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PLOS ONE  2012 

Molecular Characterization of TGF-β Type I Receptor Gene (Tgfbr1) in Chlamys farreri, and the Association of Allelic Variants with Growth Traits

DOI: 10.1371/journal.pone.0051005

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Abstract:

Background Scallops are an economically important aquaculture species in Asian countries, and growth-rate improvement is one of the main focuses of scallop breeding. Investigating the genetic regulation of scallop growth could benefit scallop breeding, as such research is currently limited. The transforming growth factor beta (TGF-β) signaling through type I and type II receptors, plays critical roles in regulating cell proliferation and growth, and is thus a plausible candidate growth regulator in scallops. Results We cloned and characterized the TGF-β type I receptor (Tgfbr1) gene from Zhikong scallops (Chlamys farreri). The deduced amino acid sequence contains characteristic residues and exhibits the conserved structure of Tgfbr1 proteins. A high expression level of scallop Tgfbr1 was detected during early embryonic stages, whereas Tgfbr1 expression was enriched in the gonad and striated muscle in adults. A single nucleotide polymorphism (SNP, c. 1815C>T) in the 3′ UTR was identified. Scallops with genotype TT had higher growth traits values than those with genotype CC or CT in a full-sib family, and significant differences were found between genotypes CC and TT for shell length, shell height, and striated muscle weight. An expression analysis detected significantly more Tgfbr1 transcripts in the striated muscle of scallops with genotype CC compared to those with genotype TT or CT. Further evaluation in a population also revealed higher striated muscle weight in scallops with genotype TT than those with the other two genotypes. The inverse correlation between striated muscle mass and Tgfbr1 expression is consistent with TGF-β signaling having a negative effect on cell growth. Conclusion The scallop Tgfbr1 gene was cloned and characterized, and an SNP potentially associated with both scallop growth and Tgfbr1 expression was identified. Our results suggest the negative regulation of Tgfbr1 in scallop growth and provide a candidate marker for Zhikong scallop breeding.

References

[1]  Shumway SE, Parsons GJ (2006) Scallops: Biology, Ecology and Aquaculture, Second Edition. Amsterdam: Elsevier.
[2]  Chen X, Zhang Y, Zhang X (2008) China Agriculture Statistical Report, 2007: Ministry of Agricultue, PRC. 109 p.
[3]  Kingsley DM (1994) The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes and Development 8: 133–146.
[4]  Massagué J, Blain SW, Lo RS (2000) TGF-β signaling in growth control, cancer, and heritable disorders. Cell 103: 295–309.
[5]  ten-Dijke P, Miyazonot K, Heldin CH (1996) Signaling via hetero-oligomeric complexes of type I and type II serine/threonine kinase receptors. Current Opinion in Cell Biology 8: 139–145.
[6]  Shi Y, Massagué J (2003) Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113: 685–700.
[7]  Massagué J, Wotton D (2000) Transcriptional control by the TGF-β/Smad signaling system. The EMBO Journal 19: 1745–1754.
[8]  Massagué J (1996) TGF-β Signaling: Receptors, Transducers, and Mad Proteins. Cell 85: 947–950.
[9]  Massagué J, Chen YG (2000) Controlling TGF-β signaling. Genes and Development 14: 627–644.
[10]  Kaklamani VG, Pasche B (2004) Role of TGF-β in cancer and the potential for therapy and prevention. Expert Review of Anticancer Therapy 4: 649–661.
[11]  Kollias HD, McDermott JC (2008) Transforming growth factor-β and myostatin signaling in skeletal muscle. Journal of Applied Physiology 104: 579–587.
[12]  Massagué J (1998) TGF-β signal transduction. Annual Review of Biochemistry 67: 753–791.
[13]  Loeys B, Chen J, Neptune ER, Judge DP, Podowski M, et al. (2005) A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nature Genetics 37: 275–281.
[14]  Valle L, Serena-Acedo T, Liyanarachchi S, Hampel H, Comeras I, et al. (2008) Germline allele-specific expression of TGFBR1 confers an increased risk of colorectal cancer. Science 321: 1361–1365.
[15]  Castillejo A, Mata-Balaguer T, Guarinos C, Castillejo MI, Martínez-Cantó A, et al. (2009) The Int7G24A variant of transforming growth factor-beta receptor type I is a risk factor for colorectal cancer in the male Spanish population: a case-control study. BMC Cancer 9: 406–412.
[16]  Pasche B, Wisinski KB, Sadim M, Kaklamani V, Pennison MJ, et al. (2010) Constitutively decreased TGFBR1 allelic expression is a common finding in colorectal cancer and is associated with three TGFBR1 SNPs. Journal of Experimental & Clinical Cancer Research 29: 57–62.
[17]  Kopecny M, Stratil A, Poucke MV, Bartenschlager H, Geldermann H, et al. (2004) PCR-RFLPs, linkage and RH mapping of the porcine TGFB1 and TGFBR1 genes. Animal Genetics 35: 253–255.
[18]  Hu Z, Dracheva S, Jang W, Maglott D, Bastiaansen J, et al. (2005) A QTL resource and comparison tool for pigs: PigQTLDB. Mammalian Genome 15: 792–800.
[19]  Shimanuki S, Mikawa A, Miyake Y, Hamasima N, Mikawa S, et al. (2005) Structure and polymorphism analysis of transforming growth factor beta receptor 1 (TGFBR1) in pigs. Biochemical Genetics 43: 491–500.
[20]  Chen K, Hawken R, Flickinger GH, Rodriguez-Zas SL, Rund LA, et al. (2012) Association of the porcine transforming growth factor beta type I receptor (TGFBR1) gene with growth and carcass traits. Animal Biotechnology 23: 43–63.
[21]  Herpin A, Favrel P, Cunningham C (2002) Gene structure and expression of cg-ALR1, a type I activin-like receptor from the bivalve mollusc Crassostrea gigas. Gene 301: 21–30.
[22]  Herpin A, Lelong C, Favrel P (2004) Transforming growth factor-β-related proteins: an ancestral and widespread superfamily of cytokines in metazoans. Developmental and Comparative Immunology 28: 461–485.
[23]  Herpin A, Lelong C, Becker T, Rosa FM, Favrel P, et al. (2005) Structural and functional evidences for a type 1 TGF-β sensu stricto receptor in the lophotrochozoan Crassostrea gigas suggest conserved molecular mechanisms controlling mesodermal patterning across bilateria. Mechanisms of Development 122: 695–705.
[24]  Herpin A, Lelong C, Becker T, Rosa F, Favrel P, et al. (2005) Structural and functional evidence for a singular repertoire of BMP receptor signal transducing proteins in the lophotrochozoan Crassostrea gigas suggests a shared ancestral BMP/activin pathway. The FEBS Journal 272: 3424–3440.
[25]  Le-Quéré H, Herpin A, Huvet A, Lelong C, Favrel P (2009) Structural and functional characterizations of an Activin type II receptor orthologue from the Pacific oyster Crassostrea gigas. Gene 436: 101–107.
[26]  Miyashita T, Hanashita T, Toriyama M, Takagi R, Akashika T, et al. (2008) Gene cloning and biochemical characterization of the BMP-2 of Pinctada fucata. Bioscience Biotechnology and Biochemistry 72: 37–47.
[27]  Zhou Y, He Z, Li Q, Xie L, Zhang R (2008) Cloning and expression pattern of a Smad3 homolog from the Pearl oyster, Pinctada fucata. Acta Biochimica et Biophysica Sinica 40: 244–252.
[28]  Zhou Y, He Z, Huang J, Gong N, Yan Z, et al. (2010) Cloning and characterization of the activin like receptor 1 homolog (Pf-ALR1) in the Pearl oyster, Pinctada fucata. Comparative Biochemistry and Physiology, Part B 156: 158–167.
[29]  Kim HW, Mykles DL, Goetz FW, Roberts SB (2004) Characterization of a myostatin-like gene from the bay scallop, Argopecten irradians. Biochimica et Biophysica Acta 1679: 174–179.
[30]  Hu X, Guo H, He Y, Wang S, Zhang L, et al. (2010) Molecular characterization of myostatin gene from Zhikong scallop Chlamys farreri (Jones et Preston 1904). Genes and Genetic Systems 85: 207–218.
[31]  Wang X, Meng X, Song B, Qiu X, Liu H (2010) SNPs in the myostatin gene of the mollusk Chlamys farreri: association with growth traits. Comparative Biochemistry and Physiology, Part B 155: 327–330.
[32]  Guo L, Li L, Zhang S, Guo X, Zhang G (2011) Novel polymorphisms in the myostatin gene and their association with growth traits in a variety of bay scallop, Argopecten irradians. Animal Genetics 42: 339–340.
[33]  Sambrook J (2001) Molecular Cloning: A Laboratory Mannual, Third Edition. New York: Cold Spring Harbor Laboratory Press.
[34]  Wang S, Zhang L, Meyer E, Matz MV (2009) Construction of a high-resolution genetic linkage map and comparative genome analysis for the reef-building coral Acropora millepora. Genome Biology 10: R126.
[35]  Lin J, Yao D, Qian J, Chen Q, Qian W, et al. (2011) Recurrent DNMT3A R882 Mutations in Chinese Patients with Acute Myeloid Leukemia and Myelodysplastic Syndrome. PLoS ONE 6: e26906.
[36]  Wang S, Bao Z, Hu X, Shao M, Zhang L, et al. (2008) Two novel elements (CFG1 and PYG1) of Mag lineage of Ty3/Gypsy retrotransposons from Zhikong scallop (Chlamys farreri) and Japanese scallop (Patinopecten yessoensis). Genetica 133: 37–46.
[37]  Hu X, Bao Z, Hu J, Shao M, Zhang L, et al. (2006) Cloning and characterization of tryptophan 2,3-dioxygenase gene of Zhikong scallop Chlamys farreri (Jones and Preston 1904). Aquaculture Research 37: 1187–1194.
[38]  Yang J, Wang L, Zhang H, Qiu L, Wang H, et al. (2011) C-Type Lectin in Chlamys farreri (CfLec-1) Mediating Immune Recognition and Opsonization. PLoS One 6: e17089.
[39]  Zhou Z, Yang J, Wang L, Zhang H, Gao Y, et al. (2011) A Dopa Decarboxylase Modulating the Immune Response of Scallop Chlamys farreri. PLoS ONE 6: e18596.
[40]  Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. Journal of Computational Biology 12: 1047–1064.
[41]  Wrana J, Attisano L, Wieser R, Ventura F, Massagué J (1994) Mechanism of activation of the TGF-β receptor. Nature 370: 341–347.
[42]  Wrana J, Tran H, Attisano L, Arora K, Childs S, et al. (1994) Two distinct transmembrane serine/threonine kinases from Drosophila melanogaster form an activin receptor complex. Molecular and Cellular Biology 14: 944–950.
[43]  Chen YG, Hata A, Lo RS, Wotton D, Shi Y, et al. (1998) Determinants of specificity in TGF-β signal transduction. Genes and Development 12: 2144–2152.
[44]  Huse M, Chen YG, Massagué J, Kuriyan J (1999) Crystal structure of the cytoplasmic domain of the type I TGFβ receptor in complex with FKBP12. Cell 96: 425–436.
[45]  Sharp PA (1981) Speculations on RNA splicing. Cell 23: 643–646.
[46]  Roelen BA, Eijk MJV, Rooijen MAV, Bevers MM, Larson JH, et al. (1998) Molecular cloning, genetic mapping, and developmental expression of a bovine transforming growth factor beta (TGF-β) type I receptor. Molecular Reproduction and Development 49: 1–9.
[47]  Juengel JL, McNatty KP (2005) The role of proteins of the transforming growth factor-β superfamily in the intraovarian regulation of follicular development. Human Reproduction Update 11: 144–161.
[48]  Polley S, De S, Brahma B, Mukherjee A, Vinesh PV, et al. (2010) Polymorphism of BMPR1B, BMP15 and GDF9 fecundity genes in prolific Garole sheep Tropical Animal Health and Production. 42: 985–993.
[49]  Tomoda T, Kudoh T, Noma T, Nakazawa A, Muramatsu M, et al. (1994) Molecular cloning of a mouse counterpart for human TGF-β type I receptor. Biochemical and Biophysical Research Communications 198: 1054–1062.
[50]  Vellucci VF, Reiss M (1997) Cloning and genomic organization of the human transforming growth factor-β type I receptor gene. Genomics 46: 278–283.
[51]  Chen K, Rund LA, Beever JE, Schook LB (2006) Isolation and molecular characterization of the porcine transforming growth factor beta type I receptor (TGFBR1) gene. Gene 384: 62–72.
[52]  Roelen BA, Goumans MJ, Zwijsen A, Mummery CL (1998) Identification of two distinct functions for TGF-β in early mouse development. Differentiation 64: 19–31.
[53]  Aoki TO, David NB, Minchiotti G, Saint-Etienne L, Dickmeis T, et al. (2002) Molecular integration of casanova in the Nodal signalling pathway controlling endoderm formation. Development 129: 275–286.
[54]  Li Q, Agno JE, Edson MA, Nagaraja AK, Nagashima T, et al. (2011) Transforming growth factor β receptor type 1 is essential for female reproductive tract Integrity and function. PLoS Genetics 7: e1002320.
[55]  Corporeau C, Groisillier A, Jeudy A, Barbeyron T, Fleury E, et al. (2011) A functional study of transforming growth factor-beta from the gonad of Pacific Oyster Crassostrea gigas. Marine Biotechnology 13: 971–980.
[56]  Lafyatis R, Lechleider R, Roberts AB, Sporn MB (1991) Secretion and transcriptional regulation of transforming growth factor-β3 during myogenesis. Molecular and Cellular Biology 11: 3795–3803.
[57]  Koishi K, Dalzell KG, McLennan IS (2000) The expression and structure of TGF-β2 transcripts in rat muscles. Biochimica et Biophysica Acta 1492: 311–319.
[58]  Rodgers BD, Garikipati DK (2008) Clinical, agricultural, and evolutionary biology of myostatin: a comparative review. Endocrine Reviews 29: 513–534.
[59]  Liu D, Black BL, Derynck R (2001) TGF-β inhibits muscle differentiation through functional repression of myogenic transcription factors by Smad3. Genes and Development 15: 2950–2966.
[60]  Schabort EJ, Merwe Mvd, Loos B, Moore FP, Niesler CU (2009) TGF-β’s delay skeletal muscle progenitor cell differentiation in an isoform-independent manner. Experimental Cell Research 315: 373–384.
[61]  Maehr T, Wang TH, Vecino JLG, Wadsworth S, Secombes CJ (2011) Cloning and expression analysis of the transforming growth factor-beta receptors type 1 and 2 in the rainbow trout Oncorhynchus mykiss. Developmental and Comparative Immunology: In press.
[62]  Liu X, Chang Y, Xiang J, Song J, Ding J (2002) Analysis of effects of shell size characters on live weight in Chinese scallop Chlamys Farreri. Oceanologia et Limnologia Sinica 33: 673–677.

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