Neuronal regulation of tendon homoeostasis

International Journal of Experimental Pathology

Volumn 94, Issue 4, 2013, Pages 271-286

  Ackermann, Paul W ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Homeostasis; Peripheral nervous system; Tendon

Indexed keywords

ACETYLCHOLINE; CANNABINOID; GLUTAMIC ACID; NEUROPEPTIDE; NORADRENALIN;

ADRENERGIC SYSTEM; CHRONIC PAIN; HEALING; HOMEOSTASIS; HUMAN; INFLAMMATION; MEDIATOR; NERVE CELL PLASTICITY; NEUROANATOMY; PRIORITY JOURNAL; REVIEW; SENSORY NERVE; TENDINITIS; TENDON; TENDON INJURY; TENDON RECONSTRUCTION; TISSUE ENGINEERING; TISSUE REACTION;

HOMEOSTASIS; PERIPHERAL NERVOUS SYSTEM; TENDON;

ANIMALS; HOMEOSTASIS; HUMANS; INFLAMMATION; NEURONS; PERIPHERAL NERVOUS SYSTEM; TENDINOPATHY; TENDON INJURIES; TENDONS;

EID: 84880283604     PISSN: 09599673     EISSN: 13652613     Source Type: Journal    
DOI: 10.1111/iep.12028     Document Type: Review

References (86)

1. Ackermann P.W. (2001) Peptidergic innervation of periarticular tissue. In Molecular Medicine and Surgery. Karolinska Institutet.
2. Ackermann P.W. (2012) Katz et al., efficacy and safety of tanezumab in the treatment of chronic low back pain [Pain 2011;152:2248-2258] and Hill, blocking the effects of NGF as a route to safe and effective pain relief - fact or fancy? [Pain 2011;152:2200-2201]. Pain 153, 1128-1129; author reply 1129-1131.
3. Ackermann P.W., Finn A., Ahmed M. (1999) Sensory neuropeptidergic pattern in tendon, ligament and joint capsule. A study in the rat. NeuroReport 10, 2055-2060.
4. Ackermann P.W., Li J., Finn A., Ahmed M., Kreicbergs A. (2001a) Autonomic innervation of tendons, ligaments and joint capsules. A morphologic and quantitative study in the rat. J. Orthop. Res. 19, 372-378.
5. Ackermann P.W., Spetea M., Nylander I., Ploj K., Ahmed M., Kreicbergs A. (2001b) An opioid system in connective tissue: a study of achilles tendon in the rat. J. Histochem. Cytochem. 49, 1387-1395.
6. Ackermann P.W., Ahmed M., Kreicbergs A. (2002) Early nerve regeneration after achilles tendon rupture-a prerequisite for healing? A study in the rat. J. Orthop. Res. 20, 849-856.
7. Ackermann P.W., Li J., Lundeberg T., Kreicbergs A. (2003) Neuronal plasticity in relation to nociception and healing of rat achilles tendon. J. Orthop. Res. 21, 432-441.
8. Ackermann P.W., Calder J., Aspenberg P. (2008) Healing and repair mechanisms. In: Achilles Tendon Rupture, pp. 17-26 (eds N. Van Dijk, J. Karlsson, N. Maffulli, H. Thermann ), Guildford, Surrey, UK: DJO Publications.
9. Ackermann P.W., Salo P.T., Hart D.A. (2009) Neuronal pathways in tendon healing. Front. Biosci. 14, 5165-5187.
10. Ackermann P.W., Domeij-Arverud E., Leclerc P., Amoudrouz P., Nader G.A. (2012) Anti-inflammatory cytokine profile in early human tendon repair. Knee Surg Sports Traumatol Arthrosc.
11. Ahmed A.S., Schizas N., Li J. et al. (2012) Type 2 diabetes impairs tendon repair after injury in a rat model. J. Appl. Physiol. 113, 1784-1791.
12. Alfredson H., Forsgren S., Thorsen K., Lorentzon R. (2001) In vivo microdialysis and immunohistochemical analyses of tendon tissue demonstrated high amounts of free glutamate and glutamate NMDAR1 receptors, but no signs of inflammation, in Jumper's knee. J. Orthop. Res. 19, 881-886.
13. Aubdool A.A. & Brain S.D. (2011) Neurovascular aspects of skin neurogenic inflammation. J. Investig. Dermatol. Symp. Proc. 15, 33-39.
14. Audet M. & Bouvier M. (2012) Restructuring G-protein- coupled receptor activation. Cell 151, 14-23.
15. Backman L.J., Andersson G., Wennstig G., Forsgren S., Danielson P. (2011) Endogenous substance P production in the Achilles tendon increases with loading in an in vivo model of tendinopathy-peptidergic elevation preceding tendinosis-like tissue changes. J. Musculoskelet. Neuronal Interact. 11, 133-140.
16. Bayliss W.M. (1901) On the origin from the spinal cord of the vaso-dilator fibres of the hind-limb, and on the nature of these fibres. J. Physiol. 26, 173-209.
17. Bjur D., Danielson P., Alfredson H., Forsgren S. (2007) Presence of a non-neuronal cholinergic system and occurrence of up- and down-regulation in expression of M2 muscarinic acetylcholine receptors: new aspects of importance regarding Achilles tendon tendinosis (tendinopathy). Cell Tissue Res. 331, 385-400.
18. Bjur D., Danielson P., Alfredson H., Forsgren S. (2008) Immunohistochemical and in situ hybridization observations favor a local catecholamine production in the human Achilles tendon. Histol. Histopathol. 23, 197-208.
19. Brain S.D. & Williams T.J. (1985) Inflammatory oedema induced by synergism between calcitonin gene-related peptide (CGRP) and mediators of increased vascular permeability. Br. J. Pharmacol. 86, 855-860.
20. Brain S.D., Williams T.J., Tippins J.R., Morris H.R., MacIntyre I. (1985) Calcitonin gene-related peptide is a potent vasodilator. Nature 313, 54-56.
21. Bring D.K., Kreicbergs A., Renstrom P.A., Ackermann P.W. (2007) Physical activity modulates nerve plasticity and stimulates repair after Achilles tendon rupture. J. Orthop. Res. 25, 164-172.
22. Bring D., Reno C., Renstrom P., Salo P., Hart D., Ackermann P. (2009a) Prolonged immobilization compromises up-regulation of repair genes after tendon rupture in a rat model. Scand. J. Med. Sci. Sports 20, 411-417.
23. Bring D.K.I., Reno C., Renstrom P., Salo P., Hart D.A., Ackermann P.W. (2009b) Joint immobilization reduces the expression of sensory neuropeptide receptors and impairs healing after tendon rupture in a rat model. J. Orthop. Res. 27, 274-280.
24. Bring D.K., Paulson K., Renstrom P., Salo P., Hart D.A., Ackermann P.W. (2012) Residual substance P levels after capsaicin treatment correlate with tendon repair. Wound Repair Regen. 20, 50-60.
25. Burssens P., Steyaert A., Forsyth R., van Ovost E.J., De Paepe Y., Verdonk R. (2005) Exogenously administered substance P and neutral endopeptidase inhibitors stimulate fibroblast proliferation, angiogenesis and collagen organization during Achilles tendon healing. Foot Ankle Int. 26, 832-839.
26. Carlsson O., Schizas N., Li J., Ackermann P.W. (2011) Substance P injections enhance tissue proliferation and regulate sensory nerve ingrowth in rat tendon repair. Scand. J. Med. Sci. Sports 21, 562-569.
27. Danielson P., Alfredson H., Forsgren S. (2006) Immunohistochemical and histochemical findings favoring the occurrence of autocrine/paracrine as well as nerve-related cholinergic effects in chronic painful patellar tendon tendinosis. Microsc. Res. Tech. 69, 808-819.
28. Danielson P., Alfredson H., Forsgren S. (2007a) In situ hybridization studies confirming recent findings of the existence of a local nonneuronal catecholamine production in human patellar tendinosis. Microsc. Res. Tech. 70, 908-911.
29. Danielson P., Alfredson H., Forsgren S. (2007b) Studies on the importance of sympathetic innervation, adrenergic receptors, and a possible local catecholamine production in the development of patellar tendinopathy (tendinosis) in man. Microsc. Res. Tech. 70, 310-324.
30. Danielson P., Andersson G., Alfredson H., Forsgren S. (2007c) Extensive expression of markers for acetylcholine synthesis and of M2 receptors in tenocytes in therapy-resistant chronic painful patellar tendon tendinosis - a pilot study. Life Sci. 80, 2235-2238.
31. Dwyer K.W., Provenzano P.P., Muir P., Valhmu W.B., Vanderby R. Jr. (2004) Blockade of the sympathetic nervous system degrades ligament in a rat MCL model. J. Appl. Physiol. 96, 711-718.
32. Fernandes E.S., Schmidhuber S.M., Brain S.D. (2009) Sensory-nerve-derived neuropeptides: possible therapeutic targets. Handb. Exp. Pharmacol. 393-416. doi: 10.1007/978-3-540-79090-7_11.
33. Gargiulo P., Reynisson P.J., Helgason B. et al. (2011) Muscle, tendons, and bone: structural changes during denervation and FES treatment. Neurol. Res. 33, 750-758.
34. Greve K., Domeij-Arverud E., Labruto F. et al. (2012) Metabolic activity in early tendon repair can be enhanced by intermittent pneumatic compression. Scand. J. Med. Sci. Sports 22, e55-e63.
35. Grorud K.W., Jensen K.T., Provenzano P.P., Vanderby R. Jr. (2007) Adjuvant neuropeptides can improve neuropathic ligament healing in a rat model. J. Orthop. Res. 25, 703-712.
36. Haegerstrand A., Dalsgaard C.J., Jonzon B., Larsson O., Nilsson J. (1990) Calcitonin gene-related peptide stimulates proliferation of human endothelial cells. Proc. Natl Acad. Sci. USA 87, 3299-3303.
37. Hogervorst T. & Brand R.A. (1998) Mechanoreceptors in joint function. J. Bone Joint Surg. Am. 80, 1365-1378.
38. Hokfelt T., Johansson O., Ljungdahl A., Lundberg J.M., Schultzberg M. (1980) Peptidergic neurones. Nature 284, 515-521.
39. Hong H.S., Lee J., Lee E. et al. (2009) A new role of substance P as an injury-inducible messenger for mobilization of CD29(+) stromal-like cells. Nat. Med. 15, 425-435.
40. Hukkanen M., Konttinen Y.T., Santavirta S. et al. (1993) Rapid proliferation of calcitonin gene-related peptide-immunoreactive nerves during healing of rat tibial fracture suggests neural involvement in bone growth and remodelling. Neuroscience 54, 969-979.
41. Ivie T.J., Bray R.C., Salo P.T. (2002) Denervation impairs healing of the rabbit medial collateral ligament. J. Orthop. Res. 20, 990-995.
42. Jonsdottir I.H. (2000) Special feature for the olympics: effects of exercise on the immune system: neuropeptides and their interaction with exercise and immune function. Immunol. Cell Biol. 78, 562-570.
43. Jozsa L. & Kannus P. (1997) Human Tendons. Anatomy, Physiology, and Pathology. Danvers, MA: Human Kinetics.
44. Kager I., Mousa S.A., Sieper J., Stein C., Pipam W., Likar R. (2011) Blockade of intra-articular adrenergic receptors increases analgesic demands for pain relief after knee surgery. Rheumatol. Int. 31, 1299-1306.
45. Karanth S.S., Dhital S., Springall D.R., Polak J.M. (1990) Reinnervation and neuropeptides in mouse skin flaps. J. Auton. Nerv. Syst. 31, 127-134.
46. Kishimoto S. (1984) The regeneration of substance P-containing nerve fibers in the process of burn wound healing in the guinea pig skin. J. Invest. Dermatol. 83, 219-223.
47. Klatt S., Fassold A., Straub R.H. (2012) Sympathetic nerve fiber repulsion: testing norepinephrine, dopamine, and 17beta-estradiol in a primary murine sympathetic neurite outgrowth assay. Ann. N. Y. Acad. Sci. 1261, 26-33.
48. Li J., Ahmad T., Spetea M., Ahmed M., Kreicbergs A. (2001) Bone reinnervation after fracture: a study in the rat. J. Bone Miner. Res. 16, 1505-1510.
49. Lian O., Dahl J., Ackermann P.W., Frihagen F., Engebretsen L., Bahr R. (2006) Pronociceptive and antinociceptive neuromediators in patellar tendinopathy. Am. J. Sports Med. 34, 1801-1808.
50. Ljung B.O., Forsgren S., Friden J. (1999) Sympathetic and sensory innervations are heterogeneously distributed in relation to the blood vessels at the extensor carpi radialis brevis muscle origin of man. Cells Tissues Organs 165, 45-54.
51. Madden D.R. (2002) The structure and function of glutamate receptor ion channels. Nat. Rev. Neurosci. 3, 91-101.
52. Maffulli N., Irwin A.S., Kenward M.G., Smith F., Porter R.W. (1998) Achilles tendon rupture and sciatica: a possible correlation. Br. J. Sports Med. 32, 174-177.
53. Maggi C.A. (1995) Tachykinins and calcitonin gene-related peptide (CGRP) as co-transmitters released from peripheral endings of sensory nerves. Prog. Neurobiol. 45, 1-98.
54. Magnusson S.P., Langberg H., Kjaer M. (2010) The pathogenesis of tendinopathy: balancing the response to loading. Nat. Rev. Rheumatol. 6, 262-268.
55. Mammoto T., Seerattan R.A., Paulson K.D., Leonard C.A., Bray R.C., Salo P.T. (2008) Nerve growth factor improves ligament healing. J. Orthop. Res. 26, 957-964.
56. Martin P. (1997) Wound healing-aiming for perfect skin regeneration. Science 276, 75-81.
57. McNeilly C.M., Banes A.J., Benjamin M., Ralphs J.R. (1996) Tendon cells in vivo form a three dimensional network of cell processes linked by gap junctions. J. Anat. 189(Pt 3), 593-600.
58. Micera A., Lambiase A., Stampachiacchiere B., Bonini S., Bonini S., Levi-Schaffer F. (2007) Nerve growth factor and tissue repair remodeling: trkA(NGFR) and p75(NTR), two receptors one fate. Cytokine Growth Factor Rev. 18, 245-256.
59. Molloy T.J., Kemp M.W., Wang Y., Murrell G.A. (2006a) Microarray analysis of the tendinopathic rat supraspinatus tendon: glutamate signaling and its potential role in tendon degeneration. J. Appl. Physiol. 101, 1702-1709.
60. Molloy T.J., Wang Y., Horner A., Skerry T.M., Murrell G.A. (2006b) Microarray analysis of healing rat Achilles tendon: evidence for glutamate signaling mechanisms and embryonic gene expression in healing tendon tissue. J. Orthop. Res. 24, 842-855.
61. Moody T.W., Ito T., Osefo N., Jensen R.T. (2011) VIP and PACAP: recent insights into their functions/roles in physiology and disease from molecular and genetic studies. Curr. Opin. Endocrinol. Diabetes Obes. 18, 61-67.
62. Narici M.V., Maffulli N., Maganaris C.N. (2008) Ageing of human muscles and tendons. Disabil. Rehabil. 30, 1548-1554.
63. Nilsson J., von Euler A.M., Dalsgaard C.J. (1985) Stimulation of connective tissue cell growth by substance P and substance K. Nature 315, 61-63.
64. Pradhan L., Nabzdyk C., Andersen N.D., LoGerfo F.W., Veves A. (2009) Inflammation and neuropeptides: the connection in diabetic wound healing. Expert Rev. Mol. Med. 11, e2.
65. Ramchurn N., Mashamba C., Leitch E. et al. (2009) Upper limb musculoskeletal abnormalities and poor metabolic control in diabetes. Eur. J. Intern. Med. 20, 718-721.
66. Reeves N.D., Maganaris C.N., Narici M.V. (2003) Effect of strength training on human patella tendon mechanical properties of older individuals. J. Physiol. 548, 971-981.
67. Salo P.T., Beye J.A., Seerattan R.A., Leonard C.A., Ivie T.J., Bray R.C. (2008) Plasticity of peptidergic innervation in healing rabbit medial collateral ligament. Can. J. Plast. Surg. 51, 167-172.
68. Sanchis-Alfonso V., Rosello-Sastre E., Subias-Lopez A. (2001) Neuroanatomic basis for pain in patellar tendinosis ("jumper's knee"): a neuroimmunohistochemical study. Am. J. Knee Surg. 14, 174-177.
69. Schizas N., Andersson T., Fahlgren A., Aspenberg P., Ahmed M., Ackermann P. (2010a) Compression therapy promotes proliferative repair during rat achilles tendon immobilization. J. Orthop. Res. 28, 852.
70. Schizas N., Lian O., Frihagen F., Engebretsen L., Bahr R., Ackermann P.W. (2010b) Coexistence of up-regulated NMDA receptor 1 and glutamate on nerves, vessels and transformed tenocytes in tendinopathy. Scand. J. Med. Sci. Sports 20, 208-215.
71. Schizas N., Weiss R., Lian O., Frihagen F., Bahr R., Ackermann P.W. (2012) Glutamate receptors in tendinopathic patients. J. Orthop. Res. 30, 1447-1452.
72. Schubert T.E., Weidler C., Lerch K., Hofstadter F., Straub R.H. (2005) Achilles tendinosis is associated with sprouting of substance P positive nerve fibres. Ann. Rheum. Dis. 64, 1083-1086.
73. Scott A., Alfredson H., Forsgren S. (2007) VGluT2 expression in painful Achilles and patellar tendinosis: evidence of local glutamate release by tenocytes. J. Orthop. Res. 26, 685-689.
74. Steinbrech D.S., Longaker M.T., Mehrara B.J. et al. (1999) Fibroblast response to hypoxia: the relationship between angiogenesis and matrix regulation. J. Surg. Res. 84, 127-133.
75. Steyaert A.E., Burssens P.J., Vercruysse C.W., Vanderstraeten G.G., Verbeeck R.M. (2006) The effects of substance P on the biomechanic properties of ruptured rat Achilles' tendon. Arch. Phys. Med. Rehabil. 87, 254-258.
76. Stilwell D.L. Jr. (1957) The innervation of tendons and aponeuroses. Am. J. Anat. 100, 289-317.
77. Strasmann T., Weihe E., Halata Z. (1990) CGRP-like immunoreactivity in sensory nerve endings of the Golgi tendon organ. A light- and electron-microscopic study in the grey short-tailed opossum (Monodelphis domestica). Acta Anat. 137, 278-281.
78. Tracey K.J. (2002) The inflammatory reflex. Nature 420, 853-859.
79. Waggett A.D., Benjamin M., Ralphs J.R. (2006) Connexin 32 and 43 gap junctions differentially modulate tenocyte response to cyclic mechanical load. Eur. J. Cell Biol. 85, 1145-1154.
80. Wall M.E., Faber J.E., Yang X., Tsuzaki M., Banes A.J. (2004) Norepinephrine-induced calcium signaling and expression of adrenoceptors in avian tendon cells. Am. J. Physiol. 287, C912-C918.
81. Wang J.H., Guo Q., Li B. (2012) Tendon biomechanics and mechanobiology-a minireview of basic concepts and recent advancements. J. Hand Ther. 25, 133-140; quiz 141.
82. Wozniak K.M., Rojas C., Wu Y., Slusher B.S. (2012) The role of glutamate signaling in pain processes and its regulation by GCP II inhibition. Curr. Med. Chem. 19, 1323-1334.
83. Ytteborg E., Torgersen J.S., Pedersen M.E., Helland S.J., Grisdale-Helland B., Takle H. (2012) Exercise induced mechano-sensing and Substance P mediated bone modeling in Atlantic salmon. Bone.
84. Zhang H. & Faber J.E. (2001) Trophic effect of norepinephrine on arterial intima-media and adventitia is augmented by injury and mediated by different alpha1-adrenoceptor subtypes. Circ. Res. 89, 815-822.
85. Ziche M., Morbidelli L., Pacini M., Geppetti P., Alessandri G., Maggi C.A. (1990) Substance P stimulates neovascularization in vivo and proliferation of cultured endothelial cells. Microvasc. Res. 40, 264-278.
86. Zukowska-Grojec Z., Karwatowska-Prokopczuk E., Rose W. et al. (1998) Neuropeptide Y: a novel angiogenic factor from the sympathetic nerves and endothelium. Circ. Res. 83, 187-195.