A high-fat diet has negative effects on tendon resident cells in an in vivo rat model.
Achilles tendon
Animal model
High-fat diet
Obesity
Journal
International orthopaedics
ISSN: 1432-5195
Titre abrégé: Int Orthop
Pays: Germany
ID NLM: 7705431
Informations de publication
Date de publication:
05 2022
05 2022
Historique:
received:
02
10
2021
accepted:
04
02
2022
pubmed:
25
2
2022
medline:
14
4
2022
entrez:
24
2
2022
Statut:
ppublish
Résumé
Tendinopathy is a major complication of diet-induced obesity. However, the effects of a high-fat diet (HFD) on tendon have not been well characterised. We aimed to determine: [1] the impact of a HFD on tendon properties and gene expression; and [2] whether dietary transition to a control diet (CD) could restore normal tendon health. Sprague-Dawley rats were randomised into three groups from weaning and fed either a: CD, HFD or HFD for 12 weeks and then CD thereafter (HF-CD). Biomechanical, histological and structural evaluation of the Achilles tendon was performed at 17 and 27 weeks of age. Tail tenocytes were isolated with growth rate and collagen production determined. Tenocytes and activated THP-1 cells were exposed to conditioned media (CM) of visceral adipose tissue explants, and gene expression was analysed. There were no differences in the biomechanical, histological or structural tendon properties between groups. However, tenocyte growth and collagen production were increased in the HFD group at 27 weeks. There was lower SOX-9 expression in the HFD and HF-CD groups at 17 weeks and higher expression of collagen-Iα1 and matrix metalloproteinase-13 in the HFD group at 27 weeks. THP-1 cells exposed to adipose tissue CM from animals fed a HFD or HF-CD had lower expression of Il-10 and higher expression of Il-1β. In this rodent model, a HFD negatively altered tendon cell characteristics. Dietary intervention restored some gene expression changes; however, adipose tissue secretions from the HF-CD group promoted an increased inflammatory state in macrophages. These changes may predispose tendon to injury and adverse events later in life.
Sections du résumé
BACKGROUND
Tendinopathy is a major complication of diet-induced obesity. However, the effects of a high-fat diet (HFD) on tendon have not been well characterised. We aimed to determine: [1] the impact of a HFD on tendon properties and gene expression; and [2] whether dietary transition to a control diet (CD) could restore normal tendon health.
METHODS
Sprague-Dawley rats were randomised into three groups from weaning and fed either a: CD, HFD or HFD for 12 weeks and then CD thereafter (HF-CD). Biomechanical, histological and structural evaluation of the Achilles tendon was performed at 17 and 27 weeks of age. Tail tenocytes were isolated with growth rate and collagen production determined. Tenocytes and activated THP-1 cells were exposed to conditioned media (CM) of visceral adipose tissue explants, and gene expression was analysed.
RESULTS
There were no differences in the biomechanical, histological or structural tendon properties between groups. However, tenocyte growth and collagen production were increased in the HFD group at 27 weeks. There was lower SOX-9 expression in the HFD and HF-CD groups at 17 weeks and higher expression of collagen-Iα1 and matrix metalloproteinase-13 in the HFD group at 27 weeks. THP-1 cells exposed to adipose tissue CM from animals fed a HFD or HF-CD had lower expression of Il-10 and higher expression of Il-1β.
CONCLUSIONS
In this rodent model, a HFD negatively altered tendon cell characteristics. Dietary intervention restored some gene expression changes; however, adipose tissue secretions from the HF-CD group promoted an increased inflammatory state in macrophages. These changes may predispose tendon to injury and adverse events later in life.
Identifiants
pubmed: 35201374
doi: 10.1007/s00264-022-05340-1
pii: 10.1007/s00264-022-05340-1
pmc: PMC9001221
doi:
Substances chimiques
Collagen
9007-34-5
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1181-1190Informations de copyright
© 2022. The Author(s).
Références
Upadhyay J, Farr O, Perakakis N, Ghaly W, Mantzoros C (2018) Obesity as a Disease. Med Clin North Am 102:13–33
doi: 10.1016/j.mcna.2017.08.004
pubmed: 29156181
Nantel J, Mathieu M-E, Prince F (2011) Physical activity and obesity: biomechanical and physiological key concepts. J Obes 2011:650230. https://doi.org/10.1155/2011/650230
doi: 10.1155/2011/650230
pubmed: 21113311
Anandacoomarasamy A, Caterson I, Sambrook P, Fransen M, March L (2008) The impact of obesity on the musculoskeletal system. Int J Obes 32:211–222
doi: 10.1038/sj.ijo.0803715
Pottie P, Presle N, Terlain B, Netter P, Mainard D, Berenbaum F (2006) Obesity and osteoarthritis: More complex than predicted! Ann Rheum Dis 65:1403–1405
doi: 10.1136/ard.2006.061994
pubmed: 17038451
pmcid: 1798356
Collins KH, Herzog W, MacDonald GZ, Reimer RA, Rios JL, Smith IC, Zernicke RF, Hart DA (2018) Obesity, metabolic syndrome, and musculoskeletal disease: Common inflammatory pathways suggest a central role for loss of muscle integrity. Front. Physiol. 9
Macchi M, Spezia M, Elli S, Schiaffini G, Chisari E (2020) Obesity Increases the Risk of Tendinopathy, Tendon Tear and Rupture, and Postoperative Complications. Clin Orthop Relat Res 1. https://doi.org/10.1097/corr.0000000000001261
Abate M, Salini V, Andia I (2016) How obesity affects tendons? Advances in Experimental Medicine and Biology. Springer, New York LLC, pp 167–177
Scott A, Zwerver J, Grewal N, de Sa A, Alktebi T, Granville DJ, Hart DA (2015) Lipids, adiposity and tendinopathy: is there a mechanistic link? Critical review. Br J Sports Med 49:984–988. https://doi.org/10.1136/bjsports-2014-093989
doi: 10.1136/bjsports-2014-093989
pubmed: 25488953
Gaida JE, Alfredson H, Kiss ZS, Bass SL, Cook JL (2010) Asymptomatic Achilles tendon pathology is associated with a central fat distribution in men and a peripheral fat distribution in women: a cross sectional study of 298 individuals. BMC Musculoskelet Disord 11:41. https://doi.org/10.1186/1471-2474-11-41
doi: 10.1186/1471-2474-11-41
pubmed: 20196870
pmcid: 2841085
Holmes GB, Lin J (2006) Etiologic factors associated with symptomatic Achilles tendinopathy. Foot Ankle Int 27:952–959. https://doi.org/10.1177/107110070602701115
doi: 10.1177/107110070602701115
pubmed: 17144959
Klein EE, Weil L, Weil LS, Fleischer AE (2013) Body mass index and achilles tendonitis: a 10-year retrospective analysis. Foot Ankle Spec 6:276–282. https://doi.org/10.1177/1938640013489343
doi: 10.1177/1938640013489343
pubmed: 23687343
Scott RT, Hyer CF, Granata A (2013) The Correlation of Achilles Tendinopathy and Body Mass Index. Foot Ankle Spec 6:283–285. https://doi.org/10.1177/1938640013490019
doi: 10.1177/1938640013490019
pubmed: 23687344
Maffulli N, Testa V, Capasso G, Oliva F, Sullo A, Benazzo F, Regine R, King JB (2006) Surgery for chronic achilles tendinopathy yields worse results in nonathletic patients. Clin J Sport Med 16:123–128. https://doi.org/10.1097/00042752-200603000-00007
doi: 10.1097/00042752-200603000-00007
pubmed: 16603881
Firth EC, Haysom S, Vickers MH, Barker CN, McGlashan SR (2016) High-fat diet from weaning age induces defects in knee osteochondral junctions in young adult rats. Osteoarthr Cartil 24:S402–S403. https://doi.org/10.1016/j.joca.2016.01.728
doi: 10.1016/j.joca.2016.01.728
Collins KH, Hart DA, Reimer RA, Seerattan RA, Waters-Banker C, Sibole SC, Herzog W (2016) High-fat high-sucrose diet leads to dynamic structural and inflammatory alterations in the rat vastus lateralis muscle. J Orthop Res 34:2069–2078. https://doi.org/10.1002/jor.23230
doi: 10.1002/jor.23230
pubmed: 26990324
Conde J, Gomez R, Bianco G, Scotece M, Lear P, Dieguez C, Gomez-Reino J, Lago F, Gualillo O (2011) Expanding the adipokine network in cartilage: Identification and regulation of novel factors in human and murine chondrocytes. Ann Rheum Dis 70:551–559. https://doi.org/10.1136/ard.2010.132399
doi: 10.1136/ard.2010.132399
pubmed: 21216818
Berry PA, Jones SW, Cicuttini FM, Wluka AE, Maciewicz RA (2011) Temporal relationship between serum adipokines, biomarkers of bone and cartilage turnover, and cartilage volume loss in a population with clinical knee osteoarthritis. Arthritis Rheum 63:700–707. https://doi.org/10.1002/art.30182
doi: 10.1002/art.30182
pubmed: 21305502
Lago R, Gomez R, Otero M, Lago F, Gallego R, Dieguez C, Gomez-Reino JJ, Gualillo O (2008) A new player in cartilage homeostasis: adiponectin induces nitric oxide synthase type II and pro-inflammatory cytokines in chondrocytes. Osteoarthr Cartil 16:1101–1109. https://doi.org/10.1016/j.joca.2007.12.008
doi: 10.1016/j.joca.2007.12.008
Gaida JE, Alfredson L, Kiss ZS, Wilson AM, Alfredson H, Cook JL (2009) Dyslipidemia in Achilles tendinopathy is characteristic of insulin resistance. Med Sci Sports Exerc 41:1194–1197. https://doi.org/10.1249/MSS.0b013e31819794c3
doi: 10.1249/MSS.0b013e31819794c3
pubmed: 19461549
Collins KH, Hart DA, Smith IC, Issler AM, Reimer RA, Seerattan RA, Rios JL, Herzog W (2017) Acute and chronic changes in rat soleus muscle after high-fat high-sucrose diet. Physiol Rep 5:e13270 . https://doi.org/10.14814/phy2.13270
Coelho M, Oliveira T, Fernandes R (2013) Biochemistry of adipose tissue: An endocrine organ. Arch Med Sci 9:191–200
doi: 10.5114/aoms.2013.33181
pubmed: 23671428
pmcid: 3648822
Snedeker JG, Foolen J (2017) Tendon injury and repair – A perspective on the basic mechanisms of tendon disease and future clinical therapy. Acta Biomater 63:18–36
doi: 10.1016/j.actbio.2017.08.032
pubmed: 28867648
Qin Z (2012) The use of THP-1 cells as a model for mimicking the function and regulation of monocytes and macrophages in the vasculature. Atherosclerosis 221:2–11
doi: 10.1016/j.atherosclerosis.2011.09.003
pubmed: 21978918
du Sert NP, Hurst V, Ahluwalia A, Alam S, Avey MT, Baker M, Browne WJ, Clark A, Cuthill IC, Dirnagl U, Emerson M, Garner P, Holgate ST, Howells DW, Karp NA, Lazic SE, Lidster K, MacCallum CJ, Macleod M, Pearl EJ, Petersen OH, Rawle F, Reynolds P, Rooney K, Sena ES, Silberberg SD, Steckler T, Würbel H (2020) The arrive guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol 18. https://doi.org/10.1371/journal.pbio.3000410
Bolam S, Park Y, Konar S, Callon K, Workman J, Monk A, Coleman B, Cornish J, Vickers M, Munro J, Musson D (2021) Obesity impairs enthesis healing after rotator cuff repair in a rat model. Am J Sports Med. https://doi.org/10.1177/03635465211049219
doi: 10.1177/03635465211049219
pubmed: 34694156
Eliasson P, Fahlgren A, Pasternak B, Aspenberg P (2007) Unloaded rat Achilles tendons continue to grow, but lose viscoelasticity. J Appl Physiol 103:459–463. https://doi.org/10.1152/japplphysiol.01333.2006
doi: 10.1152/japplphysiol.01333.2006
pubmed: 17412787
Eliasson P, Andersson T, Aspenberg P (2009) Rat Achilles tendon healing: Mechanical loading and gene expression. J Appl Physiol 107:399–407. https://doi.org/10.1152/japplphysiol.91563.2008
doi: 10.1152/japplphysiol.91563.2008
pubmed: 19541731
Musson DS, Tay ML, Chhana A, Pool B, Coleman B, Naot D, Cornish J (2017) Lactoferrin and parathyroid hormone are not harmful to primary tenocytes in vitro, but PDGF may be. Muscles Ligaments Tendons J 7:215–222 . https://doi.org/10.11138/mltj/2017.7.2.215
Lam YY, Janovská A, McAinch AJ, Belobrajdic DP, Hatzinikolas G, Game P, Wittert GA (2011) The use of adipose tissue-conditioned media to demonstrate the differential effects of fat depots on insulin-stimulated glucose uptake in a skeletal muscle cell line. Obes Res Clin Pract 5. https://doi.org/10.1016/j.orcp.2010.12.002
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
doi: 10.1006/meth.2001.1262
pubmed: 11846609
Nagakura R, Yamamoto M, Jeong J, Hinata N, Katori Y, Chang WJ, Abe S (2020) Switching of Sox9 expression during musculoskeletal system development. Sci Rep 10. https://doi.org/10.1038/s41598-020-65339-9
Grewal N, Thornton GM, Behzad H, Sharma A, Lu A, Zhang P, Reid WD, Granville DJ, Scott A (2014) Accumulation of oxidized LDL in the tendon tissues of C57BL/6 or apolipoprotein e knock-out mice that consume a high fat diet: Potential impact on tendon health. PLoS ONE 9:e114214. https://doi.org/10.1371/journal.pone.0114214
doi: 10.1371/journal.pone.0114214
pubmed: 25502628
pmcid: 4264764
Jones GC, Corps AN, Pennington CJ, Clark IM, Edwards DR, Bradley MM, Hazleman BL, Riley GP (2006) Expression profiling of metalloproteinases and tissue inhibitors of metalloproteinases in normal and degenerate human Achilles tendon. Arthritis Rheum 54:832–842. https://doi.org/10.1002/art.21672
doi: 10.1002/art.21672
pubmed: 16508964
Abate M, Oliva F, Schiavone C, Salini V (2012) Achilles tendinopathy in amateur runners: Role of adiposity (Tendinopathies and obesity). Muscles Ligaments Tendons J 2:44–48
pubmed: 23738273
pmcid: 3666497
Abate M, Schiavone C, Di Carlo L, Salini V (2012) Achilles tendon and plantar fascia in recently diagnosed type II diabetes: role of body mass index. Clin Rheumatol 31:1109–1113. https://doi.org/10.1007/s10067-012-1955-y
doi: 10.1007/s10067-012-1955-y
pubmed: 22349878
Wearing SC, Hooper SL, Grigg NL, Nolan G, Smeathers JE (2013) Overweight and obesity alters the cumulativetransverse strain in the Achilles tendon immediately following exercise. J Bodyw Mov Ther 17:316–321. https://doi.org/10.1016/j.jbmt.2012.11.004
doi: 10.1016/j.jbmt.2012.11.004
pubmed: 23768275
Eriksen C, Svensson RB, Scheijen J, Hag AMF, Schalkwijk C, Praet SFE, Schjerling P, Kjær M, Magnusson SP, Couppé C (2014) Systemic stiffening of mouse tail tendon is related to dietary advanced glycation end products but not high-fat diet or cholesterol. J Appl Physiol 117:840–847. https://doi.org/10.1152/japplphysiol.00584.2014
doi: 10.1152/japplphysiol.00584.2014
pubmed: 25103969
Boivin GP, Platt KM, Corbett J, Reeves J, Hardy AL, Elenes EY, Charnigo RJ, Hunter SA, Pearson KJ (2013) The effects of high-fat diet, branched-chain amino acids and exercise on female C57BL/6 mouse Achilles tendon biomechanical properties. Bone Joint Res 2:186–192. https://doi.org/10.1302/2046-3758.29.2000196
doi: 10.1302/2046-3758.29.2000196
pubmed: 24021530
pmcid: 3774102
Rios JL, Ko L, Joumaa V, Liu S, Diefenthaeler F, Sawatsky A, Hart DA, Reimer RA, Herzog W (2019) The mechanical and biochemical properties of tail tendon in a rat model of obesity: Effect of moderate exercise and prebiotic fibre supplementation. J Biomech 88:148–154. https://doi.org/10.1016/j.jbiomech.2019.03.031
doi: 10.1016/j.jbiomech.2019.03.031
pubmed: 30954249
David MA, Jones KH, Inzana JA, Zuscik MJ, Awad HA, Mooney RA (2014) Tendon repair is compromised in a high fat diet-induced mouse model of obesity and type 2 diabetes. PLoS ONE 9:e91234. https://doi.org/10.1371/journal.pone.0091234
doi: 10.1371/journal.pone.0091234
pubmed: 24658034
pmcid: 3962358
Novak ML, Koh TJ (2013) Macrophage phenotypes during tissue repair. J Leukoc Biol 93:875–881. https://doi.org/10.1189/jlb.1012512
doi: 10.1189/jlb.1012512
pubmed: 23505314
pmcid: 3656331