USF1 promotes the development of knee osteoarthritis by activating the NF‑κB signaling pathway

Song,Xiandong; Zhu,Min; Li,Hao; Liu,Bo; Yan,Zhaowei; Wang,Weican; Li,Hongyi; Sun,Jiping; Li,Shixing

doi:10.3892/etm.2018.6608

USF1 promotes the development of knee osteoarthritis by activating the NF‑κB signaling pathway

Authors:
- Xiandong Song
- Min Zhu
- Hao Li
- Bo Liu
- Zhaowei Yan
- Weican Wang
- Hongyi Li
- Jiping Sun
- Shixing Li
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Affiliations: Department of Orthopedics, Hongqi Hospital Affiliated with Mudanjiang Medical University, Mudanjiang, Heilongjiang 157011, P.R. China, Department of Radiology, Hongqi Hospital Affiliated with Mudanjiang Medical University, Mudanjiang, Heilongjiang 157011, P.R. China
Published online on: August 14, 2018 https://doi.org/10.3892/etm.2018.6608
Pages: 3518-3524
Copyright: © Song et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The current study mainly aims to evaluate the expression pattern and underlying mechanism of upstream stimulating factor 1 (USF1) in the muscle tissues of knee osteoarthritis (KOA) patients. In accordance with previous findings, our data showed that muscle strength was significantly decreased in KOA patients compared with controls. Furthermore, several inflammatory factors, including tumor necrosis factor α (TNFα), IL‑8, IL‑6 and MCP‑1, were associated with reduced muscle strength in KOA patients. Not surprisingly, NF‑κB signaling was significantly activated in the muscle tissues of KOA patients compared with control individuals. Furthermore, we showed that USF1 was increased in the muscles of KOA patients compared with controls. More importantly, overexpression of USF1 in primary human skeletal muscle cells significantly increased the activation of NF‑κB signaling as well as the levels of pro‑inflammatory factors. In summary, we showed novel data that the upregulation of USF1 promoted NF‑κB activation‑induced inflammatory responses in muscle tissues of KOA patients.

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1	Michael JW, Schlüter-Brust KU and Eysel P: The epidemiology, etiology, diagnosis, and treatment of osteoarthritis of the knee. Dtsch Arztebl Int. 107:152–162. 2010.PubMed/NCBI
2	Richter F, Natura G, Löser S, Schmidt K, Viisanen H and Schaible HG: Tumor necrosis factor causes persistent sensitization of joint nociceptors to mechanical stimuli in rats. Arthritis Rheum. 62:3806–3814. 2010. View Article : Google Scholar : PubMed/NCBI
3	Park SK, Kobsar D and Ferber R: Relationship between lower limb muscle strength, self-reported pain and function, and frontal plane gait kinematics in knee osteoarthritis. Clin Biomech (Bristol, Avon). 38:68–74. 2016. View Article : Google Scholar : PubMed/NCBI
4	Macías-Hernández SI, Miranda-Duarte A, Ramírez-Mora I, Cortés-González S, Morones-Alba JD, Olascoaga-Gómez A, Coronado-Zarco R, Soria-Bastida MLA, Nava-Bringas TI and Cruz-Medina E: Knee muscle strength correlates with joint cartilage T2 relaxation time in young participants with risk factors for osteoarthritis. Clin Rheumatol. 35:2087–2092. 2016. View Article : Google Scholar : PubMed/NCBI
5	Ruhdorfer A, Wirth W and Eckstein F: Association of knee pain with a reduction in thigh muscle strength-a cross-sectional analysis including 4553 osteoarthritis initiative participants. Osteoarthritis Cartilage. 25:658–666. 2017. View Article : Google Scholar : PubMed/NCBI
6	Farrokhi S, Voycheck CA, Gustafson JA, Fitzgerald GK and Tashman S: Knee joint contact mechanics during downhill gait and its relationship with varus/valgus motion and muscle strength in patients with knee osteoarthritis. Knee. 23:49–56. 2016. View Article : Google Scholar : PubMed/NCBI
7	Sarkar D and Fisher PB: Molecular mechanisms of aging-associated inflammation. Cancer Lett. 236:13–23. 2006. View Article : Google Scholar : PubMed/NCBI
8	Peake J, Della Gatta P and Cameron-Smith D: Aging and its effects on inflammation in skeletal muscle at rest and following exercise-induced muscle injury. Am J Physiol Regul Integr Comp Physiol. 298:R1485–R1495. 2010. View Article : Google Scholar : PubMed/NCBI
9	Russell AP: Molecular regulation of skeletal muscle mass. Clin Exp Pharmacol Physiol. 37:378–384. 2010. View Article : Google Scholar : PubMed/NCBI
10	Buch A, Carmeli E, Boker LK, Marcus Y, Shefer G, Kis O, Berner Y and Stern N: Muscle function and fat content in relation to sarcopenia, obesity and frailty of old age-an overview. Exp Gerontol. 76:25–32. 2016. View Article : Google Scholar : PubMed/NCBI
11	Mishra SK and Misra V: Muscle sarcopenia: An overview. Acta Myol. 22:43–47. 2003.PubMed/NCBI
12	Zhang L, Handel MV, Schartner JM, Hagar A, Allen G, Curet M and Badie B: Regulation of IL-10 expression by upstream stimulating factor (USF-1) in glioma-associated microglia. J Neuroimmunol. 184:188–197. 2007. View Article : Google Scholar : PubMed/NCBI
13	Cheung E, Mayr P, Coda-Zabetta F, Woodman PG and Boam DS: DNA-binding activity of the transcription factor upstream stimulatory factor 1 (USF-1) is regulated by cyclin-dependent phosphorylation. Biochem J. 344:145–152. 1999. View Article : Google Scholar : PubMed/NCBI
14	Naukkarinen J, Gentile M, Soro-Paavonen A, Saarela J, Koistinen HA, Pajukanta P, Taskinen MR and Peltonen L: USF1 and dyslipidemias: Converging evidence for a functional intronic variant. Hum Mol Genet. 14:2595–2605. 2005. View Article : Google Scholar : PubMed/NCBI
15	Rada-Iglesias A, Ameur A, Kapranov P, Enroth S, Komorowski J, Gingeras TR and Wadelius C: Whole-genome maps of USF1 and USF2 binding and histone H3 acetylation reveal new aspects of promoter structure and candidate genes for common human disorders. Genome Res. 18:380–392. 2008. View Article : Google Scholar : PubMed/NCBI
16	Sellak H, Choi C, Browner N and Lincoln TM: Upstream stimulatory factors (USF-1/USF-2) regulate human cGMP-dependent protein kinase I gene expression in vascular smooth muscle cells. J Biol Chem. 280:18425–18433. 2005. View Article : Google Scholar : PubMed/NCBI
17	Malyankar UM, Hanson R, Schwartz SM, Ridall AL and Giachelli CM: Upstream stimulatory factor 1 regulates osteopontin expression in smooth muscle cells. Exp Cell Res. 250:535–547. 1999. View Article : Google Scholar : PubMed/NCBI
18	Irrcher I, Ljubicic V, Kirwan AF and Hood DA: AMP-activated protein kinase-regulated activation of the PGC-1alpha promoter in skeletal muscle cells. PLoS One. 3:e36142008. View Article : Google Scholar : PubMed/NCBI
19	Gustafsson T, Osterlund T, Flanagan JN, von Waldén F, Trappe TA, Linnehan RM and Tesch PA: Effects of 3 days unloading on molecular regulators of muscle size in humans. J Appl Physiol 1985. 109:721–727. 2010. View Article : Google Scholar : PubMed/NCBI
20	Huebner JL, Landerman LR, Somers TJ, Keefe FJ, Guilak F, Blumenthal JA, Caldwell DS and Kraus VB: Exploratory secondary analyses of a cognitive-behavioral intervention for knee osteoarthritis demonstrate reduction in biomarkers of adipocyte inflammation. Osteoarthritis Cartilage. 24:1528–1534. 2016. View Article : Google Scholar : PubMed/NCBI
21	Neogi T, Guermazi A, Roemer F, Nevitt MC, Scholz J, Arendt-Nielsen L, Woolf C, Niu J, Bradley LA, Quinn E and Law LF: Association of joint inflammation with pain sensitization in knee osteoarthritis: The multicenter osteoarthritis study. Arthritis Rheumatol. 68:654–661. 2016. View Article : Google Scholar : PubMed/NCBI
22	Henricsdotter C, Ellegaard K, Klokker L, Bartholdy C, Bandak E, Bartels EM, Bliddal H and Henriksen M: Changes in ultrasound assessed markers of inflammation following intra-articular steroid injection combined with exercise in knee osteoarthritis: Exploratory outcome from a randomized trial. Osteoarthritis Cartilage. 24:814–821. 2016. View Article : Google Scholar : PubMed/NCBI
23	Veronesi F, Giavaresi G, Maglio M, Scotto d'Abusco A, Politi L, Scandurra R, Olivotto E, Grigolo B, Borzì RM and Fini M: Chondroprotective activity of N-acetyl phenylalanine glucosamine derivative on knee joint structure and inflammation in a murine model of osteoarthritis. Osteoarthritis Cartilage. 25:589–599. 2017. View Article : Google Scholar : PubMed/NCBI
24	Rantanen T, Volpato S, Ferrucci L, Heikkinen E, Fried LP and Guralnik JM: Handgrip strength and cause-specific and total mortality in older disabled women: Exploring the mechanism. J Am Geriatr Soc. 51:636–641. 2003. View Article : Google Scholar : PubMed/NCBI
25	Hoeksma AF, ter Steeg AM, Nelissen RG, van Ouwerkerk WJ, Lankhorst GJ and de Jong BA: Neurological recovery in obstetric brachial plexus injuries: an historical cohort study. Dev Med Child Neurol. 46:76–83. 2004. View Article : Google Scholar : PubMed/NCBI
26	Franceschi C, Capri M, Monti D, Giunta S, Olivieri F, Sevini F, Panourgia MP, Invidia L, Celani L, Scurti M, et al: Inflammaging and anti-inflammaging: A systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev. 128:92–105. 2007. View Article : Google Scholar : PubMed/NCBI
27	Taekema DG, Westendorp RG, Frölich M and Gussekloo J: High innate production capacity of tumor necrosis factor-alpha and decline of handgrip strength in old age. Mech Ageing Dev. 128:517–521. 2007. View Article : Google Scholar : PubMed/NCBI
28	Gopinath SD and Rando TA: Stem cell review series: Aging of the skeletal muscle stem cell niche. Aging Cell. 7:590–598. 2008. View Article : Google Scholar : PubMed/NCBI
29	Cai D, Frantz JD, Tawa NE Jr, Melendez PA, Oh BC, Lidov HG, Hasselgren PO, Frontera WR, Lee J, Glass DJ and Shoelson SE: IKKbeta/NF-kappaB activation causes severe muscle wasting in mice. Cell. 119:285–298. 2004. View Article : Google Scholar : PubMed/NCBI
30	Hunter RB and Kandarian SC: Disruption of either the Nfkb1 or the Bcl3 gene inhibits skeletal muscle atrophy. J Clin Invest. 114:1504–1511. 2004. View Article : Google Scholar : PubMed/NCBI
31	Barradeau S, Imaizumi-Scherrer T, Weiss MC and Faust DM: Muscle-regulated expression and determinants for neuromuscular junctional localization of the mouse RIalpha regulatory subunit of cAMP-dependent protein kinase. Proc Natl Acad Sci USA. 98:5037–5042. 2001. View Article : Google Scholar : PubMed/NCBI
32	Whetstine JR, Witt TL and Matherly LH: The human reduced folate carrier gene is regulated by the AP2 and sp1 transcription factor families and a functional 61-base pair polymorphism. J Biol Chem. 277:43873–43880. 2002. View Article : Google Scholar : PubMed/NCBI
33	Apone S and Hauschka SD: Muscle gene E-box control elements. Evidence for quantitatively different transcriptional activities and the binding of distinct regulatory factors. J Biol Chem. 270:21420–21427. 1995. View Article : Google Scholar : PubMed/NCBI