The role of semaphorin 3A on chondrogenic differentiation.
ATDC5
Cartilage
Cartilage substrate
Endochondral ossification
Semaphorin3A
Journal
In vitro cellular & developmental biology. Animal
ISSN: 1543-706X
Titre abrégé: In Vitro Cell Dev Biol Anim
Pays: Germany
ID NLM: 9418515
Informations de publication
Date de publication:
10 May 2024
10 May 2024
Historique:
received:
22
12
2023
accepted:
03
04
2024
medline:
10
5
2024
pubmed:
10
5
2024
entrez:
10
5
2024
Statut:
aheadofprint
Résumé
Osteoblast-derived semaphorin3A (Sema3A) has been reported to be involved in bone protection, and Sema3A knockout mice have been reported to exhibit chondrodysplasia. From these reports, Sema3A is considered to be involved in chondrogenic differentiation and skeletal formation, but there are many unclear points about its function and mechanism in chondrogenic differentiation. This study investigated the pharmacological effects of Sema3A in chondrogenic differentiation. The amount of Sema3A secreted into the culture supernatant was measured using an enzyme-linked immunosorbent assay. The expression of chondrogenic differentiation-related factors, such as Type II collagen (COL2A1), Aggrecan (ACAN), hyaluronan synthase 2 (HAS2), SRY-box transcription factor 9 (Sox9), Runt-related transcription factor 2 (Runx2), and Type X collagen (COL10A1) in ATDC5 cells treated with Sema3A (1,10 and 100 ng/mL) was examined using real-time reverse transcription polymerase chain reaction. Further, to assess the deposition of total glycosaminoglycans during chondrogenic differentiation, ATDC5 cells were stained with Alcian Blue. Moreover, the amount of hyaluronan in the culture supernatant was measured by enzyme-linked immunosorbent assay. The addition of Sema3A to cultured ATDC5 cells increased the expression of Sox9, Runx2, COL2A1, ACAN, HAS2, and COL10A1 during chondrogenic differentiation. Moreover, it enhanced total proteoglycan and hyaluronan synthesis. Further, Sema3A was upregulated in the early stages of chondrogenic differentiation, and its secretion decreased later. Sema3A increases extracellular matrix production and promotes chondrogenic differentiation. To the best of our knowledge, this is the first study to demonstrate the role of Sema3A on chondrogenic differentiation.
Identifiants
pubmed: 38727898
doi: 10.1007/s11626-024-00909-z
pii: 10.1007/s11626-024-00909-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Atsumi T, Ikawa Y, Miwa Y, Kimata K (1990) A chondrogenic cell line derived from a differentiating culture of AT805 teratocarcinoma cells. Cell Differ Dev 30:109–116. https://doi.org/10.1016/0922-3371(90)90079-C
doi: 10.1016/0922-3371(90)90079-C
pubmed: 2201423
Behar O, Goldent JA, Mashimo H et al (1996) Semaphorin III is needed for normal patterning and growth of nerves, bones, and heart. Nature 383:525–528
doi: 10.1038/383525a0
pubmed: 8849723
Chen H, Chédotal A, He Z et al (1997) Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 19:547–559. https://doi.org/10.1016/S0896-6273(00)80371-2
doi: 10.1016/S0896-6273(00)80371-2
pubmed: 9331348
Chen H, Ghori-Javed FY, Rashid H et al (2014) Runx2 regulates endochondral ossification through control of chondrocyte proliferation and differentiation. J Bone Miner Res 29:2653–2665. https://doi.org/10.1002/jbmr.2287
doi: 10.1002/jbmr.2287
pubmed: 24862038
Goldring MB, Tsuchimochi K, Ijiri K (2006) The control of chondrogenesis. J Cell Biochem 97:33–44. https://doi.org/10.1002/jcb.20652
doi: 10.1002/jcb.20652
pubmed: 16215986
Hayashi M, Nakashima T, Taniguchi M et al (2012) Osteoprotection by semaphorin 3A. Nature 485:69–74. https://doi.org/10.1038/nature11000
doi: 10.1038/nature11000
pubmed: 22522930
Hayashi M, Nakashima T, Yoshimura N et al (2019) Autoregulation of osteocyte Sema3A orchestrates estrogen action and counteracts bone aging. Cell Metab 29:627–637. https://doi.org/10.1016/j.cmet.2018.12.021
doi: 10.1016/j.cmet.2018.12.021
pubmed: 30661929
Kajii TS, Oka A, Hatta M et al (2018) PLXNA2 identified as a candidate gene by genome-wide association analysis for mandibular prognathism in human chondrocytes. Biomedical Reports 9:253–258. https://doi.org/10.3892/br.2018.1128
doi: 10.3892/br.2018.1128
pubmed: 30271602
pmcid: 6158401
Kaneko S, Iwanami A, Nakamura M et al (2006) A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat Med 12:1380–1389. https://doi.org/10.1038/nm1505
doi: 10.1038/nm1505
pubmed: 17099709
Kolodkin AL, Levengood DV, Rowe EG et al (1997) Neuropilin is a semaphorin III receptor. Cell 90:753–762. https://doi.org/10.1016/S0092-8674(00)80535-8
doi: 10.1016/S0092-8674(00)80535-8
pubmed: 9288754
Kolodkin AL, Matthes DJ, Goodman CS (1993) The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75:1389–1399. https://doi.org/10.1016/0092-8674(93)90625-Z
doi: 10.1016/0092-8674(93)90625-Z
pubmed: 8269517
Kumanogoh A, Marukawa S, Suzuki K et al (2002) Class IV semaphorin Sema4A enhances T-cell activation and interacts with Tim-2. Nature 419:629–633. https://doi.org/10.1038/nature01037
doi: 10.1038/nature01037
pubmed: 12374982
Mackie EJ, Ahmed YA, Tatarczuch L et al (2008) Endochondral ossification: How cartilage is converted into bone in the developing skeleton. Int J Biochem Cell Biol 40:46–62. https://doi.org/10.1016/j.biocel.2007.06.009
doi: 10.1016/j.biocel.2007.06.009
pubmed: 17659995
Magee C, Nurminskaya M, Linsenmayer TF (2001) UDP-glucose pyrophosphorylase: Up-regulation in hypertrophic cartilage and role in hyaluronan synthesis. Biochemical Journal 360:667–674. https://doi.org/10.1042/0264-6021:3600667
doi: 10.1042/0264-6021:3600667
pubmed: 11736658
pmcid: 1222271
Nagata K, Hojo H, Chang SH et al (2022) Runx2 and Runx3 differentially regulate articular chondrocytes during surgically induced osteoarthritis development. Nature Communications 13:433. https://doi.org/10.1038/s41467-022-33744-5
doi: 10.1038/s41467-022-33744-5
Nakatani S, Mano H, Im R et al (2007) Glucosamine regulates differentiation of a chondrogenic cell line, ATDC5. Biol Pharm Bull 30:433–438. https://doi.org/10.1248/bpb.30.433
doi: 10.1248/bpb.30.433
pubmed: 17329833
Nishimura R, Wakabayashi M, Hata K et al (2012) Osterix regulates calcification and degradation of chondrogenic matrices through matrix metalloproteinase 13 (MMP13) expression in association with transcription factor Runx2 during endochondral ossification. J Biol Chem 287:33179–33190. https://doi.org/10.1074/jbc.M111.337063
doi: 10.1074/jbc.M111.337063
pubmed: 22869368
pmcid: 3460424
Ono K, Hata K, Nakamura E et al (2021) Dmrt2 promotes transition of endochondral bone formation by linking Sox9 and Runx2. Communications Biology 4:1–13. https://doi.org/10.1038/s42003-021-01848-1
doi: 10.1038/s42003-021-01848-1
Sekido Y, Bader S, Latif F et al (1996) Human semaphorins A(V) and IV reside in the 3p21.3 small cell lung cancer deletion region and demonstrate distinct expression patterns. Proc Natl Acad Sci USA 93:4120–4125. https://doi.org/10.1073/pnas.93.9.4120
doi: 10.1073/pnas.93.9.4120
pubmed: 8633026
pmcid: 39497
Serini G, Valdembri D, Zanivan S et al (2003) Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424:391–397
doi: 10.1038/nature01784
pubmed: 12879061
Shukunami C, Ishizeki K, Atsumi T et al (1997) Cellular hypertrophy and calcification of embryonal carcinoma-derived chondrogenic cell line ATDC5 in vitro. J Bone Miner Res 12:1174–1188. https://doi.org/10.1359/jbmr.1997.12.8.1174
doi: 10.1359/jbmr.1997.12.8.1174
pubmed: 9258747
Sumi C, Hirose N, Yanoshita M et al (2018) Semaphorin 3A inhibits inflammation in chondrocytes under excessive mechanical stress. Mediators of Inflammation 2018:57. https://doi.org/10.1155/2018/5703651
doi: 10.1155/2018/5703651
Suzuki A, Tanimoto K, Ohno S et al (2005) The metabolism of hyaluronan in cultured rabbit growth plate chondrocytes during differentiation. Biochimica Et Biophysica Acta - Molecular Cell Research 1743:57–63. https://doi.org/10.1016/j.bbamcr.2004.08.007
doi: 10.1016/j.bbamcr.2004.08.007
Takahashi T, Strittmatter SM (2001) PlexinA1 autoinhibition by the Plexin sema domain. Neuron 29:429–439. https://doi.org/10.1016/S0896-6273(01)00216-1
doi: 10.1016/S0896-6273(01)00216-1
pubmed: 11239433
Winberg ML, Noordermeer JN, Tamagnone L et al (1998) Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95:903–916. https://doi.org/10.1016/S0092-8674(00)81715-8
doi: 10.1016/S0092-8674(00)81715-8
pubmed: 9875845
Woods A, Wang G, Dupuis H et al (2007) Rac1 signaling stimulates N-cadherin expression, mesenchymal condensation, and chondrogenesis. J Biol Chem 282:23500–23508. https://doi.org/10.1074/jbc.M700680200
doi: 10.1074/jbc.M700680200
pubmed: 17573353
Yamaguchi Y, Kumagai K, Imai S et al (2018) Sclerostin is upregulated in the early stage of chondrogenic differentiation, but not required in endochondral ossification in vitro. PLoS ONE 13:20894. https://doi.org/10.1371/journal.pone.0201839
doi: 10.1371/journal.pone.0201839
Yazdani U, Terman JR (2006) The semaphorins. Genome Biol 7:211. https://doi.org/10.1186/gb-2006-7-3-211
doi: 10.1186/gb-2006-7-3-211
pubmed: 16584533
pmcid: 1557745
Yonashiro R, Sugiura A, Miyachi M et al (2009) Sox9 family members negatively regulate maturation and calcification of chondrocytes through up-regulation of parathyroid hormone–related protein. Mol Biol Cell 20:4541–4551. https://doi.org/10.1091/mbc.E09
doi: 10.1091/mbc.E09
Yoshida S, Wada N, Hasegawa D et al (2016) Semaphorin 3A Induces Odontoblastic Phenotype in Dental Pulp Stem Cells. J Dent Res 95:1282–1290. https://doi.org/10.1177/0022034516653085
doi: 10.1177/0022034516653085
pubmed: 27302880
Yoshioka Y, Kozawa E, Urakawa H et al (2015) Inhibition of hyaluronan synthesis alters sulfated glycosaminoglycans deposition during chondrogenic differentiation in ATDC5 cells. Histochem Cell Biol 144:167–177. https://doi.org/10.1007/s00418-015-1325-3
doi: 10.1007/s00418-015-1325-3
pubmed: 25929745
Zhou Y, Gunput RAF, Pasterkamp RJ (2008) Semaphorin signaling: progress made and promises ahead. Trends Biochem Sci 33:161–170. https://doi.org/10.1016/j.tibs.2008.01.006
doi: 10.1016/j.tibs.2008.01.006
pubmed: 18374575