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Sonic Hedgehog Controls the Phenotypic Fate and Therapeutic Efficacy of Grafted Neural Precursor Cells in a Model of Nigrostriatal Neurodegeneration
Journal article   Open access   Peer reviewed

Sonic Hedgehog Controls the Phenotypic Fate and Therapeutic Efficacy of Grafted Neural Precursor Cells in a Model of Nigrostriatal Neurodegeneration

Lalitha Madhavan, Brian F Daley, Beverly L Davidson, Ryan L Boudreau, Jack W Lipton, Allyson Cole-Strauss, Kathy Steece-Collier and Timothy J Collier
PloS one, Vol.10(9), pp.e0137136-e0137136
2015
DOI: 10.1371/journal.pone.0137136
PMCID: PMC4560385
PMID: 26340267
url
https://doi.org/10.1371/journal.pone.0137136View
Published (Version of record) Open Access

Abstract

The expression of soluble growth and survival promoting factors by neural precursor cells (NPCs) is suggested to be a prominent mechanism underlying the protective and regenerative effects of these cells after transplantation. Nevertheless, how and to what extent specific NPC-expressed factors contribute to therapeutic effects is not well understood. Using RNA silencing, the current study investigated the roles of two donor NPC molecules, namely glial cell-line derived neurotrophic factor (GDNF) and sonic hedgehog (SHH), in the protection of substantia nigra dopamine neurons in rats treated with 6-hydroxydopamine (6-OHDA). Analyses indicate that as opposed to the knock-down of GDNF, SHH inhibition caused a profound decline in nigrostriatal neuroprotection. Further, SHH silencing also curbed endogenous neurogenesis and the migration of host brdU+/dcx+ neural precursors into the striatum, which was present in the animals receiving control or GDNF silenced NPCs. A change in graft phenotype, mainly reflected by a reduced proportion of undifferentiated nestin+ cells, as well as a significantly greater host microglial activity, suggested an important role for these processes in the attenuation of neuroprotection and neurogenesis upon SHH silencing. Overall these studies reveal core mechanisms fundamental to grafted NPC-based therapeutic effects, and delineate the particular contributions of two graft-expressed molecules, SHH and GDNF, in mediating midbrain dopamine neuron protection, and host plasticity after NPC transplantation.
Substantia Nigra - growth & development RNA, Small Interfering - genetics Substantia Nigra - pathology Dopaminergic Neurons - pathology Mesencephalon - metabolism Humans Rats, Inbred F344 Alkaline Phosphatase - metabolism Hedgehog Proteins - metabolism Glial Cell Line-Derived Neurotrophic Factor - antagonists & inhibitors Substantia Nigra - metabolism Neural Stem Cells - cytology Oxidopamine Neurogenesis - genetics Glial Cell Line-Derived Neurotrophic Factor - metabolism Hedgehog Proteins - genetics Gene Expression Regulation, Developmental Isoenzymes - metabolism Dopaminergic Neurons - metabolism Neural Stem Cells - transplantation Neostriatum - metabolism Transgenes Disease Models, Animal Mesencephalon - pathology Animals, Newborn Neostriatum - growth & development Neostriatum - pathology Alkaline Phosphatase - genetics Rats, Transgenic Signal Transduction Isoenzymes - genetics Glial Cell Line-Derived Neurotrophic Factor - genetics Rats Neurodegenerative Diseases - genetics Neurodegenerative Diseases - therapy Hedgehog Proteins - antagonists & inhibitors Neurodegenerative Diseases - metabolism GPI-Linked Proteins - metabolism Stereotaxic Techniques Phenotype Animals Neurodegenerative Diseases - chemically induced Graft Survival - genetics Mesencephalon - growth & development Primary Cell Culture Neural Stem Cells - metabolism GPI-Linked Proteins - genetics RNA, Small Interfering - metabolism

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