Synovial fluid pretreatment with hyaluronidase facilitates isolation of CD44+ extracellular vesicles

Journal of Extracellular Vesicles

Volumn 5, Issue 1, 2016, Pages

  Boere, Janneke ^a,b,c   van de Lest, Chris H A ^a,b   Libregts, Sten F W M ^b   Arkesteijn, Ger J A ^a,b   Geerts, Willie J C ^d   Nolte 't Hoen, Esther N M ^b   Malda, Jos ^a,c   van Weeren, P René ^a   Wauben, Marca H M ^b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

CD44; cryo TEM; equine; extracellular vesicles; high resolution flow cytometry; hyaluronidase; isolation; joint; standardization; synovial fluid

Indexed keywords

CD9 ANTIGEN; CONTRAST MEDIUM; HERMES ANTIGEN; HYALURONIC ACID; HYALURONIDASE;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; EXOSOME; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; NONHUMAN; PROTEIN ANALYSIS; SEDIMENT; STANDARDIZATION; SUCROSE DENSITY GRADIENT CENTRIFUGATION; SYNOVIAL FLUID; ULTRACENTRIFUGATION; VISCOSITY; WESTERN BLOTTING;

EID: 85015638729     PISSN: None     EISSN: 20013078     Source Type: Journal    
DOI: 10.3402/jev.v5.31751     Document Type: Article

References (51)

1. Malda J, Boere J, van de Lest CH, van Weeren PR, Wauben MH. Extracellular vesicles–new tool for joint repair and regeneration. Nat Rev Rheumatol. 2016; 12: 243–9.
2. Berckmans RJ, Nieuwland R, Tak PP, Boing AN, Romijn FP, Kraan MC, etal. Cell-derived microparticles in synovial fluid from inflamed arthritic joints support coagulation exclusively via a factor VII-dependent mechanism. Arthritis Rheum. 2002; 46: 2857–66.
3. Berckmans RJ, Nieuwland R, Kraan MC, Schaap MC, Pots D, Smeets TJ, etal. Synovial microparticles from arthritic patients modulate chemokine and cytokine release by synoviocytes. Arthritis Res Ther. 2005; 7: R536–44.
4. Biró E, Nieuwland R, Tak PP, Pronk LM, Schaap MC, Sturk A, etal. Activated complement components and complement activator molecules on the surface of cell-derived microparticles in patients with rheumatoid arthritis and healthy individuals. Ann Rheum Dis. 2007; 66: 1085–92.
5. Boilard E, Nigrovic PA, Larabee K, Watts GF, Coblyn JS, Weinblatt ME, etal. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science. 2010; 327: 580–3.
6. Cloutier N, Tan S, Boudreau LH, Cramb C, Subbaiah R, Lahey L, etal. The exposure of autoantigens by microparticles underlies the formation of potent inflammatory components: the microparticle-associated immune complexes. EMBO Mol Med. 2013; 5: 235–49.
7. Duchez AC, Boudreau LH, Bollinger J, Belleannee C, Cloutier N, Laffont B, etal. Platelet microparticles are internalized in neutrophils via the concerted activity of 12-lipoxygenase and secreted phospholipase A2-IIA. Proc Natl Acad Sci USA. 2015; 112: E3564–73.
8. Fourcade O, Simon MF, Viode C, Rugani N, Leballe F, Ragab A, etal. Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell. 1995; 80: 919–27.
9. György B, Szabo TG, Turiak L, Wright M, Herczeg P, Ledeczi Z, etal. Improved flow cytometric assessment reveals distinct microvesicle (cell-derived microparticle) signatures in joint diseases. PLoS One. 2012; 7: e49726.
10. György B, Modos K, Pallinger E, Paloczi K, Pasztoi M, Misjak P, etal. Detection and isolation of cell-derived microparticles are compromised by protein complexes resulting from shared biophysical parameters. Blood. 2011; 117: e39–48.
11. Headland SE, Jones HR, Norling LV, Kim A, Souza PR, Corsiero E, etal. Neutrophil-derived microvesicles enter cartilage and protect the joint in inflammatory arthritis. Sci Transl Med. 2015; 7: 315ra190.
12. Junkar I, Sustar V, Frank M, Jansa V, Zavec A, Rozman B, etal. Blood and synovial microparticles as revealed by atomic force and scanning electron microscope. Open Autoimmun J. 2009; 1: 50–8.
13. Martínez-Lorenzo MJ, Anel A, Saez-Gutierrez B, Royo-Canas M, Bosque A, Alava MA, etal. Rheumatoid synovial fluid T cells are sensitive to APO2L/TRAIL. Clin Immunol. 2007; 122: 28–40.
14. Matei CI, Boulocher C, Boule C, Schramme M, Viguier E, Roger T, etal. Ultrastructural analysis of healthy synovial fluids in three mammalian species. Microsc Microanal. 2014; 20: 903–11.
15. Messer L, Alsaleh G, Freyssinet J, Zobairi F, Leray I, Gottenberg J, etal. Microparticle-induced release of B-lymphocyte regulators by rheumatoid synoviocytes. Arthritis Res Ther. 2009; 11: R40.
16. Pásztói M, Sodar B, Misjak P, Paloczi K, Kittel A, Toth K, etal. The recently identified hexosaminidase D enzyme substantially contributes to the elevated hexosaminidase activity in rheumatoid arthritis. Immunol Lett. 2013; 149: 71–6.
17. Reich N, Beyer C, Gelse K, Akhmetshina A, Dees C, Zwerina J, etal. Microparticles stimulate angiogenesis by inducing ELR(+) CXC-chemokines in synovial fibroblasts. J Cell Mol Med. 2011; 15: 756–62.
18. Skriner K, Adolph K, Jungblut PR, Burmester GR. Association of citrullinated proteins with synovial exosomes. Arthritis Rheum. 2006; 54: 3809–14.
19. Mustonen AM, Nieminen P, Joukainen A, Jaroma A, Kaariainen T, Kroger H, etal. First in vivo detection and characterization of hyaluronan-coated extracellular vesicles in human synovial fluid. J Orthop Res. 2016. doi: http://dx.doi.org/10.1002/jor.23212.
20. Malda J, Benders KE, Klein TJ, de Grauw JC, Kik MJ, Hutmacher DW, etal. Comparative study of depth-dependent characteristics of equine and human osteochondral tissue from the medial and lateral femoral condyles. Osteoarthr Cartil. 2012; 20: 1147–51.
21. Hurtig MB, Buschmann MD, Fortier LA, Hoemann CD, Hunziker EB, Jurvelin JS, etal. Preclinical studies for cartilage repair: recommendations from the International Cartilage Repair Society. Cartilage. 2011; 2: 137–52.
22. McIlwraith CW, Frisbie DD, Kawcak CE. The horse as a model of naturally occurring osteoarthritis. Bone Joint Res. 2012; 1: 297–309.
23. Witwer KW, Buzas EI, Bemis LT, Bora A, Lasser C, Lotvall J, etal. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles. 2013; 2: 20360,. doi: http://dx.doi.org/10.3402/jev.v2i0.20360. eCollection 2013.
24. Zonneveld MI, Brisson AR, van Herwijnen MJ, Tan S, van de Lest CH, Redegeld FA, etal. Recovery of extracellular vesicles from human breast milk is influenced by sample collection and vesicle isolation procedures. J Extracell Vesicles. 2014; 3: 24215,. doi: http://dx.doi.org/10.3402/jev.v3.24215. eCollection 2014.
25. Lacroix R, Judicone C, Mooberry M, Boucekine M, Key NS, Dignat-George F, etal. Standardization of pre-analytical variables in plasma microparticle determination: results of the International Society on Thrombosis and Haemostasis SSC Collaborative workshop. J Thromb Haemost. 2013. doi: http://dx.doi.org/10.1111/jth.12207.
26. Dahl LB, Dahl IM, Engstrom-Laurent A, Granath K. Concentration and molecular weight of sodium hyaluronate in synovial fluid from patients with rheumatoid arthritis and other arthropathies. Ann Rheum Dis. 1985; 44: 817–22.
27. Murai T. Lipid raft-mediated regulation of hyaluronan-CD44 interactions in inflammation and cancer. Front Immunol. 2015; 6: 420.
28. Nolte-‘t Hoen EN, van der Vlist EJ, Aalberts M, Mertens HC, Bosch BJ, Bartelink W, etal. Quantitative and qualitative flow cytometric analysis of nanosized cell-derived membrane vesicles. Nanomedicine. 2012; 8: 712–20.
29. van der Vlist EJ, Nolte-‘t Hoen EN, Stoorvogel W, Arkesteijn GJ, Wauben MH. Fluorescent labeling of nano-sized vesicles released by cells and subsequent quantitative and qualitative analysis by high-resolution flow cytometry. Nat Protoc. 2012; 7: 1311–26.
30. Arraud N, Linares R, Tan S, Gounou C, Pasquet JM, Mornet S, etal. Extracellular vesicles from blood plasma: determination of their morphology, size, phenotype and concentration. J Thromb Haemost. 2014; 12: 614–27.
31. Lotvall J, Hill AF, Hochberg F, Buzas EI, Di Vizio D, Gardiner C, etal. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J Extracell Vesicles. 2014; 3: 26913,. doi: http://dx.doi.org/10.3402/jev.v3.26913.
32. Graham JM. OptiPrep density gradient solutions for nonmammalian organelles. Sci World J. 2002; 2: 1444–8.
33. Kormelink TG, Arkesteijn GJ, Nauwelaers FA, van den Engh G, Nolte-‘t Hoen EN, Wauben MH. Prerequisites for the analysis and sorting of extracellular vesicle subpopulations by high-resolution flow cytometry. Cytometry A. 2016; 89: 135–47.
34. Bartok B, Firestein GS. Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev. 2010; 233: 233–55.
35. Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol. 2003; 4: 33–45.
36. Mikecz K, Dennis K, Shi M, Kim JH. Modulation of hyaluronan receptor (CD44) function in vivo in a murine model of rheumatoid arthritis. Arthritis Rheum. 1999; 42: 659–68.
37. Hoog JL, Lotvall J. Diversity of extracellular vesicles in human ejaculates revealed by cryo-electron microscopy. J Extracell Vesicles. 2015; 4: 28680,. doi: http://dx.doi.org/10.3402/jev.v4.28680.
38. Yuana Y, Koning RI, Kuil ME, Rensen PC, Koster AJ, Bertina RM, etal. Cryo-electron microscopy of extracellular vesicles in fresh plasma. J Extracell Vesicles. 2013; 2: 21494,. doi: http://dx.doi.org/10.3402/jev.v2i0.21494. eCollection 2013 Dec 31.
39. Linares R, Tan S, Gounou C, Arraud N, Brisson AR. High-speed centrifugation induces aggregation of extracellular vesicles. J Extracell Vesicles. 2015; 4: 29509,. doi: http://dx.doi.org/10.3402/jev.v4.29509.
40. Yuana Y, Boing AN, Grootemaat AE, van der Pol E, Hau CM, Cizmar P, etal. Handling and storage of human body fluids for analysis of extracellular vesicles. J Extracell Vesicles. 2015; 4: 29260,. doi: http://dx.doi.org/10.3402/jev.v4.29260.
41. van Antwerpen R, La Belle M, Navratilova E, Krauss RM. Structural heterogeneity of apoB-containing serum lipoproteins visualized using cryo-electron microscopy. J Lipid Res. 1999; 40: 1827–36.
42. Masuko K, Murata M, Yudoh K, Kato T, Nakamura H. Anti-inflammatory effects of hyaluronan in arthritis therapy: not just for viscosity. Int J Gen Med. 2009; 2: 77–81.
43. Smith MM, Ghosh P. The synthesis of hyaluronic acid by human synovial fibroblasts is influenced by the nature of the hyaluronate in the extracellular environment. Rheumatol Int. 1987; 7: 113–22.
44. Rilla K, Tiihonen R, Kultti A, Tammi M, Tammi R. Pericellular hyaluronan coat visualized in live cells with a fluorescent probe is scaffolded by plasma membrane protrusions. J Histochem Cytochem. 2008; 56: 901–10.
45. Mu W, Rana S, Zoller M. Host matrix modulation by tumor exosomes promotes motility and invasiveness. Neoplasia. 2013; 15: 875–87.
46. Choi DS, Park JO, Jang SC, Yoon YJ, Jung JW, Choi DY, etal. Proteomic analysis of microvesicles derived from human colorectal cancer ascites. Proteomics. 2011; 11: 2745–51.
47. Park JO, Choi DY, Choi DS, Kim HJ, Kang JW, Jung JH, etal. Identification and characterization of proteins isolated from microvesicles derived from human lung cancer pleural effusions. Proteomics. 2013; 13: 2125–34.
48. Majeed M, McQueen F, Yeoman S, McLean L. Relationship between serum hyaluronic acid level and disease activity in early rheumatoid arthritis. Ann Rheum Dis. 2004; 63: 1166–8.
49. Turan Y, Bal S, Gurgan A, Topac H, Koseoglu M. Serum hyaluronan levels in patients with knee osteoarthritis. Clin Rheumatol. 2007; 26: 1293–8.
50. Wyatt HA, Dhawan A, Cheeseman P, Mieli-Vergani G, Price JF. Serum hyaluronic acid concentrations are increased in cystic fibrosis patients with liver disease. Arch Dis Child. 2002; 86: 190–3.
51. Peng C, Wallwiener M, Rudolph A, Cuk K, Eilber U, Celik M, etal. Plasma hyaluronic acid level as a prognostic and monitoring marker of metastatic breast cancer. Int J Cancer. 2016; 138: 2499–509.