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The Journal of Neuroscience, June 7, 2006, 26(23):6269-6281; doi:10.1523/JNEUROSCI.4212-05.2006

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Development/Plasticity/Repair
Neuronal Pentraxins Mediate Synaptic Refinement in the Developing Visual System

Lisa Bjartmar,^1 * Andrew D. Huberman,^5 * Erik M. Ullian,^5,8 * René C. Rentería,⁸ Xiaoqin Liu,¹ Weifeng Xu,^5,6 Jennifer Prezioso,¹ Michael W. Susman,⁵ David Stellwagen,^5,6 Caleb C. Stokes,⁵ Richard Cho,⁷ Paul Worley,⁷ Robert C. Malenka,^5,6 Sherry Ball,^2,3 Neal S. Peachey,^2,3 David Copenhagen,⁸ Barbara Chapman,⁴ Masaru Nakamoto,¹ Ben A. Barres,⁵ and Mark S. Perin¹

Departments of ¹Neurosciences and ²Ophthalmic Research, Cleveland Clinic Foundation, Cleveland, Ohio 44195; ³Research Service, Cleveland VA Medical Center, Cleveland, Ohio 44106; ⁴Center for Neuroscience, University of California, Davis, California 95616; Departments of ⁵Neurobiology and ⁶Psychiatry, Stanford University School of Medicine, Stanford, California 94305; ⁷Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205; and ⁸Department of Ophthalmology, University of California, San Francisco, San Francisco, California 94143

Correspondence should be addressed to Mark S. Perin, Department of Neurosciences, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195. Email: perinm{at}ccf.org

Neuronal pentraxins (NPs) define a family of proteins that are homologous to C-reactive and acute-phase proteins in the immune system and have been hypothesized to be involved in activity-dependent synaptic plasticity. To investigate the role of NPs in vivo, we generated mice that lack one, two, or all three NPs. NP1/2 knock-out mice exhibited defects in the segregation of eye-specific retinal ganglion cell (RGC) projections to the dorsal lateral geniculate nucleus, a process that involves activity-dependent synapse formation and elimination. Retinas from mice lacking NP1 and NP2 had cholinergically driven waves of activity that occurred at a frequency similar to that of wild-type mice, but several other parameters of retinal activity were altered. RGCs cultured from these mice exhibited a significant delay in functional maturation of glutamatergic synapses. Other developmental processes, such as pathfinding of RGCs at the optic chiasm and hippocampal long-term potentiation and long-term depression, appeared normal in NP-deficient mice. These data indicate that NPs are necessary for early synaptic refinements in the mammalian retina and dorsal lateral geniculate nucleus. We speculate that NPs exert their effects through mechanisms that parallel the known role of short pentraxins outside the CNS.

Key words: retinogeniculate; neuronal pentraxins; synaptic plasticity; LTP; long-term potentiation; LTD; long-term depression; development; knock-out; retinal ganglion cell

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Received Oct. 3, 2005; revised April 16, 2006; accepted April 18, 2006.

Correspondence should be addressed to Mark S. Perin, Department of Neurosciences, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195. Email: perinm{at}ccf.org

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