Lubricin Surface Modification Improves Extrasynovial Tendon Gliding in a Canine Model in Vitro

Taguchi, Manabu MD; Sun, Yu-Long PhD; Zhao, Chunfeng MD; Zobitz, Mark E. MS; Cha, Chung-Ja PhD; Jay, Gregory D. MD, PhD; An, Kai-Nan PhD; Amadio, Peter C. MD

Journal of Bone & Joint Surgery - American Volume:
doi: 10.2106/JBJS.G.00045
Scientific Articles
Abstract

Background: Lubricin is the principal lubricant in synovial fluid. Although lubricin has been identified in tendons, especially on the surface of intrasynovial tendons such as the flexor digitorum profundus tendon, its ability to improve tendon gliding is unknown. The purpose of this study was to investigate the effects of exogenously applied lubricin on the gliding of extrasynovial tendons in a canine model in vitro.

Methods: Forty peroneus longus tendons, along with the proximal pulley in the ipsilateral hind paw, were harvested from adult mongrel dogs. After the gliding resistance of the normal tendons was measured, the tendons were treated with one of the following solutions: saline solution, lubricin, carbodiimide derivatized gelatin (cd-gelatin), carbodiimide derivatized gelatin with hyaluronic acid (cd-HA-gelatin), or carbodiimide derivatized gelatin to which lubricin had been added in a second step (cd-gelatin plus lubricin). Tendon gliding resistance was measured for 1000 cycles of simulated flexion-extension motion of the tendon. Transverse sections of the tendons were examined qualitatively at 100× magnification to estimate surface smoothness after 1000 cycles.

Results: There was no significant difference in the gliding resistance between the tendons treated with saline solution and those treated with lubricin alone, or between the tendons treated with cd-HA-gelatin and those treated with cd-gelatin plus lubricin; however, the gliding resistance of the tendons treated with cd-gelatin plus lubricin was significantly lower than that of the tendons treated with saline solution, lubricin alone, or cd-gelatin alone (p < 0.05). After 1000 cycles of tendon motion, the gliding resistance of the tendons treated with cd-gelatin plus lubricin decreased 18.7% compared with the resistance before treatment, whereas the gliding resistance of the saline-solution-treated controls increased >400%. The tendon surfaces treated with cd-gelatin plus lubricin or with cd-HA-gelatin appeared smooth even after 1000 cycles of tendon motion, whereas the other surfaces appeared roughened.

Conclusions: While the addition of lubricin alone did not affect friction in this tendon gliding model, the results indicate that lubricin may preferentially adhere to a tendon surface pretreated with cd-gelatin and, when so fixed in place, lubricin does have an important effect on tendon lubrication.

Clinical Relevance: This in vitro canine study suggests that modification of a tendon surface with lubricin can improve the tendon's gliding ability, potentially improving clinical outcomes of extrasynovial tendon grafting.

Author Information

1Biomechanics Laboratory, Mayo Clinic College of Medicine, 200 First Street S.W., Rochester, MN 55905. E-mail address for P.C. Amadio: pamadio@mayo.edu

2Department of Medicine and Division of Engineering, Rhode Island Hospital and Brown University, Providence, RI 02912

Article Outline

Restoration of function of a digit with damage to the flexor tendon, particularly in zone II, is a difficult task. In such cases, tendon grafting still plays an important role in reconstruction to restore finger function. Clinically, most tendon grafts are obtained from extrasynovial tendon sources that are easily harvested without any risk of important functional loss1. However, the resulting finger function after tendon grafting is occasionally poor2,3. Extrasynovial tendon grafts develop more adhesions to the surrounding tissue than do intrasynovial tendon grafts4-6.

The friction of extrasynovial tendons is higher than that of intrasynovial tendons, and repeated motion results in irregularity of collagen fiber bundles on the surface of the peroneus longus tendon7,8. Increased friction on repaired canine flexor digitorum profundus tendons9 is associated with increased adhesion formation. Thus, if extrasynovial tendon friction could be reduced, the outcome of tendon grafting might be improved.

The mechanism of lubrication between the intrasynovial tendon and its pulley has only recently been investigated10. Among the candidates for the principal lubricants are hyaluronic acid11, phospholipids12,13, and lubricin14,15, also known as superficial zone protein and proteoglycan 4 (PRG4).

Lubricin is a mucinous glycoprotein responsible for the boundary lubrication of articular cartilage16,17. It has the same lubricating ability as normal synovial fluid in vitro. Recent studies have indicated that lubricin may play an important role in controlling adhesion-dependent synovial growth18, preventing protein deposition onto cartilage from synovial fluid, and inhibiting the adhesion of synovial cells to the cartilage surface14,19,20 in addition to providing the lubrication necessary for normal joint function16. Lubricin has also been identified in tendons, including the surface of the flexor digitorum profundus tendon14,15.

Lubricin expression is absent in camptodactyly-arthropathy-coxa vara-pericarditis (CACP) syndrome, a syndrome of precocious joint failure associated with noninflammatory synoviocyte hyperplasia and subintimal fibrosis of the joint capsule. It is an autosomal recessive disorder20,21. A number of abnormalities in the function of tendons within tenosynovial sheaths, and tendon adhesion formation, have also been described in CACP syndrome21.

Recently, a carbodiimide derivatized hyaluronic acid preparation was reported to decrease tendon gliding resistance8. This modification is based on the use of EDC (1-ethyl-3[3-dimethylaminopropyl] carbodiimide hydrochloride), an agent that activates the carboxyl groups in the hyaluronic acid molecule to form the intermediate O-acylisourea. The activated intermediate O-acylisourea can then covalently bind to exposed amino groups that exist in the collagenous tendon matrix. However, whether this modification would be effective in binding lubricin is not clear.

The purpose of this study was to investigate the effects of exogenously applied lubricin on the gliding resistance of extrasynovial tendons, with and without preliminary carbodiimide derivatization, after 1000 cycles of tendon motion in a canine model in vitro.

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Materials and Methods

Specimen Preparation

Forty canine peroneus longus tendons were obtained from twenty adult mongrel dogs that had been killed for other projects approved by our Institutional Animal Care and Use Committee. The superficial aspect of the paratenon was removed, as recommended when extrasynovial tendons are used clinically for tendon grafting22,23.

The second digit was dissected from each hindpaw. The proximal pulley, proximal and middle phalanges, and flexor digitorum superficialis tendon and insertion were preserved. The proximal interphalangeal joint was fixed in full extension with a longitudinal 1.5-mm Kirschner wire.

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Tendon Surface Modification

The peroneus longus tendons were randomly assigned to five treatment groups of eight tendons each (Table I). Lubricin was purified from bovine synovial fluid as reported in a previous study24 and preserved at −20°C until use.

In the cd-gelatin, cd-HA-gelatin, and cd-gelatin plus lubricin groups, 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide hydrochloride (EDC) and N-hydroxysuccinimide (NHS) with or without hyaluronic acid (HA) were mixed and put into a syringe, and the gelatin was put into another syringe. These two syringes were connected with a common needle, and their contents were injected simultaneously into one dish. Tendons were immersed in the combined solution for thirty seconds and then allowed to “cure” for ten minutes while wrapped in a smooth rubber sheet within a saline-solution-moistened towel to keep them hydrated until grafting. After the tendons were treated with cd-gelatin or cd-HA-gelatin, the resulting layer of gel on the tendon surface was rather thick (∼0.5 to 2 mm). To allow the gel to pass easily and with a uniform thickness through the pulley, the outer portion of the gel was removed by several initial passes under the pulley. The tendon was placed under the pulley, the tendon ends were grasped with forceps, and the entire tendon was then passed under the pulley in a to-and-fro manner. Because we wished to add the lubricin to the attached gelatin, and not remove it with any excess gelatin, the lubricin was applied to the surface after the excess gelatin was removed. After five cycles of tendon motion (flexion-extension simulation), the tendon was immersed in 260 μg/mL of lubricin for thirty minutes. In the saline-solution and lubricin groups, the tendons were immersed in saline solution and 260 μg/mL of lubricin, respectively, for thirty minutes and then tested.

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Measurement of Frictional Force

We used a modified version of a previously described and validated testing device to measure the gliding resistance between the peroneus longus tendon and the ipsilateral proximal pulley of the second digit25-27. Each digit was secured on the custom-made device with the volar side upward in a saline solution bath (ISOTEMP 202; Fisher Scientific, Houston, Texas) at 37°C. The measurement system consisted of one mechanical actuator with a linear potentiometer, two custom-made tensile load transducers, and a mechanical pulley (Fig. 1). The load transducers were connected to the distal and proximal ends of the peroneus longus tendon. A 4.9-N weight was connected to the distal transducer (F1 in Fig. 1) to maintain tension on the peroneus longus tendon. The proximal load transducer (F2) was connected to the custom-made mechanical actuator with a small linear slide driven by a precision gear head direct-current motor. On the basis of the experience in previous studies25,28,29, a set arc of contact, 30° and 20° between the horizontal plane and the proximal and distal transducer cables, respectively, was used to measure the gliding resistance. The tendon was pulled proximally by the actuator against the 4.9-N weight at a rate of 2 mm/s. The excursion distance was 14 mm, which is an average distance for canine digital flexor tendon excursion30. The force at the proximal and distal tendon ends and the tendon excursion were recorded.

As described in previous publications7, the force differential between the proximal and distal tendon ends represents the gliding resistance of the peroneus longus tendon against the ipsilateral proximal pulley of the second digit. During flexion, the gliding resistance is equal to F2flexion – F1 flexion, where F2flexion is the proximal force and F1flexion is the distal force. During extension, the gliding resistance is equal to F1extension − F2extension, where F1extension is the proximal force and F2extension is the distal force. The gliding resistance was averaged as follows: (F2flexion − F1flexion) + (F1extension − F2extension)/2. Since F1flexion = F1extension = 4.9 N, the previous equation can be simplified as: (F2flexion – F2extension)/2.

The data for the normal peroneus longus tendon were initially recorded for one cycle. After treatment of the tendon surface, the data were recorded after every fifty cycles up to 500 cycles and then after every 100 cycles up to 1000 cycles.

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Statistical Analysis

The gliding resistance prior to the surface treatment and after 1000 cycles of tendon motion was analyzed with use of one-way analysis of variance. A Tukey-Kramer post-hoc test for individual comparisons was used if there was a significant difference. A significance level of p < 0.05 was used in all cases.

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Histological Evaluation

After measurement of gliding resistance, the harvested tendons were saturated in a 20% sucrose buffer for cryoprotection at 4°C, mounted and frozen in Tissue-Tek (Sakura Finetek, Torrance, California), and subsequently sectioned transversely at 10 μm with use of a cryostat (CM1850; Leica, Wetzlar, Germany). The sections were collected on charged glass slides (Fisher Scientific, Pittsburgh, Pennsylvania), air-dried, and refrigerated overnight. The sections were then fixed in a solution of 4% paraformaldehyde in 0.1M phosphate buffer, pH 7.4, for five minutes and stained with hematoxylin and eosin. The tendon surfaces were then assessed qualitatively for smoothness. We also included a normal tendon with no treatment and no tendon motion for comparison.

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Results

There was no significant difference in the gliding resistance of the peroneus longus tendon before treatment among the five groups (p = 0.167) (Fig. 2). After 1000 cycles of tendon motion, the mean gliding resistance (and standard deviation) of the peroneus longus tendons treated with saline solution, lubricin, cd-gelatin, cd-HA-gelatin, and cd-gelatin plus lubricin was 0.91 ± 0.11 N, 0.91 ± 0.13 N, 0.34 ± 0.17 N, 0.21 ± 0.07 N, and 0.11 ± 0.01 N, respectively (Fig. 2). There was no significant difference in the gliding resistance after 1000 cycles between the tendons treated with saline solution and those treated with 260 μg/mL of lubricin alone. The gliding resistance of the tendons treated with cd-gelatin, cd-HA-gelatin, or cd-gelatin plus lubricin was significantly lower than that of the saline-solution-treated controls after 1000 cycles (p < 0.05). The tendons treated with cd-gelatin plus lubricin had the lowest gliding resistance after 1000 cycles, which decreased 18.7% compared with the resistance prior to treatment, whereas the gliding resistance of the saline-solution-treated controls increased 418.3%. Moreover, the gliding resistance of the tendons treated with cd-gelatin plus lubricin was significantly lower than that of the cd-gelatin-treated tendons after 1000 cycles (p < 0.05). Although the gliding resistance of the tendons treated with cd-gelatin plus lubricin trended lower than that of the cd-HA-gelatin-treated tendons, the two groups were not significantly different.

The gliding resistance of the peroneus longus tendons treated with saline solution and lubricin alone increased rapidly over the first 400 cycles and then increased more slowly over the next 600 cycles (Fig. 3). The gliding resistance of the tendons in the cd-gelatin and cd-HA-gelatin groups increased at a more gradual rate over the 1000 cycles. The gliding resistance of the tendons treated with cd-gelatin plus lubricin decreased within the first fifty cycles and then stabilized for the remaining cycles up to 1000 cycles.

On histological examination, the tendon surfaces treated with saline solution, lubricin, or cd-gelatin alone appeared rough, while the tendon surfaces treated with cd-gelatin plus lubricin or cd-HA-gelatin were still smooth even after 1000 cycles of tendon motion (Fig. 4).

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Discussion

The friction on a normal intrasynovial tendon is very small and remains stable with repeated cycles of tendon motion because of the smooth surface and the lubrication mechanism7,11. Under smaller loads, an intrasynovial tendon is provided with hydrodynamic lubrication by an intervening fluid film. With larger loads, this intervening fluid film is squeezed out and boundary lubrication becomes the dominant interaction10.

Lubricin is the principal lubricant of articular cartilage16,31. The abundance of negatively charged sugars O-linked to the mucin domain of lubricin creates strong hydration24 or steric repulsive32 forces that enable the protein to act as a boundary lubricant. Lubricin has been noted to decrease the coefficient of friction in a number of test bearing systems including a rabbit phalanx sliding against glass16, latex apposed to glass17, and most recently cartilage apposed to cartilage33. The third study33 also showed that lubricin combined with hyaluronic acid further decreased friction, a finding that was observed in the latex-glass-bearing study as well17. Our study suggests that lubricin may also be effective in reducing the gliding resistance of tendons.

The experimental groups in our study were chosen to assess the effects of lubricin, alone and in the presence of an activated tendon surface pretreated with carbodiimide derivatized gelatin to expose multiple carboxyl groups for linkage to the lubricin. The rationale for our use of carbodiimide derivatization is that the EDC activates the carboxyl groups in the gelatin molecule and forms the intermediate O-acylisourea, which can chemically bind to exposed amino groups in both the tendon matrix and the lubricin. The increased availability of covalent bond opportunities should, according to this rationale, increase the binding of lubricin on the tendon surface. Our comparison groups included the activated surface alone, a saline-solution control, and a treatment known to improve tendon lubrication (a carbodiimide-activated combination of hyaluronan and gelatin)8.

In our study, we found no significant difference in the gliding resistance after 1000 cycles between the saline-solution controls and the tendons treated with lubricin alone. The tendon surfaces in these two groups were also similarly rough after 1000 cycles. These results suggest that when lubricin was simply placed on the surface of peroneus longus tendons it did not bind strongly to that surface, was easily rubbed away with repeated tendon motion, and did not function as a lubricant on the rougher surface of these extrasynovial tendons. The cd-gelatin, cd-HA-gelatin, and combination of cd-gelatin and lubricin all improved the gliding resistance significantly compared with that of the controls. The frictional force in the tendons treated with cd-gelatin plus lubricin was significantly lower than the frictional force in the tendons treated with lubricin alone. This suggests that lubricin preferentially adheres to an activated tendon surface, in this case one pretreated with cd-gelatin. The cd-gelatin can also fill any gaps and or irregularities on the peroneus longus tendon surface and this may provide a smoother surface for the lubricin binding.

Hyaluronic acid also has a lubricating effect, and its effectiveness as a lubricant has been shown to be maximized when it is attached to a surface34. In this study, the difference in gliding resistance between the group treated with cd-gelatin plus lubricin and that treated with cd-HA-gelatin was not significant, but there was a trend toward lower gliding resistance of the tendons treated with cd-gelatin plus lubricin.

A smooth surface was observed on the tendons treated with cd-gelatin plus lubricin or with cd-HA-gelatin, even after 1000 cycles of repetitive motion. While it is possible that the smooth surface was partly due to carbodiimide-activated native collagen on the tendon surface, the effect of the treatment with cd-gelatin plus lubricin or with cd-HA-gelatin was much greater than that with cd-gelatin alone, suggesting that cross-linking of native collagen alone is not sufficient to overcome the adverse effects of repetitive motion.

The principal limitation of this study is that it was an in vitro investigation. However, we believe that lubricin would have an even greater effect on tendon gliding in vivo, since it also plays an important cytoprotective role by preventing cellular adhesion to the tendon surface14.

In summary, we have shown that the addition of lubricin to a peroneus longus tendon surface pretreated with cd-gelatin can significantly reduce the gliding resistance of the tendon and maintain a qualitatively smooth tendon surface after 1000 cycles of simulated flexion-extension tendon motion. These findings may have important implications for our understanding of lubrication as it affects normal tendon function. In addition, the findings suggest a possible role for lubricin as a therapeutic adjunct, which might be helpful in ameliorating the adverse effects of tendon injury on tendon gliding and lubrication.

Disclosure: In support of their research for or preparation of this work, one or more of the authors received, in any one year, outside funding or grants in excess of $10,000 from the National Institutes of Health/National Institutes of Arthritis and Musculoskeletal and Skin Diseases (AR44391). Neither they nor a member of their immediate families received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, division, center, clinical practice, or other charitable or nonprofit organization with which the authors, or a member of their immediate families, are affiliated or associated.

Investigation performed at the Mayo Clinic College of Medicine, Rochester, Minnesota

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