Bidirectional communication between sensory neurons and osteoblasts in an <i>in vitro</i> coculture system

Kodama, Daisuke; Hanabusa, Takao; Kondo, Hisataka; Hamamura, Kazunori; Togari, Akifumi

doi:10.1002/1873-3468.12561

Cited by 15 publications

(18 citation statements)

References 49 publications

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“…In several studies, the coculture system had been used to investigate the communication between neurons and other cells [ 16 , 40 – 43 ]. It was reported that DRG could promote the proliferation of osteoblasts differentiated from BMSCs and the osteogenic gene expression under direct contact condition [ 40 ].…”

Section: Discussionmentioning

confidence: 99%

Dorsal Root Ganglion Maintains Stemness of Bone Marrow Mesenchymal Stem Cells by Enhancing Autophagy through the AMPK/mTOR Pathway in a Coculture System

Zhang

Jiang

et al. 2018

Stem Cells International

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Our previous studies found that sensory nerve tracts implanted in tissue-engineered bone (TEB) could result in better osteogenesis. To explore the mechanism of the sensory nerve promoting osteogenesis in TEB in vitro, a transwell coculture experiment was designed between dorsal root ganglion (DRG) cells and bone marrow mesenchymal stem cells (BMSCs). BMSC proliferation was determined by CCK8 assay, and osteo-, chondro-, and adipogenic differentiation were assessed by alizarin red, alcian blue, and oil red staining. We found that the proliferation and multipotent differentiation of BMSCs were all enhanced in the coculture group compared to the BMSCs group. Crystal violet staining showed that the clone-forming ability of BMSCs in the coculture group was also enhanced and mRNA levels of Sox2, Nanog, and Oct4 were significantly upregulated in the coculture group. Moreover, the autophagy level of BMSCs, regulating their stemness, was promoted in the coculture group, mediated by the AMPK/mTOR pathway. In addition, AMPK inhibitor compound C could significantly downregulate the protein expression of LC3 and the mRNA level of stemness genes in the coculture group. Finally, we found that the NK1 receptor antagonist, aprepitant, could partly block this effect, which indicated that substance P played an important role in the effect. Together, we conclude that DRG could maintain the stemness of BMSCs by enhancing autophagy through the AMPK/mTOR pathway in a transwell coculture system, which may help explain the better osteogenesis after implantation of the sensory nerve into TEB.

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Section: Discussionmentioning

confidence: 99%

Dorsal Root Ganglion Maintains Stemness of Bone Marrow Mesenchymal Stem Cells by Enhancing Autophagy through the AMPK/mTOR Pathway in a Coculture System

Zhang

Jiang

et al. 2018

Stem Cells International

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“…Notwithstanding the ongoing debate on which joint tissues give rise to pain in OA (nociceptive versus neuropathic) 35 , the bioelectric concept has some merit since sympathetic and sensory fibres densely innervate bone and joint tissues like the synovium, and can modulate inflammation, vascularization, matrix differentiation, and bone mass 34 . Kodama and colleagues have also recently proposed that osteoblasts, and possibly other bone surface cells, might serve as 'sensors' for environmental stimuli and transmit this perception to the CNS via afferent nerves 36 . Sensory nerves have even been observed in contact with a subpopulation of chondrocytes at the surface of articular cartilage 37 .…”

Section: P 89mentioning

confidence: 99%

Defining the osteoarthritis patient: back to the future

Dobson

Letson

Grant

et al. 2018

Osteoarthritis and Cartilage

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The history of osteoarthritis (OA) is important because it can help broaden our perspective on past and present controversies. The naming of OA, beginning with Heberden's nodes, is itself a fascinating story. According to Albert Hoffa, R. Llewellyn Jones and Archibald Edward Garrod, the name OA was introduced in the mid-nineteenth century by surgeon Richard von Volkmann who distinguished it from rheumatoid arthritis and gout. Others preferred the terms 'chronical rheumatism', 'senile arthritis', 'hypertrophic arthritis' or 'arthritis deformans'. A similar narrative applies to the concept of OA affecting the whole joint vs the 'wear-and-tear' hypothesis, inflammation and the role of the central nervous system (CNS). In the late nineteenth and early twentieth centuries, the Garrods (father and son) and Hermann Senator argued that OA was a whole joint disease, and that inflammation played a major role in its progression. Garrod Jnr and John Spender also linked OA to a neurogenic lesion 'outside the joint'. The remaining twentieth century was no less dynamic, with major advances in basic science, diagnostics, treatments, surgical interventions and technologies. Today, OA is characterized as a multi-disease with inflammation, immune and CNS dysfunction playing central roles in whole joint damage, injury progression, pain and disability. In the current 'omics' era (genomics, proteomics and metabolomics), we owe a great debt to past physicians and surgeons who dared to think 'outside-the-box' to explain and treat OA. Over 130 years later, despite these developments, we still don't fully understand the underlying complexities of OA, and we still don't have a cure.

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“…In a very recent study, Kodama et al describe a bi-directional communication of osteoblastic MC3T3-E1 cells and dorsal root ganglion-derived sensory neurons [91]. The authors show that the efferent signal is transmitted via SP and glutamate and that osteoblast-like cells communicate to the afferent neural arm via adenosine triphosphate (ATP) exocytosis after perception of an inflammatory stimulus like bradykinin.…”

Section: Sensory and Sympathetic Neurotransmitters And Their Recepmentioning

confidence: 99%

Peripheral Nerve Fibers and Their Neurotransmitters in Osteoarthritis Pathology

Grässel

Muschter

2017

IJMS

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The importance of the nociceptive nervous system for maintaining tissue homeostasis has been known for some time, and it has also been suggested that organogenesis and tissue repair are under neuronal control. Changes in peripheral joint innervation are supposed to be partly responsible for degenerative alterations in joint tissues which contribute to development of osteoarthritis. Various resident cell types of the musculoskeletal system express receptors for sensory and sympathetic neurotransmitters, allowing response to peripheral neuronal stimuli. Among them are mesenchymal stem cells, synovial fibroblasts, bone cells and chondrocytes of different origin, which express distinct subtypes of adrenoceptors (AR), receptors for vasoactive intestinal peptide (VIP), substance P (SP) and calcitonin gene-related peptide (CGRP). Some of these cell types synthesize and secrete neuropeptides such as SP, and they are positive for tyrosine-hydroxylase (TH), the rate limiting enzyme for biosynthesis of catecholamines. Sensory and sympathetic neurotransmitters are involved in the pathology of inflammatory diseases such as rheumatoid arthritis (RA) which manifests mainly in the joints. In addition, they seem to play a role in pathogenesis of priori degenerative joint disorders such as osteoarthritis (OA). Altogether it is evident that sensory and sympathetic neurotransmitters have crucial trophic effects which are critical for joint tissue and bone homeostasis. They modulate articular cartilage, subchondral bone and synovial tissue properties in physiological and pathophysiological conditions, in addition to their classical neurological features.

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Bidirectional communication between sensory neurons and osteoblasts in an in vitro coculture system

Cited by 15 publications

References 49 publications

Dorsal Root Ganglion Maintains Stemness of Bone Marrow Mesenchymal Stem Cells by Enhancing Autophagy through the AMPK/mTOR Pathway in a Coculture System

Dorsal Root Ganglion Maintains Stemness of Bone Marrow Mesenchymal Stem Cells by Enhancing Autophagy through the AMPK/mTOR Pathway in a Coculture System

Defining the osteoarthritis patient: back to the future

Peripheral Nerve Fibers and Their Neurotransmitters in Osteoarthritis Pathology

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