Sarcomeric myosin expression in the tongue body of humans, macaques and rats

Cells Tissues Organs

Volumn 191, Issue 5, 2010, Pages 431-442

  Rahnert, Jill A ^a   Sokoloff, Alan J ^b   Burkholder, Thomas J ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

Myosin; PCR; Tongue

Indexed keywords

ISOPROTEIN; MESSENGER RNA; MYOSIN HEAVY CHAIN; MYOSIN HEAVY CHAIN 2A; MYOSIN HEAVY CHAIN 2B; MYOSIN HEAVY CHAIN 2X; MYOSIN HEAVY CHAIN ALPHA; MYOSIN HEAVY CHAIN BETA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; MACACA; MOVEMENT (PHYSIOLOGY); MUSCLE CELL; MUSCLE CONTRACTION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SARCOMERE; SWALLOWING; TONGUE;

AGED; AGED, 80 AND OVER; ANIMALS; FEMALE; HUMANS; MACACA MULATTA; MALE; MICE; MIDDLE AGED; MYOSIN HEAVY CHAINS; PROTEIN ISOFORMS; RATS; TONGUE;

HOMO; MACACA; MAMMALIA; RATTUS;

EID: 77951499806     PISSN: 14226405     EISSN: None     Source Type: Journal    
DOI: 10.1159/000258678     Document Type: Article

References (78)

1. Agbulut, O., P. Noirez, F. Beaumont, G. Butler-Browne (2003) Myosin heavy chain isoforms in postnatal muscle development of mice. Biol Cell 95: 399-406. (Pubitemid 37220806)
2. Allen, D.L., C.A. Sartorius, L.K. Sycuro, L.A. Leinwand (2001) Different pathways regulate expression of the skeletal myosin heavy chain genes. J Biol Chem 276: 43524-43533. (Pubitemid 37383910)
3. Ambion (2009) Use of internal and external standards or reference RNAs for accurate quantitation of RNA levels. Ambion Technical Bulletins. Technical Bulletin 151.
4. Austin, Ambion. Andruchov, O., Y. Wang, O. Andruchova, S. Galler (2004) Functional properties of skinned rabbit skeletal and cardiac muscle preparations containing alpha-cardiac myosin heavy chain. Pflugers Arch 448: 44-53. (Pubitemid 38657204)
5. Bormioli, S.P., P. Torresan, S. Sartore, G.B. Moschini, S. Schiaffino (1979) Immunohistochemical identification of slow-tonic fibers in human extrinsic eye muscles. Invest Ophthalmol Vis Sci 18: 303-306. (Pubitemid 9111232)
6. Bottinelli, R. (2001) Functional heterogeneity of mammalian single muscle fibres: do myosin isoforms tell the whole story? Pflugers Arch 443: 6-17. (Pubitemid 33070885)
7. Brandon, C.A., C. Rosen, G. Georgelis, M.J. Horton, M.P. Mooney, J.J. Sciote (2003) Staining of human thyroarytenoid muscle with myosin antibodies reveals some unique extrafusal fibers, but no muscle spindles. J Voice 17: 245-254. (Pubitemid 36666390)
8. Bredman, J.J., A. Wessels, W.A. Weijs, J.A. Korfage, C.A. Soffers, A.F. Moorman (1991) Demonstration of 'cardiac-specific' myosin heavy chain in masticatory muscles of human and rabbit. Histochem J 23: 160-170.
9. Brozanski, B.S., M.J. Daood, J.F. Watchko, W.A. LaFramboise, R.D. Guthrie (1993) Postnatal expression of myosin isoforms in the genioglossus and diaphragm muscles. Pediatr Pulmonol 15: 212-219.
10. Buckingham, M., L. Bajard, T. Chang, P. Daubas, J. Hadchouel, S. Meilhac, D. Montarras, D. Rocancourt, F. Relaix (2003) The formation of skeletal muscle: from somite to limb. J Anat 202: 59-68. (Pubitemid 36503969)
11. Caiozzo, V.J., M.J. Baker, K. Huang, H. Chou, Y.Z. Wu, K.M. Baldwin (2003) Single-fiber myosin heavy chain polymorphism: how many patterns and what proportions? Am J Physiol Regul Integr Comp Physiol 285: R570-R580. (Pubitemid 37040565)
12. d'Albis, A., R. Couteaux, C. Janmot, A. Roulet (1989) Specific programs of myosin expression in the postnatal development of rat muscles. Eur J Biochem 183: 583-590. (Pubitemid 19218518)
13. DePaul, R., J.H. Abbs (1996) Quantitative morphology and histochemistry of intrinsic lingual muscle fibers in Macaca fascicularis. Acta Anat (Basel) 155: 29-40.
14. Desjardins, P.R., J.M. Burkman, J.B. Shrager, L.A. Allmond, H.H. Stedman (2002) Evolutionary implications of three novel members of the human sarcomeric myosin heavy chain gene family. Mol Biol Evol 19: 375-393
15. Gadberry, M.D., S.T. Malcomber, A.N. Doust, E.A. Kellogg (2005) Primaclade - a flexible tool to find conserved PCR primers across multiple species. Bioinformatics 21: 1263-1264.
16. Gaige, T.A., T. Benner, R. Wang, V.J. Wedeen, R.J. Gilbert (2007) Three dimensional myoarchitecture of the human tongue determined in vivo by diffusion tensor imaging with tractography. J Magn Reson Imaging 26: 654-661 (Pubitemid 350194588)
17. Galler, S., K. Hilber, B. Gohlsch, D. Pette (1997) Two functionally distinct myosin heavy chain isoforms in slow skeletal muscle fibres. FEBS Lett 410: 150-152. (Pubitemid 27304054)
18. Gilbert, R.J., V.J. Napadow, T.A. Gaige, V.J. Wedeen (2007) Anatomical basis of lingual hydrostatic deformation. J Exp Biol 210: 4069-4082.
19. Goldspink, G., A. Scutt, J. Martindale, T. Jaenicke, L. Turay, G.F. Gerlach (1991) Stretch and force generation induce rapid hypertrophy and myosin isoform gene switching in adult skeletal muscle. Biochem Soc Trans 19: 368-373.
20. Hamalainen, N., D. Pette (1995) Patterns of myosin isoforms in mammalian skeletal muscle fibres. Microsc Res Tech 30: 381-389.
21. Han, Y., J. Wang, D.A. Fischman, H.F. Biller, I. Sanders (1999) Slow tonic muscle fibers in the thyroarytenoid muscles of human vocal folds; a possible specialization for speech. Anat Rec 256: 146-157. (Pubitemid 29442080)
22. Hartmann, N., J.M. Martrette, A. Westphal (2001) Influence of the Lurcher mutation on myosin heavy chain expression in skeletal and cardiac muscles. J Cell Biochem Suppl suppl 36: 222-231.
23. Hill, A.V. (1950) The dimensions of animals and their muscular dynamics. Sci Prog 38: 209-230.
24. Hoh, J.F. (2002) 'Superfast' or masticatory myosin and the evolution of jaw-closing muscles of vertebrates. J Exp Biol 205: 2203-2210.
25. Hoh, J.F. (2005) Laryngeal muscle fibre types. Acta Physiol Scand 183: 133-149.
26. Hoh, J.F., Y. Kim, L.G. Sieber, W.W. Zhong, C.A. Lucas (2000) Jaw-closing muscles of kangaroos express alpha-cardiac myosin heavy chain. J Muscle Res Cell Motil 21: 673-680. (Pubitemid 32128231)
27. Horton, M.J., C. Rosen, J.M. Close, J.J. Sciote (2008) Quantification of myosin heavy chain RNA in human laryngeal muscles: differential expression in the vertical and horizontal posterior cricoarytenoid and thyroarytenoid. Laryngoscope 118: 472-477. (Pubitemid 351640628)
28. Jaschinski, F., M. Schuler, H. Peuker, D. Pette (1998) Changes in myosin heavy chain mRNA and protein isoforms of rat muscle during forced contractile activity. Am J Physiol 274: C365-C370. (Pubitemid 28140779)
29. Jee, H., T. Sakurai, S. Kawada, N. Ishii, Y. Atomi (2009) Significant roles of microtubules in mature striated muscle deduced from the correlation between tubulin and its molecular chaperone alphaB-crystallin in rat muscles. J Physiol Sci 59: 149-155.
30. Jung, H.H., S.H. Han, J.O. Choi (1999) Expression of myosin heavy chain mRNA in rat laryngeal muscles. Acta Otolaryngol 119: 396-402. (Pubitemid 29227409)
31. Jung, H.H., R.L. Lieber, A.F. Ryan (1998) Quantification of myosin heavy chain mRNA in somatic and branchial arch muscles using competitive PCR. Am J Physiol 275: C68-C74 (Pubitemid 28381304)
32. Jung, H.H., S.H. Han, S.Y. Nam, Y.H. Kim, J.L. Kim (2004) Myosin heavy chain composition of rat middle ear muscles. Acta Otolaryngol 124: 569-573. (Pubitemid 38858223)
33. Kelly, R.G., L.A. Jerome-Majewska, V.E. Papaioannou (2004) The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Hum Mol Genet 13: 2829-2840.
34. Kjellgren, D., L.E. Thornell, J. Andersen, F. Pedrosa-Domellöf (2003) Myosin heavy chain isoforms in human extraocular muscles. Invest Ophthalmol Vis Sci 44: 1419-1425. (Pubitemid 36378563)
35. Kohn, T.A., L.C. Hoffman, K.H. Myburgh (2007) Identification of myosin heavy chain isoforms in skeletal muscle of four Southern African wild ruminants. Comp Biochem Physiol A Mol Integr Physiol 148: 399-407.
36. Korfage, J.A., P. Brugman, T.M. Van Eijden (2000) Intermuscular and intramuscular differences in myosin heavy chain composition of the human masticatory muscles. J Neurol Sci 178: 95-106.
37. Korfage, J.A., T. Van Wessel, G.E. Langenbach, T.M. Van Eijden (2006) Heterogeneous postnatal transitions in myosin heavy chain isoforms within the rabbit temporalis muscle. Anat Rec A Discov Mol Cell Evol Biol 288: 1095-1104 (Pubitemid 44521964)
38. Kranjc, B.S., J. Sketelj, A.D. Albis, M. Ambroz, I. Erzen (2000) Fibre types and myosin heavy chain expression in the ocular medial rectus muscle of the adult rat. J Muscle Res Cell Motil 21: 753-761. (Pubitemid 32423410)
39. Leinwand, L.A., R.E. Fournier, B. Nadal-Ginard, T.B. Shows (1983) Multigene family for sarcomeric myosin heavy chain in mouse and human DNA: localization on a single chromosome. Science 221: 766-769.
40. Lim, S.J., H.H. Jung, Y.A. Cho (2006) Postnatal development of myosin heavy chain isoforms in rat extraocular muscles. Mol Vis 12: 243-250
41. Liu, J.X., P.O. Eriksson, L.E. Thornell, F. Pedrosa-Domellöf (2002) Myosin heavy chain composition of muscle spindles in human biceps brachii. J Histochem Cytochem 50: 171-183. (Pubitemid 34106756)
42. Lloyd, J.S., B.S. Brozanski, M. Daood, J.F. Watchko (1996) Developmental transitions in the myosin heavy chain phenotype of human respiratory muscle. Biol Neonate 69: 67-75. (Pubitemid 26090373)
43. Mascarello, F., A. Veggetti, E. Cerpenè, A. Rowlerson (1983) An immunohistochemical study of the middle ear muscles of some carnivores and primates, with special reference to the IIM and slow-tonic fibre types. J Anat 137: 95-108. (Pubitemid 13042214)
44. Moore, W.A., S.J. Goldberg, M.S. Shall (2007) Effects of artificial rearing on contractile properties of genioglossus muscle in Sprague- Dawley rat. Arch Oral Biol 52: 133-141.
45. Mu, L., H. Su, J. Wang, Y. Han, I. Sanders I (2004) Adult human mylohyoid muscle fibers express slow-tonic, alpha-cardiac, and developmental myosin heavy-chain isoforms. Anat Rec A Discov Mol Cell Evol Biol 279: 749-760. (Pubitemid 39038468)
46. Noden, D.M., P. Francis-West (2006) The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235: 1194-1218. (Pubitemid 43843907)
47. Pette, D., R.S. Staron (2000) Myosin isoforms, muscle fiber types, and transitions. Microsc Res Tech 50: 500-509.
48. Peuker, H., D. Pette (1995) Reverse transcriptase- polymerase chain reaction detects induction of cardiac-like alpha myosin heavy chain mRNA in low frequency stimulated rabbit fast-twitch muscle. FEBS Lett 367: 132-136.
49. Porter, J.D. (2002) Extraocular muscle: cellular adaptations for a diverse functional repertoire. Ann NY Acad Sci 956: 7-16.
50. Reiser, P.J., R.L. Moss, G.G. Giulian, M.L. Greaser (1985) Shortening velocity in single fibers from adult rabbit soleus muscles is correlated with myosin heavy chain composition. J Biol Chem 260: 9077-9080.
51. Rinaldi, C., F. Haddad, P.W. Bodell, A.X. Qin, W. Jiang, K.M. Baldwin (2008) Intergenic bidirectional promoter and cooperative regulation of the IIx and IIb MHC genes in fast skeletal muscle. Am J Physiol Regul Integr Comp Physiol 295: R208-R218.
52. Rosser, B.W., D.M. Waldbillig, S.D. Lovo, J.D. Armstrong, E. Bandman (1995) Myosin heavy chain expression within the tapered ends of skeletal muscle fibers. Anat Rec 242: 462-470.
53. Russell, S.D., N. Cambon, B. Nadal-Ginard, R.G. Whalen (1988) Thyroid hormone induces a nerve-independent precocious expression of fast myosin heavy chain mRNA in rat hindlimb skeletal muscle. J Biol Chem 263: 6370-6374.
54. Saboisky, J.P., J.E. Butler, R.B. Fogel, J.L. Taylor, J.A. Trinder, D.P. White, S.C. Gandevia (2006) Tonic and phasic respiratory drives to human genioglossus motoneurons during breathing. J Neurophysiol 95: 2213-2221.
55. Saito, T., Y. Ohnuki, A. Yamane, Y. Saeki (2002) Effects of diet consistency on the myosin heavy chain mRNAs of rat masseter muscle during postnatal development. Arch Oral Biol 47: 109-115. (Pubitemid 34094182)
56. Schmittgen, T.D., B.A. Zakrajsek (2000) Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J Biochem Biophys Methods 46: 69-81.
57. Serrano, A.L., M. Perez, A. Lucía, J.L. Chicharro, E. Quiroz-Rothe, J.L. Rivero (2001) Immunolabelling, histochemistry and in situ hybridisation in human skeletal muscle fibres to detect myosin heavy chain expression at the protein and mRNA level. J Anat 199: 329-337. (Pubitemid 32825627)
58. Shipley, L.A., J.E. Gross, D.E. Spalinger, N.T. Hobbs, B.A. Wunder (1994) The scaling of intake rate in mammalian herbivores. Am Nat 143: 1055-1082. (Pubitemid 2108444)
59. Smerdu, V., I. Erzen (2001) Dynamic nature of fibre-type specific expression of myosin heavy chain transcripts in 14 different human skeletal muscles. J Muscle Res Cell Motil 22: 647-655.
60. Smith, J.C., S.J. Goldberg, M.S. Shall (2006) Myosin heavy chain and fibre diameter of extrinsic tongue muscles in rhesus monkey. Arch Oral Biol 51: 520-525.
61. Sokoloff, A.J., H. Li, T.J. Burkholder (2007a) Limited expression of slow tonic myosin heavy chain in human cranial muscles. Muscle Nerve 36: 183-189. (Pubitemid 47221855)
62. Sokoloff, A.J., B. Yang, H. Li, T.J. Burkholder (2007b) Immunohistochemical characterization of slow and fast myosin heavy chain composition of muscle fibres in the styloglossus muscle of the human and macaque (Macaca rhesus). Arch Oral Biol 52: 533-543. (Pubitemid 46550996)
63. Sokoloff, A.J., M. Daugherty, H. Li (2009) Myosin heavy-chain composition of the human hyoglossus muscle. Dysphagia, E-pub ahead of print.
64. Stål, P., S. Marklund, L.E. Thornell, R. De Paul, P.O. Eriksson (2003) Fibre composition of human intrinsic tongue muscles. Cells Tissues Organs 173: 147-161. (Pubitemid 36407818)
65. Stedman, H.H., B.W. Kozyak, A. Nelson, D.M. Thesier, L.T. Su, D.W. Low, C.R. Bridges, J.B. Shrager, N. Minugh-Purvis, M.A. Mitchell (2004) Myosin gene mutation correlates with anatomical changes in the human lineage. Nature 428: 415-418. (Pubitemid 38419685)
66. Subramaniam, S. (1998) The Biology Workbench - a seamless database and analysis environment for the biologist. Proteins 32: 1-2. (Pubitemid 28313246)
67. Sugimoto, N., S. Nakano, M. Yoneyama, K. Honda (1996) Improved thermodynamic parameters and helix initiation factor to predict stability of DNA duplexes. Nucleic Acids Res 24: 4501-4505. (Pubitemid 26388637)
68. Sundman, E., T. Ansved, G. Margolin, R. Kuylenstierna, L.I. Eriksson (2004) Fibertype composition and fiber size of the human cricopharyngeal muscle and the pharyngeal constrictor muscle. Acta Anaesthesiol Scand 48: 423-429. (Pubitemid 38523548)
69. Tellis, C.M., C. Rosen, A. Thekdi, J.J. Sciote (2004) Anatomy and fiber type composition of human interarytenoid muscle. Ann Otol Rhinol Laryngol 113: 97-107. (Pubitemid 38222504)
70. Termin, A., R. S. Staron, D. Pette (1989) Changes in myosin heavy chain isoforms during chronic low-frequency stimulation of rat fast hindlimb muscles. A single-fiber study. Eur J Biochem 186: 749-754. (Pubitemid 20030131)
71. Termin, A., D. Pette (1991) Myosin heavy-chainbased isomyosins in developing, adult fasttwitch and slow-twitch muscles. Eur J Biochem 195: 577-584.
72. Toniolo, L., P. Cancellara, L. Maccatrozzo, M. Patruno, F. Mascarello, C. Reggiani (2008) Masticatory myosin unveiled: first determination of contractile parameters of muscle fibers from carnivore jaw muscles. Am J Physiol Cell Physiol 295: C1535-C1542.
73. van Willigen, J.D., J. Weijs-Boot (1984) Phasic and rhythmic responses of the oral musculature to mechanical stimulation of the rat palate. Arch Oral Biol 29: 7-11.
74. Vincent, H.K., R.A. Shanely, D.J. Stewart, H.A. Demirel, K.L. Hamilton, A.D. Ray, C. Michlin, G.A. Farkas, S.K. Powers (2002) Adaptation of upper airway muscles to chronic endurance exercise. Am J Respir Crit Care Med 166: 287-293. (Pubitemid 34864415)
75. Volz, L.M., L.B. Mann, J.A. Russell, M.A. Jackson, G.E. Leverson, N.P. Connor (2007) Biochemistry of anterior, medial, and posterior genioglossus muscle in the rat. Dysphagia 22: 210-214.
76. Wieczorek, D.F., M. Periasamy, G.S. Butler-Browne, R.G. Whalen, B. Nadal-Ginard (1985) Co-expression of multiple myosin heavy chain genes, in addition to a tissuespecific one, in extraocular musculature. J Cell Biol 101: 618-629. (Pubitemid 15239139)
77. Yang, S., M. Alnaqeeb, H. Simpson, G. Goldspink (1996) Cloning and characterization of an IGF-1 isoform expressed in skeletal muscle subjected to stretch. J Muscle Res Cell Motil 17: 487-495. (Pubitemid 26298531)
78. Yu, F., P. Stål, L.E. Thornell, L. Larsson (2002) Human single masseter muscle fibers contain unique combinations of myosin and myosin binding protein C isoforms. J Muscle Res Cell Motil 23: 317-326. (Pubitemid 36223033)