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Original Research

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Changes in Type I and Type II Collagen Expression in Rat Mandibular Condylar Cartilage Associated with Aging and Dietary Loading

  • Pertti Pirttiniemi1
  • Aune Raustia2
  • Hanna-Marja Voipio3
  • Egle Jonaviciute3
  • Eerika Mursu1
  • Riikka Hauru2
  • Sakari Laaksonen4
  • Marko Orajärvi5,*,

1Univ Oulu, Inst Dent, Dept Prosthet Dent & Stomatognath Physiol, POB 5281, FI-90014 Oulu, Finland

2Univ Oulu, Lab Anim Ctr, Oulu, Finland

3Univ Oulu, Inst Dent, Oulu, Finland

4Univ Oulu, Oulu Univ Hosp, Med Res Ctr, Dept Prosthet Dent & Stomatognath Physiol, Oulu, Finland

5Univ Oulu, Oulu Univ Hosp, Med Res Ctr, Dept Oral Dev & Orthodont, Oulu, Finland

DOI: 10.11607/ofph.1581 Vol.32,Issue 3,September 2018 pp.258-265

Published: 30 September 2018

*Corresponding Author(s): Marko Orajärvi E-mail: marko.orajarvi@oulu.fi

Abstract

Aims: To evaluate the usefulness of diet board feeding as a model for temporomandibular joint (TMJ) research, characterize dietary loading–related morphometric changes in the mandibular condylar cartilage of aging rats, and investigate changes in type I and type II collagen expression in different age, sex, and diet groups. Methods: Material was collected from a study that examined the effects of 1-year and 2-year diet board feeding on rats. In diet board feeding, rats must gnaw wood to reach their food, leading to a higher masticatory workload. The material analyzed was comprised of 150 TMJ samples from 75 Hsd:Sprague Dawley rats grouped according to feeding method (diet board [experimental group] or ad libitum [control group]), sex, and experiment length (1 or 2 years). The rats were sacrificed at the age of 15 or 26 months (15-M rats or 26-M rats). From the TMJ samples, 5-µm–thick sections were cut parallel to the sagittal plane of the mandibular condyle. Histomorphometric analysis of the thickness of the condylar cartilage and the number of cartilage cells was performed after toluidine blue staining. Immunohistochemical staining included type I and type II collagen antigens. Differences in the thickness of the cellular layer and the number of cells in the condylar cartilage were analyzed by means of a repeated-measures analysis of variance (ANOVA) model, and differences in the type of collagen with a one-way random-effects ANOVA model. Results: Condylar cartilage was significantly thicker in the 15-M diet board–fed rats than in the 15-M control rats and in the 26-M rats than in the 15-M rats. The number of cells was larger in the 26-M female rats than in the 26-M male rats. Type I collagen expression was significantly higher in the 15-M diet board–fed female rats than in the 15-M controls. Type II collagen showed increased expression in older rats compared to younger rats. Conclusion: Condylar cartilage is sensitive to the interplay between loading, aging, and sex of middle-aged and older rats. High loading of condylar cartilage increased the thickness of cartilage in younger rats.

Keywords

age-related changes;diet board;joint loading;mandibular condylar cartilage;rat;type I collagen;type II collagen

Cite and Share

Pertti Pirttiniemi,Aune Raustia,Hanna-Marja Voipio,Egle Jonaviciute,Eerika Mursu,Riikka Hauru,Sakari Laaksonen,Marko Orajärvi. Changes in Type I and Type II Collagen Expression in Rat Mandibular Condylar Cartilage Associated with Aging and Dietary Loading. Journal of Oral & Facial Pain and Headache. 2018. 32(3);258-265.

References

1.Yu SB, Wang MQ, Li YQ, et al. The effects of age and sex on the expression of oestrogen and its receptors in rat mandibular condylar cartilages. Arch Oral Biol 2009;54:479–485.

2.Buckwalter JA, Mankin HJ. Articular cartilage: Tissue design and chondrocyte-matrix interactions. Instr Course Lect 1998; 47:477–486.

3.Kuroda S, Tanimoto K, Izawa T, Fujihara S, Koolstra JH, Tanaka E. Biomechanical and biochemical characteristics of the mandibular condylar cartilage. Osteoarthritis Cartilage 2009; 17:1408–1415.

4.Agarwal S, Long P, Gassner R, Piesco NP, Buckley MJ. Cyclic tensile strain suppresses catabolic effects of interleukin-1be-ta in fibrochondrocytes from the temporomandibular joint. Arthritis Rheum 2001;44:608–617.

5.Ishibashi H, Takenoshita Y, Ishibashi K, Oka M. Age-related chang-es in the human mandibular condyle: A morphologic, radiologic, and histologic study. J Oral Maxillofac Surg 1995;53:1016–1023.

6.Koike H, Ejiri S, Hanada K, Ozawa H. Age-related histologi-cal changes in rat mandibular condyle. J Bone Miner Metab 1995;13:10–16.

7.Papachristou DJ, Pirttiniemi P, Kantomaa T, Papavassiliou AG, Basdra EK. JNK/ERK-AP-1/Runx2 induction “paves the way” to cartilage load-ignited chondroblastic differentiation. Histochem Cell Biol 2005;124:215–223.

8.Herring SW. TMJ anatomy and animal models. J Musculoskelet Neuronal Interact 2003;3:391–394.

9.Nadon NL. Gerontology and age-sssociated lesions. In: Suckow MA, Weisbroth SH, Franklin CL (eds). The Laboratory Rat. Amsterdam: Elsevier, 2006:761–772.

10.Kohn DF, Clifford CB. Biology and diseases of rats. In: Fox JG, Anderson LC, Loew FM, Quimby FW (eds). Laboratory Animal Medicine. Amsterdam: Academic, 2002:121–165.

11.Sharp PE, La Regina MC, Suckow MA. The Laboratory Rat. Boca Raton, New York: CRC, 1998.

12.Jiao K, Dai J, Wang MQ, Niu LN, Yu SB, Liu XD. Age- and sex-related changes of mandibular condylar cartilage and sub-chondral bone: A histomorphometric and micro-CT study in rats. Arch Oral Biol 2010;55:155–163.

13.Kasanen I. The Diet Board-A Novel Method of Dietary Restriction for Laboratory Rats [thesis]. Helsinki: University of Helsinki, 2009.

14.Kasanen IH, Inhilä KJ, Nevalainen JI, et al. A novel dietary re-striction method for group-housed rats: Weight gain and clini-cal chemistry characterization. Lab Anim 2009;43:138–148.

15.Laaksonen KS, Nevalainen TO, Haasio K, Kasanen IH, Nieminen PA, Voipio HM. Food and water intake, growth, and adiposity of Sprague-Dawley rats with diet board for 24 months. Lab Anim 2013;47:245–256.

16.Parliament of Finland. Act on the Use of Animals for Exper-imental Purposes (62/2006). National Animal Experiment Board, 2006.

17.Ministry of Agriculture and Forestry of Finland. Decree of the Ministry of Agriculture and Forestry on the Use of Animals for Experimental Purposes (36/EEO/2006). Ministry of Agriculture and Forestry of Finland, 2006.

18.Council of Europe. European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes (ETS No. 123). Strasbourg: Council of Europe, 1986.

19.European Parliament and the Council of the European Union. Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Official J Eur Union 2010;L276.

20.Nicklas W, Baneux P, Boot R, et al. Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab Anim 2002;36:20–42.

21.Singer JD. Using SAS PROC MIXED to fit multilevel models, hierarchical models, and individual growth models. J Educ Behav Stat 1998;24:323–355.

22.Orajärvi M, Puijola E, Yu SB, et al. Effect of estrogen and dietary loading on condylar cartilage. J Orofac Pain 2012;26:328–336.

23.Thomas NR, Peyton SC. An electromyographic study of mastication in the freely-moving rat. Arch Oral Biol 1983;28: 939–945.

24.Hunt HR, Rosen S, Hoppert CA. Morphology of molar teeth and occlusion in young rats. J Dent Res 1970;49:508–514.

25.Simon MR. The role of compressive forces in the normal mat-uration of the condylar cartilage in the rat. Acta Anat (Basel) 1977;97:351–360.

26.Hinton RJ, Carlson DS. Response of the mandibular joint to loss of incisal function in the rat. Acta Anat (Basel) 1986; 125:145–151.

27.Singh M, Detamore MS. Tensile properties of the mandibular condylar cartilage. J Biomech Eng 2008;130:011009.

28.Hinton RJ. Effect of dietary consistency on matrix synthe-sis and composition in the rat condylar cartilage. Acta Anat (Basel) 1993;147:97–104.

29.Kantomaa T, Tuominen M, Pirttiniemi P. Effect of mechanical forces on chondrocyte maturation and differentiation in the mandibular condyle of the rat. J Dent Res 1994;73:1150–1156.

30.Pirttiniemi P, Kantomaa T, Salo L, Tuominen M. Effect of re-duced articular function on deposition of type I and type II collagens in the mandibular condylar cartilage of the rat. Arch Oral Biol 1996;41:127–131.

31. Kiliaridis S, Thilander B, Kjellberg H, Topouzelis N, Zafiriadis A. Effect of low masticatory function on condylar growth: A morpho-metric study in the rat. Am J Orthod Dentofacial Orthop 1999; 116:121–125.

32.Pirttiniemi P, Kantomaa T, Sorsa T. Effect of decreased loading on the metabolic activity of the mandibular condylar cartilage in the rat. Eur J Orthod 2004;26:1–5.

33.Milam SB. Pathogenesis of degenerative temporomandibular joint arthritides. Odontology 2005;93:7–15.

34.Kuroda S, Tanimoto K, Izawa T, Fujihara S, Koolstra JH, Tanaka E. Biomechanical and biochemical characteristics of the mandibular condylar cartilage. Osteoarthritis Cartilage 2009; 17:1408–1415.

35.Orajarvi M, Hirvonen O, Yu SB, et al. Effect of estrogen and altered diet hardness on the expression of estrogen receptor alpha and matrix metalloproteinase-8 in rat condylar cartilage. J Orofac Pain 2011;25:261–268.

36.Orajärvi M, Thesleff I, Hartikainen H, Raustia A, Pirttiniemi P. Effect of estrogen and food hardness on metabolism and turn-over of condylar cartilage. J Oral Facial Pain Headache 2015; 29:297–307.

37.Chen X, Cai C, Liu J, Wen L, Wang X, Ding Y. Impact of estro-gen-related receptor α on the biological characteristics of rat man-dibular condylar chondrocytes. Mol Med Rep 2014;10:195–202.

38.Athanasiou KA, Almarza AA, Detamore MS, Kalpakci KN. Cartilage of the mandibular condyle. In: Athanasiou KA (ed). Tissue Engineering of Temporomandibular Joint Cartilage. San Rafael, CA: Morgan & Claypool, 2009:41–46.

39.Mizoguchi I, Takahashi I, Nakamura M, et al. An immunohis-tochemical study of regional differences in the distribution of type I and type II collagens in rat mandibular condylar cartilage. Arch Oral Biol 1996;41:863–869.

40.Luder HU. Postnatal Development, Aging, and Degeneration of the Temporomandibular Joint in Humans, Monkeys, and Rats. Ann Arbor, MI: Center for Human Growth and Development, University of Michigan, 1996.

41.Waldman SD, Couto DC, Grynpas MD, Pilliar RM, Kandel RA. A single application of cyclic loading can accelerate matrix deposition and enhance the properties of tissue-engineered cartilage. Osteoarthritis Cartilage 2006;14:323–330.

42.Chen JL, Duan L, Zhu W, Xiong J, Wang D. Extracellular matrix production in vitro in cartilage tissue engineering. J Transl Med 2014;12:88.

43.Huang K, Wu LD. Suppression of aggrecanase: A novel pro-tective mechanism of dehydroepiandrosterone in osteoarthri-tis? Mol Biol Rep 2010;37:1241–1245.

44.Abubaker AO, Raslan WF, Sotereanos GC. Estrogen and progesterone receptors in temporomandibular joint discs of symptomatic and asymptomatic persons: A preliminary study. J Oral Maxillofac Surg 1993;51:1096–1100.

45.Kamiya Y, Chen J, Xu M, et al. Increased mandibular condylar growth in mice with estrogen receptor beta deficiency. J Bone Miner Res 2013;28:1127–1134.

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