Repetitive mechanical stretching modulates IL-1β induced COX-2, MMP-1 expression, and PGE2 production in human patellar tendon fibroblasts
Open accessAbstract
While mechanical loading is known to be essential in maintaining tendon homeostasis, repetitive mechanical loading has also been implicated in the etiology of tendon overuse injuries. The purpose of this study was to determine whether cyclic mechanical stretching regulates inflammatory responses induced by interleukin-1beta (IL-1beta) treatment in human patellar tendon fibroblasts (HPTFs). HPTFs were grown in microgrooved silicone dishes, where they became elongated in shape and aligned with the microgrooves, which is similar to the shape and organization of tendon fibroblasts in vivo. Cyclic uniaxial stretching was then applied to silicone culture dishes with a 4% or 8% stretch at a stretching frequency of 0.5 Hz for a duration of 4 h in the presence or absence of 10 pM IL-1beta treatment. Non-stretched cells in the presence or absence of IL-1beta were used for controls, respectively. The expression of cyclooxygenase-2 (COX-2), matrix metalloproteinase-1 (MMP-1), and the production of prostaglandin E2 (PGE2) were measured. In the absence of stretching, it was found that 10 pM of IL-1beta markedly induced higher levels of COX-2, MMP-1 gene expression, and PGE2 production than non-treated cells. Furthermore, cells with 4% stretching decreased the COX-2 and MMP-1 gene expression and PGE2 production that were stimulated by IL-1beta, whereas cells with 8% stretching further increased these gene products and/or expression levels in addition to the effects of IL-1beta stimulation. Thus, the results suggest that repetitive, small-magnitude stretching is anti-inflammatory, whereas large-magnitude stretching is pro-inflammatory. Therefore, moderate exercise may be beneficial to reducing tendon inflammation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Even minor increments in mechanical strain result in activation of COX-2 and production of PGE2, the basic biochemical mechanisms underlying tissue injury, and also in production of interleukin-8.
“However, even minor increments in mechanical strain resulted and the activation of COX-2 and the production of PGE2, the basic biochemical mechanisms underlying tissue injury [54], and also in the production of interleukin-8 [65].”
From The pathophysiology of endometriosis and adenomyosis, tissue injury and repair (2009) · cites this paper as [54]
Following termination of unphysiological strain and healing, this process is down-regulated and local production of estrogen or up-regulation of estrogen-dependent genes ceases.
“Following termination of unphysiological strain and healing, this process is down-regulated and the local production of estrogen or up-regulation of estrogen-dependent genes ceases [54, 57].”
From The pathophysiology of endometriosis and adenomyosis, tissue injury and repair (2009) · cites this paper as [54]
Cites
Cyclooxygenase in biology and disease
Dubois, R. N., Abramson, S. B., Crofford, L., Gupta, R., Simon, L. S., Putte, L., & Lipsky, P. (1998) · The FASEB Journal · doi:10.1096/fasebj.12.12.1063 · Cited by 2,606 · see citing works
Prostanoid Receptors: Structures, Properties, and Functions
Narumiya, S., Sugimoto, Y., & Ushikubi, F. (1999) · Physiological Reviews · doi:10.1152/physrev.1999.79.4.1193 · Cited by 2,414 · see citing works
Role of Extracellular Matrix in Adaptation of Tendon and Skeletal Muscle to Mechanical Loading
Kjær, M. (2004) · Physiological Reviews · doi:10.1152/physrev.00031.2003 · Cited by 1,596 · see citing works
Baracos, V. E., Rodemann, H. P., Dinarello, C. A., & Goldberg, A. L. (1983) · New England Journal of Medicine · doi:10.1056/nejm198303103081002 · Cited by 687 · see citing works
Cytokine hypothesis of overtraining: a physiological adaptation to excessive stress?
SMITH, L. L. (2000) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200002000-00011 · Cited by 537 · see citing works
Patellar tendinopathy: some aspects of basic science and clinical management.
Khan, K. M., Maffulli, N., Coleman, B. D., Cook, J. L., & Taunton, J. E. (1998) · British Journal of Sports Medicine · doi:10.1136/bjsm.32.4.346 · Cited by 509 · see citing works
Etiology, diagnosis, and treatment of tendonitis: an analysis of the literature
Almekinders, L. C., & Temple, J. D. (1998) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199808000-00001 · Cited by 350 · see citing works
Specificity of endothelial cell reorientation in response to cyclic mechanical stretching
Wang, J. H., Goldschmidt‐Clermont, P. J., Wille, J. J., & Yin, F. C.-P. (2001) · Journal of Biomechanics · doi:10.1016/s0021-9290(01)00150-6 · Cited by 342 · see citing works
Self-citationDevelopments in Quantitative PCR
Orlando, C., Pinzani, P., & Pazzagli, M. (1998) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.1998.045 · Cited by 333 · see citing works
Fiorucci, S., Meli, R., Bucci, M., & Cirino, G. (2001) · Biochemical Pharmacology · doi:10.1016/s0006-2952(01)00747-x · Cited by 285 · see citing works
PDGF-BB, IGF-I and mechanical load stimulate DNA synthesis in avian tendon fibroblasts in vitro
Banes, A. J., Tsuzaki, M., Hu, P., Brigman, B. E., Brown, T., Almekinders, L. C., Lawrence, W., & Fischer, T. H. (1995) · Journal of Biomechanics · doi:10.1016/0021-9290(95)00098-4 · Cited by 221 · see citing works
Wang, J. H., Jia, F., Yang, G., Yang, S., Campbell, B. H., Stone, D. A., & Woo, S. L. (2003) · Connective Tissue Research · doi:10.1080/03008200390223909 · Cited by 191 · see citing works
Self-citationStretch and interleukin‐1β induce matrix metalloproteinases in rabbit tendon cells in vitro
Archambault, J. M., Tsuzaki, M., Herzog, W., & Banes, A. J. (2002) · Journal of Orthopaedic Research® · doi:10.1016/s0736-0266(01)00075-4 · Cited by 186 · see citing works
Nakatani, T., Marui, T., Hitora, T., Doita, M., Nishida, K., & Kurosaka, M. (2002) · Journal of Orthopaedic Research® · doi:10.1016/s0736-0266(02)00046-3 · Cited by 148 · see citing works
Wang, J. H., & Grood, E. S. (2000) · Connective Tissue Research · doi:10.3109/03008200009005639 · Cited by 138 · see citing works
Self-citationInflammatory Response of Human Tendon Fibroblasts to Cyclic Mechanical Stretching
Li, Z., Yang, G., Khan, M. H., Stone, D. A., Woo, S. L., & Wang, J. H. (2004) · The American Journal of Sports Medicine · doi:10.1177/0095399703258680 · Cited by 134 · see citing works
Self-citationCyclic Tensile Strain Acts as an Antagonist of IL-1β Actions in Chondrocytes
Xu, Z., Buckley, M. J., Evans, C. H., & Agarwal, S. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.1.453 · Cited by 117 · see citing works
Wang, J. H., Yang, G., Li, Z., & Shen, W. (2003) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2003.09.011 · Cited by 116 · see citing works
Self-citationGilroy, D. W., Tomlinson, A., & Willoughby, D. A. (1998) · Inflammation Research · doi:10.1007/s000110050285 · Cited by 101 · see citing works
Prostaglandin E2 Affects Proliferation and Collagen Synthesis by Human Patellar Tendon Fibroblasts
Çilli, F., Khan, M. H., Fu, F. H., & Wang, J. H. (2004) · Clinical Journal of Sport Medicine · doi:10.1097/00042752-200407000-00006 · Cited by 92 · see citing works
Self-citationChowdhury, T. T., Bader, D. L., & Lee, D. A. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.5311 · Cited by 90 · see citing works
Long, P., HU, J. L., Piesco, N. P., Buckley, M. J., & Agarwal, S. (2001) · Journal of Dental Research · doi:10.1177/00220345010800050601 · Cited by 89 · see citing works
Agarwal, S., Long, P., al., S. B. E. A. S. B. E., Piesco, N. P., Shree, A., & Gassner, R. J. (2003) · The FASEB Journal · doi:10.1096/fj.02-0901fje · Cited by 83 · see citing works
Yamaguchi, M., Shimizu, N., Goseki, T., Shibata, Y., Takiguchi, H., Iwasawa, T., & Abiko, Y. (1994) · Archives of Oral Biology · doi:10.1016/0003-9969(94)90019-1 · Cited by 76 · see citing works
Long, P., Liu, F., Piesco, N. P., Kapur, R., & Agarwal, S. (2002) · Bone · doi:10.1016/s8756-3282(02)00673-7 · Cited by 76 · see citing works
Growth Factor Effects on the Expression of Collagenase and TIMP‐1 in Periodontal Ligament Cells
Alvares, O., Klebe, R. J., Grant, G., & Cochran, D. L. (1995) · Journal of Periodontology · doi:10.1902/jop.1995.66.7.552 · Cited by 70 · see citing works
Patellar tendon matrix changes associated with aging and voluntary exercise
VAILAS, A. C., Pedrini, V., Pedrini‐Mille, A., & Holloszy, J. O. (1985) · Journal of Applied Physiology · doi:10.1152/jappl.1985.58.5.1572 · Cited by 70 · see citing works
Nitric oxide enhances cyclooxygenase activity in articular cartilage
Manfield, L., Jang, D., & Murrell, G. A. C. (1996) · Inflammation Research · doi:10.1007/bf02259612 · Cited by 68 · see citing works
Sun, H., & Yokota, H. (2002) · Matrix Biology · doi:10.1016/s0945-053x(02)00003-3 · Cited by 62 · see citing works
Role of cyclooxygenase-1 and -2 in health and disease.
Lipsky, P. E. (1999) · PubMed · Cited by 61 · see citing works
The activation of human fibroblast prostaglandin E production by interleukin 1
Newton, R. C., & Covington, M. B. (1987) · Cellular Immunology · doi:10.1016/0008-8749(87)90127-4 · Cited by 54 · see citing works
Adam, R. M., Borer, J. G., Williams, B. J., Eastham, J. A., Loughlin, K. R., & Freeman, M. R. (1999) · Endocrinology · doi:10.1210/endo.140.12.7221 · Cited by 49 · see citing works
Tewari, D. S., Qian, Y., Tewari, M., Pieringer, J., Thornton, R. D., Taub, R. A., & Mochan, E. (1994) · Archives of Oral Biology · doi:10.1016/0003-9969(94)90091-4 · Cited by 37 · see citing works
Wang, J., Jia, F., Yang, G., et al. (2003) · Connective Tissue Research · doi:10.1080/713713684 · Cited by 37 · see citing works
Self-citationFukuda, K., Ohtani, K., Dan, H., & Tanaka, S. (1995) · Inflammation Research · doi:10.1007/bf01782816 · Cited by 17 · see citing works
Adam, R. M. (1999) · Endocrinology · doi:10.1210/en.140.12.5866 · Cited by 13 · see citing works
Straub, R. H., & Cutolo, M. (2001) · Arthritis & Rheumatism · doi:10.1002/1529-0131(200103)44:3
Flagged first, then by citations
Cited by
Sorted by citations
Pathogenesis of tendinopathies: inflammation or degeneration?
Abate, M., Silbernagel, K. G., Siljeholm, C., Iorio, A. D., Amicis, D. D., Salini, V., Werner, S., & Paganelli, R. (2009) · Arthritis Research & Therapy · doi:10.1186/ar2723 · Cited by 571 · see citing works
Structure‐function relationships in tendons: a review
BENJAMIN, M., Kaiser, E., & Milz, S. (2008) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.00864.x · Cited by 510 · see citing works
The pathophysiology of endometriosis and adenomyosis, tissue injury and repair
Leyendecker, G., Wildt, L., & Mall, G. (2009) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-009-1191-0 · Cited by 418 · see citing works
“However, even minor increments in mechanical strain resulted and the activation of COX-2 and the production of PGE2, the basic biochemical mechanisms underlying tissue injury [ 54 ], and also in the production of interleukin-8 [65].”
BackgroundInfluentialMechanosensitive mechanisms in transcriptional regulation
Mammoto, A., Mammoto, T., & Ingber, D. E. (2012) · Journal of Cell Science · doi:10.1242/jcs.093005 · Cited by 393 · see citing works
Snedeker, J. G., & Foolen, J. (2017) · Acta Biomaterialia · doi:10.1016/j.actbio.2017.08.032 · Cited by 376 · see citing works
From mechanical loading to collagen synthesis, structural changes and function in human tendon
Kjær, M., Langberg, H., Heinemeier, K. M., Bayer, M. L., Hansen, M., Holm, L., Doessing, S., Kongsgaard, M., Krogsgaard, M. R., & Magnusson, S. P. (2009) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2009.00986.x · Cited by 344 · see citing works
The role of mechanobiology in tendon healing
Killian, M. L., Cavinatto, L., Galatz, L. M., & Thomopoulos, S. (2012) · Journal of Shoulder and Elbow Surgery · doi:10.1016/j.jse.2011.11.002 · Cited by 333 · see citing works
Mechanoactive Tenogenic Differentiation of Human Mesenchymal Stem Cells
Kuo, C. K., & Tuan, R. S. (2008) · Tissue Engineering Part A · doi:10.1089/ten.tea.2006.0415 · Cited by 305 · see citing works
Adenomyosis: Mechanisms and Pathogenesis
Zhai, J., Vannuccini, S., Petraglia, F., & Giudice, L. C. (2020) · Seminars in Reproductive Medicine · doi:10.1055/s-0040-1716687 · Cited by 331 · see citing works
Inflammation is Present in Early Human Tendinopathy
Millar, N. L., Hueber, A. J., Reilly, J. H., Xu, Y., Fazzi, U. G., Murrell, G. A. C., & McInnes, I. B. (2010) · The American Journal of Sports Medicine · doi:10.1177/0363546510372613 · Cited by 287 · see citing works
Mechanoregulation of gene expression in fibroblasts
Wang, J. H., Thampatty, B. P., Lin, J.-S., & Im, H. (2007) · Gene · doi:10.1016/j.gene.2007.01.014 · Cited by 267 · see citing works
Self-citationChen, J., Yin, Z., Shen, W., Chen, X., Heng, B. C., Zou, X., & Ouyang, H. W. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.08.011 · Cited by 241 · see citing works
HGF Mediates the Anti-inflammatory Effects of PRP on Injured Tendons
Zhang, J., Middleton, K. K., Fu, F. H., Im, H., & Wang, J. H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067303 · Cited by 214 · see citing works
Self-citationSkeletal muscle mechanics, energetics and plasticity
Lieber, R. L., Roberts, T. J., Blemker, S. S., Lee, S. S. M., & Herzog, W. (2017) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/s12984-017-0318-y · Cited by 183 · see citing works
The pathogenesis of Achilles tendinopathy: A systematic review
Magnan, B., Bondi, M., Pierantoni, S., & Samaila, E. M. (2014) · Foot and Ankle Surgery · doi:10.1016/j.fas.2014.02.010 · Cited by 177 · see citing works
Im, H., Muddasani, P., Natarajan, V., Schmid, T. M., Block, J. A., Davis, F. J., van Wijnen, A. J., & Loeser, R. F. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m609040200 · Cited by 176 · see citing works
Self-citationWhat are the validated animal models for tendinopathy?
Lui, P. P. Y., Maffulli, N., Rolf, C. G., & Smith, R. K. W. (2010) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2010.01164.x · Cited by 168 · see citing works
The Pathogenesis of Adenomyosis vis-à-vis Endometriosis
Guo, S.-W. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020485 · Cited by 165 · see citing works
“HIF-1α-induced COX-2 expression leads to elevated PGE2 levels, which can induce PGE2-mediated vascularization [87,88].”
BackgroundInfluentialSchulze-Tanzil, G. G., Al-Sadi, O., Wiegand, E., Ertel, W., Busch, C., Kohl, B., & Pufe, T. (2011) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2010.01265.x · Cited by 158 · see citing works
Mechanosignaling to the Cell Nucleus and Gene Regulation
Shivashankar, G. V. (2011) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-042910-155319 · Cited by 158 · see citing works
A new concept of endometriosis and adenomyosis, tissue injury and repair (TIAR)
Leyendecker, G., & Wildt, L. (2011) · hmbci · doi:10.1515/hmbci.2011.002 · Cited by 147 · see citing works
Deciphering the pathogenesis of tendinopathy: a three-stages process
Fu, S., Rolf, C. G., Cheuk, Y., Lui, P. P. Y., & Chan, K.-M. (2010) · BMC Sports Science Medicine and Rehabilitation · doi:10.1186/1758-2555-2-30 · Cited by 144 · see citing works
D’Addona, A., Maffulli, N., Formisano, S., & Rosa, D. (2017) · The Surgeon · doi:10.1016/j.surge.2017.04.004 · Cited by 140 · see citing works
Tian, F., Wang, J.-H., Zhang, Z., & Yang, J. (2020) · Biological Research · doi:10.1186/s40659-020-00275-6 · Cited by 134 · see citing works
Self-citationProgrammable mechanical stimulation influences tendon homeostasis in a bioreactor system
Wang, T., Lin, Z., Day, R. E., Gardiner, B. S., Landao‐Bassonga, E., Rubenson, J., Kirk, T. B., Smith, D. W., Lloyd, D. G., Hardisty, G., et al. (2012) · Biotechnology and Bioengineering · doi:10.1002/bit.24809 · Cited by 131 · see citing works
Resolving an inflammatory concept: The importance of inflammation and resolution in tendinopathy
Dakin, S. G., Dudhia, J., & Smith, R. K. W. (2014) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2014.01.007 · Cited by 129 · see citing works
O'Brien, E. J. O., Frank, C. B., Shrive, N. G., Hallgrímsson, B., & Hart, D. A. (2012) · International Journal of Experimental Pathology · doi:10.1111/j.1365-2613.2012.00829.x · Cited by 126 · see citing works
Thankam, F. G., Roesch, Z. K., Dilisio, M. F., Radwan, M. M., Kovilam, A. N., Gross, R. M., & Agrawal, D. K. (2018) · Scientific Reports · doi:10.1038/s41598-018-27250-2 · Cited by 121 · see citing works
Effect of bench press exercise intensity on muscle soreness and inflammatory mediators
Uchida, M. C., Nosaka, K., Ugrinowitsch, C., Yamashita, A. S., Martins, E., Moriscot, A. S., & Aoki, M. S. (2009) · Journal of Sports Sciences · doi:10.1080/02640410802632144 · Cited by 114 · see citing works
Histopathology of Rotator Cuff Tears
Longo, U. G., Berton, A., Khan, W. S., Maffulli, N., & Denaro, V. (2011) · Sports Medicine and Arthroscopy Review · doi:10.1097/jsa.0b013e318213bccb · Cited by 116 · see citing works
Popov, C., Burggraf, M., Kreja, L., Ignatius, A. A., Schieker, M., & Docheva, D. (2015) · BMC Molecular Biology · doi:10.1186/s12867-015-0036-6 · Cited by 112 · see citing works
Davis, M. E., Gumucio, J. P., Sugg, K. B., Bedi, A., & Mendias, C. L. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00137.2013 · Cited by 112 · see citing works
Chapter 7 Mechanobiology of Adult and Stem Cells
Wang, J. H., & Thampatty, B. P. (2008) · International review of cytology · doi:10.1016/s1937-6448(08)01207-0 · Cited by 111 · see citing works
Self-citationThe effect of mechanical load on degenerated soft tissue
Hammer, W. I. (2008) · Journal of Bodywork and Movement Therapies · doi:10.1016/j.jbmt.2008.03.007 · Cited by 111 · see citing works
Inactivity and Inflammation in the Critically Ill Patient
Winkelman, C. (2007) · Critical Care Clinics · doi:10.1016/j.ccc.2006.11.002 · Cited by 105 · see citing works
Thampatty, B. P., Li, H., Im, H., & Wang, J. H. (2006) · Gene · doi:10.1016/j.gene.2006.08.027 · Cited by 107 · see citing works
Self-citationBirukova, A. A., Fu, P., Xing, J., Yakubov, B., Cokic, I., & Birukov, K. G. (2010) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00263.2009 · Cited by 103 · see citing works
A systematic review of the histological and molecular changes in rotator cuff disease
Dean, B. J. F., Franklin, S. L., & Carr, A. J. (2012) · Bone and Joint Research · doi:10.1302/2046-3758.17.2000115 · Cited by 103 · see citing works
Dex, S., Alberton, P., Willkomm, L., Söllradl, T., Bago, S., Milz, S., Shakibaei, M., Ignatius, A. A., Bloch, W., Clausen‐Schaumann, H., et al. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.05.003 · Cited by 100 · see citing works
The roles of inflammatory mediators and immunocytes in tendinopathy
Tang, C., Chen, Y., Huang, J., Zhao, K., Chen, X., Yin, Z., Heng, B. C., Chen, W., & Shen, W. (2018) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2018.03.003 · Cited by 98 · see citing works
Chondrocyte Phenotype and Ectopic Ossification in Collagenase-induced Tendon Degeneration
Lui, P. P. Y., Fu, S., Chan, L.-S., Hung, L., & Chan, K.-M. (2008) · Journal of Histochemistry & Cytochemistry · doi:10.1369/jhc.2008.952143 · Cited by 98 · see citing works
In Vitro Innovation of Tendon Tissue Engineering Strategies
Citeroni, M. R., Ciardulli, M. C., Russo, V., Porta, G. D., Mauro, A., Khatib, M. E., Mattia, M. D., Galesso, D., Barbera, C., Forsyth, N. R., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186726 · Cited by 98 · see citing works
Tomás, A. R., Gonçalves, A. I., Paz, E., Freitas, P. P., Domingues, R. M. A., & Gomes, M. E. (2019) · Nanoscale · doi:10.1039/c9nr04355a · Cited by 96 · see citing works
Cell-material interactions in tendon tissue engineering
Lin, J., Zhou, W., Han, S., Bunpetch, V., Zhao, K., Liu, C., Yin, Z., & Ouyang, H. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.01.012 · Cited by 96 · see citing works
Bioreactor Design for Tendon/Ligament Engineering
Wang, T., Gardiner, B. S., Lin, Z., Rubenson, J., Kirk, T. B., Wang, A. W., Xu, J., Smith, D. W., Lloyd, D. G., & Zheng, M. (2012) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2012.0295 · Cited by 94 · see citing works
Dakin, S. G., Werling, D., Hibbert, A. P., Abayasekara, D. R. E., Young, N. J., Smith, R. K. W., & Dudhia, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032333 · Cited by 93 · see citing works
Gelberman, R. H., Linderman, S. W., Jayaram, R., Dikina, A. D., Sakiyama‐Elbert, S. E., Alsberg, E., Thomopoulos, S., & Shen, H. (2017) · Clinical Orthopaedics and Related Research · doi:10.1007/s11999-017-5369-7 · Cited by 89 · see citing works
Meltzer, K. R., & Standley, P. R. (2007) · PubMed · Cited by 91 · see citing works
Bosch, G., de Mos, M., van Binsbergen, R., van Schie, H. T. M., van de Lest, C. H. A., & van Weeren, P. R. (2009) · Equine Veterinary Journal · doi:10.2746/042516409x370766 · Cited by 91 · see citing works
The biophysical, biochemical, and biological toolbox for tenogenic phenotype maintenance in vitro
Spanoudes, K., Gaspar, D., Pandit, A. S., & Zeugolis, D. I. (2014) · Trends in biotechnology · doi:10.1016/j.tibtech.2014.06.009 · Cited by 91 · see citing works
Saini, K., Cho, S., Dooling, L. J., & Discher, D. E. (2020) · Matrix Biology · doi:10.1016/j.matbio.2019.06.001 · Cited by 90 · see citing works
Pelvic floor disorders following vaginal or cesarean delivery
Memon, H., & Handa, V. L. (2012) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e328357628b · Cited by 86 · see citing works
The Role of Mechanical Loading in Ligament Tissue Engineering
Benhardt, H. A., & Cosgriff‐Hernandez, E. (2009) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2008.0687 · Cited by 83 · see citing works
Marcos, R. L., Leal‐Junior, E. C. P., Arnold, G., Magnenet, V., Rahouadj, R., Wang, X., Demeurie, F., Magdalou, J., de Carvalho, M. H. C., & Lopes‐Martins, R. Á. B. (2012) · Journal of Orthopaedic Research® · doi:10.1002/jor.22156 · Cited by 83 · see citing works
The role of the immune system in tendon healing: a systematic review.
Chisari, E., Rehak, L., Khan, W., & Maffulli, N. (2020) · British Medical Bulletin · doi:10.1093/bmb/ldz040 · Cited by 76 · see citing works
Wang, C.-L., Zeng, L.-H., Zhang, T., Liu, J.-K., & Wang, W.-B. (2016) · Inflammation · doi:10.1007/s10753-016-0309-3 · Cited by 79 · see citing works
In vitro expansion affects the response of chondrocytes to mechanical stimulation
Das, R. H. J., Jahr, H., Verhaar, J. A. N., van der Linden, J. C., van Osch, G. J. V. M., & Weinans, H. (2007) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2007.07.014 · Cited by 74 · see citing works
Harmful Effects of Leukocyte-Rich Platelet-Rich Plasma on Rabbit Tendon Stem Cells In Vitro
Zhang, L., Chen, S., Chang, P., Bao, N., Yang, C., Ti, Y., Zhou, L., & Zhao, J. (2016) · The American Journal of Sports Medicine · doi:10.1177/0363546516644718 · Cited by 74 · see citing works
In vitro loading models for tendon mechanobiology
Wang, T., Chen, P., Zheng, M., Wang, A. W., Lloyd, D. G., Leys, T., Zheng, Q., & Zheng, M. (2017) · Journal of Orthopaedic Research® · doi:10.1002/jor.23752 · Cited by 73 · see citing works
Engineering of extensor tendon complex by an ex vivo approach
Wang, B., Liu, W., Zhang, Y., Jiang, Y., Zhang, W. J., Zhou, G., Cui, L., & Cao, Y. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2008.03.038 · Cited by 73 · see citing works
Genes and Musculoskeletal Soft-Tissue Injuries
Rahim, M., Collins, M., & September, A. V. (2016) · Medicine and sport science/Medicine and sport · doi:10.1159/000445243 · Cited by 71 · see citing works
Donnelly, E. L., Ascenzi, M., & Farnum, C. E. (2009) · Journal of Orthopaedic Research® · doi:10.1002/jor.20946 · Cited by 71 · see citing works
Tendon tissue engineering: progress, challenges, and translation to the clinic.
Shearn, J. T., Kinneberg, K. R. C., Dyment, N. A., Galloway, M. T., Kenter, K., Wylie, C. C., & Butler, D. L. (2011) · PubMed · Cited by 71 · see citing works
Sun, Q., Liu, L., Roth, M., Tian, J., He, Q., Zhong, B., Bao, R., Lan, X., Jiang, C., Sun, J., et al. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402465 · Cited by 70 · see citing works
Inflamm-Aging and Arachadonic Acid Metabolite Differences with Stage of Tendon Disease
Dakin, S. G., Dudhia, J., Werling, N. J., Werling, D., Abayasekara, D. R. E., & Smith, R. K. W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048978 · Cited by 70 · see citing works
Tozzi, P. (2015) · Journal of Bodywork and Movement Therapies · doi:10.1016/j.jbmt.2015.03.002 · Cited by 69 · see citing works
Models for the study of tendinopathy.
Dirks, R. C., & Warden, S. J. (2011) · PubMed · Cited by 69 · see citing works
Park, H., Nazhat, S. N., & Rosenzweig, D. H. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121606 · Cited by 68 · see citing works
Jones, E. R., Jones, G. C., Legerlotz, K., & Riley, G. P. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.06.019 · Cited by 69 · see citing works
Laraia, É. M. S., Silva, I. S., Pereira, D. M., dos Reis, F. A., Albertini, R., de Almeida, P., Leal‐Junior, E. C. P., & de Carvalho, P. D. T. C. (2012) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2012.01179.x · Cited by 67 · see citing works
Birukova, A. A., Tian, Y., Meliton, A. Y., Leff, A. R., Wu, T., & Birukov, K. G. (2012) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00292.2011 · Cited by 67 · see citing works
Tendon healing in presence of chronic low-level inflammation: a systematic review
Chisari, E., Rehak, L., Khan, W. S., & Maffulli, N. (2019) · British Medical Bulletin · doi:10.1093/bmb/ldz035 · Cited by 66 · see citing works
Tendon healing is adversely affected by low-grade inflammation
Chisari, E., Rehak, L., Khan, W. S., & Maffulli, N. (2021) · Journal of Orthopaedic Surgery and Research · doi:10.1186/s13018-021-02811-w · Cited by 65 · see citing works
Engineering Tendon: Scaffolds, Bioreactors, and Models of Regeneration
Youngstrom, D. W., & Barrett, J. G. (2015) · Stem Cells International · doi:10.1155/2016/3919030 · Cited by 62 · see citing works
Mechanotransduction in Skin Inflammation
Shutova, M. S., & Boehncke, W. (2022) · Cells · doi:10.3390/cells11132026 · Cited by 60 · see citing works
Human-Based Biological and Biomimetic Autologous Therapies for Musculoskeletal Tissue Regeneration.
Padilla, S., Sanchez, M., Orive, G., & Anitua, E. (2017) · Trends in Biotechnology · doi:10.1016/j.tibtech.2016.09.008 · Cited by 55 · see citing works
Chen, C., Li, D.-L., Chuang, A. D., Dash, B. S., & Chen, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222011215 · Cited by 56 · see citing works
Mesenchymal stem cells: An efficient cell therapy for tendon repair (Review)
Jiang, L., Lu, J., Chen, Y., Lyu, K., Long, L., Wang, X., Liu, T., & Li, S. (2023) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2023.5273 · Cited by 60 · see citing works
Relevance of bioreactors and whole tissue cultures for the translation of new therapies to humans
Peroglio, M., Gaspar, D., Zeugolis, D. I., & Alini, M. (2017) · Journal of Orthopaedic Research® · doi:10.1002/jor.23655 · Cited by 54 · see citing works
Wang, J. H., & Li, B. (2010) · BMC Sports Science Medicine and Rehabilitation · doi:10.1186/1758-2555-2-16 · Cited by 52 · see citing works
Self-citationAbrams, G. D., Luria, A., Carr, R. A., Rhodes, C., Robinson, W. H., & Sokolove, J. B. (2016) · Journal of Shoulder and Elbow Surgery · doi:10.1016/j.jse.2015.10.011 · Cited by 51 · see citing works
Jenssen, K. K., Lundgreen, K., Madsen, J. E., Kvakestad, R., Pripp, A. H., & Dimmen, S. (2018) · Arthroscopy The Journal of Arthroscopic and Related Surgery · doi:10.1016/j.arthro.2018.05.036 · Cited by 50 · see citing works
Biomechanical and biochemical protective effect of low-level laser therapy for Achilles tendinitis
Marcos, R. L., Arnold, G., Magnenet, V., Rahouadj, R., Magdalou, J., & Lopes‐Martins, R. Á. B. (2013) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2013.08.028 · Cited by 49 · see citing works
Towards an Understanding of the Genetics of Tendinopathy
September, A. V., Rahim, M., & Collins, M. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-33943-6_9 · Cited by 48 · see citing works
Current progress in growth factors and extracellular vesicles in tendon healing
Wang, Y., & Li, J. (2023) · International Wound Journal · doi:10.1111/iwj.14261 · Cited by 49 · see citing works
Whyte, W., Goswami, D., Wang, S. X., Fan, Y., Ward, N. A., Levey, R. E., Beatty, R., Robinson, S. T., Sheppard, D., O’Connor, R., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32147-w · Cited by 47 · see citing works
Chen, Y., Peng, S., Cen, H., Lin, Y., Huang, C., Chen, Y., Shan, H., Su, Y., & Zeng, L. (2019) · International Journal of Oncology · doi:10.3892/ijo.2019.4803 · Cited by 47 · see citing works
Soft robot–mediated autonomous adaptation to fibrotic capsule formation for improved drug delivery
Beatty, R., Mendez, K. L., Schreiber, L. H. J., Tarpey, R., Whyte, W., Fan, Y., Robinson, S. T., O’Dwyer, J., Simpkin, A. J., Tannian, J., et al. (2023) · Science Robotics · doi:10.1126/scirobotics.abq4821 · Cited by 47 · see citing works
Abraham, T., Fong, G., & Scott, A. (2011) · BMC Musculoskeletal Disorders · doi:10.1186/1471-2474-12-26 · Cited by 45 · see citing works
A proteomic analysis of engineered tendon formation under dynamic mechanical loading in vitro
Jiang, Y., Liu, H., Li, H., Wang, F., Cheng, K., Zhou, G., Zhang, W., Ye, M., Cao, Y., Liu, W., et al. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.02.033 · Cited by 45 · see citing works
Induction of IL-6 and MMP-8 in human periodontal fibroblasts by static tensile strain
Jacobs, C., Walter, C., Ziebart, T., Grimm, S., Meila, D., Krieger, E., & Wehrbein, H. (2013) · Clinical Oral Investigations · doi:10.1007/s00784-013-1032-1 · Cited by 45 · see citing works
Costa, F. R., Marques, M. R. C., Costa, V. C., Santos, G. S., Martins, R. A., Santos, M. D. S., Santana, M. H. A., Nallakumarasamy, A., Jeyaraman, M., Lana, J. V., et al. (2023) · Biomedicines · doi:10.3390/biomedicines11041061 · Cited by 44 · see citing works
Zhang, J., Nie, D., Rocha, J. L., Hogan, M. V., & Wang, J. H. (2018) · Journal of Tissue Engineering · doi:10.1177/2041731418801103 · Cited by 44 · see citing works
Self-citationImmobilization After Rotator Cuff Repair
Hsu, J. E., Horneff, J. G., & Gee, A. O. (2015) · Orthopedic Clinics of North America · doi:10.1016/j.ocl.2015.08.017 · Cited by 43 · see citing works
Repetitive Mechanical Stretch Increases Extracellular Collagenase Activity in Vaginal Fibroblasts
Zong, W., Jallah, Z. C., Stein, S. E., Abramowitch, S. D., & Moalli, P. (2010) · Urogynecology · doi:10.1097/spv.0b013e3181ed30d2 · Cited by 42 · see citing works
Effect of training and sudden detraining on the patellar tendon and its enthesis in rats
Frizziero, A., Fini, M., Salamanna, F., Veicsteinas, A., Maffulli, N., & Marini, M. (2011) · BMC Musculoskeletal Disorders · doi:10.1186/1471-2474-12-20 · Cited by 42 · see citing works
Alda-1, an activator of ALDH2, ameliorates Achilles tendinopathy in cellular and mouse models
Liu, Y.-C., Wang, H., Huang, Y., Weng, Y.-H., Chen, R., Tsai, W., Yeh, T., Lu, C.-S., Chen, Y., Lin, Y.-W., et al. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.113919 · Cited by 41 · see citing works
Achilles tendon compositional and structural properties are altered after unloading by botox
Khayyeri, H., Blomgran, P., Hammerman, M., Turunen, M. J., Löwgren, A., Guizar‐Sicairos, M., Aspenberg, P., & Isaksson, H. (2017) · Scientific Reports · doi:10.1038/s41598-017-13107-7 · Cited by 41 · see citing works
Vashaghian, M., Diedrich, C. M., Zandieh‐Doulabi, B., Werner, A., Smit, T. H., & Roovers, J. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.11.034 · Cited by 42 · see citing works
Genetic stretching factors in masseter muscle after orthognathic surgery
Breuel, W., Krause, M., Schneider, M., & Harzer, W. (2012) · British Journal of Oral and Maxillofacial Surgery · doi:10.1016/j.bjoms.2012.11.009 · Cited by 40 · see citing works
- Authors
- Yang, G., Im, H.-J., & Wang, J. H.-C.
- Affiliations
- University of Pittsburgh (US)
- Rush University Medical Center (US)
- Corresponding author
- Wang, James H.-C.
- Venue
- Gene
- Publisher
- Elsevier BV
- Published
- 2005-12
- Volume
- 363
- Pages
- 166-172
- ISSN
- 0378-1119 (ISSN-L)
- PMC
- PMC2901527
- OpenAlex
- W2082252073
- Cited by
- 282
- References
- 36
- Citations by year
- 2026: 11 · 2025: 9 · 2024: 5 · 2023: 12 · 2022: 15 · 2021: 10 · 2020: 19 · 2019: 17 · 2018: 13 · 2017: 15 · 2016: 14 · 2015: 20 · 2014: 13 · 2013: 13 · 2012: 22
- FWCI
- 8.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Gene (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Veterans Affairs (I01BX002647)
- U.S. Public Health Service (049921)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR053220)
- Topics
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Tendon Structure and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Health Sciences › Medicine › Rheumatology › Osteoarthritis Treatment and Mechanisms
- Keywords
- IL-1β, cyclooxygenase-2, MMP-1, prostaglandin E2, tendon inflammation, tendon homeostasis, anti-inflammatory effects of exercise
- MeSH terms
- Adolescent, Adult, Base Sequence, Fibroblasts, Humans, Interleukin-1, Male, Patella, Physical Stimulation, Tendons, Dinoprostone, DNA Primers, Reverse Transcriptase Polymerase Chain Reaction, Matrix Metalloproteinase 1, Cyclooxygenase 2
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review