Absence of morphological and molecular correlates of sarcopenia in the macaque tongue muscle styloglossus

Abstract

Introduction Equivocal decline of tongue muscle performance with age is compatible with resistance of the tongue to sarcopenia, the loss of muscle volume and function that typically occurs with aging. To test this possibility we characterized anatomical and molecular indices of sarcopenia in the macaque tongue muscle styloglossus (SG). Methods We quantified myosin heavy chain (MHC), muscle fiber MHC phenotype and size and total and phosphorylated growth- and atrophy-related proteins by sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE), immunoblot and immunohistochemistry (IHC) in the SG in twenty-four macaque monkeys (Macaca rhesus, age range 9 months to 31 years) categorized into Young (<8 years of age), Middle-aged (15–21 years of age) and Old (> 22 years of age) groups. Results In Young, Middle and Old age groups, by SDS-PAGE MHCI comprised ~1/3 and MHCII ~2/3 of total MHC. MHCI relative frequency was lower and MHCII higher in Middle versus Young (p=0.0099) and Middle versus Old (p=0.052). Relative frequencies of MHC fiber phenotype were not different by age but were different by phenotype (rates 233, 641 and 111 per 1000 fibers for MHCI, MHCII and MHCI-II respectively, P = 0.03). Few or no fibers were positive for developmental MHC. Mean cross-sectional area (CSA) was not different among the three age groups for MHCII and MHCI-II; however MHCI fibers tended to be larger in Middle versus Old and Young (mean = 2257 um2, 1917 um2 (p=0.05) and 1704 um2 (p=0.06), respectively). For each age group, mean CSA increased across MHC phenotype (lowest mean CSA for MHCI and highest mean CSA for MHCII). Spearman analysis demonstrated age-related increases in total p70 ribosomal protein S6 kinase (P70), phosphorylated P70421/424, phosphorylated P38 mitogen-activated protein kinase and muscle atrophy F-Box, a trend to age-related decrease in total extracellular signal-regulated kinase (ERK), and no age-related change in total protein kinase B (Akt/PKB), phosphorylated Akt, phosphorylated ERK, phosphorylated c-Jun N-terminal kinase (JNK46) and phosphorylated P70389. Conclusion Common anatomical and molecular indices of sarcopenia are absent in our sample of macaque SG. Relative frequencies of MHCII protein and phenotype are preserved with age. Although MAFbx expression increases with age, this is not associated with fiber atrophy, perhaps reflecting compensatory growth signaling by p70. The resistant nature of the styloglossus muscle to sarcopenia may be related to routine activation of tongue muscles in respiration and swallowing and the preservation of hypoglossal motoneuron number with age.

Alterations of intrinsic tongue muscle properties with aging

“…Different age ranges, muscle sample locations, and muscle fiber selection parameters may have contributed to the divergent findings. Mixed results have also been reported on the impact of aging on the extrinsic lingual muscles . Because imaging and electromyographic studies have indicated that the transverse and verticalis muscles may work with the genioglossus to propel the bolus during swallowing, decreasing muscle fiber size in the transverse and verticalis muscles, as reported in our study, may contribute to the reductions in maximum tongue pressure found with age …”

Sarcopenia and dysphagia: Position paper by four professional organizations

“…Furthermore, many suprahyoid, infrahyoid, pharyngeal and laryngeal muscles receive constant input stimulation from the respiratory center, and their activities are potentially synchronized with the contraction and relaxation of the diaphragm. In particular, the styloglossus muscle has been shown to exhibit resistance against sarcopenia both immunohistochemically and molecularly . Such activities are believed to render these muscles more resistant to disuse‐related atrophy than general somatic muscles.…”

“…In particular, the styloglossus muscle has been shown to exhibit resistance against sarcopenia both immunohistochemically and molecularly. 26 Such activities are believed to render these muscles more resistant to disuse-related atrophy than general somatic muscles. Thus, these differences should be taken into consideration when the pathophysiology of sarcopenia is discussed.…”

Decreased swallowing function in the sarcopenic elderly, without clinical dysphagia: a case-control study

“…Features common to sarcopenic appendicular muscle, i.e., a shift to slower myosin heavy chain isoforms, type II muscle fiber atrophy and neuromuscular junction dysmorphology, are absent or minimal in rat tongue muscles (30,31). In particular, the styloglossus muscle has been shown to exhibit resistance against sarcopenia both molecularly and immunohistochemically (32). It was reported that normal and effortful swallow pressures do not decline with age (13) and by some measures tongue functional reserve is maintained with age (33).…”