Mutations in PTF1A cause pancreatic and
cerebellar agenesis
Gabrielle S Sellick
1
, Karen T Barker
1
, Irene Stolte-Dijkstra
2
, Christina Fleischmann
1
, Richard J Coleman
1
,
Christine Garrett
3
, Anna L Gloyn
4
, Emma L Edghill
4
, Andrew T Hattersley
4
, Peter K Wellauer
5
,
Graham Goodwin
6
& Richard S Houlston
1
Individuals with permanent neonatal diabetes mellitus usually
present within the first three months of life and require insulin
treatment
1,2
. We recently identified a locus on chromosome
10p13–p12.1 involved in permanent neonatal diabetes mellitus
associated with pancreatic and cerebellar agenesis in a
genome-wide linkage search of a consanguineous Pakistani
family
3
. Here we report the further linkage analysis of this
family and a second family of Northern European descent
segregating an identical phenotype. Positional cloning
identified the mutations 705insG and C886T in the gene
PTF1A, encoding pancreas transcription factor 1a, as disease-
causing sequence changes. Both mutations cause truncation
of the expressed PTF1A protein C-terminal to the
basic-helix-loop-helix domain. Reporter-gene studies using a
minimal PTF1A deletion mutant indicate that the deleted
region defines a new domain that is crucial for the function of
this protein. PTF1A is known to have a role in mammalian
pancreatic development
4,5
, and the clinical phenotype of the
affected individuals implicated the protein as a key regulator of
cerebellar neurogenesis. The essential role of PTF1A in normal
cerebellar development was confirmed by detailed
neuropathological analysis of Ptf1a
À/À
mice.
Linkage to our previously identified locus on 10p13–p12.1 associated
with permanent neonatal diabetes mellitus (PNDM) defined by the
single-nucleotide polymorphism (SNP) markers rs1398431 and
rs2149639 in the Pakistani family (Family 1; Fig. 1a) was confirmed
in both families using microsatellite markers (Fig. 1a,b). Marker data
allowed further positional refinement of the linked region to the 7.7-
Mb interval between rs1398431 and D10S586. The combined lod score
for both families between markers D10S548 and D10S586 was 4.4.
We selected three genes mapping to the region of linkage, PIP5K2A,
PTF1A and CACNB2, for candidate gene screening because of their
expression in human or mouse pancreatic and cerebellar tissue and
implied biological function. We sequenced coding regions including
all exon-intron boundaries of each gene using genomic DNA from all
available members of both families. In addition to a common
polymorphism detected in family 1 (787T-C, dbSNP identifier
rs7918487, control C allele frequency 0.45), which did not segregate
with the disease phenotype, we identified two different mutations in
PTF1A, both of which resulted in truncation of the expressed protein
(Fig. 2a). In family 1, affected individuals (V:4, V:8 and V:9; Fig. 1a)
were homozygous with respect to a 886C-T transition in exon 2
causing a nonsense mutation (R296X). In family 2, the affected
individual (V:1; Fig. 2a) was homozygous with respect to a single–
base pair insertion (705insG) in exon 1, which caused a frameshift
mutation (P236fsX270) and truncation of the PTF1A protein at codon
270 (Fig. 2a,b). The mutations segregated with the disease phenotype
and carrier status in both families. Neither mutation was present in
190 alleles from healthy, unrelated individuals or had been previously
documented by either dbSNP or the Celera Human SNP databases.
The 705insG and 886C-T mutations in PTF1A cause truncation of
the C-terminal 32 amino acids of the expressed protein, which is a
functional domain a priori. To examine the effect of the deletion on
transcriptional activity, we compared the abilities of full-length and
truncated PTF1A (PTF1ADC) to activate a luciferase reporter con-
struct containing Ptf1-E47 recognition motifs.
The availability of a mouse Ptf1a clone and literature describing
the binding motif recognized by murine Ptf1 led us to work with
the mouse clone, constructing a truncated version at the position
equivalent to the most C-terminal deletion in the human sequence.
The Ptf1-E47 recognition motif of the rat chymotrypsin gene com-
prises two conserved sequences: an A box that is unique to Ptf1
binding sites
6
and an E box recognized by ordinary basic helix-loop-
helix (bHLH) proteins
7
. E47 is a protein that heterodimerizes with
bHLH proteins to stimulate transcription from E box–containing
promoters. Using a promoter containing four repeats of the A/E
motif of the rat chymotrypsinogen B gene, Obata et al.
8
showed that
Published online 14 November 2004; doi:10.1038/ng1475
1
Section of Cancer Genetics, Institute of Cancer Research, Surrey SM2 5NG, UK.
2
Department of Clinical Genetics, University Hospital Groningen, Groningen 9700
RB, The Netherlands.
3
North West Thames Regional Genetics Service, Kennedy-Galton Centre, North West London Hospitals NHS Trust, Harrow HA1 3UJ, UK.
4
Diabetes and Vascular Medicine, Peninsula Medical School, Exeter EX2 5AX, UK.
5
Swiss Institute for Experimental Cancer Research (ISREC), CH-1066 Epalinges,
Switzerland.
6
Section of Molecular Carcinogenesis, Institute of Cancer Research, Surrey SM2 5NG, UK. Correspondence should be addressed to R.S.H.
(Richard.Houlston@icr.ac.uk).
NATURE GENETICS VOLUME 36 [ NUMBER 12 [ DECEMBER 2004 1301
LETTERS
© 2004 Nature Publishing Group http://www.nature.com/naturegenetics