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Origin of Insulin Receptor-Like Tyrosine Kinases in Marine Sponges.

Introduction

The Porifera [sponges] are the oldest metazoan phylum; they existed 40 to 50 million years prior to the onset of the "Cambrian Explosion" (Valentine et al., 1996), the time of main divergence of metazoan phyla (Valentine, 1994). Highly conserved amino acid (aa) sequences in sponges indicate that the Porifera share one common ancestor with other metazoan phyla (Mtiller et al., 1994; also see Mtiller, 1995, 1997, and 1998). These sequences include those (i) for transmembrane receptors, e.g., transmembrane tyrosine kinase [TK] receptors [RTKs] (Muller and Schacke, 1996); (ii) for transmembrane adhesion molecules, e.g., the integrins (Pancer et al., 1997a); and (iii) for G-protein linked transmembrane receptors for signaling molecules, e.g., the metabotropic glutamate receptor (Perovic et al., 1999). Additional sequences from homeodomain transcription factors show that the transcriptional control of gene expression in the oldest Metazoa is similar to that of the most recent phyla (Seimiya et al., 1994; Richelle-Maurer et al., 1998; Coutinho et al., 1998). One metazoan autapomorphic character restricted to Porifera is the presence of high telomerase activity in all (or almost all) cells, including somatic cells (Koziol et al., 1998).

The discovery that sponges contain transmembrane (Schacke et al., 1994a), cytoplasmic (Ottilie et al., 1992), and nuclear TKs (Cetkovic et al., 1998) suggests that the signaling system in these animals is sophisticated enough to respond to peptide growth factors and to cell adhesion (Muller and Muller, 1999). The catalytic domain of the RTKs is related to that of the cytoplasmic protein tyrosine kinases [PTKs] and the Ser/Thr kinases (Hanks and Hunter, 1995; Kruse et al., 1997). The catalytic domain of the TKs is subdivided into 12 smaller subdomains, the first eight of which are most highly conserved (Hardie and Hanks, 1995). In addition to the characteristic tyrosine protein kinase-specific active-site signature, the previously described catalytic domain of the RTK from the demosponge Geodia cydonium contains no further site that marks this molecule as belonging to a specific class of RTKs (Schacke et al., 1994a). In this study, we have demonstrated for the first time that one distinct subfamily of the RTKs is already present in all three classes of Porifera, and that it contains the TK class II signature with the consensus pattern D-[LIV]-Y-[x.sub.3]-Y-Y-R (PC/GENE, 1995 [Prosite]). By choosing appropriate primers for the polymerase chain reaction, sequences were obtained from sponges that must be grouped with the insulin receptors [InsRs] of vertebrates (Ullrich et al., 1985), the insulin-like growth factor I receptors [IGF-I-Rs] of vertebrates (Ullrich et al., 1986), the InsR-related receptors of vertebrates (Shier and Watt, 1989), and the InsR homolog from Drosophila melanogaster (Fernandez et al., 1995). These molecules are all members of the class II RTKs which display, within subdomain VII, the following consensus for InsRs, GF-I-Rs, and InsR-homologs R-D-[IV]-Y-E-[TS]-D-Y (Hardie and Hanks, 1995).

Here we present the TK domains of InsR-(like) molecules that have been isolated from the hexactinellid sponge Aphrocallistes vastus, the demosponge Suberites domuncula, and the calcareous sponge Sycon raphanus. From S. raphanus, three full-length clones from the InsR-like molecules are given. All of the sequences were used for phylogenetic analyses. These revealed that the sponge InsR-like molecules are statistically significantly distinct from the related molecules of higher Metazoa, and allowed an assessment of the evolutionary order in which the three classes of Porifera appeared.

Materials and Methods

Materials

Restriction endonucleases and other enzymes for recombinant DNA techniques and vectors were obtained from Stratagene (La Jolla, CA; USA), QIAGEN (Hilden; Germany), Boehringer Mannheim (Mannheim; Germany), GibcoBRL (Grand Island, NY; USA), Amersham (Buckinghamshire; UK), USB (Cleveland, OH; USA), DUPONT (Bad Homburg; Germany), Epicentre Technologies (Madison, WI; USA), and Promega (Madison, WI; USA). Taq DNA polymerase, DIG [digoxigenin] DNA labeling kit, DIG-11-dUTP, anti-DIG AP Fab fragments, and CDP [disodium 2-chloro-5-(4-methoxyspiro {1,2-dioxetane-3,2[prime](5[prime]-chloro)-tricyclo[[3.3.1.1.sup.3,7]]decan)-4-yl)phenyl phosphate] were from Boehringer Mannheim (Mannheim; Germany).

Sponges

Live specimens of Sycon raphanus [Schmidt] (Porifera, Calcarea, Calcaronea, Leucosoleniida, Sycettidae) and Suberites domuncula [Olivi] (Porifera, Demospongiae, Tetractinomorpha, Hadromerida, Suberitidae) were collected from the Adriatic Sea near Rovinj (Croatia). The specimens of Aphrocallistes vastus [Schulze] (Porifera, Hexactinellida, Hexasterophora, Hexactinosida, Aphrocallistidae) were collected from Saanich Inlet and Barkley Sound, British Columbia (Canada) by scuba diving. They were a gift of Dr. Sally P. Leys (Department of Biology, University of Victoria, P.O. Box 1700, Victoria, BC, Canada). The material was immediately frozen in liquid nitrogen until use.

Construction of cDNA library from A. vastus

Total RNA was extracted from sponge tissue, and poly-adenylated mRNA was isolated from total RNA as already described (Pfeifer et al., 1993a and b). cDNA was prepared with a ZAP Express cDNA synthesis kit. The cDNA library of A. vastus was prepared in Hybri ZAPII (Stratagene) and packaged in vitro with the MaxPlax Packaging Extract (Epicentre Technologies). The library contained approximately 2.4 X [10.sup.6] independent plaque forming units (pfu); the amplified library was stored at 4 [degrees] C.

Screening and isolation of the cDNAs encoding InsR-like molecules

The complete cDNAs as well as those encoding the catalytic domains were cloned by the polymerase chain reaction (PCR) from the A. vastus cDNA library (see above), the S. domuncula (Kruse et al., 1997), or the S. raphanus cDNA libraries (Kruse et al., 1997). The degenerate sense primer 5[prime]-TTYGGIATGGTITAYGARGG-3[prime] (Y = pyrimidine, R = purine, I = inosine) and the downstream primer (anti sense) 5[prime]-TARTARTCIGTYTCRTADATRTC-3[prime] were designed against the conserved regions of TK subdomain I (FGMVYEG) and TK subdomain VII (DIYETDY) of InsRs as well as IGF-I-Rs from mammalian species; these regions are different from the corresponding protein kinases of other classes (Scavo et al., 1991). The two primers define a 470-490 bp long sequence encoding part of the TK catalytic domain [ILLUSTRATION FOR FIGURE 1 OMITTED]. The PCR was carried out using a GeneAmp 9600 thermal cycler (Perkin Elmer), with an initial denaturation at 95 [degrees] C for 3 min, then 35 amplification cycles each at 95 [degrees] C for 30 s, 50 [degrees] C for 45 s, 72 [degrees] C for 1.5 min, and a final extension step at 74 [degrees] C for 10 min. The reaction mixture of 50[[micro]liter] included 20 pmol of the respective degenerate primer and 10 pmol of the primer T7 (Stratagene), 200 [[micro]molar] of each nucleotide, 1 [[micro]liter] of the respective cDNA libraries, buffer, and 2.5 units of Taq DNA polymerase. The expected amplified products were purified and concentrated using Geneclean Spin Kit and directly ligated into pGEM-T vector. After isolation and purification, the plasmid DNAs were sequenced with an automatic DNA sequenator [Li-Cor 4200].

The TK catalytic domains of the three S. raphanus InsR-like molecules were used and completed by both 5[prime]- and 3[prime]-RACE, using the kits "5[prime]-" and "3[prime]-RACE System" to full-length cDNAs.

Sequence analyses

Sequences were analyzed using PC/GENE, release 14.0, from IntelliGenetics, Mountain View, CA (USA). Similarity searches and sequence retrieval were performed via the e-mail servers at the European Bioinformatics Institute, Hinxton Hall, UK (BLITZ and FASTA), and the National Institutes of Health,

Bethesda, MD, USA (BLAST). The phylogenetic tree was constructed from an aa alignment by the neighbor-joining method (Saitou and Nei, 1987) applying the PHYLIP package version 3.5c program (Felsenstein, 1993). The degree of support for internal branches was further assessed by bootstrapping. The distance matrix was calculated as described (Dayhoff et al., 1978). Multiple alignments were performed with CLUSTAL W version 1.6 (Thompson et al., 1994) and their graphic presentations by the program GeneDoc (Nicholas and Nicholas, 1997).

Northern blot

RNA was extracted from liquid-nitrogen-pulverized sponge tissue with TRIzol Reagent (GibcoBRL) as recommended by the manufacturer. Total RNA (1 [[micro]gram]) was electrophoresed through formaldehyde/agarose gel and blotted onto Hybond N+ membrane following the manufacturer's instructions (Amersham). Hybridization experiments were performed with the probes SRINR1, SRINR2, or SRINR3 [[approximately equal to]600 bp segments] from S. raphanus. These probes were labeled with DIG-11-dUTP by the DIG DNA labeling kit. Hybridization was performed with the anti sense DIG-labeled probes at 42 [degrees] C overnight using 50% formamide containing 5xSSC, 2% blocking reagent [Boehringer], 7% [w/v] SDS, and 0.1% [w/v] N-lauroylsarcosine, following the instructions of the manufacturer [Boehringer]. After washing, DIG-labeled nucleic acid was detected with anti-DIG Fab fragments [conjugated to alkaline phosphatase] and visualized by a chemiluminescence technique using CDP, the chemiluminescence substrate for alkaline phosphatase, according to the instructions of the manufacturer [Boehringer].

Results

Cloning and sequencing the cDNAs encoding the InsR-like molecules

The S. domuncula nt sequence, SDINR, is 491 nt long and has a potential open reading frame [ORF] of 489 bases encoding a deduced protein sequence of 163 aa residues. The sequence from A. vastus, AVINR, is 490 nt long with an ORF of 489 nt (163 aa).

Three putative sequences of InsR-like molecules were isolated from the cDNA library of S. raphanus. The cDNA for type 1 InsR, SRINR1, is 2026 nt long with an ORF of 1848 nt encoding a putative sequence of 616 aa [ILLUSTRATION FOR FIGURES 1 AND 2 OMITTED]; type 2 InsR, SRINR2, is 2150 nt long with an ORF of 1842 nt (614 aa); and type 3 InsR [ILLUSTRATION FOR FIGURE 2 OMITTED], SRINR3, is 1433 nt long with an ORF of 1368 nt (456 aa) [ILLUSTRATION FOR FIGURE 2 OMITTED]. Northern blot analyses were performed with these S. raphanus cDNA probes. One band each of approximately 2.2 kb (type 1), 2.3 kb (type 2), and 1.6 kb (type 3) were obtained, confirming that the full-length cDNAs were isolated [ILLUSTRATION FOR FIGURE 3 OMITTED].

Deduced aa sequences of the catalytic domains of the putative sponge InsRs

The deduced aa sequences of the catalytic domains of the InsR-like sequences between subdomains I to VII have been aligned [ILLUSTRATION FOR FIGURE 1 OMITTED]. The borders of subdomains I to VII (according to Hardie and Hanks, 1995), could be defined for all sponge sequences unequivocally [ILLUSTRATION FOR FIGURE 1 OMITTED]. Specific sites and sequence characteristics were also present as outlined earlier (Muller and Schacke, 1996): in subdomain I, the ATP-binding site [consensus: GxGxxGxV; but in the hexactinellid INR_AV sequence G is replaced by R]; within subdomain II, the residue Lys in the consensus VAxK, which is required for kinase activity; within subdomain Vib: the aa D [Asp] and N [Asn] as well as in subdomain VII: the DFG tripeptide is present. The DFG segment has been implicated in ATP binding (Hanks et al., 1988) and represents the most conserved portion within the catalytic domain. The tyrosine residue (Y) in subdomain VII (aa no. 180 of the catalytic domain, with respect to the G. cydonium RTK) undergoes phosphorylation and is the tyrosine kinase phosphorylation site. Signatures within subdomains VIII, IX, X, and XI are generally less well conserved. Therefore, the PCR-based sequencing was restricted to the part within subdomains I to VII. The TK-specific active-site signature, D-L-A-T/A-R-N, characteristic for both vertebrate and invertebrate TKs (Ottilie et al., 1992; Hanks et al., 1988) is found in subdomain Vib. Within the subdomain VII the signature for the TK class II receptors with the consensus pattern is found, D-[LIV]-Y-x3-Y-Y-R (PC/GENE, 1995 [Prosite]).

The PCR primers were chosen to identify, in sponges, those catalytic domains of class II RTKs that share the highest similarity to InsRs, IGF-I-Rs, to InsR-related receptors, and to the insulin receptor homolog from D. melanogaster (Fernandez et al., 1995). These receptors have the consensus within the class II signature of R-D-[IV]-Y-E[TS]-D-Y (Hardie and Hanks, 1995). As seen in Figure 1, this consensus is, as expected, present in all sponge sequences; therefore the sequences from the demosponge S. domuncula, the calcareous sponge S. raphanus, and the hexactinellid sponge A. vastus were termed InsR-like molecules.

Complete aa sequences of the InsR-like sequences from S. raphanus

Three cDNAs encoding complete putative InsR-like sequences from S. raphanus have been isolated from the library. The sequences are termed type 1, SRINR1, type 2, SRINR2, and type 3, SRINR3, InsR-like molecules. The putative 616 aa sequence INR_SR1 (deduced from SRINR1) has a calculated [M.sub.r] of 69,477; INR_SR2 of 614 aa has an Mr of 69,213, and INR_SR3 of 456 aa has an Mr of 51,259.

The sequence INR_SR2 was selected for the analysis given here. The transmembrane segment, determined according to the program "RAOARGOS" (PC/GENE, 1995) ranges from aa181 to [aa.sub.196]. The intracellular domain is, as in other RTKs (Hardie and Hanks, 1995), divided into a juxtamembrane domain ([aa.sub.197] to [aa.sub.242]) and the catalytic domain [TK domain] ([aa.sub.243] to [aa.sub.521]) [ILLUSTRATION FOR FIGURE 2 OMITTED]. The catalytic domain is subdivided into 12 subdomains and contains the characteristic TK-specific active-site signature and the RTK class II signature (see above); in addition, the putative ATP-binding site (Hanks et al., 1988) is present [ILLUSTRATION FOR FIGURE 2 OMITTED].

The extracellular domain contains one calcium-binding, epidermal growth factor receptor [EGF]-like domain that reads D-x-N-E-[C.sup.1]-D-[x.sub.5]-[C.sup.2]-D-E-[C.sup.3]-Q-N-[C.sup.4]-x-N-[x.sub.6]-[C.sup.5]-xN-[x.sub.3]-[C.sup.6]-D; it is located from [aa.sub.129] to [aa.sub.162] [the Cys residues are numbered consecutively]. This EGF-like domain consists of six Cys residues, flanked by aa with carbonyl oxygen atoms, which are arranged slightly differently from those found in molecules from higher Metazoa. In particular, the [Cys.sup.4] and [Cys.sup.5] are separated by more than one aa (Bork et al., 1996). Furthermore, an incomplete EGF-like domain is present from [aa.sub.49] to [aa.sub.128]. The two other types of InsR-like molecules from S. raphanus also have two EGF-like domains, and they are similarly arranged. This finding is the first demonstration that EGF-like domains are present in the lowest metazoan phylum. Until now, this domain, which is widely found in vertebrate receptors - e.g., mammalian epidermal growth factor receptors (Geer et al., 1994) and matrix proteins like fibulin (Pan et al., 1993) - has only been identified among invertebrates in Caenorhabditis elegans (Campbell and Bork, 1993).

Phylogenetic analyses

When the deduced aa sequences of the TK catalytic domains from the three sponge species were analyzed using the programs BLITZ, FASTA, and BLAST, they displayed highest similarity to the polypeptides from both invertebrates and vertebrates. Among invertebrates, these domains were most similar to the insulin-like receptors from the insects Aedes aegypti and D. melanogaster, as well as to the insulin receptor of the mollusc Aplysia californica. In addition an InsR-homolog sequence isolated, so far, from one cephalochordate, Branchiostoma lanceolatum, as well as InsRs, IGF-I-Rs, or InsR-homologs from selected vertebrates (human, mouse and rat) were highly similar to the sponge sequences. They share about 40%-45% of identical aa and about 60%-65% of similar aa (including identical aa) with the selected corresponding molecules. Taking only the sponge sequences, the sequence from S. raphanus, type 1, is identical in 67% of the aa (similarity of 78%) within the catalytic domain with A. vastus and in 69% (79%) with S. domuncula. The finding that the three sequences obtained from S. raphanus differ considerably from each other is interesting; type 1 shares only 75% identical aa (similarity 86%) with type 2 and only 79% identical aa (similarity 88%) with type 3.

The phylogenetic tree was constructed and rooted with the sequence of the catalytic domain of the Fes/FER nonreceptor TK domain from S. raphanus (Cetkovic et al., 1998; [ILLUSTRATION FOR FIGURE 4A OMITTED]). All sequences used were cut for the alignment to obtain the 12 subdomains, comprising approximately 300 aa. All of the sponge sequences fall into one branch of the tree, whereas the selected sequences of InsRs, IGF-I-Rs, or InsR-related sequences from invertebrates and vertebrates are grouped together into a second one. This relationship is statistically very robust as analyzed by bootstrapping. Hence, support for monophyly of Porifera can be deduced. In consequence, the presented findings, based on the data obtained with the catalytic domains of the InsR-like molecules from sponges, shed new light on the assumed uncertain position of sponges as reviewed by Rodrigo et al. (1994). In addition, the data given do not support earlier notions which suggested that the phylum Porifera might be paraphyletic (Cavalier-Smith et al., 1996).

Rate of evolution of the catalytic domains of sponge InsR-like molecules

Use of our data collected on the percentage of aa identity among the polypeptide sequences from the different sponge species on one side and the sponge sequences in comparison to those from higher metazoan allows a relative approach to determining the time of divergence of the sponge classes from a common ancestor. This estimation, which is based on the number of point mutations per 100 aa within given polypeptides, might reflect the time of divergence of two taxa. The evolutionary rates - expressed as [k.sub.aa]-values - vary between different proteins (Zuckerkandl and Pauling, 1965; Kimura, 1983; Li et al., 1987). In a previous study, the galectin protein from the sponge G. cydonium (Pfeifer et al., 1993b) was calculated to have an estimated evolutionary rate of 0.97 x [10.sup.-9] aa substitutions/site/year (Hirabayashi and Kasai, 1993); a value of 1.24 x [10.sup.-9] was calculated for the RTK from G. cydonium (Schacke et al., 1994b) from the same animal.

Dating based on the molecular clock is inaccurate because its rate often varies. If we accept this insecurity, reject the estimated evolutionary rate from sponge genes, and accept the one calculated from the time of protostomedeuterostome divergence - 700 MYA (Dayhoff 1978) - we can postulate the time of separation of the sponges from the common metazoan ancestor, as follows. If we take the calculated [k.sub.aa]-value for the human to D. melanogaste (0.46) as a reference for the protostome-deuterostome split, then the hexactinellid sponge A. vastus branched off 1400 MYA ([k.sub.aa]-value of 0.92), followed by the demosponge S. domuncula 1300 ([k.sub.aa]-value of 0.84) and the calcareous sponge S. raphanus 1200 MYA for type 1 and 2 ([k.sub.aa]-value of 0.80) and for type 3 1100 MYA ([k.sub.aa]-value of 0.77). Recent fossil data show (Li et al., 1998) that sponges existed in much their present form 580 MYA [ILLUSTRATION FOR FIGURE 4B OMITTED].

Discussion

We have shown that all three classes of the phylum Porifera express molecules related to InsR; and these molecules display, in their extracellular domains, EGF-like sequences (as shown here for S. raphanus). This finding implies that animals of the lowest metazoan phylum already contain growth factor receptors that allow them to react to nutrient cues and also to neighboring, individual cells, with a complex intracellular signaling reaction. The InsR-homologs, which are putative transmembrane receptors, presumably allow the transduction of signals through the cellular membrane. Usually signaling by RTKs involves ligand-mediated receptor dimerization (Geer et al., 1994), a process that has not yet been studied in Porifera. InsRs, IGF-I-Rs, and InsR-related receptors or InsR-homologs of higher metazoan taxa do not contain, in their extracellular loops, EGF-like domains, but rather cysteine-rich regions (Geer et al., 1994). This finding underlines again previous findings, that most polypeptides deduced from the cDNA sequences of sponges are assembled by an unusually large variety of modules. For one example, the putative sponge aggregation receptor is composed of scavenger receptor cysteine-rich domains as well as of short consensus repeats (Pancer et al., 1997b; Blumbach et al., 1998) in a structural complexity not known in higher Metazoa.

From the evolutionary point of view, the present contribution makes three points. First, it establishes that molecules similar to the InsR-homologs have evolved prior to the "Cambrian Explosion." Suga et al. (1997) suggested that most of the PTK subfamilies, including InsRs, diverged by domain shufflings, together with gene duplications before the diploblast-triplobast split. As a result of recent findings that the Porifera already existed before this event (Li et al., 1998), we can assume that this class of key molecules, involved in the complex network of intracellular signaling, could have been one major driving force that allowed the other metazoan phyla to arise. Second, the phylogenetic analyses confirm that, based on the autapomorphic character for Metazoa, the RTKs, sponges as a taxon are monophyletic; the Hexactinellida have been calculated to be the oldest class, followed by the Demospongia and finally by the Calcarea. Third, EGF-like domains are already present in sponges, where they were inserted into potential cell surface receptors and also into matrix molecules.

Acknowledgments

This work was supported by grants from the Deutsche Forschungsgemeinschaft [Mu 348/12-1] and from the International Human Frontier Science Program [W. E.G. Muller; RG-333/96-M].

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Author:Skorokhod, Alexader; Gamulin, Vera; Gundacker, Dietmar; Kavsan, Vadim; Muller, Isabel M.; Muller, We
Publication:The Biological Bulletin
Geographic Code:1USA
Date:Oct 1, 1999
Words:5061
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