Effects of age and diet consistency on the expression of myosin heavy-chain isoforms on jaw-closing and jaw-opening muscles in a rat model.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Additional Information
    • Source:
      Publisher: Blackwell Scientific Publications Country of Publication: England NLM ID: 0433604 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-2842 (Electronic) Linking ISSN: 0305182X NLM ISO Abbreviation: J Oral Rehabil Subsets: MEDLINE
    • Publication Information:
      Original Publication: Oxford, Blackwell Scientific Publications.
    • Subject Terms:
    • Abstract:
      Background: Skeletal craniofacial morphology can be influenced by changes in masticatory muscle function, which may also change the functional profile of the muscles.
      Objectives: To investigate the effects of age and functional demands on the expression of Myosin Heavy-Chain (MyHC) isoforms in representative jaw-closing and jaw-opening muscles, namely the masseter and digastric muscles respectively.
      Methods: Eighty-four male Wistar rats were divided into four age groups, namely an immature (n = 12; 4-week-old), early adult (n = 24; 16-week-old), adult (n = 24; 26-week-old) and mature adult (n = 24; 38-week-old) group. The three adult groups were divided into two subgroups each based on diet consistency; a control group fed a standard (hard) diet, and an experimental group fed a soft diet. Rats were sacrificed, and masseter and digastric muscles dissected. Real-time quantitative polymerase chain reaction was used to compare the mRNA transcripts of the MyHC isoforms-Myh7 (MyHC-I), Myh2 (MyHC-IIa), Myh4 (MyHC-IIb) and Myh1 (MyHC-IIx)-of deep masseter and digastric muscles.
      Results: In the masseter muscle, hypofunction increases Myh1 (26, 38 weeks; p < .0001) but decreases Myh4 (26 weeks; p = .046) and Myh2 (26 weeks; p < .0001) expression in adult rats. In the digastric muscle, hypofunction increases Myh1 expression in the mature adult rats (38 weeks; p < .0001), while Myh2 expression decreases in adult rats (26 weeks; p = .021) as does Myh4 (26 weeks; p = .001). Myh7 expression is increased in the digastric muscle of mature adult rats subjected to hypofunction (38 weeks; p = <.0001), while it is very weakly expressed in the masseter.
      Conclusion: In jaw-opening and jaw-closing muscles, differences in myosin expression between hard- and soft-diet-fed rats become evident in adulthood, suggesting that long-term alteration of jaw function is associated with changes in the expression of MyHC isoforms and potential fibre remodelling. This may give insight into the role of function on masticatory muscles and the resultant craniofacial morphology.
      (© 2024 The Authors. Journal of Oral Rehabilitation published by John Wiley & Sons Ltd.)
    • References:
      Kiliaridis S. Masticatory muscle influence on craniofacial growth. Acta Odontol Scand. 1995;53(3):196‐202.
      Kiliaridis S. Masticatory muscle function and craniofacial morphology. An experimental study in the growing rat fed a soft diet. Swed Dent J Suppl. 1986;36:1‐55.
      Schiaffino S, Reggiani C. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev. 1996;76(2):371‐423.
      Pette D. The adaptive potential of skeletal muscle fibers. Can J Appl Physiol. 2002;27(4):423‐448.
      Kiliaridis S, Engström C, Thilander B. Histochemical analysis of masticatory muscle in the growing rat after prolonged alteration in the consistency of the diet. Arch Oral Biol. 1988;33(3):187‐193.
      Saito T, Ohnuki Y, Yamane A, Saeki Y. Effects of diet consistency on the myosin heavy chain mRNAs of rat masseter muscle during postnatal development. Arch Oral Biol. 2002;47(2):109‐115.
      Braun T, Gautel M. Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat Rev Mol Cell Biol. 2011;12(6):349‐361.
      Greising SM, Gransee HM, Mantilla CB, Sieck GC. Systems biology of skeletal muscle: fiber type as an organizing principle. Wiley Interdiscip Rev Syst Biol Med. 2012;4(5):457‐473.
      Gundersen K. Excitation‐transcription coupling in skeletal muscle: the molecular pathways of exercise. Biol Rev Camb Philos Soc. 2011;86(3):564‐600.
      Dos Santos M, Backer S, Saintpierre B, et al. Single‐nucleus RNA‐seq and FISH identify coordinated transcriptional activity in mammalian myofibers. Nat Commun. 2020;11(1):5102.
      Wright C, Haddad F, Qin AX, Baldwin KM. Analysis of myosin heavy chain mRNA expression by RT‐PCR. J Appl Physiol (1985). 1997;83(4):1389‐1396.
      Zurmanova J, Soukup T. Comparison of myosin heavy chain mRNAs, protein isoforms and fiber type proportions in the rat slow and fast muscles. Physiol Res. 2013;62(4):445‐453.
      Schiaffino S. Muscle fiber type diversity revealed by anti‐myosin heavy chain antibodies. FEBS J. 2018;285(20):3688‐3694.
      Bottinelli R, Reggiani C. Human skeletal muscle fibres: molecular and functional diversity. Prog Biophys Mol Biol. 2000;73(2–4):195‐262.
      Thomas NR, Peyton SC. An electromyographic study of mastication in the freely‐moving rat. Arch Oral Biol. 1983;28(10):939‐945.
      Cobos AR, Segade LA, Fuentes I. Muscle fibre types in the suprahyoid muscles of the rat. J Anat. 2001;198(Pt 3):283‐294.
      Percie du Sert N, Ahluwalia A, Alam S, et al. Reporting animal research: explanation and elaboration for the ARRIVE guidelines 2.0. PLoS Biol. 2020;18(7):e3000411.
      Lagou A, Schaub L, Ait‐Lounis A, Denes BJ, Kiliaridis S, Antonarakis GS. Myosin heavy‐chain messenger ribonucleic acid (mRNA) expression and fibre cross‐sectional area in masseter, digastric, gastrocnemius and soleus muscles of young and adult rats. Biology (Basel). 2023;12(6):842.
      Kawai N, Sano R, Korfage JA, et al. Adaptation of rat jaw muscle fibers in postnatal development with a different food consistency: an immunohistochemical and electromyographic study. J Anat. 2010;216(6):717‐723.
      Hiiemäe KM, Ardran GM. A cinefluorographic study of mandibular movement during feeding in the rat (Rattus norvegicus). J Zool. 1968;154(2):139‐154.
      Sano R, Tanaka E, Korfage JA, et al. Heterogeneity of fiber characteristics in the rat masseter and digastric muscles. J Anat. 2007;211(4):464‐470.
      Kawai N, Sano R, Korfage JA, et al. Functional characteristics of the rat jaw muscles: daily muscle activity and fiber type composition. J Anat. 2009;215(6):656‐662.
      Kiliaridis S, Shyu BC. Isometric muscle tension generated by masseter stimulation after prolonged alteration of the consistency of the diet fed to growing rats. Arch Oral Biol. 1988;33(7):467‐472.
      Saito T, Fukui K, Akutsu S, et al. Effects of diet consistency on the expression of insulin‐like growth factors (IGFs), IGF receptors and IGF binding proteins during the development of rat masseter muscle soon after weaning. Arch Oral Biol. 2004;49(10):777‐782.
      Miehe B, Fanghanel J, Kubein‐Meesenburg D, Nagerl H, Schwestka‐Polly R. Masticatory musculature under altered occlusal relationships — a model study with experimental animals. Ann Anat. 1999;181(1):37‐40.
      Schiaffino S, Reggiani C. Myosin isoforms in mammalian skeletal muscle. J Appl Physiol (1985). 1994;77(2):493‐501.
      Muller J, Vayssiere N, Royuela M, et al. Comparative evolution of muscular dystrophy in diaphragm, gastrocnemius and masseter muscles from old male mdx mice. J Muscle Res Cell Motil. 2001;22(2):133‐139.
      Lee WH, Abe S, Kim HJ, et al. Characteristics of muscle fibers reconstituted in the regeneration process of masseter muscle in an mdx mouse model of muscular dystrophy. J Muscle Res Cell Motil. 2006;27(3–4):235‐240.
      Kiliaridis S, Engstrom C, Thilander B. The relationship between masticatory function and craniofacial morphology. I. A cephalometric longitudinal analysis in the growing rat fed a soft diet. Eur J Orthod. 1985;7(4):273‐283.
      Abed GS, Buschang PH, Taylor R, Hinton RJ. Maturational and functional related differences in rat craniofacial growth. Arch Oral Biol. 2007;52(11):1018‐1025.
      Mavropoulos A, Odman A, Ammann P, Kiliaridis S. Rehabilitation of masticatory function improves the alveolar bone architecture of the mandible in adult rats. Bone. 2010;47(3):687‐692.
      Kiliaridis S, Mejersjo C, Thilander B. Muscle function and craniofacial morphology: a clinical study in patients with myotonic dystrophy. Eur J Orthod. 1989;11(2):131‐138.
      Rowlerson A, Raoul G, Daniel Y, et al. Fiber‐type differences in masseter muscle associated with different facial morphologies. Am J Orthod Dentofacial Orthop. 2005;127(1):37‐46.
      Bakke M, Michler L. Temporalis and masseter muscle activity in patients with anterior open bite and craniomandibular disorders. Scand J Dent Res. 1991;99(3):219‐228.
      Ingervall B, Helkimo E. Masticatory muscle force and facial morphology in man. Arch Oral Biol. 1978;23(3):203‐206.
      Proffit WR, Fields HW, Nixon WL. Occlusal forces in normal‐ and long‐face adults. J Dent Res. 1983;62(5):566‐570.
      Hunt NP, Cunningham SJ. The influence of orthognathic surgery on occlusal force in patients with vertical facial deformities. Int J Oral Maxillofac Surg. 1997;26(2):87‐91.
      Proffit WR, Turvey TA, Fields HW, Phillips C. The effect of orthognathic surgery on occlusal force. J Oral Maxillofac Surg. 1989;47(5):457‐463.
      Throckmorton GS, Buschang PH, Ellis E 3rd. Improvement of maximum occlusal forces after orthognathic surgery. J Oral Maxillofac Surg. 1996;54(9):1080‐1086.
      Harzer W, Worm M, Gedrange T, Schneider M, Wolf P. Myosin heavy chain mRNA isoforms in masseter muscle before and after orthognathic surgery. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;104(4):486‐490.
      Gedrange T, Buttner C, Schneider M, et al. Change of mRNA amount of myosin heavy chain in masseter muscle after orthognathic surgery of patients with malocclusion. J Craniomaxillofac Surg. 2006;34(Suppl 2):110‐115.
      Shah F, Stal P, Li J, Sessle BJ, Avivi‐Arber L. Tooth extraction and subsequent dental implant placement in Sprague‐Dawley rats induce differential changes in anterior digastric myofibre size and myosin heavy chain isoform expression. Arch Oral Biol. 2019;99:141‐149.
      Buvinic S, Balanta‐Melo J, Kupczik K, Vasquez W, Beato C, Toro‐Ibacache V. Muscle‐bone crosstalk in the masticatory system: from biomechanical to molecular interactions. Front Endocrinol (Lausanne). 2020;11:606947.
      Widmer CG, English AW, Morris‐Wiman J. Developmental and functional considerations of masseter muscle partitioning. Arch Oral Biol. 2007;52(4):305‐308.
      Endo Y, Mizuno T, Fujita K, Funabashi T, Kimura F. Soft‐diet feeding during development enhances later learning abilities in female rats. Physiol Behav. 1994;56(4):629‐633.
      Cox RD, Buckingham ME. Actin and myosin genes are transcriptionally regulated during mouse skeletal muscle development. Dev Biol. 1992;149(1):228‐234.
      Ciurana N, Artells R, Munoz C, et al. Expression of MyHC isoforms mRNA transcripts in different regions of the masseter and medial pterygoid muscles in chimpanzees. Arch Oral Biol. 2017;83:63‐67.
      Korfage JA, Koolstra JH, Langenbach GE, van Eijden TM. Fiber‐type composition of the human jaw muscles—(part 2) role of hybrid fibers and factors responsible for inter‐individual variation. J Dent Res. 2005;84(9):784‐793.
      Pette D, Staron RS. Myosin isoforms, muscle fiber types, and transitions. Microsc Res Tech. 2000;50(6):500‐509.
      Sengupta P. The laboratory rat: relating its age with Human's. Int J Prev Med. 2013;4(6):624‐630.
      Yu Y, Fuscoe JC, Zhao C, et al. A rat RNA‐Seq transcriptomic BodyMap across 11 organs and 4 developmental stages. Nat Commun. 2014;5:3230.
    • Grant Information:
      31003A_176131 Swiss National Science Foundation (FNS)
    • Contributed Indexing:
      Keywords: aging; jaw muscles; messenger RNA; myosin heavy chains; rats; soft diet
    • Publication Date:
      Date Created: 20240313 Date Completed: 20240427 Latest Revision: 20240516
    • Publication Date:
      20240516
    • Accession Number:
      10.1111/joor.13676
    • Accession Number:
      38475932