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The role of nitric oxide (NO) in the body growth rate of birds

Published online by Cambridge University Press:  12 September 2018

V.YU. TITOV ,
A.M. DOLGORUKOVA ,
V.I. FISININ ,
E.N. BORKHUNOVA ,
G.V. KONDRATOV ,
N.A. SLESARENKO  and
I.I. KOCHISH
V.YU. TITOV*
Affiliation:
All-Russian Scientific Research & Technological Institute of Poultry, Russia
A.M. DOLGORUKOVA
Affiliation:
All-Russian Scientific Research & Technological Institute of Poultry, Russia
V.I. FISININ
Affiliation:
All-Russian Scientific Research & Technological Institute of Poultry, Russia
E.N. BORKHUNOVA
Affiliation:
Moscow State Academy of Veterinary Medicine and Biotechnology, Russia
G.V. KONDRATOV
Affiliation:
Moscow State Academy of Veterinary Medicine and Biotechnology, Russia
N.A. SLESARENKO
Affiliation:
Moscow State Academy of Veterinary Medicine and Biotechnology, Russia
I.I. KOCHISH
Affiliation:
Moscow State Academy of Veterinary Medicine and Biotechnology, Russia
*
Corresponding author: [email protected]
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Abstract

It has been established that embryogenesis is accompanied by the intense production of nitric oxide (NO). Based on available data, the rate of NO production is roughly equal in all embryos of the same poultry species. However, the rate of NO oxidation to nitrate in embryos of meat breeds is higher than in embryos of egg breeds. In broiler embryos about 90% of all produced NO is oxidised to nitrate. In embryos from egg breeds only several per cent of the NO oxidised to nitrate and the other NO is stored in the embryonic tissues included in NO donors. The intensity of NO oxidation in bird embryo is not depended on sex, age of the layer and feeding regime. Intensity of oxidation varies by no more than 10% within a breed strain or cross. Breeding to increase meat productivity is always associated with an increase in the intensity of NO oxidation in the embryo. There is no direct relationship between the increase in NO oxidation and the live weight gain. It can vary from hundreds of percent to several percent depending on the breed. Moreover, morphological differences between breeds with high and low intensity of embryonic NO oxidation are manifested only after hatching, as synthesis of NO is much lower than in the embryo. It has been presumed that NO oxidation is associated with the synthesis or activation of the factor(s) involved with enhanced growth of meat tissue. This is predetermined genetically and can be partly induced by exogenous stimulants, such as green light. The rate of embryonic NO oxidation can therefore be a useful criterion in practical selection of poultry and in the evaluation of growth enhancers acting at the embryonic level.

Keywords

nitrogen oxideembryogenesisnitro- and nitroso-compoundsselection criterion
Type
Review
Information
World's Poultry Science Journal , Volume 74 , Issue 4 , December 2018 , pp. 675 - 686
Copyright
Copyright © World's Poultry Science Association 2018 

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References

ANDERSON, J. (2000) A Role for Nitric Oxide in Muscle Repair: Nitric Oxide–mediated Activation of Muscle Satellite Cells. Molecular Biology of the Cell 11: 1859-1874.Google Scholar
BATTAGLIA, C., CIOTTII, P., NOTARANGELO, L., FRATTO, R., FACCHINETTI, F. and DE ALOYSIO, D. (2003) Embryonic production of nitric oxide and its role in implantation: a pilot study. Journal of Assisted Reproduction and Genetics 20: 449-454.Google Scholar
BLUM, J., DOSOGNE, H., HOEBEN, D., VANGROENWEGHE, F., HAMMON, H., BRUCKMAIER, R. and BURVENICH, C. (2000) Tumor necrosis factor-alpha and nitrite/nitrate responses during acute mastitis induced by Escherichia coli infection and endotoxin in dairy cows. Domestic Animal Endocrinology 9: 223-235.Google Scholar
BLUM, J., MOREL, C., HAMMON, H., BRUCKMAIER, R., JAGGY, A., ZURBRIGGEN, A. and JUNGI, T. (2001) High constitutional nitrate status in young cattle. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 130: 271-282.Google Scholar
BORKHUNOVA, Ye., KONDRATOV, G. and TITOV, V.Yu. (2014) Morphological and biochemical characteristics of hen skeletal muscle on the example of B56 and B79 lines. Russian Veterinary Journal 3: 22-30.Google Scholar
CARRERAS, M., PARGAMENT, G., CATZ, S., PODEROSO, J. and BOVERIS, A. (1994) Kinetics of nitric oxide and hydrogen peroxide production and formation of peroxinitrite during the respiratory burst of human neutrophyls. FEBS Letters 341: 65-68.Google Scholar
CAZZATO, D., ASSI, E., MOSCHENI, C., BRUNELLI, S., DE PALMA, C., CERVIA, D., PERROTTA, C. and CLEMENTI, E. (2014) Nitric oxide drives embryonic myogenesis in chicken through the upregulation of myogenic differentiation factors. Experimental Cell Research 320: 269-280.Google Scholar
DEROEE, A., NARAGHI, M., SONTOU, A., EBRAHIMKHANI, M. and DEHPOUR, A. (2009) Nitric oxide metabolites as biomarkers for follow-up after chronic rhinosinusitis surgery. American Journal of Rhinology & Allergy 23: 159-161.Google Scholar
GHIMIRE, K., ALTMANN, H., STRAUB, A. and ISENBERG, J. (2017) Nitric oxide: what's new to NO? American Journal of Physiology. Cell Physiology 312: C254-C262.Google Scholar
GLADWIN, M., SHELHAMER, J., SCHECHTER, A., PEASE-FYE, M., WACLAWIW, M., PANZA, J., OGNIBENE, F. and CANNON, R. (2000) Role of circulating nitrite and S-nitrosohemoglobin in the regulation of regional blood flow in humans. Proceedings of National Academy of Sciences of USA 97: 11482-11487.Google Scholar
HALEVY, O., PIESTUN, Y., ALLOUH, M., ROSSER, B., RINKEVICH, Y., RESHEF, R., ROZENBOIM, I., WLEKLINSKI-LEE, M. and YABLONKA-REUVENI, Z. (2004) Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Developmental Dynamics 231: 489-502.Google Scholar
HALEVY, O., PIESTUN, Y., ROZENBOIM, I. and YABLONKA-REUVENI, Z. (2006) In ovo exposure to monochromatic green light promotes skeletal muscle cell proliferation and affects myofiber growth in posthatch chicks. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 290: R1062-R1070.Google Scholar
HICKOK, J., SAHNI, S., SHEN, H., ARVIND, A., ANTONIOU, C., FUNG, L. and THOMAS, D. (2011) Dinitrosyliron complexes are the most abundant nitric oxide – derived cellular adduct. Biological parameters of assembly and disappearance. Free Radical Biology & Medicine 5: 11558-11566.Google Scholar
KHAN, H., KUSAKABE, K., WAKITANI, S., HIYAMA, M., TAKESHITA, A. and KISO, Y. (2012) Expression and localization of NO Synthase Isoenzymes (iNOS and eNOS) in development of the rabbit placenta. Journal of Reproduction and Development 58: 231-236.Google Scholar
KIM, Y., CHUNG, H., SIMMONS, R. and BILLIAR, T. (2000) Cellular non-heme iron content is a determinant of nitric oxide-mediated apoptosis, necrosis, and caspase inhibition. Journal of Biological Chemistry 275: 10954-10961.Google Scholar
LEE, H., BAEK, M., MOON, K., SONG, W., CHUNG, Ch., HA, D. and KANG, M-S. (1994) Nitric Oxide as a messenger molecule for myoblast fusion. Journal of Biological Chemistry 269: 14371-14374.Google Scholar
LI, J., BILLIAR, T., TALANIAN, R. and KIM, Y. (1997) Nitric oxide reversibly inhibits seven members of the caspase family via S-nitrosylation. Biochemical and Biophysical Research Communications 240: 419-424.Google Scholar
MONCADA, S., PALMER, R. and HIGGS, E. (1991) Nitric Oxide: Physiology, Pathophysiology, and Pharmacology. Pharmacological Reviews 43: 109-142.Google Scholar
MALYSHEV, I.Y., ZENINA, T.A., GOLUBEVA, L.Y., SALTYKOVA, V.A., MANUKHINA, E.B., MIKOYAN, V.D., KUBRINA, L.N. and VANIN, A.F. (1999) NO-dependent mechanism of adaptation to hypoxia. Nitric Oxide 3: 105-113.Google Scholar
RASSAF, T., PREIK, M., KLEINBONGARD, P., LAUER, T., HEI, C., STRAUER, B., FEELISCH, M. and KELM, M. (2002) Evidence for in vivo transport of bioactive nitric oxide in human plasma. Journal of Clinical Investigation 109: 1241-1248.Google Scholar
RIBEIRO, M.L., OGANDO, D., FARINA, M. and FRANCHI, A. (2004) Epidermal growth factor modulation of prostaglandins and nitrite biosynthesis in rat fetal membranes. Prostaglandins Leukotrienes and Essential Fatty Acids 70: 33-40.Google Scholar
ROSSIG, L., FICHTLSCHERER, B., BREITSCHOPF, K., HAENDELER, J., ZEIHER, A., MULSCH, A. and DIMMELER, S. (1999) Nitric oxide inhibits caspase-3 by S-nitrosation in vivo. Journal of Biological Chemistry 274: 6823-6826.Google Scholar
ROYTER, Y., YEGOROVA, A., VARAKINA, R. and SHAKHNOVA, L. (2005) Industrial poultry breeding. Characteristics of poultry species, lines and crosses. (Sergiev Posad, VNITIP).Google Scholar
ROZENBOIM, I., HUISINGA, R., HALEVY, O. and EL HALAWANI, M. (2003) Effect of Embryonic Photostimulation on the Posthatch Growth of Turkey Poults. Poultry Science 82: 1181-1187.Google Scholar
ROZENBOIM, I., PIESTUN, Y., MOBARKEY, N., BARAK, M., HOYZMAN, A. and HALEVY, O. (2004) Monochromatic light stimuli during embryogenesis enhance embryo development and posthatch growth. Poultry Science 83: 1413-1419.Google Scholar
ROZENBOIM, I., EL HALAWANI, M., KASHASH, Y., PIESTUN, Y. and HALEVY, O. (2013) The effect of monochromatic photostimulation on growth and development of broiler birds. General and Comparative Endocrinology 190: 214-219.Google Scholar
SENGOKU, K., TAKUMA, N., HORIKAWA, M., TSUCHIYA, K., KOMORI, H., SHARIFA, D., TAMATE, K. and ISHIKAWA, M. (2001) Requirement of nitric oxide for murine oocyte maturation, embryo development, and trophoblast outgrowth in vitro. Molecular Reproduction and Development 58: 262-268.Google Scholar
SEVERINA, I., BUSSYGINA, O., PYATAKOVA, N., MALENKOVA, I. and VANIN, A. (2003) Activation of soluble guanylate cyclase by NO donors--S-nitrosothiols, and dinitrosyl-iron complexes with thiolcontaining ligands. Nitric Oxide 8: 155-163.Google Scholar
SOBOLEWSKA, A., ELMINOWSKA-WENDA, G., BOGUCKA, J., SZPINDA, M., WALASIK, K., BEDNARCZYK, M. and PARUSZEWSKA-ACHTEL, M. (2011) Myogenesis--possibilities of its stimulation in chickens. Folia Biologica (Krakow) 59: 85-90.Google Scholar
SOCCO, S., BOVEE, R., PALCZEWSKI, M., HICKOK, J. and THOMAS, D. (2017) Epigenetics: The third pillar of nitric oxide signaling. Pharmacological Research 121: 52-58.Google Scholar
STALMER, J., SINGEL, D. and LOSCALZO, J. (1992) Biochemistry of nitric oxide and its redox-activated forms. Science 258: 1898-1902.Google Scholar
STAMLER, J. and MEISSNER, G. (2001) Physiology of nitric oxide in skeletal muscle. Physiological Reviews 81: 209-237.Google Scholar
TIRONE, M., CONTI, V., MANENTI, F., NICOLOSI, P., D'ORLANDO, C., AZZONI, E. and BRUNELLI, S. (2016) Nitric Oxide Donor Molsidomine Positively Modulates Myogenic Differentiation of Embryonic Endothelial Progenitors. PLoS One. 11 (10): e0164893. doi: 10.1371/journal.pone.0164893.Google Scholar
TITOV, V., VINNIKOVA, E., FISININ, V., BLIZNETSOVA, G. and RETSKY, M. (2008) Significance of Nitrogen Oxide and Its Metabolites in the Development of Embryos. Russian Agricultural Sciences 34: 264-265.Google Scholar
TITOV, V., AKIMOVA, N., VINNIKOVA, E. and FISININ, V. (2009) Nitrogen Oxide Metabolism in Embryos of Fast- and Slow-Growing Poultry Forms. Russian Agricultural Sciences 35: 266-268.Google Scholar
TITOV, V.Y., IVANOVA, A.V., PETROV, V.A., SEREZHENKOV, V.A., MIKOYAN, V.D., VANIN, A.F. and OSIPOV, A.N. (2012a) Can Summary Nitrite+Nitrate Content Serve as an Indicator of NO Synthesis Intensity in Body Tissues? Bulletin of Experimental Biology and Medicine 153: 839-842.Google Scholar
TITOV, V.Yu., VINNIKOVA, E.Z., AKIMOVA, N.S. and FISININ, V.I. (2012b) Nitric oxide (NO) in bird embryogenesis: physiological role and ability of practical use. World's Poultry Science Journal 68: 83-95.Google Scholar
TITOV, V., AKIMOVA, N., IVANOVA, A. and FISININ, V. (2012c) Mechanism of the Relation between the Content of Nitro and Nitroso Compounds in Amnion and Allantois of Chicken Embryos and Rate of Posthatch Chick Growth. Russian Agricultural Sciences 38: 47-50.Google Scholar
TITOV, V.Yu., KOSENKO, O.V., AKIMOVA, N.S. and FISININ, V.I. (2013) Nitric Oxide Metabolism in Poultry Embryo Tissue. Russian Agricultural Sciences 39: 438-441.Google Scholar
TITOV, V.Yu., KONDRATOV, G.V. and IVANOVA, A.V. (2015) Specific Role of Nitric Oxide (NO) in Avian Embryonic Myogenesis. Bulletin of Experimental Biology and Medicine 158: 508-512.Google Scholar
TIWARI, M., PRASAD, S., PANDEY, A., PREMKUMAR, K., TRIPATHI, A., GUPTA, A., CHETAN, D., YADAV, P., SHRIVASTAV, T. and CHAUBE, S. (2017) Nitric oxide signaling during meiotic cell cycle regulation in mammalian oocytes. Frontiers in Bioscience (Scholar Edition) 9: 307-318.Google Scholar
TOMANKOVA, S., ABAFFY, P. and SINDELKA, R. (2017) The role of nitric oxide during embryonic epidermis development of Xenopus laevis. Biology Open 6: 862-871.Google Scholar
VANHOUTTE, P. (2018) Nitric Oxide: From Good to Bad. Annals of Vascular Diseases 11: 41-51Google Scholar
VANIN, A. (2009) Dinitrosyl iron complexes with thiolate ligands: physico-chemistry, biochemistry and physiology. Nitric Oxide 21: 1-13.Google Scholar
VANIN, A., MULLER, B., ALENCAR, J., LOBYSHEVA, I., NEPVEU, F. and STOCLET, J. (2002) Evidence that intrinsic iron but not intrinsic copper determines S-nitrosocysteine decomposition in buffer solution. Nitric Oxide 7: 194-209.Google Scholar
VASIL'EVA, S.V., STUPAKOVA, M.V., LOBYSHEVA, I.I., MIKOYAN, V.D. and VANIN, A.F. (2001) Activation of the Escherichia coli SoxRS-regulon by nitric oxide and its physiological donors. Biochemistry (Moscow) 66: 984-988.Google Scholar
VASUDEVAN, D., BOVEE, R. and THOMAS, D. (2016) Nitric oxide, the new architect of epigenetic landscapes. Nitric Oxide 59: 54-62.Google Scholar
VIGNINI, A., TURI, A., GIANNUBILO, S., PESCOSOLIDO, D., SCOGNAMIGLIO, P., ZANCONI, S., SILVI, C., MAZZANTI, L. and TRANQUILLI, A. (2008) Follicular fluid nitric oxide (NO) concentrations in stimulated cycles: the relationship to embryo grading. Archives of Gynecology and Obstetrics 277: 229-232.Google Scholar
VINNIKOVA, E. and TITOV, V. (2008) Determination of phenotypic ulterior ostrich forms. Ptitsevodstvo 12: 33-34.Google Scholar
VON MANDACH, U., LAUTH, D. and HUCH, R. (2003) Maternal and fetal nitric oxide production in normal and abnormal pregnancy. Journal of Maternal-Fetal and Neonatal Medicine 13: 22-27.Google Scholar
ZHOU, J. and BRUNE, B. (2005) NO and transcriptional regulation: from signalling to death. Toxicology 208: 223-233.Google Scholar