Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 7 February 1986:
Vol. 231. no. 4738, pp. 597 - 600
DOI: 10.1126/science.3945800
Prev | Table of Contents | Next

Articles

Science, Vol 231, Issue 4738, 597-600
Copyright © 1986 by American Association for the Advancement of Science

articles

All members of the MHC multigene family respond to thyroid hormone in a highly tissue-specific manner

S Izumo, B Nadal-Ginard, and V Mahdavi

In mammals different isoforms of myosin heavy chain are encoded by the members of a multigene family. The expression of each gene of this family is regulated in a tissue- and developmental stage-specific manner as well as by hormonal and various pathological stimuli. In this study the molecular basis of isoform switches induced in myosin heavy chain by thyroid hormone was investigated. The expression of the myosin heavy chain gene family was analyzed in seven different muscles of adult rats subjected to hypo- or hyperthyroidism with complementary DNA probes specific for six different myosin heavy chain genes. The results demonstrate that all six genes are responsive to thyroid hormone. More interestingly, the same myosin heavy chain gene can be regulated by thyroid hormone in highly different modes, even in opposite directions, depending on the tissue in which it is expressed. Furthermore, the skeletal embryonic and neonatal myosin heavy chain genes, so far considered specific to these two developmental stages, can be reinduced by hypothyroidism in specific adult muscles.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Influence of hyperthyroid conditions on gene expression in extraocular muscles of rats.
T. S. Postler, M. T. Budak, T. S. Khurana, and N. A. Rubinstein (2009)
Physiol Genomics 37, 231-238
   Abstract »    Full Text »    PDF »
Cellular and Molecular Basis of Deiodinase-Regulated Thyroid Hormone Signaling.
B. Gereben, A. M. Zavacki, S. Ribich, B. W. Kim, S. A. Huang, W. S. Simonides, A. Zeold, and A. C. Bianco (2008)
Endocr. Rev. 29, 898-938
   Abstract »    Full Text »    PDF »
Developmental effects on myonuclear domain size of rat diaphragm fibers.
C. B. Mantilla, R. V. Sill, B. Aravamudan, W.-Z. Zhan, and G. C. Sieck (2008)
J Appl Physiol 104, 787-794
   Abstract »    Full Text »    PDF »
The expression of NFATc1 in adult rat skeletal muscle fibres.
G. Mutungi (2008)
Exp Physiol 93, 399-406
   Abstract »    Full Text »    PDF »
Thyroid hormone is required for the phenotype transitions induced by the pharmacological inhibition of calcineurin in adult soleus muscle of rats.
N. Koulmann, L. Bahi, F. Ribera, H. Sanchez, B. Serrurier, R. Chapot, A. Peinnequin, R. Ventura-Clapier, and X. Bigard (2008)
Am J Physiol Endocrinol Metab 294, E69-E77
   Abstract »    Full Text »    PDF »
Calcium-Independent Negative Inotropy by {beta}-Myosin Heavy Chain Gene Transfer in Cardiac Myocytes.
T. J. Herron, R. Vandenboom, E. Fomicheva, L. Mundada, T. Edwards, and J. M. Metzger (2007)
Circ. Res. 100, 1182-1190
   Abstract »    Full Text »    PDF »
Mechanisms underlying myosin heavy chain expression during development of the rat diaphragm muscle.
P. C. Geiger, J. P. Bailey, C. B. Mantilla, W.-Z. Zhan, and G. C. Sieck (2006)
J Appl Physiol 101, 1546-1555
   Abstract »    Full Text »    PDF »
Thyroid hormone downregulates the expression and function of sarcoplasmic reticulum-associated CaM kinase II in the rabbit heart.
M. Jiang, A. Xu, and N. Narayanan (2006)
Am J Physiol Heart Circ Physiol 291, H1384-H1394
   Abstract »    Full Text »    PDF »
Avian MyoD and c-Jun Coordinately Induce Transcriptional Activity of the 3,5,3'-Triiodothyronine Nuclear Receptor c-ErbA{alpha}1 in Proliferating Myoblasts.
M. Busson, L. Daury, P. Seyer, S. Grandemange, L. Pessemesse, F. Casas, C. Wrutniak-Cabello, and G. Cabello (2006)
Endocrinology 147, 3408-3418
   Abstract »    Full Text »    PDF »
Regulation of antisense RNA expression during cardiac MHC gene switching in response to pressure overload.
F. Haddad, A. X. Qin, P. W. Bodell, L. Y. Zhang, H. Guo, J. M. Giger, and K. M. Baldwin (2006)
Am J Physiol Heart Circ Physiol 290, H2351-H2361
   Abstract »    Full Text »    PDF »
Fiber-type Composition of the Human Jaw Muscles--(Part 2) Role of Hybrid Fibers and Factors Responsible for Inter-individual Variation.
J.A.M Korfage, J.H. Koolstra, G.E.J. Langenbach, and T.M.G.J. van Eijden (2005)
Journal of Dental Research 84, 784-793
   Abstract »    Full Text »    PDF »
Aberrant expression of myosin isoforms in skeletal muscles from mice lacking the rev-erbA{alpha} orphan receptor gene.
P. Pircher, P. Chomez, F. Yu, B. Vennstrom, and L. Larsson (2005)
Am J Physiol Regulatory Integrative Comp Physiol 288, R482-R490
   Abstract »    Full Text »    PDF »
Coordinate downregulation of CaM kinase II and phospholamban accompanies contractile phenotype transition in the hyperthyroid rabbit soleus.
M. Jiang, A. Xu, D.L. Jones, and N. Narayanan (2004)
Am J Physiol Cell Physiol 287, C622-C632
   Abstract »    Full Text »    PDF »
Thyroid Hormone Resistance in the Heart: Role of the Thyroid Hormone Receptor {beta} Isoform.
T. M. Ortiga-Carvalho, K. Hashimoto, C. C. Pazos-Moura, D. Geenen, R. Cohen, R. M. Lang, and F. E. Wondisford (2004)
Endocrinology 145, 1625-1633
   Abstract »    Full Text »    PDF »
Role of Antisense RNA in Coordinating Cardiac Myosin Heavy Chain Gene Switching.
F. Haddad, P. W. Bodell, A. X. Qin, J. M. Giger, and K. M. Baldwin (2003)
J. Biol. Chem. 278, 37132-37138
   Abstract »    Full Text »    PDF »
Regulation of myosin expression during myotome formation.
L. D. Sacks, G. M. Cann, W. Nikovits Jr, S. Conlon, N. R. Espinoza, and F. E. Stockdale (2003)
Development 130, 3391-3402
   Abstract »    Full Text »    PDF »
Effects of thyroxine on myosin isoform expression and mechanical properties in guinea-pig smooth muscle.
M. Lofgren, K. Fagher, G. Woodard, and A. Arner (2002)
J. Physiol. 543, 757-766
   Abstract »    Full Text »    PDF »
Effects of Aging on Human Skeletal Muscle Myosin Heavy-Chain mRNA Content and Protein Isoform Expression.
J. O. Marx, W. J. Kraemer, B. C. Nindl, and L. Larsson (2002)
J. Gerontol. A Biol. Sci. Med. Sci. 57, B232-238
   Abstract »    Full Text »
Differing mechanisms of cold-induced changes in capillary supply in m. tibialis anterior of rats and hamsters.
D. Deveci and S. Egginton (2002)
J. Exp. Biol. 205, 829-840
   Abstract »    Full Text »    PDF »
Thyroid Hormone Export Varies among Primary Cells and Appears to Differ from Hormone Uptake.
F. A. R. Neves, R. R. Cavalieri, L. A. Simeoni, D. G. Gardner, J. D. Baxter, B. F. Scharschmidt, N. Lomri, and R. C. J. Ribeiro (2002)
Endocrinology 143, 476-483
   Abstract »    Full Text »    PDF »
TRs Have Common and Isoform-Specific Functions in Regulation of the Cardiac Myosin Heavy Chain Genes.
A. Mansen, F. Yu, D. Forrest, L. Larsson, and B. Vennstrom (2001)
Mol. Endocrinol. 15, 2106-2114
   Abstract »    Full Text »    PDF »
Altered K+ channel gene expression in diabetic rat ventricle: isoform switching between Kv4.2 and Kv1.4.
A. Nishiyama, D. N. Ishii, P. H. Backx, B. E. Pulford, B. R. Birks, and M. M. Tamkun (2001)
Am J Physiol Heart Circ Physiol 281, H1800-H1807
   Abstract »    Full Text »    PDF »
The {alpha}1- and {alpha}2-isoforms of Na-K-ATPase play different roles in skeletal muscle contractility.
S. He, D. A. Shelly, A. E. Moseley, P. F. James, J. H. James, R. J. Paul, and J. B. Lingrel (2001)
Am J Physiol Regulatory Integrative Comp Physiol 281, R917-R925
   Abstract »    Full Text »    PDF »
Developmental expression analysis of thyroid hormone receptor isoforms reveals new insights into their essential functions in cardiac and skeletal muscles.
P. WHITE, K. A. BURTON, A. L. FOWDEN, and M. J. DAUNCEY (2001)
FASEB J 15, 1367-1376
   Abstract »    Full Text »    PDF »
Increased Expression of Thyroid Hormone Receptor Isoforms in End-Stage Human Congestive Heart Failure.
G. d’Amati, C. R. T. di Gioia, D. Mentuccia, D. Pistilli, L. Proietti-Pannunzi, F. Miraldi, P. Gallo, and F. S. Celi (2001)
J. Clin. Endocrinol. Metab. 86, 2080-2084
   Abstract »    Full Text »
In vivo regulation of the {beta}-myosin heavy chain gene in hypertensive rodent heart.
C. E. Wright, P. W. Bodell, F. Haddad, A. X. Qin, and K. M. Baldwin (2001)
Am J Physiol Cell Physiol 280, C1262-C1276
   Abstract »    Full Text »    PDF »
Plasticity in Skeletal, Cardiac, and Smooth Muscle: Invited Review: Plasticity and energetic demands of contraction in skeletal and cardiac muscle.
G. C. Sieck and M. Regnier (2001)
J Appl Physiol 90, 1158-1164
   Abstract »    Full Text »    PDF »
Molecular cloning and sequence of Sparus aurata skeletal myosin light chains expressed in white muscle: developmental expression and thyroid regulation.
K. A. Moutou, A. V. M. Canario, Z. Mamuris, and D. M. Power (2001)
J. Exp. Biol. 204, 3009-3018
   Abstract »    Full Text »    PDF »
Plasticity in Skeletal, Cardiac, and Smooth Muscle: Invited Review: Effects of different activity and inactivity paradigms on myosin heavy chain gene expression in striated muscle.
K. M. Baldwin and F. Haddad (2001)
J Appl Physiol 90, 345-357
   Abstract »    Full Text »    PDF »
Molecular Regulation of Tongue and Craniofacial Muscle Differentiation.
C.F. Shuler and K.R. Dalrymple (2001)
Critical Reviews in Oral Biology & Medicine 12, 3-17
   Abstract »    Full Text »    PDF »
Type 2 Iodothyronine Deiodinase Transgene Expression in the Mouse Heart Causes Cardiac-Specific Thyrotoxicosis.
J. Pachucki, J. Hopkins, R. Peeters, H. Tu, S. D. Carvalho, H. Kaulbach, E. D. Abel, F. E. Wondisford, J. S. Ingwall, and P. R. Larsen (2001)
Endocrinology 142, 13-20
   Abstract »    Full Text »    PDF »
Independent Signals Control Expression of the Calcineurin Inhibitory Proteins MCIP1 and MCIP2 in Striated Muscles.
J. Yang, B. Rothermel, R. B. Vega, N. Frey, T. A. McKinsey, E. N. Olson, R. Bassel-Duby, and R. S. Williams (2000)
Circ. Res. 87 , e61-e68
   Abstract »    Full Text »    PDF »
Denervation alters myosin heavy chain expression and contractility of developing rat diaphragm muscle.
G. C. Sieck and W.-Z. Zhan (2000)
J Appl Physiol 89, 1106-1113
   Abstract »    Full Text »    PDF »
Single-Fiber Myosin Heavy-Chain Isoform Composition of Rodent Laryngeal Muscle: Modulation by Thyroid Hormone.
Y. Z. Wu, M. J. Baker, R. L. Crumley, and V. J. Caiozzo (2000)
Arch Otolaryngol Head Neck Surg 126, 874-880
   Abstract »    Full Text »    PDF »
Effects of thyroid hormone receptor gene disruption on myosin isoform expression in mouse skeletal muscles.
F. Yu, S. Gothe, L. Wikstrom, D. Forrest, B. Vennstrom, and L. Larsson (2000)
Am J Physiol Regulatory Integrative Comp Physiol 278, R1545-R1554
   Abstract »    Full Text »    PDF »
Fiber-type-specific alpha B-crystallin distribution and its shifts with T3 and PTU treatments in rat hindlimb muscles.
Y. Atomi, K. Toro, T. Masuda, and H. Hatta (2000)
J Appl Physiol 88, 1355-1364
   Abstract »    Full Text »    PDF »
MHC polymorphism in rodent plantaris muscle: effects of mechanical overload and hypothyroidism.
V. J. Caiozzo, F. Haddad, M. Baker, S. McCue, and K. M. Baldwin (2000)
Am J Physiol Cell Physiol 278, C709-C717
   Abstract »    Full Text »    PDF »
Single-fiber myosin heavy chain polymorphism during postnatal development: modulation by hypothyroidism.
N. A. di Maso, V. J. Caiozzo, and K. M. Baldwin (2000)
Am J Physiol Regulatory Integrative Comp Physiol 278, R1099-R1106
   Abstract »    Full Text »    PDF »
Cardiac Dysfunction Caused by Myocardium-Specific Expression of a Mutant Thyroid Hormone Receptor.
C. Pazos-Moura, E. D. Abel, M.-E. Boers, E. Moura, T. G. Hampton, J. Wang, J. P. Morgan, and F. E. Wondisford (2000)
Circ. Res. 86, 700-706
   Abstract »    Full Text »    PDF »
Thyroid hormones differentially modulate enolase isozymes during rat skeletal and cardiac muscle development.
T. Merkulova, A. Keller, P. Oliviero, F. Marotte, J.-L. Samuel, L. Rappaport, N. Lamande, and M. Lucas (2000)
Am J Physiol Endocrinol Metab 278, E330-E339
   Abstract »    Full Text »    PDF »
Myosin heavy chains in fibers of TTX-paralyzed rat soleus and medial gastrocnemius muscles.
B. Cormery, F. Pons, J.-F. Marini, and P. F. Gardiner (2000)
J Appl Physiol 88, 66-76
   Abstract »    Full Text »    PDF »
Growth Hormone Improves Body Mass Recovery with Refeeding after Chronic Undernutrition-Induced Muscle Atrophy in Aging Male Rats.
B. T. Ameredes, J. F. Watchko, M. J. Daood, J. F. Rosas, M. P. Donahoe, and R. M. Rogers (1999)
J. Nutr. 129, 2264-2270
   Abstract »    Full Text »
Growth hormone restores aged diaphragm myosin composition and performance after chronic undernutrition.
B. T. Ameredes, J. F. Watchko, M. J. Daood, J. F. Rosas, M. P. Donahoe, and R. M. Rogers (1999)
J Appl Physiol 87, 1253-1259
   Abstract »    Full Text »    PDF »
Thyroid Hormone Regulates Hyperpolarization-Activated Cyclic Nucleotide-Gated Channel (HCN2) mRNA in the Rat Heart.
J. Pachucki, L. A. Burmeister, and P. R. Larsen (1999)
Circ. Res. 85, 498-503
   Abstract »    Full Text »    PDF »
Evidence for a Novel Cardiac-enriched Retinoid X Receptor Partner.
S. Cresci, M. L. Clabby, and D. P. Kelly (1999)
J. Biol. Chem. 274, 25668-25674
   Abstract »    Full Text »    PDF »
In vivo regulation of beta -MHC gene in rodent heart: role of T3 and evidence for an upstream enhancer.
C. E. Wright, F. Haddad, A. X. Qin, P. W. Bodell, and K. M. Baldwin (1999)
Am J Physiol Cell Physiol 276, C883-C891
   Abstract »    Full Text »    PDF »
Changes in satellite cell content and myosin isoforms in low-frequency-stimulated fast muscle of hypothyroid rat.
C. T. Putman, S. Dusterhoft, and D. Pette (1999)
J Appl Physiol 86, 40-51
   Abstract »    Full Text »    PDF »
Interaction of hyperthyroidism and hindlimb suspension on skeletal myosin heavy chain expression.
F. Haddad, A. X. Qin, M. Zeng, S. A. McCue, and K. M. Baldwin (1998)
J Appl Physiol 85, 2227-2236
   Abstract »    Full Text »    PDF »
Novel transitions in MHC isoforms: separate and combined effects of thyroid hormone and mechanical unloading.
V. J. Caiozzo, M. J. Baker, and K. M. Baldwin (1998)
J Appl Physiol 85, 2237-2248
   Abstract »    Full Text »    PDF »
Tissue-Restricted Expression of the Cardiac alpha -Myosin Heavy Chain Gene Is Controlled by a Downstream Repressor Element Containing a Palindrome of Two Ets-Binding Sites.
M. Gupta, R. Zak, T. A. Libermann, and M. P. Gupta (1998)
Mol. Cell. Biol. 18, 7243-7258
   Abstract »    Full Text »
Effects of thyroid status on expression of voltage-gated potassium channels in rat left ventricle.
A. Nishiyama, F. Kambe, K. Kamiya, H. Seo, and J. Toyama (1998)
Cardiovasc Res 40, 343-351
   Abstract »    Full Text »    PDF »
Proximal Sequences of the Aldolase A Fast Muscle-specific Promoter Direct Nerve- and Activity-dependent Expression in Transgenic Mice.
F. Spitz, Z. A. De Vasconcelos, F. Chatelet, J. Demignon, A. Kahn, J.-C. Mira, P. Maire, and D. Daegelen (1998)
J. Biol. Chem. 273, 14975-14981
   Abstract »    Full Text »    PDF »
Thyroid receptor plasticity in striated muscle types: effects of altered thyroid state.
F. Haddad, A. X. Qin, S. A. McCue, and K. M. Baldwin (1998)
Am J Physiol Endocrinol Metab 274, E1018-E1026
   Abstract »    Full Text »    PDF »
Myosin Heavy Chains IIa and IId Are Functionally Distinct in the Mouse.
C. A. Sartorius, B. D. Lu, L. Acakpo-Satchivi, R. P. Jacobsen, W. C. Byrnes, and L. A. Leinwand (1998)
J. Cell Biol. 141, 943-953
   Abstract »    Full Text »    PDF »
Reappearance of the minor alpha -sarcomeric actins in postnatal muscle.
T. Collins, J. E. Joya, R. M. Arkell, V. Ferguson, and E. C. Hardeman (1997)
Am J Physiol Cell Physiol 273, C1801-C1810
   Abstract »    Full Text »    PDF »
Neurotrophin-3-enhanced Nerve Regeneration Selectively Improves Recovery of Muscle Fibers Expressing Myosin Heavy Chains 2b.
G.D. Sterne, G.R. Coulton, R.A. Brown, C.J. Green, and G. Terenghi (1997)
J. Cell Biol. 139, 709-715
   Abstract »    Full Text »    PDF »
Analysis of myosin heavy chain mRNA expression by RT-PCR.
C. Wright, F. Haddad, A. X. Qin, and K. M. Baldwin (1997)
J Appl Physiol 83, 1389-1396
   Abstract »    Full Text »    PDF »
Gender-specific effects of dexamethasone treatment on rat diaphragm structure and function.
D. J. Prezant, M. L. Karwa, B. Richner, D. Maggiore, E. I. Gentry, and J. Cahill (1997)
J Appl Physiol 82, 125-133
   Abstract »    Full Text »    PDF »
Isolation and Characterization of an Avian Slow Myosin Heavy Chain Gene Expressed during Embryonic Skeletal Muscle Fiber Formation.
W. Nikovits Jr., G. F. Wang, J. L. Feldman, J. B. Miller, R. Wade, L. Nelson, and F. E. Stockdale (1996)
J. Biol. Chem. 271, 17047-17056
   Abstract »    Full Text »    PDF »
Molecular characterization of a developmentally regulated porcine skeletal myosin heavy chain gene and its 5' regulatory region.
K. Chang, K Fernandes, and M. Dauncey (1995)
J. Cell Sci. 108, 1779-1789
   Abstract »    PDF »
Complex fiber-type-specific expression of fast skeletal muscle troponin I gene constructs in transgenic mice.
P. Hallauer, H. Bradshaw, and K. Hastings (1993)
Development 119, 691-701
   Abstract »    PDF »
Selective accumulation of MyoD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormones.
S. Hughes, J. Taylor, S. Tapscott, C. Gurley, W. Carter, and C. Peterson (1993)
Development 118, 1137-1147
   Abstract »    PDF »
Developmental modulation of myosin expression by thyroid hormone in avian skeletal muscle.
M. Gardahaut, J Fontaine-Perus, T Rouaud, E Bandman, and R Ferrand (1992)
Development 115, 1121-1131
   Abstract »    PDF »
Response and Binding Elements for Ligand-dependent Positive Transcription Factors Integrate Positive and Negative Regulation of Gene Expression.
M.G. Rosenfeld, C.K. Glass, S. Adler, E.B. Crenshaw III, X. He, S.A. Lira, H.P. Elsholtz, H.J. Mangalam, J.M. Holloway, C. Nelson, et al. (1988)
Cold Spring Harb Symp Quant Biol 53, 545-556
   Abstract »    PDF »
Effects of hypothyroidism on maximum specific force in rat diaphragm muscle fibers.
P. C. Geiger, M. J. Cody, Y. S. Han, L. W. Hunter, W.-Z. Zhan, and G. C. Sieck (2002)
J Appl Physiol 92, 1506-1514
   Abstract »    Full Text »    PDF »
Irx4 Forms an Inhibitory Complex with the Vitamin D and Retinoic X Receptors to Regulate Cardiac Chamber-specific slow MyHC3 Expression.
G. F. Wang, W. Nikovits Jr., Z.-Z. Bao, and F. E. Stockdale (2001)
J. Biol. Chem. 276, 28835-28841
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)