Developmentally Expressed Ca2+-sensitive Adenylyl Cyclase Activity Is Disrupted in the Brains of Type I Adenylyl Cyclase Mutant Mice
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The type I Ca(2+)-sensitive adenylyl cyclase has been implicated in several forms of synaptic plasticity in vertebrates. Mutant mice in which this enzyme was inactivated by targeted mutagenesis show deficient spatial memory and altered long term potentiation (Wu, Z. L., Thomas, S. A., Villacres, E. C., Xia, Z., Simmons, M. L., Chavkin, C., Palmiter, R. D., and Storm, D. R. (1995) Proc. Natl Acad Sci. U. S. A. 92, 220-224). Long term potentiation in the CA1 region of the rat hippocampus develops during the first 2 weeks after birth and reaches maximal expression at postnatal day 15 with a gradual decline at later stages of development. Here we report that Ca(2+)-stimulated adenylyl cyclase activity in rat hippocampus, cerebellum, and cortex increases significantly between postnatal days 1-16. This increase appears to be due to enhanced expression of type I adenylyl cyclase rather than type VIII adenylyl cyclase, the other adenylyl cyclase that is directly stimulated by Ca2+ and calmodulin. Type I adenylyl cyclase mRNA in the hippocampus increased 7-fold during this developmental period. The developmental expression of Ca(2+)-stimulated adenylyl cyclase activity in mouse brain was attenuated in mutant mice lacking type I adenylyl cyclase. Changes in expression of the type I adenylyl cyclase during the period of long term potentiation development are consistent with the hypothesis that this enzyme is important for neuroplasticity and spatial memory in vertebrates.
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Wild-type hippocampus expresses nearly equivalent amounts of AC1 and AC8 mRNA.
“The wild-type hippocampus expresses nearly equivalent amounts of AC1 and AC8 mRNA (Villacres et al., 1995).”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Villacres et al., 1995
Ca2+ sensitivity of adenylyl cyclase in membranes from AC1 mutant mice was less than wild-type mice.
“In addition, the Ca 2ϩ sensitivity of the adenylyl cyclase in membranes from AC1 mutant mice was less than wild-type mice, consistent with Ca 2ϩ activation of AC8 (Villacres et al., 1995).”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Villacres et al., 1995
This increase is attributable primarily to the increased expression of AC1.
“This increase is attributable primarily to the increased expression of AC1 (Villacres et al., 1995).”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Villacres et al., 1995
AC1 is expressed developmentally and reaches a maximum at postnatal day 16.
“Because AC1 is expressed developmentally and reaches a maximum at postnatal day 16 (Villacres et al., 1995), we were concerned that the hippocampus of AC1 mutant mice might not develop normally.”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Villacres et al., 1995
Ca2+ -stimulated adenylyl cyclase activity in the hippocampus of mice and rats increases between postnatal days 1 and 14.
“C a 2ϩ -stimulated adenylyl cyclase activity in the hippocampus of mice and rats increases between postnatal days 1 and 14.”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Villacres et al., 1995
The Ca2+ sensitivity of AC8 is approximately five times lower than AC1.
“The Ca 2ϩ sensitivity of AC8 is approximately five times lower than AC1 (Villacres et al., 1995), and it is not stimulated by G s -coupled receptors, even in the presence of Ca 2ϩ (Nielsen et al., 1996).”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Villacres et al., 1995
AC1 is stimulated by free Ca2+ as low as 150-200 nM.
“It is stimulated by free Ca 2ϩ as low as 150 -200 nM (Choi et al., 1992;Villacres et al., 1995)”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Villacres et al., 1995
Cites
Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons
Frey, U., Huang, Y.-Y., & Kandel, E. R. (1993) · Science · doi:10.1126/science.8389057 · Cited by 1,218 · see citing works
Noradrenergic enhancement of long-term potentiation at mossy fiber synapses in the hippocampus
Hopkins, W. F., & Johnston, D. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.59.2.667 · Cited by 310 · see citing works
Type I Calmodulin‐Sensitive Adenylyl Cyclase Is Neural Specific
Xia, Z., Choi, E., Wang, F., Blazynski, C., & Storm, D. R. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb05852.x · Cited by 178 · see citing works
Self-citationSynergistic activation of the type I adenylyl cyclase by Ca2+ and Gs-coupled receptors in vivo.
Wayman, G. A., Impey, S., Wu, Z., Kindsvogel, W., Prichard, L., & Storm, D. R. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47263-8 · Cited by 166 · see citing works
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Wong, S. T., Athos, J., Figueroa, X. A., Pineda, V. V., Schaefer, M. L., Chavkin, C. C., Muglia, L. J., & Storm, D. R. (1999) · Neuron · doi:10.1016/s0896-6273(01)80036-2 · Cited by 486 · see citing works
Self-citationSadana, R., & Dessauer, C. W. (2009) · Neurosignals · doi:10.1159/000166277 · Cited by 361 · see citing works
Regulation and organization of adenylyl cyclases and cAMP
COOPER, D. M. F. (2003) · Biochemical Journal · doi:10.1042/bj20031061 · Cited by 356 · see citing works
Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation
Villacres, E. C., Wong, S. T., Chavkin, C., & Storm, D. R. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03186.1998 · Cited by 187 · see citing works
Self-citationLoss of adenylyl cyclase I activity disrupts patterning of mouse somatosensory cortex
Abdel-Majid, R. M., Leong, W. L., Schalkwyk, L. C., Smallman, D. S., Wong, S. T., Storm, D. R., Fine, A., Dobson, M. J., Guernsey, D. L., & Neumann, P. E. (1998) · Nature Genetics · doi:10.1038/980 · Cited by 163 · see citing works
Self-citationImpaired Cerebellar Long-Term Potentiation in Type I Adenylyl Cyclase Mutant Mice
Storm, D. R., Hansel, C., Hacker, B., Parent, A., & Linden, D. J. (1998) · Neuron · doi:10.1016/s0896-6273(00)80500-0 · Cited by 159 · see citing works
Self-citationAltered Stress-Induced Anxiety in Adenylyl Cyclase Type VIII-Deficient Mice
Schaefer, M. L., Wong, S. T., Wozniak, D. F., Muglia, L. M., Liauw, J. A., Zhuo, M., Nardi, A., Hartman, R. E., Vogt, S. K., Luedke, C. E., et al. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-13-04809.2000 · Cited by 152 · see citing works
Self-citationGarelick, M. G., Chan, G. C. K., DiRocco, D. P., & Storm, D. R. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0553-09.2009 · Cited by 18 · see citing works
Self-citationCalcium activated adenylyl cyclase AC8 but not AC1 is required for prolonged behavioral anxiety
Bernabucci, M., & Zhuo, M. (2016) · Molecular Brain · doi:10.1186/s13041-016-0239-x · Cited by 11 · see citing works
- Authors
- Villacres, E. C., Wu, Z., Hua, W., Nielsen, M. D., Watters, J. J., Yan, C., Beavo, J., & Storm, D. R.
- Affiliations
- University of Washington (US)
- Corresponding author
- Storm, Daniel R.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 1995-06
- Volume
- 270
- Issue
- 24
- Pages
- 14352-14357
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2055918680
- Cited by
- 61
- References
- 4
- Citations by year
- 2025: 1 · 2021: 2 · 2019: 1 · 2018: 2 · 2016: 3 · 2015: 2
- FWCI
- 2.53
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5k08ns001653-05)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 21723, R01DK021723)
- National Institute of Neurological Disorders and Stroke (R01NS020498, NS20498, NS 01653)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Keywords
- hippocampus, cerebellum, cerebral cortex, postnatal brain development, long-term potentiation, spatial memory, synaptic plasticity, neuroplasticity, calmodulin
- MeSH terms
- Adenylyl Cyclases, Animals, Brain, Calcium, Cell Line, Enzyme Activation, Mice, Inbred C57BL, Mice, Mutant Strains, RNA, Messenger, Gene Expression Regulation, Enzymologic, Rats, Sprague-Dawley, In Situ Hybridization, Gene Expression Regulation, Developmental, Mice, Rats
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