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Recovery of cDNAs encoding ribosomal proteins S9 and L26 from Aedes albopictus mosquito cells and identification of their homologs in the malaria vector Anopheles gambiae.

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Li and Fallon
Archives of Insect Biochemistry and Physiology 60:44–53 (2005)
Recovery of cDNAs Encoding Ribosomal Proteins S9
and L26 From Aedes albopictus Mosquito Cells and
Identification of Their Homologs in the Malaria Vector,
Anopheles gambiae
Lei Li and A.M. Fallon*
We used PCR-based approaches to obtain the full-length cDNA sequences encoding ribosomal protein (Rp) S9 and L26 from a
mosquito (Aedes albopictus) C7-10 cell line. The deduced mosquito RpS9 protein has a mass of 22,826 Da and a pI of
11.41, while RpL26 had a mass of 17,442 Da and a pI of 11.52. Both cDNAs initiated with the 5′-polypyrimidine motif
characteristic of ribosomal protein transcripts. Using the Aedes protein and nucleic acid sequences, we identified rpS9 and
rpL26 as single copy genes in the Anopheles gambiae genome. In An. gambiae, the RpS9 coding region was distributed over
3 exons, spanning 2.6 kb, but the Anopheles rpL26 protein coding region lacked introns. The Aedes and Anopheles RpS9 and
RpL26 proteins shared 96 and 92% identity, respectively. Despite low numbers of parsimony-informative amino acid substitutions, phylogenies based on the ribosomal protein sequences accurately group the Aedes and Anopheles proteins with high
bootstrap values. Arch. Insect Biochem. Physiol. 60:44–53, 2005. © 2005 Wiley-Liss, Inc.
KEYWORDS: Aedes albopictus; Anopheles gambiae; cell line; genome; mosquito; protein synthesis; ribosomal
protein; RpS9; RpL26
In adult female mosquitoes, the blood meal initiates a cycle of ribosome biosynthesis, and in the
fat body, the accumulated ribosomes provide protein synthetic machinery that supports synthesis of
the egg yolk proteins, or vitellogenins. The approximately 80 individual ribosomal proteins (Rp) that
are assembled into the small and large ribosomal
subunits play diverse roles in maintaining ribosome structure and participating in specific aspects
of protein synthesis. Some of the ribosomal proteins also have important extra-ribosomal functions, including roles in DNA replication and repair
and in RNA processing (Wool, 1996). Our interest
in ribosomal proteins relates to their potential manipulation in transgenic mosquitoes to disrupt vector-parasite interactions. Qian et al. (1988) showed
that transgenic disruption of the synthesis of a
single ribosomal protein caused sterility in female
Drosophila melanogaster.
With the exception of an unusual C-terminal
extension on mosquito RpS6 (Hernandez et al.,
2003), the amino acid sequences of homologous
ribosomal proteins that have been described from
Aedes and Anopheles mosquitoes are well conserved.
In the cases where genomic DNA has been sequenced, exon-intron organization is also conserved. In general, Exon 1 in mosquito ribosomal
protein genes is short, and may not be translated.
Department of Entomology, University of Minnesota, St. Paul, Minnesota
Contract grant sponsor: National Institutes of Health; Contract grant number: AI20385; Contract grant sponsor: University of Minnesota Experiment Station, St.
Paul, MN.
*Correspondence to: Ann M. Fallon, Department of Entomology, University of Minnesota, 1980 Folwell Ave., St. Paul, MN 55108. E-mail: [email protected]
Received 22 January 2005; Accepted 18 April 2005
© 2005 Wiley-Liss, Inc.
DOI: 10.1002/arch.20083
Published online in Wiley InterScience (
Archives of Insect Biochemistry and Physiology
Mosquito Ribosomal Proteins S9 and L26
The AUG start codon is typically located near the
end of Exon 1 or close to the 5′-end of Exon 2.
Aedes albopictus rpS6 (Hernandez et al., 2003), rpL8
(Lan and Fallon, 1992), and rpL34 (Niu and
Fallon, 1999) genes each contain a long Exon 3,
which encodes the remainder of the protein. The
5′-end of the known mosquito Rp mRNAs is C/Trich (Niu and Fallon, 1999), and the 3′-end is
polyadenylated (Durbin et al., 1988).
Because their sequence and structure are relatively well conserved, it will be of interest to compare phylogenies based on ribosomal proteins
with results derived from rRNA genes, which have
been used extensively as molecular data to reconstruct relationships among insect taxa (Pawlowski
et al., 1996). In bacteria, phylogenies based on
the fused sequences of the 53 ribosomal proteins
have shown good agreement with rRNA-based
phylogenies (Matte-Tailliez et al., 2002). Because
mRNA encoding ribosomal proteins is relatively
abundant (Durbin et al., 1988), our unanticipated
recovery of mosquito RpS9 and RpL26 sequences
among PCR products obtained with degenerate
primers was not surprising. In the case of these
two proteins, the availability of a full-length sequence from both Drosophila melanogaster and the
silk moth, Bombyx mori, and our identification of
homologs in the Anopheles gambiae database, allowed us to construct phylogenies based on all
known insect RpS9 and RpL26 proteins, using the
rat homolog as the outgroup. Despite relatively
few parsimony-informative characters, individual
phylogenies based on RpS9 and RpL26 group the
Aedes and Anopheles proteins with high bootstrap
values, but only RpS9 reliably includes Drosophila
with the mosquitoes. Analyses with RpL26 consistently yield two trees, in which B. mori, or alternatively D. melanogaster, is the sister group to
the mosquitoes.
Cell Line and Culture Conditions
Ae. albopictus C7-10 mosquito cells (Fallon,
1997) were maintained as monolayers at 28°C in
Eagle’s minimal medium supplemented with nonSeptember 2005
essential amino acids, glutamine, and 5% heat-inactivated fetal bovine serum (Shih et al., 1998).
RNA Isolation and PCR-Based Cloning
Total RNA was obtained from C7-10 cells using
Qiagen’s RNeasy kit (Valencia, CA). A PCR product
encoding the 5′-end of rpS9 was recovered by
5′RACE, using the GeneRacer kit from Invitrogen
(Carlsbad, CA) and a degenerate reverse primer designed to recognize a mosquito homolog of the tumor suppressor protein, p53. The remainder of the
rpS9 cDNA sequence was obtained using reverse
transcriptase (RT)-PCR with a specific forward
G), from the 5′-untranslated region (Fig. 1A), and
oligo(dT) as the reverse primer. PCR was done using 35 cycles of 30 sec denaturation at 94°C, 45 sec
annealing at 58°C, and 1 min extension at 72°C.
PCR was terminated with a 2-min extension at 72°C.
The band was cloned as described below.
A PCR product encoding the C-terminal end
of RpL26 was likewise obtained fortuitously using a heterologous primer. Based on the sequence
of the initial product, specific reverse primers (Fig.
1B) were designed to obtain the complete cDNA
sequence using the 5′-primer supplied in the
GeneRacer kit. Using L26-1, we obtained a mixture of PCR products using a touchdown PCR protocol (denaturation at 94°C for 2 min, followed
by denaturation at 94°C for 30 sec and annealing
at 72°C for 45 sec (5 cycles); denaturation at 94°C
for 30 sec with annealing at 70°C for 45 sec (5
cycles), followed by 25 cycles of denaturation at
94°C for 30 sec, annealing at 62°C for 30 sec,
and extension at 72°C for 45 sec. The PCR product was re-amplified with the internal primer L262 and the GeneRacer 5′-nested primer using 1
cycle at 94°C for 5 min, 25 cycles of denaturation
at 94°C for 30 sec, annealing at 62°C for 30 sec,
and extension at 72°C for 30 sec, followed by one
cycle at 72°C for 3 min. The resulting, discrete
band was cloned into pGEM®-T Easy vector
(Promega, Madison, WI) and introduced into
competent DH5α® Escherichia coli (Invitrogen, La
Jolla, CA) using standard procedures.
Li and Fallon
Fig. 1. Mosquito RpS9 (A) and RpL26 (B) cDNAs. The ATG translation start codons
and TAA stop codons are boxed, and the polypyrimidine tracts at the 5′-end of each
transcript are underlined. The position and orientation of horizontal arrows designate primers used to obtain the sequence. In A, inverted triangles indicate positions
of introns within the coding sequence, based on a comparison with the An. gambiae
genome. In B, a consensus polyadenylation signal is doubly underlined.
Aedes albopictus rpS9 and rpL26 cDNAs
The complete nucleotide sequences of Ae.
albopictus RpS9 cDNA (GenBank Accession no.
AY847002) and Ae. albopictus RpL26 cDNA (GenBank Accession no. AY885229) are shown in Figure 1A and B. The 5′-ends of the RpS9 and RpL26
mRNAs extended 78 and 79 nucleotides, respec-
tively, upstream of the AUG translation initiation
codon. Both cDNAs contained the polypyrimidine
motif characteristic of Rp transcripts at their 5′ends. In Figure 1, the initiation and termination
codons are boxed, and the specific primers S9-1,
L26-1, and L26-2 used to obtain the complete sequences are designated by arrows showing the direction of extension. In the rpL26 cDNA, a putative
polyadenylation signal is doubly underlined. AlArchives of Insect Biochemistry and Physiology
Mosquito Ribosomal Proteins S9 and L26
Fig. 1 (continued)
though an exact consensus signal is absent from
the 3′-untranslated region in the rpS9 cDNA, there
are several A/T-rich motifs that may serve as
polyadenylation signals.
RpS9 and RpL26 Homologs in Anopheles gambiae
When the protein sequences deduced from these
cDNAs were compared to the An. gambiae genome
using the program BLAST at the National Center
for Biotechnology Information (NCBI) website
(http: //, we found the homologous rpS9 gene on An. gambiae chromosome
2L, encoding the conceptual protein identified by
XP_313936), which was reported to be incomplete
on the N-terminal end. Alignment with the Ae.
albopictus sequence showed that the Anopheles protein initiated at the methionine represented by the
third codon in XP_313936. An. gambiae rpL26
mapped to chromosome 2R, corresponding to protein XP_312471. This RpL26 entry was also reported
September 2005
as incomplete at the N-terminus, but direct comparison with the Aedes sequence indicates that translation of Anopheles RpL26 initiates at an internal
methionine (residue 25) in XP_312471. Both genes
occurred as a single-copy in the An. gambiae genome.
Translation of the An. gambiae genomic DNA
sequence and alignment with the Ae. albopictus coding sequence indicated that in An. gambiae, the rpS9
coding region is distributed over 3 exons, spanning 2.6 kb. Within the coding sequence, intron
boundaries were verified by the presence of
consensus nucleotides, and their relative positions
are indicated by inverted open triangles in Figure
1A. Lengths of the upstream and downstream introns in the An. gambiae gene are 222 and 1,754
nucleotides, respectively. By way of contrast, the
An. gambiae RpL26 coding sequence is not interrupted by introns, as is shown by the alignment of
Anopheles genomic DNA with the Ae. albopictus
cDNA (Fig. 2). In D. melanogaster, the rpL26 cod-
Li and Fallon
Fig. 2. Alignment of An. gambiae RpL26 genomic DNA
sequence with Aedes albopictus RpL26 cDNA. The alignment shows the Anopheles sequence at top (lowercase letters) and the Aedes sequence at bottom (uppercase letters).
Protein initiation and termination codons are boxed. Identities are represented by vertical lines, and gaps (indicated
by dots) were introduced to maximize the alignment.
Archives of Insect Biochemistry and Physiology
Mosquito Ribosomal Proteins S9 and L26
ing region of gene CG6846 also lacks introns
(FlyBase Consortium, 2003).
DNA Upstream of the Coding Region
Using 5′RACE, obtaining the 5′-end of eukaryotic mRNAs is relatively straightforward, and the
cDNAs shown in Figure 1 contain 5′-untranslated
regions (UTR) upstream of the translational start
codon. The cDNA sequence does not, however, include introns that may interrupt the 5′-UTR. Thus,
comparison of the Ae.albopictus cDNA sequences
with An. gambiae genomic DNA facilitates identification of introns present within the coding sequence
by simple comparison of the An. gambiae open reading frame with the deduced translation product from
the Aedes cDNA. Introns within the 5′-UTR are more
difficult to detect because they lie outside the open
reading frame defined by the cDNA.
For example, with the introduction of an eightnucleotide gap in the Ae. albopictus RpL26 cDNA
sequence, the 5′-ends of the cDNA and the genomic DNA upstream of the AUG start codon in
An. gambiae were well conserved (Fig. 2), suggesting that in An. gambiae, the rpL26 gene lacks an
intron in the 5′-UTR. In the Drosophila homolog,
however, an intron is indicated in the DNA upstream of the RpL26 (CG6846) coding region
Fig. 3. Analysis of the An. gambiae nucleotide sequence
immediately upstream of the RpS9 coding region. In the
top sequence, the 5′-end of the experimentally-determined
Ae. albopictus RpS9 sequence (uppercase letters) is boxed.
September 2005
(FlyBase Consortium, 2003), which would be represented by a gap corresponding to the length of
the intron in the cDNA sequence, relative to genomic DNA. Without additional experimental data
from Anopheles gambiae, however, we cannot exclude the possibility that the high level of nucleotide homology is simply fortuitous.
In the case of rpS9, the alignment suggests that
an intron is present upstream of the coding region.
Here again, in silico comparisons between Aedes
and Anopheles sequences are not entirely unambiguous because the Anopheles sequence contains a
stretch of 20 unidentified residues (represented by
a series of n’s in Fig. 3) upstream of the coding
region. Using the GCG (Genetics Computer Group,
Madison, WI) program Bestfit, we noted relatively
weak homology between the Ae. albopictus 5′-UTR
and the putative upstream region in the An.
gambiae gene. Nevertheless, a polypyrimidine tract
that resembles the 5′-end of a ribosomal protein
mRNA is found in the Anopheles sequence immediately upstream of the coding region.
RpS9 and RpL26 Proteins
The Ae. albopictus RpS9 contained 195 amino
acid residues, with a calculated mass of 22,826 and
pI of 11.41. RpS9 from Ae. albopictus and An.
In the An. gambiae sequence (lowercase), a potential
polypyrimidine tract [poly(PY)] is boxed. The box surrounding both sequences corresponds to nucleotides encoding the N-terminus of the homologous RpS9 proteins.
Li and Fallon
Phylogenetic Analysis
gambiae shared 99% similarity, 96% identity. Features of mosquito RpS9 shared with homologs
from other organisms include the ~45 residue putative RNA binding domain (boxed in Fig. 4) and
a series of five to six C-terminal acidic amino acids, which show a single conservative E/D substitution between the two mosquito sequences. Some,
but not all, of the tripeptide repeats described in
rat RpS9 (Chan et al., 1993) are also well conserved
in insect RpS9. The Ae. albopictus RpL26 protein
(Fig. 5) contained 151 residues, a deduced molecular mass of 17,442 and a pI of 11.52. Relative to
the An. gambiae sequence, identity was 92%, and
similarity was 95%. Of three putative 9-residue repeats with the consensus sequence VQVXRXKYK
described for rat RpL26 (Paz et al., 1989; see the
bars at the top of the alignment shown in Fig. 5),
the repeat closest to the C-terminus was poorly
conserved between the rat and insect proteins.
Although the deduced amino acid sequences of
relatively few insect ribosomal proteins are available in the databases, we tested the construction
of phylogenies using the protein sequences of
Aedes, Anopheles, and Drosophila flies, and the moth,
Bombyx mori. The alignments shown in Figures 4
and 5 were analyzed based on parsimony using
the default parameters of PAUP* (Swofford, 2000)
to obtain the phylograms shown in Figure 6, in
which the rat sequence was designated as the
outgroup. For RpS9, bootstrap values (Fig. 6, circled
values) were based on 1,000 replications, while for
RpL26, 10,000 replications were used. Note that
for both proteins, An. gambiae was most closely
related to Ae. albopictus. However, for RpL26, bootstrap support for inclusion of Drosophila with the
mosquitoes was low.
Fig. 4. Alignment of RpS9 proteins from mosquitoes with
homologs from D. melanogaster, B. mori, and the rat. The
alignment was produced using ClustalX, version 1.83 (Thompson et al., 1997) with default settings. A single gap in
the B. mori sequence is indicated by a dash, and consensus residues are indicated by asterisks below the align-
ment. Double dots (:) and single dots (.) designate highly
conserved, and less well-conserved amino acid replacements, respectively. The boxed region designates the RNA
binding domain, and bars above the alignment indicate
triplet peptides identified in the rat sequence by Chan et
al. (1993).
Archives of Insect Biochemistry and Physiology
Mosquito Ribosomal Proteins S9 and L26
Fig. 5. Alignment of RpL26 proteins. The alignment was
produced using ClustalX, version 1.83, as described in the
legend to Figure 4. Bars at the top of the alignment desig-
nate putative 9-residue repeats in the rat sequence described by Paz et al. (1989).
quences are deposited in the databases, it will be
of interest to revisit their potential value in phylogenetic comparisons.
Eukaryotic RpS9 is a component of the small
ribosomal subunit homologous to Escherichia coli
RpS4 (Chan et al., 1993). The observation that bacterial RpS4 mutants have high translational error
rates suggested that the wild type RpS4 participates
in ribosome assembly (Davies and Nomura, 1992).
Nowotny and Nierhaus (1988) showed that E. coli
RpS4 and RpS7 nucleate an assembly domain for
16S rRNA. In the fungus, Podospora anserina, mutations in the gene encoding RpS9 confer resistance
to paromomycin (Dequard-Chablat, 1985), which
suggests that RpS9 plays a similar role in translational accuracy in eukaryotic cells. The crystal structure of RpS4 from Bacillus stearothermophilus suggests
that the RNA binding domain is predominantly
on one side of the protein, is highly positively
charged, and contains two conserved arginine residues (Davies et al., 1998; Markus et al., 1998).
Aside from mosquitoes and D. melanogaster, partial RpS9 sequences have been reported from the
flies Drosophila yakuba and Sarcophaga crassipalpis.
Insofar as sequence is available, the two Drosophila
RpS9 proteins are 100% identical to each other,
and to the partial sequence from S. crassipalpis.
In the evolution of the ribosome, selection acts
at the level of the amino acid sequence of the protein (see Wittmann-Liebold et al., 1990), which
determines how the protein interacts with the rRNA
scaffold and with other proteins. The degree of conservation between ribosomal proteins varies, with
identities between rat and yeast homologs ranging
from 40 to 80% (Wool et al., 1990). In the phylogenetic analysis presented here (Fig. 6) the three
dipteran RpS9 sequences grouped together with
high confidence, while for RpL26, the positions of
D. melanogaster and B. mori were reversed roughly
50% of the time. Thus, for RpL26, a tree based on
protein sequence correctly shows the two mosquitoes as most closely related to one another, but
does not reliably distinguish between a member
of the higher Diptera (D. melanogaster) and a moth.
Given these differences, it is of interest to note that
for RpS9, there were 195 characters (amino acids),
of which 154 were constant, 32 variable, but parsimony uninformative, and only 9 parsimony informative characters. For RpL26, there were 151
characters, of which 92 were constant, 41 variable
but uninformative, and 18 were parsimony informative. As additional insect ribosomal protein seSeptember 2005
Li and Fallon
Fig. 6. Phylograms based on
the alignments shown in Figures 4 and 5. A parsimony
analysis was done with PAUP*
(Swofford, 2000) with default
settings, and the trees were
rooted by designating the rat
sequence as the outgroup.
Branch lengths are displayed as
integers. Bootstrap values are
circled and based on 1,000
replicates for RpS9 and 10,000
replicates for RpL26.
RNAi directed towards Drosophila RpS9 has been
reported to affect cell growth and viability (FlyBase
Consortium, 2003), and in rat neuronal cells, RpS9
has been associated with protection from oxidative damage (Kim et al., 2003).
RpL26 is located on the large ribosomal subunit. In contrast to RpS9, RpL26 has been little
studied, but like rpS9, sequences are available for
B. mori and D. melanogaster. Eukaryotic RpL26 is
most closely related to bacterial RpL24, and in
yeast, Villarreal and Lee (1998) have shown that
the protein is located at the interface between the
small and large ribosomal subunits. Larede et al.
(2001) identified RpL26 from a marine snail, and
in this species, RpL26 is up-regulated during anoxia. Because larvae of mosquitoes and other
aquatic insects may experience anoxic conditions
during development, it will be of interest to examine this potential function in mosquitoes.
We thank Dr. G. Jayachandran for participation
in early stages of this work.
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homology, l26, aedes, mosquitoes, identification, vectors, gambia, cells, cdna, malaria, anopheles, recovery, albopictus, protein, ribosomal, encoding
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