Báo cáo Y học: Ascidian arrestin (Ci-arr), the origin of the visual and nonvisual arrestins of vertebrate pdf

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Báo cáo Y học: Ascidian arrestin (Ci-arr), the origin of the visual and nonvisual arrestins of vertebrate pdf

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PRIORITY PAPER Ascidian arrestin (Ci-arr), the origin of the visual and nonvisual arrestins of vertebrate Masashi Nakagawa 1 , Hidefumi Orii 1 , Norihiro Yoshida 2 , Eri Jojima 3 , Takeo Horie 1 , Reiko Yoshida 1 , Tatsuya Haga 3 and Motoyuki Tsuda 1 1 Department of Life Science, Graduate School of Science, Himeji Institute of Technology, Kamigori, Akoh-Gun, Hyogo, Japan; 2 Department of Neurochemistry, Faculty of Medicine, The University of Tokyo, Bunkyo-ku, Japan; 3 Institute for Biomolecular Science, Faculty of Science, Gakushuin University, Toshima-ku, Tokyo, Japan Arrestin is one of the key proteins for the termination of G protein signaling. Activated G protein-coupled receptors (GPCRs) are specifically phosphorylated by G protein- coupled receptor kinases (GRKs) and then bind to arrestins to preclude the receptor/G protein interaction, resulting in quenching of the following signal transduction. Vertebrates possess two types of arrestin; visual arrestin expressed exclusively in photoreceptor cells in retinae and pineal organs, and b-arrestin, which is expressed ubiquitously. Unlike visual arrestin, b-arrestin contains the clathrin- binding domain at the C-terminus, responsible for the agonist-induced internalization of GPCRs. Here, we isolated a novel arrestin gene (Ci-arr) from the primitive chordate, the ascidian Ciona intestinalis larvae. The deduced amino acid sequence suggests that Ci-Arr be closely related to vertebrate arrestins. Interestingly, this arrestin has the feature of both visual and b-arrestin. Whereas the expression of Ci-arr was restricted to the photoreceptors in the larvae similarly to visual arrestin, the gene product, containing the clathrin-binding domain, promoted the GPCR internal- ization in HEK293tsA201 cells similarly to b-arrestin. The phylogenetic tree shows that Ci-Arr is branched from a common root of visual and b-arrestins. Southern analysis suggests that the Ciona genome contains only one gene for the arrestin family. These results suggest that the visual and b-arrestin genes were generated by the duplication of the prototypical arrestin gene like Ci-arr in the early evolution of vertebrates. Keywords: arrestin; Ascidian; photoreceptors; internali- zation. G protein-coupled receptors (GPCRs) transduce a wide variety of external stimuli including light, odors, hormones, and neurotransmitters. Upon stimulation by these extra- celluar signals, GPCRs promote the activation of heterotri- meric G proteins by catalyzing the exchange of GDP for GTP on the G protein a-subunit, followed by initiation of the intracelluar signal transduction cascade. The active form of GPCR must be inactivated within a proper time range for cells to adapt to the changing environment. A two-step process is involved in the inactivation mechanism. First the activated GPCR is specifically phosphorylated by G protein-coupled receptor kinase (GRK). Subsequently, a soluble regulatory protein, arrestin, binds with high affinity to the phosphorylated receptor to sterically inhibit the interaction of the receptor with G protein, resulting in the shutting-down of the downstream signaling [1–4]. Vertebrate arrestins can be divided into two classes; visual arrestins and nonvisual, b-arrestins. Visual arrestins are composed of rod- and cone-arrestins, both of which are expressed exclusively in photoreceptor cells in the retina and pineal organs and are thought to play a role in the regulation of photo-signal transduction. Alternatively, b-arrestins, which can be subdivided into b-arrestin1 and b-arrestin2, are expressed ubiquitously and regulate various GPCRs [4,5]. Some agonist-activated GPCRs are translocated from the cell surface membrane to intracellular compartments. This phenomenon is referred to as internalization or sequestra- tion. b-Arrestin, but not the visual arrestins, plays a central role in this internalization. b-Arrestin bound to the phos- phorylated receptor recruits other key proteins, clathrin and the AP2 complex, via distinct binding sites which are conserved in the C-terminus of b-arrestin, leading to endocytosis of the GPCRs [6–10]. Recent evidence showed that b-arrestin is also involved in the switching from the classical G protein mediated signaling to a different signaling pathway, involving the MAPK cascades, where b-arrestin functions both as an adaptor and a scaffold [11–13]. Ascidians, sea squirts, belong to the phylum Protochor- data, which is thought to be a prototype of the vertebrate group. Unlike the sessile adult, the larva is tadpole shaped Correspondence to M. Nakagawa, Department of Life Science, Graduate School of Science, Himeji Institute of Technology, 3-2-1 Koto, Kamigori, Akoh-Gun, Hyogo 678-1297, Japan. Fax: +81 791 58 0197, Tel.: + 81 791 58 0195, E-mail: nakagawa@sci.himeji-tech.ac.jp Abbreviations: GPCR, G protein-coupled receptor; b 2 -AR, b 2 -adrenergic receptor. Note: The nucleotide sequence reported in this paper has been deposited in the DDBJ/EMBL/GenBank under the accession number AB052668. (Received 23 June 2002, revised 18 August 2002, accepted 9 September 2002) Eur. J. Biochem. 269, 5112–5118 (2002) Ó FEBS 2002 doi:10.1046/j.1432-1033.2002.03240.x and possesses some of the features typical of a vertebrate, including a dorsal tubular central nervous system and a notochord underlying the caudal neural tube [14–16]. Thus, ascidians are attractive animals for researchers who are interested in the early processes of vertebrate evolution. In this study, we isolated cDNA encoding arrestin (Ci- arr) from the larvae of the ascidian Ciona intestinalis.The deduced amino acid sequence suggests that Ci-arr is more closely related to vertebrate arrestins than to other inver- tebrate ones. Interestingly, this arrestin possesses character- istics of both visual and b-arrestin; the gene is expressed only in the photoreceptor of the ocellus, but promotes agonist- induced internalization in the cell culture HEK293tsA201. We will discuss the relationship between the diversity and function of the arrestin family. MATERIALS AND METHODS Cloning and sequencing of Ci-arr cDNA cDNA was synthesized from Ciona larvae mRNA with First-strand cDNA Sythesis Kit (Amersham Pharmacia Biotech). The cDNA was amplified by PCR using a set of degenerate primers for the conserved region among various arrestins: the forward primer (5¢-TG AAGCTTYMGITAY GGIMGIGARGA-3¢: underline is HindIII site) and reverse primer (5¢-AGG AGATCTTGIARCATIACISWRCAN GG-3¢: underline is BglII site) corresponded to the amino acid sequences FRYGRED and PCSVMLQ, respectively. Finally, based on the nucleotide sequence of the PCR products, specific primers were synthesized and used for 5¢-and3¢-RACE. Based on the sequence of 5¢-and3¢- flanking region of ORF of Ci-arr (Ar-full-N (5¢-CTGT G CTCGAGTTTGTACTCTGTCTAAC-3¢: underline is XhoI site) and Ar-full-C (5¢-ACA GGATCCAACAT TTTGTGTAATATTT-3¢: underline is BamHI site) was synthesized. The cDNA library of Ciona larvae on kZAPII (a generous gift from T. Iwasa (Muroran Institute of Technology, Japan)) was amplified using them and cloned into pBluescript SKII + using XhoIandBamHI sites. To eliminate PCR errors, several cDNA clones covering the coding region were isolated and sequenced on both strands. To analyze the expression levels of two isoforms, semi- quantitative RT-PCR was performed using a set of primers, Ar-ImunoFw (5¢-GCAGATCTGGACCCAATCATAGG TTC-3) and Ar-full-C. Whole-mount in situ hybridization A full-length Ci-arr cDNA was used as a template to synthesize digoxigenin-labeled antisense RNA probe. Whole-mount in situ hybridization was performed accord- ing to the procedure described by S. Wada [17]. Signals were detected by 1/8 of AP substrate tablet Red of Multi color Detection Set (Boehringer Mannheim) solubilized in 1 mL of Tris/Mg/NaCl buffer [100 m M Tris/HCl (pH 9.5), 50 m M MgCl 2 ,100m M NaCl]. Sequence data source Sequence data used in the present analyses were taken from GenBank, EMBL, SWISS-PROT or NCBI databases, with following accession numbers: human rod (P10523), cone (P36575), b-arrestin1 (P49407), and b-arrestin2 (P32121); bovine rod (P08168), b-arrestin1 (P17870), and b-arrestin2 (P32120); mouse rod (P20443), rat rod (P15887), b-arrestin1 (P29066), and b-arrestin2 (P29067); bullfrog rod arrestin (X92399); leopard frog rod (X92398) and cone (X92400) arrestins; clawed frog rod (U41623) and cone (L40463) arrestins; rainbow trout red blood cell arrestin (P51466); killifish rod1 (AB002554), rod2 (AB029392), and cone (AB002555) arrestins; fruit fly arrestin1 (P15372) and arrestin2 (P19107); bluebottle fly arrestin1 (X79072) and arrestin2 (X79073); migratory locust arrestin (S57174); horseshoe crab arrestin (U08883); fruit fly kurtz (AF221066); planarian arrestin (Orii et al. unpublished); nematode arrestin (P51485). Southern blot hybridization Three types of the probes, a full-length Ci-arr cDNA (F), 5¢-region probe (N, XhoI–PstI fragment) and 3¢region (C, PstI–BamHI fragment) were labeled with [ 32 P]dCTP using a BcaBest labeling kit (Takara) and used as probes for hybridization. Total DNA was isolated from the ovary of a single adult of Ciona according to the standard method. Ten micro- grams of DNA were digested with PstIorSpeI, separated on 0.8% agarose gel, transferred onto nylon membranes (Hybond-N + , Amersham Pharmacia Biotech) and immo- bilized by UV cross-linking. The membrane was incubated in 6 · NaCl/Cit containing 0.5% SDS, 5 · Denhardt’s solution and 100 lgÆmL )1 salmon sperm DNA at 60 °C for 1 h. The radioactive probe was added to the prehybridi- zation solution and incubated at 60 °C for 24 h. The membrane was washed twice with 2 · NaCl/Cit containing 0.1% SDS at 60 °C for 20 min. The size of DNA was estimated using kDNA digested with HindIII (Gibco BRL) as standards. After autoradiography, the membrane was washed out three times with 0.1% SDS at 100 °Ctoremove the probe and then was hybridized again with another probe. b 2 -Adrenergic receptor sequestration assay The cDNAs encoding Ci-Arr and the mutant (V55D), constructed by the inverted amplification method [18], were subcloned into XhoIandBamHI site of the expression vector pEF-BOS. pEF-b 2 -AR was constructed by using cDNA encoding b 2 -AR, generously provided by R. J. Lefkowitz (Duke University Medical Center, Durham, USA). HEK293tsA201 cells, generously provided by C. J. van Koppen (Institute fur Pharmakologie Universitatskli- nikum Essen, Germany) were grown on 60-mm plates as described elsewhere [19] and transfected with 0.5 lgof pEF-b 2 -AR, in addition to either 2 lg of pEF-Ci-arr, pEF- Ci-arr(V55D), or pEF-BOS(control vector), by LipofectA- MINE2000 (Gibco) according to the manufacturer’s instructions. After 24 h transfection, cells were replated on poly L -lysine-coated 24-well plates and allowed to reattach and grow for further 24 h. Then cells were incubated with 10 l M isoproterenol for the indicated times (time course experiment) or with the indicated concentrations of isoproterenol for 30 min (dose- dependence experiment). After washing with ice-cold phos- phate-buffered saline, cells were incubated with 12 n M [ 3 H]CGP-12177 (NEN Life Science Products) in 25 m M Ó FEBS 2002 Origin of vertebrate visual and nonvisual arrestins (Eur. J. Biochem. 269) 5113 Hepes-buffered Dulbecco’s modified Eagle’s medium/F-12 medium with and without 40 l M alpranolol to measure total and nonspecific binding, respectively. After incubation at 4 °C for 3 h, cells were washed with ice-cold phosphate- buffered saline, solubilized in 1% Triton X-100 and mixed with scintillation cocktail and then the radioactivity was measured. Untransfected HEK293 tsA201 does not express detectable levels of b 2 -adrenergic receptors. The expression of Ci-Arr and Ci-Arr (V55D) was confirmed by Western blotting with anti-(Ci-Arr) Ig. RESULTS We isolated two distinct cDNAs encoding an arrestin from larvae of the ascidian Ciona intestinalis. They were identical except for the 3¢ region, where 59 bp was deleted in one form. RT-PCR showed that the longer form was expressed at levels 16 times higher than the shorter one in the larvae (T. Horie, M. Nakgawa, H. Orii & M. Tsuda, unpublished work). Hence, we refer to the longer form as Ci-arr and the shorter one as the truncated form. Figure 1 shows the deduced amino acid sequence of Ci-arr aligned with those of other arrestins. Ci-Arr was similar to other arrestins except for the C-terminal region with 50–55% identity to verteb- rate visual arrestins and 63–65% identity to vertebrate nonvisual b-arrestins. In contrast, it had significantly lower identity to the arthropod arrestins. JGI Ciona genome project database (http://www.jgi.doe.gov/programs/cio- na.htm) and our partial analysis of the genomic DNA revealed that at least 12 introns interrupt the coding region of Ci-arr. Among them, nine introns are same in their positions as those of vertebrate visual and b-arrestin genes (Fig. 1), supporting close relationship between Ci-Arr and vertebrate arrestins. Fig. 1. Comparison of the amino acid sequences of Ci-Arr with some types of arrestins. The alignment of the deduced amino acid sequence of Ci-arr and the typical animal arrestins was performed using a CLUSTALW program [20]. Since the insertion sequence of C-terminus apparently disturbed the sequence alignment in the C-terminal portion, we manually optimized it from 350 to the end of the sequence. Dashes indicate gaps introduced to optimize the alignment. Asterisks and dots under the sequences represent the identical and similar amino acids in eight sequences. Open and solid wedges indicate the position of introns in Ci-arr and human visual arrestin genes, respectively. The box indicates the clathrin binding domain [21,22] which may be responsible for the receptor internalization. White letters indicate AP2 binding site in b-arrestins [23]. White and black arrows indicate the splicing sites in Ci-arr and bovine rod arrestin, respectively [24,25]. 5114 M. Nakagawa et al. (Eur. J. Biochem. 269) Ó FEBS 2002 Comparison of two types of cDNA and genomic DNA revealed that splicing of intron 11 resulted in the shift of the reading frame in the truncated form, in which Asn387 in Ci-Arr was replaced with Lys followed by stop codon (Fig. 1 white arrowhead). Similar truncated form of arrestin, termed p44, in which the last 35 amino acids are replaced by a single Ala, was detected in bovine retinal rod cells [24,25] (Fig. 1 black arrowhead). Since p44 was present abundantly in the outer segment of a rod photoreceptor cell and inhibited the activity of phosphodiesterase much more effectively than the full-length form, p44 is thought to be a key component in phototransduction [24,26]. There is no report on such alternative splicing in the C-terminus of b-arrestin. In the C-terminus, b-arrestins contain a characteristic domain (371–379 for bovine b-arrestin2; arrestin3), which visual arrestins lack [27]. This domain is known as the clathrin-binding domain, which is responsible for the receptor internalization [9,27,28]. Recently, the specific arginine residues (R394 and R396 for b-arrestin2) in b-arrestin that mediate its binding to AP2 were identified [23]. The presence of the clathrin-binding domain and AP2 binding site in Ci-Arr (Fig. 1) suggests that this arrestin also has the ability to internalize the receptor like b-arrestins. Thus, we investigated whether Ci-Arr can promote the internalization of GPCR by using HEK293tsA201 cells exogenously expressing b 2 -adrenergic receptor (b 2 -AR), established as the internalization assay system. Upon the exposure of 10 l M isoproterenol, b 2 -AR agonist, the numbers of the receptor at the cell surface with and without overexpression of exogenous Ci-arr decreased by about 30 and 60% for 60 min, respectively (Fig. 2B). This indicates that Ci-Arr significantly promoted the internalization of b-AR. b-arrestin1 V53D (b-arrestin2 V54D) mutant is known as a dominant negative mutant to suppress b 2 -AR internalization [7], because it binds to the clathrin cages with high affinity but is significantly impaired in its ability to interact with b 2 -ARs [27]. We constructed the correspond- ing mutant for Ci-Arr (V55D). This mutant, however, showed that the extent of the internalization was almost the same as that of the control (Fig. 2B) in spite of the same levels of the expression (Fig. 2A). This result will be discussed later. The isoproterenol concentration dependence also showed that Ci-Arr induced about twofold sequestra- tion of the receptors compared with control and V55D (Fig. 2C). These results indicated that Ci-Arr was able to promote the agonist-induced receptor internalization. It should be noted that Ci-Arr promoted the internalization of not only b 2 -AR, but also m2- and m4- muscarinic receptors (data not shown). The internalization of b 2 -ARs has been reported to be unaffected by coexpression of b-arrestin1 but significantly attenuated by coexpression of b-arrestin1 (V53D) [7,28]. We confirmed these observations by experiments carried out in parallel with the experiments on Ci-Arr (data not shown). These results indicate that the Ci-Arr (V55D) does not function in a dominant negative manner for endogenous b-arrestin or related proteins, and that Ci-Arr enhances the internalization of b 2 -ARs by the mechanism independent of the function of endogenous b-arrestin or related proteins. To know the expression pattern of Ci-arr gene in the larva, we performed whole-mount in situ hybridization using the digoxigenin-labeled riboprobe (Fig. 3). The signal was observable in the photoreceptor cells on the right side of the pigment cup of ocellus. No expression of Ci-arr gene was detected in any other regions of the larva. The expression pattern was identical to that of the opsin gene Ci-opsin1 [29]. Furthermore, this result was confirmed by immunohistochemical staining using the anti-(Ci-Arr) Ig (T. Horie, M. Nakgawa, H. Orii & M. Tsuda, unpublished work). As far as the expression sites, Ci-Arr can be regarded as visual arrestin in the ascidian larvae. Thus, Ci-Arr has both features of visual arrestins (the exclusive expression in photoreceptors) and b-arrestins (the function of promoting the receptor internalization). To examine the evolutionary relationship among triploblastica Fig. 2. Effects of wild-type and V55D mutant Ci-Arr on sequestration of b 2 -adrenergic receptor in HEK293 tsA201 cells. (A) Detection of Ci-Arr in HEK293 tsA201 cells transfected with pEF-BOS (control), pEF- Ci-arr (WT), or pEF-Ci-arr (V55D) by immunoblotting using the anti-(Ci-Arr) Ig. (B and C) HEK293 tsA201 cells transfected with pEF- b 2 -AR together with WT, V55D, or control vector were incubated at 37 °C in the absence and presence of 10 l M isoproterenol for the indicated period (B) or with the indicated concentrations of isopro- terenol for 30 min (C). Data are the mean ± SE from triplicate experiments. Ó FEBS 2002 Origin of vertebrate visual and nonvisual arrestins (Eur. J. Biochem. 269) 5115 arrestin family, we constructed a molecular phylogenetic tree. This tree demonstrates that triploblastica arrestins can be classified into two major classes: vertebrate and protos- tome arrestins (Fig. 4). Vertebrate arrestins are subdivided into two groups, visual arrestins and b-arrestins. The tree showed that Ci-Arr was more closely related to the vertebrate arrestins than to protostome arrestins and that it was branched from a common root of the vertebrate visual and b-arrestins. This result allows us to propose a hypothesis that Ci-Arr is the prototype of vertebrate arrestin and that in the evolutionary process to vertebrates the duplication of the prototype resulted in two different types of arrestins, visual and b-arrestins. If so, Ciona must have only one gene for arrestin. Fig. 5. Genomic Southern blot analysis. (A) The probes used for hybridization were schematically drawn under Ci-arr cDNA. It should be noted that there is no SpeIsiteinCi-arr cDNA. (B) Genomic DNA extracted from an individual adult of Ciona was digested with SpeIor PstI. Each lane was loaded with a digest of 10 lg DNA. The same blot was hybridized repeatedly with a full length probe (F), 5¢-region probe (N) or 3¢-region probe (C) of Ci-arr cDNA in the low stringency condition (6 · NaCl/Cit, 60 °C). Fig. 4. Phylogenetic tree of arrestin family. The molecular phylo- genetic tree was constructed by the neighbor-joining method [30] based on the amino acid sequences of various arrestins using CLUSTALW program [20]. Bar indicates 10% replacement of amino acid per site. Numbers at nodes are percentage of 1000 bootstrap replicates that support the branches. Fig. 3. Localization of Ci-arr mRNA in Ciona intestinalis larva. Ci-arr mRNA was detected by whole-mount in situ hybridization using a digoxigenin-labeled riboprobe. Dorsal views of (A) the whole larva (scale bar, 100 lm), (B) magnified trunk region (scale bar, 50 lm) Ciona larva has two pigments in the brain vesicle: the anterior pigment is otolith (OT), the putative gravity sense organ and the posterior pigment is ocellus (OC). The expression of Ci-arr is restricted to the photoreceptors in the right side of the OC. 5116 M. Nakagawa et al. (Eur. J. Biochem. 269) Ó FEBS 2002 To confirm this hypothesis, we performed Southern analysis with the genomic DNA of a single adult using three types of probes: F (the full length of Ci-arr), N (5¢ fragment when the full-length was digested with PstI), and C (3¢ fragment with PstI digestion) (Fig. 5A). The hybridiza- tion condition was low enough stringency (6 · NaCl/Cit at 60 °C) to detect other arrestin genes, because Lohse et al.[2] could isolate b-arrestin clone from bovine brain cDNA library using full length cDNA of bovine rod arrestin at higher stringency condition (0.5 · NaCl/Cit at 65 °C). In SpeIorPstI digestion, a single band was detected using probes N or C, whereas both corresponding bands were detected using probe F (Fig. 5B). Since cDNA of Ci-arr contains a single PstI site but no SpeI (Fig. 5A), this result indicated that single SpeI site is in an intron. These results suggest that Ciona genome contains only one gene for arrestin family. BLAST search of Ci-arr against JGI Ciona genome project database indicated that all of 18 hits of genomic DNA fragments were almost identical to Ci-arr and that there are no hits with some similarity except for them. This result also supports the suggestion that Ciona does not contain any arrestin genes other than Ci-arr. DISCUSSION Gene duplication is thought to have occurred two times in the early process of vertebrate evolution [31]. This hypothesis is in agreement with our present results; the first gene duplication of the prototypical arrestin gene like Ci-arr might result in the ancestral visual and b-arrestins, the second duplication might result in cone and rod arrestins from the former, and b-arrestin1 and b-arresin2 from the latter. Recently, it was reported that Drosophila visual arrestin (Arr2) was involved in the apoptosis of the photoreceptor cells [32,33]. In the photoreceptors of mutant flies whose retinae degrade in light dependent manner, Arr2 was tightly bound to photoactivated and phosphorylated rhodopsin and the complex was dynamin-dependently internalized to induce the apoptotic cell death of the photoreceptors, although Arr2 dose not contain the consensus sequence for clathrin binding (Fig. 1). In contrast, vertebrate visual arrestin does not have the ability to bind clathrin and cannot induce receptor internalization [6,8]. Ci-Arr retaining this function is apparently close from the viewpoint of the amino acid sequence similarity and the position of the intron to the vertebrate type of arrestin (Fig. 1). Therefore, it may be presumed that the function was lost in vertebrate visual arrestin during the evolution. The branch length of the phylogenetic tree (Fig. 4) suggested that the evolutionary rates of the amino acid substitutions in vertebrate visual arrestins was higher than those of vertebrate b-arrestins as already reported by Hisatomi et al. [34]. This is consistent with an idea that the evolutionary rates of the molecules strongly depend on their tissues [35]. Visual arrestin has the high receptor specificity for rhodopsin, whereas b-arrestin only modestly discriminates among rhodopsin, m2 muscarinic acetylcholine receptor and b 2 -AR [36]. Therefore, it is possible that visual arrestins widely were diverged with the divergence of opsin genes. 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(1994) Gene duplications and the origins of vertebrate develop- ment. Dev Suppl. 125–133. 32. Alloway, P.G., Howard, L. & Dolph, P.J. (2000) The formation of stable rhodopsin-arrestin complexes induces apoptosis and pho- toreceptor cell degeneration. Neuron 28, 129–138. 33. Kiselev,A.,Socolich,M.,Vinos,J.,Hardy,R.W.,Zuker,C.S.& Ranganathan, R. (2000) A molecular pathway for light-dependent photoreceptor apoptosis in Drosophila. Neuron 28, 139–152. 34. Hisatomi, O., Imanishi, Y., Satoh, T. & Tokunaga, F. (1997) Arrestins expressed in killifish photoreceptor cells. FEBS Lett. 411, 12–18. 35. Kuma, K., Iwabe, N. & Miyata, T. (1995) Functional con- straints against variations on molecules from the tissue level: slowly evolving brain-specific genes demonstrated by protein kinase and immunoglobulin supergene families. Mol. Biol. Evol. 12, 123–130. 36. Gurevich, V.V., Dion, S.B., Onorato, J.J., Ptasienski, J., Kim, C.M.,Sterne-Marr,R.,Hosey,M.M.&Benovic,J.L.(1995) Arrestin interactions with G protein-coupled receptors. Direct binding studies of wild type and mutant arrestins with rhodopsin, b 2 -adrenergic, and m2 muscarinic cholinergic receptors. J.Biol. Chem. 270, 720–731. 5118 M. Nakagawa et al. (Eur. J. Biochem. 269) Ó FEBS 2002 . the shutting-down of the downstream signaling [1–4]. Vertebrate arrestins can be divided into two classes; visual arrestins and nonvisual, b -arrestins. Visual arrestins are composed of rod- and cone -arrestins, . a hypothesis that Ci-Arr is the prototype of vertebrate arrestin and that in the evolutionary process to vertebrates the duplication of the prototype resulted in two different types of arrestins, visual. PRIORITY PAPER Ascidian arrestin (Ci-arr), the origin of the visual and nonvisual arrestins of vertebrate Masashi Nakagawa 1 , Hidefumi Orii 1 , Norihiro Yoshida 2 , Eri Jojima 3 ,

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