Abstract
Here we investigated the morphology, quantity, distribution and gene expression of mechanoreceptors in the anterior cruciate ligament (ACL), posterior cruciate ligament (PCL), medial collateral ligament (MCL), lateral collateral ligament (LCL), patellar tendon (PaT) and popliteal tendon (PoT) of the knee joint. Twelve 6-month-old rabbits were divided into two groups. In one group, the ACL, PCL, MCL, LCL, PaT and PoT were collected to observe the morphology, distribution and quantity of mechanoreceptors. In another group, the ACL, PCL, MCL, LCL, PaT and PoT of bilateral knee joints were used to determine S100B, CGRP and NEFM gene levels. Five types of mechanoreceptors were observed including Ruffini corpuscles, Pacinian corpuscles, Golgi-tendon bodies, atypical mechanoreceptors and free nerve endings. The total amount of mechanoreceptors was significantly lower in MCL, LCL, PaT and PoT as compared with ACL and PCL (P < 0.001). All examined mechanoreceptors were present in ACL, PCL and LCL. However, no Pacinian corpuscles and Golgi-tendon bodies were found in MCL and PoT as well as Pacinian corpuscles were not observed in PaT. The present study indicated that the levels of NEFM was significantly lower in PCL, MCL, LCL, PaT and PoT as compared with ACL (P < 0.05), but there was no significant difference in CGRP level between ACL and other ligaments except LCL (P > 0.05). Thus, the quantity, type and gene expression of mechanoreceptors are different in various ligaments. Thus, the quantity and distribution of mechanoreceptors may be related to ligament's function.
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Adachi N, Ochi M, Uchio Y, Iwasa J, Ryoke K, Kuriwaka M (2002) Mechanoreceptors in the anterior cruciate ligament contribute to the joint position sense. Acta Orthop Scand 73:330–334. https://doi.org/10.1080/000164702320155356
Arcand MA, Rhalmi S, Rivard CH (2000) Quantification of mechanoreceptors in the canine anterior cruciate ligament. Int Orthop 24:272–275. https://doi.org/10.1007/s002640000153
Ariel de Lima D, Helito CP, Lacerda de Lima L, Dias Leite JA, Costa Cavalcante ML (2019) Study of the nerve endings and mechanoreceptors of the anterolateral ligament of the knee. Arthroscopy 35:2918–2927. https://doi.org/10.1016/j.arthro.2019.05.023
Beaulieu JM, Robertson J, Julien JP (1999) Interactions between peripherin and neurofilaments in cultured cells: disruption of peripherin assembly by he NF-M and NF-H subunits. Biochem Cell Biol 77:41–45
Benarroch EE (2011) CGRP: sensory neuropeptide with multiple neurologic implications. Neurology 77:281–287. https://doi.org/10.1212/WNL.0b013e31822550e2
Çabuk H, Kuşku Çabuk F, Tekin AÇ, Dedeoğlu SS, Çakar M, Büyükkurt CD (2017) Lower numbers of mechanoreceptors in the posterior cruciate ligament and anterior capsule of the osteoarthritic knees. Knee Surg Sports Traumatol Arthrosc 25:3146–3154. https://doi.org/10.1007/s00167-016-4221-z
Chun KC, Lee SH, Kim JW, Jin EJ, Kim KM, Chun CH (2017) Immunohistochemical and immunocytochemical study of mechanoreceptors in anterior cruciate ligament reconstruction with the remnant-preserving technique using Achilles tendon allografts. J Orthop Surg Res 12:93. https://doi.org/10.1186/s13018-017-0593-0
Delhaye BP, Long KH, Bensmaia SJ (2018) Neural basis of touch and proprioception in primate cortex. Compr Physiol 8:1575–1602. https://doi.org/10.1002/cphy.c170033
Dhillon MS, Bali K, Prabhakar S (2012) Differences among mechanoreceptors in healthy and injured anterior cruciate ligaments and their clinical importance. Muscles Ligaments Tendons J 2:38–43
Donato R, Cannon BR, Sorci G, Riuzzi F, Hsu K, Weber DJ, Geczy CL (2013) Functions of S100 proteins. Curr Mol Med 13:24–57
Franchi A, Zaccherotti G, Aglietti P (1995) Neural system of the human posterior cruciate ligament in osteoarthritis. J Arthroplast 10:679–682. https://doi.org/10.1016/s0883-5403(05)80215-3
Frank CB (2004) Ligament structure, physiology and function. J Musculoskelet Neuronal Interact 4:199–201
Halata Z, Wagner C, Baumann KI (1999) Sensory nerve endings in the anterior cruciate ligament (Lig. cruciatum anterius) of sheep. Anat Rec 254:13–21
Henry M, Baudry S (2019) Age-related changes in leg proprioception: implications for postural control. J Neurophysiol 122:525–538. https://doi.org/10.1152/jn.00067.2019
Kanamiya T, Whiteside LA, Nakamura T, Mihalko WM, Steiger J, Naito M (2002) Ranawat award paper. Effect of selective lateral ligament release on stability in knee arthroplasty. Clin Orthop Relat Res 404:24–31. https://doi.org/10.1097/00003086-200211000-00005
Kapetanakis S, Gkasdaris G, Daneva E, Givissis P, PaPaThanasiou J, Xanthos T (2018) Mechanoreceptors of the Achilles tendon: a histomorphological study in pigs with clinical significance for humans. Muscles Ligaments Tendons J 7:558–563. https://doi.org/10.11138/mltj/2017.7.4.558
Kennedy JC, Alexander IJ, Hayes KC (1982) Nerve supply of the human knee and its functional importance. Am J Sports Med 10:329–335. https://doi.org/10.1177/036354658201000601
Kholinne E, Lee HJ, Kim GY, Deslivia MF, Adikrishna A, Bin Z, Lee SJ, Rhyu IJ, Lim SJ, Hong HP, Jeon IH (2018) Mechanoreceptors distribution in the human medial collateral ligament of the elbow. Orthop Traumatol Surg Res 104:251–255. https://doi.org/10.1016/j.otsr.2018.01.005
Kosy JD, Mandalia VI (2018) Anterior cruciate ligament mechanoreceptors and their potential importance in remnant-preserving reconstruction: a review of basic science and clinical findings. J Knee Surg 31:736–746. https://doi.org/10.1055/s-0037-1608941
Krauspe R, Schmitz F, Zöller G, Drenckhahn D (1995) Distribution of neurofilament-positive nerve fibres and sensory endings in the human anterior cruciate ligament. Arch Orthop Trauma Surg 114:194–198. https://doi.org/10.1007/bf00444261
LaPrade RF, Wozniczka JK, Stellmaker MP, Wijdicks CA (2010) Analysis of the static function of the popliteus tendon and evaluation of an anatomic reconstruction: the "fifth ligament" of the knee. Am J Sports Med 38:543–549. https://doi.org/10.1177/0363546509349493
Lephart SM, Pincivero DM, Giraldo JL, Fu FH (1997) The role of proprioception in the management and rehabilitation of athletic injuries. Am J Sports Med 25:130–137. https://doi.org/10.1177/036354659702500126
Li B, Luo X, Wen Y (2019) Changes in mechanoreceptors in rabbits' anterior cruciate ligaments with age. J Mol Histol 50:229–237. https://doi.org/10.1007/s10735-019-09820-4
Nayak M, Nag HL, Gaba S, Nag TC, Sharma S (2018) Quantitative correlation of mechanoreceptors in tibial remnant of ruptured human anterior cruciate ligament with duration of injury and its significance: an immunohistochemistry-based observational study. J Orthop Traumatol 19:5. https://doi.org/10.1186/s10195-018-0498-7
Raunest J, Sager M, Burgener E (1998) Proprioception of the cruciate ligaments: receptor mapping in an animal model. Arch Orthop Trauma Surg 118:159–163. https://doi.org/10.1007/s004020050338
Rein S, Hagert E, Hanisch U, Lwowski S, Fieguth A, Zwipp H (2013) Immunohistochemical analysis of sensory nerve endings in ankle ligaments: a cadaver study. Cells Tissues Organs 197:64–76. https://doi.org/10.1159/000339877
Sha L, Xie G, Zhao S, Zhao J (2017) A morphologic and quantitative comparison of mechanoreceptors in the tibial remnants of the ruptured human anterior cruciate ligament. Medicine 96:e6081. https://doi.org/10.1097/MD.0000000000006081
Shigemitsu T, Tobe M, Mizutani K, Murakami K, Ishikawa Y, Sato F (2007) Innervation of the triangular fibrocartilage complex of the human wrist: quantitative immunohistochemical study. Anat Sci Int 82:127–132. https://doi.org/10.1111/j.1447-073X.2007.00173.x
Solomonow M (2006) Sensory-motor control of ligaments and associated neuromuscular disorders. J Electromyogr Kinesiol 16:549–567. https://doi.org/10.1016/j.jelekin.2006.08.004
Young SW, Valladares RD, Loi F, Dragoo JL (2016) Mechanoreceptor reinnervation of autografts versus allografts after anterior cruciate ligament reconstruction. Orthop J Sports Med 4:2325967116668782. https://doi.org/10.1177/2325967116668782
Zimny ML, Wink CS (1991) Neuroreceptors in the tissues of the knee joint. J Electromyogr Kinesiol 1:148–157. https://doi.org/10.1016/1050-6411(91)90031-Y
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This study was supported by the Key Projects of Natural Science Foundation of Liaoning Province (No. 20170540998).
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Han, Yh., Li, B. & Wen, Y. Distribution, quantity and gene expression of mechanoreceptors in ligaments and tendons of knee joint in rabbits. J Mol Hist 51, 233–240 (2020). https://doi.org/10.1007/s10735-020-09875-8
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DOI: https://doi.org/10.1007/s10735-020-09875-8