Autologous microfragmented adipose tissue reduces inflammatory and catabolic markers in supraspinatus tendon cells derived from patients affected by rotator cuff tears.
Mesenchymal stromal cells
Microfragmented adipose tissue
Paracrine action
Rotator cuff
Supraspinatus
Tendon
Journal
International orthopaedics
ISSN: 1432-5195
Titre abrégé: Int Orthop
Pays: Germany
ID NLM: 7705431
Informations de publication
Date de publication:
02 2021
02 2021
Historique:
received:
23
01
2020
accepted:
29
06
2020
pubmed:
10
7
2020
medline:
24
4
2021
entrez:
10
7
2020
Statut:
ppublish
Résumé
Rotator cuff tears are common musculoskeletal disorders, and surgical repair is characterized by a high rate of re-tear. Regenerative medicine strategies, in particular mesenchymal stem cell-based therapies, have been proposed to enhance tendon healing and reduce the re-tear rate. Autologous microfragmented adipose tissue (μFAT) allows for the clinical application of cell therapies and showed the ability to improve tenocyte proliferation and viability in previous in vitro assessments. The hypothesis of this study is that μFAT paracrine action would reduce the catabolic and inflammatory marker expression in tendon cells (TCs) derived from injured supraspinatus tendon (SST). TCs derived from injured SST were co-cultured with autologous μFAT in transwell for 48 h. Metabolic activity, DNA content, the content of soluble mediators in the media, and the gene expression of tendon-specific, inflammatory, and catabolic markers were analyzed. μFAT-treated TCs showed a reduced expression of PTGS2 and MMP-3 with respect to untreated controls. Increased IL-1Ra, VEGF, and IL-6 content were observed in the media of μFAT-treated samples, in comparison with untreated TCs. μFAT exerted an anti-inflammatory action on supraspinatus tendon cells in vitro through paracrine action, resulting in the reduction of catabolic and inflammatory marker expression. These observations potentially support the use of μFAT as adjuvant therapy in the treatment of rotator cuff disease.
Identifiants
pubmed: 32642826
doi: 10.1007/s00264-020-04693-9
pii: 10.1007/s00264-020-04693-9
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
419-426Références
Schmidt CC, Jarrett CD, Brown BT (2015) Management of Rotator Cuff Tears. J Hand Surg Am 40:399–408. https://doi.org/10.1016/j.jhsa.2014.06.122
doi: 10.1016/j.jhsa.2014.06.122
pubmed: 25557775
Svendsen SW, Frost P, Jensen LD (2012) Time trends in surgery for non-traumatic shoulder disorders and postoperative risk of permanent work disability: a nationwide cohort study. Scand J Rheumatol 41:59–65. https://doi.org/10.3109/03009742.2011.595375
doi: 10.3109/03009742.2011.595375
pubmed: 22103333
Colvin AC, Egorova N, Harrison AK et al (2012) National trends in rotator cuff repair. J Bone Joint Surg Am 94:227–233. https://doi.org/10.2106/JBJS.J.00739
doi: 10.2106/JBJS.J.00739
pubmed: 22298054
pmcid: 3262185
Chen M, Xu W, Dong Q et al (2013) Outcomes of single-row versus double-row arthroscopic rotator cuff repair: a systematic review and meta-analysis of current evidence. Arthroscopy 29:1437–1449. https://doi.org/10.1016/j.arthro.2013.03.076
doi: 10.1016/j.arthro.2013.03.076
pubmed: 23711754
Rhee YG, Cho NS, Yoo JH (2014) Clinical outcome and repair integrity after rotator cuff repair in patients older than 70 years versus patients younger than 70 years. Arthroscopy 30:546–554. https://doi.org/10.1016/j.arthro.2014.02.006
doi: 10.1016/j.arthro.2014.02.006
pubmed: 24630958
McElvany MD, McGoldrick E, Gee AO et al (2015) Rotator cuff repair: published evidence on factors associated with repair integrity and clinical outcome. Am J Sports Med 43:491–500. https://doi.org/10.1177/0363546514529644
doi: 10.1177/0363546514529644
pubmed: 24753240
Liu C-F, Aschbacher-Smith L, Barthelery NJ et al (2011) What we should know before using tissue engineering techniques to repair injured tendons: a developmental biology perspective. Tissue Eng Part B Rev 17:165–176. https://doi.org/10.1089/ten.TEB.2010.0662
doi: 10.1089/ten.TEB.2010.0662
pubmed: 21314435
pmcid: 3098959
Evans RB (2012) Managing the injured tendon: current concepts. J Hand Ther 25:173–189; quiz 190. https://doi.org/10.1016/j.jht.2011.10.004
doi: 10.1016/j.jht.2011.10.004
pubmed: 22326362
Hoppe S, Alini M, Benneker LM et al (2013) Tenocytes of chronic rotator cuff tendon tears can be stimulated by platelet-released growth factors. J Shoulder Elb Surg 22:340–349. https://doi.org/10.1016/j.jse.2012.01.016
doi: 10.1016/j.jse.2012.01.016
Weeks KD, Dines JS, Rodeo SA, Bedi A (2014) The basic science behind biologic augmentation of tendon-bone healing: a scientific review. Instr Course Lect 63:443–450
pubmed: 24720329
Abtahi AM, Granger EK, Tashjian RZ (2015) Factors affecting healing after arthroscopic rotator cuff repair. World J Orthop 6:211–220. https://doi.org/10.5312/wjo.v6.i2.211
doi: 10.5312/wjo.v6.i2.211
pubmed: 25793161
pmcid: 4363803
Randelli P, Randelli F, Ragone V et al (2014) Regenerative medicine in rotator cuff injuries. Biomed Res Int 2014. https://doi.org/10.1155/2014/129515
Murphy MB, Moncivais K, Caplan AI (2013) Mesenchymal stem cells: environmentally responsive therapeutics for regenerative medicine. Exp Mol Med 45:e54. https://doi.org/10.1038/emm.2013.94
doi: 10.1038/emm.2013.94
pubmed: 24232253
pmcid: 3849579
Abat F, Alfredson H, Cucchiarini M et al (2018) Current trends in tendinopathy: consensus of the ESSKA basic science committee. Part II: treatment options. J Exp Orthop 5. https://doi.org/10.1186/s40634-018-0145-5
Canapp SO, Canapp DA, Ibrahim V et al (2016) The use of adipose-derived progenitor cells and platelet-rich plasma combination for the treatment of supraspinatus tendinopathy in 55 dogs: a retrospective study. Front Vet Sci 3:61. https://doi.org/10.3389/fvets.2016.00061
doi: 10.3389/fvets.2016.00061
pubmed: 27668218
pmcid: 5016533
Jo CH, Chai JW, Jeong EC et al (2018) Intratendinous injection of autologous adipose tissue-derived mesenchymal stem cells for the treatment of rotator cuff disease: a first-in-human trial. Stem Cells 36:1441–1450. https://doi.org/10.1002/stem.2855
doi: 10.1002/stem.2855
pubmed: 29790618
Mussano F, Genova T, Corsalini M et al (2017) Cytokine, chemokine, and growth factor profile characterization of undifferentiated and osteoinduced human adipose-derived stem cells. Stem Cells Int 2017:6202783. https://doi.org/10.1155/2017/6202783
doi: 10.1155/2017/6202783
pubmed: 28572824
pmcid: 5442436
Salmikangas P, Schuessler-Lenz M, Ruiz S et al (2015) Marketing regulatory oversight of advanced therapy medicinal products (ATMPs) in Europe: the EMA/CAT perspective. Adv Exp Med Biol 871:103–130. https://doi.org/10.1007/978-3-319-18618-4_6
doi: 10.1007/978-3-319-18618-4_6
pubmed: 26374215
Guess AJ, Daneault B, Wang R et al (2017) Safety profile of good manufacturing practice manufactured interferon γ-primed mesenchymal stem/stromal cells for clinical trials. Stem Cells Transl Med 6:1868–1879. https://doi.org/10.1002/sctm.16-0485
doi: 10.1002/sctm.16-0485
pubmed: 28887912
pmcid: 6430053
Polancec D, Zenic L, Hudetz D et al (2019) Immunophenotyping of a stromal vascular fraction from microfragmented lipoaspirate used in osteoarthritis cartilage treatment and its lipoaspirate counterpart. Genes (Basel) 10. https://doi.org/10.3390/genes10060474
Nava S, Sordi V, Pascucci L et al (2019) Long-lasting anti-inflammatory activity of human microfragmented adipose tissue. Stem Cells Int 2019:5901479. https://doi.org/10.1155/2019/5901479
doi: 10.1155/2019/5901479
pubmed: 30915125
pmcid: 6399530
Paolella F, Manferdini C, Gabusi E et al (2019) Effect of microfragmented adipose tissue on osteoarthritic synovial macrophage factors. J Cell Physiol 234:5044–5055. https://doi.org/10.1002/jcp.27307
doi: 10.1002/jcp.27307
pubmed: 30187478
Randelli P, Menon A, Ragone V et al (2016) Lipogems product treatment increases the proliferation rate of human tendon stem cells without affecting their stemness and differentiation capability. Stem Cells Int 2016:4373410. https://doi.org/10.1155/2016/4373410
doi: 10.1155/2016/4373410
pubmed: 27057170
pmcid: 4736573
Bianchi F, Maioli M, Leonardi E et al (2013) A new nonenzymatic method and device to obtain a fat tissue derivative highly enriched in pericyte-like elements by mild mechanical forces from human lipoaspirates. Cell Transplant 22:2063–2077. https://doi.org/10.3727/096368912X657855
doi: 10.3727/096368912X657855
pubmed: 23051701
Shah D, Naciri M, Clee P, Al-Rubeai M (2006) NucleoCounter—an efficient technique for the determination of cell number and viability in animal cell culture processes. Cytotechnology 51:39–44. https://doi.org/10.1007/s10616-006-9012-9
doi: 10.1007/s10616-006-9012-9
pubmed: 19002893
pmcid: 3449478
Stanco D, Viganò M, Perucca Orfei C et al (2015) Multidifferentiation potential of human mesenchymal stem cells from adipose tissue and hamstring tendons for musculoskeletal cell-based therapy. Regen Med 10:729–743. https://doi.org/10.2217/rme.14.92
doi: 10.2217/rme.14.92
pubmed: 25565145
Desjardins P, Conklin D (2010) NanoDrop microvolume quantitation of nucleic acids. J Vis Exp. https://doi.org/10.3791/2565
Viganò M, Perucca Orfei C, de Girolamo L et al (2018) Housekeeping gene stability in human mesenchymal stem and tendon cells exposed to tenogenic factors. Tissue Eng Part C Methods 24:360–367. https://doi.org/10.1089/ten.TEC.2017.0518
doi: 10.1089/ten.TEC.2017.0518
pubmed: 29676207
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
doi: 10.1093/nar/29.9.e45
Bailey AJ, Robins SP, Balian G (1974) Biological significance of the intermolecular crosslinks of collagen. Nature 251:105–109
doi: 10.1038/251105a0
Nho SJ, Yadav H, Shindle MK, Macgillivray JD (2008) Rotator cuff degeneration: etiology and pathogenesis. Am J Sports Med 36:987–993. https://doi.org/10.1177/0363546508317344
doi: 10.1177/0363546508317344
pubmed: 18413681
Abraham AC, Shah SA, Thomopoulos S (2017) Targeting inflammation in rotator cuff tendon degeneration and repair. Tech Shoulder Elb Surg 18:84–90. https://doi.org/10.1097/BTE.0000000000000124
doi: 10.1097/BTE.0000000000000124
pubmed: 28947893
pmcid: 5609736
Thankam FG, Roesch ZK, Dilisio MF et al (2018) Association of inflammatory responses and ECM disorganization with HMGB1 upregulation and NLRP3 inflammasome activation in the injured rotator cuff tendon. Sci Rep 8:8918. https://doi.org/10.1038/s41598-018-27250-2
doi: 10.1038/s41598-018-27250-2
pubmed: 29891998
pmcid: 5995925
Gotoh M, Hamada K, Yamakawa H et al (1997) Significance of granulation tissue in torn supraspinatus insertions: an immunohistochemical study with antibodies against interleukin-1 beta, cathepsin D, and matrix metalloprotease-1. J Orthop Res 15:33–39. https://doi.org/10.1002/jor.1100150106
doi: 10.1002/jor.1100150106
pubmed: 9066524
Riley GP, Curry V, DeGroot J et al (2002) Matrix metalloproteinase activities and their relationship with collagen remodelling in tendon pathology. Matrix Biol 21:185–195
doi: 10.1016/S0945-053X(01)00196-2
Zhang J, Wang JH-C (2010) Production of PGE(2) increases in tendons subjected to repetitive mechanical loading and induces differentiation of tendon stem cells into non-tenocytes. J Orthop Res 28:198–203. https://doi.org/10.1002/jor.20962
doi: 10.1002/jor.20962
pubmed: 19688869
Schneider M, Angele P, Järvinen TAH, Docheva D (2018) Rescue plan for Achilles: therapeutics steering the fate and functions of stem cells in tendon wound healing. Adv Drug Deliv Rev 129:352–375. https://doi.org/10.1016/j.addr.2017.12.016
doi: 10.1016/j.addr.2017.12.016
pubmed: 29278683
Hammerman M, Blomgran P, Ramstedt S, Aspenberg P (2015) COX-2 inhibition impairs mechanical stimulation of early tendon healing in rats by reducing the response to microdamage. J Appl Physiol 119:534–540. https://doi.org/10.1152/japplphysiol.00239.2015
doi: 10.1152/japplphysiol.00239.2015
pubmed: 26159755
Rundle CH, Chen S-T, Coen MJ et al (2014) Direct lentiviral-cyclooxygenase 2 application to the tendon-bone interface promotes osteointegration and enhances return of the pull-out tensile strength of the tendon graft in a rat model of biceps tenodesis. PLoS One 9:e98004. https://doi.org/10.1371/journal.pone.0098004
doi: 10.1371/journal.pone.0098004
pubmed: 24848992
pmcid: 4029780
Bergqvist F, Carr AJ, Wheway K et al (2019) Divergent roles of prostacyclin and PGE2 in human tendinopathy. Arthritis Res Ther 21. https://doi.org/10.1186/s13075-019-1855-5
Millar NL, Wei AQ, Molloy TJ et al (2009) Cytokines and apoptosis in supraspinatus tendinopathy. J Bone Joint Surg (Br) 91:417–424. https://doi.org/10.1302/0301-620X.91B3.21652
doi: 10.1302/0301-620X.91B3.21652
Ackermann PW, Domeij-Arverud E, Leclerc P et al (2013) Anti-inflammatory cytokine profile in early human tendon repair. Knee Surg Sports Traumatol Arthrosc 21:1801–1806. https://doi.org/10.1007/s00167-012-2197-x
doi: 10.1007/s00167-012-2197-x
pubmed: 22983752
Millar NL, Akbar M, Campbell AL et al (2016) IL-17A mediates inflammatory and tissue remodelling events in early human tendinopathy. Sci Rep 6. https://doi.org/10.1038/srep27149
Yoshihara Y, Hamada K, Nakajima T et al (2001) Biochemical markers in the synovial fluid of glenohumeral joints from patients with rotator cuff tear. J Orthop Res 19:573–579. https://doi.org/10.1016/S0736-0266(00)00063-2
doi: 10.1016/S0736-0266(00)00063-2
pubmed: 11518264
Lo IKY, Marchuk LL, Hollinshead R et al (2004) Matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase mRNA levels are specifically altered in torn rotator cuff tendons. Am J Sports Med 32:1223–1229. https://doi.org/10.1177/0363546503262200
doi: 10.1177/0363546503262200
pubmed: 15262646
Assunção JH, Godoy-Santos AL, Dos Santos MCLG et al (2017) Matrix metalloproteases 1 and 3 promoter gene polymorphism is associated with rotator cuff tear. Clin Orthop Relat Res 475:1904–1910. https://doi.org/10.1007/s11999-017-5271-3
doi: 10.1007/s11999-017-5271-3
pubmed: 28160256
pmcid: 5449328
Del Buono A, Oliva F, Longo UG et al (2012) Metalloproteases and rotator cuff disease. J Shoulder Elb Surg 21:200–208. https://doi.org/10.1016/j.jse.2011.10.020
doi: 10.1016/j.jse.2011.10.020
Costa-Almeida R, Berdecka D, Rodrigues MT et al (2018) Tendon explant cultures to study the communication between adipose stem cells and native tendon niche. J Cell Biochem 119:3653–3662. https://doi.org/10.1002/jcb.26573
doi: 10.1002/jcb.26573
pubmed: 29231990
Costa-Almeida R, Calejo I, Reis RL, Gomes ME (2018) Crosstalk between adipose stem cells and tendon cells reveals a temporal regulation of tenogenesis by matrix deposition and remodeling. J Cell Physiol 233:5383–5395. https://doi.org/10.1002/jcp.26363
doi: 10.1002/jcp.26363
pubmed: 29215729
Gotoh M, Mitsui Y, Shibata H et al (2013) Increased matrix metalloprotease-3 gene expression in ruptured rotator cuff tendons is associated with postoperative tendon retear. Knee Surg Sports Traumatol Arthrosc 21:1807–1812. https://doi.org/10.1007/s00167-012-2209-x
doi: 10.1007/s00167-012-2209-x
pubmed: 23000921
Shukunami C, Takimoto A, Oro M, Hiraki Y (2006) Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes. Dev Biol 298:234–247. https://doi.org/10.1016/j.ydbio.2006.06.036
doi: 10.1016/j.ydbio.2006.06.036
pubmed: 16876153
Veronesi F, Della Bella E, Torricelli P et al (2015) Effect of adipose-derived mesenchymal stromal cells on tendon healing in aging and estrogen deficiency: an in vitro co-culture model. Cytotherapy 17:1536–1544. https://doi.org/10.1016/j.jcyt.2015.07.007
doi: 10.1016/j.jcyt.2015.07.007
pubmed: 26305076
Thankam FG, Evan DK, Agrawal DK, Dilisio MF (2018) Collagen type III content of the long head of the biceps tendon as an indicator of glenohumeral arthritis. Mol Cell Biochem. https://doi.org/10.1007/s11010-018-3449-y
Pajala A, Melkko J, Leppilahti J et al (2009) Tenascin-C and type I and III collagen expression in total Achilles tendon rupture. An immunohistochemical study. Histol Histopathol 24:1207–1211. https://doi.org/10.14670/HH-24.1207
doi: 10.14670/HH-24.1207
pubmed: 19688689
Dabrowski MP, Stankiewicz W, Płusa T et al (2001) Competition of IL-1 and IL-1ra determines lymphocyte response to delayed stimulation with PHA. Mediat Inflamm 10:101–107
doi: 10.1080/09629350124376
Palomo J, Dietrich D, Martin P et al (2015) The interleukin (IL)-1 cytokine family – balance between agonists and antagonists in inflammatory diseases. Cytokine 76:25–37. https://doi.org/10.1016/j.cyto.2015.06.017
doi: 10.1016/j.cyto.2015.06.017
pubmed: 26185894
Luo J, Xiong Y, Han X, Lu Y (2011) VEGF non-angiogenic functions in adult organ homeostasis: therapeutic implications. J Mol Med; New York 89:635–645. https://doi.org/10.1007/s00109-011-0739-1
doi: 10.1007/s00109-011-0739-1
pubmed: 21365187
Cohen T, Nahari D, Cerem LW et al (1996) Interleukin 6 induces the expression of vascular endothelial growth factor. J Biol Chem 271:736–741
doi: 10.1074/jbc.271.2.736
Legerlotz K, Jones ER, Screen HRC, Riley GP (2012) Increased expression of IL-6 family members in tendon pathology. Rheumatology (Oxford) 51:1161–1165. https://doi.org/10.1093/rheumatology/kes002
doi: 10.1093/rheumatology/kes002
Liu Z, Simpson RJ, Cheers C (1995) Interaction of interleukin-6, tumour necrosis factor and interleukin-1 during Listeria infection. Immunology 85:562–567
pubmed: 7558150
pmcid: 1383784
Chen S, Deng G, Li K et al (2018) Interleukin-6 promotes proliferation but inhibits Tenogenic differentiation via the Janus kinase/signal transducers and activators of transcription 3 (JAK/STAT3) pathway in tendon-derived stem cells. Med Sci Monit 24:1567–1573. https://doi.org/10.12659/MSM.908802
doi: 10.12659/MSM.908802
pubmed: 29547593
pmcid: 5868364
Lin TW, Cardenas L, Glaser DL, Soslowsky LJ (2006) Tendon healing in interleukin-4 and interleukin-6 knockout mice. J Biomech 39:61–69. https://doi.org/10.1016/j.jbiomech.2004.11.009
doi: 10.1016/j.jbiomech.2004.11.009
pubmed: 16271588
John T, Lodka D, Kohl B et al (2010) Effect of pro-inflammatory and immunoregulatory cytokines on human tenocytes. J Orthop Res 28:1071–1077. https://doi.org/10.1002/jor.21079
doi: 10.1002/jor.21079
pubmed: 20127972
Pauly S, Klatte-Schulz F, Stahnke K et al (2018) The effect of autologous platelet rich plasma on tenocytes of the human rotator cuff. BMC Musculoskelet Disord 19:422. https://doi.org/10.1186/s12891-018-2339-5
doi: 10.1186/s12891-018-2339-5
pubmed: 30497435
pmcid: 6267832