A systematic study of the effect of different molecular weights of hyaluronic acid on mesenchymal stromal cell-mediated immunomodulation

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Gómez Aristizábal, Alejandro ^a   Kim, Kyung Phil ^b   Viswanathan, Sowmya ^a,b,c  

^a TORONTO WESTERN HOSPITAL   (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD163 ANTIGEN; CD206 ANTIGEN; GAMMA INTERFERON; HYALURONIC ACID; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 2; LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG; IMMUNOLOGIC FACTOR;

ARTICLE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; HELPER CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; LYMPHOCYTE ACTIVATION; MESENCHYMAL STROMA CELL; MOLECULAR WEIGHT; OSTEOARTHRITIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN ANALYSIS; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; CELL CULTURE; CHEMISTRY; COCULTURE; DRUG EFFECTS; MACROPHAGE; PHYSIOLOGY; PRECLINICAL STUDY;

CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DRUG EVALUATION, PRECLINICAL; GENE EXPRESSION; HUMANS; HYALURONIC ACID; IMMUNOLOGIC FACTORS; IMMUNOMODULATION; MACROPHAGES; MESENCHYMAL STROMAL CELLS; MOLECULAR WEIGHT; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY;

EID: 84958211481     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0147868     Document Type: Article

References (61)

1. de Lange-Brokaar BJE, Ioan-Facsinay A, van Osch G JVM, Zuurmond A-M, Schoones J, Toes REM, et al. Synovial inflammation, immune cells and their cytokines in osteoarthritis: a review. Osteoarthritis Cartilage. 2012;20:1484-1499. doi: 10.1016/j.joca.2012.08.027 PMID: 22960092
2. Blom AB, van Lent PL, Libregts S, Holthuysen AE, van der Kraan PM, van Rooijen N, et al. Crucial role of macrophages in matrix metalloproteinase-mediated cartilage destruction during experimental osteoarthritis: Involvement of matrix metalloproteinase 3. Arthritis Rheum. 2007;56:147-157. doi: 10.1002/art.22337 PMID: 17195217
3. Sakkas LI, Platsoucas CD. The role of T cells in the pathogenesis of osteoarthritis. Arthritis Rheum. 2007;56:409-424. doi: 10.1002/art.22369 PMID: 17265476
4. Lawrence RC, Felson DT, Helmick CG, Arnold LM, Choi H, Deyo RA, et al. Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II. Arthritis Rheum. 2008;58:26-35. doi: 10.1002/art.23176 PMID: 18163497
5. Ashford S, Williard J. Osteoarthritis: A review. Nurse Pract. 2014;39:1-8.
6. Vincent HK, Percival SS, Conrad BP, Seay AN, Montero C, Vincent KR. Hyaluronic Acid (HA) Viscosupplementation on Synovial Fluid Inflammation in Knee Osteoarthritis: A Pilot Study. Open Orthop J. 2013;7:378-384. doi: 10.2174/1874325001307010378 PMID: 24093052
7. Colen S, van den Bekerom MPJ, Mulier M, Haverkamp D. Hyaluronic acid in the treatment of knee osteoarthritis: a systematic review and meta-analysis with emphasis on the efficacy of different products. BioDrugs Clin Immunother Biopharm Gene Ther. 2012;26:257-268.
8. Maheu E, Zaim M, Appelboom T, Jeka S, Trc T, Berenbaum F, et al. Comparative efficacy and safety of two different molecular weight (MW) hyaluronans F60027 and Hylan G-F20 in symptomatic osteoarthritis of the knee (KOA). Results of a non inferiority, prospective, randomized, controlled trial. Clin Exp Rheumatol. 2011;29:527-535. PMID: 21722501
9. Karatay S, Kiziltunc A, Yildirim K, Karanfil RC, Senel K. Effects of Different Hyaluronic Acid Products on Synovial Fluid Levels of Intercellular Adhesion Molecule-1 and Vascular Cell Adhesion Molecule-1 in Knee Osteoarthritis. Ann Clin Lab Sci. 2004;34:330-335. PMID: 15487709
10. Petrella RJ, Decaria J, Petrella M. Long term efficacy and safety of a combined low and high molecular weight hyaluronic acid in the treatment of osteoarthritis of the knee. Rheumatol Rep. 2011;3. doi: 10. 4081/rr.2011.e4
11. Berenbaum F, Grifka J, Cazzaniga S, D'Amato M, Giacovelli G, Chevalier X, et al. A randomised, doubleblind, controlled trial comparing two intra-articular hyaluronic acid preparations differing by their molecular weight in symptomatic knee osteoarthritis. Ann Rheum Dis. 2012;71:1454-1460. doi: 10. 1136/annrheumdis-2011-200972 PMID: 22294639
12. Duchman KR, Gao Y, Pugely AJ, Martin CT, Callaghan JJ. Differences in short-term complications between unicompartmental and total knee arthroplasty: a propensity score matched analysis. J Bone Joint Surg Am. 2014;96:1387-1394. doi: 10.2106/JBJS. M.01048 PMID: 25143499
13. Viswanathan S, Gomez-Aristizabal A. Review of Patents and Commercial Opportunities Involving Mesenchymal Stromal Cells (MSCs) Therapies in Osteoarthritis. Recent Pat Regen Med. 2014;4:1-15. doi: 10.2174/2210296504666140307010938
14. Wong KL, Lee KBL, Tai BC, Law P, Lee EH, Hui JHP. Injectable cultured bone marrow-derived mesenchymal stem cells in varus knees with cartilage defects undergoing high tibial osteotomy: a prospective, randomized controlled clinical trial with 2 years' follow-up. Arthrosc J Arthrosc Relat Surg Off Publ Arthrosc Assoc N Am Int Arthrosc Assoc. 2013;29:2020-2028. doi: 10.1016/j.arthro.2013.09.074
15. University of Jordan. Mesenchymal Stem Cells in Knee Cartilage Injuries. In: ClinicalTrials.gov [Internet]. 2014. Available: https://www.clinicaltrials.gov/ct2/show/NCT02118519.
16. Chahal J, Viswanathan S. Human Autologous MSCs for the Treatment of Mid to Late Stage Knee OA. In: ClinicalTrials.gov [Internet]. 2015. Available: https://www.clinicaltrials.gov/ct2/show/NCT02351011.
17. Espinoza F. A Study to Assess Safety and Efficacy of Umbilical Cord-derived Mesenchymal Stromal Cells in Knee Osteoarthritis. In: ClinicalTrials.gov [Internet]. 2015. Available: https://www.clinicaltrials. gov/ct2/show/NCT02580695.
18. Shenzhen Hornetcorn Bio-technology Company, LTD, The Fifth Affiliated Hospital of Guangzhou Medical University. Human Umbilical Cord Mesenchymal Stem Cell Transplantation in Articular Cartilage Defect. In: ClinicalTrials.gov [Internet]. 2015. Available: https://www.clinicaltrials.gov/ct2/show/NCT02291926.
19. Translational Biosciences. Clinical Study of Umbilical Cord Tissue Mesenchymal Stem Cells (UCMSC) for Treatment of Osteoarthritis. In: ClinicalTrials.gov [Internet]. 2015. Available: https://www.clinicaltrials.gov/ct2/show/NCT02237846.
20. Universidad de Navarra. Treatment of Osteoarthritis by Intra-articular Injection of Bone Marrow Mesenchymal Stem Cells With Platelet Rich Plasma (CMM-PRGF/ART). In: ClinicalTrials.gov [Internet]. 2015. Available: https://www.clinicaltrials.gov/ct2/show/NCT02365142.
21. Murphy JM, Fink DJ, Hunziker EB, Barry FP. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum. 2003;48:3464-3474. doi: 10.1002/art.11365 PMID: 14673997
22. Singh A, Goel SC, Gupta KK, Kumar M, Arun GR, Patil H, et al. The role of stem cells in osteoarthritis. Bone Jt Res. 2014;3:32-37. doi: 10.1302/2046-3758.32.2000187
23. Al Faqeh H, Nor Hamdan BMY, Chen HC, Aminuddin BS, Ruszymah BHI. The potential of intra-articular injection of chondrogenic-induced bone marrow stem cells to retard the progression of osteoarthritis in a sheep model. Exp Gerontol. 2012;47:458-464. doi: 10.1016/j.exger.2012.03.018 PMID: 22759409
24. Sato M, Uchida K, Nakajima H, Miyazaki T, Guerrero AR, Watanabe S, et al. Direct transplantation of mesenchymal stem cells into the knee joints of Hartley strain guinea pigs with spontaneous osteoarthritis. Arthritis Res Ther. 2012;14:R31. doi: 10.1186/ar3735 PMID: 22314040
25. Suhaeb AM, Naveen S, Mansor A, Kamarul T. Hyaluronic acid with or without bone marrow derivedmesenchymal stem cells improves osteoarthritic knee changes in rat model: a preliminary report. Indian J Exp Biol. 2012;50:383-390. PMID: 22734248
26. Mokbel AN, El Tookhy OS, Shamaa AA, Rashed LA, Sabry D, El Sayed AM. Homing and reparative effect of intra-articular injection of autologus mesenchymal stem cells in osteoarthritic animal model. BMC Musculoskelet Disord. 2011;12:259. doi: 10.1186/1471-2474-12-259 PMID: 22085445
27. Dvorakova J, Velebny V, Kubala L. Hyaluronan influence on the onset of chondrogenic differentiation of mesenchymal stem cells. Neuro Endocrinol Lett. 2008;29:685-690. PMID: 18987597
28. Band PA, Heeter J, Wisniewski H-G, Liublinska V, Pattanayak CW, Karia RJ, et al. Hyaluronan molecular weight distribution is associated with the risk of knee osteoarthritis progression. Osteoarthritis Cartilage. 2015;23:70-76. doi: 10.1016/j.joca.2014.09.017 PMID: 25266961
29. Shen P-C, Wu C-L, Jou I-M, Lee C-H, Juan H-Y, Lee P-J, et al. T helper cells promote disease progression of osteoarthritis by inducing macrophage inflammatory protein-1γ. Osteoarthritis Cartilage. 2011;19:728-736. doi: 10.1016/j.joca.2011.02.014 PMID: 21376128
30. Verreck FAW, de Boer T, Langenberg DML, van der Zanden L, Ottenhoff THM. Phenotypic and functional profiling of human proinflammatory type-1 and anti-inflammatory type-2 macrophages in response to microbial antigens and IFN-γ- and CD40L-mediated costimulation. J Leukoc Biol. 2006;79:285-293. doi: 10.1189/jlb.0105015 PMID: 16330536
31. Fahy N, de Vries-van Melle ML, Lehmann J, Wei W, Grotenhuis N, Farrell E, et al. Human osteoarthritic synovium impacts chondrogenic differentiation of mesenchymal stem cells via macrophage polarisation state. Osteoarthr Cartil OARS Osteoarthr Res Soc. 2014;22:1167-1175.
32. Chinnadurai R, Copland IB, Patel SR, Galipeau J. IDO-Independent Suppression of T Cell Effector Function by IFN-γ-Licensed Human Mesenchymal Stromal Cells. J Immunol. 2014; doi: 10.4049/jimmunol.1301828
33. Vangsness CT Jr, Burke WS, Narvy SJ, MacPhee RD, Fedenko AN. Human knee synovial fluid cytokines correlated with grade of knee osteoarthritis-a pilot study. Bull NYU Hosp Jt Dis. 2011;69:122-127. PMID: 22035391
34. Hagmann S, Gotterbarm T, Müller T, Baesig A-M, Gantz S, Dreher T, et al. The influence of bone marrowand synovium-derived mesenchymal stromal cells from osteoarthritis patients on regulatory T cells in co-culture. Clin Exp Immunol. 2013;173:454-462. doi: 10.1111/cei.12122 PMID: 23607395
35. Abumaree MH, Al Jumah MA, Kalionis B, Jawdat D, Al Khaldi A, Abomaray FM, et al. Human placental mesenchymal stem cells (pMSCs) play a role as immune suppressive cells by shifting macrophage differentiation from inflammatory M1 to anti-inflammatory M2 macrophages. Stem Cell Rev. 2013;9:620-641. doi: 10.1007/s12015-013-9455-2 PMID: 23812784
36. Adutler-Lieber S, Ben-Mordechai T, Naftali-Shani N, Asher E, Loberman D, Raanani E, et al. Human macrophage regulation via interaction with cardiac adipose tissue-derived mesenchymal stromal cells. J Cardiovasc Pharmacol Ther. 2013;18:78-86. doi: 10.1177/1074248412453875 PMID: 22894882
37. Del Papa B, Sportoletti P, Cecchini D, Rosati E, Balucani C, Baldoni S, et al. Notch1 modulates mesenchymal stem cells mediated regulatory T-cell induction. Eur J Immunol. 2013;43:182-187. doi: 10. 1002/eji.201242643 PMID: 23161436
38. Dayan V, Yannarelli G, Filomeno P, Keating A. Human mesenchymal stromal cells improve scar thickness without enhancing cardiac function in a chronic ischaemic heart failure model. Interact Cardiovasc Thorac Surg. 2012;14:516-520. doi: 10.1093/icvts/ivs048 PMID: 22361124
39. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method. Methods San Diego Calif. 2001;25:402-408.
40. Fellows I. Deducer: A Data Analysis GUI for R. J Stat Softw. 2012;49:1-15.
41. Seddiki N. Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J Exp Med. 2006;203:1693-1700. doi: 10.1084/jem.20060468 PMID: 16818676
42. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004;25:677-686. doi: 10.1016/j.it. 2004.09.015 PMID: 15530839
43. Bottero V, Imbert V, Frelin C, Formento J-L, Peyron J-F. Monitoring NF-kappa B transactivation potential via real-time PCR quantification of I kappa B-alpha gene expression. Mol Diagn J Devoted Underst Hum Dis Clin Appl Mol Biol. 2003;7:187-194.
44. Campo GM, Avenoso A, Campo S, D'Ascola A, Traina P, Rugolo CA, et al. Differential effect of molecular mass hyaluronan on lipopolysaccharide-induced damage in chondrocytes. Innate Immun. 2010;16:48-63. doi: 10.1177/1753425909340419 PMID: 19710088
45. Campo GM, Avenoso A, Campo S, D'Ascola A, Nastasi G, Calatroni A. Small hyaluronan oligosaccharides induce inflammation by engaging both toll-like-4 and CD44 receptors in human chondrocytes. Biochem Pharmacol. 2010;80:480-490. doi: 10.1016/j.bcp. 2010.04.024 PMID: 20435021
46. Föger N, Marhaba R, Zöller M. CD44 supports T cell proliferation and apoptosis by apposition of protein kinases. Eur J Immunol. 2000;30:2888-2899. doi: 10.1002/1521-4141 (200010) 30:10<2888::AIDIMMU2888> 3.0. CO;2-4 PMID: 11069071
47. Darżynkiewicz Z, Balazs EA. Effect of connective tissue intercellular matrix on lymphocyte stimulation: I. Suppression of Lymphocyte stimulation by hyaluronic acid. Exp Cell Res. 1971;66:113-123. doi: 10. 1016/S0014-4827 (71) 80018-6 PMID: 5104191
48. Shiedlin A, Bigelow R, Christopher W, Arbabi S, Yang L, Maier RV, et al. Evaluation of Hyaluronan from Different Sources: Streptococcus zooepidemicus, Rooster Comb, Bovine Vitreous, and Human Umbilical Cord. Biomacromolecules. 2004;5:2122-2127. doi: 10.1021/bm0498427 PMID: 15530025
49. Bollyky PL, Falk BA, Long A, Preisinger A, Braun KR, Wu RP, et al. CD44 co-stimulation promotes FoxP3+ regulatory T-cell persistence and function via production of IL-2, IL-10 and TGF-beta. J Immunol Baltim Md 1950. 2009;183:2232-2241. doi: 10.4049/jimmunol.0900191
50. Tiemessen MM, Jagger AL, Evans HG, van Herwijnen MJC, John S, Taams LS. CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci. 2007;104:19446-19451. doi: 10.1073/pnas.0706832104 PMID: 18042719
51. Farahat MN, Yanni G, Poston R, Panayi GS. Cytokine expression in synovial membranes of patients with rheumatoid arthritis and osteoarthritis. Ann Rheum Dis. 1993;52:870-875. doi: 10.1136/ard.52. 12.870 PMID: 8311538
52. Baeva LF, Lyle DB, Rios M, Langone JJ, Lightfoote MM. Different molecular weight hyaluronic acid effects on human macrophage interleukin 1ß production. J Biomed Mater Res A. 2013; doi: 10.1002/jbm.a.34704
53. Yang C, Cao M, Liu H, He Y, Xu J, Du Y, et al. The High and Low Molecular Weight Forms of Hyaluronan Have Distinct Effects on CD44 Clustering. J Biol Chem. 2012;287:43094-43107. doi: 10.1074/jbc. M112.349209 PMID: 23118219
54. Fuchs K, Hippe A, Schmaus A, Homey B, Sleeman JP, Orian-Rousseau V. Opposing effects of highand low-molecular weight hyaluronan on CXCL12-induced CXCR4 signaling depend on CD44. Cell Death Dis. 2013;4:e819. doi: 10.1038/cddis.2013.364 PMID: 24091662
55. Brown T, Laurent U, Fraser. Turnover of hyaluronan in synovial joints: elimination of labelled hyaluronan from the knee joint of the rabbit. Exp Physiol. 1991;76:125-134. doi: 10.1113/expphysiol.1991. sp003474 PMID: 2015069
56. Larsen NE, Dursema HD, Pollak CT, Skrabut EM. Clearance kinetics of a hylan-based viscosupplement after intra-articular and intravenous administration in animal models. J Biomed Mater Res B Appl Biomater. 2012;100 B: 457-462. doi: 10.1002/jbm.b.31971
57. Essendoubi M, Gobinet C, Reynaud R, Angiboust JF, Manfait M, Piot O. Human skin penetration of hyaluronic acid of different molecular weights as probed by Raman spectroscopy. Skin Res Technol Off J Int Soc Bioeng Skin ISBS Int Soc Digit Imaging Skin ISDIS Int Soc Skin Imaging ISSI. 2015; doi: 10.1111/srt.12228
58. Sall I, Férard G. Comparison of the sensitivity of 11 crosslinked hyaluronic acid gels to bovine testis hyaluronidase. Polym Degrad Stab. 2007;92:915-919. doi: 10.1016/j.polymdegradstab.2006.11.020
59. Edsman K, Hjelm R, Lärkner H, Nord LI, Karlsson A, Wiebensjö A, et al. Intra-articular Duration of DurolaneTM after Single Injection into the Rabbit Knee. Cartilage. 2011;2:384-388. doi: 10.1177/1947603511400184 PMID: 26069596
60. Ottaviani RA, Wooley P, Song Z, Markel DC. Inflammatory and Immunological Responses to Hyaluronan Preparations. J Bone Jt Surg Am. 2007;89:148-157. doi: 10.2106/JBJS. E.01135
61. Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, Xu W, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci. 2013;110:3507-3512. doi: 10.1073/pnas.1222878110 PMID: 23401516