Mutations in the Pre-mRNA Splicing-Factor Genes
PRPF3, PRPF8, and PRPF31 in Spanish Families with
Autosomal Dominant Retinitis Pigmentosa
Marı ´a Martı ´nez-Gimeno,
1,2
Marı ´a Jose ´ Gamundi,
1,2
Imma Hernan,
1
Miquel Maseras,
3
Elena Milla´,
3
Carmen Ayuso,
4
Blanca Garcı ´a-Sandoval,
5
Magdalena Beneyto,
6
Concha Vilela,
7
Montserrat Baiget,
8
Guillermo Antin˜olo,
9
and Miguel Carballo
1
PURPOSE. Mutations in the systemically expressed pre-mRNA
splicing-factor genes PRPF3, PRPF8, and PRPF31 have re-
cently been associated with autosomal dominant retinitis pig-
mentosa (adRP). This study was intended to identify mutations
in PRPF3, PRPF8, and PRPF31 in 150 Spanish families affected
by adRP, to measure the contribution of mutations in these
genes to adRP in that population, and to correlate RP pheno-
type expression with mutations in pre-mRNA splicing-factor
genes.
METHODS. Denaturing gradient gel electrophoresis (DGGE) and
direct genomic sequencing were used to evaluate the complete
coding region and flanking intronic sequences of the PRPF31
gene, exon 42 of PRPF8, and exon 11 of PRPF3 for mutations
in 150 unrelated index patients with adRP. Ophthalmic and
electrophysiological examination of patients with RP and their
relatives was performed according to preexisting protocols.
RESULTS. Three nonsense mutations caused by insertion and
deletion sequences and two missense mutations (Arg2310Gly)
and within the stop codon of the PRPF8 gene (TGA3 TTG),
were detected in five unrelated heterozygous patients. Three
patients were heterozygous carriers of different nonsense mu-
tations in exon 8 of the PRPF31, gene and one Thr494Met
mutation was found in exon 11 of the PRPF3 gene. Cosegre-
gation of the mutation in PRPF8 and PRPF3 with adRP was
observed. However, two nonsense mutations in PRPF31 caus-
ing adRP detected in two families showed asymptomatic car-
riers.
CONCLUSIONS. Nine mutations, six of which are novel, in the
pre-mRNA splicing-factor genes PRPF3, PRPF8, and PRPF31,
causing adRP have been identified in the Spanish population.
Their contribution to adRP is approximately 5% after correc-
tion in relation to mutations found in other genes causing
adRP. The patients carrying a mutation in the pre-mRNA splic-
ing-factor PRPF8 gene showed a type 1 diffuse RP. The exis-
tence of asymptomatic carriers of the nonsense mutation in the
PRPF31 gene suggests incomplete penetrance for these muta-
tions in the families. (Invest Ophthalmol Vis Sci. 2003;44:
2171–2177) DOI:10.1167/iovs.02-0871
R
etinitis pigmentosa (RP) is a group of hereditary retinal
degenerations with a worldwide incidence of approxi-
mately 1 in 3500 individuals. Clinical characteristics include
night blindness, loss of peripheral visual field, characteristic
changes in the ocular fundus, and depression of the normal
ocular electrophysiological responses.
1
The genetics of RP is
complex, and the disorder may be inherited through an auto-
somal dominant (adRP), autosomal recessive (arRP), X-linked
(XLRP),
2,3
or digenic
4
trait. Mutations within six genes (RHO,
peripherin/RDS, RP1, NRL, CRX, and FSCN2) that encode
proteins specifically expressed in photoreceptor cells have
been reported to cause adRP.
5–9
Such proteins are involved in
specific functions in the retina, such as the visual transduction
cycle and structural components of the rod and cone photo-
receptor cells or transcription factors. Furthermore, genetic
linkage studies and mutation detection resulted in the charac-
terization of mutation in genes with systemic expression im-
plicated in adRP.
10 –12
Three of these genes, PRPF3 (RP18), PRPF8 (RP13), and
PRPF31 (RP11), are members of the pre-mRNA splicing-factor
components of the U4/U6-U5 tri-snRNP particle
13–15
that is
dynamically assembled and dissociated at each round of the
splicing cycle. Although little is known about the association
and dissociation of the U4/U6 and U5 snRNP, protein–protein
interaction and rearrangement are believed to take part in the
formation and function of the tri-snRNP particle.
16
It is there-
fore plausible that some mutation in one of the protein com-
ponents of the tri-snRNP affects its structure and the splicing
function. Mutations in the pre-mRNA splicing-factor genes
reported so far in humans seem to produce pathologic ef-
fects in the retina only. The mutations reported to date in
PRPF8
11
and PRPF3
12
are clustered within a 14 (exon 42) and
2 (exon 11)-codon stretch respectively, whereas mutations in
PRPF31
10
are more dispersed within the transcript sequence.
Mutations in the rhodopsin (RHO) and peripherin/RDS
genes are the cause of 20% of the adRP in the Spanish popu-
lation.
17
Mutation in other genes associated with adRP such as
NRL
18
and RP1 (unpublished results) have also been detected
in the Spanish population, contributing to 5% of total cases of
adRP in Spain. To determine the contribution of mutation in
the pre-mRNA splicing-factor genes PRPF3, PRPF8, and
PRPF31 in adRP-carrying Spanish families, screening for muta-
tion in the complete coding region of the PRPF31 gene was
performed. Because mutations in the PRPF3 and PRPF8 gene
causing adRP reported so far are clustered in exons 11 and 42
From the
1
Laboratory of Biology and Molecular Genetics, Labora-
tory of Service and the
3
Service of Ophthalmology, Consorci Sanitari de
Terrassa, Hospital de Terrassa, Terrassa, Spain; the Services of
4
Genet-
ics and the
5
Ophthalmology, Fundacio´n Jime´nez Dı ´az, Madrid, Spain;
the Services of
6
Genetics and of
7
Neurophysiology, Hospital La Fe,
Valencia, Spain; the
8
Service of Molecular Genetics, Hospital de La
Santa Creu i Sant Pau, Barcelona, Spain; and the
9
Service of Genetics
and Prenatal Diagnostics, Hospital Virgen del Rocı ´o, Sevilla, Spain.
2
Contributed equally to the work and therefore should be consid-
ered as equivalent first authors.
Supported in part by grants from Fondo de Investigacio´n Sanitaria
(FIS 99/0780, 01/0081-01), ONCE, and Fundacio´n ONCE.
Submitted for publication August 26, 2002; revised December 3,
2002; accepted December 14, 2002.
Disclosure: M. Martı ´nez-Gimeno, None; M.J. Gamundi, None;
I. Hernan, None; M. Maseras, None; E. Milla´ , None; C. Ayuso,
None; B. Garcı ´a-Sandoval, None; M. Beneyto, None; C. Vilela,
None; M. Baiget, None; G. Antin˜olo, None; M. Carballo, None
The publication costs of this article were defrayed in part by page
charge payment. This article must therefore be marked “advertise-
ment” in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Corresponding author: Miguel Carballo, Hospital de Terrassa, Ctra.
Torrebonica s/n, 08227 Terrassa, Spain; carballolab@terra.es.
Investigative Ophthalmology & Visual Science, May 2003, Vol. 44, No. 5
Copyright © Association for Research in Vision and Ophthalmology 2171