Skip to main content
Log in

Ultrastructural study of myotendinous junction plasticity: from disuse to exercise

  • Review
  • Published:
Sport Sciences for Health Aims and scope Submit manuscript

Abstract

In the musculoskeletal system, the interface between muscle and tendon, called the myotendinous junction, has the key role of transferring the contractile strength from muscular belly to its tendon. At the ultrastructural level, the myotendinous junction is characterized by tendon finger-like processes that penetrate into the muscle mass, amplifying the interaction between tissues. For many years, this anatomical region has been considered a passive interface and researchers’ attention was focused on muscle and tendon as independent structures. On the contrary, the plasticity of the myotendinous junction in response to different physiological or pathological conditions has been revealed and these changes appear at the morphological, structural and functional levels. In this work, the ultrastructural adaptations of the myotendinous junction to different physiological conditions have been described, suggesting possible causes that could control this plasticity. In particular, while muscle atrophy can reduce the contact interface between tissues, training protocols can amplify this area, allowing an improved ability to transfer increased levels of contractile strength. Moreover, given the frequency of muscle injuries at this level, the potential preventive role of exercise is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Pratesi A, Tarantini F, Di Bari M (2013) Skeletal muscle: an endocrine organ. Clin Cases Miner Bone Metab 10(1):11–14. doi:10.11138/ccmbm/2013.10.1.011

    PubMed  PubMed Central  Google Scholar 

  2. Covington JD, Tam CS, Bajpeyi S, Galgani JE, Noland RC, Smith SR, Redman LM, Ravussin E (2016) Myokine expression in muscle and myotubes in response to exercise stimulation. Med Sci Sports Exerc 48(3):384–390. doi:10.1249/MSS.0000000000000787

    Article  CAS  PubMed  Google Scholar 

  3. Mörl F, Siebert T, Häufle D (2016) Contraction dynamics and function of the muscle-tendon complex depend on the muscle fibre-tendon length ratio: a simulation study. Biomech Model Mechanobiol 15(1):245–258. doi:10.1007/s10237-015-0688-7 (Epub 4 Jun 2015)

    Article  PubMed  Google Scholar 

  4. Ciena AP, Luques IU, Dias FJ, Yokomizo de Almeida SR, Iyomasa MM, Watanabe IS (2010) Ultrastructure of the myotendinous junction of the medial pterygoid muscle of adult and aged Wistar rats. Micron 41(8):1011–1014. doi:10.1016/j.micron.2010.04.006

    Article  PubMed  Google Scholar 

  5. Folland JP, Williams AG (2007) The adaptations to strength training: morphological and neurological contributions to increased strength. Sports Med 37(2):145–168

    Article  PubMed  Google Scholar 

  6. Secomb JL, Lundgren LE, Farley OR, Tran TT, Nimphius S, Sheppard JM (2015) Relationships between lower-body muscle structure and lower-body strength, power, and muscle-tendon complex stiffness. J Strength Cond Res 29(8):2221–2228. doi:10.1519/JSC.0000000000000858

    Article  PubMed  Google Scholar 

  7. Hyodo M, Kawakita S, Desaki J (2001) Scanning electron microscopic study of the muscle fiber ends at the myotendinous junction in the posterior cricoarytenoid and cricothyroid muscles in rats. Acta Otolaryngol 121(8):953–956

    Article  CAS  PubMed  Google Scholar 

  8. Knudsen AB, Larsen M, Mackey AL, Hjort M, Hansen KK, Qvortrup K, Kjaer M, Krogsgaard MR (2015) The human myotendinous junction: an ultrastructural and 3D analysis study. Scand J Med Sci Sports 25(1):e116–e123. doi:10.1111/sms.12221 (Epub 10 Apr 2014)

    Article  CAS  PubMed  Google Scholar 

  9. Watanabe T, Imamura Y, Hosaka Y, Ueda H, Takehana K (2007) Graded arrangement of collagen fibrils in the equine superficial digital flexor tendon. Connect Tissue Res 48(6):332–337

    Article  CAS  PubMed  Google Scholar 

  10. Law DJ, Lightner VA (1993) Divalent cation-dependent adhesion at the myotendinous junction: ultrastructure and mechanics of failure. J Muscle Res Cell Motil 14(2):173–185

    Article  CAS  PubMed  Google Scholar 

  11. Curzi D, Ambrogini P, Falcieri E, Burattini S (2014) Morphogenesis of rat myotendinous junction. Muscles Ligaments Tendons J 3(4):275–280

    PubMed  PubMed Central  Google Scholar 

  12. Spierts I, Akster H, Vos I, Osse J (1996) Local differences in myotendinous junctions in axial muscle fibres of carp (Cyprinus carpio L.). J Exp Biol 199(Pt 4):825–833

    PubMed  Google Scholar 

  13. Mayer U (2003) Integrins: redundant or important players in skeletal muscle? J Biol Chem 278(17):14587–14590

    Article  CAS  PubMed  Google Scholar 

  14. Michele DE, Campbell KP (2003) Dystrophin-glycoprotein complex: post-translational processing and dystroglycan function. J Biol Chem 278(18):15457–15460

    Article  CAS  PubMed  Google Scholar 

  15. Hohenester E, Yurchenco PD (2013) Laminins in basement membrane assembly. Cell Adh Migr 7(1):56–63. doi:10.4161/cam.21831

    Article  PubMed  PubMed Central  Google Scholar 

  16. Charvet B, Guiraud A, Malbouyres M, Zwolanek D, Guillon E, Bretaud S, Monnot C, Schulze J, Bader HL, Allard B, Koch M, Ruggiero FS (2013) Knockdown of col22a1 gene in zebrafish induces a muscular dystrophy by disruption of the myotendinous junction. Development 140(22):4602–4613. doi:10.1242/dev.096024

    Article  CAS  PubMed  Google Scholar 

  17. Reis GF, de la Motte G, Gooding R, Laing NG, Margeta M (2015) Complex sarcolemmal invaginations mimicking myotendinous junctions in a case of Laing early-onset distal myopathy. Neuropathology 35(6):575–581. doi:10.1111/neup.12220

    Article  PubMed  Google Scholar 

  18. Guerini H, Pluot E, Pessis E, Thevenin F, Campagna R, Feydy A, Gaudin P, Drapé JL (2015) Tears at the myotendinous junction of the infraspinatus: ultrasound findings. Diagn Interv Imaging 96(4):349–356. doi:10.1016/j.diii.2014.11.009

    Article  CAS  PubMed  Google Scholar 

  19. Blankenbaker DG, De Smet A (2004) MR imaging of muscle injuries. Appl Radiol 33(4):14–26

    Google Scholar 

  20. Fiorentino NM, Epstein FH, Blemker SS (2012) Activation and aponeurosis morphology affect in vivo muscle tissue strains near the myotendinous junction. J Biomech 45(4):647–652. doi:10.1016/j.jbiomech.2011.12.015

    Article  PubMed  PubMed Central  Google Scholar 

  21. Hauraix H, Nordez A, Dorel S (2013) Shortening behavior of the different components of muscle-tendon unit during isokinetic plantar flexions. J Appl Physiol 115(7):1015–1024. doi:10.1152/japplphysiol.00247.2013

    Article  PubMed  Google Scholar 

  22. Tidball JG (1984) Myotendinous junction: morphological changes and mechanical failure associated with muscle cell atrophy. Exp Mol Pathol 40(1):1–12

    Article  CAS  PubMed  Google Scholar 

  23. Tidball JG, Quan DM (1992) Reduction in myotendinous junction surface area of rats subjected to 4-day spaceflight. J Appl Physiol 73(1):59–64

    CAS  PubMed  Google Scholar 

  24. Tidball JG, Quan DM (1992) Modifications in myotendinous junction structure following denervation. Acta Neuropathol 84(2):135–140

    Article  CAS  PubMed  Google Scholar 

  25. Curzi D, Lattanzi D, Ciuffoli S, Burattini S, Grindeland RE, Edgerton VR, Roy RR, Tidball JG, Falcieri E (2013) Growth hormone plus resistance exercise attenuate structural changes in rat myotendinous junctions resulting from chronic unloading. Eur J Histochem 57(4):e37. doi:10.4081/ejh.2013.e37

    Article  CAS  PubMed  Google Scholar 

  26. Zamora AJ, Carnino A, Roffino S, Marini JF (1995) Respective effects of hindlimb suspension, confinement and spaceflight on myotendinous junction ultrastructure. Acta Astronaut 36(8–12):693–706

    Article  CAS  PubMed  Google Scholar 

  27. Roffino S, Carnino A, Charpiot P, Marini JF (1998) Increase in rat soleus myotendinous interface after a 14-d spaceflight. C R Acad Sci III 321(7):557–564

    Article  CAS  PubMed  Google Scholar 

  28. Roffino S, Carnino A, Chopard A, Mutin M, Marini JF (2006) Structural remodeling of unweighted soleus myotendinous junction in monkey. C R Biol 329(3):172–179

    Article  PubMed  Google Scholar 

  29. Kim JW, Kwon OY, Kim MH (2007) Differentially expressed genes and morphological changes during lengthened immobilization in rat soleus muscle. Differentiation 75(2):147–157

    Article  CAS  PubMed  Google Scholar 

  30. Kvist M, Hurme T, Kannus P, Järvinen T, Maunu VM, Jozsa L, Järvinen M (1995) Vascular density at the myotendinous junction of the rat gastrocnemius muscle after immobilization and remobilization. Am J Sports Med 23(3):359–364

    Article  CAS  PubMed  Google Scholar 

  31. de Palma L, Marinelli M, Pavan M, Bertoni-Freddari C (2011) Involvement of the muscle-tendon junction in skeletal muscle atrophy: an ultrastructural study. Rom J Morphol Embryol 52(1):105–109

    PubMed  Google Scholar 

  32. Chopard A, Pons F, Marini JF (2001) Cytoskeletal protein contents before and after hindlimb suspension in a fast and slow rat skeletal muscle. Am J Physiol Regul Integr Comp Physiol 280(2):R323–R330

    CAS  PubMed  Google Scholar 

  33. Chopard A, Arrighi N, Carnino A, Marini JF (2005) Changes in dysferlin, proteins from dystrophin glycoprotein complex, costameres, and cytoskeleton in human soleus and vastus lateralis muscles after a long-term bedrest with or without exercise. FASEB J 19(12):1722–1724

    CAS  PubMed  Google Scholar 

  34. Kannus P, Jozsa L, Renstrom P, Jarvinen M, Krist M, Lehto M, Oja P, Vuort I (1992) The effect of training, immobilization and remobilization on musculoskeletal. Part 1: training and immobilization. Scand J Med Sci Sports 2:100–118

    Article  Google Scholar 

  35. Samukawa M, Hattori M, Sugama N, Takeda N (2011) The effects of dynamic stretching on plantar flexor muscle-tendon tissue properties. Man Ther 16(6):618–622. doi:10.1016/j.math.2011.07.003

    Article  PubMed  Google Scholar 

  36. Nakamura M, Ikezoe T, Takeno Y, Ichihashi N (2012) Effects of a 4-week static stretch training program on passive stiffness of human gastrocnemius muscle-tendon unit in vivo. Eur J Appl Physiol 112(7):2749–2755. doi:10.1007/s00421-011-2250-3

    Article  PubMed  Google Scholar 

  37. Konrad A, Tilp M (2014) Increased range of motion after static stretching is not due to changes in muscle and tendon structures. Clin Biomech 29(6):636–642. doi:10.1016/j.clinbiomech.2014.04.013

    Article  Google Scholar 

  38. Konrad A, Tilp M (2014) Effects of ballistic stretching training on the properties of human muscle and tendon structures. J Appl Physiol 117(1):29–35. doi:10.1152/japplphysiol.00195.2014

    Article  PubMed  Google Scholar 

  39. Nakamura M, Ikezoe T, Takeno Y, Ichihashi N (2013) Time course of changes in passive properties of the gastrocnemius muscle-tendon unit during 5 min of static stretching. Man Ther 18(3):211–215. doi:10.1016/j.math.2012.09.010

    Article  PubMed  Google Scholar 

  40. Mizuno T, Matsumoto M, Umemura Y (2013) Viscoelasticity of the muscle-tendon unit is returned more rapidly than range of motion after stretching. Scand J Med Sci Sports 23(1):23–30. doi:10.1111/j.1600-0838.2011.01329.x

    Article  CAS  PubMed  Google Scholar 

  41. Cè E, Longo S, Rampichini S, Devoto M, Limonta E, Venturelli M, Esposito F (2015) Stretch-induced changes in tension generation process and stiffness are not accompanied by alterations in muscle architecture of the middle and distal portions of the two gastrocnemii. J Electromyogr Kinesiol 25(3):469–478. doi:10.1016/j.jelekin.2015.03.001

    Article  PubMed  Google Scholar 

  42. Freitas SR, Mil-Homens P (2015) Effect of 8-week high-intensity stretching training on biceps femoris architecture. J Strength Cond Res 29(6):1737–1740

    Article  PubMed  Google Scholar 

  43. Gossman MR, Rose SJ, Sahrmann SA, Katholi CR (1986) Length and circumference measurements in one-joint and multijoint muscles in rabbits after immobilization. Phys Ther 66(4):516–520

    CAS  PubMed  Google Scholar 

  44. Kasper CE (1999) Recovery of plantaris muscle from impaired physical mobility. Biol Res Nurs 1:4–11

    Article  CAS  PubMed  Google Scholar 

  45. Heslinga JW, te Kronnie G, Huijing PA (1995) Growth and immobilization effects on sarcomeres: a comparison between gastrocnemius and soleus muscles of the adult rat. Eur J Appl Physiol Occup Physiol 70:49–57

    Article  CAS  PubMed  Google Scholar 

  46. Sonoda M, Moriya H, Shimada Y (1993) Fine structure of transverse tubules and the sarcoplasmic reticulum at the myotendinous junction of stretched muscle fibers of the rat. Microsc Res Tech 24(3):281–286

    Article  CAS  PubMed  Google Scholar 

  47. De Jaeger D, Joumaa V, Herzog W (2015) Intermittent stretch training of rabbit plantarflexor muscles increases soleus mass and serial sarcomere number. J Appl Physiol 118(12):1467–1473. doi:10.1152/japplphysiol.00515.2014 (Epub 2 Apr 2015)

    Article  PubMed  Google Scholar 

  48. Aro AA, Vidal BC, Tomiosso TC, Gomes L, Matiello-Rosa SM, Pimentel ER (2008) Structural and biochemical analysis of the effect of immobilization followed by stretching on the calcaneal tendon of rats. Connect Tissue Res 49(6):443–454. doi:10.1080/03008200802325250

    Article  CAS  PubMed  Google Scholar 

  49. Archambault JM, Tsuzaki M, Herzog W, Banes AJ (2002) Stretch and interleukin-1β induce matrix metalloproteinases in rabbit tendon cells in vitro. J Orthop Res 20:36–39

    Article  CAS  PubMed  Google Scholar 

  50. Boccafoschi F, Mosca C, Bosetti M, Cannas M (2011) The role of mechanical stretching in the activation and localization of adhesion proteins and related intracellular molecules. J Cell Biochem 112(5):1403–1409. doi:10.1002/jcb.23056

    Article  CAS  PubMed  Google Scholar 

  51. Kasemkijwattana C, Menetrey J, Bosch P, Somogyi G, Moreland MS, Fu FH, Buranapanitkit B, Watkins SS, Huard J (2000) Use of growth factors to improve muscle healing after strain injury. Clin Orthop Relat Res 370:272–285

    Article  Google Scholar 

  52. Baker SJ, Kelly NM, Eston RG (1997) Pressure pain tolerance at different sites on the quadriceps femoris prior to and following eccentric exercise. Eur J Pain 1(3):229–233

    Article  CAS  PubMed  Google Scholar 

  53. Yanagisawa O, Kurihara T, Okumura K, Fukubayashi T (2010) Effects of strenuous exercise with eccentric muscle contraction: physiological and functional aspects of human skeletal muscle. Magn Reson Med Sci 9(4):179–186

    Article  PubMed  Google Scholar 

  54. Lau WY, Blazevich AJ, Newton MJ, Wu SS, Nosaka K (2015) Reduced muscle lengthening during eccentric contractions as a mechanism underpinning the repeated-bout effect. Am J Physiol Regul Integr Comp Physiol 308(10):R879–R886

    Article  CAS  PubMed  Google Scholar 

  55. Duclay J, Martin A, Duclay A, Cometti G, Pousson M (2009) Behavior of fascicles and the myotendinous junction of human medial gastrocnemius following eccentric strength training. Muscle Nerve 39(6):819–827. doi:10.1002/mus.21297

    Article  PubMed  Google Scholar 

  56. Blazevich AJ (2006) Effects of physical training and detraining, immobilisation, growth and aging on human fascicle geometry. Sports Med 36:1003–1017

    Article  PubMed  Google Scholar 

  57. Franchi MV, Atherton PJ, Reeves ND, Flück M, Williams J, Mitchell WK, Selby A, Beltran Valls RM, Narici MV (2014) Architectural, functional and molecular responses to concentric and eccentric loading in human skeletal muscle. Acta Physiol (Oxf) 210(3):642–654. doi:10.1111/apha.12225

    Article  CAS  Google Scholar 

  58. Blazevich A, Cannavan D, Coleman DR, Horne S (2007) Influence of concentric and eccentric resistance training on architectural adaptation in human quadriceps muscles. J Appl Physiol 5:1565–1575. doi:10.1152/japplphysiol.00578.2007

    Article  Google Scholar 

  59. Frenette J, Côté CH (2000) Modulation of structural protein content of the myotendinous junction following eccentric contractions. Int J Sports Med 21(5):313–320

    Article  CAS  PubMed  Google Scholar 

  60. Franchi MV, Wilkinson DJ, Quinlan JI, Mitchell WK, Lund JN, Williams JP, Reeves ND, Smith K, Atherton PJ, Narici MV (2015) Early structural remodeling and deuterium oxide-derived protein metabolic responses to eccentric and concentric loading in human skeletal muscle. Physiol Rep 3(11):e12593. doi:10.14814/phy2.12593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Curzi D, Salucci S, Marini M, Esposito F, Agnello L, Veicsteinas A, Burattini S, Falcieri E (2012) How physical exercise changes rat myotendinous junctions: an ultrastructural study. Eur J Histochem 56(2):e19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Kojima H, Sakuma E, Mabuchi Y, Mizutani J, Horiuchi O, Wada I, Horiba M, Yamashita Y, Herbert DC, Soji T, Otsuka T (2008) Ultrastructural changes at the myotendinous junction induced by exercise. J Orthop Sci 13(3):233–239

    Article  PubMed  Google Scholar 

  63. Curzi D, Baldassarri V, De Matteis R, Salamanna F, Bolotta A, Frizziero A, Fini M, Marini M, Falcieri E (2015) Morphological adaptation and protein modulation of myotendinous junction following moderate aerobic training. Histol Histopathol 30(4):465–472

    CAS  PubMed  Google Scholar 

  64. Boppart MD, Volker SE, Alexander N, Burkin DJ, Kaufman SJ (2008) Exercise promotes alpha7 integrin gene transcription and protection of skeletal muscle. Am J Physiol Regul Integr Comp Physiol 295(5):R1623–R1630. doi:10.1152/ajpregu.00089.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

I would like to thank Prof. Elisabetta Falcieri for critical reading and Urbino University for its support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Davide Curzi.

Ethics declarations

Conflict of interest

The author declares that he has no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Curzi, D. Ultrastructural study of myotendinous junction plasticity: from disuse to exercise. Sport Sci Health 12, 279–286 (2016). https://doi.org/10.1007/s11332-016-0301-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11332-016-0301-1

Keywords

Navigation