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The effect of hyperammonemia on myostatin and myogenic regulatory factor gene expression in broiler embryos

Published online by Cambridge University Press:  18 February 2015

R. A. Stern ,
C. M. Ashwell ,
S. Dasarathy  and
P. E. Mozdziak
R. A. Stern*
Affiliation:
Prestage Department of Poultry Science, North Carolina State University, Raleigh, NC 27695, USA
C. M. Ashwell
Affiliation:
Prestage Department of Poultry Science, North Carolina State University, Raleigh, NC 27695, USA
S. Dasarathy
Affiliation:
Department of Pathobiology, Lerner Research Institute, Cleveland Clinic, Cleveland, OH 44195, USA Department of Gastroenterology, Digestive Disease Institute, Cleveland Clinic, Cleveland, OH 44195, USA
P. E. Mozdziak
Affiliation:
Prestage Department of Poultry Science, North Carolina State University, Raleigh, NC 27695, USA
*
†E-mail: [email protected]
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Abstract

Myogenesis is facilitated by four myogenic regulatory factors and is significantly inhibited by myostatin. The objective of the current study was to examine embryonic gene regulation of myostatin/myogenic regulatory factors, and subsequent manipulations of protein synthesis, in broiler embryos under induced hyperammonemia. Broiler eggs were injected with ammonium acetate solution four times over 48 h beginning on either embryonic day (ED) 15 or 17. Serum ammonia concentration was significantly higher (P<0.05) in ammonium acetate injected embryos for both ED17 and ED19 collected samples when compared with sham-injected controls. Expression of mRNA, extracted from pectoralis major of experimental and control embryos, was measured using real-time quantitative PCR for myostatin, myogenic regulatory factors myogenic factor 5, myogenic determination factor 1, myogenin, myogenic regulatory factor 4 and paired box 7. A significantly lower (P<0.01) myostatin expression was accompanied by a higher serum ammonia concentration in both ED17 and ED19 collected samples. Myogenic factor 5 expression was higher (P<0.05) in ED17 collected samples administered ammonium acetate. In both ED17 and ED19 collected samples, myogenic regulatory factor 4 was lower (P⩽0.05) in ammonium acetate injected embryos. No significant difference was seen in myogenic determination factor 1, myogenin or paired box 7 expression between treatment groups for either age of sample collection. In addition, there was no significant difference in BrdU staining of histological samples taken from treated and control embryos. Myostatin protein levels were evaluated by Western blot analysis, and also showed lower myostatin expression (P<0.05). Overall, it appears possible to inhibit myostatin expression through hyperammonemia, which is expected to have a positive effect on embryonic myogenesis and postnatal muscle growth.

Keywords

broilerhyperammonemiamyogenesismyogenic regulatory factormyostatin
Type
Research Article
Information
animal , Volume 9 , Supplement 6 , June 2015 , pp. 992 - 999
Copyright
© The Animal Consortium 2015 

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References

Amthor, H, Nicholas, G, McKinnell, I, Kemp, CF, Sharma, M, Kambadur, R and Patel, K 2004. Follistatin complexes myostatin and antagonises myostatin-mediated inhibition of myogenesis. Developmental Biology 270, 19–30.Google Scholar
Andrews, R, Walsh, JT, Evans, A, Curtis, S and Cowley, AJ 1997. Abnormalities of skeletal muscle metabolism in patients with chronic heart failure: evidence that they are present at rest. Heart 77, 159–163.CrossRefGoogle ScholarPubMed
Bishonga, C, Robinson, JJ, McEvoy, TG, Findlay, P, Aitken, RP and Robertson, I 1996. Excess dietary urea intake in ewes and its effect on ovulation rate and embryo development. The Japanese Journal of Veterinary Research 44, 139–151.Google Scholar
Bonetto, A, Penna, F, Minero, VG, Reffo, P, Costamagna, D, Bonelli, G, Baccino, FM and Costelli, P 2011. Glutamine prevents myostatin hyperexpression and protein hypercatabolism induced in C2C12 myotubes by tumor necrosis factor-α. Amino Acids 40, 585–594.Google Scholar
Calvert, LD, Steiner, MC, Morgan, MD and Singh, SJ 2010. Plasma ammonia response to incremental cycling and walking tests in COPD. Respiratory Medicine 104, 675–681.Google Scholar
Campbell, JW and Vorhaben, JE 1976. Avian mitochondrial glutamine metabolism. The Journal of Biological Chemistry 251, 781–786.Google Scholar
Dasarathy, S, Dodig, M, Muc, SM, Kalhan, SC and McCullough, AJ 2004. Skeletal muscle atrophy is associated with an increased expression of myostatin and impaired satellite cell function in the portacaval anastamosis rat. American Journal of Physiology. Gastrointestinal and Liver Physiology 287, 1124–1130.Google Scholar
Hammon, DS, Wang, S and Holyoak, GR 2000. Ammonia concentration in bovine follicular fluid and its effect during in vitro maturation on subsequent embryo development. Animal Reproduction Science 58, 1–8.Google Scholar
Han, HQ and Mitch, WE 2011. Targeting the myostatin signaling pathway to treat muscle wasting diseases. Current Opinion in Supportive and Palliative Care 5, 334–341.Google Scholar
Hartley, RS, Bandman, E and Yablonka-Reuveni, Z 1992. Skeletal muscle satellite cells appear during late chicken embryogenesis. Developmental Biology 153, 206–216.Google Scholar
He, Y, Hakvoort, TBM, Vermeulen, JLM, Lamers, WH and Van Roon, MA 2007. Glutamine synthetase is essential in early mouse embryogenesis. Developmental Dynamics: an Official Publication of the American Association of Anatomists 236, 1865–1875.Google Scholar
He, Y, Hakvoort, TBM, Köhler, SE, Vermeulen, JLM, de Waart, DR, de Theije, C, GAM, ten Have, HMH, van Eijk, Kunne, C, Labruyere, WT, Houten, SM, Sokolovic, M, Ruijter, JM, Deutz, NEP and Lamers, WH 2010. Glutamine synthetase in muscle is required for glutamine production during fasting and extrahepatic ammonia detoxification. The Journal of Biological Chemistry 285, 9516–9524.Google Scholar
Hickson, RC, Czerwinski, SM and Wegrzyn, LE 1995. Glutamine prevents downregualtion of myosin heavy chain synthesis and muscle atrophy from glucocorticoids. American Journal of Physiology. Endocrinology and Metabolism 268, 730–734.Google Scholar
Hod, G, Chaouat, M, Haskel, Y, Lernau, OZ, Nissan, S and Mayer, M 1982. Ammonia uptake by skeletal muscle in the hyperammonaemic rat. European Journal of Clinical Investigation 12, 445–450.Google Scholar
Hope, M, Haynes, F, Oddy, H, Koohmaraie, M, Al-Owaimer, A and Geesink, G 2013. The effects of the myostatin g+6723G>A mutation on carcass and meat quality of lamb. Meat Science 95, 118–122.Google Scholar
Kosenko, E, Montoliu, C, Giordano, G, Kaminsky, Y, Venediktova, N, Buryanov, Y and Felipo, V 2004. Acute ammonia intoxication indices an NMDA receptor-mediated increase in poly(ADP-ribose) polymerase level and NAD+ metabolism in nuclei of rat brain cells. Journal of Neurochemistry 89, 1101–1110.Google Scholar
Langley, B, Thomas, M, Bishop, A, Sharma, M, Gilmour, S and Kambadur, R 2002. Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. The Journal of Biological Chemistry 277, 49831–49840.CrossRefGoogle ScholarPubMed
Lavoinne, A, Husson, A, Quillard, M, Chédeville, A and Fairand, A 1996. Glutamine inhibits the lowering effect of glucose on the level of phosphoenolpyruvate carboxykinase mRNA in isolated rat hepatocytes. European Journal of Biochemistry 242, 537–543.CrossRefGoogle ScholarPubMed
Lee, S-J and McPherron, AC 2001. Regulation of myostatin activity and muscle growth. Proceedings of the National Academy of Sciences of the United States of America 98, 9306–9311.Google Scholar
Maier, A 1993. Development of chicken intrafusal muscle fibers. Cell and Tissue Research 274, 383–391.Google Scholar
McCroskery, S, Thomas, M, Maxwell, L, Sharma, M and Kambadur, R 2003. Myostatin negatively regulates satellite cell activation and self-renewal. The Journal of Cell Biology 162, 1135–1147.Google Scholar
McEvoy, TG, Robinson, JJ, Aitken, RP, Findlay, PA and Robertson, IS 1997. Dietary excesses of urea influence the viability and metabolism of preimplantation sheep embryos and may affect fetal growth among survivors. Animal Reproduction Science 47, 71–90.Google Scholar
McPherron, AC and Lee, S-J 1997. Double muscling in cattle due to mutations in the myostatin gene. Proceedings of the National Academy of Sciences of the United States of America 94, 12457–12461.Google Scholar
McPherron, AC, Lawler, AM and Lee, S-J 1997. Regulation of skeletal muscle mass in mice by a new TGF-β superfamily member. Nature 387, 83–90.Google Scholar
Mozdziak, PE, Schultz, E and Cassens, RG 1997. Myonuclear accretion is a major determinant of avian skeletal muscle growth. American Journal of Physiology. Cell Physiology 272, 565–571.Google Scholar
Nabeshima, Y, Hanaoka, K, Hayasaka, M, Esumi, E, Li, S, Nonaka, I, Nabeshima, Y-I 1993. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532–535.Google Scholar
Pfaffl, MW 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.Google Scholar
Qiu, J, Thapaliya, S, Runkana, A, Yang, Y, Tsien, C, Mohan, ML, Narayanan, A, Eghtesad, B, Mozdziak, PE, McDonald, C, Stark, GR, Welle, S, Naga Prasad, SV and Dasarathy, S 2013. Hyperammonemia in cirrhosis induces transcriptional regulation of myostatin by an NF-κB-mediated mechanism. Proceedings of the National Academy of Sciences of the United States of America 110, 18162–18167.Google Scholar
Qiu, J, Tsien, C, Thapalaya, S, Narayanan, A, Weihl, CC, Ching, JK, Eghtesad, B, Singh, K, Fu, X, Dubyak, G, McDonald, C, Almasan, A, Hazen, SL, Naga Prasad, SV and Dasarathy, S 2012. Hyperammonemia-mediated autophagy in skeletal muscle contributes to sarcopenia of cirrhosis. American Journal of Physiology. Endocrinology and Metabolism 303, 983–993.CrossRefGoogle ScholarPubMed
Remignon, H, Gardahaut, M-F, Marche, G and Ricard, F-H 1995. Selection for rapid growth increases the number and the size of muscle fibers without changing their typing in chickens. Journal of Muscle Research and Cell Motility 16, 95–102.CrossRefGoogle ScholarPubMed
Rudnicki, MA, Braun, T, Hinuma, S and Jaenisch, R 1992. Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal development. Cell 71, 383–390.Google Scholar
Rudnicki, MA, Schnegelsberg, PNJ, Stead, RH, Braun, T, Arnold, H-H and Jaenisch, R 1993. MyoD or Myf- 5 is required for the formation of skeletal muscle. Cell 75, 1351–1359.Google Scholar
Salehian, B, Mahabadi, V, Bilas, J, Taylor, WE and Ma, K 2006. The effect of glutamine on prevention of glucocorticoid-induced skeletal muscle atrophy is associated with myostatin suppression. Metabolism. Clinical and Experimental 55, 1239–1247.Google Scholar
Seale, P, Sabourin, LA, Girgis-Gabardo, A, Mansouri, A, Gruss, P and Rudnicki, MA 2000. Pax7 is required for the specification of myogenic satellite cells. Cell 102, 777–786.Google Scholar
Shiokawa, K, Kawazoe, Y, Nomura, H, Miura, T, Nakakura, N, Horiuchi, T and Yamana, K 1986. Ammonium ion as a possible regulator of the commencement of rRNA synthesis in Xenopus laevis embryogenesis. Developmental Biology 115, 380–391.Google Scholar
Shiokawa, K, Aso, M, Kondo, T, Takai, J-I, Yoshida, J, Mishina, T, Fuchimukai, K, Ogasawara, T, Kariya, T, Tashiro, K and Igarashi, K 2010. Effects of S-adenosylmethionine decarboxylase, polyamines, amino acids, and weak bases (amines and ammonia) on development and ribosomal RNA synthesis in Xenopus embryos. Amino Acids 38, 439–449.Google Scholar
Stockdale, FE, Raman, N and Baden, H 1981. Myosin light chains and the developmental origin of fast muscle. Proceedings of the National Academy of Sciences of the United States of America 78, 931–935.Google Scholar
Terjesen, BF, Finn, RN, Norberg, B and Ronnestad, I 2002. Kinetics and fates of ammonia, urea, and uric acid during oocyte maturation and ontogeny of the atlantic halibut (Hippoglossus hippoglossus L.). Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 131, 433–455.Google Scholar
Thompson, JR and Wu, G 1991. The effect of ketone bodies on nitrogen metabolism in skeletal muscle. Comparative Biochemistry and Physiology Part B: Molecular Biology and Biochemistry 100, 209–216.Google Scholar
Webb, DJ and Charbonneau, M 1987. Weak bases inhibit cleavage and embryogenesis in amphibians and echinoderms. Cell Differentiation 20, 33–44.Google Scholar
Wiener, P, Woolliams, JA, Frank-Lawale, A, Ryan, M, Richardson, RI, Nute, GR, Wood, JD, Homer, D and Williams, JL 2009. The effects of a mutation in the myostatin gene on meat and carcass quality. Meat Science 83, 127–134.CrossRefGoogle ScholarPubMed
Wiggins, D, Lund, P and Krebs, HA 1982. Adaptation of urate synthesis in chicken liver. Comparative Biochemistry and Physiology Part B: Molecular Biology and Biochemistry 72, 565–568.CrossRefGoogle ScholarPubMed
Wilson, RP, Muhrer, ME and Bloomfield, RA 1968. Comparative ammonia toxicity. Comparative Biochemistry and Physiology 25, 295–301.Google Scholar
Yonden, Z, Aydin, M, Kilbas, A, Demrin, H, Sutcu, R and Delibas, N 2010. Effects of ammonia and allopurinol on rat hippocampal NMDA receptors. Cell Biochemistry and Function 28, 159–163.Google Scholar
Zammit, PS, Golding, JP, Nagata, Y, Hudon, V, Partridge, TA and Beauchamp, JR 2004. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? The Journal of Cell Biology 166, 347–357.Google Scholar
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