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ORIGINAL RESEARCH

α-Chaconine Facilitates Chondrocyte Pyroptosis and Nerve Ingrowth to Aggravate Osteoarthritis Progression by Activating NF-κB Signaling

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Pages 5873-5888 | Received 16 Jul 2022, Accepted 30 Sep 2022, Published online: 17 Oct 2022

References

  • Nelson AE. Osteoarthritis year in review 2017: clinical. Osteoarthritis Cartilage. 2018;26(3):319–325. doi:10.1016/j.joca.2017.11.014
  • Hunter DJ, Bierma-Zeinstra S. Osteoarthritis. Lancet. 2019;393(10182):1745–1759. doi:10.1016/S0140-6736(19)30417-9
  • Charlier E, Deroyer C, Ciregia F, et al. Chondrocyte dedifferentiation and osteoarthritis (OA). Biochem Pharmacol. 2019;165:49–65. doi:10.1016/j.bcp.2019.02.036
  • Berenbaum F, Wallace IJ, Lieberman DE, Felson DT. Modern-day environmental factors in the pathogenesis of osteoarthritis. Nat Rev Rheumatol. 2018;14(11):674–681. doi:10.1038/s41584-018-0073-x
  • Sánchez Romero EA, Meléndez Oliva E, Alonso Pérez JL, et al. Relationship between the gut microbiome and osteoarthritis pain: review of the literature. Nutrients. 2021;13(3):716. doi:10.3390/nu13030716
  • McAlindon T, Felson DT. Nutrition: risk factors for osteoarthritis. Ann Rheum Dis. 1997;56(7):397–400. doi:10.1136/ard.56.7.397
  • Schrenk D, Bignami M, Bodin L, et al. Risk assessment of glycoalkaloids in feed and food, in particular in potatoes and potato-derived products. EFSA. 2020;18(8):e06222. doi:10.2903/j.efsa.2020.6222
  • Yang SA, Paek SH, Kozukue N, Lee KR, Kim JA. Alpha-chaconine, a potato glycoalkaloid, induces apoptosis of HT-29 human colon cancer cells through caspase-3 activation and inhibition of ERK 1/2 phosphorylation. Food Chem Toxicol. 2006;44(6):839–846. doi:10.1016/j.fct.2005.11.007
  • Friedman M. Potato glycoalkaloids and metabolites: roles in the plant and in the diet. J Agric Food Chem. 2006;54(23):8655–8681. doi:10.1021/jf061471t
  • Liu Q, Hebert JR, Shivappa N, et al. Inflammatory potential of diet and risk of incident knee osteoarthritis: a prospective cohort study. Arthritis Res Ther. 2020;22(1):209. doi:10.1186/s13075-020-02302-z
  • Iablokov V, Sydora BC, Foshaug R, et al. Naturally occurring glycoalkaloids in potatoes aggravate intestinal inflammation in two mouse models of inflammatory bowel disease. Dig Dis Sci. 2010;55(11):3078–3085. doi:10.1007/s10620-010-1158-9
  • Best vegetables for arthritis; 2022. Available from: https://www.arthritis.org/health-wellness/healthy-living/nutrition/healthy-eating/best-vegetables-for-arthritis#:~:text=Eggplants%2C%20peppers%2C%20tomatoes%20and%20potatoes%20are%20all%20members,some%20people%20claim%20aggravates%20arthritis%20pain%20and%20inflammation. Accessed August 31, 2022.
  • Langkilde S, Mandimika T, Schrøder M, et al. A 28-day repeat dose toxicity study of steroidal glycoalkaloids, alpha-solanine and alpha-chaconine in the Syrian Golden hamster. Food Chem Toxicol. 2009;47(6):1099–1108. doi:10.1016/j.fct.2009.01.045
  • Friedman M, Henika PR, Mackey BE. Effect of feeding solanidine, solasodine and tomatidine to non-pregnant and pregnant mice. Food Chem Toxicol. 2003;41(1):61–71. doi:10.1016/S0278-6915(02)00205-3
  • Stoppiello LA, Mapp PI, Wilson D, Hill R, Scammell BE, Walsh DA. Structural associations of symptomatic knee osteoarthritis. Arthritis Rheumatol. 2014;66(11):3018–3027. doi:10.1002/art.38778
  • Zeng N, Yan ZP, Chen XY, Ni GX. Infrapatellar fat pad and knee osteoarthritis. Aging Dis. 2020;11(5):1317–1328. doi:10.14336/AD.2019.1116
  • Kwon H, Brown WE, Lee CA, et al. Surgical and tissue engineering strategies for articular cartilage and meniscus repair. Nat Rev Rheumatol. 2019;15(9):550–570. doi:10.1038/s41584-019-0255-1
  • Zhu S, Zhu J, Zhen G, et al. Subchondral bone osteoclasts induce sensory innervation and osteoarthritis pain. J Clin Invest. 2019;129(3):1076–1093. doi:10.1172/JCI121561
  • Fang C, Guo JW, Wang YJ, et al. Diterbutyl phthalate attenuates osteoarthritis in ACLT mice via suppressing ERK/c-fos/NFATc1 pathway, and subsequently inhibiting subchondral osteoclast fusion. Acta Pharmacol Sin. 2022;43(5):1299–1310. doi:10.1038/s41401-021-00747-9
  • Jiang W, Jin Y, Zhang S, et al. PGE2 activates EP4 in subchondral bone osteoclasts to regulate osteoarthritis. Bone Res. 2022;10(1):27. doi:10.1038/s41413-022-00201-4
  • Lee KI, Choi S, Matsuzaki T, et al. FOXO1 and FOXO3 transcription factors have unique functions in meniscus development and homeostasis during aging and osteoarthritis. Proc Natl Acad Sci U S A. 2020;117(6):3135–3143. doi:10.1073/pnas.1918673117
  • Greene MA, Loeser RF. Aging-related inflammation in osteoarthritis. Osteoarthritis Cartilage. 2015;23(11):1966–1971. doi:10.1016/j.joca.2015.01.008
  • Jiang W, Wang H, Li YS, Luo W. Role of vasoactive intestinal peptide in osteoarthritis. J Biomed Sci. 2016;23(1):63. doi:10.1186/s12929-016-0280-1
  • Belluzzi E, Macchi V, Fontanella CG, et al. Infrapatellar fat pad gene expression and protein production in patients with and without osteoarthritis. Int J Mol Sci. 2020;21(17):6016. doi:10.3390/ijms21176016
  • Ozeki N, Koga H, Sekiya I. Degenerative meniscus in knee osteoarthritis: from pathology to treatment. Life. 2022;12(4):603. doi:10.3390/life12040603
  • Gram AM, Booty LM, Bryant CE; Chopping GSDMD. caspase-8 has joined the team of pyroptosis-mediating caspases. EMBO J. 2019;38(10):e102065. doi:10.15252/embj.2019102065
  • An S, Hu H, Li Y, Hu Y. Pyroptosis plays a role in osteoarthritis. Aging Dis. 2020;11(5):1146–1157. doi:10.14336/AD.2019.1127
  • Lin C, Liu L, Zeng C, et al. Activation of mTORC1 in subchondral bone preosteoblasts promotes osteoarthritis by stimulating bone sclerosis and secretion of CXCL12. Bone Res. 2019;7:5. doi:10.1038/s41413-018-0041-8
  • Hu Y, Chen X, Wang S, Jing Y, Su J. Subchondral bone microenvironment in osteoarthritis and pain. Bone Res. 2021;9(1):20. doi:10.1038/s41413-021-00147-z
  • Jimi E, Fei H, Nakatomi C. NF-κB signaling regulates physiological and pathological chondrogenesis. Int J Mol Sci. 2019;20(24):6275. doi:10.3390/ijms20246275
  • Choi MC, Jo J, Park J, Kang HK, Park Y. NF-κB signaling pathways in osteoarthritic cartilage destruction. Cells. 2019;8(7):734. doi:10.3390/cells8070734
  • Lepetsos P, Papavassiliou KA, Papavassiliou AG. Redox and NF-κB signaling in osteoarthritis. Free Radic Biol Med. 2019;132:90–100. doi:10.1016/j.freeradbiomed.2018.09.025
  • Paradisi A, Maisse C, Bernet A, et al. NF-kappaB regulates netrin-1 expression and affects the conditional tumor suppressive activity of the netrin-1 receptors. Gastroenterology. 2008;135(4):1248–1257. doi:10.1053/j.gastro.2008.06.080
  • Mandimika T, Baykus H, Vissers Y, et al. Differential gene expression in intestinal epithelial cells induced by single and mixtures of potato glycoalkaloids. J Agric Food Chem. 2007;55(24):10055–10066. doi:10.1021/jf0724320
  • Hu J, Zhou J, Wu J, et al. Loganin ameliorates cartilage degeneration and osteoarthritis development in an osteoarthritis mouse model through inhibition of NF-κB activity and pyroptosis in chondrocytes. J Ethnopharmacol. 2020;247:112261. doi:10.1016/j.jep.2019.112261
  • Glasson SS, Blanchet TJ, Morris EA. The surgical destabilization of the medial meniscus (DMM) model of osteoarthritis in the 129/SvEv mouse. Osteoarthritis Cartilage. 2007;15(9):1061–1069. doi:10.1016/j.joca.2007.03.006
  • Lim NH, Wen C, Vincent TL. Molecular and structural imaging in surgically induced murine osteoarthritis. Osteoarthritis Cartilage. 2020;28(7):874–884. doi:10.1016/j.joca.2020.03.016
  • Yu H, Yao S, Zhou C, et al. Morroniside attenuates apoptosis and pyroptosis of chondrocytes and ameliorates osteoarthritic development by inhibiting NF-κB signaling. J Ethnopharmacol. 2021;266:113447. doi:10.1016/j.jep.2020.113447
  • Timmins KA, Leech RD, Batt ME, Edwards KL. Running and knee osteoarthritis: a systematic review and meta-analysis. Am J Sports Med. 2017;45(6):1447–1457. doi:10.1177/0363546516657531
  • McGehee DS, Krasowski MD, Fung DL, Wilson B, Gronert GA, Moss J. Cholinesterase inhibition by potato glycoalkaloids slows mivacurium metabolism. Anesthesiology. 2000;93(2):510–519. doi:10.1097/00000542-200008000-00031
  • Alozie SO, Sharma RP, Salunkhe DK. Inhibition of rat cholinesterase isoenzymes in vitro and in vivo by the potato alkaloid, α-Chaconine1,2. J Food Biochem. 1978;2:3. doi:10.1111/j.1745-4514.1978.tb00621.x
  • Hellenäs KE, Nyman A, Slanina P, Lööf L, Gabrielsson J. Determination of potato glycoalkaloids and their aglycone in blood serum by high-performance liquid chromatography. Application to pharmacokinetic studies in humans. J Chromatogr. 1992;573(1):69–78. doi:10.1016/0378-4347(92)80476-7
  • Mandimika T, Baykus H, Poortman J, Garza C, Kuiper H, Peijnenburg A. Induction of the cholesterol biosynthesis pathway in differentiated Caco-2 cells by the potato glycoalkaloid alpha-chaconine. Food Chem Toxicol. 2007;45(10):1918–1927. doi:10.1016/j.fct.2007.04.009
  • Guilak F, Nims RJ, Dicks A, Wu CL, Meulenbelt I. Osteoarthritis as a disease of the cartilage pericellular matrix. Matrix Biol. 2018;71:40–50. doi:10.1016/j.matbio.2018.05.008
  • Schou WS, Ashina S, Amin FM, Goadsby PJ, Ashina M. Calcitonin gene-related peptide and pain: a systematic review. J Headache Pain. 2017;18(1):34. doi:10.1186/s10194-017-0741-2
  • Burr DB, Gallant MA. Bone remodelling in osteoarthritis. Nat Rev Rheumatol. 2012;8(11):665–673. doi:10.1038/nrrheum.2012.130
  • Chen Z, Ge Y, Zhou L, et al. Pain relief and cartilage repair by nanofat against osteoarthritis: preclinical and clinical evidence. Stem Cell Res Ther. 2021;12(1):477. doi:10.1186/s13287-021-02538-9
  • McAllister MJ, Chemaly M, Eakin AJ, Gibson DS, McGilligan VE. NLRP3 as a potentially novel biomarker for the management of osteoarthritis. Osteoarthritis Cartilage. 2018;26(5):612–619. doi:10.1016/j.joca.2018.02.901
  • Sharma AR, Jagga S, Lee SS, Nam JS. Interplay between cartilage and subchondral bone contributing to pathogenesis of osteoarthritis. Int J Mol Sci. 2013;14(10):19805–19830. doi:10.3390/ijms141019805
  • Matsuoka T, Yoshimatsu G, Sakata N, et al. Inhibition of NLRP3 inflammasome by MCC950 improves the metabolic outcome of islet transplantation by suppressing IL-1β and islet cellular death. Sci Rep. 2020;10(1):17920. doi:10.1038/s41598-020-74786-3
  • Guo R, Wang H, Cui N. Autophagy regulation on pyroptosis: mechanism and medical implication in sepsis. Mediators Inflamm. 2021;2021:9925059. doi:10.1155/2021/9925059
  • Vande Walle L, Lamkanfi M. Pyroptosis. Curr Biol. 2016;26(13):R568–R572. doi:10.1016/j.cub.2016.02.019
  • Sharma BR, Kanneganti TD. NLRP3 inflammasome in cancer and metabolic diseases. Nat Immunol. 2021;22(5):550–559. doi:10.1038/s41590-021-00886-5
  • Liu Z, Gan L, Xu Y, et al. Melatonin alleviates inflammasome-induced pyroptosis through inhibiting NF-κB/GSDMD signal in mice adipose tissue. J Pineal Res. 2017;63:1. doi:10.1111/jpi.12414
  • Yan Z, Qi W, Zhan J, et al. Activating Nrf2 signalling alleviates osteoarthritis development by inhibiting inflammasome activation. J Cell Mol Med. 2020;24(22):13046–13057. doi:10.1111/jcmm.15905
  • Mapp PI, Walsh DA. Mechanisms and targets of angiogenesis and nerve growth in osteoarthritis. Nat Rev Rheumatol. 2012;8(7):390–398. doi:10.1038/nrrheum.2012.80
  • Martel-Pelletier J, Barr AJ, Cicuttini FM, et al. Osteoarthritis. Nat Rev Dis Primers. 2016;2:16072. doi:10.1038/nrdp.2016.72
  • Li Z, Huang Z, Zhang H, et al. P2X7 receptor induces pyroptotic inflammation and cartilage degradation in osteoarthritis via NF-κB/NLRP3 crosstalk. Oxid Med Cell Longev. 2021;2021:8868361. doi:10.1155/2021/8868361
  • Chang SH, Mori D, Kobayashi H, et al. Excessive mechanical loading promotes osteoarthritis through the gremlin-1-NF-κB pathway. Nat Commun. 2019;10(1):1442. doi:10.1038/s41467-019-09491-5
  • Chen Z, Lin CX, Song B, et al. Spermidine activates RIP1 deubiquitination to inhibit TNF-α-induced NF-κB/p65 signaling pathway in osteoarthritis. Cell Death Dis. 2020;11(7):503. doi:10.1038/s41419-020-2710-y
  • Bowles RD, Mata BA, Bell RD, et al. In vivo luminescence imaging of NF-κB activity and serum cytokine levels predict pain sensitivities in a rodent model of osteoarthritis. Arthritis Rheumatol. 2014;66(3):637–646. doi:10.1002/art.38279
  • Muraki I, Rimm EB, Willett WC, Manson JE, Hu FB, Sun Q. Potato consumption and risk of type 2 diabetes: results from three prospective cohort studies. Diabetes Care. 2016;39(3):376–384. doi:10.2337/dc15-0547
  • Baur S, Frank O, Hausladen H, et al. Biosynthesis of α-solanine and α-chaconine in potato leaves (Solanum tuberosum L.) – a (13)CO(2) study. Food Chem. 2021;365:130461. doi:10.1016/j.foodchem.2021.130461
  • Yamashoji S, Matsuda T. Synergistic cytotoxicity induced by α-solanine and α-chaconine. Food Chem. 2013;141(2):669–674. doi:10.1016/j.foodchem.2013.03.104
  • Baker D, Keeler R, Gaffield W. Lesions of potato sprout and extracted potato sprout alkaloid toxicity in Syrian hamsters. J Toxicol Clin Toxicol. 1987;25(3):199–208. doi:10.3109/15563658708992624
  • Friedman M, Henika PR, Mackey BE. Feeding of potato, tomato and eggplant alkaloids affects food consumption and body and liver weights in mice. J Nutr. 1996;126(4):989–999. doi:10.1093/jn/126.4.989
  • Caldwell KA, Grosjean OK, Henika PR, Friedman M. Hepatic ornithine decarboxylase induction by potato glycoalkaloids in rats. Food Chem Toxicol. 1991;29(8):531–535. doi:10.1016/0278-6915(91)90045-9
  • Gaffield W, Keeler RF. Implication of C-5, C-6 unsaturation as a key structural factor in steroidal alkaloid-induced mammalian teratogenesis. Experientia. 1993;49(10):922–924. doi:10.1007/BF01952611
  • Friedman M, Rayburn JR, Bantle JA. Developmental toxicology of potato alkaloids in the frog embryo teratogenesis assay—Xenopus (FETAX). Food Chem Toxicol. 1991;29(8):537–547. doi:10.1016/0278-6915(91)90046-A