Research Progress in Neurogram and Neuro-Immune Interaction of Joints in the Case of Osteoarthritis

Jian GU, Tao JIANG

Acta Academiae Medicinae Sinicae ›› 2024, Vol. 46 ›› Issue (5) : 776-782.

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Acta Academiae Medicinae Sinicae

Abbreviation (ISO4): Acta Academiae Medicinae Sinicae      Editor in chief: Xuetao CAO

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Acta Academiae Medicinae Sinicae ›› 2024, Vol. 46 ›› Issue (5) : 776-782. DOI: 10.3881/j.issn.1000-503X.15872
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Research Progress in Neurogram and Neuro-Immune Interaction of Joints in the Case of Osteoarthritis

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Abstract

the joints have abundant sensory nerves and sympathetic nerve fibers,which convert physical and chemical stimuli in the joints into nerve impulses that are transmitted to the central nervous system and participate in the hypersensitivity reactions of inflammatory joint diseases such as osteoarthritis(OA).This paper summarizes the distribution and functional characteristics of intra-articular nerves and focuses on the mechanism of the vagus-sympathetic autonomic circuit in regulating the immune microenvironment in joints in the case of OA.in addition,intra-articular inflammatory cytokines represented by tumor necrosis factor-αand interleukin-6 directly or indirectly induce sensory nerve action potential and activate the pain transduction pathway from the local joint to the central nervous system.the sensory nerves in the joints in the case of OA are also involved in the recruitment of immune cells and inflammatory cytokines.This neuro-immune interaction model not only provides a variety of new targets for the treatment of OA but also suggests that the treatment of OA should adopt a holistic view with comprehensive consideration of the nerve and immune microenvironment in the bone and joint and their mutual influences。

Key words

osteoarthritis / sensory nerve / autonomic nerve / inflammatory cytokines / interaction

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Jian GU , Tao JIANG. Research Progress in Neurogram and Neuro-Immune Interaction of Joints in the Case of Osteoarthritis[J]. Acta Academiae Medicinae Sinicae. 2024, 46(5): 776-782 https://doi.org/10.3881/j.issn.1000-503X.15872

References

[1]
Hunter DJ, Bierma-Zeinstra S. Osteoarthritis[J]. Lancet, 2019, 393(10182):1745-1759.DOI:10.1016/S0140-6736(19)30417-9.
[2]
Sharma L. Osteoarthritis of the knee[J]. New Engl J Med, 2021, 384(1):51-59.DOI:10.1056/NEJMcp1903768.
[3]
Jiang W, Jin Y, Zhang S, et al. PGE2 activates EP4 in subchondral bone osteoclasts to regulate osteoarthritis[J]. Bone Res, 2022, 10(1):27.DOI:10.1038/s41413-022-00201-4.
[4]
Zhu S, Zhu J, Zhen G, et al. Subchondral bone osteoclasts induce sensory innervation and osteoarthritis pain[J]. J Clin Invest, 2019, 129(3):1076-1093.DOI:10.1172/JCI121561.
[5]
Grubb BD. Activation of sensory neurons in the arthritic joint[J]. Novartis Found Symp, 2004, 260:28-36,36-48,100-104,277-279.
[6]
Thai J, Kyloh M, Travis L, et al. Identifying spinal afferent (sensory) nerve endings that innervate the marrow cavity and periosteum using anterograde tracing[J]. J Comp Neurol, 2020, 528(11):1903-1916.DOI:10.1002/cne.24862.
[7]
Dye SF, Vaupel GL, Dye CC. Conscious neurosensory mapping of the internal structures of the human knee without intraarticular anesthesia[J]. Am J Sport Med, 1998, 26(6):773-777.DOI:10.1177/03635465980260060601.
[8]
Saxler G, Loer F, Skumavc M, et al. Localization of SP-and CGRP-immunopositive nerve fibers in the hip joint of patients with painful osteoarthritis and of patients with painless failed total hip arthroplasties[J]. Eur J Pain, 2007, 11(1):67-74.DOI:10.1016/j.ejpain.2005.12.011.
[9]
Liu S, Liu S, Li S, et al. Nerves within bone and their application in tissue engineering of bone regeneration[J]. Front Neurol, 2022, 13:1085560.DOI:10.3389/fneur.2022.1085560.
[10]
Chartier SR, Mitchell S, Majuta LA, et al. The changing sensory and sympathetic innervation of the young,adult and aging mouse femur[J]. Neuroscience, 2018, 387:178-190.DOI:10.1016/j.neuroscience.2018.01.047.
[11]
Mei H, Wu Y, Feng Q, et al. The interplay between the nerves and skeleton:a 30-year bibliometric analysis[J]. Ann Transl Med, 2023, 11(1):9.DOI:10.21037/atm-22-3323.
[12]
Laumonerie P, Dalmas Y, Tibbo ME, et al. Sensory innervation of the hip joint and referred pain:a systematic review of the literature[J]. Pain Med, 2021, 22(5):1149-1157.DOI:10.1093/pm/pnab061.
[13]
De Marziani L, Boffa A, Angelelli L, et al. Infrared thermography in symptomatic knee osteoarthritis:joint temperature differs based on patient and pain characteristics[J]. J Clin Med, 2023, 12(6):2319.DOI:10.3390/jcm12062319.
[14]
Basbaum AI, Bautista DM, Scherrer G, et al. Cellular and molecular mechanisms of pain[J]. Cell, 2009, 139(2):267-284.DOI:10.1016/j.cell.2009.09.028.
[15]
Malfait AM, Schnitzer TJ. Towards a mechanism-based approach to pain management in osteoarthritis[J]. Nat Rev Rheumatol, 2013, 9(11):654-664.DOI:10.1038/nrrheum.2013.138.
[16]
Shin SM, Moehring F, Itson-Zoske B, et al. Piezo2 mechanosensitive ion channel is located to sensory neurons and nonneuronal cells in rat peripheral sensory pathway:implications in pain[J]. Pain, 2021, 162(11):2750-2768.DOI:10.1097/j.pain.0000000000002356.
[17]
Finnerup NB, Kuner R, Jensen TS. Neuropathic pain:from mechanisms to treatment[J]. Physiol Rev, 2021, 101(1):259-301.DOI:10.1152/physrev.00045.2019.
[18]
Woolf CJ. Central sensitization:implications for the diagnosis and treatment of pain[J]. Pain, 2011, 152(3 Suppl):S2-S15.DOI:10.1016/j.pain.2010.09.030.
[19]
Clauw DJ, Hassett AL. The role of centralised pain in osteoarthritis[J]. Clin Exp Rheumatol, 2017, 35 Suppl 107(5):79-84.
[20]
Sohn R, Rosch G, Junker M, et al. Adrenergic signalling in osteoarthritis[J]. Cell Signal, 2021, 82:109948.DOI:10.1016/j.cellsig.2021.109948.
[21]
Grassel S, Muschter D. Peripheral nerve fibers and their neurotransmitters in osteoarthritis pathology[J]. Int J Mol Sci, 2017, 18(5):931.DOI:10.3390/ijms18050931.
[22]
Mitchell J, Lai LP, Peralta F, et al. β2-adrenergic receptors inhibit the expression of collagen type Ⅱ in growth plate chondrocytes by stimulating the AP-1 factor Jun-B[J]. Am J Physiol Endocrinol Metab, 2011, 300(4):E633-E639.DOI:10.1152/ajpendo.00515.2010.
[23]
Miller LE, Grifka J, Scholmerich J, et al. Norepinephrine from synovial tyrosine hydroxylase positive cells is a strong indicator of synovial inflammation in rheumatoid arthritis[J]. J Rheumatol, 2002, 29(3):427-435.
[24]
Lorenz J, Schäfer N, Bauer R, et al. Norepinephrine modulates osteoarthritic chondrocyte metabolism and inflammatory responses[J]. Osteoarthritis Cartilage, 2016, 24(2):325-334.DOI:10.1016/j.joca.2015.08.007.
[25]
Kang X, Qian Z, Liu J, et al. Neuropeptide Y acts directly on cartilage homeostasis and exacerbates progression of osteoarthritis through NPY2R[J]. J Bone Miner Res, 2020, 35(7):1375-1384.DOI:10.1002/jbmr.3991.
[26]
Hasebe R, Murakami K, Harada M, et al. ATP spreads inflammation to other limbs through crosstalk between sensory neurons and interneurons[J]. J Exp Med, 2022, 219(6):e20212019.DOI:10.1084/jem.20212019.
[27]
Rösch G, El Bagdadi K, Muschter D, et al. Sympathectomy aggravates subchondral bone changes during osteoarthritis progression in mice without affecting cartilage degeneration or synovial inflammation[J]. Osteoarthritis Cartilage, 2022, 30(3):461-474.DOI:10.1016/j.joca.2021.11.016.
[28]
Tracey KJ. The inflammatory reflex[J]. Nature, 2002, 420(6917):853-859.DOI:10.1038/nature01321.
[29]
Akoolo L, Djokic V, Rocha SC, et al. Sciatic-vagal nerve stimulation by electroacupuncture alleviates inflammatory arthritis in lyme disease-susceptible C3H mice[J]. Front Immunol, 2022, 13:930287.DOI:10.3389/fimmu.2022.930287.
[30]
Chakrabarti S, Pattison LA, Singhal K, et al. Acute inflammation sensitizes knee-innervating sensory neurons and decreases mouse digging behavior in a TRPV1-dependent manner[J]. Neuropharmacology, 2018, 143:49-62.DOI:10.1016/j.neuropharm.2018.09.014.
[31]
Ishihara S, Obeidat AM, Wokosin DL, et al. The role of intra-articular neuronal CCR2 receptors in knee joint pain associated with experimental osteoarthritis in mice[J]. Arthritis Res Ther, 2021, 23(1):103.DOI:10.1186/s13075-021-02486-y.
[32]
Schaible HG, von Banchet GS, Boettger MK, et al. The role of proinflammatory cytokines in the generation and maintenance of joint pain[J]. Ann Ny Acad Sci, 2010, 1193:60-69.DOI:10.1111/j.1749-6632.2009.05301.x.
[33]
Kapoor M, Martel-Pelletier J, Lajeunesse D, et al. Role of proinflammatory cytokines in the pathophysiology of osteoarthritis[J]. Nat Rev Rheumatol, 2011, 7(1):33-42.DOI:10.1038/nrrheum.2010.196.
[34]
Pan F, Tian J, Cicuttini F, et al. Prospective association between inflammatory markers and knee cartilage volume loss and pain trajectory[J]. Pain Ther, 2022, 11(1):107-119.DOI:10.1007/s40122-021-00341-1.
[35]
Kaaij MH, van Tok MN, Blijdorp IC, et al. Transmembrane TNF drives osteoproliferative joint inflammation reminiscent of human spondyloarthritis[J]. J Exp Med, 2020, 217(10):e20200288.DOI:10.1084/jem.20200288.
[36]
Liao Y, Ren Y, Luo X, et al. Interleukin-6 signaling mediates cartilage degradation and pain in posttraumatic osteoarthritis in a sex-specific manner[J]. Sci Signal, 2022, 15(744):eabn7082.DOI:10.1126/scisignal.abn7082.
[37]
Takano S, Uchida K, Miyagi M, et al. Nerve growth factor regulation by TNF-alpha and IL-1beta in synovial macrophages and fibroblasts in osteoarthritic mice[J]. J Immunol Res, 2016, 2016:5706359.DOI:10.1155/2016/5706359.
[38]
Vincent TL. Peripheral pain mechanisms in osteoarthritis[J]. Pain, 2020, 161 Suppl 1(1):S138-S146.DOI:10.1097/j.pain.0000000000001923.
[39]
LaBranche TP, Bendele AM, Omura BC, et al. Nerve growth factor inhibition with tanezumab influences weight-bearing and subsequent cartilage damage in the rat medial meniscal tear model[J]. Ann Rheum Dis, 2017, 76(1):295-302.DOI:10.1136/annrheumdis-2015-208913.
[40]
von Loga IS, El-Turabi A, Jostins L, et al. Active immunisation targeting nerve growth factor attenuates chronic pain behaviour in murine osteoarthritis[J]. Ann Rheum Dis, 2019, 78(5):672-675.DOI:10.1136/annrheumdis-2018-214489.
[41]
Mailhot B, Christin M, Tessandier N, et al. Neuronal interleukin-1 receptors mediate pain in chronic inflammatory diseases[J]. J Exp Med, 2020, 217(9):e20191430.DOI:10.1084/jem.20191430.
[42]
Chandran V, Abji F, Perruccio AV, et al. Serum-based soluble markers differentiate psoriatic arthritis from osteoarthritis[J]. Ann Rheum Dis, 2019, 78(6):796-801.DOI:10.1136/annrheumdis-2018-214737.
[43]
Moon HJ, Yurube T, Lozito TP, et al. Effects of secreted factors in culture medium of annulus fibrosus cells on microvascular endothelial cells:elucidating the possible pathomechanisms of matrix degradation and nerve in-growth in disc degeneration[J]. Osteoarthritis Cartilage, 2014, 22(2):344-354.DOI:10.1016/j.joca.2013.12.008.
[44]
Tewari D, Cook AD, Lee MC, et al. Granulocyte-macrophage colony stimulating factor as an indirect mediator of nociceptor activation and pain[J]. J Neurosci, 2020, 40(11):2189-2199.DOI:10.1523/JNEUROSCI.2268-19.2020.
[45]
Raoof R, Martin GC, Lafeber F, et al. Dorsal root ganglia macrophages maintain osteoarthritis pain[J]. J Neurosci, 2021, 41(39):8249-8261.DOI:10.1523/JNEUROSCI.1787-20.2021.
[46]
Baliu-Pique M, Jusek G, Holzmann B. Neuroimmunological communication via CGRP promotes the development of a regulatory phenotype in TLR4-stimulated macrophages[J]. Eur J Immunol, 2014, 44(12):3708-3716.DOI:10.1002/eji.201444553.
[47]
Suvas S. Role of substance P neuropeptide in inflammation,wound healing,and tissue homeostasis[J]. J Immunol, 2017, 199(5):1543-1552.DOI:10.4049/jimmunol.1601751.
[48]
Sun J, Ramnath RD, Zhi L, et al. Substance P enhances NF-kappaB transactivation and chemokine response in murine macrophages via ERK1/2 and p38 MAPK signaling pathways[J]. Am J Physiol-Cell Ph, 2008, 294(6):C1586-C1596.DOI:10.1152/ajpcell.00129.2008.
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