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From Salmonid Fish (Oncorhynchus Kisutch) Comp. Biochem. Physiol. Vol. 9311, No. 4, pp. 835-845, 1989 0305-0491/89 $3.00+ 0.00 Printed in Great Britain © 1989 Pergamon Press pie CHARACTERIZATION OF ELASTIN PROTEIN AND mRNA FROM SALMONID FISH (ONCORHYNCHUS KISUTCH) MARGUERITECHOW,*t CHARLESD. BOYD,* MARIA-LUISAIRUELA-ARISPE,* DAVID S. WRENN,§ ROBERT MECHAM¶ and E. HELENESAGE*tt *Department of Biological Structure, University of Washington, Seattle, WA 98195, USA (Tel 206 545 1192); ,Department of Surgery, UMDNJ-Robert Wood Johnson Medical School, New Brunswick, NJ 08903, USA; §Department of Pathology, Memorial Hospital, Pawtucket, RI 02860, USA; and ¶Department of Medicine, Jewish Hospital at Washington University, School of Medicine, St Louis, MO 63110, USA (Receioed 16 December 1988) Abstract--1. Elastin was isolated from the bulbus arteriosus of a salmonid fish. Monoclonal and poly¢lonal antibodies, elicited against a CNBr digest of this protein, immunoprecipitated a polypeptide of Mr 43,000 from fish cell culture medium. 2. Cell-free translation of salmon poly A ÷ RNA produced a protein of approximately 43 kD that was immunoprecipitated with anti-elastin antibodies. The corresponding mRNA had an approximate Mr of 2kb. 3. Despite similarities in amino acid composition, the differences in M r between mammalian and salmon mRNA and protein suggest a divergence of fish and higher vertebrate elastins from an earlier ancestral gene. INTRODUCTION species of approximately 3.5 kb in mammals and birds (Rosenbloom, 1984; Sandberg and Davidson, The problem of tissue resilience has been satisfied by 1984). several genetically unrelated proteins throughout the From earlier studies on the elastin protein in blood animal kingdom. In vertebrates, elastin confers the vessels, Sage and Gray (1979, 1980, 1981) made property of rubber elasticity to the tissues in which it several observations regarding its evolutionary his- is most abundant (aorta, ligament, skin) (for recent tory: (a) elastin occurred only in vertebrates and reviews, see Sandberg and Davidson, 1984 and appeared first in cartilagenous fish; it was absent from Rosenbloom, 1984). The protein is secreted as tro- cyclostomes, the present-day descendants of jawless poelastin into the connective tissue extracellular space fishes, (b) the morphology of aortic elastin fibers was and assembled into elastin-containing fibers. variable; thicker lamellae were generally associated Elastin was one of the first "modular" proteins to with higher blood pressures, (c) the hydrophobicity of be characterized. With an Mr of 68,000-72,000, both elastin increased with the evolution of the more the mammalian and avian proteins contain large complex circulatory systems associated with numbers of unusually hydrophobic peptide repeats homeothermic animals, (d) coacervation (fiber for- (e.g. PGVG, GGVP, PGVGVA) that form fl-spirals, mation) and elasticity were related to the hydropho- and Ala-rich, or-helical regions that contain Lys bicity of the protein, and (e) elastin and other and/or the Des/Ide crosslinks (Sandberg and David- structural connective tissue proteins did not have a son, 1984; Bressan et al., 1987). Recent studies on the common genetic origin, although there could be structure of human, sheep, and bovine elastin genes distinct genetic types of elastin (for reviews see Sage, have revealed that the hydrophobic and crosslinking 1982 and 1983). domains are encoded in separate exons of disparate These conclusions were based on a definition of the size and are separated by large intervening sequences elastin protein that included several criteria (a charac- (Rosenbloom, 1984). The levels of elastin in develop- teristic amino acid composition, the presence of Des ing systems appear to be under transcriptional con- and Ide, histological appearance, and physicochemi- trol, and Northern blotting has revealed mRNA cal properties). Biochemical analysis revealed in- creases in both the degree of crosslinking and hydrophobicity in elastins from higher vertebrates tCurrent address: Department of Anatomy, University of (mammals and birds) as compared to those from Pennsylvania, Philadelphia, PA 19104, USA. bony fish (teleosts). It was of particular interest that tSAuthor to whom correspondence should be addressed. selection for an increasingly hydrophobic elastin ap- Abbreviations used--Des, desmosine; DMEM, Dulbec¢o peared to parallel the development of a highly pres- Modified Eagle's Medium; DTT, dithiothreitol; ELISA, enzyme-linked immunosorbent assay; FITC, fluorescein surized, closed circulatory system in homeothermic isothiocyanate; HPLC, high pressure liqud chromatog- animals. Moreover, the increase in hydrophobicity raphy; Ide, isodesmosine; kD, kilodaltons; kb, kilobases; was found to be related to the thermodynamic prop- PBS, phosphate-buffered saline; Tris-saline-0.15M erties of the elastin polymer. NaCI, 50raM Tris-HC1, pH 7.5; SDS-PAGE, sodium The rather significant changes in the levels of dodecylsulfate-polyacrylamide gel eleetrophoresis. certain amino acids in elastins from different verte- 835 836 MARGUERITE CHow et al. brate classes, as well as the presence of discrete adjuvant (Gibco Laboratories, Grand Island, NY). New domains in elastin, suggest an evolutionary assembly Zealand rabbits were immunized by subcutaneous and from smaller units which later underwent a multifold intramuscular injections and boosted every 21 days there- duplication (Sage and Gray, 1981). One of the conse- after with 1 mg of the immunogen emulsified in Freund's quences of this mechanism is the creation of gene incomplete adjuvant. 5 10 ml of serum were collected prior to each immunization. A polyclonal antibody raised against products of different molecular size. If any of these homogenates of insoluble elastin, as well as elastin solubi- putative elastin isoforms were retained in present day lized by oxalic acid treatment of rainbow trout (Salmo organisms, one would predict that such differences gairdneri) bulbus arteriosus, was a gift from Anna Jacques would be apparent both in the mRNA and its (University of St. Andrews, Fife, Scotland) (Wright et al., translation product(s). 1988). In this study we have initiated a comparison be- Monoclonal antibodies were raised in mice against a tween mammalian and teleost elastin genes by char- CNBr digest of salmon elastin peptides (Wrenn el al., 1986). acterizing elastin mRNA and protein from salmonid Tissue culture supernates from several clones reacted posi- tively by ELISA and Western blotting with the immunogen, fish. We show that salmon elastin mRNA and its and one of them (Mab G7) was used in this study. translated protein are considerably smaller than those Solubilized peptides and control proteins (e.g. BSA, colla- of mammals (approximately 2.0 kb and 43 kD in the gens, fibronectin) were coated onto polystyrene 96-well fish versus 3.5 kb and 70 kD in mammals). Moreover, costar dishes and incubated with an elastin antibody as monoclonal and polyclonal antibodies raised against previously described (Mecham and Lange, 1982). Competi- salmon elastin peptides reacted with a soluble protein tion ELISAs were performed by incubation of increasing of Mr43,000 secreted by fish cells in culture. Al- amounts of soluble elastin CNBr peptides (0.1 10#g), though the amino acid compositions of the salmon dissolved either in PBS or in a 50 mM Tris-HCl buffer, elastin peptides were similar to those of elastins found pH 7.5, containing from 1 4 M urea, with a fixed amount of anti-elastin antisera, prior to addition to the elastin-coated in mammals, there were distinct differences with wells. respect to several of the most abundant residues. These data support an evolutionary divergence of the Cell culture and metabolic labeling genes encoding elastin in bony fish and higher verte- Cells from bluegill fry (Lepomis macrochirus) (BF-2, brates from a common ancestor. American Type Culture Collection, Rockville, MD) and rainbow trout gonadal tissue (Salmo gairdneri) (a gift from Kathleen Saybo, University of Washington, Seattle, WA) MATERIALS AND METHODS were grown at room temperature in L-15 medium (Sigma Isolation c~f elastin Chemical Co., St Louis, MO) containing antibiotics and 10%, by volume, fetal calf serum (lot # 1 ll 1593, Hyclone Elastin was extracted from the bulbus arteriosus of Laboratories, Sterile Systems, Inc., Logan, UT). The embry- mature Pacific Northwest Coho Salmon (Oncorhynchus onic cell line CSE-119, derived from Oncorhynchus kisutch, kisuteh) as previously described (Sage and Gray, 1979). The was a gift from Dr C. Lannan (Marine Science Center, purified insoluble protein was solubilized with CNBr (East- Newport, OR) (Lannan et al., 1984). At 80% confluency, man Chemical Co., Rochester, NY) in 70% formic acid, cells were metabolically radiolabeled with [35S]-methionine according to the procedure of Rasmussen et al. (1975). (50 #Ci/ml culture medium, approximately 1000 Ci/mmol, Soluble peptides were chromatographed at 4°C on Sephadex ICN Radiochemicals, Irvine, CA) in serum-free DMEM G-100 (Pharmacia Fine Chemicals, Piscataway, NJ) equili- supplemented with Na ascorbate (50#g/ml) and fl- brated with 0.05 M acetic acid. Alternatively, the CNBr aminopropionitrile fumarate (64 #g/ml) (Gibco Laborato- digest was fractionated by reverse-phase HPLC on a Vydac ries, Grand Island, NY). After 24 hr, media were removed C18 column (Separations Group, Hesperia, CA) as de- in the presence of protease inhibitors, and the secreted scribed by Kapoor et al. (1986). proteins were precipitated in 10% trichloroacetic
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