Citation: Mustafa, S.; Hussain, M.F.;
Latif, M.; Ijaz, M.; Asif, M.; Hassan,
M.; Faisal, M.; Iqbal, F. A Missense
Mutation (c.1037 G > C, p. R346P) in
PAPSS2 Gene Results in Autosomal
Recessive form of Brachyolmia Type 1
(Hobaek Form) in A Consanguineous
Family. Genes 2022, 13, 2096. https://
doi.org/10.3390/genes13112096
Academic Editor: Amy
Jayne McKnight
Received: 11 October 2022
Accepted: 8 November 2022
Published: 11 November 2022
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genes
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Article
A Missense Mutation (c.1037 G > C, p. R346P) in PAPSS2 Gene
Results in Autosomal Recessive form of Brachyolmia Type 1
(Hobaek Form) in A Consanguineous Family
Saima Mustafa
1
, Malik Fiaz Hussain
1
, Muhammad Latif
2,
*, Maryam Ijaz
1
, Muhammad Asif
1
,
Mubashir Hassan
3
, Muhammad Faisal
4
and Furhan Iqbal
1,
*
1
Institute of Pure and Applied Biology, Zoology Division, Bahauddin Zakariya University,
Multan 60800, Pakistan
2
Department of Zoology, Division of Science and Technology, University of Education, Lahore 54770, Pakistan
3
The Steve and Cindy Rasmussen Institute for Genomic Medicine, Nationwide Children’s Hospital,
Columbus, OH 43205, USA
4
Faculty of Health Studies, University of Bradford, Bradford BD7 1DP, UK
* Correspondence: muhammad.lateef@ue.edu.pk (M.L.); furhan.iqbal@bzu.edu.pk (F.I.)
Abstract: Background: Brachyolmia is a skeletal disorder with an autosomal mode of inheritance
(both dominant and recessive) in which the patients have a short height, scoliosis and a reduced
trunk size. Methods: From the Muzaffargarh District in Pakistan, a consanguineous family with
multiple Brachyolmia-affected subjects were enrolled in the present study. Basic epidemiological
data and radiographs were collected for the subjects. Whole exome sequencing (WES) which was
followed by Sanger sequencing was applied to report the geneticbasic of Brachyolmia. Results: The
WES identified a missense mutation (c.1037 G > C, p. R346P) in exon 9 of the PAPSS2 gene that was
confirmed by the Sanger sequencing in the enrolled subjects. The mutation followed a Mendalian
pattern with an autosomal recessive inheritance mode. Multiple sequence alignment by Clustal
Omega indicated that the PAPSS2 mutation-containing domain is highly conserved. The HEK293T
whole-cell extract that was transfected with the Myc-tagged PCMV6-PAPSS2 of both the wild and
mutant constructs were resolved by SDS-PAGE as well as by a Western blot, which confirmed that
there are different PAPSS2 protein expression patterns when they were compared between the control
and Brachyolmia patients. This difference between the normal and mutated protein was not evident
when the three-dimensional computational structures were generated using homology modeling.
Conclusion: We report a missense mutation (c.1037 G > C, p. R346P) in the PAPSS2 gene that caused
Brachyolmia in a consanguineous Pakistani family.
Keywords: brachyolmia; WES; sanger sequencing; Western blot; 3D protein structure
1. Introduction
Brachyolmia is a skeletal dysplasia in which the subjects have a short stature and a
short trunk with an affected spine [1,2]). Brachyolmia has been characterized into four
clinically well-defined types. Brachyolmia type 1 is a name that is given to the Hobaek
and Toledo forms. It has an autosomal recessive mode of inheritance. Patients suffering
from this type of disease have platyspondyly with a widening of the vertebral bodies, their
inter vertebral spaces are irregular and narrow, and they have scoliosis [1,3]. Brachyolmia
type 2, also known as Maroteaux type, is similar to type one as it has also an autosomal
recessive mode of inheritance, but the patients have rounded vertebral bodies and pedicles
that are less over-faced which makes this type different from type 1 [4]. Brachyolmia type 3
transmits in an autosomal dominant form, and the patients have severe kyphoscoliosis, and
their cervical vertebrae are irregular and flattened [5]. Brachyolmia type 4 is also known
as the spondyloepimetaphyseal dysplasia [SEMD] Pakistani type, and it is an autosomal
Genes 2022, 13, 2096. https://doi.org/10.3390/genes13112096 https://www.mdpi.com/journal/genes