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The Journal of Neuroscience, September 21, 2005, 25(38):8601-8610; doi:10.1523/JNEUROSCI.2122-05.2005

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Cellular/Molecular
Downregulation of Platelet-Derived Growth Factor- Receptor-Mediated Tyrosine Kinase Activity as a Cellular Mechanism for K⁺-Channel Regulation during Oligodendrocyte Development In Situ

Ramesh Chittajallu, Adan A. Aguirre, and Vittorio Gallo

Center for Neuroscience Research, Children's Research Institute, Children's National Medical Center, Washington, DC 20010

Oligodendrocyte maturation has been defined based on expression of developmentally regulated antigens. However, transitions at early stages of the lineage have not been functionally characterized fully in situ. Combining 2',3'-cyclic nucleotide 3'-phosphodiesterase (CNP)-promoter driven enhanced green fluorescent protein expression and whole-cell capacitance measurements permitted a reliable distinction between subcortical white matter NG2⁺ oligodendrocyte progenitors (OPs) and O4⁺ preoligodendrocytes (pre-OLs) in situ. We focused on K⁺ channels because their expression has been associated previously with the proliferation and differentiation potential of OPs. Using whole-cell patch clamp, we observed a downregulation of the delayed outward-rectifying current (I_KDR) between the NG2⁺ and O4⁺ stages but no significant changes in transient K⁺-channel current (I_KA) amplitude. Tyrosine kinase inhibition in NG2⁺ cells reduced I_KDR amplitude with no effect on I_KA, which mimicked the endogenous changes observed between OPs and pre-OLs. Tyrosine kinase inhibition also reduced the proliferative capacity of NG2⁺ OPs in slice cultures. Conversely, acute platelet-derived growth factor receptor- (PDGFR-) activation caused an increase of I_KDR in NG2⁺ but not in O4⁺ cells. Consistent with this finding, PDGFR- immunoreactivity was confined to NG2⁺ cells with undetectable levels in O4⁺ cells, suggesting that PDGFR- signaling is absent in pre-OLs in situ. Importantly, the PDGF-induced increase of I_KDR in NG2⁺ cells was prevented by tyrosine kinase inhibition. Together, these data indicate that PDGFR- and tyrosine kinase activity act via a common pathway that influences functional expression of K⁺ channels and proliferative capacity of OPs in situ.

Key words: oligodendrocyte progenitor; whole-cell patch clamp; white matter; CNP-EGFP mouse; cell proliferation; maturation

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Received May 26, 2005; revised August 8, 2005; accepted August 8, 2005.

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