Abstract
Adult myogenesis responsible for the maintenance and repair of muscle tissue is mainly under the control of myogenic regulatory factors (MRFs) and a few other genes. Transthyretin gene (TTR), codes for a carrier protein for thyroxin (T4) and retinol binding protein bound with retinol in blood plasma, plays a critical role during the early stages of myogenesis. Herein, we investigated the relationship of TTR with other muscle-specific genes and report their expression in muscle satellite cells (MSCs), and increased messenger RNA (mRNA) and protein expression of TTR during MSCs differentiation. Silencing of TTR resulted in decreased myotube formation and decreased expression of myosin light chain (MYL2), myosin heavy chain 3 (MYH3), matrix gla protein (MGP), and voltage-dependent L type calcium channel (Cav1.1) genes. Increased mRNA expression observed in TTR and other myogenic genes with the addition of T4 decreased significantly following TTR knockdown, indicating the critical role of TTR in T4 transportation. Similarly, decreased expression of MGP and Cav1.1 following TTR knockdown signifies the dual role of TTR in controlling muscle myogenesis via regulation of T4 and calcium channel. Our computational and experimental evidences indicate that TTR has a relationship with MRFs and may act on calcium channel and related genes.
Similar content being viewed by others
References
Anderson JE (2000) A role for nitric oxide in muscle repair: Nitric oxide-mediated activation of muscle satellite cells. Mol Biol Cell 11:1859–1874
Asakura A (2003) Stem cells in adult skeletal muscle. Trends Cardiovasc Med 13:123–128
Beermann DH, Liboff M, Wilson DB, Hood LF (1983) Effects of exogenous thyroxine and growth hormone on satellite cell and myonuclei populations in rapidly growing rat skeletal muscle. Growth 47:426–436
Berchtold MW, Brinkmeier H, Müntener M (2000) Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol Rev 80:1215–1265
Berkes CA, Tapscott SJ (2005) MyoD and the transcriptional control of myogenesis. Semin Cell Dev Biol 16:585–595
Bidaud I, Monteil A, Nargeot J, Lory P (2006) Properties and role of voltage-dependent calcium channels during mouse skeletal muscle differentiation. J Muscle Res Cell Motil 27:75–81
Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Chargé SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238
Chen X, Li Y (2009) Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis. Cell Adhes Migr 3:337–341
Cheng SY, Leonard JL, Davis PJ (2010) Molecular aspects of thyroid hormone actions. Endocr Rev 31:139–170
Episkopou V, Maeda S, Nishiguchi S, Shimada K, Gaitanaris GA, Gottesman ME, Robertson EJ (1993) Disruption of the transthyretin gene results in mice with depressed levels of plasma retinol and thyroid hormone. Proc Natl Acad Sci U S A 90:2375–2379
Farzaneh-Far A, Proudfoot D, Peter L, Weissberg, Catherine MS (2000) Matrix Gla protein is regulated by a mechanism functionally related to the calcium-sensing receptor. Biochem Biophys Res Commun 277:736–740
Florini JR, Ewton DZ, Magri KA (1991) Hormones, growth factors, and myogenic differentiation. Ann Rev Physiol 53:201–216
Fraser JD, Price PA (1988) Lung, heart, and kidney express high levels of mRNA for the vitamin K-dependent matrix Gla protein. Implications for the possible functions of matrix Gla protein and for the tissue distribution of the gamma-carboxylase. J Biol Chem 263:11033–11036
Guerin C, Kramer S (2009) Cytoskeletal remodeling during myotube assembly and guidance: Coordinating the actin and microtubule networks. Commun Integr Biol 2:452–457
Hagiwara Y, Ozawa E (2008) Class specificity of avian and mammalian sera in regards to myogenic cell growth in vitro. possible role of transferrin in the specificity. Develop Growth Differ 24:115–123
Hara M, Tabata K, Suzuki T, Do MK, Mizunoya W, Nakamura M, Nishimura S, Tabata S, Ikeuchi Y, Sunagawa K, Anderson JE, Allen RE, Tatsumi R (2012) Calcium influx through a possible coupling of cation channels impacts skeletal muscle satellite cell activation in response to mechanical stretch. Am J Physiol Cell Physiol 302:C1741–C1750
Hauser J, Saarikettu J, Grundström T (2008) Calcium regulation of myogenesis by differential calmodulin inhibition of basic helix-loop-helix transcription factors. Mol Biol Cell 19:2509–2519
Heidt AB, Rojas A, Harris IS, Black BL (2007) Determinants of myogenic specificity within MyoD are required for noncanonical E box binding. Mol Cell Biol 27:5910–5920
Herbert J, Wilcox JN, Pham KT, Fremeau RT Jr, Zeviani M, Dwork A, Soprano DR, Makover A, Goodman DS, Zimmerman EA et al (1986) Transthyretin: a choroid plexus-specific transport protein in human brain. Neurology 36:900–911
Ho JWK, Stefani M, Remedios CG, Charleston MA (2008) Differential variability analysis of gene expression and its application to human diseases. Bioinformatics 24:390–398
Khan A, Wang W, Khan S R (2013) Calcium oxalate nephrolithiasis and expression of matrix GLA protein in the kidneys. World J Urol
Kumar D, Shadrach JL, Wagers AJ, Lassar AB (2009) Id3 is a direct transcriptional target of Pax7 in quiescent satellite cells. Mol Biol Cell 20:3170–3177
Lee EJ, Shin YM, Lee HJ, Yoon DH, Chun TH, Lee YS, Choi I (2010) Identification of cuts-specific myogenic marker genes in Hanwoo by DNA microarray. J Anim Sci Technol 52:329–336
Lee EJ, Lee HJ, Kamli MR, Pokharel S, Bhat AR, Lee YH (2012a) Depotspecific gene expression profiles during differentiation and transdifferentiation of bovine muscle satellite cells, and differentiation of preadipocytes. Genomics 100:195–202
Lee EJ, Kamli MR, Bhat AR, Pokharel S, Lee DM, Ki SH, Kim TI, Hong S, Choi I (2012b) Effect of porcine placenta steroid extract on myogenic satellite cell proliferation, transdifferentiation, and lipid accumulation. In Vitro Cell Dev Biol Anim 48:326–333
Lee EJ, Bhat AR, Kamli MR, Pokharel S, Chun T, Lee YH, Nahm SS, Nam JH, Hong SK, Yang B, Chung KY, Kim SH, Choi I (2013a) Transthyretin is a key regulator of myoblast differentiation. PLoS ONE 22:e63627
Lee EJ, Kamli MR, Pokharel S, Malik A, Tareq KMA, Bhat AR, Park HB, Lee SY, Kim SH, Yang B, Tirosh S, Jeong KY, Choi I (2013b) Expressed sequence tags for bovine muscle satellite cells, Myotube formed-cells and adipocyte-like cells. PLoS ONE 8:e79780
Lipscombe D, Helton TD, Xu W (2004) L-type calcium channels: the low down. J Neurophysiol 92:2633–2641
Lu X, Gao B, Yasui T, Li Y, Liu T, Mao X, Hirose M, Wu Y, Yu D, Zhu Q, Kohri K, Xiao C (2013) Matrix Gla protein is involved in crystal formation in kidney of hyperoxaluric rats. Kidney Blood Press Res 37:15–23
Merkulova T, Keller A, Oliviero P, Marotte F, Samuel JL, Rappaport L, Lamandé N, Lucas M (2000) Thyroid hormones differentially modulate enolase isozymes during rat skeletal and cardiac muscle development. Am J Physiol Endocrinol Metab 278:E330–E339
Miller KJ, Thaloor D, Matteson S, Pavlath GK (2000) Hepatocyte growth factor affects satellite cell activation and differentiation in regenerating skeletal muscle. Am J Physiol Cell Physiol 278:C174–C181
Mizuno R, Cavallaro T, Herbert J (1992) Temporal expression of the transthyretin gene in the developing rat eye. Invest Ophthalmol Vis Sci 33:341–349
Monaco HL (2000) The transthyretin-retinol-binding protein complex. Biochim Biophys Acta 1482:65–72
Monk JA, Sims NA, Dziegielewska KM, Weiss RE, Ramsay RG, Richardson SJ (2012) Delayed development of specific thyroid hormone-regulated events in transthyretin null mice. Am J Physiol Endocrinol Metab 304:E23–E31
Moran JL, Li Y, Hill AA, Mounts WM, Miller CP (2002) Gene expression changes during mouse skeletal myoblast differentiation revealed by transcriptional profiling. Physiol Genomics 10:103–111
Myung N, Connelly S, Kim B, Park SJ, Wilson IA, Kelly JW, Choi S (2013) Bifunctional coumarin derivatives that inhibit transthyretin amyloidogenesis and serve as fluorescent transthyretin folding sensors. Chem Commun (Camb) 49:9188–9190
Olguin HC, Yang Z, Tapscott SJ, Olwin BB (2007) Reciprocal inhibition between Pax7 and muscle regulatory factors modulates myogenic cell fate determination. J Cell Biol 177:769–779
Palha JA, Ballinari D, Amboldi N, Cardoso I, Fernandes R, Bellotti V, Merlini G, Saraiva MJ (2000) 4'-Iodo-4'-deoxydoxorubicin disrupts the fibrillar structure of transthyretin amyloid. Am J Pathol 156:1919–1925
Péault B, Rudnicki M, Torrente Y, Cossu G, Tremblay JP, Partridge T, Gussoni E, Kunkel ML, Huard J (2007) Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 15:867–877
Przybylski RJ, Szigeti V, Davidheiser S, Kirby AC (1994) Calcium regulation of skeletal myogenesis. II. Extracellular and cell surface effects. Cell Calcium 15:132–142
Refai E, Dekki N, Yang SN, Imreh G, Cabrera O, Yu L, Yang G, Norgren S, Rössner SM, Inverardi L, Ricordi C, Olivecrona G, Andersson M, Jörnvall H, Berggren PO, Juntti-Berggren L (2005) Transthyretin constitutes a functional component in pancreatic beta-cell stimulus-secretion coupling. Proc Natl Acad Sci U S A 102:17020–17025
Richardson SJ (2007) Cell and molecular biology of transthyretin and thyroid hormones. Int Rev Cytol 258:137–193
Ruberg FL, Berk JL (2012) Transthyretin (TTR) cardiac amyloidosis. Circulation 126:1286–1300
Sabourin LA, Rudnicki MA (2000) The molecular regulation of myogenesis. Clin Genet 57:16–25
Sandra MO, Isabel C, Maria JS (2012) Transthyretin: roles in the nervous system beyond thyroxine and retinol transport. Expert Rev Endocrinol Metab 7:181–189
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504
Shin DM, Muallem S (2008) Skeletal muscle dressed in SOCs. Nat Cell Biol 10:639–641
Silaghi CN, Fodor D, Crăciun AM (2013) Circulating matrix Gla protein: a potential tool to identify minor carotid stenosis with calcification in a risk population. Clin Chem Lab Med 51:1115–1123
Sterrenburg E, Turk R, ‘t Hoen PAC, van Deutekom JC, Boer JM et al (2004) Large-scale gene expression analysis of human skeletal myoblast differentiation. Neuromuscul Disord 14:507–518
Tchkonia T, Lenburg M, Thomou T, Giorgadze N, Frampton G, Pirtskhalava T, Cartwright A, Cartwright M, Flanagan J, Karagiannides I, Gerry N, Forse RA, Tchoukalova Y, Jensen MD, Pothoulakis C, Kirkland JL (2006) Identification of depot-specific human fat cell progenitors through distinct expression profiles and developmental gene patterns. Am J Physiol Endocrinol Metab 292:E298–E307
Valmiki RR, Jang E, Inho Choi I, Heo KN, Duhak Yoon, Kim TH, Lee H (2011) Proteomic analysis of bovine muscle satellite cells during myogenic differentiation. (Report). Asian-Aust J Anim Sci 24:1288–1302
Warde-Farley D, Donaldson SL, Comes O, Zuberi K, Badrawi R, Chao P, Franz M, Grouios C, Kazi F, Lopes CT, Maitland A, Mostafavi S, Montojo J, Shao Q, Wright G, Bader GD, Morris Q (2010) The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res 38:W214–W220
Waung JA, Bassett JH, Williams GR (2012) Thyroid hormone metabolism in skeletal development and adult bone maintenance. Trends Endocrinol Metab 23:155–162
Wei B, Jin JP (2011) Troponin T isoforms and posttranscriptional modifications: Evolution, regulation and function. Arch Biochem Biophys 15:144–154
Westermark GT, Westermark P (2008) Transthyretin and amyloid in the islets of Langerhans in type-2 diabetes. Exp Diabetes Res 429274:2008
Yablonka-Reuveni Z (2011) The skeletal muscle satellite cell: Still young and fascinating at 50. J Histochem Cytochem 59:1041–1059
Zammit PS (2008) All muscle satellite cells are equal, but are some more equal than others? J Cell Sci 15:2975–2982
Zhang SZ, Xu Y, Xie HQ, Li XQ, Wei YQ, Yang ZM (2009) The possible role of myosin light chain in myoblast proliferation. Biol Res 42:121–132
Zhao J, Araki N, Nishimotom SK (1995) Quantitation of matrix Gla protein mRNA by competitive polymerase chain reaction using glyceraldehyde-3-phosphate dehydrogenase as an internal control. Gene 3:159–165
Acknowledgments
This work was supported by a grant from the BioGreen 21 Program (Project No. PJ907099), Rural Development Administration, Republic of Korea. All research materials used in this study were provided by the Bovine Genome Resources Bank, Yeungnam University, Gyeongsan, Korea.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Editor: T. Okamoto
Smritee Pokharel and Majid Rasool Kamli contributed equally to this work
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Table 1
(DOCX 13.1 kb)
Supplementary Table 2
(DOCX 21.6 kb)
Supplementary Figure 1
A) Timecourse study on MyoD on MSCs cultured for 10, 12,14, 16 and 18 days. B) T4 treatment and its effect on TTR mRNA expression at day 16. (TIFF 1.25 mb)
Fig6
A) Timecourse study on MyoD on MSCs cultured for 10, 12,14, 16 and 18 days. B) T4 treatment and its effect on TTR mRNA expression at day 16. (GIF 75.9 mb)
Rights and permissions
About this article
Cite this article
Pokharel, S., Kamli, M.R., Mir, B.A. et al. Expression of Transthyretin during bovine myogenic satellite cell differentiation. In Vitro Cell.Dev.Biol.-Animal 50, 756–765 (2014). https://doi.org/10.1007/s11626-014-9757-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11626-014-9757-y