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J. Biol. Chem., Vol. 282, Issue 34, 25053-25066, August 24, 2007

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MicroRNA (miRNA) Transcriptome of Mouse Retina and Identification of a Sensory Organ-specific miRNA Cluster^*

Shunbin Xu¹, P. Dane Witmer^¶, Stephen Lumayag, Beatrix Kovacs, and David Valle²

From the Department of Ophthalmology and Neurological Sciences, Rush University Medical Center, Chicago, Illinois 60302 and McKusick-Nathans Institute of Genetic Medicine, ^¶Predoctoral Training Program in Human Genetics, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205

Although microRNAs (miRNAs) provide a newly recognized level of regulation of gene expression, the miRNA transcriptome of the retina and the contributions of miRNAs to retinal development and function are largely unknown. To begin to understand the functions of miRNAs in retina, we compared miRNA expression profiles in adult mouse retina, brain, and heart by microarray analysis. Our results show that at least 78 miRNAs are expressed in adult mouse retina, 21 of which are potentially retina-specific. Among these, we identified a polycistronic, sensory organ-specific paralogous miRNA cluster that includes miR-96, miR-182, and miR-183 on mouse chromosome 6qA3 with conservation of synteny to human chromosome 7q32.2. In situ hybridization showed that members of this cluster are expressed in photoreceptors, retinal bipolar and amacrine cells. Consistent with their genomic organization, these miRNAs have a similar expression pattern during development with abundance increasing postnatally and peaking in adult retina. Target prediction and in vitro functional studies showed that MITF, a transcription factor required for the establishment and maintenance of retinal pigmented epithelium, is a direct target of miR-96 and miR-182. Additionally, to identify miRNAs potentially involved in circadian rhythm regulation of the retina, we performed miRNA expression profiling with retinal RNA harvested at noon (Zeitgeber time 5) and midnight (Zeitgeber time 17) and identified a subgroup of 12 miRNAs, including members of the miR-183/96/182 cluster with diurnal variation in expression pattern. Our results suggest that miR-96 and miR-182 are involved in circadian rhythm regulation, perhaps by modulating the expression of adenylyl cyclase VI (ADCY6).

Received for publication, January 18, 2007 , and in revised form, May 29, 2007.

^* This work was supported by grants from the University Committee for Research, Rush University Medical Center and Lincy Foundation (to S. X.), the Foundation Fighting Blindness (to D. V.), Predoctoral Training Program in Human Genetics Grant NIGMS 5T32GM07814, and NEI Visual Neuroscience Training Program Grant T32EY07143 (P. D. W.) from the National Institutes of Health. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Tables 1–14 and Fig. 1.

¹ To whom correspondence may be addressed: Rush University Medical Center, Department of Ophthalmology and Neurological Sciences, 1735 W. Harrison St. 318, Chicago, IL 60612. Tel.: 312-563-3554; Fax: 312-563-3571; E-mail: shunbin_xu{at}rush.edu. ² To whom correspondence may be addressed: Johns Hopkins University, School of Medicine, McKusick-Nathans Institute of Genetic Medicine, 519 BRB, 733 N Broadway, Baltimore, MD 21205. Tel.: 410-955-4260; Fax: 410-955-7397; E-mail: dvalle{at}jhmi.edu.

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