The role of chondrocyte mitochondrial biogenesis in the pathogenesis of osteoarthritis_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

ZHOU Shengliang , SI Haibo , PENG Linbo ,  SHEN Bin

Department of Orthopedics, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P. R. China;

Corresponding author：

SHEN Bin, Email: shenbin_1971@163.com

Keywords：

Osteoarthritis; chondrocytes; mitochondrial biogenesis; peroxisome proliferator-activated receptor-gamma coactivator 1 alpha

DOI：

10.7507/1002-1892.202109091

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the role of chondrocytes mitochondrial biogenesis in the pathogenesis of osteoarthritis (OA), and analyze the applications in the treatment of OA. Methods A review of recent literature was conducted to summarize the changes in mitochondrial biogenesis in the course of OA, the role of major signaling molecules in OA chondrocytes, and the prospects for OA therapeutic applications. Results Recent studies reveales that mitochondria are significant energy metabolic centers in chondrocytes and its dysfunction has been considered as an essential mechanism in the pathogenesis of OA. Mitochondrial biogenesis is one of the key processes maintaining the normal quantity and function of mitochondria, and peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1α) is the central regulator of this process. A regulatory network of mitochondrial biogenesis with PGC-1α as the center, adenosine monophosphate-activated protein kinase, sirtuin1/3, and cyclic adenosine monophosphate response element-binding protein as the main upstream regulatory molecules, and nuclear respiratory factor 1, estrogen-related receptor α, and nuclear respiratory factor 2 as the main downstream regulatory molecules has been reported. However, the role of mitochondrial biogenesis in OA chondrocytes still needs further validation and in-depth exploration. It has been demonstrated that substances such as puerarin and omentin-1 can retard the development of OA by activating the damaged mitochondrial biogenesis in OA chondrocytes, which proves the potential to be used in the treatment OA. Conclusion Mitochondrial biogenesis in chondrocytes plays an important role in the pathogenesis of OA, and further exploring the related mechanisms is of great clinical significance.

Citation： ZHOU Shengliang, SI Haibo, PENG Linbo, SHEN Bin. The role of chondrocyte mitochondrial biogenesis in the pathogenesis of osteoarthritis. Chinese Journal of Reparative and Reconstructive Surgery, 2022, 36(2): 242-248. doi: 10.7507/1002-1892.202109091 Copy

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10.	Blanco FJ, López-Armada MJ, Maneiro E. Mitochondrial dysfunction in osteoarthritis. Mitochondrion, 2004, 4(5-6): 715-728.
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1. Woolf AD, Pfleger B. Burden of major musculoskeletal conditions. Bull World Health Organ, 2003, 81(9): 646-656.
2. Loeser RF, Collins JA, Diekman BO. Ageing and the pathogenesis of osteoarthritis. Nat Rev Rheumatol, 2016, 12(7): 412-420.
3. Cram P, Lu X, Kates SL, et al. Total knee arthroplasty volume, utilization, and outcomes among Medicare beneficiaries, 1991-2010. JAMA, 2012, 308(12): 1227-1236.
4. Li PA, Hou X, Hao S. Mitochondrial biogenesis in neurodegeneration. J Neurosci Res, 2017, 95(10): 2025-2029.
5. Popov LD. Mitochondrial biogenesis: An update. J Cell Mol Med, 2020, 24(9): 4892-4899.
6. Jamwal S, Blackburn JK, Elsworth JD. Pparγ/pgc1α signaling as a potential therapeutic target for mitochondrial biogenesis in neurodegenerative disorders. Pharmacol Ther, 2021, 219: 107705. doi: 10.1016/j.pharmthera.2020.107705.
7. Jornayvaz FR, Shulman GI. Regulation of mitochondrial biogenesis. Essays in Biochem, 2010, 47: 69-84.
8. Mao X, Fu P, Wang L, et al. Mitochondria: Potential targets for osteoarthritis. Front Med (Lausanne), 2020, 7: 581402. doi: 10.3389/fmed.2020.581402.
9. Wang Y, Zhao X, Lotz M, et al. Mitochondrial biogenesis is impaired in osteoarthritis chondrocytes but reversible via peroxisome proliferator-activated receptor γ coactivator 1α. Arthritis Rheumatol, 2015, 67(8): 2141-2153.
10. Blanco FJ, López-Armada MJ, Maneiro E. Mitochondrial dysfunction in osteoarthritis. Mitochondrion, 2004, 4(5-6): 715-728.
11. Onuora S. Osteoarthritis: Chondrocyte clock maintains cartilage tissue. Nat Rev Rheumatol, 2016, 12(2): 71. doi: 10.1038/nrrheum.2015.183.
12. Mitrovic D, Quintero M, Stankovic A, et al. Cell density of adult human femoral condylar articular cartilage. Joints with normal and fibrillated surfaces. Lab Invest, 1983, 49(3): 309-316.
13. Blanco FJ, Guitian R, Vázquez-Martul E, et al. Osteoarthritis chondrocytes die by apoptosis. A possible pathway for osteoarthritis pathology. Arthritis Rheum, 1998, 41(2): 284-289.
14. Bullough PG. Osteoarthritis: pathogenesis and aetiology. Br J Rheumatol, 1984, 23(3): 166-169.
15. Otte P. Basic cell metabolism of articular cartilage. Manometric studies. Z Rheumatol, 1991, 50(5): 304-312.
16. Jahr H, Gunes S, Kuhn AR, et al. Bioreactor-controlled physoxia regulates TGF-β signaling to alter extracellular matrix synthesis by human chondrocytes. Int J Mol Sci, 2019, 20(7): 1715. doi: 10.3390/ijms20071715.
17. Wang Y, Chen LY, Liu-Bryan R. Mitochondrial biogenesis, activity, and DNA isolation in chondrocytes. Methods Mol Biol, 2021, 2245: 195-213.
18. Maneiro E, López-Armada MJ, de Andres MC, et al. Effect of nitric oxide on mitochondrial respiratory activity of human articular chondrocytes. Ann Rheum Dis, 2005, 64(3): 388-395.
19. Du K, Ramachandran A, McGill MR, et al. Induction of mitochondrial biogenesis protects against acetaminophen hepatotoxicity. Food Chem Toxicol, 2017, 108(Pt A): 339-350.
20. Murphy MP, Smith RA. Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Annu Rev Pharmacol Toxicol, 2007, 47: 629-656.
21. Coppi L, Ligorio S, Mitro N, et al. Pgc1s and beyond: Disentangling the complex regulation of mitochondrial and cellular metabolism. Int J Mol Sci, 2021, 22(13): 6913. doi: 10.3390/ijms22136913.
22. Fontecha-Barriuso M, Martin-Sanchez D, Martinez-Moreno JM, et al. The role of pgc-1α and mitochondrial biogenesis in kidney diseases. Biomolecules, 2020, 10(2): 347. doi: 10.3390/biom10020347.
23. Simmons EC, Scholpa NE, Schnellmann RG. Mitochondrial biogenesis as a therapeutic target for traumatic and neurodegenerative cns diseases. Exp Neurol, 2020, 329: 113309. doi: 10.1016/j.expneurol.2020.113309.
24. Dorn GW, Vega RB, Kelly DP. Mitochondrial biogenesis and dynamics in the developing and diseased heart. Genes Dev, 2015, 29(19): 1981-1991.
25. Zhao X, Petursson F, Viollet B, et al. Peroxisome proliferator-activated receptor γ coactivator 1α and foxo3a mediate chondroprotection by amp-activated protein kinase. Arthritis Rheumatol, 2014, 66(11): 3073-3082.
26. Wang J, Wang K, Huang C, et al. SIRT3 activation by dihydromyricetin suppresses chondrocytes degeneration via maintaining mitochondrial homeostasis. Int J Biol Sci, 2018, 14(13): 1873-1882.
27. Liu D, Cai ZJ, Yang YT, et al. Mitochondrial quality control in cartilage damage and osteoarthritis: New insights and potential therapeutic targets. Osteoarthritis Cartilage, 2021. doi: 10.1016/j.joca.2021.10.009.
28. Soto-Hermida A, Fernández-Moreno M, Pértega-Díaz S, et al. Mitochondrial DNA haplogroups modulate the radiographic progression of spanish patients with osteoarthritis. Rheumatol Int, 2015, 35(2): 337-344.
29. Wang J, Li J, Song D, et al. Ampk: Implications in osteoarthritis and therapeutic targets. Am J Transl Res, 2020, 12(12): 7670-7681.
30. Hardie DG. AMP-activated protein kinase: maintaining energy homeostasis at the cellular and whole-body levels. Annu Rev Nutr, 2014, 34: 31-55.
31. Herzig S, Shaw RJ. AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol, 2018, 19(2): 121-135.
32. Carling D, Zammit VA, Hardie DG. A common bicyclic protein kinase cascade inactivates the regulatory enzymes of fatty acid and cholesterol biosynthesis. FEBS Lett, 1987, 223(2): 217-222.
33. Toyama EQ, Herzig S, Courchet J, et al. Metabolism. AMP-activated protein kinase mediates mitochondrial fission in response to energy stress. Science, 2016, 351(6270): 275-281.
34. Salminen A, Kaarniranta K. AMP-activated protein kinase (AMPK) controls the aging process via an integrated signaling network. Ageing Res Rev, 2012, 11(2): 230-241.
35. Liu-Bryan R. Inflammation and intracellular metabolism: new targets in OA. Osteoarthritis Cartilage, 2015, 23(11): 1835-1842.
36. Chen LY, Wang Y, Terkeltaub R, et al. Activation of AMPK-SIRT3 signaling is chondroprotective by preserving mitochondrial DNA integrity and function. Osteoarthritis Cartilage, 2018, 26(11): 1539-1550.
37. Terkeltaub R, Yang B, Lotz M, et al. Chondrocyte AMP-activated protein kinase activity suppresses matrix degradation responses to proinflammatory cytokines interleukin-1β and tumor necrosis factor α. Arthritis Rheum, 2011, 63(7): 1928-1937.
38. Matsuzaki T, Matsushita T, Takayama K, et al. Disruption of sirt1 in chondrocytes causes accelerated progression of osteoarthritis under mechanical stress and during ageing in mice. Ann Rheum Dis, 2014, 73(7): 1397-1404.
39. Tang BL. Sirt1 and the Mitochondria. Mol Cells, 2016, 39(2): 87-95.
40. Haigis MC, Guarente LP. Mammalian sirtuins-emerging roles in physiology, aging, and calorie restriction. Genes Dev, 2006, 20(21): 2913-2921.
41. Shen P, Lin W, Ba X, et al. Quercetin-mediated SIRT1 activation attenuates collagen-induced mice arthritis. J Ethnopharmacol, 2021, 279: 114213. doi: 10.1016/j.jep.2021.114213.
42. Onyango P, Celic I, McCaffery JM, et al. SIRT3, a human SIR2 homologue, is an NAD-dependent deacetylase localized to mitochondria. Proc Natl Acad Sci U S A, 2002, 99(21): 13653-13658.
43. Schwer B, North BJ, Frye RA, et al. The human silent information regulator (Sir)2 homologue hSIRT3 is a mitochondrial nicotinamide adenine dinucleotide-dependent deacetylase. J Cell Biol, 2002, 158(4): 647-657.
44. He Y, Wu Z, Xu L, et al. The role of SIRT3-mediated mitochondrial homeostasis in osteoarthritis. Cell Mol Life Sci, 2020, 77(19): 3729-3743.
45. He W, Newman JC, Wang MZ, et al. Mitochondrial sirtuins: regulators of protein acylation and metabolism. Trends Endocrinol Metab, 2012, 23(9): 467-476.
46. Almeida M, Porter RM. Sirtuins and FoxOs in osteoporosis and osteoarthritis. Bone, 2019, 121: 284-292.
47. Li Y, Ma Y, Song L, et al. SIRT3 deficiency exacerbates p53/Parkin-mediated mitophagy inhibition and promotes mitochondrial dysfunction: Implication for aged hearts. Int J Mol Med, 2018, 41(6): 3517-3526.
48. Torrens-Mas M, Pons DG, Sastre-Serra J, et al. SIRT3 silencing sensitizes breast cancer cells to cytotoxic treatments through an increment in ROS production. J Cell Biochem, 2017, 118(2): 397-406.
49. Puigserver P, Wu Z, Park CW, et al. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell, 1998, 92(6): 829-839.
50. Viña J, Gomez-Cabrera MC, Borras C, et al. Mitochondrial biogenesis in exercise and in ageing. Adv Drug Deliv Rev, 2009, 61(14): 1369-1374.
51. Virbasius JV, Scarpulla RC. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc Natl Acad Sci U S A, 1994, 91(4): 1309-1313.
52. Zhang X, Bu Y, Zhu B, et al. Global transcriptome analysis to identify critical genes involved in the pathology of osteoarthritis. Bone Joint Res, 2018, 7(4): 298-307.
53. Ekstrand MI, Falkenberg M, Rantanen A, et al. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum Mol Genet, 2004, 13(9): 935-944.
54. Larsson NG, Wang J, Wilhelmsson H, et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet, 1998, 18(3): 231-236.
55. Cotney J, McKay SE, Shadel GS. Elucidation of separate, but collaborative functions of the rRNA methyltransferase-related human mitochondrial transcription factors B1 and B2 in mitochondrial biogenesis reveals new insight into maternally inherited deafness. Hum Mol Genet, 2009, 18(14): 2670-2682.
56. Metodiev MD, Lesko N, Park CB, et al. Methylation of 12S rRNA is necessary for in vivo stability of the small subunit of the mammalian mitochondrial ribosome. Cell Metab, 2009, 9(4): 386-397.
57. Wu Z, Puigserver P, Andersson U, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell, 1999, 98(1): 115-124.
58. Yang ZF, Drumea K, Mott S, et al. GABP transcription factor (nuclear respiratory factor 2) is required for mitochondrial biogenesis. Mol Cell Biol, 2014, 34(17): 3194-3201.
59. Suliman HB, Carraway MS, Welty-Wolf KE, et al. Lipopolysaccharide stimulates mitochondrial biogenesis via activation of nuclear respiratory factor-1. J Biol Chem, 2003, 278(42): 41510-41518.
60. Mattingly KA, Ivanova MM, Riggs KA, et al. Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol Endocrinol, 2008, 22(3): 609-622.
61. Luo J, Sladek R, Carrier J, et al. Reduced fat mass in mice lacking orphan nuclear receptor estrogen-related receptor alpha. Mol Cell Biol, 2003, 23(22): 7947-7956.
62. Scarpulla RC. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev, 2008, 88(2): 611-638.
63. Schreiber SN, Emter R, Hock MB, et al. The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)-induced mitochondrial biogenesis. Proc Natl Acad Sci U S A, 2004, 101(17): 6472-6477.
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Chinese Journal of Reparative and Reconstructive Surgery

The role of chondrocyte mitochondrial biogenesis in the pathogenesis of osteoarthritis

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