Biochimica et Biophysica Acta, 1131 (1992) 239-242 © 1992 Elsevier Science Publishers B.V. All rights reserved 0167-4781/92/$05.00

239

BBAEXP 90366

Short Sequence-Paper

Isolation and characterization of cDNA clones encoding the skeletal and smooth muscle Xenopus laevis tropomyosin isoforms Serge Hardy and Pierre Thiebaud Laboratoire de Biologic et G~n~tique du D&~eloppement, URA CNRS 256, Facult~ des Sciences, Campus de Beaulieu, Rennes (France) (Received 16 April 1992)

Key words: Tropomyosin; cDNA; Skeletal muscle; Smooth muscle

cDNAs clones corresponding to the skeletal and smooth muscle /3 tropomyosins isoforms were isolated from a Xenopus laev& embryo cDNA library. Sequence analysis indicated that the two isoforms are coded by a single gene that uses two couples of alternative exons. The expression of the X. laevis/3 tropomyosin gene closely resembles that of the mammalian gene but differs from the avian gene.

Tropomyosins (TM) constitute a family of related proteins present in all eukaryotic cells. In striated muscle cells, TM in association with the troponin complex are involved in contraction while in non muscle cells they are components of the microfilaments apparatus but their role is less well understood. In skeletal and smooth muscle cells the two major TM isoforms a and/3 are coded by separate genes [1-8]. The diversity of T M isoforms is generated by a combination of differential promoter usage and alternative splicing of primary R N A transcripts [9]. We have recently investigated TM gene expression in Xenopus laevis and characterized the cDNAs corresponding to the skeletal muscle and non muscle isoforms generated from the X. laevis a TM gene [11]. We have shown that the two mRNAs are transcribed from different promoters that are developmentally regulated. We report here the isolation and characterization of two cDNA clones encoding skeletal and smooth muscle mRNAs generated from the X. laevis/3 TM gene. A stage 42 embryo Agtl0 cDNA library [10] was screened with the pSMT10 cDNA probe corresponding to chicken gizzard /3TM sequences [10]. Two positive

The sequence data in this paper have been submitted to the EMBL/Genbank Data Libraries under the accession number M87307. Correspondence to: P. Thiebaud, Laboratoire de Biologie et G6n6tique du D6veloppement, Facult6 des Sciences, Beaulieu, 35042 Rennes cedex, France.

clones XTM/34 and XTM/35 were characterized. They both contain an 852 bp open reading frame representing a 284 amino acid coding capacity which is the size of the muscle TM proteins. The two sequences show 95% homology at the nucleotide level over the amino acid regions 1 to 188 and 214 to 257 while the regions corresponding to amino acid 189 to 213 and 258 to 284 show only 37% homology (Fig. 1). The amino acid regions 189 to 213 and 258 to 284 correspond to alternatively spliced exons 6 A / 6 B and 9 A / 9 D in all vertebrate/3 TM genes, while the amino acid regions 1 to 188 and 214 to 257 constitute a highly conserved core sequence present in all muscle isoforms deriving from the /3 TM gene [9]. When compared to vertebrates TM sequences, XTM/34 shows 87% homology with rat or chicken skeletal muscle sequences while XTM/35 is more closely related to smooth muscle sequences showing 84% identity with the mammalian or avian sequences (Fig. 2). Moreover, this identity rises to 88% over the alternative exons 6 A / 6 B . Conversely, when amino acid region 189-213 of XTM/34 is compared with the corresponding mammalian or avian smooth muscle sequences the identity is only 60%. More strikingly, XTM/34 shows over the amino acid region 258-284, 92% homology with the corresponding mammalian or avian skeletal muscle regions, while there is only 26% homology with the same region in smooth muscle sequences. On the other hand, XTM/34 and XTM/35 show only 60% homology with the X. laevis a tropomyosin sequences (data not shown). Together

240

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Fig. 2. Comparison of the amino acid sequences of XTM/34 (A) and XTM/35 (B) with rat and chicken skeletal and smooth muscle tropomyosins. Amino acid homology is indicated by dots and the position of the alternatively spliced exons in rat and chicken genes by vertical arrowheads. The tropomyosin sequences are from the following references: chk.sk/3 and chk.sm/3 [6], rat.sk/3 and rat.sm/3 [1].

these sequence comparisons unambiguously identify XTM/34 and XTM/35, respectively, as the skeletal and smooth muscle TM mRNAs generated from the/3 TM gene. The slight nucleotide divergence between XTM/34 and XTM/35 over their common coding region cannot be explained solely by allelic variation but is probably related to the well known X. laeuis genome duplication that occurred during evolution [12]. In this case XTM/34 and XTM/35 could represent the two duplicated genes. This situation has been reported in many instances like homeobox genes, MyoD or Myc genes [13-15].

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Fig. 3. Northern blot analysis of the X. laevis fl tropomyosin gene expression. 15 p.g of total RNA were separated on formaldehyde agarose gel and blotted onto nylon membranes. The membrane was hybridized with the complete XTM/35 eDNA probe (A) or the 3' untranslated regions of XTM/34 (B) or XTM/35 (C). The RNA is from stage VI oocytes (O), unfertilized eggs (E), stage 20, 30, 35 or 42 embryos (20, 30, 35, 42), liver (L), skeletal muscle (M), stomach (St), oviduct (Ov) and adult heart (H).

As shown in Fig. 3A when the complete XTM/35 eDNA was used to probe Northern blots, a single 1.5 kb signal was detected in total RNA from embryo (lanes 35 and 42). A same size transcript was detected in RNA from skeletal muscle (lane M) and from smooth muscles like oviduct or stomach (lanes Ov and St). There was no detectable signal even after a long exposure in egg and adult heart RNAs (Fig. 3A, lanes E and H). The presence of the very conserved core sequences in XTM/35 eDNA clone allows us to detect under the high stringency hybridization conditions that we used all the tropomyosin transcripts deriving from the /3 TM gene. Therefore, we can conclude that the X. laevis /3 TM gene is expressed in embryo and

Fig. 1. Nucleotide and derived amino acid sequences of XTM/34 and XTM/35 cDNAs clones. The two sequences have been aligned for comparison and nucleotide identity is indicated by dashes. The location of the restriction sites used for the subcloning of specific probes and the adaptator sequence used during the construction of the library have been underlined.

242 skeletal and smooth muscle tissues but contrary to the T M gene in neither adult cardiac muscle nor eggs. Moreover the a and /3 T M genes show a different temporal expression during X. laevis early development. Transcripts from the /3 TM gene are first detected in stage 35 embryo and then accumulate rapidly (Fig. 3A) while we have shown that transcripts from the c~ T M gene accumulated from stage 18 [10]. We generated subclones of the 3' untranslated regions of XTM/34 and XTM/35 in order to identify their corresponding transcripts. XTM/344 is a 340 bp SspI-EcoRI fragment of XTM/34 and XTM/352 is a 380 bp HindIII-EcoRI fragment of XTM/35 (see Fig. 1). Under high stringency conditions XTM/344 and XTM/352 gave a 1.5 kb signal, respectively, in skeletal muscle and smooth muscle R N A s (Fig. 3B and C). Both probes hybridized to a 1.5 kb transcript in embryo R N A but no signal was observed in oocyte or cardiac tissue RNAs. T o g e t h e r these results confirm that XTM/34 and XTM/35 encode, respectively, the X. laevis skeletal and smooth muscle /3 T M isoforms. Like their vertebrate counterparts the two isoforms are generated from a single gene by the use of two couples of alternatively spliced exons [9]. A striking feature that emerges from our studies on X. laevis T M gene expression is that the a and /3 amphibian genes are more related to the m a m m a l i a n genes than to their avian counterparts. Indeed, the amphibian and m a m m a l i a n /3 genes are not expressed in adult heart which expresses the a gene [1,11]. In avians the cardiac isoform is coded by a gene distinct from the a or 13 genes [16]. Moreover, it seems that the amphibian /3 T M gene does not generate a low molecular weight non muscle isoform. W e postulate this from the absence in oocyte of transcripts related to /3 T M sequences while non muscle transcripts deriving from the a gene are a b u n d a n t at this developmental stage. However, this can only be confirmed by cloning and complete characterization of the gene. In conclusion, X. laevis seems an attractive sys-

tem for studying the transcriptional control of the a and /3 T M genes during development. We thank M. Fiszman for providing the pSMT10 probe and H.B. Osborne for critical reading of the manuscript. This work was supported by grants from the Association Fran~aise contre les Myopathies and the Association pour la R e c h e r c h e sur le Cancer. S.H. was supported by a fellowship from the Association Fran~aise contre les Myopathies. We thank L. C o m m u nier for graphic work. References

1 Helfman, D.M., Cheley, S., Kuismanen, E., Finn, L.A. and Yamawaki-Kataoka, Y. (1986) Mol. Cell. Biol. 6, 3582-3595. 2 Pearson-White, S.H. and Emerson, C.P., Jr. (1987)J. Biol. Chem. 262, 15998-16010. 3 Ruiz-Opazo, N. and NadaI-Ginard, B. (1987) J. Biol. Chem. 262, 4755-4765. 4 MacLeod, A.R. and Gooding, C. (1988) Mol. Cell. Biol. 8, 433 440. 5 Wieczorek, D.F., Smith, C.M.J. and Nadal-Ginard, B. (1988) Mol. Cell. Biol. 8, 679-694. 6 Libri, D., Lemmonier, M., Meinnel, T. and Fiszman, M.Y. (1989) J. Biol. Chem. 264, 2935-2944. 7 Lindquester, G.J., Flach, J.E., Fleenor, D.E., Hickman, K.H. and Devlin, R.B. (1989)Nucleic Acids Res. 17, 2099-2117. 8 Forry-Schaudies, S., Maihle, N.J. and Hughes, S.H. (1990) J. Mol. Biol. 211,321-330. 9 Lees-Miller, J.P. and Helfman, D.M. (1991) Bioessays 13, 429437. 10 Hardy, S., Fiszman, M., Osborne, H.B. and Thiebaud, P. (1991) Eur. J. Biochem. 202, 431-440. 11 Helfman, D.M., Feramisco, J.R., Ricci, W.M. and Hughes, S.H. (1984) J. Biol. Chem. 259, 14136-14143. 12 Bisbee, C.A., Baker, M.A., Wilson, A.C., Hadji-Azimi, I. and Fischberg, M. (1977) Science 195, 785-787. 13 Fritz, A.F., Cho, K.W.Y., Wright, C.V.E., Jegallian, B.G. and De Robertis, E.M. (1989) Dev. Biol. 131,584-588. 14 Harvey, R.P. (1990) Development 108, 669-680. 15 Taylor, M.V., Gusse, M., Evan, G.I., Dathan, N. and Mechali, M. (1986) EMBO J. 5, 3563-3570. 16 Forry-Schaudies, S., Gruber, C.E. and Hughes, S.H. (1990) Cell Growth Diff. 1,473-481.

Isolation and characterization of cDNA clones encoding the skeletal and smooth muscle Xenopus laevis beta tropomyosin isoforms.

cDNAs clones corresponding to the skeletal and smooth muscle beta tropomyosins isoforms were isolated from a Xenopus laevis embryo cDNA library. Seque...
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