Calcium ions have a detrimental impact on the boundary lubrication property of hyaluronic acid and lubricin (PRG-4) both alone and in combination

Mingyu Han; Matthew J Russo; Pauline E Desroches; Saimon M Silva; Anita F Quigley; Robert M I Kapsa; Simon E Moulton; George W Greene

doi:10.1016/j.colsurfb.2023.113741

Calcium ions have a detrimental impact on the boundary lubrication property of hyaluronic acid and lubricin (PRG-4) both alone and in combination

Colloids Surf B Biointerfaces. 2024 Feb:234:113741. doi: 10.1016/j.colsurfb.2023.113741. Epub 2024 Jan 2.

Authors

Mingyu Han¹, Matthew J Russo², Pauline E Desroches³, Saimon M Silva⁴, Anita F Quigley⁵, Robert M I Kapsa⁵, Simon E Moulton⁶, George W Greene⁷

Affiliations

¹ Institute for Frontier Materials and ARC Centre of Excellence for Electromaterials Science, Deakin University, Melbourne, Victoria 3216, Australia; ARC Centre of Excellence for Electromaterials Science, Faculty of Science, Engineering and Technology, Swinburne University of Technology, Hawthorn, Victoria 3122, Australia; Commonwealth Scientific and Industrial Research Organisation (CSIRO), Agriculture and Food, 671 Sneydes Road, Private Bag 16, Werribee, Victoria 3030, Australia. Electronic address: mingyu.han@csiro.au.
² Institute for Frontier Materials and ARC Centre of Excellence for Electromaterials Science, Deakin University, Melbourne, Victoria 3216, Australia; Department of Chemistry, Colorado State University, Fort Collins, CO 80523-1872, USA.
³ Institute for Frontier Materials and ARC Centre of Excellence for Electromaterials Science, Deakin University, Melbourne, Victoria 3216, Australia; ARC Centre of Excellence for Electromaterials Science, Faculty of Science, Engineering and Technology, Swinburne University of Technology, Hawthorn, Victoria 3122, Australia.
⁴ The Aikenhead Centre for Medical Discovery, St Vincent's Hospital Melbourne, Fitzroy, Victoria 3065, Australia; Iverson Health Innovation Research Institute, Swinburne University of Technology, Australia; Department of Chemistry, Colorado State University, Fort Collins, CO 80523-1872, USA; Department of Chemistry and Physics, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, Victoria 3086, Australia.
⁵ ARC Centre of Excellence for Electromaterials Science, Faculty of Science, Engineering and Technology, Swinburne University of Technology, Hawthorn, Victoria 3122, Australia; School of Electrical and Biomedical Engineering, RMIT University, Melbourne, Victoria 3001, Australia.
⁶ ARC Centre of Excellence for Electromaterials Science, Faculty of Science, Engineering and Technology, Swinburne University of Technology, Hawthorn, Victoria 3122, Australia; The Aikenhead Centre for Medical Discovery, St Vincent's Hospital Melbourne, Fitzroy, Victoria 3065, Australia; Iverson Health Innovation Research Institute, Swinburne University of Technology, Australia.
⁷ Institute for Frontier Materials and ARC Centre of Excellence for Electromaterials Science, Deakin University, Melbourne, Victoria 3216, Australia; ARC Centre of Excellence for Electromaterials Science, Faculty of Science, Engineering and Technology, Swinburne University of Technology, Hawthorn, Victoria 3122, Australia; Department of Chemistry and Physics, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, Victoria 3086, Australia. Electronic address: W.Greene@latrobe.edu.au.

PMID: 38184943
DOI: 10.1016/j.colsurfb.2023.113741

Abstract

Cartilage demineralisation in Osteoarthritis (OA) patients can elevate calcium ion levels in synovial fluid, as evidenced by the prevalence of precipitated calcium phosphate crystals in OA synovial fluid. Although it has been reported that there is a potential connection between elevated concentrations of calcium ions and a deterioration in the lubrication and wear resistance of cartilage tissues, the mechanism behind the strong link between calcium ion concentration and decreased lubrication performance is unclear. In this work, the AFM friction, imaging, and normal force distance measurements were used to investigate the lubrication performances of hyaluronic acid (HA), Lubricin (LUB), and HA-LUB complex in the presence of calcium ions (5 mM, 15 mM, and 30 mM), to understand the possible mechanism behind the change of lubrication property. The results of AFM friction measurements suggest that introducing calcium ions to the environment effectively eliminated the lubrication ability of HA and HA-LUB, especially with relatively low loading applied. The AFM images indicate that it is unlikely that structural or morphological changes in the surface-bound layer upon calcium ions addition are primarily responsible for the friction results demonstrated. Further, the poor correlation between the effect of calcium ions on the adhesion forces and its impact on friction suggests that the decrease in the lubricating ability of both layers is likely a result of changes in the hydration of the HA-LUB surface bound layers than changes in intermolecular or intramolecular binding. This work provides the first experimental evidence lending towards the relationship between bone demineralisation and articular cartilage degradation at the onset of OA and the mechanism through which elevated calcium levels in the synovial fluid act on joint lubrication.

Keywords: Boundary lubrication; Calcium ions; Cartilage; Friction; Hyaluronic acid; Lubricin.

MeSH terms

Calcium / metabolism
Cartilage, Articular* / metabolism
Friction
Glycoproteins*
Humans
Hyaluronic Acid / chemistry
Lubrication
Osteoarthritis*
Synovial Fluid / chemistry

Substances

lubricin
Hyaluronic Acid
Calcium
Glycoproteins