Abstract
The objective of the present study was to review the molecular mechanisms of the adverse effects of environmental pollutants on chondrocytes and extracellular matrix (ECM). Existing data demonstrate that both heavy metals, including cadmium (Cd), lead (Pb), and arsenic (As), as well as organic pollutants, including polychlorinated dioxins and furans (PCDD/Fs) and polychlorinated biphenyls (PCB), bisphenol A, phthalates, polycyclic aromatic hydrocarbons (PAH), pesticides, and certain other organic pollutants that target cartilage ontogeny and functioning. Overall, environmental pollutants reduce chondrocyte viability through the induction apoptosis, senescence, and inflammatory response, resulting in cell death and impaired ECM production. The effects of organic pollutants on chondrocyte development and viability were shown to be mediated by binding to the aryl hydrocarbon receptor (AhR) signaling and modulation of non-coding RNA expression. Adverse effects of pollutant exposures were observed in articular and growth plate chondrocytes. These mechanisms also damage chondrocyte precursors and subsequently hinder cartilage development. In addition, pollutant exposure was shown to impair chondrogenesis by inhibiting the expression of Sox9 and other regulators. Along with altered Runx2 signaling, these effects also contribute to impaired chondrocyte hypertrophy and chondrocyte-to-osteoblast trans-differentiation, resulting in altered endochondral ossification. Several organic pollutants including PCDD/Fs, PCBs and PAHs, were shown to induce transgenerational adverse effects on cartilage development and the resulting skeletal deformities. Despite of epidemiological evidence linking human environmental pollutant exposure to osteoarthritis or other cartilage pathologies, the data on the molecular mechanisms of adverse effects of environmental pollutant exposure on cartilage tissue were obtained from studies in laboratory rodents, fish, or cell cultures and should be carefully extrapolated to humans, although they clearly demonstrate that cartilage should be considered a putative target for environmental pollutant toxicity.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
Abbreviations
- 6-OH-BDE-47:
-
6: Hydroxy-2,2′,4,4′-tetrabromodiphenyl ether
- ACAN:
-
Type 2 collagen (COL2A1) and aggrecan
- Adamts5A:
-
Disintegrin and metalloproteinase with thrombospondin motifs 5
- AhR:
-
Aryl hydrocarbon receptor
- BaP:
-
Benzo[a]pyrene
- BMP-2:
-
Bone morphogenetic protein 2
- BPA:
-
Bisphenol A
- BPAF:
-
Bisphenol AF
- BPS:
-
Bisphenol S
- CCL2:
-
C–C motif ligand 2
- circRNAs:
-
Circular RNAs
- COX-2:
-
Cyclooxygenase-2
- CTSK:
-
Cathepsin K
- cxcr4:
-
CXC chemokine 4
- CYP450:
-
Cytochrome P450
- DBP:
-
Dibutylphthalate
- Dio:
-
Deiodinases
- DKK1:
-
Dickkopf-1
- DNMT1:
-
DNA methyltransferase 1
- ECM:
-
Extracellular matrix
- ER:
-
Estrogen receptor
- ERK:
-
Extracellular signal-regulated kinases
- FoxO:
-
Forkhead box protein O
- GALE:
-
UDP-galactose-4 epimerase
- GH:
-
Growth hormone
- Gpx:
-
Glutathione peroxidase
- GSK-3β:
-
Glycogen synthase kinase-3 beta
- HIF-1α:
-
Hypoxia-inducible factor 1 alpha
- Hsp27:
-
Heat shock protein 27
- IGF-1:
-
Insulin-like growth factor 1
- Ihh:
-
Indian hedgehog
- IL-1β:
-
Interleukin-1β
- il-7r:
-
Interleukin-7 receptor
- iNOS:
-
Inducible nitric oxide synthase
- JNK:
-
C-Jun N-terminal kinase
- lncRNAs:
-
Long non-coding RNAs
- LPS:
-
Lipopolysaccharide
- miRNA:
-
MicroRNAs
- MMP:
-
Metalloproteinase
- MSCs:
-
Mesenchymal stem cells
- mTOR:
-
Mammalian target of rapamycin
- NAC:
-
N-acetylcysteine
- NF-κB:
-
Nuclear factor kappa-B
- NHANES:
-
National health and nutrition examination survey
- NLRP3:
-
NLR family pyrin domain containing 3
- NOAEL:
-
No observed adverse effect level
- OPN:
-
Osteopontin
- PAH:
-
Polycyclic aromatic hydrocarbons
- PAI-1:
-
Plasminogen activator inhibitor-1
- PBDE:
-
Polybrominated diphenyl ethers
- PCB:
-
Polychlorinated biphenyls
- PCNA:
-
Proliferating cell nuclear antigen
- PKC-δ:
-
Protein kinase C delta type
- PTHrP:
-
Parathyroid hormone-related peptide
- PUMA:
-
P53-upregulated modulator of apoptosis
- RARα:
-
Retinoic acid receptor α
- rgs1:
-
Regulator of G-protein signaling 1
- ROS:
-
Reactive oxygen species
- sdf-1:
-
Stromal cell-derived factor 1
- Shh:
-
Sonic hedgehog
- Sox9:
-
SRY-box transcription factor 9
- TBT:
-
Tributyltin
- TCDD:
-
2,3,7,8-Tetrachlorodibenzodioxin
- TD:
-
Tibial dyschondroplasia
- TGF-β:
-
Transforming growth factor beta
- TIMP3:
-
Metalloproteinase inhibitor 3
- TNFα:
-
Tumor necrosis factor α
- Txnrd:
-
Thioredoxin reductase
- VEGF:
-
Vascular endothelial growth factor
- VEGFR:
-
VEGF receptor
References
Abbas S, Khan K, Khan MP, Nagar GK, Tewari D, Maurya SK, Dubey J, Ansari NG, Bandyopadhyay S, Chattopadhyay N (2013) Developmental exposure to As, Cd, and Pb mixture diminishes skeletal growth and causes osteopenia at maturity via osteoblast and chondrocyte malfunctioning in female rats. Toxicol Sci 134(1):207–220. https://doi.org/10.1093/toxsci/kft093
Abdullah M, Rahman FA, Gnanasegaran N, Govindasamy V, Abu Kasim NH, Musa S (2014) Diverse effects of lead nitrate on the proliferation, differentiation, and gene expression of stem cells isolated from a dental origin. Sci World J 2014:235941. https://doi.org/10.1155/2014/235941
Abella V, Santoro A, Scotece M, Conde J, López-López V, Lazzaro V, Gómez-Reino JJ, Meli R, Gualillo O (2015) Non-dioxin-like polychlorinated biphenyls (PCB 101, PCB 153 and PCB 180) induce chondrocyte cell death through multiple pathways. Toxicol Lett 234(1):13–19. https://doi.org/10.1016/j.toxlet.2015.02.001
Abraham A, Chakraborty P (2020) A review on sources and health impacts of bisphenol A. Rev Environ Health 35(2):201–210. https://doi.org/10.1515/reveh-2019-0034
Alex AM, Kunkel G, Sayles H, Flautero Arcos JD, Mikuls TR, Kerr GS (2020) Exposure to ambient air pollution and autoantibody status in rheumatoid arthritis. Clin Rheumatol 39(3):761–768. https://doi.org/10.1007/s10067-019-04813-w
Amini Z, Mahdavi-Shahri N, Lari R, Behnam Rassouli F (2019) The effects of lead on the development of somites in chick embryos (Gallus gallus domesticus) under in vitro conditions: a histological study. Toxicol Res (camb) 8(3):373–380. https://doi.org/10.1039/c8tx00340h
Ansari MM, Neha Khan HA (2015) Effect of cadmium chloride exposure during the induction of collagen induced arthritis. Chem Biol Interact 238:55–65. https://doi.org/10.1016/j.cbi.2015.06.001
Aschner M, Skalny AV, Lu R, Santamaria A, Zhou JC, Ke T, Karganov MY, Tsatsakis A, Golokhvast KS, Bowman AB, Tinkov AA (2023) The role of hypoxia-inducible factor 1 alpha (HIF-1α) modulation in heavy metal toxicity. Arch Toxicol 97(5):1299–1318. https://doi.org/10.1007/s00204-023-03483-7
Auxietre TA, Dumontier MF, Balguy I, Frapart Y, Canivenc-Lavier MC, Berges R, Boudalia S, Auger J, Corvol MT, Savouret JF (2014) Sub-NOAEL amounts of vinclozolin and xenoestrogens target rat chondrogenesis in vivo. Biochimie 99:169–177. https://doi.org/10.1016/j.biochi.2013.12.001
Aybar Odstrcil AC, Carino SN, Ricci JC, Mandalunis PM (2010) Effect of arsenic in endochondral ossification of experimental animals. Exp Toxicol Pathol 62(3):243–249. https://doi.org/10.1016/j.etp.2009.04.001
Beier EE, Sheu TJ, Buckley T, Yukata K, O’Keefe R, Zuscik MJ, Puzas JE (2014) Inhibition of beta-catenin signaling by Pb leads to incomplete fracture healing. J Orthop Res 32(11):1397–1405. https://doi.org/10.1002/jor.22677
Bortoluzzi A, Furini F, Scirè CA (2018) Osteoarthritis and its management—epidemiology, nutritional aspects and environmental factors. Autoimmun Rev 17(11):1097–1104. https://doi.org/10.1016/j.autrev.2018.06.002
Brankovič J, Jan J, Fazarinc G, Vrecl M (2020) Bone tissue morphology of rat offspring lactationally exposed to polychlorinated biphenyl 169 and 155. Sci Rep 10(1):19016. https://doi.org/10.1038/s41598-020-76057-7
Brodziak-Dopierala B, Kwapulinski J, Gajda Z, Toborek J, Bogunia M (2006) Changes of heavy metal concentrations in cross-sections of human femur head. Biol Trace Elem Res 114(1–3):107–114. https://doi.org/10.1385/BTER:114:1:107
Brodziak-Dopierała B, Kwapuliński J, Sobczyk K, Wiechuła D (2015) Analysis of the content of cadmium and zinc in parts of the human hip joint. Biol Trace Elem Res 163(1–2):73–80. https://doi.org/10.1007/s12011-014-0168-4
Burns FR, Peterson RE, Heideman W (2015) Dioxin disrupts cranial cartilage and dermal bone development in zebrafish larvae. Aquat Toxicol 164:52–60. https://doi.org/10.1016/j.aquatox.2015.04.005
Caito S, Lopes ACBA, Paoliello MM, Aschner M (2017) Toxicology of lead and its damage to mammalian organs. Met Ions Life Sci 17:501–534
Carmouche JJ, Puzas JE, Zhang X, Tiyapatanaputi P, Cory-Slechta DA, Gelein R, Zuscik M, Rosier RN, Boyce BF, O’Keefe RJ, Schwarz EM (2005) Lead exposure inhibits fracture healing and is associated with increased chondrogenesis, delay in cartilage mineralization, and a decrease in osteoprogenitor frequency. Environ Health Perspect 113(6):749–755. https://doi.org/10.1289/ehp.7596
Casey CE, Guthrie BE, Robinson MF (1982) Copper, manganese, zinc, and cadmium in tissues from New Zealanders. Biol Trace Elem Res 4(2–3):105–115. https://doi.org/10.1007/BF02783251
Cedervall T, Lind PM, Sävendahl L (2015) Expression of the aryl hydrocarbon receptor in growth plate cartilage and the impact of its local modulation on longitudinal bone growth. Int J Mol Sci 16(4):8059–8069. https://doi.org/10.3390/ijms16048059
Chandra Sekaran SP, Thotakura B, Jyothi AK, Manickam S, Chanemougavally J, Prabhu K, Gopalan DH (2023) Effect of chlorpyrifos and its metabolites on skeletal system development of chick embryo. Birth Defects Res 115(11):1063–1078. https://doi.org/10.1002/bdr2.2170
Chau TT, Wang KY (2020) An association between air pollution and daily most frequently visits of eighteen outpatient diseases in an industrial city. Sci Rep 10(1):2321. https://doi.org/10.1038/s41598-020-58721-0
Chen CH, Guo YL (2013) Effects of endocrine-disrupting substances on bone and joint. Eff Persistent Bioact Organic Pollut Hum Health 16:332–361
Chen H, Wu J, Wang M, Wang S, Wang J, Yu H, Hu Y, Shang S (2021a) Impact of exposure to ambient fine particulate matter pollution on adults with knee osteoarthritis. Int J Environ Res Public Health 18(18):9644. https://doi.org/10.3390/ijerph18189644
Chen SM, Jahejo AR, Nabi F, Ahmed S, Zhao JF, Yu J, Zhang CL, Ning GB, Zhang D, Raza SHA, Tian WX (2021b) Janus kinase/signal transducer and activator of transcription signaling pathway-related genes STAT3, SOCS3 and their role in thiram induced tibial dyschondroplasia chickens. Res Vet Sci 136:25–31. https://doi.org/10.1016/j.rvsc.2021.01.024
Chin KY, Pang KL, Mark-Lee WF (2018) A review on the effects of bisphenol a and its derivatives on skeletal health. Int J Med Sci 15(10):1043–1050. https://doi.org/10.7150/ijms.25634
Chung YP, Chen YW, Weng TI, Yang RS, Liu SH (2020) Arsenic induces human chondrocyte senescence and accelerates rat articular cartilage aging. Arch Toxicol 94(1):89–101. https://doi.org/10.1007/s00204-019-02607-2
Chung YP, Weng TI, Chan DC, Yang RS, Liu SH (2023) Low-dose tributyltin triggers human chondrocyte senescence and mouse articular cartilage aging. Arch Toxicol 97(2):547–559. https://doi.org/10.1007/s00204-022-03407-x
Cima F (2011) Tin: environmental pollution and health effects. Encycl Environ Health 2:65–75
Cocchi D, Tulipano G, Colciago A, Sibilia V, Pagani F, Viganò D, Rubino T, Parolaro D, Bonfanti P, Colombo A, Celotti F (2009) Chronic treatment with polychlorinated biphenyls (PCB) during pregnancy and lactation in the rat: part 1— effects on somatic growth, growth hormone-axis activity and bone mass in the offspring. Toxicol Appl Pharmacol 237(2):127–136. https://doi.org/10.1016/j.taap.2009.03.008
Collin MS, Venkatraman SK, Vijayakumar N, Kanimozhi V, Arbaaz SM, Stacey RS, Anusha J, Choudhary R, Lvov V, Tovar GI, Senatov F (2022) Bioaccumulation of lead (Pb) and its effects on human: a review. J Hazard Mater Adv 7:100094
Cooper J, Dobson H (2007) The benefits of pesticides to mankind and the environment. Crop Prot 26(9):1337–1348
Deane KD, Demoruelle MK, Kelmenson LB, Kuhn KA, Norris JM, Holers VM (2017) Genetic and environmental risk factors for rheumatoid arthritis. Best Pract Res Clin Rheumatol 31(1):3–18. https://doi.org/10.1016/j.berh.2017.08.003
Deprouw C, Courties A, Fini JB, Clerget-Froidevaux MS, Demeneix B, Berenbaum F, Sellam J, Louati K (2022) Pollutants: a candidate as a new risk factor for osteoarthritis-results from a systematic literature review. RMD Open 8(2):e001983. https://doi.org/10.1136/rmdopen-2021-001983
Di D, Zhang L, Wu X, Leng R (2020) Long-term exposure to outdoor air pollution and the risk of development of rheumatoid arthritis: a systematic review and meta-analysis. Semin Arthritis Rheum 50(2):266–275. https://doi.org/10.1016/j.semarthrit.2019.10.005
Díaz-Martín RD, Carvajal-Peraza A, Yáñez-Rivera B, Betancourt-Lozano M (2021) Short exposure to glyphosate induces locomotor, craniofacial, and bone disorders in zebrafish (Danio rerio) embryos. Environ Toxicol Pharmacol 87:103700. https://doi.org/10.1016/j.etap.2021.103700
Ding Y, Yao W, Fakhar-E-Alam Kulyar M, Mo Q, Pan H, Zhang Y, Ma B, He Y, Zhang M, Hong J, Waqas M, Li J (2021) Taurine is an effective therapy against thiram induced tibial dyschondroplasia via HIF-1α/VEGFA and β-catenin/ GSK-3β pathways in broilers. Ecotoxicol Environ Saf 228:112981. https://doi.org/10.1016/j.ecoenv.2021.112981
Djordjevic AB, Antonijevic E, Curcic M, Milovanovic V, Antonijevic B (2020) Endocrine-disrupting mechanisms of polychlorinated biphenyls. Curr Opin Toxicol 19:42–49
Dohi Y, Sugimoto K, Yoshikawa T, Ohgushi H, Katsuda T, Tabata S, Moriyama T (1993) Effect of cadmium on osteogenesis within diffusion chambers by bone marrow cells: biochemical evidence of decreased bone formation capacity. Toxicol Appl Pharmacol 120(2):274–280. https://doi.org/10.1006/taap.1993.1112
Dong W, Hinton DE, Kullman SW (2012) TCDD disrupts hypural skeletogenesis during medaka embryonic development. Toxicol Sci 125(1):91–104. https://doi.org/10.1093/toxsci/kfr284
Duan L, Deng H, Zhang Q, Gao P, Wu L (2023) Environmentally relevant levels of BPA and NOR disturb early skeletal development in zebrafish. Comp Biochem Physiol C Toxicol Pharmacol 271:109662. https://doi.org/10.1016/j.cbpc.2023.109662
Đukić-Ćosić D, Baralić K, Javorac D, Djordjevic AB, Bulat Z (2020) An overview of molecular mechanisms in cadmium toxicity. Curr Opin Toxicol 19:56–62
Duval E, Leclercq S, Elissalde JM, Demoor M, Galéra P, Boumédiene K (2009) Hypoxia-inducible factor 1alpha inhibits the fibroblast-like markers type I and type III collagen during hypoxia-induced chondrocyte redifferentiation: hypoxia not only induces type II collagen and aggrecan, but it also inhibits type I and type III collagen in the hypoxia-inducible factor 1alpha-dependent redifferentiation of chondrocytes. Arthritis Rheum 60(10):3038–3048. https://doi.org/10.1002/art.24851
Egger AE, Grabmann G, Gollmann-Tepeköylü C, Pechriggl EJ, Artner C, Türkcan A, Hartinger CG, Fritsch H, Keppler BK, Brenner E, Grimm M, Messner B, Bernhard D (2019) Chemical imaging and assessment of cadmium distribution in the human body. Metallomics 11(12):2010–2019. https://doi.org/10.1039/c9mt00178f
Elter E, Wagner M, Buchenauer L, Bauer M, Polte T (2020) Phthalate exposure during the prenatal and lactational period increases the susceptibility to rheumatoid arthritis in mice. Front Immunol 11:550. https://doi.org/10.3389/fimmu.2020.00550
Fan X, Wu L, Hou T, He J, Wang C, Liu Y, Wang Z (2018) Maternal bisphenol a exposure impaired endochondral ossification in craniofacial cartilage of rare minnow (Gobiocypris rarus) offspring. Ecotoxicol Environ Saf 163:514–520. https://doi.org/10.1016/j.ecoenv.2018.07.100
Fang L, Zhao H, Chen Y, Ma Y, Xu S, Xu S, Pan G, Cai G, Shuai Z, Pan F (2023) The combined effect of heavy metals and polycyclic aromatic hydrocarbons on arthritis, especially osteoarthritis, in the US adult population. Chemosphere. https://doi.org/10.1016/j.chemosphere.2023.137870
Fujun T, Jiabao S, Jianmin Y, Qiyu W (2023) Hexabromocyclododecane (HBCD) induced PANoptosis of chondrocytes via activation of the NLRP3 inflammasome and decreased the exercise ability of mice in vivo. Toxicology 499:153659. https://doi.org/10.1016/j.tox.2023.153659
Gao H, Liu CP, Song SQ, Fu J (2016) Effects of dietary selenium against lead toxicity on mRNA levels of 25 selenoprotein genes in the cartilage tissue of broiler chicken. Biol Trace Elem Res 172(1):234–241. https://doi.org/10.1007/s12011-015-0579-x
Garcia GR, Goodale BC, Wiley MW, La Du JK, Hendrix DA, Tanguay RL (2017) In vivo characterization of an ahr-dependent long noncoding rna required for proper Sox9b expression. Mol Pharmacol 91(6):609–619. https://doi.org/10.1124/mol.117.108233
Garcia GR, Shankar P, Dunham CL, Garcia A, La Du JK, Truong L, Tilton SC, Tanguay RL (2018) Signaling events downstream of ahr activation that contribute to toxic responses: the functional role of an ahr-dependent long noncoding rna (slincR) using the zebrafish model. Environ Health Perspect 126(11):117002. https://doi.org/10.1289/EHP3281
Garg UK, Pal AK, Jha GJ, Jadhao SB (2004) Pathophysiological effects of chronic toxicity with synthetic pyrethroid, organophosphate and chlorinated pesticides on bone health of broiler chicks. Toxicol Pathol 32(3):364–369. https://doi.org/10.1080/01926230490431745
González-Riola J, Hernández ER, Escribano A, Revilla M, Ca-Seco VLF, Rico H (1997) Effect of lead on bone and cartilage in sexually mature rats: a morphometric and histomorphometry study. Environ Res 74(1):91–93. https://doi.org/10.1006/enrs.1997.3760
Grässel S, Aszódi A (2016) Cartilage. Springer, Berlin
Gu J, Li S, Wang G, Zhang X, Yuan Y, Liu X, Bian J, Tong X, Liu Z (2021) Cadmium toxicity on chondrocytes and the palliative effects of 1α, 25-dihydroxy vitamin d3 in white leghorns chicken’s embryo. Front Vet Sci 8:637369. https://doi.org/10.3389/fvets.2021.637369
Guo L, Zhao Y, Zhang S, Liu K (2008) Anti-estrogenic effect of dioxin on rat skeleton development. Wei Sheng Yan Jiu 37(5):563–565
Hannan FM, Newey PJ, Whyte MP, Thakker RV (2020) Genetics of skeletal disorders. Handb Exp Pharmacol 262:325–351. https://doi.org/10.1007/164_2020_350
He C, Zuo Z, Shi X, Li R, Chen D, Huang X, Chen Y, Wang C (2011) Effects of benzo(a)pyrene on the skeletal development of Sebastiscus marmoratus embryos and the molecular mechanism involved. Aquat Toxicol 101(2):335–341. https://doi.org/10.1016/j.aquatox.2010.11.008
Heluany CS, De Palma A, Day NJ, Farsky SHP, Nalesso G (2023) Hydroquinone, an environmental pollutant, affects cartilage homeostasis through the activation of the aryl hydrocarbon receptor pathway. Cells 12(5):690. https://doi.org/10.3390/cells12050690
Hicks DG, O’Keefe RJ, Reynolds KJ, Cory-Slechta DA, Puzas JE, Judkins A, Rosier RN (1996) Effects of lead on growth plate chondrocyte phenotype. Toxicol Appl Pharmacol 140(1):164–172. https://doi.org/10.1006/taap.1996.0209
Holz JD, Beier E, Sheu TJ, Ubayawardena R, Wang M, Sampson ER, Rosier RN, Zuscik M, Puzas JE (2012) Lead induces an osteoarthritis-like phenotype in articular chondrocytes through disruption of TGF-β signaling. J Orthop Res 30(11):1760–1766. https://doi.org/10.1002/jor.22117
Hoogduijn MJ, Rakonczay Z, Genever PG (2006) The effects of anticholinergic insecticides on human mesenchymal stem cells. Toxicol Sci 94(2):342–350. https://doi.org/10.1093/toxsci/kfl101
Hu YC, Cheng HL, Hsieh BS, Huang LW, Huang TC, Chang KL (2012) Arsenic trioxide affects bone remodeling by effects on osteoblast differentiation and function. Bone 50(6):1406–1415. https://doi.org/10.1016/j.bone.2012.03.012
Huang SC, Li L, Rehman MU, Gao JD, Zhang LH, Tong XL, Waqas M, Li JK (2019) Tibial growth plate vascularization is inhibited by the dithiocarbamate pesticide thiram in chickens: potential relationship to peripheral platelet counts alteration. Environ Sci Pollut Res Int 26(36):36322–36332. https://doi.org/10.1007/s11356-019-06664-z
Huang W, Zheng S, Xiao J, Liu C, Du T, Wu K (2020) Parental exposure to bisphenol a affects pharyngeal cartilage development and causes global transcriptomic changes in zebrafish (Danio rerio) offspring. Chemosphere 249:126537. https://doi.org/10.1016/j.chemosphere.2020.126537
Huang W, Wang X, Zheng S, Wu R, Liu C, Wu K (2021) Effect of bisphenol a on craniofacial cartilage development in zebrafish (Danio rerio) embryos: a morphological study. Ecotoxicol Environ Saf 212:111991. https://doi.org/10.1016/j.ecoenv.2021.111991
Huang W, Shi X, Chen Y, Zhang Q, Peng J, Zheng S, Wu K (2023) Comparative pharyngeal cartilage developmental toxicity of bisphenol A, bisphenol S and bisphenol AF to zebrafish (Danio rerio) larvae: a combination of morphometry and global transcriptome analyses. Sci Total Environ 868:161702. https://doi.org/10.1016/j.scitotenv.2023.161702
Iqbal MK, Liu J, Nabi F, Rehman MU, Zhang H, Tahir AH, Li J (2016) recovery of chicken growth plate by heat-shock protein 90 inhibitors epigallocatechin-3-gallate and apigenin in thiram-induced tibial dyschondroplasia. Avian Dis 60(4):773–778. https://doi.org/10.1637/11425-041816-Reg
Iskandarani L, McHattie T, Robaire B, Hales BF (2022) Effects of bisphenols A, AF, and S on endochondral ossification and the transcriptome of murine limb buds. Toxicol Sci 187(2):234–253. https://doi.org/10.1093/toxsci/kfab145
Itokawa Y, Nishino K, Takashima M, Nakata T, Kaito H, Okamoto E, Daijo K, Kawamura J (1978) Renal and skeletal lesions in experimental cadmium poisoning of rats Histology and Renal Function. Environ Res 15(2):206–217. https://doi.org/10.1016/0013-9351(78)90097-x
Jergensen T, Cusmano D, Roy NM (2019) Di-butyl phthalate (DBP) induces craniofacial defects during embryonic development in zebrafish. Ecotoxicology 8:995–1002. https://doi.org/10.1007/s10646-019-02100-7
Katsikantami I, Sifakis S, Tzatzarakis MN, Vakonaki E, Kalantzi OI, Tsatsakis AM, Rizos AK (2016) A global assessment of phthalates burden and related links to health effects. Environ Int 97:212–236. https://doi.org/10.1016/j.envint.2016.09.013
Kim SH, Kim SS, Kwon O, Sohn KH, Kwack SJ, Choi YW, Han SY, Lee MK, Park KL (2002) Effects of dibutyl phthalate and monobutyl phthalate on cytotoxicity and differentiation in cultured rat embryonic limb bud cells; protection by antioxidants. J Toxicol Environ Health A 65(5–6):461–472. https://doi.org/10.1080/15287390252808118
Kim KH, Kabir E, Jahan SA (2017) Exposure to pesticides and the associated human health effects. Sci Total Environ 575:525–535. https://doi.org/10.1016/j.scitotenv.2016.09.009
Kirkpatrick CJ, Mohr W, Haferkamp O (1982) The effects of nickel ions on articular chondrocyte growth in monolayer culture. Res Exp Med (berl) 181(3):259–264. https://doi.org/10.1007/BF01851199
Korbas M, Macdonald TC, Pickering IJ, George GN, Krone PH (2012) Chemical form matters: differential accumulation of mercury following inorganic and organic mercury exposures in zebrafish larvae. ACS Chem Biol 7(2):411–420. https://doi.org/10.1021/cb200287c
Kosik-Bogacka DI, Lanocha-Arendarczyk N, Kot K, Ciosek Z, Zietek P, Karaczun M, Pilarczyk B, Tomza-Marciniak A, Podlasinska J, Kalisinska E, Pyzia J (2017) Effects of biological factors and health condition on mercury and selenium concentrations in the cartilage, meniscus and anterior cruciate ligament. J Trace Elem Med Biol 44:201–208. https://doi.org/10.1016/j.jtemb.2017.08.008
Kosik-Bogacka DI, Lanocha-Arendarczyk N, Kot K, Zietek P, Karaczun M, Prokopowicz A, Kupnicka P, Ciosek Z (2018) Calcium, magnesium, zinc and lead concentrations in the structures forming knee joint in patients with osteoarthritis. J Trace Elem Med Biol 50:409–414. https://doi.org/10.1016/j.jtemb.2018.08.007
Krishnan Y, Grodzinsky AJ (2018) Cartilage diseases. Matrix Biol 71–72:51–69. https://doi.org/10.1016/j.matbio.2018.05.005
Kulyar MF, Yao W, Ding Y, Du H, Li K, Zhang L, Li A, Huachun P, Waqas M, Mehmood K, Li J (2021) Cluster of differentiation 147 (CD147) expression is linked with thiram induced chondrocyte’s apoptosis via Bcl-2/Bax/Caspase-3 signalling in tibial growth plate under chlorogenic acid repercussion. Ecotoxicol Environ Saf 213:112059. https://doi.org/10.1016/j.ecoenv.2021.112059
Kulyar MF, Mo Q, Yao W, Ding Y, Yan Z, Du H, Pan H, Li K, Gao J, Shahzad M, Mansoor MK, Iqbal M, Waqas M, Akhtar M, Bhutta ZA, Li J (2022a) Chlorogenic acid suppresses miR-460a in the regulation of Bcl-2, causing interleukin-1β reduction in thiram exposed chondrocytes via caspase-3/caspase-7 pathway. Phytomedicine 104:154296. https://doi.org/10.1016/j.phymed.2022.154296
Kulyar MF, Yao W, Mo Q, Ding Y, Zhang Y, Gao J, Li K, Pan H, Nawaz S, Shahzad M, Mehmood K, Iqbal M, Akhtar M, Bhutta ZA, Waqas M, Li J, Qi D (2022b) Regulatory role of apoptotic and inflammasome related proteins and their possible functional aspect in thiram associated tibial dyschondroplasia of poultry. Animals (basel) 12(16):2028. https://doi.org/10.3390/ani12162028
Kung MH, Yukata K, O’Keefe RJ, Zuscik MJ (2012) Aryl hydrocarbon receptor-mediated impairment of chondrogenesis and fracture healing by cigarette smoke and benzo(a)pyrene. J Cell Physiol 227(3):1062–1070. https://doi.org/10.1002/jcp.22819
Lanocha N, Kalisińska E, Kosik-Bogacka D, Budis H, Sokołowski S, Bohatyrewicz A (2012a) Comparison of concentrations of lead and cadmium in various parts of the femur head in patients after arthroplasty of the hip joint in Northwest Poland. Biomed Environ Sci 25(5):577–582. https://doi.org/10.3967/0895-3988.2012.05.012
Lanocha N, Kalisinska E, Kosik-Bogacka DI, Budis H (2012b) Evaluation of dog bones in the indirect assessment of environmental contamination with trace elements. Biol Trace Elem Res 147(1–3):103–112. https://doi.org/10.1007/s12011-011-9315-3
Lee HG, Yang JH (2010) PKC-δ mediates TCDD-induced apoptosis of chondrocyte in ROS-dependent manner. Chemosphere 81(8):1039–1044
Lee HG, Yang JH (2012) PCB126 induces apoptosis of chondrocytes via ROS-dependent pathways. Osteoarthr Cartil 20(10):1179–1185. https://doi.org/10.1016/j.joca.2012.06.004
Lenkowski JR, McLaughlin KA (2010) Acute atrazine exposure disrupts matrix metalloproteinases and retinoid signaling during organ morphogenesis in Xenopus laevis. J Appl Toxicol 30(6):582–589. https://doi.org/10.1002/jat.1529
Li Z, Li A, Zhang J, Wang Y, Zhang H, Mehmood K, Lian Y, Iqbal M, Li J (2020) Identification and expression analysis of microRNAs in tibial growth plate of chicken through thiram toxicity. Environ Sci Pollut Res Int 27(6):6628–6636. https://doi.org/10.1007/s11356-019-06648-z
Li G, Xiong C, Xu W, Mei R, Cheng T, Yu X (2021) Factors affecting the aluminum, arsenic, cadmium and lead concentrations in the knee joint structures. Front Public Health 9:758074. https://doi.org/10.3389/fpubh.2021.758074
Lin YT, Lee YL, Jung CR, Jaakkola JJ, Hwang BF (2014) Air pollution and limb defects: a matched-pairs case-control study in Taiwan. Environ Res 132:273–280. https://doi.org/10.1016/j.envres.2014.04.028
Lindgren A, Danielsson BR, Dencker L, Vahter M (1984) Embryotoxicity of arsenite and arsenate: distribution in pregnant mice and monkeys and effects on embryonic cells in vitro. Acta Pharmacol Toxicol (copenh) 54(4):311–320. https://doi.org/10.1111/j.1600-0773.1984.tb01936.x
Litchfield TM, Ishikawa Y, Wu LN, Wuthier RE, Sauer GR (1998) Effect of metal ions on calcifying growth plate cartilage chondrocytes. Calcif Tissue Int 62(4):341–349. https://doi.org/10.1007/s002239900442
Liu J, Kapron CM (2010) Differential induction of MAP kinase signalling pathways by cadmium in primary cultures of mouse embryo limb bud cells. Reprod Toxicol 29(3):286–291. https://doi.org/10.1016/j.reprotox.2010.02.001
Liu X, Sakai H, Nishigori M, Suyama K, Nawaji T, Ikeda S, Nishigouchi M, Okada H, Matsushima A, Nose T, Shimohigashi M, Shimohigashi Y (2019) Receptor-binding affinities of bisphenol A and its next-generation analogs for human nuclear receptors. Toxicol Appl Pharmacol 377:114610. https://doi.org/10.1016/j.taap.2019.114610
Liu X, Li X, Tao Y, Li N, Ji M, Zhang X, Chen Y, He Z, Yu K, Yu Z (2020) TCDD inhibited the osteogenic differentiation of human fetal palatal mesenchymal cells through AhR and BMP-2/TGF-β/Smad signaling. Toxicology 431:152353. https://doi.org/10.1016/j.tox.2019.152353
Liu Z, Huang Y, Jin X, Liu L, Gu H (2022) PCB153 suppressed autophagy via PI3K/Akt/mTOR and RICTOR/Akt/mTOR signaling by the upregulation of microRNA-155 in rat primary chondrocytes. Toxicol Appl Pharmacol 449:116135. https://doi.org/10.1016/j.taap.2022.116135
Liu X, Hu M, Zhao W, Zhang Y, Meng B, Yang S, Peng Q, Zhang L, Wang J (2024) Cadmium promotes senescence of annulus fibrosus cells via activation of PI3K/Akt signaling pathway. Chin J Tissue Eng Res 28(8):1217
Loganathan BG, Masunaga S (2020) PCBs, dioxins, and furans human exposure and health effects. In: Loganathan BG, Masunaga S (eds) Handbook of toxicology of chemical warfare agents. Academic Press, Massachusetts, pp 267–278
López-Barrera LD, Díaz-Torres R, Macay AL, López-Reyes AG, Olmos SP, Ramírez-Noguera P (2019) Oxidative stress modulation induced by chitosan-glutathione nanoparticles in chondrocytes. Pharmazie 74(7):406–411. https://doi.org/10.1691/ph.2019.8166
Lu Y, Xu H, Jiang Y, Hu Z, Du R, Zhao X, Tian Y, Zhu Q, Zhang Y, Liu Y, Wang Y (2022) Comprehensive analysis of differently expression mRNA and non-coding RNAs, and their regulatory mechanisms on relationship in thiram-induced tibial dyschondroplasia in chicken. Ecotoxicol Environ Saf 242:113924. https://doi.org/10.1016/j.ecoenv.2022.113924
Lyche JL, Gutleb AC, Bergman A, Eriksen GS, Murk AJ, Ropstad E, Saunders M, Skaare JU (2009) Reproductive and developmental toxicity of phthalates. J Toxicol Environ Health B Crit Rev 12(4):225–249. https://doi.org/10.1080/10937400903094091
Macaulay LJ, Chen A, Rock KD, Dishaw LV, Dong W, Hinton DE, Stapleton HM (2015) Developmental toxicity of the PBDE metabolite 6-OH-BDE-47 in zebrafish and the potential role of thyroid receptor β. Aquat Toxicol 168:38–47. https://doi.org/10.1016/j.aquatox.2015.09.007
Mallah MA, Changxing L, Mallah MA, Noreen S, Liu Y, Saeed M, Xi H, Ahmed B, Feng F, Mirjat AA, Wang W, Jabar A, Naveed M, Li JH, Zhang Q (2022) Polycyclic aromatic hydrocarbon and its effects on human health: an overeview. Chemosphere 296:133948. https://doi.org/10.1016/j.chemosphere.2022.133948
Marques VB, Faria RA, Dos Santos L (2018) Overview of the pathophysiological implications of organotins on the endocrine system. Front Endocrinol (lausanne). 9:101. https://doi.org/10.3389/fendo.2018.00101
Martínez-Nava GA, Mendoza-Soto L, Fernández-Torres J, Zamudio-Cuevas Y, Reyes-Hinojosa D, Plata-Rodríguez R, Olivos-Meza A, Ruíz-Huerta EA, Armienta-Hernández MA, Hernández-Álvarez E, Vargas-Sandoval B, Landa-Solís C, Suárez-Ahedo C, Barbier OC, Narváez-Morales J, Del Razo LM, Camacho-Rea MC, Martínez-Flores K (2020) Effect of cadmium on the concentration of essential metals in a human chondrocyte micromass culture. J Trace Elem Med Biol 62:126614. https://doi.org/10.1016/j.jtemb.2020.126614
Matta C, Zakany R (2013) Calcium signalling in chondrogenesis: implications for cartilage repair. Front Biosci-Sch 5(1):305–324
Mehmood K, Zhang H, Jiang X, Yao W, Tong X, Iqbal MK, Rehman MU, Iqbal M, Waqas M, Qamar H, Zhang J, Li J (2019) Ligustrazine recovers thiram-induced tibial dyschondroplasia in chickens: involvement of new molecules modulating integrin beta 3. Ecotoxicol Environ Saf 168:205–211. https://doi.org/10.1016/j.ecoenv.2018.10.080
Meirer F, Pemmer B, Pepponi G, Zoeger N, Wobrauschek P, Sprio S, Tampieri A, Goettlicher J, Steininger R, Mangold S, Roschger P, Berzlanovich A, Hofstaetter JG, Streli C (2011) Assessment of chemical species of lead accumulated in tidemarks of human articular cartilage by X-ray absorption near-edge structure analysis. J Synchrotron Radiat 18(Pt 2):238–244. https://doi.org/10.1107/S0909049510052040
Meneely GA, Wyttenbach CR (1989) Effects of the organophosphate insecticides diazinon and parathion on bobwhite quail embryos: skeletal defects and acetylcholinesterase activity. J Exp Zool 252(1):60–70. https://doi.org/10.1002/jez.1402520109
Misawa M, Doull J, Uyeki EM (1982) Teratogenic effects of cholinergic insecticides in chick embryos III development of cartilage and bone. J Toxicol Environ Health 10(4–5):551–563. https://doi.org/10.1080/15287398209530276
Mo Q, Kulyar MF, Quan C, Ding Y, Zhang Y, Zhang L, Pan H, Li J (2023) Thiram-induced hyperglycemia causes tibial dyschondroplasia by triggering aberrant ECM remodeling via the gut-pancreas axis in broiler chickens. J Hazard Mater 444(Pt A):130368. https://doi.org/10.1016/j.jhazmat.2022.130368
Moore JM, Norris JM, Clark ML (2004) Exposure to air pollutants and rheumatoid arthritis biomarkers: a scoping review. Semin Arthritis Rheu. https://doi.org/10.1016/j.semarthrit.2024.152365
Newey PJ, Gorvin CM, Whyte MP, Thakker RV (2018) Introduction to genetics of skeletal and mineral metabolic diseases. In: Newey PJ, Gorvin CM, Whyte MP, Thakker RV (eds) Genetics of bone biology and skeletal disease. Academic Press, Massachusetts, pp 1–21
Nürnberger S, Marlovits S (2017) Cartilage biology: essentials and methods. Princ Bone Joint Res 2017:139–151
Nyffeler J, Chovancova P, Dolde X, Holzer AK, Purvanov V, Kindinger I, Kerins A, Higton D, Silvester S, van Vugt-Lussenburg BM, Glaab E (2018) A structure–activity relationship linking non-planar PCBs to functional deficits of neural crest cells: new roles for connexins. Arch Toxicol 92:1225–1247
Olufsen M, Arukwe A (2011) Developmental effects related to angiogenesis and osteogenic differentiation in salmon larvae continuously exposed to dioxin-like 3,3’,4,4’-tetrachlorobiphenyl (congener 77). Aquat Toxicol 105(3–4):669–680. https://doi.org/10.1016/j.aquatox.2011.09.005
Ou YC, Thompson SA, Ponce RA, Schroeder J, Kavanagh TJ, Faustman EM (1999) Induction of the cell cycle regulatory gene p21 (Waf1, Cip1) following methylmercury exposure in vitro and in vivo. Toxicol Appl Pharmacol 157(3):203–212. https://doi.org/10.1006/taap.1999.8685
Öznurlu Y, Özaydın T, Sur E, Özparlak H (2021) The effects of in ovo administered bisphenol A on tibial growth plate histology in chicken. Birth Defects Res 113(15):1130–1139. https://doi.org/10.1002/bdr2.1925
Pamphlett R, Kum Jew S (2019) Mercury Is taken up selectively by cells involved in joint, bone, and connective tissue disorders. Front Med 6:168. https://doi.org/10.3389/fmed.2019.00168
Powe DK, Dasmahapatra AK, Russell JL, Tchounwou PB (2018) Toxicity implications for early life stage Japanese medaka (Oryzias latipes) exposed to oxyfluorfen. Environ Toxicol 33(5):555–568. https://doi.org/10.1002/tox.22541
Rafiei H, Ashrafizadeh M (2018) Expression of collagen type II and osteocalcin genes in mesenchymal stem cells from rats treated with lead acetate II. Iranian J Toxicol 12(5):35–40
Rasaputra KS, Liyanage AB, Lay JO Jr, McCarthy FM, Rath NC (2010) Tibial dyschondroplasia-associated proteomic changes in chicken growth plate cartilage. Avian Dis 54(4):1166–1171. https://doi.org/10.1637/9384-050110-Reg.1
Rasaputra KS, Liyanage R, Lay JO Jr, Slavik MF, Rath NC (2013) Effect of thiram on avian growth plate chondrocytes in culture. J Toxicol Sci 38(1):93–101. https://doi.org/10.2131/jts.38.93
Rath NC, Huff WE, Bayyari GR, Balog JM (1995) Effect of thiram on chick chondrocytes in culture. J Toxicol Environ Health 44(3):369–376. https://doi.org/10.1080/15287399509531965
Rath NC, Huff WE, Balog JM, Huff GR (2004) Comparative efficacy of different dithiocarbamates to induce tibial dyschondroplasia in poultry. Poult Sci 83(2):266–274. https://doi.org/10.1093/ps/83.2.266
Rath NC, Richards MP, Huff WE, Huff GR, Balog JM (2005) Changes in the tibial growth plates of chickens with thiram-induced dyschondroplasia. J Comp Pathol 133(1):41–52. https://doi.org/10.1016/j.jcpa.2005.01.005
Rath NC, Huff WE, Huff GR (2007a) Thiram-induced changes in the expression of genes relating to vascularization and tibial dyschondroplasia. Poult Sci 86(11):2390–2395. https://doi.org/10.3382/ps.2007-00219
Rath NC, Huff WE, Huff GR, Kannan L (2007b) Induction of tibial dyschondroplasia by carbamate and thiocarbamate pesticides. Avian Dis 51(2):590–593. https://doi.org/10.1637/0005-2086(2007)51[590:IOTDBC]2.0.CO;2
Romereim SM, Conoan NH, Chen B, Dudley AT (2014) A dynamic cell adhesion surface regulates tissue architecture in growth plate cartilage. Development 141(10):2085–2095. https://doi.org/10.1242/dev.105452
Roschger A, Hofstaetter JG, Pemmer B, Zoeger N, Wobrauschek P, Falkenberg G, Simon R, Berzlanovich A, Thaler HW, Roschger P, Klaushofer K, Streli C (2013) Differential accumulation of lead and zinc in double-tidemarks of articular cartilage. Osteoarthr Cartil 21(11):1707–1715. https://doi.org/10.1016/j.joca.2013.06.029
Seemann F, Peterson DR, Witten PE, Guo BS, Shanthanagouda AH, Ye RR, Zhang G, Au DWT (2015) Insight into the transgenerational effect of benzo[a]pyrene on bone formation in a teleost fish (Oryzias latipes). Comp Biochem Physiol C Toxicol Pharmacol 178:60–67. https://doi.org/10.1016/j.cbpc.2015.10.001
Seemann F, Jeong CB, Zhang G, Wan MT, Guo B, Peterson DR, Lee JS, Au DW (2017) Ancestral benzo[a]pyrene exposure affects bone integrity in F3 adult fish (Oryzias latipes). Aquat Toxicol 183:127–134. https://doi.org/10.1016/j.aquatox.2016.12.018
Shankar P, Villeneuve DL (2023) AOP report: aryl hydrocarbon receptor activation leads to early-life stage mortality via Sox9 repression-induced craniofacial and cardiac malformations. Environ Toxicol Chem 42(10):2063–2077. https://doi.org/10.1002/etc.5699
Sharifi AM, Ghazanfari R, Tekiyehmaroof N, Sharifi MA (2011) Investigating the effect of lead acetate on rat bone marrow-derived mesenchymal stem cells toxicity: role of apoptosis. Toxicol Mech Method 21(3):225–230. https://doi.org/10.3109/15376516.2010.543943
Shearer JJ, Figueiredo Neto M, Umbaugh CS, Figueiredo ML (2017) In vivo exposure to inorganic arsenic alters differentiation-specific gene expression of adipose-derived mesenchymal stem/stromal cells in C57BL/6J mouse model. Toxicol Sci 157(1):172–182. https://doi.org/10.1093/toxsci/kfx026
Shen X, Liu W, Chen Y, Guo Y, Gao M, Chen W, Liu Y, Liu S (2019) Diagnostic significance of metallothionein members in recognizing cadmium exposure in various organs under low-dose exposure. Chemosphere 229:32–40. https://doi.org/10.1016/j.chemosphere.2019.04.192
Shi X, He C, Zuo Z, Li R, Chen D, Chen R, Wang C (2012) Pyrene exposure influences the craniofacial cartilage development of Sebastiscus marmoratus embryos. Mar Environ Res 77:30–34. https://doi.org/10.1016/j.marenvres.2012.01.003
Spector TD, MacGregor AJ (2004) Risk factors for osteoarthritis: genetics. Osteoarthr Cartil. https://doi.org/10.1016/j.joca.2003.09.005
Ströbel S, Loparic M, Wendt D, Schenk AD, Candrian C, Lindberg RL, Moldovan F, Barbero A, Martin I (2010) Anabolic and catabolic responses of human articular chondrocytes to varying oxygen percentages. Arthritis Res Ther 12(2):34. https://doi.org/10.1186/ar2942
Suminda GG, Min Y, Kim M, Heo Y, Do K, Son YO (2023) Hexavalent chromium induces cartilage degeneration and osteoarthritis pathogenesis. Exposure and Health 15(2):439–453
Suminda GGD, Min Y, Ha MW, Ghosh M, Lee DS, Son YO (2024) In vitro and in vivo investigations on arsenic-induced cartilage degeneration in osteoarthritis. J Hazard Mater 461:132570. https://doi.org/10.1016/j.jhazmat.2023.132570
Sun Q, Wu S, Liu K, Li Y, Mehmood K, Nazar M, Hu L, Pan J, Tang Z, Liao J, Zhang H (2023) miR-181b-1-3p affects the proliferation and differentiation of chondrocytes in TD broilers through the WIF1/Wnt/β-catenin pathway. Pestic Biochem Physiol 197:105649. https://doi.org/10.1016/j.pestbp.2023.105649
Tamura Y, Fuangtharnthip P, Uehara T, Iwamoto T, Waki Y (2021) Metallothionein expression in zinc-treated cartilage precursor ATDC5 cells. Biomed Res Trace Elem 32(1):23–29
Tang FH, Lenzen M, McBratney A, Maggi F (2021) Risk of pesticide pollution at the global scale. Nat Geosci 14(4):206–210
Tomaszewska E, Dobrowolski P, Winiarska-Mieczan A, Kwiecień M, Tomczyk A, Muszyński S, Radzki R (2016) Alteration in bone geometric and mechanical properties, histomorphometrical parameters of trabecular bone, articular cartilage, and growth plate in adolescent rats after chronic co-exposure to cadmium and lead in the case of supplementation with green, black, red and white tea. Environ Toxicol Pharmacol 46:36–44. https://doi.org/10.1016/j.etap.2016.06.027
Tomaszewska E, Dobrowolski P, Winiarska-Mieczan A, Kwiecień M, Muszyński S, Tomczyk A (2017a) The effect of tannic acid on bone mechanical and geometric properties, bone density, and trabecular histomorphometry as well as the morphology of articular and growth cartilages in rats co-exposed to cadmium and lead is dose dependent. Toxicol Ind Health 33(11):855–866. https://doi.org/10.1177/0748233717718973
Tomaszewska E, Dobrowolski P, Winiarska-Mieczan A, Kwiecień M, Tomczyk A, Muszyński S (2017b) The effect of tannic acid on the bone tissue of adult male Wistar rats exposed to cadmium and lead. Exp Toxicol Pathol 69(3):131–141. https://doi.org/10.1016/j.etp.2016.12.003
Tsai SC, Tseng YJ, Wu SM (2023) Reproductive and developmental alterations on zebrafish (Danio rerio) upon long-term exposure of di-ethyl phthalate (DEP), di-isononyl phthalate (DINP) and di (2-ethylhexyl) phthalate (DEHP). Bull Environ Contam Toxicol 110(2):49. https://doi.org/10.1007/s00128-023-03689-6
Tseng YJ, Chen TH, Tsai SC, Wu SM (2021) Effects of bisphenol A or diethyl phthalate on cartilage development and the swimming behavior of zebrafish (Danio rerio) through maternal exposure. Comp Biochem Physiol C Toxicol Pharmacol 247:109057. https://doi.org/10.1016/j.cbpc.2021.109057
Tseng YJ, Lu FI, Wu SM (2023) Generational effects and abnormalities in craniofacial chondrogenesis in zebrafish (Danio rerio) embryos upon maternal exposure to estrogen endocrine disrupting chemicals. Comp Biochem Physiol C Toxicol Pharmacol 273:109743. https://doi.org/10.1016/j.cbpc.2023.109743
Tussellino M, Ronca R, Carotenuto R, Pallotta MM, Furia M, Capriglione T (2016) Chlorpyrifos exposure affects fgf8, sox9, and bmp4 expression required for cranial neural crest morphogenesis and chondrogenesis in Xenopus laevis embryos. Environ Mol Mutagen 57(8):630–640. https://doi.org/10.1002/em.22057
Umlauf D, Frank S, Pap T, Bertrand J (2010) Cartilage biology, pathology, and repair. Cell Mol Life Sci 67(24):4197–4211. https://doi.org/10.1007/s00018-010-0498-0. (Epub 2010 Aug 25)
Uyeki EM, Nakanishi S, Fremming L (1986) Chromium effects on chondrocytic differentiation in vitro. J Toxicol Environ Health 19(1):137–145. https://doi.org/10.1080/15287398609530914
van Boxtel AL, Pieterse B, Cenijn P, Kamstra JH, Brouwer A, van Wieringen W, de Boer J, Legler J (2010) Dithiocarbamates induce craniofacial abnormalities and downregulate sox9a during zebrafish development. Toxicol Sci 117(1):209–217. https://doi.org/10.1093/toxsci/kfq169
Walker BS, Kramer AG, Lassiter CS (2018) Atrazine affects craniofacial chondrogenesis and axial skeleton mineralization in zebrafish (Danio rerio). Toxicol Ind Health 34(5):329–338. https://doi.org/10.1177/0748233718760419
Wang KC, Lin YF, Qin CH, Chen TL, Chen CH (2010) Bisphenol-A interferes with estradiol-mediated protection in osteoarthritic chondrocytes. Toxicol Lett 198(2):127–133. https://doi.org/10.1016/j.toxlet.2010.06.007
Wang Q, Li Y, Chen Y, Tian L, Gao D, Liao H, Kong C, Chen X, Junaid M, Wang J (2022) Toxic effects of polystyrene nanoplastics and polybrominated diphenyl ethers to zebrafish (Danio rerio). Fish Shellfish Immunol 126:21–33. https://doi.org/10.1016/j.fsi.2022.05.025
Waqas M, Qamar H, Zhang J, Yao W, Li A, Wang Y, Iqbal M, Mehmood K, Jiang X, Li J (2020) Puerarin enhance vascular proliferation and halt apoptosis in thiram-induced avian tibial dyschondroplasia by regulating HIF-1α, TIMP-3 and BCL-2 expressions. Ecotoxicol Environ Saf 190:110126. https://doi.org/10.1016/j.ecoenv.2019.110126
Watson AT, Planchart A, Mattingly CJ, Winkler C, Reif DM, Kullman SW (2017) From the cover: embryonic exposure to TCDD impacts osteogenesis of the axial skeleton in Japanese medaka Oryzias Latipes. Toxicol Sci 155(2):485–496. https://doi.org/10.1093/toxsci/kfw229
Webber RJ, Dollins SC, Harris M, Hough AJ Jr (1985) Effect of alkyltins on rabbit articular and growth-plate chondrocytes in monolayer culture. J Toxicol Environ Health 16(2):229–242. https://doi.org/10.1080/15287398509530736
Williams AE, Watt J, Robertson LW, Gadupudi G, Osborn ML, Soares MJ, Iqbal K, Pedersen KB, Shankar K, Littleton S, Maimone C, Eti NA, Suva LJ, Ronis MJJ (2020) Skeletal toxicity of coplanar polychlorinated biphenyl congener 126 in the rat is aryl hydrocarbon receptor dependent. Toxicol Sci 175(1):113–125. https://doi.org/10.1093/toxsci/kfaa030
Wright M, Jobanputra P, Bavington C, Salter DM, Nuki G (1996) Effects of intermittent pressure-induced strain on the electrophysiology of cultured human chondrocytes: evidence for the presence of stretch-activated membrane ion channels. Clin Sci (lond) 90(1):61–71. https://doi.org/10.1042/cs0900061
Wu CT, Lu TY, Chan DC, Tsai KS, Yang RS, Liu SH (2014) Effects of arsenic on osteoblast differentiation in vitro and on bone mineral density and microstructure in rats. Environ Health Perspect 122(6):559–565. https://doi.org/10.1289/ehp.1307832
Wu SM, Su CK, Shu LH (2018) Effects of calcium and estrogen on the development of the ceratohyal cartilage in zebrafish (Danio rerio) larvae upon embryo and maternal cadmium exposure. Comp Biochem Physiol C Toxicol Pharmacol 213:47–54. https://doi.org/10.1016/j.cbpc.2018.07.006
Xia Y, Momot KI, Chen Z, Chen CT, Kahn D, Badar F (2016) Introduction to cartilage. Xia Y, Momot KI, Chen Z, Chen CT, Kahn D, Badar F(Eds). Biophysics and biochemistry of cartilage by NMR and MRI. The Royal Society of Chemistry, London, pp 1–43
Xia F, Li Q, Luo X, Wu J (2022) Identification for heavy metals exposure on osteoarthritis among aging people and machine learning for prediction: a study based on NHANES 2011–2020. Front Public Health 10:906774. https://doi.org/10.3389/fpubh.2022.906774
Xiong KM, Peterson RE, Heideman W (2008) Aryl hydrocarbon receptor-mediated down-regulation of sox9b causes jaw malformation in zebrafish embryos. Mol Pharmacol 74(6):1544–1553. https://doi.org/10.1124/mol.108.050435
Xu Y, Gye MC (2018) Developmental toxicity of dibutyl phthalate and citrate ester plasticizers in Xenopus laevis embryos. Chemosphere 204:523–534. https://doi.org/10.1016/j.chemosphere.2018.04.077
Xu K, Zhang Y, Zheng J, Wang C, Chen R (2022) Comparative toxicity of 3–5 ringed polycyclic aromatic hydrocarbons to skeletal development in zebrafish embryos and the possible reason. Bull Environ Contam Toxicol 110(1):8. https://doi.org/10.1007/s00128-022-03644-x
Xu H, Jiang Y, Lu Y, Hu Z, Du R, Zhou Y, Liu Y, Zhao X, Tian Y, Yang C, Zhang Z, Qiu M, Wang Y (2024) Thiram exposure induces tibial dyschondroplasia in broilers via the regulation effect of circ_003084/miR-130c-5p/BMPR1A crosstalk on chondrocyte proliferation and differentiation. J Hazard Mater 465:133071. https://doi.org/10.1016/j.jhazmat.2023.133071
Yadav S, Shi Y, Wang F, Wang H (2010) Arsenite induces apoptosis in human mesenchymal stem cells by altering Bcl-2 family proteins and by activating intrinsic pathway. Toxicol Appl Pharmacol 244(3):263–272. https://doi.org/10.1016/j.taap.2010.01.001
Yan H, Hales BF (2019) Effects of organophosphate ester flame retardants on endochondral ossification in ex vivo murine limb bud cultures. Toxicol Sci 168(2):420–429. https://doi.org/10.1093/toxsci/kfy301
Yan H, Hales BF (2021) Effects of an environmentally relevant mixture of organophosphate esters derived from house dust on endochondral ossification in murine limb bud cultures. Toxicol Sci 180(1):62–75. https://doi.org/10.1093/toxsci/kfaa180
Yan R, Ding J, Yang Q, Zhang X, Han J, Jin T, Shi S, Wang X, Zheng Y, Li H, Zhang H, An Y (2023) Lead acetate induces cartilage defects and bone loss in zebrafish embryos by disrupting the GH/IGF-1 axis. Ecotoxicol Environ Saf 253:114666. https://doi.org/10.1016/j.ecoenv.2023.114666
Yang JH, Lee HG (2010) 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces apoptosis of articular chondrocytes in culture. Chemosphere 79(3):278–284. https://doi.org/10.1016/j.chemosphere.2010.01.040
Yao W, Zhang H, Fakhar-E-Alam Kulyar M, Ding Y, Waqas M, Mehmood K, Iqbal M, Du H, Jiang X, Li J (2020) Effect of total flavonoids of rhizoma drynariae in thiram induced cytotoxicity of chondrocyte via BMP-2/Runx2 and IHH/PTHrP expressions. Ecotoxicol Environ Saf 206:111194. https://doi.org/10.1016/j.ecoenv.2020.111194
Yao W, Kulyar MF, Ding Y, Du H, Hong J, Loon KS, Nawaz S, Li J (2023) The Effect of miR-140-5p with HDAC4 towards growth and differentiation signaling of chondrocytes in thiram-induced tibial dyschondroplasia. Int J Mol Sci 24(13):10975. https://doi.org/10.3390/ijms241310975
Yessica Eduviges ZC, Martínez-Nava G, Reyes-Hinojosa D, Mendoza-Soto L, Fernández-Torres J, López-Reyes A, Olivos-Meza A, Armienta-Hernández MA, Ruíz-Huerta EA, de Jesús G-G, Sandoval BV, Landa-Solís C, Sánchez-Sánchez R, Suarez-Ahedo C, Lozada-Pérez CA, Gutiérrez-Ruiz MC, Clavijo-Cornejo D, Pineda C, Jacobo-Albavera L, Domínguez-Pérez M, Martínez-Flores K (2020) Impact of cadmium toxicity on cartilage loss in a 3D in vitro model. Environ Toxicol Pharmacol 74:103307. https://doi.org/10.1016/j.etap.2019.103307
Yonemoto J, Shiraishi H, Soma Y (1993) In vitro assessment of teratogenic potential of organotin compounds using rat embryo limb bud cell cultures. Toxicol Lett 66(2):183–191. https://doi.org/10.1016/0378-4274(93)90093-d
Yoshikawa Y, Izawa T, Hamada Y, Takenaga H, Wang Z, Ishimaru N, Kamioka H (2021) Roles for B[a]P and FICZ in subchondral bone metabolism and experimental temporomandibular joint osteoarthritis via the AhR/Cyp1a1 signaling axis. Sci Rep 11(1):14927. https://doi.org/10.1038/s41598-021-94470-4
Yoshioka W, Tohyama C (2019) Mechanisms of developmental toxicity of dioxins and related compounds. Int J Mol Sci 20(3):617. https://doi.org/10.3390/ijms20030617
Yu Y, Yu L, Zhou X, Qiao N, Qu D, Tian F, Zhao J, Zhang H, Zhai Q, Chen W (2020) Effects of acute oral lead exposure on the levels of essential elements of mice: a metallomics and dose-dependent study. J Trace Elem Med Biol 62:126624. https://doi.org/10.1016/j.jtemb.2020.126624
Zhang J, Zuo Z, Sun P, Wang H, Yu A, Wang C (2012) Tributyltin exposure results in craniofacial cartilage defects in rockfish (Sebastiscus marmoratus) embryos. Mar Environ Res 77:6–11. https://doi.org/10.1016/j.marenvres.2011.12.008
Zhang H, Mehmood K, Jiang X, Yao W, Iqbal M, Waqas M, Rehman MU, Li A, Shen Y, Li J (2018) Effect of tetramethyl thiuram disulfide (thiram) in relation to tibial dyschondroplasia in chickens. Environ Sci Pollut Res Int 25(28):28264–28274. https://doi.org/10.1007/s11356-018-2824-2
Zhang H, Mehmood K, Jiang X, Li Z, Yao W, Zhang J, Tong X, Wang Y, Li A, Waqas M, Iqbal M, Li J (2019) Identification of differentially expressed MiRNAs profile in a thiram-induced tibial dyschondroplasia. Ecotoxicol Environ Saf 175:83–89. https://doi.org/10.1016/j.ecoenv.2019.03.043
Zhang Y, Chen Y, Xu K, Fang L, Huang J, Xia S, Zhou Q, Lv L, Wang C (2022a) Embryonic exposure to phenanthrene caused developmental defects of craniofacial cartilage in F1 larvae. Aquat Toxicol 243:106080. https://doi.org/10.1016/j.aquatox.2022.106080
Zhang Y, Ding Y, Mo Q, Kulyar MF, He Y, Yao W, Quan C, Gong S, Li F, Fu Y, Iqbal M, Xiao Y, Li J (2022b) Sodium butyrate ameliorates thiram-induced tibial dyschondroplasia and gut microbial dysbiosis in broiler chickens. Ecotoxicol Environ Saf 245:114134. https://doi.org/10.1016/j.ecoenv.2022.114134
Zhang Y, He L, Yang Y, Cao J, Su Z, Zhang B, Guo H, Wang Z, Zhang P, Xie J, Li J, Ye J, Zha Z, Yu H, Hong A, Chen X (2023) Triclocarban triggers osteoarthritis via DNMT1-mediated epigenetic modification and suppression of COL2A in cartilage tissues. J Hazard Mater 447:130747. https://doi.org/10.1016/j.jhazmat.2023.130747
Zheng S, Song H, Gao H, Liu C, Zhang Z, Fu J (2016) The antagonistic effect of selenium on lead-induced inflammatory factors and heat shock protein mRNA level in chicken cartilage tissue. Biol Trace Elem Res 173(1):177–184. https://doi.org/10.1007/s12011-016-0630-6
ZhitnikovMazhuga APM (1986) Changes in the metabolism of chondrocytes after chronic intake of phenol and lead. Arkh Anat Gistol Embriol 90(1):72–76
ZhitnikovMazhuga APM (1987) Reproductive kinetics of differentiating chondrocytes in normal states and in exposure to lead acetate. Tsitol Genet 21(4):248–252
ZhitnikovMazhuga APM (1988) Chondrocyte metabolism in growing and definitive cartilage exposed to lead acetate. Tsitol Genet 22(2):3–7
Zhou Y, Jiang R, An L, Wang H, Cheng S, Qiong S, Weng Y (2017) Benzo[a]pyrene impedes self-renewal and differentiation of mesenchymal stem cells and influences fracture healing. Sci Total Environ 587–588:305–315. https://doi.org/10.1016/j.scitotenv.2017.02.152
Zhu Z, Wang J, Cao Q, Liu S, Wei W, Yang H, Zhang Y (2022) Long-term BPA exposure leads to bone malformation and abnormal expression of MAPK/Wnt/FoxO signaling pathway genes in zebrafish offspring. Ecotoxicol Environ Saf 245:114082. https://doi.org/10.1016/j.ecoenv.2022.114082
Zoeger N, Roschger P, Hofstaetter JG, Jokubonis C, Pepponi G, Falkenberg G, Fratzl P, Berzlanovich A, Osterode W, Streli C, Wobrauschek P (2006) Lead accumulation in tidemark of articular cartilage. Osteoarthr Cartil 14(9):906–913. https://doi.org/10.1016/j.joca.2006.03.001
Zuscik MJ, Pateder DB, Edward Puzas J, Schwarz EM, Rosier RN, O’Keefe RJ (2002) Lead alters parathyroid hormone-related peptide and transforming growth factor-β1 effects and AP-1 and NF-κKB signaling in chondrocytes. J Orthop Res 20(4):811–818
Zuscik MJ, Ma L, Buckley T, Puzas JE, Drissi H, Schwarz EM, O’Keefe RJ (2007) Lead induces chondrogenesis and alters transforming growth factor-beta and bone morphogenetic protein signaling in mesenchymal cell populations. Environ Health Perspect 115(9):1276–1282. https://doi.org/10.1289/ehp.10028
Acknowledgements
The study was performed with the financial support of the Russian Science Foundation (project No. 24-45-00073) and National Natural Science Foundation of China (No. 82361138566).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Skalny, A.V., Aschner, M., Zhang, F. et al. Molecular mechanisms of environmental pollutant-induced cartilage damage: from developmental disorders to osteoarthritis. Arch Toxicol (2024). https://doi.org/10.1007/s00204-024-03772-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00204-024-03772-9