Abstract
Manganese (Mn) deficiency can result in perosis in chicks, but the mechanism of Mn deficiency on tibia development remains poorly understood. Ninety one-day-old Arbor Acres male broiler chickens administered with control diet (60 mg Mn/kg) and Mn-deficient diets (40 mg Mn/kg, 8.7 mg Mn/kg) to investigate the effects of Mn deficiency on morphology of tibia and related signal transduction pathways in broiler chickens. At the age of 42 days, the bone trabecula, damaged osteoblasts and OPG/RANKL mRNA expression levels were investigated by histological assessment, electron microscopic examination and real-time quantitative PCR analysis, respectively. Results of histological observations showed that decreased trabecular thickness, trabecular number and trabecular bone area (%) together with increased trabecular bone separation were involved in perosis induced by Mn deficiency. The most striking ultrastructural modifications involved disruption of nuclear membrane and mitochondria outer membrane, loss of mitochondrion cristae and alteration in endoplasmic reticulum in osteoblasts of the Mn-deficient groups. Likewise, Mn deficiency results in a significant (P < 0.05) decrease in the relative mRNA expression levels of OPG and RANKL with a significantly higher RANKL/OPG ratio (P < 0.05). In conclusion, Mn deficiency can affect the development of tibia in broiler chickens, leading to metaphyseal osteoporosis which may be due to decreased OPG/RANKL mRNA expression.
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Endo S, Connor JH, Forney B, Zhang L, Ingebritsen TS, Lee EYC, Shenolikar S (1997) Conversion of protein phosphatase 1 catalytic subunit to a Mn2þ-dependent enzyme impairs its regulation by inhibitor 1. Biochemistry 36:6986–6992
Eriksen EF, Brixen K, Charles P (1995) New markers of bone metabolism: clinical use in metabolic bone disease. Eur J Endocrinol 132:251–263
Fong L, Tan K, Tran C, Cool J, Scherer MA, Elovaris R, Coyle P, Foster BK, Rofe AM, Xian CJ (2009) Interaction of dietary zinc and intracellular binding protein metallothionein in postnatal bone growth. Bone 44:1151–1162
Gardiner EE (1972) Lack of response to added dietary manganese of chicks fed wheat-soybean meal or corn-soybean meal based diets. Can J Animal Sci 52:737–740
Halpin KM, Chausow DG, Baker DH (1986) Efficiency of manganese absorption in chicks fed corn-soy and casein diets. J Nutr 116:1747–1751
Heaney RP (1988) Nutritional factor in bone health. In Osteoporosis, Riggs, BL and Melton, LJ eds, pp 359–372
Hurley LS, Keen CL (1989) Manganese. In: Mertz W (ed) Trace element in human and animal nutrition, 5th edn. Academic, San Diego, pp 185–221
Kartsogiannis V, Zhou H, Horwood NJ, Thomas RJ, Hards DK, Quinn JM, Niforas P, Ng KW, Martin TJ, Gillespie MT (1999) Localization of RANKL (receptor activator of NF kappa B ligand) mRNA and protein in skeletal and extraskeletal tissues. Bone 25:525–534
Kenneth JL, Thomas DS (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408
Kronenberg HM (2003) Developmental regulation of the growth plate. Nature 423:332–336
Leach RM Jr, Muenster AM (1962) Studies on the role of manganese in bone formation. I. Effect upon the mucopolysccharide content of chick bone. J Nutr 78:51–56
Leach RM Jr, Muenster AM, Wein EM (1969) Studies on the role of manganese in bone formation. II. Effect upon chondroitin sulfate synthesis in chick epiphyseal cartilage. Arch Biochem Biophys 133:22–28
Ma YL, Cain RL, Halladay DL, Yang X, Zeng Q, Miles RR, Chandrasekhar S, Martin TJ, Onyia JE (2001) Catabolic effects of continuous human PTH(1–38) in vivo is associated with sustained stimulation of RANKL and inhibition of osteoprotegerin and gene-associated bone formation. Endocrinology 142:4047–4054
Nishito Y, Usui H, Shinzawa-Itoh K, Inoue R, Tanabe O, Nagase T, Murakami T, Takeda M (1999) Direct metal analyses of Mn2þ-dependent and -independent protein phosphatase 2A from human erythrocytes detect zinc and iron only in the Mn2þ-independent one. FEBS Lett 447:29–33
Nowak T, Suelter C (1982) Pyruvate kinase: activation by and catalytic role of the monovalent and divalent cations. Mol Cell Biochem 35:65–75
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007
Plebani M, Bernardi D, Zaninotto M, De Paoli M, Secchiero S, Sciacovelli L (1996) New and traditional serum markers of bone metabolism in the detection of skeletal metastases. Clin Biochem 29:67–72
Qin L, Raggatt LJ, Partridge NC (2004) Partridge Parathyroid hormone: a double-edged sword for bone metabolism. Trends Endocrinol Metab 15:60–65
Rico H, Gómez-Raso N, Revilla M, Hernández ER, Seco C, Páez E, Crespo E (2000) Effects on bone loss of manganese alone or with copper supplement in ovariectomized rats. A morphometric and densitomeric study. Eur J Obstet Gynecol Reprod Biol 90:97–101
Saltman P (1984) Trace mineral in health and diseases. In: Morin R (ed) Frontiers in longevity research. CC Thomas, Springfield, pp 162–182
Silvestrini G, Ballanti P, Patacchioli F, Leopizzi M, Gualtieri N, Monnazzi P, Tremante E, Sardella D, Bonucci E (2005) Detection of osteoprotegerin (OPG) and its ligand (RANKL) mRNA and protein in femur and tibia of the rat. J Mol Histol 36:59–67
Singh TJ (1990) Activation of a manganese-dependent membrane protein kinase by serine and tyrosine phosphorylation. Biochem Biophys Res Commun 171:75–83
Strause LB, Hegenauer J, Saltman P (1986) Effects of long-term dietary manganese and copper deficiency on rat skeleton. J Nutr 116:135–141
Takeuchi M, Ishida A, Kameshita I, Kitani T, Okuno S, Fujisawa H (2001) Identification and characterization of CaMKP-N, nuclear calmodulin-dependent protein kinase phosphatase. J Biochem (Tokyo) 130:833–840
Tian G, Kane LS, Holmes WD, Davis ST (2002) Modulation of cyclindependent kinase 4 by binding of magnesium(II) and manganese(II). Biophys Chem 95:79–90
Underwood EJ (1971) Trace elements in human and animal nutrition, 3rd edn. Academic, New York
Wilgus HS, Norris LC, Heuser GF (1937) The role of manganese and certain other trace elements in the prevention of perosis. J Nutr 14:155–167
Xian CJ, Cool JC, Pyragius T, Foster BK (2006) Damage and recovery of the bone growth mechanism in young rats following 5-fluorouracil acute chemotherapy. J Cell Biochem 99:1688–1704
Xian CJ, Cool JC, Scherer MA, Macsai CE, Fan C, Covino M (2007) Cellular mechanisms for methotrexate chemotherapy-induced bone growth defects. Bone 41:842–850
Zhaojun W, Lin W, Zhenyong W, Jian W, Ran L (2013) Effects of manganese deficiency on serum hormones and biochemical markers of bone metabolism in chicks. J Bone Miner Metab 31:285–292
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This work was supported by the foundation for the author of national excellent doctoral dissertation of PR China (No. 201266) and the fund of Fok Ying Tung education foundation under grant No. 141022.
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Liu, R., Jin, C., Wang, Z. et al. Effects of manganese deficiency on the microstructure of proximal tibia and OPG/RANKL gene expression in chicks. Vet Res Commun 39, 31–37 (2015). https://doi.org/10.1007/s11259-015-9626-5
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DOI: https://doi.org/10.1007/s11259-015-9626-5