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The Journal of Neuroscience, June 1, 2001, 21(11):3860-3870
Sparks and Puffs in Oligodendrocyte Progenitors: Cross Talk
between Ryanodine Receptors and Inositol Trisphosphate Receptors
Laurel L.
Haak1,
Long-Sheng
Song2,
Tadeusz
F.
Molinski3,
Isaac N.
Pessah4,
Heping
Cheng2, 5, and
James T.
Russell1
1 National Institute of Child Health and Human
Development, National Institutes of Health (NIH), Bethesda, Maryland
20892, 2 National Institute on Aging, NIH, Baltimore,
Maryland 21224, Departments of 3 Chemistry and
4 Molecular Bioscience, School of Veterinary Medicine,
University of California, Davis, California 95616, and
5 National Laboratory of Biomembranes and Membrane
Biotechnology, College of Life Sciences, Peking University, Beijing
100871, China
Investigating how calcium release from the endoplasmic reticulum
(ER) is triggered and coordinated is crucial to our understanding of
how oligodendrocyte progenitor cells (OPs) develop into myelinating cells. Sparks and puffs represent highly localized
Ca2+ release from the ER through ryanodine receptors
(RyRs) and inositol trisphosphate receptors (IP3Rs),
respectively. To study whether sparks or puffs trigger
Ca2+ waves in OPs, we performed rapid
high-resolution line scan recordings in fluo-4-loaded OP processes. We
found spontaneous and evoked sparks and puffs, and we have identified
functional cross talk between IP3Rs and RyRs. Local events
evoked using the IP3-linked agonist methacholine (MeCh)
showed significantly different morphology compared with events evoked
using the caffeine analog 3,7-dimethyl-1-propargylxanthine (DMPX). Pretreatment with MeCh potentiated DMPX-evoked events, whereas inhibition of RyRs potentiated events evoked by low
concentrations of MeCh. Furthermore, activation of IP3Rs
but not RyRs was critical for Ca2+ wave initiation.
Using immunocytochemistry, we show OPs express the specific
Ca2+ release channel subtypes RyR3 and
IP3R2 in patches along OP processes. RyRs are coexpressed
with IP3Rs in some patches, but IP3Rs are also
found alone. This differential distribution pattern may underlie the
differences in local and global Ca2+ signals
mediated by these two receptors. Thus, in OPs, interactions between
IP3Rs and RyRs determine the spatial and temporal
characteristics of calcium signaling, from microdomains to
intracellular waves.
Key words:
calcium; confocal microscopy; cross talk; development; IP3 receptor; muscarinic receptor; ryanodine receptor; oligodendrocyte progenitor; puffs; SERCA; sparks; Xestospongin C; wave
Copyright © 2001 Society for Neuroscience 0270-6474/01/21113860-11$05.00/0
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