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Titov V.Yu., Dolgorukova A.M., Kochish I.I., Myasnikova O.V. Nitric oxide (NO) content and expression of genes involved in myogenesis in embryonal tissues of chickens (Gallus gallus domesticus L.). Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2024, Vol. 59, № 2, p. 316-327.
(how to cite this article)

doi: 10.15389/agrobiology.2024.2.316eng

UDC: 636.5:591.3

Supported financially by the Russian Science Foundation, grant No. 24-26-00148

 

NITRIC OXIDE (NO) CONTENT AND EXPRESSION OF GENES INVOLVED IN MYOGENESIS IN EMBRYONAL TISSUES OF CHICKENS (Gallus gallus domesticus L.)

V.Yu. Titov1, 2 ✉, A.M. Dolgorukova1, I.I. Kochish2, O.V. Myasnikova2

1Federal Scientific Center All-Russian Research and Technological Poultry Institute RAS, 10, ul. Ptitsegradskaya, Sergiev Posad, Moscow Province, 141311 Russia, e-mail vtitov43@yandex.ru (✉ corresponding author), anna.dolg@mail.ru;
2Skryabin Moscow State Academy of Veterinary Medicine and Biotechnology, 23, ul. Akademika K.I. Skryabina, Moscow, 109472 Russia, e-mail kochish.i@mail.ru, omyasnikova71@gmail.com

ORCID:
Titov V.Yu. orcid.org/0000-0002-2639-7435
Kochish I.I. orcid.org/0000-0001-8892-9858
Dolgorukova A.M. orcid.org/0000-0002-9958-8777
Myasnikova O.V. orcid.org/0000-0002-9869-0876

Final revision received January 29, 2024
Accepted February 26, 2024

 

Nitric oxide is known to be involved in myogenesis in birds. Previously, we established that in the embryos of poultry bred for meat, intensive oxidation of nitric oxide occurs while in the embryos of egg hens it is insignificant and NO accumulates in donor compounds. Within the breed, line and cross, the degree of oxidation of embryonic NO varied by no more than 15 %, and this trait is inherited. In this regard, a number of questions arise. If meat productivity is somehow related to the degree of oxidation of nitric oxide, then what is its role? Does NO itself or its oxidation products have an epigenetic effect during embryogenesis? How is NO oxidized in embryonic tissues and what is the direct physiological role of this process? Is it possible to regulate embryo development by influencing NO synthesis or stimulating its oxidation? The purpose of the work was to compare changes in the NO content in the tissues of meat and egg chicken embryos with changes in the expression of a number of genes involved in myogenesis, in order to elucidate the mechanisms of the possible epigenetic effect of NO as a factor in the regulation of embryonic development. We have shown that the expression of several genes responsible for myogenesis is associated with the concentration of NO in donor compounds. For the study, embryos of chickens (Gallus gallus domesticus L.) of the Hisex White egg cross and the mini-meat breed (line A77, group 2), characterized by high and low intensity of embryonic NO oxidation, respectively, were used. In tissues of the embryo homogenate on day 6 and in homogenates of pectoral and thigh muscles on day 14, the expression of seven genes involved in or influencing myogenesis was assessed. These are the genes for myocyte proliferation factor 2c (Mef 2c), myogenic differentiation 1 (MyoD1), myogenesis factor 5 (Myf 5), myosin (Myh 1), myogenin (Myog), myostatin (MSTN), and growth hormone receptor (GHR). The housekeeping gene TBP (TATA-binding protein gene) was a reference gene. During incubation, we assessed the concentration of embryonic NO, the intensity of its oxidation and the transcriptional activity of myogenesis genes as influenced by in ovo administered nitroarginine (NA), a blocker of NO synthesis, and green light that intensifies the oxidation of embryonic NO to nitrate but does not affects the intensity of NO synthesis. NA, when administered before incubation, on day 6, led to a 70 % decrease in the concentration of NO donor compounds in the embryo homogenate and increased the expression of the MyoD1, Myog and Mef 2c genes in the embryos of Hisex White egg cross. In the mini-meat chickens (line A77, group 2), which are characterized by a low level of deposited NO, the same trend occurred, that is, a decrease in the concentration of donor compounds and an increase in the expression of the MyoD1, Myog and Mef 2c genes, but the difference between the control and test embryos was less pronounced. The use of green light during incubation also contributed to an increase in the expression of the MyoD1, Myog and Mef 2c genes on day 6. Based on these data, it can be assumed that the expression of these genes is affected by the concentration of accumulated NO in the embryo tissues. Factors that cause a decrease in the concentration of accumulated NO increase gene expression, regardless of the method of NO reduction (due to less synthesis or more active oxidation). Therefore, the oxidation of NO in the tissues of the embryo may be a way of regulating gene expression. Mechanisms that ensure this oxidation, are inherited. Artificial regulation of the level of NO donors in embryonic tissues is problematic, since arginine, the source of NO in the avian embryo, is in a saturation concentration for NO synthase, and the NO synthesis blocker nitroarginine effectively suppresses NO synthesis only during the first 7 days of incubation. Nevertheless, the rate of NO oxidation in the embryo is a highly sensitive parameter for selection.

Keywords: nitric oxide, gene expression, avian embryogenesis, myogenesis.

 

REFERENCES

  1. Battaglia C., Ciottii P., Notarangelo L., Fratto R., Facchinetti F., de Aloysio D. Embryonic production of nitric oxide and its role in implantation: a pilot study. Journal of Assisted Reproduction and Genetics,2003, 20(11): 449-454 CrossRef
  2. Ribeiro M., Ogando D., Farina M., Franchi A. Epidermal growth factor modulation of prostaglandins and nitrite biosynthesis in rat fetal membranes. Prostaglandins Leukotrienes and Essential Fatty Acids,2004,70(1): 33-40 CrossRef
  3. Vignini A., Turi A., Giannubillo S., Pescosolido D., Scognamiglio P.,  Zanconi S., Silvi C., Mazzanti L., Tranquilli A. Follicular fluid nitric oxide (NO) concentrations in stimulated cycles: the relationship to embryo grading. Arch. Gynecol. Obstet., 2008, 277(3): 229-232 CrossRef
  4. Socco S., Bovee Rh., Palczewski M., Hickok J., Thomas D. Epigenetics: the third pillar of nitric oxide signaling. Pharmacological Research, 2017, 121: 52-58 CrossRef
  5. Vasudevan D., Bovee R., Thomas D. Nitric oxide, the new architect of epigenetic landscapes. Nitric Oxide, 2016, 59: 54-62 CrossRef
  6. Vasil’eva S., Stupakova M., Lobysheva I., Mikoyan V., Vanin A.  Activation of the Escherichia coli SoxRS-regulon by nitric oxide and its physiological donors. Biochemistry (Moscow), 2001, 66: 984-988 CrossRef
  7. Green J., Rolfe M., Smith L. Transcriptional regulation of bacterial virulence gene expression by molecular oxygen and nitric oxide. Virulence, 2014, 5(8): 794-809 CrossRef
  8. Tucker N., D’autréaux B., Spiro S., Dixon R. Mechanism of transcriptional regulation by the Escherichia coli nitric oxide sensor NorR. Biochem. Soc. Trans., 2006, 34(Pt 1): 191-194 CrossRef
  9. Dokunmu T., Opara S., Imaga N., Awani O., Enoma D., Adelani B. P53 gene expression and nitric oxide levels after artemisinin-caffeine treatment in breast, lungs and liver of DMBA-induced tumorigenesis. Asian Pac. J. Cancer Prev., 2023, 24(2): 451-458 CrossRef
  10. Cazzato D., Assi E., Moscheni C., Brunelli S., De Palma C., Cervia D., Perrotta C., Clementi E. Nitric oxide drives embryonic myogenesis in chicken through the upregulation of myogenic differentiation factors. Experimental Cell Research, 2014, 320(2): 269-280 CrossRef
  11. Hickok J., Vasudevan D., Antholine W., Thomas D. Nitric oxide modifies global histone methylation by inhibiting Jumonji C Domain-containing demethylases. J. Biol. Chem., 2013, 288(22): 16004-16015 CrossRef
  12. Rezakhanlou A., Miller C., McMullin B., Ghaffari A., Garcia R., Ghahary A. Gaseous nitric oxide exhibits minimal effect on skin fibroblast extracellular matrix gene expression and immune cell viability. Cell Biol. Int., 2011, 35(4): 407-415 CrossRef
  13. Xu C., Chen X., Grzeschik S., Ganta M., Wang C. Hydroxyurea enhances SMN2 gene expression through nitric oxide release. Neurogenetics, 2011, 12(1): 19-24 CrossRef
  14. Titov V.Yu., Petrenko Yu.M., Vanin A.F., Stepuro I.I. Biofizika, 2010, 55(1): 95-106 (in Russ.).
  15. Titov V.Yu., Dolgorukova A.M., Kochish I.I., Myasnikova O.V., Nikonov I.N. Features of nitric oxide metabo-lism in embryos of different bird species as genetically determined sign associated with meat productivity. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2022, 57(2): 343-355 CrossRef
  16. Titov V.Yu., Kochish I.I., Dolgorukova A.M. Oksid azota (NO) v embrional’nom i postembrional’nom razvitii ptits [Nitric oxide (NO) in embryonic and postembryonic development of birds]. Moscow, 2022 CrossRef (in Russ.).
  17. Li Y., Wang Y., Willems E., Willemsen H., Franssens L., Buyse J., Decuypere E., Everaer N. In ovo L-arginine supplementation stimulates myoblast differentiation but negatively affects muscle development of broiler chicken after hatching. Journal of Animal Physiology and Animal Nutrition, 2016, 100: 167-177 CrossRef
  18. Sibisi N., Snyman C., Myburgh K., Niesler C. Evaluating the role of nitric oxide in myogenesis in vitro. Biochimie, 2022, 196: 216-224 CrossRef
  19. Wang R., Li K., Sun L., Jiao H., Zhou Y., Li H., Wang X., Zhao J., Lin H. L-Arginine/nitric oxide regulates skeletal muscle development via muscle fibre-specific nitric oxide/mTOR pathway in chickens. Anim Nutr., 2022, 10: 68-85 CrossRef
  20. Buono R., Vantaggiato C., Pisa V., Azzoni E., Bassi M., Brunelli S., Sciorati C., Clementi E. Nitric oxide sustains long-term skeletal muscle regeneration by regulating fate of satellite cells via signaling pathways requiring Vangl2 and cyclic GMP. Stem Cells, 2012, 30(2), 197-209 CrossRef
  21. Anderson J., Zhu A., Mizuno T. Nitric oxide treatment attenuates muscle atrophy during hind limb suspension in mice. Free Radic. Biol. Med., 2018, 115: 458-470 CrossRef
  22. Samengo G., Avik A., Fedor B., Whittaker D., Myung K., Wehling-Henricks M., Tidball J. Age-related loss of nitric oxide synthase in skeletal muscle causes reductions in calpain S-nitrosylation that increase myofibril degradation and sarcopenia. Aging Cell, 2012, 11(6): 1036-1045 CrossRef
  23. Fisinin V.I., Dyadichkina L.F., Goldin Yu.S., Pozdnyakova N.S., Melekhina T.A., Danilov R.V., Gupalo I.M., Royter L.M., Vedenkina I.V., Shinkarenko L.A., Vorontsov A.N., Bosov D.Yu., Afonin V.V. Tekhnologiya inkubatsii yaits sel’skokhozyaystvennoy ptitsy [Technology for incubating poultry eggs]. Sergiev Posad, 2016 (in Russ.).
  24. Krych-Madej J., Gebicka L. Interaction of nitrite with catalase: enzyme activity and reaction kinetics studies. Journal of Inorganic Biochemistry, 2017, 171: 10-17 CrossRef
  25. Schmittgen T., Livak K. Analyzing real-time PCR data by the comparative C(T) method. Nature Protocols, 2008, 3(6): 1101-1108 CrossRef
  26. Zazoua A., Hnaien M., Cosnier S., Jaffrezic-Renault N., Kherrat R. A new HRP/catalase biosensor based on microconductometric transduction for nitrite determination. Materials Science and Engineering C, 2009, 29: 1919-1922 CrossRef
  27. Ojani R., Raoof J.-B., Rahemi V. A simple and efficient electrochemical sensor for electrocatalytic reduction of nitrite based on poly(4-aminoacetanilide) film using carbon paste electrode. Journal of the Chinese Chemical Society, 2011, 58(2): 247-254 CrossRef
  28. Rozenboim I., El Halawani M., Kashash Y., Piestun Y, Halevy O. The effect of monochromatic photostimulation on growth and development of broiler birds. General and Comparative Endocrinology, 2013, 190: 214-219 CrossRef
  29. Sobolewska A., Elminowska-Wenda G., Bogucka J., Szpinda M., Walasik K., Bednarczyk M., Paraczewska-Achtel M. Myogenesis — possibilities of its stimulation in chickens. Folia biologica (Kraków),2011,59(3-4): 85-90 CrossRef
  30. Halevy O., Piestun Y., Rozenboim I., Yablonka-Reuveni Z.  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,2006,290(4): R1062-R1070 CrossRef

 

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