Comparative Biochemistry and Physiology Part B 127 (2000) 433 – 441 www.elsevier.com/locate/cbpb
Conserved cassette structure of vertebrate Mr 300 kDa mannose 6-phosphate receptors: partial cDNA sequence of fish MPR 300 Udaya Lakshmi Yerramalla a,b, Siva Kumar Nadimpalli a, Peter Schu b, Kurt von Figura b, Annette Hille-Rehfeld b,* a b
Protein Biochemistry Laboratory, Department of Biochemistry, Uni6ersity of Hyderabad, Hyderabad 500046, India Biochemie II, Zentrum Biochemie und Molekulare Zellbiologie, Georg-August Uni6ersita¨t, Heinrich Du¨ker Weg 12d, 37073 Go¨ttingen, Germany Received 31 March 2000; received in revised form 22 June 2000; accepted 26 June 2000
Abstract The existence of two homologous mannose 6-phosphate receptors (MPRs) with overlapping, but distinct functions has raised the question of at what stage in the phylogenetic tree the two receptors have occurred for the first time. In this paper, we present a partial cDNA sequence of Mr 300 kDa MPR (MPR 300) from poeciliid fish (Xiphophorus). It contains a 5%-untranslated region followed by the initiator ATG, and an open reading frame that corresponds to cassettes 1–5 and part of cassette 6 of mammalian MPR 300. The size of the mRNA transcript for fish MPR 300 was comparable with that of other vertebrates. The amino acid sequence of fish MPR 300 displays 48 – 52% similarity with mammalian and chicken MPR 300. In particular, all the cysteine residues involved in disulfide bonding and an arginine residue, which is considered to be part of the mannose 6-phosphate binding site in cassette 3 of mammalian MPR 300, are conserved. Sequence similarities were significantly higher within cassette 3 and within cassette 5, to which a ligand-binding function has not yet been ascribed. Sequence similarities of the internal cassettes of MPR 300 are discussed with regard to the multifunctional nature of MPR 300. © 2000 Elsevier Science Inc. All rights reserved. Keywords: cDNA sequencing; Evolution; Fish; Insulin-like growth factor-II receptor; Mannose 6-phosphate receptor; RT-PCR; Vertebrate; Xiphophorus
1. Introduction Lysosomal enzymes are synthesized at the rough endoplasmic reticulum together with secretory proteins. At the trans site of the Golgi apparatus, they must be segregated from the secretory pathway to reach the endosomal compartment and then lysosomes. Targeting of solu* Corresponding author. Tel./fax: + 49-711-5004987. E-mail addresses:
[email protected] (S.K. Nadimpalli),
[email protected] (A. Hille-Rehfeld).
ble lysosomal enzymes into clathrin-coated vesicles of the trans Golgi network has been intensively studied in mammalian cells, where it is mediated by mannose 6-phosphate-specific receptors (MPRs). There are two homologous MPRs with overlapping but distinct functions, which are designated as MPR 46 and MPR 300 according to their apparent molecular mass (for a review, see Kornfeld, 1992; Hille-Rehfeld, 1995). Both MPRs are type I transmembrane proteins. cDNA sequencing of MPR 300 from chicken and mam-
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mals revealed that its extracytoplasmic domain is built by 15 cassettes that share significant sequence similarity with each other and with the single cassette that constitutes the extracytoplasmic domain of MPR 46 (Dahms et al., 1987; Morgan et al., 1987; Pohlmann et al., 1987; Lobel et al., 1988; MacDonald et al., 1988; Oshima et al., 1988; Ko¨ster et al., 1991; Szebenyi and Rotwein, 1994; Zhou et al., 1995). MPR 300 is a multifunctional receptor. Mannose 6-phosphate-containing ligands are bound by cassettes 3 and 9 (Westlund et al., 1991; Dahms et al., 1993). In addition, mammalian MPR 300 binds insulin-like growth factor II (IGF II), whereas chicken and frog MPR 300 are not able to bind IGF II (Canfield and Kornfeld, 1989; Clairmont and Czech, 1989; Dahms et al., 1994; Schmidt et al., 1995; Garmroudi et al., 1996). The high-affinity IGF II-binding site is believed to result from an interaction of cassette 11, which by its own binds IGF II with low affinity, and cassette 13, which is thought to increase the affinity of binding to cassette 11 (Devi et al., 1998). Binding and endocytosis of IGF II by MPR 300 contributes to the regulation of embryonic development in mice. Other ligands of MPR 300 are retinoic acid (Kang et al., 1997) and urokinasetype plasminogen activator receptor (Nykjaer et al., 1998), but the physiological relevance of their binding to MPR 300 is not known yet. Binding of IGF II, retinoic acid and urokinase-type plasminogen activator receptor to MPR 300 is independent of mannose 6-phosphate. The physiological importance of multiple ligand binding to MPR 300 is evident from the fact that MPR 300-deficient mice are not viable. Lethality is apparently due to an impaired regulation of the response to IGF II, as viability of the MPR 300 knock-out mice is rescued by a simultaneous knock-out of IGF II (Filson et al., 1993). In contrast to MPR 300, MPR 46 according to the present knowledge binds mannose 6-phosphatecontaining ligands only. MPR 46-deficient mice are viable regardless of an impaired sorting of lysosomal enzymes, as MPR 300 and other carbohydrate-specific receptors can partly take over the function of MPR 46 (Ludwig et al., 1993; Ko¨ster et al., 1994). In view of the structural homology of the two MPRs and the differences in their physiological functions, it is of special interest to identify their common ancestor and to determine at what stage in the evolution MPR 300 has acquired its repetitive structure.
The occurrence of both MPRs in non-mammalian vertebrates such as bird (chicken), reptiles (garden lizard), amphibia (Xenopus) and fish (Xiphophorus) has been established by biochemical and immunological methods (Matzner et al., 1996; Siva Kumar et al., 1997, 1999). In a recent study, we have identified a Mr 300 kDa mannose 6-phosphate-binding protein from the invertebrate Unio (Udaya Lakshmi et al., 1999). In non-mammalian vertebrates and invertebrates, the machinery of lysosomal enzyme sorting has been poorly studied so far. Lysosomal enzymes of Dictyostelium discoideum were shown to contain methylated mannose 6-phosphate residues, but receptors involved in mannose 6-phosphate-specific sorting in Dictyostelium have not yet been characterized (Mehta et al., 1996, and references cited therein). Sorting of lysosomal enzymes in the unicellular trypanosomes is thought to occur independent of mannose 6-phosphate (Oeltmann et al., 1994; Huete-Pe´rez et al., 1999). As a contribution to understand the evolution of MPRs, we now present a partial cDNA sequence of fish (Xiphophorus) MPR 300. The similarities of all available sequences of MPRs are discussed with regard to their evolution.
2. Materials and methods
2.1. Isolation of total RNA Xiphophorus xiphidium embryonal cells (A2) were grown as described previously (Kuhn et al., 1979). A confluent culture (10 cm Petri dish) was used for isolation of total RNA with the RNeasy kit (Qiagen, Hilden, Germany) according to the manufacturer’s advice. Purity and integrity of the RNA was controlled by agarose (1%) gel electrophoresis under denaturing conditions (Matzner et al., 1996).
2.2. Re6erse transcriptase-polymerase chain reaction The following degenerate primer oligonucleotides were used for amplification of a cDNA fragment: 1s, TGTA/GCACTAC/TTTTGAGTGGAGGAC; and 2as, CAGGCATACTCAGTAAC/TCCACTC. Reverse transcription (RT) was performed with the first-strand cDNA synthesis kit of Pharmacia (Amersham Pharmacia Bio-
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tech, Freiburg, Germany) using Maloney Murine Leukemia Virus reverse transcriptase according to the manufacturers advice. Five micrograms of fish total RNA was denatured at 65°C for 10 min and chilled on ice. After addition of 40 pmol primer 2as, first-strand synthesis was performed at 37°C for 1 h. Then, 50% of the first-strand synthesis product was amplified by polymerase chain reaction (PCR) with 2.5 U Hot Star Taq polymerase (Qiagen) and 40 pmol primers 1s and 2as, at annealing temperature 45°C for 35 cycles. A 500 base pair (bp) RT-PCR product was gel-purified using the QIAquick gel extraction kit (Qiagen) followed by a second round of amplification by PCR. The resulting homogenous 500 bp product was gel-purified and subjected to TA cloning into pCR 2.1 (Invitrogen, Groningen, The Netherlands).
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into lZAP II was a kind gift from M. Schartl (Wu¨rzburg, Germany). For the first screening, 106 plaque forming units were used to infect Escherichia coli LE392 on 20 plates (14 cm diameter). Fifty to 60 plaque forming units were used for infection on a 10 cm plate in the secondary and tertiary screening. After plaque lifting to Hybond N membrane, membranes were exposed for 10 min to 0.5 M NaOH, 1.5 M NaCl followed by 2×10 min in 0.5 M Tris–HCl (pH 7.2), 1 mM ethylenediamine tetraacetic acid, 1.5 M NaCl and a brief rinse with 2 × SSC. UV-cross-linking, pretreatment with hybridization buffer, hybridization of the 32P-labeled probe (diluted in hybridization buffer containing 1 mg/ml pCR2.1 DNA) and washing was carried out as already described for Northern blotting.
2.5. Isolation of Phage DNA 2.3. Northern blot Fifteen micrograms of total RNA from A2 cells was subjected to denaturing agarose (1%) gel electrophoresis (Matzner et al., 1996) and transferred to Hybond N membrane (Amersham). Membranes were exposed to UV light for 15 s and incubated for 1 h at 60°C. Membranes were then incubated for 2–3 h at 42°C in hybridization buffer (100 mg/ml heat-denatured salmon sperm DNA, 40% formamide, 10% dextran sulfate, 1% Denhardt’s solution, 4.8× SSC buffer, 10 mM Tris –HCl (pH 7.4), 1% sodium dodecyl sulfate (SDS)). The cDNA-fragment RTP-f1 was subjected to radiolabeling with the random prime labeling kit (Amersham) and a32PdCTP (11.1× 1013 Bq/ mmol, Amersham). 32P-Labeled RTP-f1 was denatured at 98°C for 5 min before dilution to 37 MBq/ml in hybridization buffer. Hybridization was performed overnight at 42°C. Membranes were washed for 10 min at RT and 30 min at 65°C with 2×SSC containing 0.1% SDS followed by 0.2×SSC containing 0.1% SDS at 65°C (Sambrook et al., 1989). 32P was detected by exposure to Kodak film (XOMAT AR) with intensifying screen.
E. coli LE392 (1.5× 1010 cells in 10 ml) were infected with 5× 108 plaque forming units at 37°C for 30 min. After dilution into 400 ml Langmuir– Blodgett medium, lysis was allowed for 5–6 h at 37°C. Chloroform was added to 0.1% (final concentration). After 10 min at 37°C, the culture supernatant was cleared by centrifugation (2×10 min, 2750× g). DNA was isolated from the supernatant of a 250 ml culture with the Qiagen Lambda Maxi kit according to the manufacturer’s instructions.
2.6. DNA sequencing Dideoxy dNTP dye terminator cycle sequencing was performed according to the manufacturer’s advice (Applied biosystems). Sequence comparisons were performed with the CLUSTALW method available at the Jalview server (http:// jura.ebi.ac.uk:6543/cgi-bin/clustalw.cgi) using the blosum matrix.
3. Results
3.1. Isolation of a partial cDNA encoding fish MPR 300
2.4. Screening of the cDNA library The fish cDNA library PSM derived from Xiphophorus maculatus/Xiphophorus helleri hybrid fish melanoma (Wakamatsu, 1981) and cloned
To amplify a cDNA fragment of fish MPR 300, the available sequences of chicken and mammalian (human, bovine, rat, mouse) MPR 300 were subjected to multiple sequence alignment.
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Fig. 1. Strategy for cDNA cloning and sequencing of fish MPR 300. (A) Primary structure of human MPR 300 (Oshima et al., 1988). The arrow indicates the initiator methionine (ATG). Asterisks indicate stretches of highly conserved nucleotide sequences. 1s, 2as, Position of degenerate primers 1 sense and 2 antisense. (B) cDNA fragments of fish MPR 300 obtained by RT-PCR (RTP-f1), by phage library screening (clones 5, 7, 8) and PCR amplification from phage DNA (PCR-f2). (C) Sequencing strategy. Arrows indicate the length of overlapping sequences.
There were four stretches with conserved cDNA sequences in cassettes 1, 2, 9 and 14, and a conserved stretch within the cytoplasmic domain
Fig. 2. Amplification of a cDNA fragment of fish MPR 300 by RT-PCR. Total RNA of A2 cells was used as a template for first-strand synthesis with the degenerate primer 2as. PCR amplification was performed with primers 1s and 2as at an annealing temperature of 45°C. The PCR products were analyzed by agarose (2%) gel electrophoresis. Lane 1, RT-PCR product; lane 2, standard DNA. cDNA-fragment RTP-f1 corresponds to nucleotides 429–920 of fish MPR 300.
(asterisks in Fig. 1A). From these, two degenerate primers (sense primer 1s and antisense primer 2as) were chosen to amplify a fragment corresponding to nucleotides 447–953 of the human MPR 300 cDNA (RTP-f1; see Fig. 1B). RT-PCR was performed with total RNA from Xiphophorus embryonal cells. When annealing of primers was allowed at 45°C, multiple bands were amplified by RT-PCR, the uppermost fragment of about 0.5 kb being comparable in length with the corresponding human fragment (Fig. 2). Raising the annealing temperature above 45°C to increase specificity of the RT-PCR reaction abolished amplification. Therefore, the 0.5 kb fragment obtained with 45°C annealing temperature was gel-purified for TA cloning into pCR 2.1. Sequencing with vector-derived primers revealed a 492 bp fragment that, at amino acid level, displayed 46–48% similarity with the corresponding fragments of mammalian or chicken MPR 300. In particular, all the cysteines that are involved in disulfide bonding were conserved. When the fishderived RT-PCR fragment was used as a probe for northern blotting with total fish cell RNA, a single band of 13.5 kb was observed (Fig. 3). This result is compatible with the conclusion that the 492 bp RTP-f1 fragment was derived from fish MPR 300 RNA. MPR 300 RNA in mammals and chicken have a 7.4–7.5 kb coding region prolonged to 9.5–11 kb by 3%- and 5%-untranslated regions (Lobel et al., 1987; Oshima et al., 1988;
Fig. 3. Fish MPR 300 mRNA detected by Northern blot: 15 mg total RNA from A2 cells was subjected to denaturing agarose (1%) gel electrophoresis, transferred to Hybond N membrane and hybridized with 32P-labeled RTP-f1.
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Fig. 4. Alignment of the amino acid sequences of cassettes 1– 5 of fish MPR 300. From the partial cDNA sequence of fish MPR 300, cassettes 1 – 5 were selected using the putative signal sequence cleavage site and the conserved motif DLSXL at the carboxyterminal border of each cassette. Cassettes were aligned by the CLUSTALW method. Numbers at the end of each cassette give the carboxyterminal amino acid. Numbers in brackets give the length of each cassette of fish MPR 300 followed by the range of the length of corresponding cassettes of other vertebrate MPR 300. The bottom line shows conserved amino acids (asterisks) and conservative substitutions (dots). Cysteine residues involved in disulfide bonding are shown in bold, potential glycosylation sites are underlined.
Szebenyi and Rotwein, 1994; Matzner et al., 1996). To obtain additional 3%-coding cDNA of fish MPR 300, RTP-f1 was used as a probe to screen a Xiphophorus melanoma cDNA library. Phage clone 8 was found to encode for cassettes 1 – 4 of fish MPR 300 (Fig. 1B). Nucleotides 429 – 920 of the open reading frame of phage clone 8 were 99% identical to the sequence of RTP-f1. The sequence information of phage clone 8 was used to amplify a cDNA-fragment corresponding to nucleotides 1284– 1886 of fish MPR 300 (PCRf2; see Fig. 1B). PCR-f2 was used to rescreen the Xiphophorus library. Phage clones 5 and 7, which exclusively hybridized with PCR-f2 but not with RTP-f1, were selected for sequence analysis (Fig. 1B).
3.2. Characterization of cDNA and deduced amino acid sequence of fish MPR 300 The sequencing strategy is summarized in Fig. 1C. Overlapping sequences were always identical. The available sequence information comprises a 432 bp 5%-untranslated region. The first methionine of the open reading frame is surrounded by a nucleotide sequence (AACATGT) that conforms with the published consensus sequence for an initiator methionine (Kozak, 1981, 1986). The deduced amino acid sequence of the 2632 bp open reading frame corresponds to cassettes 1 – 5 and part of cassette 6 of the reported se-
quences of MPR 300 (cassettes 1–5 are shown in Fig. 4; the complete sequence is available from the EMBL Nucleotide Sequence Database, AJ278449). Cassette 1 is preceded by a hydrophobic signal sequence. The putative signal peptide cleavage site is between position 32 and 33: SGAEK (Nielsen et al., 1997). The carboxyterminal ends of cassettes 1–5 are defined by the conserved motif DLS(P/R/S)L. Cassettes 1–5 of fish MPR 300 show 12–31% similarity with each other.
4. Discussion MPRs are well characterized in mammals and aves. The luminal domain of MPR 46 displays 14–37% similarity to the 15 internal cassettes of MPR 300 as shown for the bovine MPRs (Lobel et al., 1988). This finding led to the assumption that MPR 300 has evolved from MPR 46 by repeated gene duplication events, and raised the question at which stage of evolution MPR 300 has occurred for the first time. First evidence for the presence of MPR 300 in fish was based on biochemical and immunological studies (Siva Kumar et al., 1999). In this paper, we present a partial cDNA sequence of the fish MPR 300. The available sequencing data show that the aminoterminal portion of fish MPR 300 displays significant sequence similarity with chicken (52%) and mammalian MPR 300 (48–50%; Table 1). The significance of these similarities is corroborated by the
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Table 1 Sequence comparison of internal cassettes in vertebrate MPR 300a Cassette
1 2 3 4 5 Partial sequence
Similarity to fish MPR 300 (%)
Function
Chicken
Murine
Rat
Bovine
Human
52 52 60 50 63 52
48 50 55 51 60 50
49 50 57 50 62 50
49 48 55 46 61 48
52 48 56 48 62 50
M6P binding
a
Cassettes were selected using the conserved motif DLXXL that defines the carboxyterminal border of each cassette, and sequence comparison was performed with the CLUSTALW method. Partial sequence refers to the total available fish sequence including the signal sequence (877 amino acids) compared with the corresponding portion of other vertebrate MPRs.
fact that fish MPR 300 shares typical structural features with mammalian and chicken MPR 300: First, the aminoterminal portion of fish MPR 300 is divided into cassettes that show similar length as their chicken and mammalian counterparts (Fig. 4). Second, the carboxyterminal border of each cassette is defined by the conserved motif DLS(P/ R/S)L, which strongly resembles the corresponding sequences found in mammalian and chicken MPRs (DLXXL). Third, all the cysteines that have been suggested to form disulfide bonds in bovine MPR 300 (Lobel et al., 1988) are present in all vertebrate species studied so far, including fish. In most instances, the amino acid sequences flanking a conserved cysteine show a remarkably high degree of similarity among all vertebrate species. Fourth, five out of six potential glycosylation sites
found in cassettes 1–5 of fish MPR 300 are conserved in chicken and mammals. Only cassette 4 of mammalian MPR 300 contains two additional glycosylation sites that are not present in fish or chicken MPR 300. Taken together, these data indicate that the cDNA sequence presented in this paper encodes for fish MPR 300. Cassettes 3 and 9 of bovine MPR 300 have been shown to contain two independent binding sites for mannose 6-phosphate-carrying ligands. Binding of mannose 6-phosphate depends on critical arginine residues, R435 in cassette 3 and R1334 in cassette 9 (Dahms et al., 1993). Fish MPR 300 contains a corresponding arginine (R422) in cassette 3, which is surrounded by the highly conserved motif CSSGFQRM(T/S)(I/V)INF(Q/E)C (bold letters in Fig. 5).
Fig. 5. Alignment of the amino acid sequences of cassette 3 of vertebrate MPR 300. Cassette 3 was selected from sequences of chicken (Zhou et al., 1995), mouse (Szebenyi and Rotwein, 1994), rat (MacDonald et al., 1988), bovine (Lobel et al., 1988) and human (Oshima et al., 1988) MPR 300, making use of the conserved motif DLXXL that defines the carboxyterminal end of cassettes. Sequence alignment was performed with the CLUSTALW method. The location of cassette 3 within the amino acid sequence of each species is given at the end. The bottom line shows conserved amino acids (asterisks) and conservative substitutions (dots). The conserved motif surrounding the arginine residue, which is critical for mannose 6-phosphate binding, is shown in bold.
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Fig. 6. Sequence comparison of internal cassettes of vertebrate MPR 300. Cassettes were selected using the conserved motif DLXXL that defines the carboxyterminal border of each cassette, and sequence comparison was performed with the CLUSTALW method. Values are the mean similarity of cassettes from available vertebrate sequences (mouse, rat, bovine, human) compared with chicken. Bars indicate the range of similarity. Arrows indicate binding of mannose 6-phosphate in cassettes 3 and 9, and of IGF II in cassette 11.
When the sequences of individual cassettes are compared between fish and other vertebrate phyla, similarities are most remarkable for cassettes 3 (55–60%) and 5 (60 – 63%), whereas cassettes 1, 2 and 4 display only 46 – 52% similarity (Table 1). For cassette 3, the high degree of similarity among vertebrates may reflect the presence of critical structural determinants for binding of mannose 6-phosphate-containing ligands. For cassette 5, no ligand-binding function has yet been described. We therefore asked whether, for the other cassettes of vertebrate MPR 300, the degree of similarity correlates with known ligand binding functions. For this purpose, all cassettes were compared with those of bird (chicken) which, among the phyla studied so far, is closest to fish in the evolutionary tree (Fig. 6). The average similarity of cassettes was 57.8% compared with chicken. Remarkably high similarity was observed for cassette 5 (65–69%), and to a somewhat lower extent for cassettes 12, 14 and 15 (60 – 64%). In agreement with earlier reports (Zhou et al., 1995), similarity was lowest for cassette 11 (44 – 47%), which is in line with the observation that chicken MPR 300 does not bind IGF II while, in mammalian MPR 300, cassette 11 binds IGF II. Cassettes 3 and 9, which contain the mannose 6-phosphate binding site, show average similarity (54 – 64%). It may be interesting to speculate whether the high degree of conservation of cas-
settes 5, 12, 14 and 15 reflects the presence of ligand binding sites, e.g. for retinoic acid (Kang et al., 1997), urokinase-type plasminogen activator receptor (Nykjaer et al., 1998) or other still unknown substances. The similarities of individual cassettes of fish MPR 300 to the corresponding cassettes of the other vertebrate phyla is always significantly higher (40–60%) than the similarities among cassettes 1–5 of fish MPR 300 (12–31%). This observation supports the notion that the cassettes of MPR 300 have evolved by gene duplication and diversification a long time before fish have been separated from other vertebrate phyla. In this context, it is interesting to note that we have recently presented preliminary evidence for the presence of MPR 300 in the invertebrate mollusc Unio. To further understand the evolution of MPRs, it will be interesting to investigate the presence and structure of MPR 300 in additional phyla that mark critical points of divergence within the evolutionary tree.
Acknowledgements The authors are indepted to Prof. Schartl (Wu¨rzburg, Germany) for providing the fish cDNA library. Y.U.L. wishes to thank Dr Thomas Dierks, Dr Christian Ko¨rner, Dr Bern-
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hard Schmidt and Dr Paul Saftig (Go¨ttingen, Germany) for valuable experimental suggestions, and to Dr Enno Hartman, Go¨ttingen, for helpful discussion. Work was supported by the Deutsche Akademische Austauschdienst by a grant to Y.U.L. (A/97/00801) and the Deutsche Forschungsgemeinschaft (SFB 525).
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