The Effect of Sutural Growth Rate on Collagen Phenotype Synthesis

Abstract

We determined the ratio of newly-synthesized type III collagen to the total of type I and type III collagen in mouse interparietal sutural tissue at selected ages between birth and adulthood (36 weeks old). We incubated mouse calvaria explants in Trowell-type organ culture dishes for one h and then added [¹⁴C]-glycine for two h. We dissected the interparietal sutural tissues for collagen solubilization by limited pepsin digestion. Fluorographic visualization of separated radiolabeled collagens, after SDS-PAGE, found the ratio of collagen type III a-chains to the total type I and type III a-chains to be age-dependent. The proportion of type III α-chains at birth was quite high, but there was a significant drop (p<0.05) during the first two days of life, probably because of the sudden environmental change from in utero. The proportion of type III α -chains rose significantly from day 2 to day 4, reaching a maximum and then dropping significantly to about the same proportion as at birth by day 7. A further significant drop took place during the second week of life, with the proportion stabilized at around 3.5% at two weeks to ten weeks of age. A final significant drop during the eleventh week of life led to no detectable synthesis of type III collagen after 12 weeks of age. The changes in the collagen phenotype ratio did not relate to changes in body weight during growth and development, which suggests that the interparietal suture may have an independent maturing pattern. Correlation of the ratio of newly-synthesized mouse interparietal sutural type III collagen with the growth rate of the rat interparietal suture (Massler and Schour, 1951) suggested a close relationship between high type III collagen ratios and periods of very rapid sutural growth. The desirable age for future orthopedic studies in Swiss male white mouse interparietal suture, in which collagen phenotype would be monitored, would be between four and ten weeks of age.

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References

Barbanell, R. ; Lian, J. ; and Keith, D. (1978): Structural Proteins of Connective Tissues. In: Textbook of Oral Biology, J.H. Shaw , E.A. Sweeney , C.C. Cappuccino , and S.M. Meller , Eds., Philadelphia: W.B. Saundcrs, pp. 419-452.

Bonner, W.M. and Laskey, R.A. (1974): A Film Detection Method for Tritium Labelled Proteins and Nucleic Acids in Polyacrylamide Gels, Eur J Biochem 46:83-88.

Bornstein, P. and Sage, H. (1980): Structurally Distinct Collagen Types, Ann Rev Biochem 49:957-1003.

Bornstein, P. and Traub, W. (1979): The Structure Proteins. In: The Proteins, New York: Plenum Press , pp. 163-273.

Butler, W.T. ; Birkedal-Hansen, H. ; Beegle, W.F. ; Taylor, R.E. ; and Chung, E. (1975): Proteins of the Periodontium. Identification of Collagens with the [α] (1)2], α2 and [α1(III)]3 Structures in Bovine Periodontal Ligament, J Biol Chem 250:8907-8912.

Chung, E. and Miller, E.J. (1974): Collagen Polymorphism: Characterization of Molecules with Chain Composition [α-1 (III)]3 in Human Tissues, Science 183:1200-1201.

Curran, R.C. and Collins, D.H. (1957): Mucopolysaccharidcs in Fields of Intramembranous Ossification in Man, J Path Bact 74:207-214.

De Angelis, V. (1968): Autoradiographic Investigation of Calvarial Growth in the Rat, Am J Anat 123:359-367.

Epstein, E.H., Jr. (1974): [α-1 (III)]3 Human Skin Collagen. Release by Pepsin Digestion and Preponderance in Fetal Life, J Biol Chem 249:3225-3231.

10.

Gay, S. and Miller, E.J. (1978): Collagen in the Physiology and Pathology of Connective Tissue, New York: Fischer Verlag , pp. 75-82.

11.

Gay, S. ; Viljanto, J. ; Raekallio, J.P.R. ; and Penttinen, R. (1978): Collagen Types in Early Phases of Wound Healing in Children, Acta Chir Scand 144:205-211.

12.

Hinrichsen, G.J. and Storey, E. (1968): The Effect of Force on Bone and Bones, Angle Orthod 38:155-165.

13.

Laemmli, U.K. (1970): Cleavage of Structural Proteins During the Assembly of the Head of the Bacteriophage, Nature 227:680-685.

14.

Massler, M. and Schour, I. (1951): The Growth Pattern of the Cranial Vault in the Albino Rat as Measured by Vital Staining with Alizarine Red S, Anat Rec 110:83-101.

15.

Meikle, M.C. ; Heath, J.K. ; Hembry, R.M. ; and Reynolds, J.J. (1982): Rabbit Cranial Suture Fibroblasts under Tension Express a Different Collagen Phenotypc, Arch Oral Biol 27:609-613.

16.

Meikle, M.C. ; Reynolds, J.J. ; Sellers, A. ; and Dingle, J.T. (1979): Rabbit Cranial Sutures in vitro. A New Experimental Model for Studying the Response of Fibrous Joints to Mechanical Stress, Calcif Tissue Int 28:137-144.

17.

Meikle, M.C. ; Sellers, A. ; and Reynolds, J.J. (1980): Effect of Tensile Mechanical Stress on Synthesis of Metalloproteinases by Rabbit Coronal Sutures in vitro, Calcif Tissue Int 30 :77-82.

18.

Miller, E.J. (1976): Biochemical Characteristics and Biological Significance of Genetically Distinct Collagens, Mol Cell Biochem 13:165-192.

19.

Moss, M.L. (1954): Growth of the Calvaria in Rat, The Determination of Osseous Morphology, Am J Anat 94:333-362.

20.

Narayanan, A.S. and Page, R.C. (1983): Connective Tissues of the Periodontium: A Summary of Current Work, Coll Relat Res 3:33-64.

21.

Navia, J.M. (1977): Animal Models in Dental Research, Birmingham : The University of Alabama Press, pp. 143-144.

22.

Page, R.C. and Schroeder, H.E. (1982): Periodontitis in Man and Other Animals, Basel: S. Karger, pp. 1-45; pp. 239-251.

23.

Reddi, A.H. ; Gay, R. ; Gay, S. ; and Miller, E.J. (1977): Transitions in Collagen Types During Matrix-induced Cartilage, Bone and Bone Marrow Formation, Proc Natl Acad Sci USA 74 :5589-5592.

24.

Steel, R. and Torrie, J. (1960): Principles and Procedures of Statistics, Chap. 8, New York: McGraw-Hill, pp. 156-159.

25.

Sykes, B. ; Puddle, B. ; Francis, M. ; and Smith, R. (1976): The Estimation of Two Collagens from Human Dermis by Interrupted Gel Electrophoresis, Biochem Biophys Res Commun 72 :1472-1480.

26.

Ten Cate, A.R. ; Freeman, E. ; and Dickinson, J.B. (1977): Sutural Development: Structure and Its Response to Rapid Expansion, Am J Orthod 71:622-636.

27.

Tonna, E.A. (1965): Skeletal Cell Aging and Its Effects on Osteogenetic Potential, Clin Orthop 40:57-81.

28.

Trowell, O.A. (1959): The Culture of Mature Organs in a Synthetic Medium , Exp Cell Res 16:118-147.

29.

Weinmann, J.P. and Sicher, H. (1955): Bone and Bones, St. Louis: C.V. Mosby Co., p. 89.

30.

Weiss, J.B. ; Shuttleworth, C.A. ; Brown, R. ; Sedow-Fia, K. ; Baildam, A. ; and Hunter, J.A. (1975): Occurrence of Type III Collagen in Inflamed Synovial Membranes: A Comparison Between Non-rheumatoid, Rheumatoid and Normal Synovial Collagens, Biochem Biophys Res Commun 65:907-912.

31.

Yen, E.H.K. and Chiang, S.K.T. (1984): A Radioautographic Study of the Effect of Age on the Protein-synthetic and Bone-deposition Activity in Interparietal Sutures of Male White Mice, Arch Oral Biol 29:1041-1047.

32.

Yen, E.H.K. ; Duncan, G.W. ; and Suga, D.M. (1984): Biological Response to Orthodontic and Orthopedic Forces in vitro: Collagen Synthesis, In: Malocclusion and the Periodontium, J.A. McNamara, Jr. and K.A. Ribbens , Eds., Ann Arbor: Center for Growth and Development, The University of Michigan, pp. 149-165.

33.

Yen, E.H.K. and Melcher, A.H. (1978): A Continuous Flow Culture System for Organ Culture of Large Explants of Adult Tissue: Effect of Oxygen Tension on Mouse Molar Periodontium, In Vitro 14:811-818.

34.

Yen, E.H.K. ; Suga, D.M. ; and Chiang, S. (1980): Identification of Collagen Types Synthesized in Interparietal Suture During Orthopedic Stress, IADR Progr & Abst 59 (Sp Iss): No. 60.

35.

Young, R.W. (1959): The Influence of Cranial Contents on Postnatal Growth of the Skull in the Rat, Am J Anat 105:383-415.

36.

Young, R.W. (1962): Autoradiographic Studies on Postnatal Growth of the Skull in Young Rats Injected with Tritiated Glycine, Anat Rec 143:1-14.