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The influence of dexamethasone administered prenatally on cartilage of newborn spiny mouse (Acomys cahirinus) offspring

Published online by Cambridge University Press:  17 November 2015

P. Iwaniak*
Affiliation:
Department of Comparative Anatomy and Anthropology, Maria Curie-Sklodowska University, Lublin, Poland
P. Dobrowolski
Affiliation:
Department of Comparative Anatomy and Anthropology, Maria Curie-Sklodowska University, Lublin, Poland
E. Tomaszewska
Affiliation:
Department of Animal Physiology, Faculty of Veterinary Medicine, University of Life Sciences in Lublin, Lublin, Poland
M. Hułas-Stasiak
Affiliation:
Department of Comparative Anatomy and Anthropology, Maria Curie-Sklodowska University, Lublin, Poland
A. Tomczyk
Affiliation:
Department of Animal Physiology, Faculty of Veterinary Medicine, University of Life Sciences in Lublin, Lublin, Poland
A. Gawron
Affiliation:
Department of Comparative Anatomy and Anthropology, Maria Curie-Sklodowska University, Lublin, Poland
*
*Address for correspondence: P. Iwaniak, Department of Comparative Anatomy and Anthropology, Maria Curie-Sklodowska University, Akademicka 19, 20-033 Lublin, Poland. (Email [email protected])

Abstract

Considering the negative effects of glucocorticoid treatment, especially during fetal development it is important to investigate effectors decreasing such disadvantages. The aim of this study was to investigate the effect of prenatally administered dexamethasone (Dex), a synthetic glucocorticoid, on the histomorphometry of the femur in the offspring of spiny mice. The study was performed on 24 pregnant spiny mice. The time of the experiment included the prenatal period between the 20th day of gestation until birth (pregnancy lasts on average of 36–38 days). The mice from the experimental group received dexamethasone per os in a dose of 125 mg/kg birth weight daily. At the end, the newborns from the experimental and control group were weighted and euthanized. Maternal Dex treatment resulted in a 17% decrease in birth weight in newborns. Dex administration significantly reduced the thickness of the hypertrophy zone of the growth plate by 34% and total thickness by 8,7%. In addition, Dex decreased the number of cells in the articular cartilage by 27% and significantly decreased their diameter by 5%. Dex also affected the structure and spatial distribution of thick and thin collagen fibers, lowering the proportion of thin fibers compared with the control group. Moreover, Dex treatment considerably lowered the amount of proteoglycans in articular and growth cartilages. Exposure to glucocorticoids in pregnant spiny mice affects cartilage development by accelerating maturity of collagen fibers and growth plate, presumably along with further disruption of longitudinal growth of long bones.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

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References

1. Stevens, DA, Graham, RW. Hormone regulation of chondrocyte differentiation and endochondral bone formation. Mol Cell Endocrinol. 1999; 151, 195204.CrossRefGoogle ScholarPubMed
2. Śliwa, E, Dobrowolski, P. Perinatal programming of skeletal system. J Pre-Clin Clin Res. 2007; 1, 112118.Google Scholar
3. Lu, NZ, Cidlowski, JA. The origin and functions of multiple human glucocorticoid receptor isoforms. Ann NY Acad Sci. 2004; 1024, 102123.CrossRefGoogle ScholarPubMed
4. Crowther, CA, McKinlay, CJ, Middleton, P, Harding, JE. Repeat doses of prenatal corticosteroids for women at risk of preterm birth for preventing neonatal respiratory disease. Cochrane Database Syst Rev. 2007; 15, 115.Google Scholar
5. Śliwa, E, Dobrowolski, P, Tatara, MR, et al. Alpha-ketoglutarate partially protects newborns from metabolic changes evoked by chronic maternal exposure to glucocorticoids. JCCR. 2007; 1, 5559.Google Scholar
6. Katta, J, Jin, Z, Ingham, E, et al. Biotribiology of articular cartilage – a review of the recent advances. Med Eng Physiol. 2008; 30, 13491363.CrossRefGoogle Scholar
7. Śliwa, E, Tatara, MR, Kowalik, S, et al. Influence of dexamethasone on the growth and mineralization of skeleton in the prenatal period in pigs. Wet Med. 2005; 61, 11451148.Google Scholar
8. Śliwa, E, Studziński, T, Tatara, MR. Glucocorticoids, metabolism and bone growth. Wet Med. 2006; 62, 377379.Google Scholar
9. Holemans, K, Aertis, L, Van Assche, A. Fetal growth and long-term consequences in animal models of growth retardation. Eur J Obstet Gynecol. 1998; 81, 149156.CrossRefGoogle ScholarPubMed
10. Roberts, D, Dalziel, S. Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst Rev. 2006; 3, 19.Google Scholar
11. Newnham, JP, Moss, TJ. Antenatal glucocorticoids and growth: single versus multiple doses in animal and human studies. Semin Neonatol. 2001; 6, 285292.CrossRefGoogle ScholarPubMed
12. Dickinson, H, Walker, DW, Wintour, EM, et al. Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse. Am J Physiol Regul Integr Comp Physiol. 2007; 292, 453461.CrossRefGoogle ScholarPubMed
13. Śliwa, E, Kowalik, S, Tatara, MR, et al. Effects of dexamethasone on physical properties and mineral density of long bones in piglets. Bull Vet Inst Pulawy. 2005; 49, 97100.Google Scholar
14. Ferretti, JL, Capozza, RF, Mondelo, N, et al. Interrelationships between densitometric, geometric and mechanical properties of rat femora: inferences concerning mechanical regulation of bone modeling. J Bone Miner Res. 1993; 8, 13951399.Google ScholarPubMed
15. Dobrowolski, P, Piersiak, T, Surve, VV, et al. Dietary α-ketoglutarate reduces gastrectomy – evoked loss of calvaria and trabecular bone in female rats. Scand J Gastroenterol. 2008; 43, 551558.CrossRefGoogle ScholarPubMed
16. Suvara, SK, Layton, C, Bancroft, JD. Bancroft’s Theory and Practice of Histological Techniques, 7th edn, 2012. Churchill Livingstone Elsevier: New York.Google Scholar
17. Rich, L, Whittaker, P. Collagen and picrosirius red staining: a polarized light assessment of fibrillar hue and spatial distribution. Braz J Morphol Sci. 2005; 22, 97104.Google Scholar
18. Dobrowolski, P, Tomaszewska, E, Bieńko, M, Radzki, RP, Pierzynowski, SG. The effect of dietary administration of 2-oxoglutaric acid on the cartilage and bone of growing rats. Br J Nutr. 2013; 110, 651658.CrossRefGoogle ScholarPubMed
19. Roach, HI, Mehta, G, Oreffo, ROC, Clarce, NMP, Cooper, C. Temporal analysis of rat growth plates cessation of growth with age despite presence of a physis. J Histochem Cytochem. 2003; 51, 373383.CrossRefGoogle ScholarPubMed
20. Bobinac, D, Spanjol, J, Zoricic, S, Maric, I. Changes in articular cartilage and subchondral bone histomorphometry in osteoarthritic knee joints in humans. Bone. 2003; 32, 284290.CrossRefGoogle ScholarPubMed
21. Hagiwara, Y, Hattori, K, Aoki, T, Ohgushi, H, Ito, H. Autofluorescence assessment of extracellular matrices of a cartilage-like tissue construct using a fluorescent image analyser. J Tissue Eng Regen Med. 2011; 5, 163168.CrossRefGoogle ScholarPubMed
22. Śliwa, E, Tatara, MR, Nowakowski, H, Pierzynowski, SG, Studziński, T. Effect of maternal dexamethasone and alpha-ketoglutarate administration on skeletal development during the last three weeks of prenatal life in pigs. J Maternal Fetal Neonatal Med. 2006; 19, 489493.CrossRefGoogle ScholarPubMed
23. Qin, W, Pan, J, Wu, Y, et al. Protection against dexamethasone-induced muscle atrophy is related to modulation by testosterone of FOXO1 and PGC-1 α. Biochem Biophys Res Commun. 2010; 403, 473478.CrossRefGoogle Scholar
24. Tomaszewska, E, Dobrowolski, P, Puzio, I. Morphological changes of the cartilage and bone in newborn piglets evoked by experimentally induced glucocorticoids excess during pregnancy. J Anim Physiol Anim Nutr. 2013; 97, 785796.CrossRefGoogle ScholarPubMed
25. Smith, NH, Ozanne, SE. Intrauterine origins of metabolic disease. Gynaecol Perinat Pract Rev. 2006; 6, 211217.Google Scholar
26. Tomaszewska, E, Dobrowolski, P, Wydrych, J. Postnatal administration of 2-oxoglutaric acid improves articular and growth plate cartilages and bone tissue morphology in pigs prenatally treated with dexamethasone. J Physiol Pharmacol. 2012; 5, 547554.Google Scholar
27. Singh, RR, Cuffe, JSM, Moritz, KM. Short and long-term effects of exposure to natural and synthetic glucocorticoids during development. Clin Exp Pharmacol Physiol. 2012; 39, 979989.CrossRefGoogle Scholar
28. Gruver-Yates, A, Cidlowski, JA. Tissue-specific actions of glucocorticoids on apoptosis: a double-edged sword. Cells. 2013; 2, 202223.CrossRefGoogle ScholarPubMed
29. Canalis, E, Delany, AM. Mechanisms of glucocorticoid action in bone. Ann NY Acad Sci. 2002; 966, 7381.CrossRefGoogle ScholarPubMed
30. Athanasiou, KA, Darling, EM, Duraine, GD, Hu, JC, Reddi, AH. Articular cartilage tissue engineering. Synth Lect Tissue Eng. 2009; 1, 1182.Google Scholar
31. Moutsatsou, P, Kassi, E, Papavassiliou, AG. Glucocorticoid receptor signaling in bone cells. Trends Mol Med. 2012; 18, 348359.CrossRefGoogle ScholarPubMed
32. Buckingham, JC. Glucocorticoids: exemplars of multi-tasking. British Journal of Pharmacology. 2006; 147, 258268.CrossRefGoogle ScholarPubMed
33. Bronner, F, Farach-Carson, MC, Rodan, GA. Bone Formation. 2010. Springer: London, UK.Google Scholar
34. Giustina, A, Angeli, A, Canalis, E, Manelli, F. Glucocorticoid-Induced Osteoporosis (vol. 30) 2002; pp. 1180. Karger AG: Front Horm Res. Basel, Karger.CrossRefGoogle Scholar
35. Harrison, JR, Woite, HW, Kream, BE. Genetic approaches to determine the role of glucocorticoid signaling in osteoblasts. Endocrine. 2002; 17, 3742.CrossRefGoogle ScholarPubMed
36. Feng, Xu, McDonald, JM. Disorders of bone remodeling. Annu Rev Pathol. 2011; 6, 121145.CrossRefGoogle ScholarPubMed
37. Buckwalter, JA, Mankin, HJ, Grodzinsky, AJ. Articular cartilage and osteoarthritis. Instr Course Lect. 2005; 54, 6580.Google ScholarPubMed
38. Ferretti, JL, Gaffuri, O, Capozza, R, et al. Dexamethasone effects on mechanical, geometric and densitometric properties of rat femur diaphyses as described by peripheral quantitative computerized tomography and bending tests. Bone. 1995; 16, 119124.CrossRefGoogle ScholarPubMed
39. Seaman-Bridges, JS, Carroll, JA, Safranski, TJ, et al. Short- and long-term influence of prenatal dexamethasone treatment on swine growth. Domest Anim Endocrinol. 2003; 24, 193208.CrossRefGoogle Scholar
40. Chen, T, Feldman, D. Glucocorticoid receptors and actions in subpopulations of cultured rat bone cells. J Clin Invest. 1979; 63, 750758.CrossRefGoogle ScholarPubMed
41. Wong, MM, Rao, LG, Ly, H, et al. Long-term effects of physiological concentration of dexamethasone on human bone-derived cells. J Bone Miner Res. 1990; 5, 803813.CrossRefGoogle ScholarPubMed
42. Smink, JJ, Gresnigt, MG, Hamers, N, et al. Short-term glucocorticoid treatment of prepubertal mice decreases growth and IGF-I expression in the growth plate. J Endocrinol. 2003; 177, 381388.CrossRefGoogle ScholarPubMed
43. Zaman, F, Chrysis, D, Huntjens, K, Fadeel, B, Sävendahl, L. Ablation of the pro-apoptotic protein Bax protects mice from glucocrticoids-induced bone growth impairment. PLoS One. 2012; 7, e33168.CrossRefGoogle ScholarPubMed