Nervous System-Driven Osseointegration
Abstract
:1. Introduction
2. Osseointegration
2.1. The Concept of Osseointegration
2.2. Four Stages throughout the Osseointegration
2.2.1. The Formation of Blood Clots
2.2.2. Immune Responses
2.2.3. Angiogenesis
2.2.4. Osteogenesis
3. The Effect of the Nervous System on Bone
3.1. Neurotrophins (NTs) and Their Receptors
3.1.1. NGF
3.1.2. NT-3
3.1.3. NT-4/5
3.1.4. BDNF
3.1.5. GDNF
3.1.6. PDGF
3.1.7. FGF
3.2. Neuropeptides
3.2.1. CGRP
3.2.2. SP
3.2.3. VIP
3.2.4. PACAP
3.2.5. NPY
3.3. Nerve Cell
3.3.1. Schwann Cell
3.3.2. Sensory Nerve Cell
4. The Impact of the Nervous System on Each Stage of Osseointegration
4.1. Immune Responses
4.2. Angiogenesis
4.3. Osteogenesis
5. Future Outlook and Limitations
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Nuss, K.M.R.; von Rechenberg, B. Biocompatibility issues with modern implants in bone—A review for clinical orthopedics. Open Orthop. J. 2008, 2, 66–78. [Google Scholar] [CrossRef]
- Liu, Y.; Rath, B.; Tingart, M.; Eschweiler, J. Role of implants surface modification in osseointegration: A systematic review. J. Biomed. Mater. Res. A 2020, 108, 470–484. [Google Scholar] [CrossRef]
- Legeros, R.Z.; Craig, R.G. Strategies to affect bone remodeling: Osteointegration. J. Bone Miner. Res. 1993, 8, S583–S596. [Google Scholar] [CrossRef]
- Albrektsson, T.; Wennerberg, A. On osseointegration in relation to implant surfaces. Clin. Implant Dent. 2019, 21, 4–7. [Google Scholar] [CrossRef]
- Zhao, H.; Shen, S.; Zhao, L.; Xu, Y.; Li, Y.; Zhuo, N. 3D printing of dual-cell delivery titanium alloy scaffolds for improving osseointegration through enhancing angiogenesis and osteogenesis. BMC Musculoskel. Dis. 2021, 22, 734. [Google Scholar] [CrossRef]
- Bai, L.; Zhao, Y.; Chen, P.; Zhang, X.; Huang, X.; Du, Z.; Crawford, R.; Yao, X.; Tang, B.; Hang, R.; et al. Targeting Early Healing Phase with Titania Nanotube Arrays on Tunable Diameters to Accelerate Bone Regeneration and Osseointegration. Small 2021, 17, 2006287. [Google Scholar] [CrossRef]
- Bai, L.; Du, Z.; Du, J.; Yao, W.; Zhang, J.; Weng, Z.; Liu, S.; Zhao, Y.; Liu, Y.; Zhang, X.; et al. A multifaceted coating on titanium dictates osteoimmunomodulation and osteo/angio-genesis towards ameliorative osseointegration. Biomaterials 2018, 162, 154–169. [Google Scholar] [CrossRef]
- Chéret, J.; Lebonvallet, N.; Carré, J.-L.; Misery, L.; Le Gall-Ianotto, C. Role of neuropeptides, neurotrophins, and neurohormones in skin wound healing. Wound Repair Regen. 2013, 21, 772–788. [Google Scholar] [CrossRef]
- Sahay, A.; Kale, A.; Joshi, S. Role of neurotrophins in pregnancy and offspring brain development. Neuropeptides 2020, 83, 102075. [Google Scholar] [CrossRef]
- Scuri, M.S.; Samsell, L.; Piedimonte, G. The role of neurotrophins in inflammation and allergy. Inflamm. Allergy Drug Targets 2010, 9, 173–180. [Google Scholar] [CrossRef]
- Chen, B.; Pei, G.-x.; Jin, D.; Wei, K.-h.; Qin, Y.; Liu, Q. Distribution and property of nerve fibers in human long bone tissue. Chin. J. Traumatol. 2007, 10, 3–9. [Google Scholar]
- García-Castellano, J.M.; Díaz-Herrera, P.; Morcuende, J.A. Is bone a target-tissue for the nervous system? New advances on the understanding of their interactions. Lowa Orthop. J. 2000, 20, 49–58. [Google Scholar]
- Jacobs, R.; van Steenberghe, D. From osseoperception to implant-mediated sensory-motor interactions and related clinical implications. J. Oral Rehabil. 2006, 33, 282–292. [Google Scholar] [CrossRef]
- Alizade, C.; Jafarov, A.; Berchenko, G.; Bicer, O.S.; Alizada, F. Investigation of the process intergrowth of bone tissue into the hole in titanium implants (Experimental research). Injury 2022, 53, 2741–2748. [Google Scholar] [CrossRef]
- Myers, R. Presentation highlights: Osseointegration. J. Rehabil. Res. Dev. 2002, 39, 7–8. [Google Scholar]
- Listgarten, M.A.; Lang, N.P.; Schroeder, H.E.; Schroeder, A. Periodontal tissues and their counterparts around endosseous implants. Clin. Oral Implants Res. 1991, 2, 1–19. [Google Scholar] [CrossRef]
- Berglundh, T.; Abrahamsson, I.; Lang, N.P.; Lindhe, J. De novo alveolar bone formation adjacent to endosseous implants. Clin. Oral Implants Res. 2003, 14, 251–262. [Google Scholar] [CrossRef]
- Wang, Y.; Zhang, Y.; Miron, R.J. Health, maintenance, and recovery of soft tissues around implants. Clin. Implant Relat. Res. 2016, 18, 618–634. [Google Scholar] [CrossRef]
- LAURENS, N.; KOOLWIJK, P.; DE MAAT, M.P.M. Fibrin structure and wound healing. J. Thromb. Haemost. 2006, 4, 932–939. [Google Scholar] [CrossRef]
- Burkhardt, M.A.; Gerber, I.; Moshfegh, C.; Lucas, M.S.; Waser, J.; Emmert, M.Y.; Hoerstrup, S.P.; Schlottig, F.; Vogel, V. Clot-entrapped blood cells in synergy with human mesenchymal stem cells create a pro-angiogenic healing response. Biomater. Sci. 2017, 5, 2009–2023. [Google Scholar] [CrossRef]
- Oryan, A.; Alidadi, S.; Moshiri, A. Current concerns regarding healing of bone defects. Hard Tissue 2013, 2, 13. [Google Scholar] [CrossRef]
- Chen, Z.; Klein, T.; Murray, R.Z.; Crawford, R.; Chang, J.; Wu, C.; Xiao, Y. Osteoimmunomodulation for the development of advanced bone biomaterials. Mater. Today 2016, 19, 304–321. [Google Scholar] [CrossRef]
- Miron, R.J.; Zohdi, H.; Fujioka-Kobayashi, M.; Bosshardt, D.D. Giant cells around bone biomaterials: Osteoclasts or multi-nucleated giant cells? Acta Biomater. 2016, 46, 15–28. [Google Scholar] [CrossRef]
- Miron, R.J.; Bosshardt, D.D. OsteoMacs: Key players around bone biomaterials. Biomaterials 2016, 82, 1–19. [Google Scholar] [CrossRef]
- Kan, L.; Liu, Y.; McGuire, T.L.; Berger, D.M.P.; Awatramani, R.B.; Dymecki, S.M.; Kessler, J.A. Dysregulation of local stem/progenitor cells as a common cellular mechanism for heterotopic ossification. Stem Cells 2009, 27, 150–156. [Google Scholar] [CrossRef]
- Alexander, K.A.; Chang, M.K.; Maylin, E.R.; Kohler, T.; Müller, R.; Wu, A.C.; Van Rooijen, N.; Sweet, M.J.; Hume, D.A.; Raggatt, L.J.; et al. Osteal macrophages promote in vivo intramembranous bone healing in a mouse tibial injury model. J. Bone Miner. Res. 2011, 26, 1517–1532. [Google Scholar] [CrossRef]
- Zhang, Y.; Zhang, M.; Zhong, M.; Suo, Q.; Lv, K. Expression profiles of miRNAs in polarized macrophages. Int. J. Mol. Med. 2013, 31, 797–802. [Google Scholar] [CrossRef]
- Mantovani, A.; Sica, A.; Locati, M. New vistas on macrophage differentiation and activation. Eur. J. Immunol. 2007, 37, 14–16. [Google Scholar] [CrossRef]
- Gordon, S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3, 23–35. [Google Scholar] [CrossRef]
- Gordon, S.; Taylor, P.R. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 2005, 5, 953–964. [Google Scholar] [CrossRef]
- Zhang, Y.; Böse, T.; Unger, R.E.; Jansen, J.A.; Kirkpatrick, C.J.; van den Beucken, J.J.J.P. Macrophage type modulates osteogenic differentiation of adipose tissue MSCs. Cell Tissue Res. 2017, 369, 273–286. [Google Scholar] [CrossRef]
- Bussolino, F.; Mantovani, A.; Persico, G. Molecular mechanisms of blood vessel formation. Trends Biochem. Sci. 1997, 22, 251–256. [Google Scholar] [CrossRef]
- Przybylski, M. A review of the current research on the role of bFGF and VEGF in angiogenesis. J. Wound Care 2009, 18, 516–519. [Google Scholar] [CrossRef]
- Folkman, J.; Klagsbrun, M. Angiogenic factors. Science 1987, 235, 442. [Google Scholar] [CrossRef]
- Hankenson, K.D.; Dishowitz, M.; Gray, C.; Schenker, M.J.I. Angiogenesis in bone regeneration. Injury 2011, 42, 556–561. [Google Scholar] [CrossRef]
- Wang, Y.; Wan, C.; Deng, L.; Liu, X.; Cao, X.; Gilbert, S.R.; Bouxsein, M.L.; Faugere, M.-C.; Guldberg, R.E.; Gerstenfeld, L.C.; et al. The hypoxia-inducible factor α pathway couples angiogenesis to osteogenesis during skeletal development. J. Clin. Investig. 2007, 117, 1616–1626. [Google Scholar] [CrossRef]
- Marco, F.; Milena, F.; Gianluca, G.; Vittoria, O. Peri-implant osteogenesis in health and osteoporosis. Micron 2005, 36, 630–644. [Google Scholar] [CrossRef]
- Keith, A. Concerning the origin and nature of osteoblasts. Proc. R. Soc. Med. 1927, 21, 301–308. [Google Scholar] [CrossRef]
- Jensen, E.D.; Gopalakrishnan, R.; Westendorf, J.J. Regulation of gene expression in osteoblasts. Biofactors 2010, 36, 25–32. [Google Scholar] [CrossRef]
- Papachroni, K.K.; Karatzas, D.N.; Papavassiliou, K.A.; Basdra, E.K.; Papavassiliou, A.G. Mechanotransduction in osteoblast regulation and bone disease. Trends Mol. Med. 2009, 15, 208–216. [Google Scholar] [CrossRef]
- Santavirta, S.; Konttinen, Y.T.; Nordström, D.; Mäkelä, A.; Sorsa, T.; Hukkanen, M.; Rokkanen, P. Immunologic studies of nonunited fractures. Acta Orthop. Scand. 1992, 63, 579–586. [Google Scholar] [CrossRef]
- Perkins, R.; Skirving, A.P. Callus formation and the rate of healing of femoral fractures in patients with head injuries. J. Bone Jt. Surg. 1987, 69, 521–524. [Google Scholar] [CrossRef]
- Lin, P.P.; Henderson, R.C. Bone mineralization in the affected extremities of children with spastic hemiplegia. Dev. Med. Child. Neurol. 1996, 38, 782–786. [Google Scholar] [CrossRef]
- Offley, S.C.; Guo, T.-Z.; Wei, T.; Clark, J.D.; Vogel, H.; Lindsey, D.P.; Jacobs, C.R.; Yao, W.; Lane, N.E.; Kingery, W.S. Capsaicin-sensitive sensory neurons contribute to the maintenance of trabecular bone integrity. J. Bone Miner. Res. 2005, 20, 257–267. [Google Scholar] [CrossRef]
- Su, Y.-W.; Chung, R.; Ruan, C.-S.; Chim, S.M.; Kuek, V.; Dwivedi, P.P.; Hassanshahi, M.; Chen, K.-M.; Xie, Y.; Chen, L.; et al. Neurotrophin-3 induces BMP-2 and VEGF activities and promotes the bony repair of injured growth plate cartilage and bone in rats. J. Bone Miner. Res. 2016, 31, 1258–1274. [Google Scholar] [CrossRef]
- Skaper, S.D. The neurotrophin family of neurotrophic factors: An overview. Methods Mol. Biol. 2012, 846, 1–12. [Google Scholar]
- Loeb, D.; Greene, L. Transfection with trk restores “slow” NGF binding, efficient NGF uptake, and multiple NGF responses to NGF-nonresponsive PC12 cell mutants. J. Neurosci. 1993, 13, 2919–2929. [Google Scholar] [CrossRef]
- Kaplan, D.R.; Miller, F.D. Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 2000, 10, 381–391. [Google Scholar] [CrossRef]
- Patapoutian, A.; Reichardt, L.F. Trk receptors: Mediators of neurotrophin action. Curr. Opin. Neurobiol. 2001, 11, 272–280. [Google Scholar] [CrossRef]
- Zaccaro, M.C.; Ivanisevic, L.; Perez, P.; Meakin, S.O.; Saragovi, H.U. p75 co-receptors regulate ligand-dependent and ligand-independent Trk receptor activation, in part by altering Trk docking subdomains. J. Biol. Chem. 2001, 276, 31023–31029. [Google Scholar] [CrossRef]
- Esposito, D.; Patel, P.; Stephens, R.M.; Perez, P.; Chao, M.V.; Kaplan, D.R.; Hempstead, B.L. The cytoplasmic and transmembrane domains of the p75 and Trk A receptors regulate high affinity binding to nerve growth factor. J. Biol. Chem. 2001, 276, 32687–32695. [Google Scholar] [CrossRef] [PubMed]
- Frade, M.J.; Rodríguez-Tébar, A.; Barde, Y.-A. Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature 1996, 383, 166–168. [Google Scholar] [CrossRef] [PubMed]
- Khursigara, G.; Bertin, J.; Yano, H.; Moffett, H.; DiStefano, P.S.; Chao, M.V. A prosurvival function for the p75 receptor death domain mediated via the caspase recruitment domain receptor-interacting protein 2. J. Neurosci. 2001, 21, 5854. [Google Scholar] [CrossRef] [PubMed]
- Casademunt, E.; Carter, B.D.; Benzel, I.; Frade, J.M.; Dechant, G.; Barde, Y.-A. The zinc finger protein NRIF interacts with the neurotrophin receptor p75NTR and participates in programmed cell death. EMBO J. 1999, 18, 6050–6061. [Google Scholar] [CrossRef]
- Carter Bruce, D.; Kaltschmidt, C.; Kaltschmidt, B.; Offenhäuser, N.; Böhm-Matthaei, R.; Baeuerle Patrick, A.; Barde, Y.-A. Selective activation of NF-κB by nerve growth factor through the neurotrophin receptor p75. Science 1996, 272, 542–545. [Google Scholar] [CrossRef]
- Friedman, W.J. Neurotrophins induce death of hippocampal neurons via the p75 receptor. J. Neurosci. 2000, 20, 6340. [Google Scholar] [CrossRef]
- Troy, C.M.; Friedman, J.E.; Friedman, W.J. Mechanisms of p75-mediated death of hippocampal neurons: Role of caspases. J. Biol. Chem. 2002, 277, 34295–34302. [Google Scholar] [CrossRef]
- Hamburger, V.; Levi-Montalcini, R. Proliferation, differentiation and degeneration in the spinal ganglia of the chick embryo under normal and experimental conditions. J. Exp. Zool. 1949, 111, 457–501. [Google Scholar] [CrossRef]
- Rost, B.; Hanf, G.; Ohnemus, U.; Otto-Knapp, R.; Groneberg, D.A.; Kunkel, G.; Noga, O. Monocytes of allergics and non-allergics produce, store and release the neurotrophins NGF, BDNF and NT-3. Regul. Pept. 2005, 124, 19–25. [Google Scholar] [CrossRef]
- Tomlinson, R.E.; Li, Z.; Li, Z.; Minichiello, L.; Riddle, R.C.; Venkatesan, A.; Clemens, T.L. NGF-TrkA signaling in sensory nerves is required for skeletal adaptation to mechanical loads in mice. Proc. Nat. Acad. Sci. USA 2017, 114, E3632. [Google Scholar] [CrossRef]
- Wang, L.; Zhou, S.; Liu, B.; Lei, D.; Zhao, Y.; Lu, C.; Tan, A. Locally applied nerve growth factor enhances bone consolidation in a rabbit model of mandibular distraction osteogenesis. J. Orthop. Res. 2006, 24, 2238–2245. [Google Scholar] [CrossRef] [PubMed]
- Jin, P.; Yin, F.; Huang, L.; Zheng, L.; Zhao, J.; Zhang, X. Guangxi cobra venom-derived NGF promotes the osteogenic and therapeutic effects of porous BCP ceramic. Exp. Mol. Med. 2017, 49, e312. [Google Scholar] [CrossRef] [PubMed]
- Hemingway, F.; Taylor, R.; Knowles, H.J.; Athanasou, N.A. RANKL-independent human osteoclast formation with APRIL, BAFF, NGF, IGF I and IGF II. Bone 2011, 48, 938–944. [Google Scholar] [CrossRef]
- Asaumi, K.; Nakanishi, T.; Asahara, H.; Inoue, H.; Takigawa, M. Expression of neurotrophins and their receptors (TRK) during fracture healing. Bone 2000, 26, 625–633. [Google Scholar] [CrossRef]
- Zhang, S.; Sun, S.; He, J.; Shen, L. NT-3 promotes osteogenic differentiation of mouse bone marrow mesenchymal stem cells by regulating the Akt pathway. J. Musculoskel. Neuronal 2020, 20, 591–599. [Google Scholar]
- Su, Y.-W.; Chim, S.M.; Zhou, L.; Hassanshahi, M.; Chung, R.; Fan, C.; Song, Y.; Foster, B.K.; Prestidge, C.A.; Peymanfar, Y.; et al. Osteoblast derived-neurotrophin-3 induces cartilage removal proteases and osteoclast-mediated function at injured growth plate in rats. Bone 2018, 116, 232–247. [Google Scholar] [CrossRef]
- Zhang, J.; Wang, L.; Cao, H.; Chen, N.; Yan, B.; Ao, X.; Zhao, H.; Chu, J.; Huang, M.; Zhang, Z. Neurotrophin-3 acts on the endothelial-mesenchymal transition of heterotopic ossification in rats. J. Cell. Mol. Med. 2019, 23, 2595–2609. [Google Scholar] [CrossRef]
- Laurenzi, M.A.; Beccari, T.; Stenke, L.; Sjolinder, M.; Stinchi, S.; Lindgren, J.A. Expression of mRNA encoding neurotrophins and neurotrophin receptors in human granulocytes and bone marrow cells–enhanced neurotrophin-4 expression induced by LTB4. J. Leukocyte Biol. 1998, 64, 228–234. [Google Scholar] [CrossRef]
- Labouyrie, E.; Dubus, P.; Groppi, A.; Mahon, F.X.; Ferrer, J.; Parrens, M.; Reiffers, J.; de Mascarel, A.; Merlio, J.P. Expression of neurotrophins and their receptors in human bone marrow. Am. J. Pathol. 1999, 154, 405–415. [Google Scholar] [CrossRef]
- Nosrat, C.A.; Fried, K.; Lindskog, S.; Olson, L. Cellular expression of neurotrophin mRNAs during tooth development. Cell Tissue Res. 1997, 290, 569–580. [Google Scholar] [CrossRef]
- Mizuno, N.; Shiba, H.; Inui, T.; Takeda, K.; Kajiya, M.; Hasegawa, N.; Kawaguchi, H.; Kurihara, H. Effect of neurotrophin-4/5 on bone/cementum-related protein expressions and DNA synthesis in cultures of human periodontal ligament cells. J. Periodontol. 2008, 79, 2182–2189. [Google Scholar] [CrossRef] [PubMed]
- Xiao, G.; Gopalakrishnan, R.; Jiang, D.; Reith, E.; Benson, M.D.; Franceschi, R.T. Bone morphogenetic proteins, extracellular matrix, and mitogen-activated protein kinase signaling pathways are required for osteoblast-specific gene expression and differentiation in MC3T3-E1 cells. J. Bone Miner. Res. 2002, 17, 101–110. [Google Scholar] [CrossRef] [PubMed]
- Cai, X.; Luo, E.; Yuan, Q. Interaction between schwann cells and osteoblasts in vitro. Int. J. Oral Sci. 2010, 2, 74–81. [Google Scholar] [CrossRef] [PubMed]
- Ida-Yonemochi, H.; Yamada, Y.; Yoshikawa, H.; Seo, K. Locally produced BDNF promotes sclerotic change in alveolar bone after nerve injury. PLoS ONE 2017, 12, e0169201. [Google Scholar]
- Ai, L.-S.; Sun, C.-Y.; Zhang, L.; Zhou, S.-C.; Chu, Z.-B.; Qin, Y.; Wang, Y.-D.; Zeng, W.; Yan, H.; Guo, T.; et al. Inhibition of BDNF in multiple myeloma blocks osteoclastogenesis via down-regulated stroma-derived RANKL expression both in vitro and in vivo. PLoS ONE 2012, 7, e46287. [Google Scholar] [CrossRef]
- Li, H.; Fu, M.; Gao, J.; Fu, J.; Li, T.; Niu, G. Genetic association between bone mineral density and the fracture of distal radius: A case-control study. Medicine 2021, 100, e27116. [Google Scholar] [CrossRef]
- Sun, C.-Y.; Chu, Z.-B.; She, X.-M.; Zhang, L.; Chen, L.; Ai, L.-S.; Hu, Y. Brain-derived neurotrophic factor is a potential osteoclast stimulating factor in multiple myeloma. Int. J. Cancer 2012, 130, 827–836. [Google Scholar] [CrossRef]
- Bennett, D.L.H.; Michael, G.J.; Ramachandran, N.; Munson, J.B.; Averill, S.; Yan, Q.; McMahon, S.B.; Priestley, J.V. A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J. Neurosci. 1998, 18, 3059. [Google Scholar] [CrossRef]
- Gale, Z.; Cooper, P.R.; Scheven, B.A. Glial cell line-derived neurotrophic factor influences proliferation of osteoblastic cells. Cytokine 2012, 57, 276–281. [Google Scholar] [CrossRef]
- Yi, S.; Kim, J.; Lee, S.Y. GDNF secreted by pre-osteoclasts induces migration of bone marrow mesenchymal stem cells and stimulates osteogenesis. BMB Rep. 2020, 53, 646–651. [Google Scholar] [CrossRef]
- Luukko, K.; Suvanto, P.; Saarma, M.; Thesleff, I. Expression of GDNF and its receptors in developing tooth is developmentally regulated and suggests multiple roles in innervation and organogenesis. Dev. Dynam. 1997, 210, 463–471. [Google Scholar] [CrossRef]
- Nencini, S.; Ringuet, M.; Kim, D.-H.; Greenhill, C.; Ivanusic, J.J. GDNF, neurturin, and artemin activate and sensitize bone afferent neurons and contribute to inflammatory bone pain. J. Neurosci. 2018, 38, 4899–4911. [Google Scholar] [CrossRef] [PubMed]
- Fredriksson, L.; Li, H.; Eriksson, U. The PDGF family: Four gene products form five dimeric isoforms. Cytokine Growth Factor Rev. 2004, 15, 197–204. [Google Scholar] [CrossRef] [PubMed]
- Heldin, C.H.; Bäckström, G.; Ostman, A.; Hammacher, A.; Rönnstrand, L.; Rubin, K.; Nistér, M.; Westermark, B. Binding of different dimeric forms of PDGF to human fibroblasts: Evidence for two separate receptor types. EMBO J. 1988, 7, 1387–1393. [Google Scholar] [CrossRef] [PubMed]
- Hollinger, J.O.; Hart, C.E.; Hirsch, S.N.; Lynch, S.; Friedlaender, G.E. Recombinant human platelet-derived growth factor: Biology and clinical applications. J. Bone Jt. Surg. 2008, 90 (Suppl. 1), 48–54. [Google Scholar] [CrossRef]
- Barnes, G.L.; Kostenuik, P.J.; Gerstenfeld, L.C.; Einhorn, T.A. Growth factor regulation of fracture repair. Exp. Biol. Med. 1999, 14, 1805–1815. [Google Scholar] [CrossRef]
- Jingushi, S.; Heydemann, A.; Kana, S.K.; Macey, L.R.; Bolander, M.E. Acidic fibroblast growth factor (aFGF) injection stimulates cartilage enlargement and inhibits cartilage gene expression in rat fracture healing. J. Orthop. Res. 1990, 8, 364–371. [Google Scholar] [CrossRef]
- Nagai, H.; Tsukuda, R.; Mayahara, H. Effects of basic fibroblast growth factor (bFGF) on bone formation in growing rats. Bone 1995, 16, 367–373. [Google Scholar] [CrossRef]
- Frenkel, S.R.; Guerra, L.A.; Mitchell, O.G.; Singh, I.J. Nerve growth factor in skeletal tissues of the embryonic chick. Cell Tissue Res. 1990, 260, 507–511. [Google Scholar] [CrossRef]
- Grills, B.L.; Schuijers, J.A. Immunohistochemical localization of nerve growth factor in fractured and unfractured rat bone. Acta Orthop. Scand. 1998, 69, 415–419. [Google Scholar] [CrossRef]
- Halvorson, K.G.; Kubota, K.; Sevcik, M.A.; Lindsay, T.H.; Sotillo, J.E.; Ghilardi, J.R.; Rosol, T.J.; Boustany, L.; Shelton, D.L.; Mantyh, P.W. A blocking antibody to nerve growth factor attenuates skeletal pain induced by prostate tumor cells growing in bone. Cancer Res. 2005, 65, 9426–9435. [Google Scholar] [CrossRef] [PubMed]
- Su, Y.-W.; Zhou, X.-F.; Foster, B.K.; Grills, B.L.; Xu, J.; Xian, C.J. Roles of neurotrophins in skeletal tissue formation and healing. J. Cell. Physiol. 2018, 233, 2133–2145. [Google Scholar] [CrossRef] [PubMed]
- Barde, Y.A.; Edgar, D.; Thoenen, H. Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1982, 1, 549–553. [Google Scholar] [CrossRef] [PubMed]
- Feng, X.; Lin, T.; Liu, X.; Yang, C.; Yang, S.; Fu, D. Long non-coding RNA BDNF-AS modulates osteogenic differentiation of bone marrow-derived mesenchymal stem cells. Mol. Cell. Biochem. 2018, 445, 59–65. [Google Scholar] [CrossRef]
- Lin Leu-Fen, H.; Doherty Daniel, H.; Lile Jack, D.; Bektesh, S.; Collins, F. GDNF: A glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 1993, 260, 1130–1132. [Google Scholar]
- Kim, S.J.; Kim, S.Y.; Kwon, C.H.; Kim, Y.K. Differential effect of FGF and PDGF on cell proliferation and migration in osteoblastic cells. Growth Factors 2007, 25, 77–86. [Google Scholar] [CrossRef]
- Sanchez-Fernandez, M.A.; Gallois, A.; Riedl, T.; Jurdic, P.; Hoflack, B. Osteoclasts control osteoblast chemotaxis via PDGF-BB/PDGF receptor beta signaling. PLoS ONE 2008, 3, e3537. [Google Scholar] [CrossRef]
- Gao, S.; Zheng, G.; Wang, L.; Liang, Y.; Zhang, S.; Lao, X.; Li, K.; Liao, G. Zoledronate suppressed angiogenesis and osteogenesis by inhibiting osteoclasts formation and secretion of PDGF-BB. PLoS ONE 2017, 12, e0179248. [Google Scholar] [CrossRef]
- Sun, S.; Diggins, N.H.; Gunderson, Z.J.; Fehrenbacher, J.C.; White, F.A.; Kacena, M.A. No pain, no gain? The effects of pain-promoting neuropeptides and neurotrophins on fracture healing. Bone 2020, 131, 115109. [Google Scholar] [CrossRef]
- Bjurholm, A. Neuroendocrine peptides in bone. Int. Orthop. 1991, 15, 325–329. [Google Scholar] [CrossRef]
- Schou, W.S.; Ashina, S.; Amin, F.M.; Goadsby, P.J.; Ashina, M. Calcitonin gene-related peptide and pain: A systematic review. J. Headache Pain 2017, 18, 34. [Google Scholar] [CrossRef] [PubMed]
- Saito, T.; Koshino, T. Distribution of neuropeptides in synovium of the knee with osteoarthritis. Clin. Orthop Relat. Res. 2000, 376, 172–182. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Shi, X.; Zhao, R.; Halloran, B.P.; Clark, D.J.; Jacobs, C.R.; Kingery, W.S. Calcitonin-gene-related peptide stimulates stromal cell osteogenic differentiation and inhibits RANKL induced NF-κB activation, osteoclastogenesis and bone resorption. Bone 2010, 46, 1369–1379. [Google Scholar] [CrossRef]
- Boyce, B.F.; Xing, L. Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch. Biochem. Biophys. 2008, 473, 139–146. [Google Scholar] [CrossRef] [PubMed]
- Huang, C.; Yang, X.; Liu, D.; Sun, Y.; Dai, X. Calcitonin gene-related peptide-induced calcium alginate gel combined with adipose-derived stem cells differentiating to osteoblasts. Cell Biochem. Biophys. 2015, 73, 609–617. [Google Scholar] [CrossRef]
- Sisask, G.; Silfverswärd, C.J.; Bjurholm, A.; Nilsson, O. Ontogeny of sensory and autonomic nerves in the developing mouse skeleton. Auton. Neurosci. 2013, 177, 237–243. [Google Scholar] [CrossRef]
- Bidegain, M.; Roos, B.A.; Hill, E.L.; Howard, G.A.; Balkan, W. Calcitonin gene-related peptide (CGRP) in the developing mouse limb. Endocr. Res. 1995, 21, 743–755. [Google Scholar] [CrossRef]
- Li, J.; Kreicbergs, A.; Bergström, J.; Stark, A.; Ahmed, M. Site-specific CGRP innervation coincides with bone formation during fracture healing and modeling: A study in rat angulated tibia. J. Orthop. Res. 2007, 25, 1204–1212. [Google Scholar] [CrossRef]
- Hukkanen, M.; Konttinen, Y.T.; Santavirta, S.; Paavolainen, P.; Gu, X.H.; Terenghi, G.; Polak, J.M. Rapid proliferation of calcitonin gene-related peptide-immunoreactive nerves during healing of rat tibial fracture suggests neural involvement in bone growth and remodelling. Neuroscience 1993, 54, 969–979. [Google Scholar] [CrossRef]
- Li, Y.; Tan, Y.; Zhang, G.; Yang, B.; Zhang, J. Effects of calcitonin gene-related peptide on the expression and activity of nitric oxide synthase during mandibular bone healing in rabbits: An experimental study. J. Oral Maxil. Surg. 2009, 67, 273–279. [Google Scholar] [CrossRef]
- Diwan, A.D.; Wang, M.X.; Jang, D.; Zhu, W.; Murrell, G.A.C. Nitric oxide modulates fracture healing. J. Bone Miner. Res. 2000, 15, 342–351. [Google Scholar] [CrossRef] [PubMed]
- Tang, P.; Duan, C.; Wang, Z.; Wang, C.; Meng, G.; Lin, K.; Yang, Q.; Yuan, Z. NPY and CGRP inhibitor influence on ERK pathway and macrophage aggregation during fracture healing. Cell. Physiol. Biochem. 2017, 41, 1457–1467. [Google Scholar] [CrossRef] [PubMed]
- Bo, Y.; Yan, L.; Gang, Z.; Tao, L.; Yinghui, T. Effect of calcitonin gene-related peptide on osteoblast differentiation in an osteoblast and endothelial cell co-culture system. Cell Biol. Int. 2012, 36, 909–915. [Google Scholar] [CrossRef] [PubMed]
- Aoki, M.; Tamai, K.; Saotome, K. Substance P- and calcitonin gene-related peptide-immunofluorescent nerves in the repair of experimental bone defects. Int. Orthop. 1994, 18, 317–324. [Google Scholar] [CrossRef] [PubMed]
- Kingery, W.S.; Offley, S.C.; Guo, T.-Z.; Davies, M.F.; Clark, J.D.; Jacobs, C.R. A substance P receptor (NK1) antagonist enhances the widespread osteoporotic effects of sciatic nerve section. Bone 2003, 33, 927–936. [Google Scholar] [CrossRef] [PubMed]
- Mori, T.; Ogata, T.; Okumura, H.; Shibata, T.; Nakamura, Y.; Kataoka, K. Substance P regulates the function of rabbit cultured osteoclast; increase of intracellular free calcium concentration and enhancement of bone resorption. Biochem. Biophys. Res. Commun. 1999, 262, 418–422. [Google Scholar] [CrossRef]
- Matayoshi, T.; Goto, T.; Fukuhara, E.; Takano, H.; Kobayashi, S.; Takahashi, T. Neuropeptide substance P stimulates the formation of osteoclasts via synovial fibroblastic cells. Biochem. Biophys. Res. Commun. 2005, 327, 756–764. [Google Scholar] [CrossRef]
- Kojima, T.; Yamaguchi, M.; Kasai, K. Substance P stimulates release of RANKL via COX-2 expression in human dental pulp cells. Inflamm. Res. 2006, 55, 78–84. [Google Scholar] [CrossRef]
- Shi, L.; Liu, Y.; Yang, Z.; Wu, T.; Lo, H.T.; Xu, J.; Zhang, J.; Lin, W.; Zhang, J.; Feng, L.; et al. Vasoactive intestinal peptide promotes fracture healing in sympathectomized mice. Calcified Tissue Int. 2021, 109, 55–65. [Google Scholar] [CrossRef]
- Hohmann, E.L.; Levine, L.; Tashjian, A.H., Jr. Vasoactive intestinal peptide stimulates bone resorption via a cyclic adenosine 3′,5′-monophosphate-dependent mechanism. Endocrinology 1983, 112, 1233–1239. [Google Scholar] [CrossRef]
- Lerner, U.H.; Lundberg, P.; Ransjö, M.; Persson, P.; Håkanson, R. Helodermin, helospectin, and PACAP stimulate cyclic AMP formation in intact bone, isolated osteoblasts, and osteoblastic cell lines. Calcified Tissue Int. 1994, 54, 284–289. [Google Scholar] [CrossRef] [PubMed]
- Ransjö, M.; Lie, A.; Mukohyama, H.; Lundberg, P.; Lerner, U.H. Microisolated mouse osteoclasts express VIP-1 and PACAP receptors. Biochem. Biophys. Res. Commun. 2000, 274, 400–404. [Google Scholar] [CrossRef] [PubMed]
- Giunta, S.; Castorina, A.; Marzagalli, R.; Szychlinska, M.A.; Pichler, K.; Mobasheri, A.; Musumeci, G. Ameliorative effects of PACAP against cartilage degeneration. Morphological, immunohistochemical and biochemical evidence from in vivo and in vitro models of rat osteoarthritis. Int. J. Mol. Sci. 2015, 16, 5922–5944. [Google Scholar] [CrossRef] [PubMed]
- Teixeira, L.; Sousa, D.M.; Nunes, A.F.; Sousa, M.M.; Herzog, H.; Lamghari, M. NPY revealed as a critical modulator of osteoblast function in vitro: New insights into the role of Y1 and Y2 receptors. J. Cell. Biochem. 2009, 107, 908–916. [Google Scholar] [CrossRef]
- Amano, S.; Arai, M.; Goto, S.; Togari, A. Inhibitory effect of NPY on isoprenaline-induced osteoclastogenesis in mouse bone marrow cells. BBA-Gen. Subj. 2007, 1770, 966–973. [Google Scholar] [CrossRef] [PubMed]
- Ducy, P.; Amling, M.; Takeda, S.; Priemel, M.; Schilling, A.F.; Beil, F.T.; Shen, J.; Vinson, C.; Rueger, J.M.; Karsenty, G. Leptin inhibits bone formation through a hypothalamic relay: A central control of bone mass. Cell 2000, 100, 197–207. [Google Scholar] [CrossRef]
- Ahmed, M.; Srinivasan, G.R.; Theodorsson, E.; Bjurholm, A.; Kreicbergs, A. Extraction and quantitation of neuropeptides in bone by radioimmunoassay. Regul. Pept. 1994, 51, 179–188. [Google Scholar] [CrossRef]
- Li, J.; Ahmad, T.; Spetea, M.; Ahmed, M.; Kreicbergs, A. Bone reinnervation after fracture: A study in the rat. J. Bone Miner. Res. 2001, 16, 1505–1510. [Google Scholar] [CrossRef]
- Liu, D.; Jiang, L.-S.; Dai, L.-Y. Substance P and its receptors in bone metabolism. Neuropeptides 2007, 41, 271–283. [Google Scholar] [CrossRef]
- v. Euler, U.S.; Gaddum, J.H. An unidentified depressor substance in certain tissue extracts. J. Physiol. 1931, 72, 74–87. [Google Scholar] [CrossRef]
- Konttinen, Y.T.; Imai, S.; Suda, A. Neuropeptides and the puzzle of bone remodeling: State of the art. Acta Orthop. Scand. 1996, 67, 632–639. [Google Scholar] [CrossRef] [PubMed]
- Bjurholm, A.; Kreicbergs, A.; Terenius, L.; Goldstein, M.; Schultzberg, M. Neuropeptide Y-, tyrosine hydroxylase- and vasoactive intestinal polypeptide-immunoreactive nerves in bone and surrounding tissues. J. Autonom. Nerv. Syst. 1988, 25, 119–125. [Google Scholar] [CrossRef]
- Schulz, S.; Röcken, C.; Mawrin, C.; Weise, W.; Höllt, V.; Schulz, S. Immunocytochemical identification of VPAC1, VPAC2, and PAC1 receptors in normal and neoplastic human tissues with subtype-specific antibodies. Clin. Cancer Res. 2004, 10, 8235. [Google Scholar]
- Gourlet, P.; Vandermeers, A.; Vertongen, P.; Rathe, J.; de Neef, P.; Cnudde, J.; Waelbroeck, M.; Robberecht, P. Development of high affinity selective VIP1 receptor agonists. Peptides 1997, 18, 1539–1545. [Google Scholar] [CrossRef]
- Tatemoto, K.; Carlquist, M.; Mutt, V. Neuropeptide Y—a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 1982, 296, 659–660. [Google Scholar] [CrossRef]
- Lee, N.J.; Herzog, H. NPY regulation of bone remodelling. Neuropeptides 2009, 43, 457–463. [Google Scholar] [CrossRef]
- Nunes, A.F.; Liz, M.A.; Franquinho, F.; Teixeira, L.; Sousa, V.; Chenu, C.; Lamghari, M.; Sousa, M.M. Neuropeptide Y expression and function during osteoblast differentiation—Insights from transthyretin knockout mice. FEBS J. 2010, 277, 263–275. [Google Scholar] [CrossRef]
- Jessen, K.R.; Mirsky, R. Signals that determine Schwann cell identity. J. Anat. 2002, 200, 367–376. [Google Scholar] [CrossRef]
- Zhu, H.; Yang, A.; Du, J.; Li, D.; Liu, M.; Ding, F.; Gu, X.; Liu, Y. Basic fibroblast growth factor is a key factor that induces bone marrow mesenchymal stem cells towards cells with Schwann cell phenotype. Neurosci. Lett. 2014, 559, 82–87. [Google Scholar] [CrossRef]
- Jones, R.E.; Salhotra, A.; Robertson, K.S.; Ransom, R.C.; Foster, D.S.; Shah, H.N.; Quarto, N.; Wan, D.C.; Longaker, M.T. Skeletal stem cell-Schwann cell circuitry in mandibular repair. Cell Rep. 2019, 28, 2757–2766.e5. [Google Scholar] [CrossRef]
- Xie, M.; Kamenev, D.; Kaucka, M.; Kastriti, M.E.; Zhou, B.; Artemov, A.V.; Storer, M.; Fried, K.; Adameyko, I.; Dyachuk, V.; et al. Schwann cell precursors contribute to skeletal formation during embryonic development in mice and zebrafish. Proc. Nat. Acad. Sci. USA 2019, 116, 15068–15073. [Google Scholar] [CrossRef] [PubMed]
- Carr, M.J.; Johnston, A.P.W. Schwann cells as drivers of tissue repair and regeneration. Curr. Opin. Neurobiol. 2017, 47, 52–57. [Google Scholar] [CrossRef] [PubMed]
- Itoyama, T.; Yoshida, S.; Tomokiyo, A.; Hasegawa, D.; Hamano, S.; Sugii, H.; Ono, T.; Fujino, S.; Maeda, H. Possible function of GDNF and Schwann cells in wound healing of periodontal tissue. J. Periodont. Res. 2020, 55, 830–839. [Google Scholar] [CrossRef]
- Johnston, A.P.W.; Yuzwa, S.A.; Carr, M.J.; Mahmud, N.; Storer, M.A.; Krause, M.P.; Jones, K.; Paul, S.; Kaplan, D.R.; Miller, F.D. Dedifferentiated Schwann cell precursors secreting paracrine factors are required for regeneration of the mammalian digit tip. Cell Stem Cell 2016, 19, 433–448. [Google Scholar] [CrossRef] [PubMed]
- Caplan, A.I.; Correa, D. PDGF in bone formation and regeneration: New insights into a novel mechanism involving MSCs. J. Orthop. Res. 2011, 29, 1795–1803. [Google Scholar] [CrossRef]
- Rydziel, S.; Shaikh, S.; Canalis, E. Platelet-derived growth factor-AA and -BB (PDGF-AA and -BB) enhance the synthesis of PDGF-AA in bone cell cultures. Endocrinology 1994, 134, 2541–2546. [Google Scholar] [CrossRef] [PubMed]
- Yu, H.; Pei, T.; Ren, J.; Ding, Y.; Wu, A.; Zhou, Y. Semaphorin 3A enhances osteogenesis of MG63 cells through interaction with Schwann cells in vitro. Mol. Med. Rep. 2018, 17, 6084–6092. [Google Scholar] [PubMed]
- Cao, J.; Zhang, S.; Gupta, A.; Du, Z.; Lei, D.; Wang, L.; Wang, X. Sensory nerves affect bone regeneration in rabbit mandibular distraction osteogenesis. Int. J. Med. Sci. 2019, 16, 831–837. [Google Scholar] [CrossRef]
- Zhang, Z.-K.; Guo, X.; Lao, J.; Qin, Y.-X. Effect of capsaicin-sensitive sensory neurons on bone architecture and mechanical properties in the rat hindlimb suspension model. J. Orthop. Transl. 2017, 10, 12–17. [Google Scholar] [CrossRef]
- Fukuda, T.; Takeda, S.; Xu, R.; Ochi, H.; Sunamura, S.; Sato, T.; Shibata, S.; Yoshida, Y.; Gu, Z.; Kimura, A.; et al. Sema3A regulates bone-mass accrual through sensory innervations. Nature 2013, 497, 490–493. [Google Scholar] [CrossRef]
- Zhu, J.; Zhen, G.; An, S.; Wang, X.; Wan, M.; Li, Y.; Chen, Z.; Guan, Y.; Dong, X.; Hu, Y.; et al. Aberrant subchondral osteoblastic metabolism modifies NaV1.8 for osteoarthritis. eLife 2020, 9, e57656. [Google Scholar] [CrossRef] [PubMed]
- Yoneda, T.; Hiasa, M.; Okui, T. Crosstalk between sensory nerves and cancer in bone. Curr. Osteoporos. Rep. 2018, 16, 648–656. [Google Scholar] [CrossRef] [PubMed]
- Nencini, S.; Ivanusic, J.J. The physiology of bone pain. How much do we really know? Front. Physiol. 2016, 7, 157. [Google Scholar] [CrossRef]
- Brjussowa, S.S.; Lebedenko, W.W. Zur Schmerzleitungsfähigkeit der Gefäße. Z. Gesa. Exp. Med. 1930, 69, 29–40. [Google Scholar] [CrossRef]
- Albrektsson, T.; Dahlin, C.; Jemt, T.; Sennerby, L.; Turri, A.; Wennerberg, A. Is marginal bone loss around oral implants the result of a provoked foreign body reaction? Clin. Implant Dent. 2014, 16, 155–165. [Google Scholar] [CrossRef]
- Ehrhard, P.B.; Ganter, U.; Stalder, A.; Bauer, J.; Otten, U. Expression of functional trk protooncogene in human monocytes. Proc. Nat. Acad. Sci. USA 1993, 90, 5423. [Google Scholar] [CrossRef]
- Horigome, K.; Pryor, J.C.; Bullock, E.D.; Johnson, E.M., Jr. Mediator release from mast cells by nerve growth factor. Neurotrophin specificity and receptor mediation. J. Biol. Chem. 1993, 268, 14881–14887. [Google Scholar] [CrossRef]
- Ehrhard, P.B.; Erb, P.; Graumann, U.; Otten, U. Expression of nerve growth factor and nerve growth factor receptor tyrosine kinase Trk in activated CD4-positive T-cell clones. Proc. Nat. Acad. Sci. USA 1993, 90, 10984. [Google Scholar] [CrossRef]
- Tsuda, T.; Wong, D.; Dolovich, J.; Bienenstock, J.; Marshall, J.; Denburg, J. Synergistic effects of nerve growth factor and granulocyte-macrophage colony-stimulating factor on human basophilic cell differentiation. Blood 1991, 77, 971–979. [Google Scholar] [CrossRef]
- Shinoda, M.; Hoffer, B.J.; Olson, L. Interactions of neurotrophic factors GDNF and NT-3, but not BDNF, with the immune system following fetal spinal cord transplantation. Brain Res. 1996, 722, 153–167. [Google Scholar] [CrossRef]
- Rossetti, A.C.; Paladini, M.S.; Trepci, A.; Mallien, A.; Riva, M.A.; Gass, P.; Molteni, R. Differential neuroinflammatory response in male and female mice: A role for BDNF. Front. Mol. Neurosci. 2019, 12, 166. [Google Scholar] [CrossRef] [PubMed]
- Sandrini, L.; Castiglioni, L.; Amadio, P.; Werba, J.P.; Eligini, S.; Fiorelli, S.; Zarà, M.; Castiglioni, S.; Bellosta, S.; Lee, F.S.; et al. Impact of BDNF val66Met polymorphism on myocardial infarction: Exploring the macrophage phenotype. Cells 2020, 9, 1084. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Wang, N.; Khoso, M.H.; Shen, C.; Guo, M.; Pang, X.; Li, D.; Wang, W. FGF-21 elevated IL-10 production to correct LPS-induced inflammation. Inflammation 2018, 41, 751–759. [Google Scholar] [CrossRef] [PubMed]
- Wang, N.; Li, J.-Y.; Zhao, T.; Li, S.; Shen, C.-B.; Li, D.-S.; Wang, W.-F. FGF-21 plays a crucial role in the glucose uptake of activated monocytes. Inflammation 2018, 41, 73–80. [Google Scholar] [CrossRef]
- Holzmann, B. Antiinflammatory activities of CGRP modulating innate immune responses in health and disease. Curr. Protein Pept. Sci. 2013, 14, 268–274. [Google Scholar] [CrossRef]
- Tran, M.T.; Lausch, R.N.; Oakes, J.E. Substance P differentially stimulates IL-8 synthesis in human corneal epithelial cells. Investig. Ophthalmol. Vis. Sci. 2000, 41, 3871–3877. [Google Scholar]
- Koon, H.-W.; Zhao, D.; Zhan, Y.; Simeonidis, S.; Moyer, M.P.; Pothoulakis, C. Substance P-stimulated interleukin-8 expression in human colonic epithelial cells involves protein kinase Cδ activation. J. Pharmacol. Exp. Ther. 2005, 314, 1393. [Google Scholar] [CrossRef]
- Serra, M.C.; Calzetti, F.; Ceska, M.; Cassatella, M.A. Effect of substance P on superoxide anion and IL-8 production by human PMNL. Immunology 1994, 82, 63–69. [Google Scholar]
- Okayama, Y.; Ono, Y.; Nakazawa, T.; Church, M.K.; Mori, M. Human skin mast cells produce TNF-α by substance P. Int. Arch. Allergy Immunol. 1998, 117 (Suppl. 1), 48–51. [Google Scholar] [CrossRef]
- Calvo, C.F.; Chavanel, G.; Senik, A. Substance P enhances IL-2 expression in activated human T cells. J. Immunol. 1992, 148, 3498. [Google Scholar]
- Rameshwar, P.; Zhu, G.; Donnelly, R.J.; Qian, J.; Ge, H.; Goldstein, K.R.; Denny, T.N.; Gascón, P. The dynamics of bone marrow stromal cells in the proliferation of multipotent hematopoietic progenitors by substance P: An understanding of the effects of a neurotransmitter on the differentiating hematopoietic stem cell. J. Neuroimmunol. 2001, 121, 22–31. [Google Scholar] [CrossRef]
- DELGADO, M.; GANEA, D. VIP and PACAP inhibit activation induced apoptosis in T lymphocytes. Ann. N. Y. Acad. Sci. 2000, 921, 55–67. [Google Scholar] [CrossRef] [PubMed]
- Dollé, J.-P.; Rezvan, A.; Allen, F.D.; Lazarovici, P.; Lelkes, P.I. Nerve growth factor-induced migration of endothelial cells. J. Pharmacol. Exp. Ther. 2005, 315, 1220. [Google Scholar] [CrossRef] [PubMed]
- Rahbek, U.L.; Dissing, S.; Thomassen, C.; Hansen, A.J.; Tritsaris, K. Nerve growth factor activates aorta endothelial cells causing PI3K/Akt- and ERK-dependent migration. Pfluegers Arch. 2005, 450, 355–361. [Google Scholar] [CrossRef]
- Seo, K.; Choi, J.; Park, M.; Rhee, C. Angiogenesis effects of nerve growth factor (NGF) on rat corneas. J. Vet. Sci. 2019, 2, 125–130. [Google Scholar] [CrossRef]
- Cantarella, G.; Lempereur, L.; Presta, M.; Ribatti, D.; Lombardo, G.; Lazarovici, P.; Zappalà, G.; Pafumi, C.; Bernardini, R. Nerve growth factor–endothelial cell interaction leads to angiogenesis in vitro and in vivo. FASEB J. 2002, 16, 1307–1309. [Google Scholar] [CrossRef]
- Lazarovici, P.; Gazit, A.; Staniszewska, I.; Marcinkiewicz, C.; Lelkes, P.I. Nerve growth factor (NGF) promotes angiogenesis in the quail chorioallantoic membrane. Endothelium 2006, 13, 51–59. [Google Scholar] [CrossRef]
- Kermani, P.; Rafii, D.; Jin, D.K.; Whitlock, P.; Schaffer, W.; Chiang, A.; Vincent, L.; Friedrich, M.; Shido, K.; Hackett, N.R.; et al. Neurotrophins promote revascularization by local recruitment of TrkB+ endothelial cells and systemic mobilization of hematopoietic progenitors. J. Clin. Investig. 2005, 115, 653–663. [Google Scholar] [CrossRef]
- Liu, Y.; Sun, L.; Huan, Y.; Zhao, H.; Deng, J. Application of bFGF and BDNF to improve angiogenesis and cardiac function. J. Surg. Res. 2006, 136, 85–91. [Google Scholar] [CrossRef]
- Shen, L.; Zeng, W.; Wu, Y.-X.; Hou, C.-L.; Chen, W.; Yang, M.-C.; Li, L.; Zhang, Y.-F.; Zhu, C.-H. Neurotrophin-3 accelerates wound healing in diabetic mice by promoting a paracrine response in mesenchymal stem cells. Cell Transplant. 2013, 22, 1011–1021. [Google Scholar] [CrossRef]
- Cristofaro, B.; Stone, O.A.; Caporali, A.; Dawbarn, D.; Ieronimakis, N.; Reyes, M.; Madeddu, P.; Bates, D.O.; Emanueli, C. Neurotrophin-3 is a novel angiogenic factor capable of therapeutic neovascularization in a mouse model of limb ischemia. Arterioscler. Thromb. Vas. Biol. 2010, 30, 1143–1150. [Google Scholar] [CrossRef] [PubMed]
- Blais, M.; Lévesque, P.; Bellenfant, S.; Berthod, F. Nerve growth factor, brain-derived neurotrophic factor, neurotrophin-3 and glial-derived neurotrophic factor enhance angiogenesis in a tissue-engineered in vitro model. Tissue Eng. Part A 2013, 19, 1655–1664. [Google Scholar] [CrossRef] [PubMed]
- Zhong, Z.; Gu, H.; Peng, J.; Wang, W.; Johnstone, B.H.; March, K.L.; Farlow, M.R.; Du, Y. GDNF secreted from adipose-derived stem cells stimulates VEGF-independent angiogenesis. Oncotarget 2016, 7, 36829–36841. [Google Scholar] [CrossRef] [PubMed]
- Shvartsman, D.; Storrie-White, H.; Lee, K.; Kearney, C.; Brudno, Y.; Ho, N.; Cezar, C.; McCann, C.; Anderson, E.; Koullias, J.; et al. Sustained delivery of VEGF maintains innervation and promotes reperfusion in ischemic skeletal muscles via NGF/GDNF signaling. Mol. Ther. 2014, 22, 1243–1253. [Google Scholar] [CrossRef] [PubMed]
- Cross, M.J.; Claesson-Welsh, L. FGF and VEGF function in angiogenesis: Signalling pathways, biological responses and therapeutic inhibition. Trends. Pharmacol. Sci. 2001, 22, 201–207. [Google Scholar] [CrossRef]
- Wong, C.G.; Rich, K.A.; Liaw, L.-H.; Hsu, H.T.; Berns, M.W. Intravitreal VEGF and bFGF produce florid retinal neovascularization and hemorrhage in the rabbit. Curr. Eye Res. 2001, 22, 140–147. [Google Scholar] [CrossRef]
- Mapp, P.I.; McWilliams, D.F.; Turley, M.J.; Hargin, E.; Walsh, D.A. A role for the sensory neuropeptide calcitonin gene-related peptide in endothelial cell proliferation in vivo. Br. J. Pharmacol. 2012, 166, 1261–1271. [Google Scholar] [CrossRef]
- Buma, P.; Elmans, L.; Oestreicher, A.B. Changes in innervation of long bones after insertion of an implant: Immunocytochemical study in goats with antibodies to calcitonin gene-related peptide and B-50/GAP-43. J. Orthop. Res. 1995, 13, 570–577. [Google Scholar] [CrossRef]
- Ziche, M.; Morbidelli, L.; Masini, E.; Amerini, S.; Granger, H.J.; Maggi, C.A.; Geppetti, P.; Ledda, F. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J. Clin. Investig. 1994, 94, 2036–2044. [Google Scholar] [CrossRef]
- Liu, L.; Dana, R.; Yin, J. Sensory neurons directly promote angiogenesis in response to inflammation via substance P signaling. FASEB J. 2020, 34, 6229–6243. [Google Scholar] [CrossRef]
- Kohara, H.; Tajima, S.; Yamamoto, M.; Tabata, Y. Angiogenesis induced by controlled release of neuropeptide substance P. Biomaterials 2010, 31, 8617–8625. [Google Scholar] [CrossRef] [PubMed]
- Ye, J.; Gong, P. NGF-CS/HA-coating composite titanium facilitates the differentiation of bone marrow mesenchymal stem cells into osteoblast and neural cells. Biochem. Biophys. Res. Commun. 2020, 531, 290–296. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Lei, L.; Yu, T.; Jiang, T.; Kang, Y. Effect of brain-derived neurotrophic factor on the neurogenesis and osteogenesis in bone engineering. Tissue Eng. Part A 2018, 24, 1283–1292. [Google Scholar] [CrossRef] [PubMed]
- Chang, P.C.; Lim, L.P.; Chong, L.Y.; Dovban, A.S.M.; Chien, L.Y.; Chung, M.C.; Lei, C.; Kao, M.J.; Chen, C.H.; Chiang, H.C.; et al. PDGF-simvastatin delivery stimulates osteogenesis in heat-induced osteonecrosis. J. Dent. Res. 2012, 91, 618–624. [Google Scholar] [CrossRef] [PubMed]
- Liu, W.; Guo, S.; Tang, Z.; Wei, X.; Gao, P.; Wang, N.; Li, X.; Guo, Z. Magnesium promotes bone formation and angiogenesis by enhancing MC3T3-E1 secretion of PDGF-BB. Biochem. Biophys. Res. Commun. 2020, 528, 664–670. [Google Scholar] [CrossRef]
- Chang, P.C.; Seol, Y.J.; Cirelli, J.A.; Pellegrini, G.; Jin, Q.; Franco, L.M.; Goldstein, S.A.; Chandler, L.A.; Sosnowski, B.; Giannobile, W.V. PDGF-B gene therapy accelerates bone engineering and oral implant osseointegration. Gene Ther. 2010, 17, 95–104. [Google Scholar] [CrossRef]
- Qu, D.; Li, J.; Li, Y.; Gao, Y.; Zuo, Y.; Hsu, Y.; Hu, J. Angiogenesis and osteogenesis enhanced by bFGF ex vivo gene therapy for bone tissue engineering in reconstruction of calvarial defects. J. Biomed. Mater. Res. A 2011, 96A, 543–551. [Google Scholar] [CrossRef]
- Takechi, M.; Tatehara, S.; Satomura, K.; Fujisawa, K.; Nagayama, M. Effect of FGF-2 and melatonin on implant bone healing: A histomorphometric study. J. Mater. Sci. Mater. Med. 2008, 19, 2949–2952. [Google Scholar] [CrossRef]
- Guo, Y.; Chen, H.; Jiang, Y.; Yuan, Y.; Zhang, Q.; Guo, Q.; Gong, P. CGRP regulates the dysfunction of peri-implant angiogenesis and osseointegration in streptozotocin-induced diabetic rats. Bone 2020, 139, 115464. [Google Scholar] [CrossRef]
- Liu, Y.; Zheng, G.; Liu, L.; Wang, Z.; Wang, Y.; Chen, Q.; Luo, E. Inhibition of osteogenesis surrounding the titanium implant by CGRP deficiency. Connect. Tissue Res. 2018, 59, 147–156. [Google Scholar] [CrossRef]
- Ye, L.; Xu, J.; Mi, J.; He, X.; Pan, Q.; Zheng, L.; Zu, H.; Chen, Z.; Dai, B.; Li, X.; et al. Biodegradable magnesium combined with distraction osteogenesis synergistically stimulates bone tissue regeneration via CGRP-FAK-VEGF signaling axis. Biomaterials 2021, 275, 120984. [Google Scholar]
- Alkhamrah, B.A.; Hoshino, N.; Kawano, Y.; Harada, F.; Hanada, K.; Maeda, T. The periodontal Ruffini endings in brain derived neurotrophic factor (BDNF) deficient mice. Arch. Histol. Cytol. 2003, 66, 73–81. [Google Scholar] [CrossRef] [PubMed]
- Yuan, Q.; Gong, P.; Tan, Z. Schwann cell graft: A method to promote sensory responses of osseointegrated implants. Med. Hypotheses 2007, 69, 800–803. [Google Scholar] [CrossRef] [PubMed]
- Fan, J.; Mu, T.; Qin, J.; Bi, L.; Pei, G. Different effects of implanting sensory nerve or blood vessel on the vascularization, neurotization, and osteogenesis of tissue-engineered bone in vivo. Biomed. Res. Int. 2014, 2014, 412570. [Google Scholar] [CrossRef]
- Ma, Y.-X.; Jiao, K.; Wan, Q.-Q.; Li, J.; Liu, M.-Y.; Zhang, Z.-B.; Qin, W.; Wang, K.-Y.; Wang, Y.-z.; Tay, F.R.; et al. Silicified collagen scaffold induces semaphorin 3A secretion by sensory nerves to improve in-situ bone regeneration. Bioact. Mater. 2022, 9, 475–490. [Google Scholar] [CrossRef]
- Zhou, P.; He, F.; Liu, B.; Wei, S. Nerve electrical stimulation enhances osseointegration of implants in the beagle. Sci. Rep. 2019, 9, 4916. [Google Scholar] [CrossRef]
- Ye, J.; Huang, B.; Gong, P. Nerve growth factor-chondroitin sulfate/hydroxyapatite-coating composite implant induces early osseointegration and nerve regeneration of peri-implant tissues in Beagle dogs. J. Orthop. Surg. Res. 2021, 16, 51. [Google Scholar] [CrossRef]
- Zhang, Y.; Xu, J.; Ruan, Y.C.; Yu, M.K.; O’Laughlin, M.; Wise, H.; Chen, D.; Tian, L.; Shi, D.; Wang, J.; et al. Implant-derived magnesium induces local neuronal production of CGRP to improve bone-fracture healing in rats. Nat. Med. 2016, 22, 1160–1169. [Google Scholar] [CrossRef]
- Kauschke, V.; Schneider, M.; Jauch, A.; Schumacher, M.; Kampschulte, M.; Rohnke, M.; Henss, A.; Bamberg, C.; Trinkaus, K.; Gelinsky, M.; et al. Effects of a pasty bone cement containing brain-derived neurotrophic factor-functionalized mesoporous bioactive glass particles on metaphyseal healing in a new murine osteoporotic fracture model. Int. J. Mol. Sci. 2018, 19, 3531. [Google Scholar] [CrossRef]
Neurotrophin | Receptor | Effect | Ref. |
---|---|---|---|
NGF | TrkA, p75 | Mediating the bone’s response to mechanical loading; enhances bone regeneration via regulation of osteogenesis and bone resorption | [58,59,60,61,62,63] |
NT-3 | TrkC | Improves bone-fracture healing by improving the formulation of osteoblasts and augments osteoclastogenesis and resorption; promote heterotopic ossification formation | [64,65,66,67] |
NT-4/5 | TrkB | Regulates the functions of periodontal ligament cells | [68,69,70,71,72] |
BDNF | TrkB | Regulates new bone formation by inducing osteoblast proliferation and activating osteoclasts | [59,73,74,75,76,77] |
GDNF | RET, GFRα-1, and GFRα-2 | Involved in the pathogenesis of bone pain; regulates bone metabolism; acts as a target-derived neurotrophic factor during tooth innervation | [78,79,80,81,82] |
PDGF | type A PDGF receptor, type B PDGF receptor | Improves reparative osseous activity; promote angiogenesis | [83,84,85,86] |
FGF | FGFR | Improves fracture healing; stimulates bone resorption; promote Angiogenesis | [87,88] |
Neuropeptides | Effect | Ref. |
---|---|---|
CGRP | Transmits pain and sensitization; is involved in fracture healing; promotes bone growth and inhibits bone resorption | [101,102,103,104,105,106,107,108,109,110,111,112,113] |
SP | Collaborates in callus development by increasing local blood flow; affects the metabolism of bones by directly impacting bone cells and affects blood vessels and the generation of other cytokines | [114,115,116,117,118] |
VIP | Aids bone fracture repair by stimulating osteoblastic activity and decreasing osteoclastic activity; improves bone density and mechanical features | [119,120,121,122] |
PACAP | Has anti-inflammatory and chondroprotective properties | [123] |
NPY | Controls bone resorption by increasing OPG expression in osteoblasts and inhibiting isoprenaline-induced osteoclastogenesis | [124,125,126] |
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Sun, R.; Bai, L.; Yang, Y.; Ding, Y.; Zhuang, J.; Cui, J. Nervous System-Driven Osseointegration. Int. J. Mol. Sci. 2022, 23, 8893. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23168893
Sun R, Bai L, Yang Y, Ding Y, Zhuang J, Cui J. Nervous System-Driven Osseointegration. International Journal of Molecular Sciences. 2022; 23(16):8893. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23168893
Chicago/Turabian StyleSun, Ruoyue, Long Bai, Yaru Yang, Yanshu Ding, Jingwen Zhuang, and Jingyuan Cui. 2022. "Nervous System-Driven Osseointegration" International Journal of Molecular Sciences 23, no. 16: 8893. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23168893