Elsevier

Meat Science

Volume 80, Issue 2, October 2008, Pages 511-521
Meat Science

Inhibition of nitric oxide release pre-slaughter increases post-mortem glycolysis and improves tenderness in ovine muscles

https://doi.org/10.1016/j.meatsci.2008.02.002Get rights and content

Abstract

The aim of this experiment was to determine the effect of inhibiting the release of nitric oxide (NO) pre-slaughter in lambs on post-slaughter muscle metabolism and meat quality. Exercise was used as a positive control as NO is known to be released in skeletal muscle during exercise. Forty Border Leicester × Merino lambs were assigned to the treatments L-NAME (NO synthase inhibitor) infusion (0 mg/kg vs. 30 mg/kg, 135 min pre-slaughter) and exercise (none vs. 15 min immediately pre-slaughter). The inhibition of NO release using L-NAME reduced Warner–Bratzler shear force (WBSF) in the longissimus thoracis et lumborum (LTL) after 3 days of ageing, while the Semimembranosous (SM) was unaffected. Inhibition of NO release with L-NAME resulted in altered glucose metabolism as indicated by reduced plasma glucose pre-slaughter particularly in exercised lambs, reduced LTL and SM glycogen of non-exercised lambs post-slaughter and increased SM lactate in exercised lambs post-slaughter. In conclusion, inhibition of NO Synthase with L-NAME pre-slaughter increases post-mortem glycolysis and improves tenderness in the loin muscle.

Introduction

Nitric oxide (NO) has emerged as an important regulator of skeletal muscle homeostasis, where it interacts with many physiological pathways, some of which are important to meat quality. Examples include nitric oxide influencing glycogenolysis (Borgs et al., 1996, Jaffrey et al., 2001), glycolysis (Mohr, Stamler, & Brune, 1996), cytosolic calcium flux (Eu et al., 1999, Ishii et al., 1998, Meszaros et al., 1996) and inhibition of calpain activity (Koh and Tidball, 2000, Michetti et al., 1995).

NO is generated from arginine by the enzyme nitric oxide synthase (NOS). While injection of inhibitors of nitric oxide synthase (NOS) into hot-boned beef has been observed to reduce tenderness in one study (Cook, Scott, & Devine, 1998), it has been hypothesised that NOS activity post-slaughter is limited (Brannan and Decker, 2001, Cottrell et al., 2002). Brannan and Decker (2002) showed NOS activity, when measured in vitro, remained until 24 h in pork muscle but disappeared immediately after slaughter in chicken, turkey and trout muscle. It is likely that this is due to the tight regulation of NO biosynthesis, which requires many co-factors, including O2 and NADPH (Bredt & Snyder, 1994), which are in low abundances in ischaemic muscle. Therefore, due to reduced substrate availability and temperature in the post-slaughter environment, it is likely that NOS activity is significantly attenuated. Since inhibition of endogenous NOS has only been attempted in hot-boned muscles (Cook et al., 1998, Cottrell et al., 2002), where activity is likely to be already attenuated (Brannan and Decker, 2001, Brannan and Decker, 2002, Cottrell et al., 2002), the real effect of endogenous NO on meat quality remains untested. The aims of this experiment therefore were to investigate the effect of endogenous NO on meat quality by increasing and decreasing muscle NOS activity with exercise (Jungersten et al., 1997, Roberts et al., 1999) and a pharmacological inhibitor, respectively.

Section snippets

Animals and catheterisation

Forty Border Leicester/Merino cross lambs, approximately six months old, ranging between 33.5 and 51.0 kg live weight were housed in individual pens with visual and audial contact for 10–14 days pre-slaughter to acclimatise. During this period, lambs had access to alfalfa chaff and concentrate pellets (Barastoc Stockfeeds) and water ad libitum. At one day pre-slaughter, a catheter was inserted into the jugular vein (i.v.). Food was removed approximately 12 h pre-slaughter, but ad libitum access to

Plasma and muscle metabolites

Plasma glucose and lactate concentrations before exercise were not influenced by L-NAME infusion (Glucose; (3.1 vs. 3.0 ± 0.04 mmol/L for 0 vs. 30 mg/kg L-NAME, P = 0.56. Lactate; 0.44 vs. 0.45 ± 0.016 mmol/L, P = 0.40). Exercise increased plasma glucose concentrations 2-fold and lactate concentrations 6-fold respectively (Table 1). In exercised lambs, pre-infusion of L-NAME reduced exercise mediated hyperglycaemia by approximately 30%, while no difference in lactate concentrations were observed.

Overall,

Discussion

The effects of animal stress on physiological components within skeletal muscle remain poorly understood. Hence, it is a high priority to understand acute skeletal muscle physiological and regulatory pathways that ultimately influence meat quality. The aim of this experiment was to determine whether endogenous synthesis of the regulatory molecule NO influenced meat glycogen content, pH, sarcomere length, colour, water holding capacity and tenderness. This was accomplished by the use of the NOS

Conclusion

These data indicate that NO plays a role in the conversion of muscle to meat, influencing muscle proteolysis and glycolysis. The reduction in plasma glucose concentrations after NOS inhibition in exercised lambs indicates that NO is involved in stimulating glucose release during exercise. This also indicates that NOS activity is increased during exercise-stress. While the glycogenolytic and glycolytic effects of NOS inhibition were observed independently of exercise, increases in muscle lactate

Acknowledgment

The funding of Meat and Livestock Australia and technical assistance of M. Kerr, L. Can, S. Baud, T. Hauke, P. Walker, B. Doughton, D. Kerton, S. Coronado and K. Perkins is gratefully acknowledged.

References (57)

  • J.P. Eu et al.

    Regulation of ryanodine receptors by reactive nitrogen species

    Biochemical Pharmacology

    (1999)
  • B.L. Firestein et al.

    Interaction of neuronal nitric-oxide synthase and phosphofructokinase-M

    Journal of Biological Chemistry

    (1999)
  • I.H. Hwang et al.

    The effect of time and type of electrical stimulation on the calpain system and meat tenderness in beef longissimus dorsi muscle

    Meat Science

    (2001)
  • K. Immonen et al.

    Variation of residual glycogen–glucose concentration at ultimate pH values below 5.75

    Meat Science

    (2000)
  • T. Ishii et al.

    Inhibition of skeletal muscle sarcoplasmic reticulum Ca2+-ATPase by nitric oxide

    FEBS Letters

    (1998)
  • A. Kaasik et al.

    Nitric oxide inhibits cardiac energy production via inhibition of mitochondrial creatine kinase

    FEBS Letters

    (1999)
  • M. Koohmaraie

    Muscle proteinases and meat ageing

    Meat Science

    (1994)
  • L.G. Meszaros et al.

    Inhibition of the skeletal muscle ryanodine receptor calcium release channel by nitric oxide

    FEBS Letters

    (1996)
  • M. Michetti et al.

    Reversible inactivation of calpain isoforms by nitric oxide

    Biochemical and Biophysical Research Communications

    (1995)
  • S. Mohr et al.

    Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase

    Journal of Biological Chemistry

    (1999)
  • S. Mohr et al.

    Posttranslational modification of glyceraldehyde-3-phosphate dehydrogenase by S-nitrosylation and subsequent NADH attachment

    Journal of Biological Chemistry

    (1996)
  • G. Monin et al.

    Influence of breed and muscle metabolic type on muscle glycolytic potential and meat pH in pigs

    Meat Science

    (1987)
  • J.A. Moy et al.

    Effects of nitric oxide on platelet-activating factor- and alpha-adrenergic-stimulated vasoconstriction and glycogenolysis in the perfused rat liver

    Journal of Biological Chemistry

    (1991)
  • A. Tatoyan et al.

    Purification and characterization of a nitric-oxide synthase from rat liver mitochondria

    Journal of Biological Chemistry

    (1998)
  • Anonymous. (1992). AUS-MEAT language, authority for uniform specification of meat and livestock. Sydney,...
  • P.E. Bouton et al.

    Effect of ultimate pH upon the water holding capacity and tenderness of mutton

    Journal of Food Science

    (1971)
  • S.J. Bradley et al.

    Nitric oxide synthase inhibition reduces leg glucose uptake but not blood flow during dynamic exercise in humans

    Diabetes

    (1999)
  • R.G. Brannan et al.

    Peroxynitrite-induced oxidation of lipids: Implications for muscle foods

    Journal of Agricultural and Food Chemistry

    (2001)
  • Cited by (25)

    • A comparative study of S-nitrosylated myofibrillar proteins between red, firm and non-exudative (RFN) and pale, soft and exudative (PSE) pork by iodoTMT-based proteomics assay

      2022, Food Chemistry
      Citation Excerpt :

      Protein S-nitrosylation, which refers to the covalent attachment of nitric oxide (NO) group to the sulfhydryl of protein cysteine to form S-nitrosothiol, is considered as a common post-translational modification in cell signaling pathway (Hess, Matsumoto, Kim, Marshall, & Stamler, 2005). Previous researches have been conducted to investigate the potential role of NO and its-induced protein S-nitrosylation in regulating fresh meat quality by managing the content of NO in postmortem muscle (Cottrell, McDonagh, Dunshea, & Warner, 2008; Cottrell, Ponnampalam, Dunshea, & Warner, 2015). A hypothesis was made that NO produced in postmortem muscle would modify the protein cysteine for S-nitrosylation, which may regulate the protein activity, function and interaction, and in turn affect physiological metabolism of muscle and the meat quality during postmortem aging (Liu, Warner, Zhou & Zhang, 2018a).

    • Muscle structure, proteins, and meat quality

      2022, New Aspects of Meat Quality: From Genes to Ethics, Second Edition
    View all citing articles on Scopus
    1

    Present address: Faculty of Land and Food Resources, University of Melbourne, Parkville 3053, Australia.

    View full text