Mutations in RNF135, a gene
within the NF1 microdeletion
region, cause phenotypic
abnormalities including
overgrowth
Jenny Douglas
1,11
, Deirdre Cilliers
1,11
, Kim Coleman
1
,
Katrina Tatton-Brown
1,2
, Karen Barker
1
, Brigitte Bernhard
3
,
John Burn
3
, Susan Huson
4
, Dragana Josifova
5
, Didier Lacombe
6
,
Mohsin Malik
7
, Sahar Mansour
2
, Evan Reid
8
,
Valerie Cormier-Daire
9
, Trevor Cole
10
, The Childhood
Overgrowth Collaboration & Nazneen Rahman
1
17q11 microdeletions that encompass NF1 cause 5%–10% of
cases of neurofibromatosis type 1, and individuals with micro-
deletions are typically taller than individuals with intragenic
NF1 mutations, suggesting that deletion of a neighboring gene
might promote human growth. We identified mutations in
RNF135, which is within the NF1 microdeletion region, in six
families characterized by overgrowth, learning disability,
dysmorphic features and variable additional features. These
data identify RNF135 as causative of a new overgrowth
syndrome and demonstrate that RNF135 haploinsufficiency
contributes to the phenotype of NF1 microdeletion cases.
Neurofibromatosis type 1 (NF1; MIM 162200) is one of the most
common genetic conditions, with an incidence of 1 in 3,000 (ref. 1).
The majority of cases are due to intragenic mutations in the NF1 gene.
However, 5%–10% are due to 17q11 microdeletions that encompass
NF1 (refs. 2,3). The most common deletion (type 1) spans 1.4 Mb,
involves 13 genes in addition to NF1 and is usually generated by
nonallelic homologous recombination between flanking low-copy
repeats known as NF1REPa and NF1REPc (ref. 4; Fig. 1a).
The phenotype of neurofibromatosis type 1 generated through
17q11 microdeletions differs from that associated with intragenic
NF1 mutations. Individuals with NF1 microdeletions are more
likely to have facial dysmorphism, learning disability, congenital
heart defects and high numbers of neurofibromas
5
. Such individuals
are also often of tall stature, both compared with individuals with
NF1 intragenic mutations and compared with the age-related peer
group
6
. Many of the additional phenotypic features that occur in
individuals with NF1 microdeletions are typical of constitutional loss
of genetic material throughout the genome, and therefore it is difficult
to discern whether they reflect a generic effect of this type of genomic
insult, or whether they are related to haploinsufficiency of specific
genes within the deleted interval. However, tall stature is very unusual
in children with chromosomal deletions, which usually result in growth
retardation
7
. Therefore, we suspected that haploinsufficiency of a gene
within the 17q11 microdeletion might promote human growth.
To investigate this, we conducted mutation screening on 12 of the
14 genes that are deleted in the type 1 microdeletion, using con-
formation-sensitive gel electrophoresis (CSGE) and bidirectional
sequencing of genomic DNA from individuals with overgrowth
phenotypes of unknown cause (Supplementary Methods and Sup-
plementary Table 1 online). We did not analyze NF1, as none of the
affected individuals had features of neurofibromatosis type 1, and we
were unable to adequately analyze LRRC37B because multiple pseu-
docopies of this gene exist. All the individuals investigated had
overgrowth in childhood (defined as height and/or head circumfer-
ence at least 2 s.d. above the mean) and some degree of learning
disability. Many had additional features that were very variable in
nature. The recognizable overgrowth conditions Sotos syndrome,
Bannayan-Riley-Ruvalcaba syndrome, Simpson-Golabi-Behmel
syndrome and Beckwith-Wiedemann syndrome were excluded
molecularly and/or clinically (Supplementary Methods).
We did not identify mutations in 11 of the 12 genes. In RNF135,
we identified truncating mutations in 4 of 245 unrelated individuals
with overgrowth (Fig. 1a,b and Table 1). A low-copy repeat,
NF1REPb, is located between RNF135 and NF1, and nonallelic
homologous recombination between NF1REPa and NF1REPb would
be predicted to result in deletion of five genes, CRLF3, C17orf41,
C17orf42, CENTA and RNF135 (ref. 4). We hypothesized that
such a microdeletion might result in an overgrowth phenotype
without features of NF1. To investigate this, we undertook multiplex
ligation-dependent probe amplification (MLPA) using the SALSA
P122 kit that includes probes throughout the deleted interval
(Fig. 1a and Supplementary Methods). In one individual, we
identified a microdeletion that included RNF135 and the four other
genes but did not include NF1, consistent with nonallelic homologous
recombination between NF1REPa and NF1REPb (Fig. 1c). We also
screened the full RNF135 gene for mutations in 510 normal indivi-
duals and for microdeletions in 192 normal individuals. We did not
identify any truncating mutations (4/245 versus 0/510, P ¼ 0.01) or
whole-gene deletions, further supporting the pathogenicity of such
abnormalities in the overgrowth cases. We identified one individual
Received 4 May; accepted 22 May; published online 15 July 2007; doi:10.1038/ng2083
1
Section of Cancer Genetics, Institute of Cancer Research, Sutton, Surrey SM2 5NG, UK.
2
S.W. Thames Regional Genetics Service, St. George’s Hospital Medical
School, London SW17 0RE, UK.
3
Institute of Human Genetics, International Centre for Life, Newcastle Upon Tyne NE1 3BZ, UK.
4
Department of Medical Genetics,
St. Mary’s Hospital, Manchester M13 OJH, UK.
5
Department of Clinical Genetics, Guy’s Hospital, London SE1 9RT, UK.
6
Department of Medical Genetics, Hopital
Pellegrin-enfants, EA2406 Bordeaux, France.
7
Queen Elizabeth the Queen Mother’s Hospital, Margate CT9 4AN, UK.
8
Medical Genetics Department, Addenbrooke’s
Hospital, Cambridge CB2 2QQ, UK.
9
Department of Medical Genetics, Hopital Necker Enfants Malades, 75015 Paris, France.
10
Clinical Genetics Unit, Birmingham
Women’s Hospital, Birmingham B15 2TG, UK.
11
These authors contributed equally to this work. Correspondence should be addressed to N.R. (nazneen.rahman@icr.ac.uk).
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