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Platelet Lysates from Aged Donors Promote Human Tenocyte Proliferation and Migration in a Concentration- Dependent Manner

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Platelet Lysates from Aged Donors Promote Human Tenocyte Proliferation and Migration in a Concentration- Dependent Manner 81.BJRBJR Follow us @BoneJointRes Freely available online OPEN ACCESS BJR RESEARCH Platelet lysates from aged donors promote human tenocyte proliferation and migration in a concentration- dependent manner D. R. Berger, Objectives C. J. Centeno, Platelet-rich plasma (PRP) is being used increasingly often in the clinical setting to treat N. J. Steinmetz tendon-related pathologies. Yet the optimal PRP preparations to promote tendon healing in different patient populations are poorly defined. Here, we sought to determine whether Interventional increasing the concentration of platelet-derived proteins within a derivative of PRP, platelet Orthopedics lysate (PL), enhances tenocyte proliferation and migration in vitro, and whether the mito- Foundation, genic properties of PL change with donor age. Broomfield, Colorado, Methods United States Concentrated PLs from both young (< 50 years) and aged (> 50 years) donors were prepared by exposing pooled PRP to a series of freeze-thaw cycles followed by dilution in plasma, and the levels of several platelet-derived proteins were measured using multiplex immunoassay technology. Human tenocytes were cultured with PLs to simulate a clinically relevant PRP treatment range, and cell growth and migration were assessed using DNA quantitation and gap closure assays, respectively. Results Platelet-derived protein levels increased alongside higher PL concentrations, and PLs from both age groups improved tenocyte proliferation relative to control conditions. However, PLs from aged donors yielded a dose-response relationship in tenocyte behaviour, with higher PL concentrations resulting in increased tenocyte proliferation and migration. Con- versely, no significant differences in tenocyte behaviour were detected when increasing the concentration of PLs from younger donors. Conclusion Higher PL concentrations, when prepared from the PRP of aged but not young donors, were more effective than lower PL concentrations at promoting tenocyte proliferation and migra- D. R. Berger, MSc, Research tion in vitro. Scientist, Interventional Orthopedics Foundation, Cite this article: Bone Joint Res 2019;8:32–40. Broomfield, Colorado, USA. C. J. Centeno, MD, President Keywords: Ageing, Platelet lysate, Tenocyte, Proliferation, Migration and Owner, Centeno-Schultz Clinic, Broomfield, Colorado, USA; Board Chairman, Interventional Article focus platelet lysate (PL) promotes tenocyte Orthopedics Foundation, Motivated by the emerging use of plate- proliferation and migration in vitro, and Broomfield, Colorado, USA; Chief Medical Officer, Regenexx, LLC, let-rich plasma (PRP) for the treatment of that differences may exist between the Broomfield, Colorado, USA. tendon-related pathologies, the primary donor age groups investigated. N. J. Steinmetz, PhD, Chief focus of this article is to determine Scientific Officer, Regenexx, LLC, whether human tenocyte behaviour is Key messages Broomfield, Colorado, USA. enhanced when cultured with increasing There is a clear dose-response relationship Correspondence should be sent to N. J. Steinmetz; email: concentrations of platelet-derived pro- between PL concentration and cell behav- [email protected] teins, and whether the cell behaviour iour in PL obtained from aged donors. doi: 10.1302/2046-3758.81.BJR- changes with blood donor age. In contrast, tenocytes displayed similar 2018-0164.R1 The present hypothesis is that increasing behaviour irrespective of PL concentra- Bone Joint Res 2019;8:32–40. the platelet-derived protein levels within tion in PL obtained from young donors. VOL. 8, NO. 1, JANUARY 2019 32 PlATeleT lYSATeS FRoM AgeD DoNoRS PRoMoTe hUMAN TeNoCYTe PRolIFeRATIoN AND MIgRATIoN IN A CoNCeNTRATIoN-DePeNDeNT MANNeR 33 Strengths and limitations of PL change with donor age. Concentrated PLs, gener- This study shows that increasing the platelet-derived ated from the pooled PRP of both young and aged protein content from aged donors can have a positive donors, were combined with cell culture medium using a effect on tenocyte behaviour. fixed volumetric ratio to model a range of PRP prepara- However, it is limited in size and scope, necessitating tions used clinically. We hypothesized that increasing the additional in vivo investigation. platelet-derived protein levels within PL would enhance tenocyte behaviour, and that differences would exist Introduction between donor age groups. Platelet-rich plasma (PRP) is gaining popularity in a variety of clinical settings as an autologous source of bioactive Materials and Methods molecules for promoting tissue repair. The supraphysio- Preparation of concentrated platelet lysates (PLs). After logical concentration of platelet-derived growth factors informed consent was obtained, whole blood from and cytokines within PRP has been thought to support the healthy adult donors (n = 14) was collected into a stan- regeneration of tendons, the connective tissue structures dard blood bag (Teruflex; Terumo BCT, Lakewood, responsible for anchoring muscle to bone and facilitating Colorado) or blood tubes (BD Vacutainer; Becton mechanical motion.1-3 Ageing tendons have limited heal- Dickinson, Franklin Lakes, New Jersey) containing anti- ing potential and undergo both cellular and extracellular coagulant citrate dextrose solution A (Baxter Healthcare changes, including reductions in tenocyte proliferation, Corporation, Deerfield, Illinois). Platelet-rich plasma (PRP) volume, and metabolic activity, as well as a loss of vascu- was manually separated from other blood components larization, decreased levels of non-collagenous matrix following centrifugation at 200 × g for ten minutes. Care components, and low collagen turnover.1,4 Together, was taken during PRP isolation to avoid disturbing the these degenerative tissue changes culminate in dimin- leucocyte-rich buffy coat, thereby minimizing nucleated ished strength, increasing the prospect of tendinous cell contamination. The leucocyte-poor nature of the PRP injury.4 Pathological tendons may well benefit from the isolated when using this methodology was confirmed growth factors found in PRP preparations, which have using a haematological analyzer (Micros 60; Horiba, been shown to promote cellular proliferation and sup- Irvine, California), with all leucocyte counts falling below port angiogenesis.5 However, the clinical efficacy of PRP the recommended reportable limit (Supplementary for the treatment of tendinopathies has been questioned, Table i). Isolated PRP was subjected to a second round as several systematic reviews of the current literature of centrifugation at 2300 × g for ten minutes to form a have drawn opposing conclusions.6-10 platelet pellet, and the platelet-poor plasma (PPP) super- Reported discrepancies among clinical trials investi- natant was completely aspirated. The remaining platelet gating the use of PRP for treating tendinopathies may be pellet was resuspended in 1/35 of the initial plasma vol- attributed in part to inconsistencies in PRP preparation ume (~70 times over the baseline), resulting in a concen- and treatment protocols,8,10 as different methodologies trated PRP solution having about 20 times more platelets for creating PRP have been reported to affect the kinetics than the original PRP (Supplementary Table ii).16 To of growth factor release.11 Furthermore, consensus as to account for the potential of platelet clumping, platelet how the most elementary of PRP components, platelet counts were obtained manually from the concentrated concentration, affects tendon healing is lacking. For PRP using a haemocytometer prior to storage at -80°C.17 instance, multiple human studies have reported higher Upon thawing at 37°C, the PRP preparations were com- platelet concentrations to have inhibitory effects on cell bined into two different pooled platelet products based proliferation in vitro,12-14 whereas others have demon- on an age cut-off of 50 years (Tables I and II), and were strated PRP to stimulate tenocyte proliferation in a dose- subjected to two additional freeze/thaw cycles at -80°C dependent manner, with platelet concentrations of more and 37°C to generate concentrated PLs.18 Fragmented than 50 times greater than physiological levels having no platelet bodies were pelleted and removed by centrifu- inhibitory effects on cell growth.15 Consequently, it is gation at 4500 × g for ten minutes, and sodium heparin currently unclear if increasing the platelet concentration (Sagent Pharmaceuticals, Inc., Schaumburg, Illinois) was in PRP is beneficial for treating tendinopathies. Moreover, added to the recovered supernatant at 100 IU/ml to pre- whether the optimal platelet concentration to promote vent hydrogel formation. Finally, the concentrated PLs tendon healing changes with patient age remains to be were serially diluted two-fold in pooled PPP in order to seen. prepare less concentrated forms with 1/2, 1/4, 1/8, and In the current study, we cultured human tenocytes 1/16 of the starting PL volume. within increasing concentrations of platelet lysate (PL), a Protein analysis. Quantitative protein analysis was per- derivative of PRP, to determine whether higher platelet- formed using a multiplex, antibody-based assay (Q-Plex derived protein levels enhance cell proliferation and Human Angiogenesis; Quansys Biosciences, Logan, Utah) migration in vitro, and whether the mitogenic properties in accordance with the manufacturer’s recommendations. VOL. 8, NO. 1, JANUARY 2019 34 D. R. BERGER, C. J. CENTENO, N. J. STEINMETZ Table I. Platelet counts in concentrated platelet-rich
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