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Home / Equine Research Bank / Cells / Hyaluronic Acid as Macromolecular Crowder in Equine Adipose-...
Cells2021; 10(4); 859; doi: 10.3390/cells10040859

Hyaluronic Acid as Macromolecular Crowder in Equine Adipose-Derived Stem Cell Cultures.

Abstract: The use of macromolecular crowding in the development of extracellular matrix-rich cell-assembled tissue equivalents is continuously gaining pace in regenerative engineering. Despite the significant advancements in the field, the optimal macromolecular crowder still remains elusive. Herein, the physicochemical properties of different concentrations of different molecular weights hyaluronic acid (HA) and their influence on equine adipose-derived stem cell cultures were assessed. Within the different concentrations and molecular weight HAs, the 10 mg/mL 100 kDa and 500 kDa HAs exhibited the highest negative charge and hydrodynamic radius, and the 10 mg/mL 100 kDa HA exhibited the lowest polydispersity index and the highest % fraction volume occupancy. Although HA had the potential to act as a macromolecular crowding agent, it did not outperform carrageenan and Ficoll, the most widely used macromolecular crowding molecules, in enhanced and accelerated collagen I, collagen III and collagen IV deposition.
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Publication Date: 2021-04-09 PubMed ID: 33918830PubMed Central: PMC8070604DOI: 10.3390/cells10040859Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article investigates the suitability of different configurations of hyaluronic acid (HA) as a macromolecular crowder in the culture of equine adipose-derived stem cells, comparing performance against commonly used crowding agents, carrageenan and Ficoll.

Objective of the Research

  • The study aims to explore and identify the optimal macromolecular crowder for use in the development of extracellular matrix-rich cell-assembled tissue equivalents, a crucial component in regenerative engineering. More specifically, the research investigates the efficacy of hyaluronic acid (HA) in different concentrations and molecular weights as a potential candidate.

Methodology

  • The physicochemical properties of HA in different concentrations and weights were evaluated for their influence on equine adipose-derived stem cell cultures. Key metrics assessed include negative charge, hydrodynamic radius, polydispersity index, and % fraction volume occupancy.
  • Specifically, the 10 mg/mL 100kDa and 500kDa configurations of HA were examined for their negative charge and hydrodynamic radius. The 10 mg/mL 100kDa HA was also evaluated for its polydispersity index and volume occupancy.

Findings

  • The findings revealed that while HA demonstrated potential as a macromolecular crowding agent, it did not exceed the performance of carrageenan and Ficoll, the most popular macromolecular crowding agents. This was validated by assessing the accelerated deposition of collagen types I, III, and IV.
  • The study found 10 mg/mL 100kDa and 500kDa HA having the highest negative charge and hydrodynamic radius. The 10 mg/mL 100kDa HA configuration exhibited the lowest polydispersity index and the highest % fraction volume occupancy.

Implications

  • This research contributes insights towards finding the best macromolecular crowder for use in extracellular matrix-rich cell-assembled tissue equivalents. It helps in understanding how HA, carrageenan and Ficoll influence the growth and development of stem cell cultures, key to enhancing regenerative medicine techniques.
  • While HA demonstrated key attributes for a crowding agent, the fact that it was outperformed by carrageenan and Ficoll suggests more research is needed to optimize its use or identify alternative compounds.

Cite This Article

APA
Garnica-Galvez S, Korntner SH, Skoufos I, Tzora A, Diakakis N, Prassinos N, Zeugolis DI. (2021). Hyaluronic Acid as Macromolecular Crowder in Equine Adipose-Derived Stem Cell Cultures. Cells, 10(4), 859. https://doi.org/10.3390/cells10040859

Publication

Cells
ISSN: 2073-4409
NlmUniqueID: 101600052
Country: Switzerland
Language: English
Volume: 10
Issue: 4
PII: 859

Researcher Affiliations

Garnica-Galvez, Sergio
  • Laboratory of Animal Science, Nutrition and Biotechnology, Department of Agriculture, University of Ioannina, 47100 Arta, Greece.
  • School of Veterinary Medicine, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece.
  • Regenerative, Modular & Developmental Engineering Laboratory (REMODEL), Biomedical Sciences Building, National University of Ireland Galway (NUI Galway), H92 W2TY Galway, Ireland.
Korntner, Stefanie H
  • Regenerative, Modular & Developmental Engineering Laboratory (REMODEL), Biomedical Sciences Building, National University of Ireland Galway (NUI Galway), H92 W2TY Galway, Ireland.
  • Science Foundation Ireland (SFI) Centre for Research in Medical Devices (CÚRAM), Biomedical Sciences Building, National University of Ireland Galway (NUI Galway), H92 W2TY Galway, Ireland.
Skoufos, Ioannis
  • Laboratory of Animal Science, Nutrition and Biotechnology, Department of Agriculture, University of Ioannina, 47100 Arta, Greece.
Tzora, Athina
  • Laboratory of Animal Science, Nutrition and Biotechnology, Department of Agriculture, University of Ioannina, 47100 Arta, Greece.
Diakakis, Nikolaos
  • School of Veterinary Medicine, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece.
Prassinos, Nikitas
  • School of Veterinary Medicine, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece.
Zeugolis, Dimitrios I
  • Regenerative, Modular & Developmental Engineering Laboratory (REMODEL), Biomedical Sciences Building, National University of Ireland Galway (NUI Galway), H92 W2TY Galway, Ireland.
  • Science Foundation Ireland (SFI) Centre for Research in Medical Devices (CÚRAM), Biomedical Sciences Building, National University of Ireland Galway (NUI Galway), H92 W2TY Galway, Ireland.
  • Regenerative, Modular & Developmental Engineering Laboratory (REMODEL), Faculty of Biomedical Sciences, Università della Svizzera Italiana (USI), 6904 Lugano, Switzerland.
  • Regenerative, Modular & Developmental Engineering Laboratory (REMODEL), School of Mechanical and Materials Engineering, University College Dublin (UCD), D04 V1W8 Dublin, Ireland.

MeSH Terms

  • Adipose Tissue / cytology
  • Animals
  • Cell Proliferation
  • Cell Shape
  • Cell Survival
  • Cells, Cultured
  • Dynamic Light Scattering
  • Horses
  • Hyaluronic Acid / metabolism
  • Macromolecular Substances / metabolism
  • Solubility
  • Stem Cells / cytology

Grant Funding

  • 866126 / European Research Council
  • 676338 / H2020 Marie Sku0142odowska-Curie Actions
  • 15/CDA/3629; 19/FFP/6982; 13/RC/2073_2. / Science Foundation Ireland

Conflict of Interest Statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

This article includes 104 references
  1. Miyagawa S, Domae K, Yoshikawa Y, Fukushima S, Nakamura T, Saito A, Sakata Y, Hamada S, Toda K, Pak K, Takeuchi M, Sawa Y. Phase I Clinical Trial of Autologous Stem Cell-Sheet Transplantation Therapy for Treating Cardiomyopathy.. J Am Heart Assoc 2017 Apr 5;6(4).
    doi: 10.1161/JAHA.116.003918pmc: PMC5532985pubmed: 28381469google scholar: lookup
  2. Sato M, Yamato M, Mitani G, Takagaki T, Hamahashi K, Nakamura Y, Ishihara M, Matoba R, Kobayashi H, Okano T, Mochida J, Watanabe M. Combined surgery and chondrocyte cell-sheet transplantation improves clinical and structural outcomes in knee osteoarthritis.. NPJ Regen Med 2019;4:4.
    doi: 10.1038/s41536-019-0069-4pmc: PMC6384900pubmed: 30820353google scholar: lookup
  3. da Cruz L, Fynes K, Georgiadis O, Kerby J, Luo YH, Ahmado A, Vernon A, Daniels JT, Nommiste B, Hasan SM, Gooljar SB, Carr AF, Vugler A, Ramsden CM, Bictash M, Fenster M, Steer J, Harbinson T, Wilbrey A, Tufail A, Feng G, Whitlock M, Robson AG, Holder GE, Sagoo MS, Loudon PT, Whiting P, Coffey PJ. Phase 1 clinical study of an embryonic stem cell-derived retinal pigment epithelium patch in age-related macular degeneration.. Nat Biotechnol 2018 Apr;36(4):328-337.
    doi: 10.1038/nbt.4114pubmed: 29553577google scholar: lookup
  4. Hirsch T, Rothoeft T, Teig N, Bauer JW, Pellegrini G, De Rosa L, Scaglione D, Reichelt J, Klausegger A, Kneisz D, Romano O, Secone Seconetti A, Contin R, Enzo E, Jurman I, Carulli S, Jacobsen F, Luecke T, Lehnhardt M, Fischer M, Kueckelhaus M, Quaglino D, Morgante M, Bicciato S, Bondanza S, De Luca M. Regeneration of the entire human epidermis using transgenic stem cells.. Nature 2017 Nov 16;551(7680):327-332.
    doi: 10.1038/nature24487pmc: PMC6283270pubmed: 29144448google scholar: lookup
  5. L'Heureux N, Dusserre N, Konig G, Victor B, Keire P, Wight TN, Chronos NA, Kyles AE, Gregory CR, Hoyt G, Robbins RC, McAllister TN. Human tissue-engineered blood vessels for adult arterial revascularization.. Nat Med 2006 Mar;12(3):361-5.
    doi: 10.1038/nm1364pmc: PMC1513140pubmed: 16491087google scholar: lookup
  6. Hernandez-Segura A, Nehme J, Demaria M. Hallmarks of Cellular Senescence.. Trends Cell Biol 2018 Jun;28(6):436-453.
    doi: 10.1016/j.tcb.2018.02.001pubmed: 29477613google scholar: lookup
  7. Ten Ham RMT, Hövels AM, Hoekman J, Frederix GWJ, Leufkens HGM, Klungel OH, Jedema I, Veld SAJ, Nikolic T, Van Pel M, Zwaginga JJ, Lin F, de Goede AL, Schreibelt G, Budde S, de Vries IJM, Wilkie GM, Dolstra H, Ovelgönne H, Meij P, Mountford JC, Turner ML, Hoefnagel MHN. What does cell therapy manufacturing cost? A framework and methodology to facilitate academic and other small-scale cell therapy manufacturing costings.. Cytotherapy 2020 Jul;22(7):388-397.
    doi: 10.1016/j.jcyt.2020.03.432pubmed: 32414635google scholar: lookup
  8. Bettinger CJ, Langer R, Borenstein JT. Engineering substrate topography at the micro- and nanoscale to control cell function.. Angew Chem Int Ed Engl 2009;48(30):5406-15.
    doi: 10.1002/anie.200805179pmc: PMC2834566pubmed: 19492373google scholar: lookup
  9. Nemir S, West JL. Synthetic materials in the study of cell response to substrate rigidity.. Ann Biomed Eng 2010 Jan;38(1):2-20.
    doi: 10.1007/s10439-009-9811-1pubmed: 19816774google scholar: lookup
  10. Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche.. Cell Stem Cell 2010 Aug 6;7(2):150-61.
    doi: 10.1016/j.stem.2010.07.007pubmed: 20682444google scholar: lookup
  11. Delaine-Smith RM, Reilly GC. The effects of mechanical loading on mesenchymal stem cell differentiation and matrix production.. Vitam Horm 2011;87:417-80.
    pubmed: 22127254doi: 10.1016/b978-0-12-386015-6.00039-1google scholar: lookup
  12. Lee D, Kim DW, Cho JY. Role of growth factors in hematopoietic stem cell niche.. Cell Biol Toxicol 2020 Apr;36(2):131-144.
    doi: 10.1007/s10565-019-09510-7pubmed: 31897822google scholar: lookup
  13. Satyam A, Kumar P, Fan X, Gorelov A, Rochev Y, Joshi L, Peinado H, Lyden D, Thomas B, Rodriguez B, Raghunath M, Pandit A, Zeugolis D. Macromolecular crowding meets tissue engineering by self-assembly: a paradigm shift in regenerative medicine.. Adv Mater 2014 May 21;26(19):3024-34.
    doi: 10.1002/adma.201304428pubmed: 24505025google scholar: lookup
  14. Gaspar D, Fuller KP, Zeugolis DI. Polydispersity and negative charge are key modulators of extracellular matrix deposition under macromolecular crowding conditions.. Acta Biomater 2019 Apr 1;88:197-210.
    doi: 10.1016/j.actbio.2019.02.050pubmed: 30831324google scholar: lookup
  15. De Pieri A, Rana S, Korntner S, Zeugolis DI. Seaweed polysaccharides as macromolecular crowding agents.. Int J Biol Macromol 2020 Dec 1;164:434-446.
    doi: 10.1016/j.ijbiomac.2020.07.087pubmed: 32679331google scholar: lookup
  16. Miyahara M, Njieha FK, Prockop DJ. Formation of collagen fibrils in vitro by cleavage of procollagen with procollagen proteinases.. J Biol Chem 1982 Jul 25;257(14):8442-8.
    doi: 10.1016/S0021-9258(18)34351-5pubmed: 6806297google scholar: lookup
  17. Zeugolis DI. Bioinspired in vitro microenvironments to control cell fate: focus on macromolecular crowding.. Am J Physiol Cell Physiol 2021 May 1;320(5):C842-C849.
    pubmed: 33656930doi: 10.1152/ajpcell.00380.2020google scholar: lookup
  18. Kuznetsova IM, Zaslavsky BY, Breydo L, Turoverov KK, Uversky VN. Beyond the excluded volume effects: mechanistic complexity of the crowded milieu.. Molecules 2015 Jan 14;20(1):1377-409.
    doi: 10.3390/molecules20011377pmc: PMC6272634pubmed: 25594347google scholar: lookup
  19. Ando T, Skolnick J. Crowding and hydrodynamic interactions likely dominate in vivo macromolecular motion.. Proc Natl Acad Sci U S A 2010 Oct 26;107(43):18457-62.
    doi: 10.1073/pnas.1011354107pmc: PMC2973006pubmed: 20937902google scholar: lookup
  20. Miyoshi D, Sugimoto N. Molecular crowding effects on structure and stability of DNA.. Biochimie 2008 Jul;90(7):1040-51.
    doi: 10.1016/j.biochi.2008.02.009pubmed: 18331845google scholar: lookup
  21. Ramisetty SK, Langlete P, Lale R, Dias RS. In vitro studies of DNA condensation by bridging protein in a crowding environment.. Int J Biol Macromol 2017 Oct;103:845-853.
    doi: 10.1016/j.ijbiomac.2017.05.079pubmed: 28536019google scholar: lookup
  22. Akabayov B, Akabayov SR, Lee SJ, Wagner G, Richardson CC. Impact of macromolecular crowding on DNA replication.. Nat Commun 2013;4:1615.
    doi: 10.1038/ncomms2620pmc: PMC3666333pubmed: 23511479google scholar: lookup
  23. Chung S, Lerner E, Jin Y, Kim S, Alhadid Y, Grimaud LW, Zhang IX, Knobler CM, Gelbart WM, Weiss S. The effect of macromolecular crowding on single-round transcription by Escherichia coli RNA polymerase.. Nucleic Acids Res 2019 Feb 20;47(3):1440-1450.
    doi: 10.1093/nar/gky1277pmc: PMC6379708pubmed: 30590739google scholar: lookup
  24. Wirth AJ, Gruebele M. Quinary protein structure and the consequences of crowding in living cells: leaving the test-tube behind.. Bioessays 2013 Nov;35(11):984-93.
    doi: 10.1002/bies.201300080pubmed: 23943406google scholar: lookup
  25. Christiansen A, Wang Q, Cheung MS, Wittung-Stafshede P. Effects of macromolecular crowding agents on protein folding in vitro and in silico.. Biophys Rev 2013 Jun;5(2):137-145.
    doi: 10.1007/s12551-013-0108-0pmc: PMC5418436pubmed: 28510156google scholar: lookup
  26. Guseman AJ, Speer SL, Perez Goncalves GM, Pielak GJ. Surface Charge Modulates Protein-Protein Interactions in Physiologically Relevant Environments.. Biochemistry 2018 Mar 20;57(11):1681-1684.
    doi: 10.1021/acs.biochem.8b00061pmc: PMC5977980pubmed: 29473738google scholar: lookup
  27. Kang H, Toan NM, Hyeon C, Thirumalai D. Unexpected Swelling of Stiff DNA in a Polydisperse Crowded Environment.. J Am Chem Soc 2015 Sep 2;137(34):10970-8.
    doi: 10.1021/jacs.5b04531pubmed: 26267166google scholar: lookup
  28. Sharp KA. Analysis of the size dependence of macromolecular crowding shows that smaller is better.. Proc Natl Acad Sci U S A 2015 Jun 30;112(26):7990-5.
    doi: 10.1073/pnas.1505396112pmc: PMC4491746pubmed: 26080429google scholar: lookup
  29. Skóra T, Vaghefikia F, Fitter J, Kondrat S. Macromolecular Crowding: How Shape and Interactions Affect Diffusion.. J Phys Chem B 2020 Sep 3;124(35):7537-7543.
    doi: 10.1021/acs.jpcb.0c04846pubmed: 32790396google scholar: lookup
  30. von Bülow S, Siggel M, Linke M, Hummer G. Dynamic cluster formation determines viscosity and diffusion in dense protein solutions.. Proc Natl Acad Sci U S A 2019 May 14;116(20):9843-9852.
    doi: 10.1073/pnas.1817564116pmc: PMC6525548pubmed: 31036655google scholar: lookup
  31. Kumar P, Satyam A, Fan X, Collin E, Rochev Y, Rodriguez BJ, Gorelov A, Dillon S, Joshi L, Raghunath M, Pandit A, Zeugolis DI. Macromolecularly crowded in vitro microenvironments accelerate the production of extracellular matrix-rich supramolecular assemblies.. Sci Rep 2015 Mar 4;5:8729.
    doi: 10.1038/srep08729pmc: PMC4348624pubmed: 25736020google scholar: lookup
  32. Rashid R, Lim NS, Chee SM, Png SN, Wohland T, Raghunath M. Novel use for polyvinylpyrrolidone as a macromolecular crowder for enhanced extracellular matrix deposition and cell proliferation.. Tissue Eng Part C Methods 2014 Dec;20(12):994-1002.
    doi: 10.1089/ten.tec.2013.0733pmc: PMC4241873pubmed: 24665935google scholar: lookup
  33. McKim JM, Willoughby JA, Blakemore WR, Weiner ML. A critical review of “A randomized trial of the effects of the no-carrageenan diet on ulcerative colitis disease activity (Nutr. Healthy Aging. 2017, 4, 181–192).”. J. Nutr. Health Aging 2019;5:149–158.
    doi: 10.3233/NHA-180051google scholar: lookup
  34. Shang Q, Sun W, Shan X, Jiang H, Cai C, Hao J, Li G, Yu G. Carrageenan-induced colitis is associated with decreased population of anti-inflammatory bacterium, Akkermansia muciniphila, in the gut microbiota of C57BL/6J mice.. Toxicol Lett 2017 Sep 5;279:87-95.
    doi: 10.1016/j.toxlet.2017.07.904pubmed: 28778519google scholar: lookup
  35. Mi Y, Chin YX, Cao WX, Chang YG, Lim PE, Xue CH, Tang QJ. Native κ-carrageenan induced-colitis is related to host intestinal microecology.. Int J Biol Macromol 2020 Mar 15;147:284-294.
    doi: 10.1016/j.ijbiomac.2020.01.072pubmed: 31926226google scholar: lookup
  36. Shendi D, Marzi J, Linthicum W, Rickards AJ, Dolivo DM, Keller S, Kauss MA, Wen Q, McDevitt TC, Dominko T, Schenke-Layland K, Rolle MW. Hyaluronic acid as a macromolecular crowding agent for production of cell-derived matrices.. Acta Biomater 2019 Dec;100:292-305.
    doi: 10.1016/j.actbio.2019.09.042pubmed: 31568877google scholar: lookup
  37. Majewski GP, Rodan K, Fields K, Falla TJ. Characterization of bound water in skin hydrators prepared with and without a 3D3P interpenetrating polymer network.. Skin Res Technol 2019 Mar;25(2):150-157.
    doi: 10.1111/srt.12624pmc: PMC7379968pubmed: 30112768google scholar: lookup
  38. Papakonstantinou E, Roth M, Karakiulakis G. Hyaluronic acid: A key molecule in skin aging.. Dermatoendocrinol 2012 Jul 1;4(3):253-8.
    doi: 10.4161/derm.21923pmc: PMC3583886pubmed: 23467280google scholar: lookup
  39. Cowman MK. Hyaluronan and Hyaluronan Fragments.. Adv Carbohydr Chem Biochem 2017;74:1-59.
    doi: 10.1016/bs.accb.2017.10.001pubmed: 29173725google scholar: lookup
  40. Uphoff CC, Drexler HG. Detection of Mycoplasma contamination in cell cultures.. Curr Protoc Mol Biol 2014 Apr 14;106:28.4.1-28.4.14.
    doi: 10.1002/0471142727.mb2804s106pubmed: 24733240google scholar: lookup
  41. Ranera B, Remacha AR, Álvarez-Arguedas S, Romero A, Vázquez FJ, Zaragoza P, Martín-Burriel I, Rodellar C. Effect of hypoxia on equine mesenchymal stem cells derived from bone marrow and adipose tissue.. BMC Vet Res 2012 Aug 22;8:142.
    doi: 10.1186/1746-6148-8-142pmc: PMC3483288pubmed: 22913590google scholar: lookup
  42. Ranera B, Lyahyai J, Romero A, Vázquez FJ, Remacha AR, Bernal ML, Zaragoza P, Rodellar C, Martín-Burriel I. Immunophenotype and gene expression profiles of cell surface markers of mesenchymal stem cells derived from equine bone marrow and adipose tissue.. Vet Immunol Immunopathol 2011 Nov 15;144(1-2):147-54.
    doi: 10.1016/j.vetimm.2011.06.033pubmed: 21782255google scholar: lookup
  43. Maia L, Landim-Alvarenga FC, Da Mota LS, De Assis Golim M, Laufer-Amorim R, De Vita B, Barberini DJ, Listoni AJ, De Moraes CN, Heckler MC, Amorim RM. Immunophenotypic, immunocytochemistry, ultrastructural, and cytogenetic characterization of mesenchymal stem cells from equine bone marrow.. Microsc Res Tech 2013 Jun;76(6):618-24.
    doi: 10.1002/jemt.22208pubmed: 23533133google scholar: lookup
  44. Barberini DJ, Freitas NP, Magnoni MS, Maia L, Listoni AJ, Heckler MC, Sudano MJ, Golim MA, da Cruz Landim-Alvarenga F, Amorim RM. Equine mesenchymal stem cells from bone marrow, adipose tissue and umbilical cord: immunophenotypic characterization and differentiation potential.. Stem Cell Res Ther 2014 Feb 21;5(1):25.
    doi: 10.1186/scrt414pmc: PMC4055040pubmed: 24559797google scholar: lookup
  45. Fülber J, Maria DA, da Silva LC, Massoco CO, Agreste F, Baccarin RY. Comparative study of equine mesenchymal stem cells from healthy and injured synovial tissues: an in vitro assessment.. Stem Cell Res Ther 2016 Mar 5;7:35.
    doi: 10.1186/s13287-016-0294-3pmc: PMC4779201pubmed: 26944403google scholar: lookup
  46. Shikh Alsook MK, Gabriel A, Piret J, Waroux O, Tonus C, Connan D, Baise E, Antoine N. Tissues from equine cadaver ligaments up to 72 hours of post-mortem: a promising reservoir of stem cells.. Stem Cell Res Ther 2015 Dec 18;6:253.
    doi: 10.1186/s13287-015-0250-7pmc: PMC4683699pubmed: 26684484google scholar: lookup
  47. Chen C, Loe F, Blocki A, Peng Y, Raghunath M. Applying macromolecular crowding to enhance extracellular matrix deposition and its remodeling in vitro for tissue engineering and cell-based therapies.. Adv Drug Deliv Rev 2011 Apr 30;63(4-5):277-90.
    doi: 10.1016/j.addr.2011.03.003pubmed: 21392551google scholar: lookup
  48. Capella-Monsonís H, Coentro JQ, Graceffa V, Wu Z, Zeugolis DI. An experimental toolbox for characterization of mammalian collagen type I in biological specimens.. Nat Protoc 2018 Mar;13(3):507-529.
    doi: 10.1038/nprot.2017.117pubmed: 29446773google scholar: lookup
  49. Cigognini D, Gaspar D, Kumar P, Satyam A, Alagesan S, Sanz-Nogués C, Griffin M, O'Brien T, Pandit A, Zeugolis DI. Macromolecular crowding meets oxygen tension in human mesenchymal stem cell culture - A step closer to physiologically relevant in vitro organogenesis.. Sci Rep 2016 Aug 1;6:30746.
    doi: 10.1038/srep30746pmc: PMC4967872pubmed: 27478033google scholar: lookup
  50. Chen CZ, Peng YX, Wang ZB, Fish PV, Kaar JL, Koepsel RR, Russell AJ, Lareu RR, Raghunath M. The Scar-in-a-Jar: studying potential antifibrotic compounds from the epigenetic to extracellular level in a single well.. Br J Pharmacol 2009 Nov;158(5):1196-209.
    doi: 10.1111/j.1476-5381.2009.00387.xpmc: PMC2782330pubmed: 19785660google scholar: lookup
  51. Prewitz MC, Stißel A, Friedrichs J, Träber N, Vogler S, Bornhäuser M, Werner C. Extracellular matrix deposition of bone marrow stroma enhanced by macromolecular crowding.. Biomaterials 2015 Dec;73:60-9.
    doi: 10.1016/j.biomaterials.2015.09.014pubmed: 26398310google scholar: lookup
  52. Graceffa V, Zeugolis DI. Macromolecular crowding as a means to assess the effectiveness of chondrogenic media.. J Tissue Eng Regen Med 2019 Feb;13(2):217-231.
    doi: 10.1002/term.2783pubmed: 30549442google scholar: lookup
  53. . Food Additives Permitted for Direct Addition to Food for Human Consumption; Folic Acid. Final rule.. Fed Regist 2016 Apr 15;81(73):22176-83.
    pubmed: 27101640
  54. Papalia R, Russo F, Torre G, Albo E, Grimaldi V, Papalia G, Sterzi S, Vadalà G, Bressi F, Denaro V. Hybrid hyaluronic acid versus high molecular weight hyaluronic acid for the treatment of osteoarthritis in obese patients.. J Biol Regul Homeost Agents 2017 Dec 27;31(4 Suppl 2):103-109.
    pubmed: 29202568
  55. Awartani FA, Tatakis DN. Interdental papilla loss: treatment by hyaluronic acid gel injection: a case series.. Clin Oral Investig 2016 Sep;20(7):1775-80.
    doi: 10.1007/s00784-015-1677-zpubmed: 26613740google scholar: lookup
  56. Cavallini M, Papagni M, Ryder TJ, Patalano M. Skin Quality Improvement With VYC-12, a New Injectable Hyaluronic Acid: Objective Results Using Digital Analysis.. Dermatol Surg 2019 Dec;45(12):1598-1604.
    doi: 10.1097/DSS.0000000000001932pubmed: 30893167google scholar: lookup
  57. Wang F, Garza LA, Kang S, Varani J, Orringer JS, Fisher GJ, Voorhees JJ. In vivo stimulation of de novo collagen production caused by cross-linked hyaluronic acid dermal filler injections in photodamaged human skin.. Arch Dermatol 2007 Feb;143(2):155-63.
    doi: 10.1001/archderm.143.2.155pubmed: 17309996google scholar: lookup
  58. Monaco G, El Haj AJ, Alini M, Stoddart MJ. Sodium Hyaluronate Supplemented Culture Media as a New hMSC Chondrogenic Differentiation Media-Model for in vitro/ex vivo Screening of Potential Cartilage Repair Therapies.. Front Bioeng Biotechnol 2020;8:243.
    doi: 10.3389/fbioe.2020.00243pmc: PMC7136394pubmed: 32296689google scholar: lookup
  59. Gallorini M, Berardi AC, Berardocco M, Gissi C, Maffulli N, Cataldi A, Oliva F. Hyaluronic acid increases tendon derived cell viability and proliferation in vitro: comparative study of two different hyaluronic acid preparations by molecular weight.. Muscles Ligaments Tendons J 2017 Apr-Jun;7(2):208-214.
    doi: 10.32098/mltj.02.2017.02pmc: PMC5725168pubmed: 29264330google scholar: lookup
  60. Osti L, Berardocco M, di Giacomo V, Di Bernardo G, Oliva F, Berardi AC. Hyaluronic acid increases tendon derived cell viability and collagen type I expression in vitro: Comparative study of four different Hyaluronic acid preparations by molecular weight.. BMC Musculoskelet Disord 2015 Oct 6;16:284.
    doi: 10.1186/s12891-015-0735-7pmc: PMC4596363pubmed: 26444018google scholar: lookup
  61. Pilloni A, Bernard GW. The effect of hyaluronan on mouse intramembranous osteogenesis in vitro.. Cell Tissue Res 1998 Nov;294(2):323-33.
    doi: 10.1007/s004410051182pubmed: 9799448google scholar: lookup
  62. Karna E, Miltyk W, Pałka JA, Jarzabek K, Wołczyński S. Hyaluronic acid counteracts interleukin-1-induced inhibition of collagen biosynthesis in cultured human chondrocytes.. Pharmacol Res 2006 Oct;54(4):275-81.
    doi: 10.1016/j.phrs.2006.06.002pubmed: 16884915google scholar: lookup
  63. Huang L, Cheng YY, Koo PL, Lee KM, Qin L, Cheng JC, Kumta SM. The effect of hyaluronan on osteoblast proliferation and differentiation in rat calvarial-derived cell cultures.. J Biomed Mater Res A 2003 Sep 15;66(4):880-4.
    doi: 10.1002/jbm.a.10535pubmed: 12926041google scholar: lookup
  64. Hegewald AA, Ringe J, Bartel J, Krüger I, Notter M, Barnewitz D, Kaps C, Sittinger M. Hyaluronic acid and autologous synovial fluid induce chondrogenic differentiation of equine mesenchymal stem cells: a preliminary study.. Tissue Cell 2004 Dec;36(6):431-8.
    doi: 10.1016/j.tice.2004.07.003pubmed: 15533458google scholar: lookup
  65. Zou L, Zou X, Chen L, Li H, Mygind T, Kassem M, Bünger C. Effect of hyaluronan on osteogenic differentiation of porcine bone marrow stromal cells in vitro.. J Orthop Res 2008 May;26(5):713-20.
    doi: 10.1002/jor.20539pubmed: 18050326google scholar: lookup
  66. Li L, Ni R, Shao Y, Mao S. Carrageenan and its applications in drug delivery.. Carbohydr Polym 2014 Mar 15;103:1-11.
    doi: 10.1016/j.carbpol.2013.12.008pubmed: 24528694google scholar: lookup
  67. Zhu Y, Potschka M, Dubin P, Cai CH. A method for the quantitation of charge by size exclusion chromatography demonstrated with components of ficoll 400. Macromol. Chem. Phys. 2001;202:61–72.
    doi: 10.1002/1521-3935(20010101)202:1<61::AID-MACP61>3.0.CO;2-Hgoogle scholar: lookup
  68. Larrañeta E, Henry M, Irwin NJ, Trotter J, Perminova AA, Donnelly RF. Synthesis and characterization of hyaluronic acid hydrogels crosslinked using a solvent-free process for potential biomedical applications.. Carbohydr Polym 2018 Feb 1;181:1194-1205.
    doi: 10.1016/j.carbpol.2017.12.015pmc: PMC5742632pubmed: 29253949google scholar: lookup
  69. Snetkov P, Zakharova K, Morozkina S, Olekhnovich R, Uspenskaya M. Hyaluronic Acid: The Influence of Molecular Weight on Structural, Physical, Physico-Chemical, and Degradable Properties of Biopolymer.. Polymers (Basel) 2020 Aug 11;12(8).
    doi: 10.3390/polym12081800pmc: PMC7464276pubmed: 32796708google scholar: lookup
  70. Hascall V, Esko J. Hyaluronan. Essentials of Glycobiology 3rd ed. Cold Spring Harbor Laboratory Press; Cold Spring Harbor, NY, USA: 2017.
  71. Tantra R, Schulze P, Quincey P. Effect of nanoparticle concentration on zeta-potential measurement results and reproducibility. Particuology 2010;8:279–285.
    doi: 10.1016/j.partic.2010.01.003google scholar: lookup
  72. Bhattacharjee S. DLS and zeta potential - What they are and what they are not?. J Control Release 2016 Aug 10;235:337-351.
    doi: 10.1016/j.jconrel.2016.06.017pubmed: 27297779google scholar: lookup
  73. Panchal J, Kotarek J, Marszal E, Topp EM. Analyzing subvisible particles in protein drug products: a comparison of dynamic light scattering (DLS) and resonant mass measurement (RMM).. AAPS J 2014 May;16(3):440-51.
    doi: 10.1208/s12248-014-9579-6pmc: PMC4012052pubmed: 24570341google scholar: lookup
  74. Mudalige T, Qu H, Van Haute D, Ansar SM, Paredes A, Ingle T. Chapter 11—Characterization of nanomaterials: Tools and challenges. Nanomaterials for Food Applications Elsevier; Amsterdam, The Netherlands: 2019. pp. 313–353.
    doi: 10.1016/B978-0-12-814130-4.00011-7google scholar: lookup
  75. Lareu RR, Subramhanya KH, Peng Y, Benny P, Chen C, Wang Z, Rajagopalan R, Raghunath M. Collagen matrix deposition is dramatically enhanced in vitro when crowded with charged macromolecules: the biological relevance of the excluded volume effect.. FEBS Lett 2007 Jun 12;581(14):2709-14.
    doi: 10.1016/j.febslet.2007.05.020pubmed: 17531987google scholar: lookup
  76. Shahid S, Hassan MI, Islam A, Ahmad F. Size-dependent studies of macromolecular crowding on the thermodynamic stability, structure and functional activity of proteins: in vitro and in silico approaches.. Biochim Biophys Acta Gen Subj 2017 Feb;1861(2):178-197.
    doi: 10.1016/j.bbagen.2016.11.014pubmed: 27842220google scholar: lookup
  77. Gaspar D, Ryan CNM, Zeugolis DI. Multifactorial bottom-up bioengineering approaches for the development of living tissue substitutes.. FASEB J 2019 Apr;33(4):5741-5754.
    doi: 10.1096/fj.201802451Rpubmed: 30681885google scholar: lookup
  78. Graceffa V, Zeugolis DI. Carrageenan enhances chondrogenesis and osteogenesis in human bone marrow stem cell culture.. Eur Cell Mater 2019 Apr 30;37:310-332.
    doi: 10.22203/eCM.v037a19pubmed: 31038192google scholar: lookup
  79. Zeiger AS, Loe FC, Li R, Raghunath M, Van Vliet KJ. Macromolecular crowding directs extracellular matrix organization and mesenchymal stem cell behavior.. PLoS One 2012;7(5):e37904.
    doi: 10.1371/journal.pone.0037904pmc: PMC3359376pubmed: 22649562google scholar: lookup
  80. Patrikoski M, Lee MHC, Mäkinen L, Ang XM, Mannerström B, Raghunath M, Miettinen S. Effects of Macromolecular Crowding on Human Adipose Stem Cell Culture in Fetal Bovine Serum, Human Serum, and Defined Xeno-Free/Serum-Free Conditions.. Stem Cells Int 2017;2017:6909163.
    doi: 10.1155/2017/6909163pmc: PMC5390653pubmed: 28465691google scholar: lookup
  81. Kumar P, Satyam A, Fan X, Rochev Y, Rodriguez BJ, Gorelov A, Joshi L, Raghunath M, Pandit A, Zeugolis DI. Accelerated Development of Supramolecular Corneal Stromal-Like Assemblies from Corneal Fibroblasts in the Presence of Macromolecular Crowders.. Tissue Eng Part C Methods 2015 Jul;21(7):660-70.
    doi: 10.1089/ten.tec.2014.0387pubmed: 25535812google scholar: lookup
  82. Tsiapalis D, De Pieri A, Spanoudes K, Sallent I, Kearns S, Kelly JL, Raghunath M, Zeugolis DI. The synergistic effect of low oxygen tension and macromolecular crowding in the development of extracellular matrix-rich tendon equivalents.. Biofabrication 2020 Feb 26;12(2):025018.
    doi: 10.1088/1758-5090/ab6412pubmed: 31855856google scholar: lookup
  83. Moreno A, Martínez A, Olmedillas S, Bello S, de Miguel F. Hyaluronic acid effect on adipose-derived stem cells. Biological in vitro evaluation.. Rev Esp Cir Ortop Traumatol 2015 Jul-Aug;59(4):215-21.
    doi: 10.1016/j.recote.2015.04.004pubmed: 25481699google scholar: lookup
  84. Kawasaki K, Ochi M, Uchio Y, Adachi N, Matsusaki M. Hyaluronic acid enhances proliferation and chondroitin sulfate synthesis in cultured chondrocytes embedded in collagen gels.. J Cell Physiol 1999 May;179(2):142-8.
    doi: 10.1002/(SICI)1097-4652(199905)179:2<142::AID-JCP4>3.0.CO;2-Qpubmed: 10199553google scholar: lookup
  85. Mast BA, Diegelmann RF, Krummel TM, Cohen IK. Hyaluronic acid modulates proliferation, collagen and protein synthesis of cultured fetal fibroblasts.. Matrix 1993 Nov;13(6):441-6.
    doi: 10.1016/S0934-8832(11)80110-1pubmed: 8309423google scholar: lookup
  86. Goldberg RL, Toole BP. Hyaluronate inhibition of cell proliferation.. Arthritis Rheum 1987 Jul;30(7):769-78.
    doi: 10.1002/art.1780300707pubmed: 3619961google scholar: lookup
  87. Wiig M, Abrahamsson SO, Lundborg G. Effects of hyaluronan on cell proliferation and collagen synthesis: a study of rabbit flexor tendons in vitro.. J Hand Surg Am 1996 Jul;21(4):599-604.
    doi: 10.1016/S0363-5023(96)80010-4pubmed: 8842950google scholar: lookup
  88. Sorushanova A, Delgado LM, Wu Z, Shologu N, Kshirsagar A, Raghunath R, Mullen AM, Bayon Y, Pandit A, Raghunath M, Zeugolis DI. The Collagen Suprafamily: From Biosynthesis to Advanced Biomaterial Development.. Adv Mater 2019 Jan;31(1):e1801651.
    doi: 10.1002/adma.201801651pubmed: 30126066google scholar: lookup
  89. Liu X, Wu H, Byrne M, Krane S, Jaenisch R. Type III collagen is crucial for collagen I fibrillogenesis and for normal cardiovascular development.. Proc Natl Acad Sci U S A 1997 Mar 4;94(5):1852-6.
    doi: 10.1073/pnas.94.5.1852pmc: PMC20006pubmed: 9050868google scholar: lookup
  90. Abreu-Velez AM, Howard MS. Collagen IV in Normal Skin and in Pathological Processes.. N Am J Med Sci 2012 Jan;4(1):1-8.
    doi: 10.4103/1947-2714.92892pmc: PMC3289483pubmed: 22393540google scholar: lookup
  91. Graham J, Raghunath M, Vogel V. Fibrillar fibronectin plays a key role as nucleator of collagen I polymerization during macromolecular crowding-enhanced matrix assembly.. Biomater Sci 2019 Nov 1;7(11):4519-4535.
    doi: 10.1039/C9BM00868Cpmc: PMC6810780pubmed: 31436263google scholar: lookup
  92. Lee CF, Bird S, Shaw M, Jean L, Vaux DJ. Combined effects of agitation, macromolecular crowding, and interfaces on amyloidogenesis.. J Biol Chem 2012 Nov 2;287(45):38006-19.
    doi: 10.1074/jbc.M112.400580pmc: PMC3488071pubmed: 22988239google scholar: lookup
  93. Chen E, Kliger DS. Time-Resolved Linear Dichroism Measurements of Carbonmonoxy Myoglobin as a Probe of the Microviscosity in Crowded Environments.. J Phys Chem B 2017 Jul 27;121(29):7064-7074.
    doi: 10.1021/acs.jpcb.7b04107pubmed: 28703591google scholar: lookup
  94. Damodarasamy M, Johnson RS, Bentov I, MacCoss MJ, Vernon RB, Reed MJ. Hyaluronan enhances wound repair and increases collagen III in aged dermal wounds.. Wound Repair Regen 2014 Jul-Aug;22(4):521-6.
    doi: 10.1111/wrr.12192pmc: PMC4822517pubmed: 25041621google scholar: lookup
  95. David-Raoudi M, Tranchepain F, Deschrevel B, Vincent JC, Bogdanowicz P, Boumediene K, Pujol JP. Differential effects of hyaluronan and its fragments on fibroblasts: relation to wound healing.. Wound Repair Regen 2008 Mar-Apr;16(2):274-87.
    doi: 10.1111/j.1524-475X.2007.00342.xpubmed: 18282267google scholar: lookup
  96. Donejko M, Przylipiak A, Rysiak E, Głuszuk K, Surażyński A. Influence of caffeine and hyaluronic acid on collagen biosynthesis in human skin fibroblasts.. Drug Des Devel Ther 2014;8:1923-8.
    pmc: PMC4206198pubmed: 25342885doi: 10.2147/dddt.s69791google scholar: lookup
  97. Croce MA, Dyne K, Boraldi F, Quaglino D Jr, Cetta G, Tiozzo R, Pasquali Ronchetti I. Hyaluronan affects protein and collagen synthesis by in vitro human skin fibroblasts.. Tissue Cell 2001 Aug;33(4):326-31.
    doi: 10.1054/tice.2001.0180pubmed: 11521947google scholar: lookup
  98. Satyam A, Kumar P, Cigognini D, Pandit A, Zeugolis DI. Low, but not too low, oxygen tension and macromolecular crowding accelerate extracellular matrix deposition in human dermal fibroblast culture.. Acta Biomater 2016 Oct 15;44:221-31.
    doi: 10.1016/j.actbio.2016.08.008pubmed: 27506127google scholar: lookup
  99. Tsiapalis D, Kearns S, Kelly JL, Zeugolis DI. Growth factor and macromolecular crowding supplementation in human tenocyte culture. Biomater. Biosyst. 2021;1:100009.
    doi: 10.1016/j.bbiosy.2021.100009google scholar: lookup
  100. Huang L, Gu H, Burd A. A reappraisal of the biological effects of hyaluronan on human dermal fibroblast.. J Biomed Mater Res A 2009 Sep 15;90(4):1177-85.
    doi: 10.1002/jbm.a.32173pubmed: 18671256google scholar: lookup
  101. Ang XM, Lee MH, Blocki A, Chen C, Ong LL, Asada HH, Sheppard A, Raghunath M. Macromolecular crowding amplifies adipogenesis of human bone marrow-derived mesenchymal stem cells by enhancing the pro-adipogenic microenvironment.. Tissue Eng Part A 2014 Mar;20(5-6):966-81.
    doi: 10.1089/ten.tea.2013.0337pmc: PMC3938936pubmed: 24147829google scholar: lookup
  102. Lee MH, Goralczyk AG, Kriszt R, Ang XM, Badowski C, Li Y, Summers SA, Toh SA, Yassin MS, Shabbir A, Sheppard A, Raghunath M. ECM microenvironment unlocks brown adipogenic potential of adult human bone marrow-derived MSCs.. Sci Rep 2016 Feb 17;6:21173.
    doi: 10.1038/srep21173pmc: PMC4756694pubmed: 26883894google scholar: lookup
  103. Obrink B. A study of the interactions between monomeric tropocollagen and glycosaminoglycans.. Eur J Biochem 1973 Mar 1;33(2):387-400.
    doi: 10.1111/j.1432-1033.1973.tb02695.xpubmed: 4266508google scholar: lookup
  104. Obrink B. The influence of glycosaminoglycans on the formation of fibers from monomeric tropocollagen in vitro.. Eur J Biochem 1973 Apr 2;34(1):129-37.
    doi: 10.1111/j.1432-1033.1973.tb02739.xpubmed: 4267112google scholar: lookup

Citations

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  1. Später T, Assunção M, Lit KK, Gong G, Wang X, Chen YY, Rao Y, Li Y, Yiu CHK, Laschke MW, Menger MD, Wang D, Tuan RS, Khoo KH, Raghunath M, Guo J, Blocki A. Engineering microparticles based on solidified stem cell secretome with an augmented pro-angiogenic factor portfolio for therapeutic angiogenesis.. Bioact Mater 2022 Nov;17:526-541.
    doi: 10.1016/j.bioactmat.2022.03.015pubmed: 35846945google scholar: lookup
  2. Li C, Zhang X, Dong M, Han X. Progress on Crowding Effect in Cell-like Structures.. Membranes (Basel) 2022 Jun 3;12(6).
    doi: 10.3390/membranes12060593pubmed: 35736300google scholar: lookup
  3. Rampin A, Skoufos I, Raghunath M, Tzora A, Diakakis N, Prassinos N, Zeugolis DI. Allogeneic Serum and Macromolecular Crowding Maintain Native Equine Tenocyte Function in Culture.. Cells 2022 May 5;11(9).
    doi: 10.3390/cells11091562pubmed: 35563866google scholar: lookup
  4. Laurent A, Porcello A, Fernandez PG, Jeannerat A, Peneveyre C, Abdel-Sayed P, Scaletta C, Hirt-Burri N, Michetti M, de Buys Roessingh A, Raffoul W, Allémann E, Jordan O, Applegate LA. Combination of Hyaluronan and Lyophilized Progenitor Cell Derivatives: Stabilization of Functional Hydrogel Products for Therapeutic Management of Tendinous Tissue Disorders.. Pharmaceutics 2021 Dec 19;13(12).
    doi: 10.3390/pharmaceutics13122196pubmed: 34959477google scholar: lookup
  5. Ryan CNM, Pugliese E, Shologu N, Gaspar D, Rooney P, Islam MN, O'Riordan A, Biggs MJ, Griffin MD, Zeugolis DI. A combined physicochemical approach towards human tenocyte phenotype maintenance.. Mater Today Bio 2021 Sep;12:100130.
    doi: 10.1016/j.mtbio.2021.100130pubmed: 34632361google scholar: lookup
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