Generation, characterization, and molecular cloning
of the Noerg-1 mutation of rhodopsin in the mouse
LAWRENCE H. PINTO,
1
MARTHA H. VITATERNA,
1
KAZUHIRO SHIMOMURA,
1
SANDRA M. SIEPKA,
1
ERIN L. MCDEARMON,
1
DEBORAH FENNER,
1
STEPHEN L. LUMAYAG,
1
CHIAKI OMURA,
1
ANNE W. ANDREWS,
1
MATTHEW BAKER,
1
BRANDON M. INVERGO,
1
MARISSA A. OLVERA,
2
EDWARD HEFFRON,
2
ROBERT F. MULLINS,
2
VAL C. SHEFFIELD,
3,4
EDWIN M. STONE,
2
and JOSEPH S. TAKAHASHI
1,4
1
Department of Neurobiology and Physiology and Center for Functional Genomics, Northwestern University, Evanston
2
Department of Ophthalmology & Visual Sciences, University of Iowa, Iowa City
3
Departments of Pediatrics and Genetics, University of Iowa, Iowa City
4
Howard Hughes Medical Institute, Carver College of Medicine, Iowa City
(Received February 14, 2005; Accepted May 18, 2005!
Abstract
We performed genome-wide mutagenesis of C57BL 06J mice using the mutagen N-ethyl-N-nitrosourea ~ ENU! and
screened the third generation ~G3! offspring for visual system alterations using electroretinography and fundus
photography. Several mice in one pedigree showed characteristics of retinal degeneration when tested at 12–14
weeks of age: no recordable electroretinogram ~ ERG!, attenuation of retinal vessels, and speckled pigmentation of
the fundus. Histological studies showed that the retinas undergo a photoreceptor degeneration with apoptotic loss of
outer nuclear layer nuclei but visual acuity measured using the optomotor response under photopic conditions
persists in spite of considerable photoreceptor loss. The Noerg-1 mutation showed an autosomal dominant pattern of
inheritance in progeny. Studies in early postnatal mice showed degeneration to occur after formation of partially
functional rods. The Noerg-1 mutation was mapped genetically to chromosome 6 by crossing C57BL06J mutants
with DBA02J or BALB0cJ mice to produce an N2 generation and then determining the ERG phenotypes and the
genotypes of the N2 offspring at multiple loci using SSLP and SNP markers. Fine mapping was accomplished with
a set of closely spaced markers. A nonrecombinant region from 112.8 Mb to 115.1 Mb was identified,
encompassing the rhodopsin ~ Rho! coding region. A single nucleotide transition from G to A was found in the Rho
gene that is predicted to result in a substitution of Tyr for Cys at position 110, in an intradiscal loop. This mutation
has been found in patients with autosomal dominant retinitis pigmentosa ~ RP! and results in misfolding of
rhodopsin expressed in vitro. Thus, ENU mutagenesis is capable of replicating mutations that occur in human
patients and is useful for generating de novo models of human inherited eye disease. Furthermore, the availability of
the mouse genomic sequence and extensive DNA polymorphisms made the rapid identification of this gene possible,
demonstrating that the use of ENU-induced mutations for functional gene identification is now practical for
individual laboratories.
Keywords: Chemical mutagenesis, ENU, Forward genetics, Retina, Mouse models, Retinitis pigmentosa, Molecular
cloning, Positional cloning, Gene discovery, Rhodopsin, Protein folding, Disulfide bond formation, Rods, Rod
photoreceptor, Rho-C
110
Y mutation, Optomotor response, Visual acuity
Introduction
Forward genetic approaches ~from phenotype to gene! have been
used to identify essential genes for many processes, facilitating
rapid progress in diverse areas ~ Takahashi et al., 1994!. One
powerful forward genetic approach combines genome-wide chem-
ical mutagenesis with phenotypic screens to identify mutants with
alterations in the process under study. Such identification of mu-
tants can open a field to molecular and genetic study. For example,
the demonstration that the Shaker gene of Drosophila encoded a
potassium channel ~ Wu et al., 1983! and the subsequent cloning of
this gene ~ Papazian et al., 1987; Tempel et al., 1987! enabled the
identification of several other families of ion channels and led to a
detailed knowledge of their structure–function relationship ~ Doyle
et al., 1998!. Likewise, the field of circadian biology was advanced
from descriptive to mechanistic analyses with the identification of
the per gene ~ Konopka & Benzer, 1971!. Essential components of
Address correspondence and reprint requests to: Lawrence H. Pinto,
Northwestern University, Department of Neurobiology and Physiology,
2205 Tech Drive, Northwestern University, Evanston, IL 60208, USA.
E-mail: larry-pinto@northwestern.edu
Visual Neuroscience ~2005!, 22, 619–629. Printed in the USA.
Copyright © 2005 Cambridge University Press 0952-5238005 $16.00
DOI: 10.10170S0952523805225117
619