Mitochondrial treason: a driver of pH decline rate in post-mortem muscle?
Nicholas J. HudsonComputational and Systems Biology, CSIRO Livestock Industries, 306 Carmody Road, St Lucia, Brisbane, Qld 4072, Australia. Email: nick.hudson@csiro.au
Animal Production Science 52(12) 1107-1110 https://doi.org/10.1071/AN12171
Submitted: 13 February 2012 Accepted: 28 June 2012 Published: 4 September 2012
Abstract
The rate and extent of post-mortem pH decline is an important determinant of meat quality, influencing among other things the incidence of pale, soft, exudative meat. In this perspective I argue two things. First, the accuracy of our modelling of pH decline rates might be improved by incorporation of a muscle mitochondrial content parameter. Second, that high mitochondrial content might help explain the surprisingly rapid pH decline that has sometimes been reported in red, oxidative muscles. The proposed physiological mechanism relates to the fact that mitochondria are known to act as net consumers, rather than producers, of ATP during periods of anoxia – a process called mitochondrial treason. To the best of my knowledge, the implications of the phenomenon of mitochondrial treason have never previously been applied or discussed in a meat science context.
References
Aalhus J, Price M (1991) Endurance-exercised growing sheep: I. Post-mortem and histological changes in skeletal muscle. Meat Science 29, 43–56.| Endurance-exercised growing sheep: I. Post-mortem and histological changes in skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbntlOitw%3D%3D&md5=fb98e4307261c45d038f829fb36b053bCAS |
Ashmore C, Parker W, Doerr L (1972) Respiration of mitochondria isolated from dark-cutting beef: postmortem changes. Journal of Animal Science 34, 46–48.
Ashmore C, Carroll F, Doerr L, Tompkins G, Stokes H, Parker W (1973) Experimental prevention of dark-cutting meat. Journal of Animal Science 36, 33–36.
Brooks G, Cassens R (1973) Respiratory functions of mitochondria isolated from stress-susceptible and stress-resistant pigs. Journal of Animal Science 37, 688–691.
Campion D, Olson J, Topel D, Christian L (1975) Mitochondrial traits of muscle from stress-susceptible pigs. Journal of Animal Science 41, 1314–1317.
Cloke JD, Davis EA, Gordon J, Hsieh SI, Grider J, Addis PB, McGrath CJ (1981) Scanning and transmission electron microscopy of normal and PSE porcine muscle. Scanning Electron Microscopy 435–446.
Daly BL, Gardner GE, Ferguson DM, Thompson JM (2006) The effect of time off feed prior to slaughter on muscle glycogen metabolism and rate of pH decline in three different muscles of stimulated and non-stimulated sheep carcasses. Australian Journal of Agricultural Research 57, 1229–1235.
| The effect of time off feed prior to slaughter on muscle glycogen metabolism and rate of pH decline in three different muscles of stimulated and non-stimulated sheep carcasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFeqsr7M&md5=9600baaf4a5e414ac9afd314e047c3ebCAS |
Devine C, Ellery S, Averill S (1984) Responses of different types of ox muscle to electrical stimulation. Meat Science 10, 35–51.
| Responses of different types of ox muscle to electrical stimulation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbmvFChsA%3D%3D&md5=6d0df073a5026c9dc8eb9fa858d84722CAS |
Dutson TR, Pearson AM, Merkel RA (1974) Ultrastructural postmortem changes in normal and low quality porcine muscle fibres. Journal of Food Science 39, 32–37.
| Ultrastructural postmortem changes in normal and low quality porcine muscle fibres.Crossref | GoogleScholarGoogle Scholar |
Ferguson D, Daly B, Gardner G, Tume R (2008) Effect of glycogen concentration and form on the response to electrical stimulation and rate of post-mortem glycolysis in ovine muscle. Meat Science 78, 202–210.
| Effect of glycogen concentration and form on the response to electrical stimulation and rate of post-mortem glycolysis in ovine muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlCrsbbL&md5=0d9658656c5d4bb454a57dca2db2de5dCAS |
Gardner GE, Pethick DW, Greenwood PL, Hegarty RS (2006) The effect of genotype and plane of nutrition on the rate of pH decline in lamb carcasses and the expression of metabolic enzymatic markers. Australian Journal of Agricultural Research 57, 661–670.
| The effect of genotype and plane of nutrition on the rate of pH decline in lamb carcasses and the expression of metabolic enzymatic markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvFaqt7g%3D&md5=9234c217d901cd75186818b3f1ed47b1CAS |
Greaser ML, Cassens RG, Briskey EJ, Hoekstra WG (1969) Post-mortem changes in subcellular fractions from normal and pale, soft, exudative, porcine muscle. 1. Calcium accumulation and adenosine triphosphatase activities. Journal of Food Science 34, 120–124.
| Post-mortem changes in subcellular fractions from normal and pale, soft, exudative, porcine muscle. 1. Calcium accumulation and adenosine triphosphatase activities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXkt1SjtLg%3D&md5=a6473d2931db87b5c655976cc90e7f64CAS |
Hamilton DN, Miller KD, Ellis M, McKeith FK, Wilson ER (2003) Relationships between longissimus glycolytic potential and swine growth performance, carcass traits, and pork quality. Journal of Animal Science 81, 2206–2212.
Hardie DG, Carling D (1997) The AMP-activated protein kinase–fuel gauge of the mammalian cell? European Journal of Biochemistry 246, 259–273.
| The AMP-activated protein kinase–fuel gauge of the mammalian cell?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjvVGrsbs%3D&md5=f3b77bc3e3fbb44e26b6689164a998aeCAS |
Hopkins D, Cassar J, Toohey E, Wynn P (2007) Examination of pH in lot fed beef for Japan. In Proceedings of the New Zealand Society of Animal Production 67, 436–440.
Hoppeler H, Mathieu O, Krauer R, Claassen H, Armstrong RB, Weibel ER (1981) Design of the mammalian respiratory system. VI Distribution of mitochondria and capillaries in various muscles. Respiration Physiology 44, 87–111.
| Design of the mammalian respiratory system. VI Distribution of mitochondria and capillaries in various muscles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M3gtVGgtA%3D%3D&md5=dd909e2169550d83ff569d49797acc7bCAS |
Kuznetsov AV, Kunz WS, Saks V, Usson Y, Mazat JP, Letellier T, Gellerich FN, Margreiter R (2003) Cryopreservation of mitochondria and mitochondrial function in cardiac and skeletal muscle fibers. Analytical Biochemistry 319, 296–303.
| Cryopreservation of mitochondria and mitochondrial function in cardiac and skeletal muscle fibers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsVSmsr0%3D&md5=052b30c79cd1d5165e632e5203c1ea4cCAS |
Lehmann G, Segal E, Muradian KK, Fraifeld VE (2008) Do mitochondrial DNA and metabolic rate complement each other in determination of the mammalian maximum longevity? Rejuvenation Research 11, 409–417.
| Do mitochondrial DNA and metabolic rate complement each other in determination of the mammalian maximum longevity?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1ansLY%3D&md5=da95cf5b3234b27b90c3701c883e4eaaCAS |
Margulis L (1970) ‘Origin of eukaryotic cells.’ (Yale University Press: New Haven, CT)
Monin G, Sellier P (1985) Pork of low technological quality with a normal rate of muscle pH fall in the immediate post-mortem period: the case of the Hampshire breed. Meat Science 13, 49–63.
Parkhouse WS, McKenzie DC, Hochachka PW, Mommsen TP, Ovalle WK, Shinn SL, Rhodes EC (Eds HG Knuttgen, JA Vogel, J Poortmans) (1983) ‘Biochemistry of exercise.’ (Human Kinetics Publishers: Champaign, IL)
Reyes BA, Pendergast JS, Yamazaki S (2008) Mammalian peripheral circadian oscillators are temperature compensated. Journal of Biological Rhythms 23, 95–98.
| Mammalian peripheral circadian oscillators are temperature compensated.Crossref | GoogleScholarGoogle Scholar |
Rogers GW, Brand MD, Petrosyan S, Ashok D, Elorza AA, Ferrick DA, Murphy AN (2011) High throughput microplate respiratory measurements using minimal quantities of isolated mitochondria. PLoS ONE 6, e21746
| High throughput microplate respiratory measurements using minimal quantities of isolated mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVKgtLvL&md5=18064e422400ae59ccb021a47a270915CAS |
Scheffler TL, Gerrard DE (2007) Mechanisms controlling pork quality development: the biochemistry controlling postmortem energy metabolism. Meat Science 77, 7–16.
| Mechanisms controlling pork quality development: the biochemistry controlling postmortem energy metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvVOgtr0%3D&md5=15c2dbab91749bc19cb13cc7add7f5cfCAS |
Schwartz RM, Dayhoff MO (1978) Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts. Science 199, 395–403.
| Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhtVSgurc%3D&md5=e827272089de89b62d16ae72226929ccCAS |
Scott ID, Nicholls DG (1980) Energy transduction in intact synaptosomes. Influence of plasma-membrane depolarization on the respiration and membrane potential of internal mitochondria determined in situ. Biochemical Journal 186, 21–33.
Shen QW, Means WJ, Thompson SA, Underwood KR, Zhu MJ, McCormick RJ, Ford SP, Du M (2006a) Pre-slaughter transport, AMP-activated protein kinase, glycolysis, and quality of pork loin. Meat Science 74, 388–395.
| Pre-slaughter transport, AMP-activated protein kinase, glycolysis, and quality of pork loin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntlWrt74%3D&md5=64f9d38b062d3eac292fbe34a3f18a1cCAS |
Shen QW, Means WJ, Underwood KR, Thompson SA, Zhu MJ, McCormick RJ, Ford SP, Ellis M, Du M (2006b) Early post-mortem AMP-activated protein kinase (AMPK) activation leads to phosphofructokinase-2 and -1 (PFK-2 and PFK-1) phosphorylation and the development of pale, soft, and exudative (PSE) conditions in porcine longissimus muscle. Journal of Agricultural and Food Chemistry 54, 5583–5589.
| Early post-mortem AMP-activated protein kinase (AMPK) activation leads to phosphofructokinase-2 and -1 (PFK-2 and PFK-1) phosphorylation and the development of pale, soft, and exudative (PSE) conditions in porcine longissimus muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtF2qsrY%3D&md5=d9914ab46592ad2246005c1b1a69565fCAS |
St-Pierre J, Brand MD, Boutilier RG (2000) Mitochondria as ATP consumers: cellular treason in anoxia. Proceedings of the National Academy of Sciences of the United States of America 97, 8670–8674.
| Mitochondria as ATP consumers: cellular treason in anoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1GnsLY%3D&md5=100a844fe3d713d6ef70b22afd380320CAS |
Storey KB, Storey JM (2005) Oxygen limitation and metabolic rate depression. In ‘Functional metabolism: regulation and adaptation’. (Ed. KB Storey) pp. 415–442. (John Wiley and Sons: Hoboken, NJ)
Talmant A, Monin G, Briand M, Dadet M, Briand Y (1986) Activities of metabolic and contractile enzymes in 18 bovine muscles. Meat Science 18, 23–40.
| Activities of metabolic and contractile enzymes in 18 bovine muscles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXjtFGisg%3D%3D&md5=bc437495d4e3e59bd0d833e5f5637544CAS |
Werner C, Opalka JR, Gellerich FN, Wicke M (2005) The influence of mitochondrial function on meat quality in turkeys and swine. Archiv Tierzucht 48, 106–114.
Werner C, Natter R, Schellander K, Wicke M (2010) Mitochondrial respiratory activity in porcine longissimus muscle fibers of different pig genetics in relation to their meat quality. Meat Science 85, 127–133.
| Mitochondrial respiratory activity in porcine longissimus muscle fibers of different pig genetics in relation to their meat quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXisFOlsrk%3D&md5=d77fc80ad1b7237b00ad98a9e5dd3691CAS |