Understanding structure-function relationships in the temporomandibular joint (TMJ) disc is a critical first step toward creating functional tissue replacements for the large population of patients suffering from TMJ disc disorders. While many of these relationships have been identified for the collagenous fraction of the disc, this same understanding is lacking for the next most abundant extracellular matrix component, sulfated glycosaminoglycans (GAGs). Though GAGs are known to play a major role in maintaining compressive integrity in GAG-rich tissues such as articular cartilage, their role in fibrocartilaginous tissues in which GAGs are much less abundant is not clearly defined. Therefore, this study investigates the contribution of GAGs to the regional viscoelastic compressive properties of the temporomandibular joint (TMJ) disc. Chondroitinase ABC (C-ABC) was used to deplete GAGs in five different disc regions, and the time course for >95% GAG removal was defined. The compressive properties of GAG depleted regional specimens were then compared to non-treated controls using an unconfined compression stress-relaxation test. Additionally, treated and non-treated specimens were assayed biochemically and histologically to confirm GAG removal. Compared to untreated controls, the only regions affected by GAG removal in terms of biomechanical properties were in the intermediate zone, the most GAG-rich portion of the disc. Without GAGs, all intermediate zone regions showed decreased tissue viscosity, and the intermediate zone lateral region also showed a 12.5% decrease in modulus of relaxation. However, in the anterior and posterior band regions, no change in compressive properties was observed following GAG depletion, though these regions showed the highest compressive properties overall. Although GAGs are not the major extracellular matrix molecule of the TMJ disc, they are responsible for some of the viscoelastic compressive properties of the tissue. Furthermore, the mechanical role of sulfated GAGs in the disc varies regionally in the tissue, and GAG abundance does not always correlate with higher compressive properties. Overall, this study found that sulfated GAGs are important to TMJ disc mechanics in the intermediate zone, an important finding for establishing design characteristics for future tissue engineering efforts.

References

References
1.
Gillbe
,
G. V.
, 1975, “
The Function of the Disc of the Temporomandibular Joint
,”
J. Prosthet. Dent.
,
33
(
2
), pp.
196
204
.
2.
Solberg
,
W. K.
,
Woo
,
M. W.
, and
Houston
,
J. B.
, 1979, “
Prevalence of Mandibular Dysfunction in Young Adults
,”
J. Am. Dent. Assoc.
,
98
(
1
), pp.
25
34
.
3.
Wilkes
,
C. H.
, 1989, “
Internal Derangements of the Temporomandibular Joint. Pathological Variations
,”
Arch. Otolaryngol. Head Neck Surg.
,
115
(
4
), pp.
469
477
.
4.
Farrar
,
W. B.
, and
McCarty
,
W. L.
, Jr.
, 1979, “
The TMJ Dilemma
,”
J. Ala. Dent. Assoc.
,
63
(
1
), pp.
19
26
.
5.
Tanaka
,
E.
,
Detamore
,
M. S.
, and
Mercuri
,
L. G.
, 2008, “
Degenerative Disorders of the Temporomandibular Joint: Etiology, Diagnosis, and Treatment
,”
J. Dent. Res.
,
87
(
4
), pp.
296
307
.
6.
Nakano
,
T.
, and
Scott
,
P. G.
, 1989, “
A Quantitative Chemical Study of Glycosaminoglycans in the Articular Disc of the Bovine Temporomandibular Joint
,”
Arch. Oral Biol.
,
34
(
9
), pp.
749
757
.
7.
Almarza
,
A. J.
,
Bean
,
A. C.
,
Baggett
,
L. S.
, and
Athanasiou
,
K. A.
, 2006, “
Biochemical Analysis of the Porcine Temporomandibular Joint Disc
,”
Br. J. Oral Maxillofac. Surg.
,
44
(
2
), pp.
124
128
.
8.
Shengyi
,
T.
, and
Xu
,
Y.
, 1991, “
Biomechanical Properties and Collagen Fiber Orientation of TMJ Discs in Dogs: Part 1. Gross Anatomy and Collagen Fiber Orientation of the Discs
,”
J. Craniomandib. Disord.
,
5
(
1
), pp.
28
34
.
9.
Scapino
,
R. P.
,
Canham
,
P. B.
,
Finlay
,
H. M.
, and
Mills
,
D. K.
, 1996, “
The Behaviour of Collagen Fibres in Stress Relaxation and Stress Distribution in the Jaw-Joint Disc of Rabbits
,”
Arch. Oral Biol.
,
41
(
11
), pp.
1039
1052
.
10.
Detamore
,
M. S.
,
Orfanos
,
J. G.
,
Almarza
,
A. J.
,
French
,
M. M.
,
Wong
,
M. E.
, and
Athanasiou
,
K. A.
, 2005, “
Quantitative Analysis and Comparative Regional Investigation of the Extracellular Matrix of the Porcine Temporomandibular Joint Disc
,”
Matrix Biol.
,
24
(
1
), pp.
45
57
.
11.
Detamore
,
M. S.
, and
Athanasiou
,
K. A.
, 2003, “
Tensile Properties of the Porcine Temporomandibular Joint Disc
,”
J. Biomech. Eng.
,
125
(
4
), pp.
558
565
.
12.
Beatty
,
M. W.
,
Bruno
,
M. J.
,
Iwasaki
,
L. R.
, and
Nickel
,
J. C.
, 2001, “
Strain Rate Dependent Orthotropic Properties of Pristine and Impulsively Loaded Porcine Temporomandibular Joint Disk
,”
J. Biomed. Mater. Res.
,
57
(
1
), pp.
25
34
.
13.
Tanne
,
K.
,
Tanaka
,
E.
, and
Sakuda
,
M.
, 1991, “
The Elastic Modulus of the Temporomandibular Joint Disc from Adult Dogs
,”
J. Dent. Res.
,
70
(
12
), pp.
1545
1548
.
14.
Allen
,
K. D.
, and
Athanasiou
,
K. A.
, 2006, “
Viscoelastic Characterization of the Porcine Temporomandibular Joint Disc under Unconfined Compression
,”
J. Biomech.
,
39
(
2
), pp.
312
322
.
15.
Kalpakci
,
K. N.
,
Willard
,
V. P.
,
Wong
,
M. E.
, and
Athanasiou
,
K. A.
, 2011, “
An Interspecies Comparison of the Temporomandibular Joint Disc
,”
J. Dent. Res.
,
90
(
2
), pp.
193
198
.
16.
Mizoguchi
,
I.
,
Scott
,
P. G.
,
Dodd
,
C. M.
,
Rahemtulla
,
F.
,
Sasano
,
Y.
,
Kuwabara
,
M.
,
Satoh
,
S.
,
Saitoh
,
S.
,
Hatakeyama
,
Y.
,
Kagayama
,
M.
, and
Mitani
,
H.
, 1998, “
An Immunohistochemical Study of the Localization of Biglycan, Decorin and Large Chondroitin-Sulphate Proteoglycan in Adult Rat Temporomandibular Joint Disc
,”
Arch. Oral Biol.
,
43
(
11
), pp.
889
898
.
17.
Nakano
,
T.
, and
Scott
,
P. G.
, 1996, “
Changes in the Chemical Composition of the Bovine Temporomandibular Joint Disc with Age
,”
Arch. Oral Biol.
,
41
(
8–9
), pp.
845
853
.
18.
Basalo
,
I. M.
,
Mauck
,
R. L.
,
Kelly
,
T. A.
,
Nicoll
,
S. B.
,
Chen
,
F. H.
,
Hung
,
C. T.
, and
Ateshian
,
G. A.
, 2004, “
Cartilage Interstitial Fluid Load Support in Unconfined Compressionfollowing Enzymatic Digestion
,”
J. Biomech. Eng.
,
126
(
6
), pp.
779
786
.
19.
Hamai
,
A.
,
Hashimoto
,
N.
,
Mochizuki
,
H.
,
Kato
,
F.
,
Makiguchi
,
Y.
,
Horie
,
K.
, and
Suzuki
,
S.
, 1997, “
Two Distinct Chondroitin Sulfate ABC Lyases. An Endoeliminase Yielding Tetrasaccharides and an Exoeliminase Preferentially Acting on Oligosaccharides
,”
J. Biol. Chem.
,
272
(
14
), pp.
9123
9130
.
20.
Katta
,
J.
,
Stapleton
,
T.
,
Ingham
,
E.
,
Jin
,
Z. M.
, and
Fisher
,
J.
, 2008, “
The Effect of Glycosaminoglycan Depletion on the Friction and Deformation of Articular Cartilage
,”
Proc. Inst. Mech. Eng. Part H, J. Eng. Med.
,
222
(
1
), pp.
1
11
.
21.
Korhonen
,
R. K.
,
Laasanen
,
M. S.
,
Toyras
,
J.
,
Lappalainen
,
R.
,
Helminen
,
H. J.
, and
Jurvelin
,
J. S.
, 2003, “
Fibril Reinforced Poroelastic Model Predicts Specifically Mechanical Behavior of Normal, Proteoglycan Depleted and Collagen Degraded Articular Cartilage
,”
J. Biomech.
,
36
(
9
), pp.
1373
1379
.
22.
Yerramalli
,
C. S.
,
Chou
,
A. I.
,
Miller
,
G. J.
,
Nicoll
,
S. B.
,
Chin
,
K. R.
, and
Elliott
,
D. M.
, 2007, “
The Effect of Nucleus Pulposus Crosslinking and Glycosaminoglycan Degradation on Disc Mechanical Function
,”
Biomech. Model Mechanobiol.
,
6
(
1–2
), pp.
13
20
.
23.
Boxberger
,
J. I.
,
Orlansky
,
A. S.
,
Sen
,
S.
, and
Elliott
,
D. M.
, 2009, “
Reduced Nucleus Pulposus Glycosaminoglycan Content Alters Intervertebral Disc Dynamic Viscoelastic Mechanics
,”
J. Biomech.
,
42
(
12
), pp.
1941
1946
.
24.
Henninger
,
H. B.
,
Underwood
,
C. J.
,
Ateshian
,
G. A.
, and
Weiss
,
J. A.
, 2010, “
Effect of Sulfated Glycosaminoglycan Digestion on the Transverse Permeability of Medial Collateral Ligament
,”
J. Biomech.
,
43
(
13
), pp.
2567
2573
.
25.
Allen
,
K. D.
, and
Athanasiou
,
K. A.
, 2005, “
A Surface-Regional and Freeze-Thaw Characterization of the Porcine Temporomandibular Joint Disc
,”
Ann. Biomed. Eng.
,
33
(
7
), pp.
951
962
.
26.
Fontenot
,
M. G.
, 1985, “
The Viscoelasticity of Human Temporomandibular-Joint Disks
,”
Am. J. Phys. Anthropol.
,
66
(
2
), pp.
168
169
.
27.
Kim
,
K. W.
,
Wong
,
M. E.
,
Helfrick
,
J. F.
,
Thomas
,
J. B.
, and
Athanasiou
,
K. A.
, 2003, “
Biomechanical Tissue Characterization of the Superior Joint Space of the Porcine Temporomandibular Joint
,”
Ann. Biomed. Eng.
,
31
(
8
), pp.
924
930
.
28.
Kuo
,
J.
,
Zhang
,
L.
,
Bacro
,
T.
, and
Yao
,
H.
, 2010, “
The Region-Dependent Biphasic Viscoelastic Properties of Human Temporomandibular Joint Discs under Confined Compression
,”
J. Biomech.
,
43
(
7
), pp.
1316
1321
.
29.
del Pozo
,
R.
,
Tanaka
,
E.
,
Tanaka
,
M.
,
Okazaki
,
M.
, and
Tanne
,
K.
, 2002, “
The Regional Difference of Viscoelastic Property of Bovine Temporomandibular Joint Disc in Compressive Stress-Relaxation
,”
Med. Eng. Phys.
,
24
(
3
), pp.
165
171
.
30.
Tanaka
,
E.
,
Hirose
,
M.
,
Yamano
,
E.
,
Dalla-Bona
,
D. A.
,
Fujita
,
R.
,
Tanaka
,
M.
,
van Eijden
,
T.
, and
Tanne
,
K.
, 2006, “
Age-Associated Changes in Viscoelastic Properties of the Bovine Temporomandibular Joint Disc
,”
Eur. J. Oral Sci.
,
114
(
1
), pp.
70
73
.
31.
Tanaka
,
E.
,
Tanaka
,
M.
,
Miyawaki
,
Y.
, and
Tanne
,
K.
, 1999, “
Viscoelastic Properties of Canine Temporomandibular Joint Disc in Compressive Load-Relaxation
,”
Arch. Oral Biol.
,
44
(
12
), pp.
1021
1026
.
32.
Beek
,
M.
,
Koolstra
,
J. H.
,
van Ruijven
,
L. J.
, and
van Eijden
,
T. M.
, 2000, “
Three-Dimensional Finite Element Analysis of the Human Temporomandibular Joint Disc
,”
J. Biomech.
,
33
(
3
), pp.
307
316
.
33.
Donzelli
,
P. S.
,
Gallo
,
L. M.
,
Spilker
,
R. L.
, and
Palla
,
S.
, 2004, “
Biphasic Finite Element Simulation of the TMJ Disc from In vivo Kinematic and Geometric Measurements
,”
J. Biomech.
,
37
(
11
), pp.
1787
1791
.
34.
Chen
,
J.
,
Akyuz
,
U.
,
Xu
,
L.
, and
Pidaparti
,
R. M.
, 1998, “
Stress Analysis of the Human Temporomandibular Joint
,”
Med. Eng. Phys.
,
20
(
8
), pp.
565
572
.
35.
Herring
,
S. W.
, and
Liu
,
Z. J.
, 2001, “
Loading of the Temporomandibular Joint: Anatomical and In vivo Evidence from the Bones
,”
Cells Tissues Organs
,
169
(
3
), pp.
193
200
.
36.
Tanaka
,
E.
,
Sasaki
,
A.
,
Tahmina
,
K.
,
Yamaguchi
,
K.
,
Mori
,
Y.
, and
Tanne
,
K.
, 2001, “
Mechanical Properties of Human Articular Disk and its Influence on TMJ Loading Studied with the Finite Element Method
,”
J. Oral Rehabil.
,
28
(
3
), pp.
273
279
.
37.
Tanaka
,
E.
,
Rodrigo
,
D. P.
,
Miyawaki
,
Y.
,
Lee
,
K.
,
Yamaguchi
,
K.
, and
Tanne
,
K.
, 2000, “
Stress Distribution in the Temporomandibular Joint Affected by Anterior Disc Displacement: A Three-Dimensional Analytic Approach with the Finite-Element Method
,”
J. Oral Rehabil.
,
27
(
9
), pp.
754
759
.
38.
Swartz
,
M. A.
, and
Fleury
,
M. E.
, 2007, “
Interstitial Flow and its Effects in Soft Tissues
,”
Annu. Rev. Biomed. Eng.
,
9
, pp.
229
256
.
39.
Ruhland
,
C.
,
Schonherr
,
E.
,
Robenek
,
H.
,
Hansen
,
U.
,
Iozzo
,
R. V.
,
Bruckner
,
P.
, and
Seidler
,
D. G.
, 2007, “
The Glycosaminoglycan Chain of Decorin Plays an Important Role in Collagen Fibril Formation at the Early Stages of Fibrillogenesis
,”
FEBS J.
,
274
(
16
), pp.
4246
4255
.
40.
Danielson
,
K. G.
,
Baribault
,
H.
,
Holmes
,
D. F.
,
Graham
,
H.
,
Kadler
,
K. E.
, and
Iozzo
,
R. V.
, 1997, “
Targeted Disruption of Decorin leads to Abnormal Collagen Fibril Morphology and Skin Fragility
,”
J. Cell Biol.
,
136
(
3
), pp.
729
743
.
41.
Corsi
,
A.
,
Xu
,
T.
,
Chen
,
X. D.
,
Boyde
,
A.
,
Liang
,
J.
,
Mankani
,
M.
,
Sommer
,
B.
,
Iozzo
,
R. V.
,
Eichstetter
,
I.
,
Robey
,
P. G.
,
Bianco
,
P.
, and
Young
,
M. F.
, 2002, “
Phenotypic Effects of Biglycan Deficiency are Linked to Collagen Fibril Abnormalities, are Synergized by Decorin Deficiency, and Mimic Ehlers-Danlos-Like Changes in Bone and other Connective Tissues
,”
J. Bone Miner. Res.
,
17
(
7
), pp.
1180
1189
.
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