. & Baraban, S. C. Neocortical integration of transplanted GABA progenitor cells from wild type and GABAB receptor knockout mouse donors. Neurosci. Lett. 561, 52–57 (2014).
pubmed: 24291697
doi: 10.1016/j.neulet.2013.11.012
Davis, M. F. et al.. Inhibitory neuron transplantation into adult visual cortex creates a new critical period that rescues impaired vision. Neuron 86, 1055–1066 (2015).
pubmed: 25937171
pmcid: 4441572
doi: 10.1016/j.neuron.2015.03.062
Priya, R. et al. Vesicular GABA transporter is necessary for transplant-induced critical period plasticity in mouse visual cortex. J. Neurosci. 39, 2635–2648 (2019).
pubmed: 30705101
pmcid: 6445995
doi: 10.1523/JNEUROSCI.1253-18.2019
Daadi, M. M. et al.. Functional engraftment of the medial ganglionic eminence cells in experimental stroke model. Cell Transplant. 18, 815–826 (2009).
pubmed: 19500468
doi: 10.3727/096368909X470829
Mancia Leon, W. R. et al. Clustered gamma-protocadherins regulate cortical interneuron programmed cell death. eLife 9, e55374 (2020).
pubmed: 32633719
pmcid: 7373431
doi: 10.7554/eLife.55374
Pancho, A. et al.. Modifying PCDH19 levels affects cortical interneuron migration. Front. Neurosci. 16, 887478 (2022).
pubmed: 36389226
pmcid: 9642031
doi: 10.3389/fnins.2022.887478
Elbert, A. et al. CTCF governs the identity and migration of MGE-derived cortical interneurons. J. Neurosci. 39, 177–192 (2019).
pubmed: 30377227
pmcid: 6331652
doi: 10.1523/JNEUROSCI.3496-17.2018
Asgarian, Z. et al. MTG8 interacts with LHX6 to specify cortical interneuron subtype identity. Nat. Commun. 13, 5217 (2022).
pubmed: 36064547
pmcid: 9445035
doi: 10.1038/s41467-022-32898-6
Lavdas, A. A., Grigoriou, M., Pachnis, V. & Parnavelas, J. G. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19, 7881–7888 (1999).
pubmed: 10479690
pmcid: 6782477
doi: 10.1523/JNEUROSCI.19-18-07881.1999
Small, S. A., Schobel, S. A., Buxton, R. B., Witter, M. P. & Barnes, C. A. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat. Rev. Neurosci. 12, 585–601 (2011).
pubmed: 21897434
pmcid: 3312472
doi: 10.1038/nrn3085
Karpf, J. et al. Dentate gyrus astrocytes exhibit layer-specific molecular, morphological and physiological features. Nat. Neurosci. 25, 1626–1638 (2022).
pubmed: 36443610
doi: 10.1038/s41593-022-01192-5
Southwell, D. G. et al. Intrinsically determined cell death of developing cortical interneurons. Nature 491, 109–113 (2012).
pubmed: 23041929
pmcid: 3726009
doi: 10.1038/nature11523
Gilani, A. I. et al. Interneuron precursor transplants in adult hippocampus reverse psychosis-relevant features in a mouse model of hippocampal disinhibition. Proc. Natl. Acad. Sci. 111, 7450–7455 (2014).
pubmed: 24794528
pmcid: 4034251
doi: 10.1073/pnas.1316488111
Blanquie, O. et al.. Electrical activity controls area-specific expression of neuronal apoptosis in the mouse developing cerebral cortex. eLife 6, e27696 (2017).
pubmed: 28826501
pmcid: 5582867
doi: 10.7554/eLife.27696
Wong, F. K. et al.. Pyramidal cell regulation of interneuron survival sculpts cortical networks. Nature 557, 668–673 (2018).
pubmed: 29849154
pmcid: 6207348
doi: 10.1038/s41586-018-0139-6
Wong, F. K. et al.. Serotonergic regulation of bipolar cell survival in the developing cerebral cortex. Cell Rep. 40, 111037 (2022).
pubmed: 35793629
pmcid: 9638000
doi: 10.1016/j.celrep.2022.111037
Picken Bahrey, H. L. & Moody, W. J. Early development of voltage-gated ion currents and firing properties in neurons of the mouse cerebral cortex. J. Neurophysiol. 89, 1761–1773 (2003).
pubmed: 12611962
doi: 10.1152/jn.00972.2002
Tezuka, Y., Hagihara, K. M., Ohki, K., Hirano, T. & Tagawa, Y. Developmental stage-specific spontaneous activity contributes to callosal axon projections. eLife 11, e72435 (2022).
pubmed: 36001081
pmcid: 9402231
doi: 10.7554/eLife.72435
Suárez, R. et al. Cortical activity emerges in region-specific patterns during early brain development. Proc. Natl. Acad. Sci. 120, e2208654120 (2023).
pubmed: 37216522
pmcid: 10235933
doi: 10.1073/pnas.2208654120
Carriere, C. H. et al. The γ-protocadherins regulate the survival of GABAergic interneurons during developmental cell death. J. Neurosci. 40, 8652–8668 (2020).
pubmed: 33060174
pmcid: 7643289
doi: 10.1523/JNEUROSCI.1636-20.2020
Pai, E. L.-L. et al.. Mafb and c-Maf have prenatal compensatory and postnatal antagonistic roles in cortical interneuron fate and function. Cell Rep. 26, 1157-1173.e5 (2019).
pubmed: 30699346
pmcid: 6602795
doi: 10.1016/j.celrep.2019.01.031
Wang, H. et al. Region-specific distribution of Olig2-expressing astrocytes in adult mouse brain and spinal cord. Mol. Brain 14, 36 (2021).
doi: 10.1186/s13041-021-00747-0
Valério-Gomes, B., Guimarães, D. M., Szczupak, D. & Lent, R. The absolute number of oligodendrocytes in the adult mouse brain. Front. Neuroanat. 12, 90 (2018).
pubmed: 30425626
pmcid: 6218541
doi: 10.3389/fnana.2018.00090
Huang, H., He, W., Tang, T. & Qiu, M. Immunological markers for central nervous system glia. Neurosci. Bull. 39, 379–392 (2023).
pubmed: 36028641
doi: 10.1007/s12264-022-00938-2
Yang, Z. & Wang, K. K. W. Glial fibrillary acidic protein: from intermediate filament assembly and gliosis to neurobiomarker. Trends Neurosci. 38, 364–374 (2015).
pubmed: 25975510
pmcid: 4559283
doi: 10.1016/j.tins.2015.04.003
Hammad, M. et al. Transplantation of GABAergic interneurons into the neonatal primary visual cortex reduces absence seizures in stargazer mice. Cereb. Cortex 25, 2970–2979 (2015).
pubmed: 24812085
doi: 10.1093/cercor/bhu094
Kriegstein, A. & Alvarez-Buylla, A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32, 149–184 (2009).
pubmed: 19555289
pmcid: 3086722
doi: 10.1146/annurev.neuro.051508.135600
Kessaris, N. et al. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci. 9, 173–179 (2006).
pubmed: 16388308
doi: 10.1038/nn1620
Arshad, M. N., Oppenheimer, S., Jeong, J., Buyukdemirtas, B. & Naegele, J. R. Hippocampal transplants of fetal GABAergic progenitors regulate adult neurogenesis in mice with temporal lobe epilepsy. Neurobiol. Dis. 174, 105879 (2022).
pubmed: 36183946
pmcid: 9724706
doi: 10.1016/j.nbd.2022.105879
Bifari, F. et al.. Neurogenic radial glia-like cells in meninges migrate and differentiate into functionally integrated neurons in the neonatal cortex. Cell Stem Cell 20, 360-373 (2017).
pubmed: 27889318
doi: 10.1016/j.stem.2016.10.020
Bathina, S. & Das, U. N. Brain-derived neurotrophic factor and its clinical implications. Arch. Med. Sci. 6, 1164–1178 (2015).
doi: 10.5114/aoms.2015.56342
Luhmann, H. J. et al. Spontaneous neuronal activity in developing neocortical networks: From single cells to large-scale interactions. Front. Neural Circuits 10, 40 (2016).
pubmed: 27252626
pmcid: 4877528
doi: 10.3389/fncir.2016.00040
Marín, O. Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107–120 (2012).
pubmed: 22251963
doi: 10.1038/nrn3155
Katsarou, A., Moshé, S. L. & Galanopoulou, A. S. Interneuronopathies and their role in early life epilepsies and neurodevelopmental disorders. Epilepsia Open 2, 284–306 (2017).
pubmed: 29062978
pmcid: 5650248
doi: 10.1002/epi4.12062
Nomura, T. Interneuron dysfunction and inhibitory deficits in autism and fragile X syndrome. Cells 10, 2610 (2021).
pubmed: 34685590
pmcid: 8534049
doi: 10.3390/cells10102610
Quattrocolo, G., Fishell, G. & Petros, T. J. Heterotopic transplantations reveal environmental influences on interneuron diversity and maturation. Cell Rep. 21, 721–731 (2017).
pubmed: 29045839
pmcid: 5662128
doi: 10.1016/j.celrep.2017.09.075
Grade, S. et al. Brain injury environment critically influences the connectivity of transplanted neurons. Sci. Adv. 8, eabg9445 (2022).
doi: 10.1126/sciadv.abg9445
Thomas, J. et al. Excessive local host-graft connectivity in aging and amyloid-loaded brain. Sci. Adv. 8, eabg9287 (2022).
pubmed: 35687689
pmcid: 9187230
doi: 10.1126/sciadv.abg9287