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«Arch. Tierz., Dummerstorf 49 (2006) Special Issue, 04-17 Institut National de la Recherche Agronomique (INRA), UMR SENAH, 35590 Saint-Gilles, France ...»

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Arch. Tierz., Dummerstorf 49 (2006) Special Issue, 04-17

Institut National de la Recherche Agronomique (INRA), UMR SENAH, 35590 Saint-Gilles, France


Myofibre typing and its relationships to growth performance and

meat quality


A dramatic increase of growth performance has been achieved through selection for muscle accretion and

improvement of nutrition and breeding conditions in meat animals. However, evidence suggests that this may have resulted in altered meat quality. Skeletal muscle is a highly heterogeneous tissue containing myofibres, connective tissue, adipocytes, vascular and neural tissues. Muscle fibres can be characterized by their total number, size and contractile and metabolic properties, and are thought to influence meat quality, even though such a direct effect has not been clearly demonstrated. After a presentation of recent knowledge underlying conventional myofibre typing, the review will focus on relationships between fibre type composition and intramuscular fat content, heritability of myofibre traits, and implications of myofibre traits for growth performance and meat quality. Thus, the presence of four adult myosin heavy chain genes (I, IIa, IIx and IIb) shows that conventional myofibre classifications in three types should be revised, at least in species where IIx and IIb isoforms are expressed, such as pigs. Beyond the difference in the amount and distribution of mitochondria between fibre types, recent studies show that mitochondria are also intrinsically different between fibre types. Interestingly, no relationship seems to exist between fibre type composition and total intramuscular fat content, suggesting that both traits can be manipulated independently. On the opposite, the content and nature of phospholipids located in membranes is closely related to fibre type composition. The high heritability and genetic variability of myofibre traits show that selection can be used to influence muscle biological properties.

Data on relationships between myofibre traits and growth performance or meat quality show that identifying the best fibre type to improve meat production and meat quality traits remains a difficult task. It is suggested that selection experiments directly based on myofibre traits and the study of the correlated responses of growth and meat quality may provide better tools to study these relationships. Finally, possible reasons which could explain the difficulty of establishing the specific influence of myofiber traits on meat production and quality traits are discussed.

Key Words: muscle fibre, intramuscular fat, heritability, growth, meat quality Zusammenfassung Titel der Arbeit: Muskelfaser-Typisierung und deren Beziehung zu Wachstumsleistung und Fleischqualität Eine drastische Zunahme der Wachstumsleistung ist bei Nutztieren durch Selektion auf Muskelansatz und die Verbesserung der Tierernährung und Haltungsbedingungen erzielt worden. Es gibt jedoch Hinweise, dass dies mit einer Veränderung der Fleischqualität einhergegangen ist. Skelettmuskulatur ist ein heterogenes Gewebe bestehend aus Muskelfasern, Bindegewebe, Fett, Blutgefäßen und Nerven. Muskelfasern können durch ihre Gesamtzahl, Größe und kontraktilen und metabolischen Eigenschaften charakterisiert werden und es wird davon ausgegangen, dass sie die Fleischqualität beeinflussen, obwohl ein solcher Effekt nie direkt gezeigt werden konnte. Neben einer Darstellung des aktuellen Kenntnisstandes zur Muskelfasertypisierung fokussiert diese Übersicht auf das Verhältnis zwischen Fasertyp und intramuskulärem Fettgehalt, Erblichkeit der Muskelfasermerkmale und ihre Bedeutung für Wachstumsleistung und Fleischqualität. Die Existenz von vier Genen für die schweren Ketten des adulten Myosins (myosin heavy chain genes (I, IIa, IIx und IIb), belegt, dass die herkömmlichen Muskelfaserklassifikationen in drei Typen verbessert werden sollten, mindestens bei den Spezies, bei denen die Isoformen IIx und IIb exprimiert werden, wie bei Schweinen. Über den Unterschied bezüglich der Menge und der Verteilung von Mitochondrien zwischen Faserarten hinaus, zeigen neue Studien, dass Mitochondrien auch zwischen Faserarten unterschiedlich sind. Interessanterweise scheint kein Zusammenhang zwischen Fasertypen und intramuskulärem Fettgehalt zu bestehen und beide Merkmale scheinen unabhängig voneinander züchterisch bearbeitet werden zu können. Im Gegensatz dazu besteht ein enger Zusammenhang zwischen Gehalt und Art der Phospholipide in den Membranen und der Muskelfasertypverteilung. Die hohe Erblichkeit und genetische Variabilität der Muskelfasermerkmale zeigen, dass Selektion auf biologische Eigenschaften des Muskels möglich ist. Daten zur Beziehung zwischen Muskelfasertypen und Wachstumsleistung und Fleischqualität zeigen, dass es nach wie vor schwierig ist die hinsichtlich dieser Merkmale vorteilhaften Muskelfasern zu benennen. Experimente mit direkter Selektion auf Muskelfasermerkmale und Erfassung von Wachstums- und Fleischqualitätsmerkmalen sollten weiteren Aufschluss über diesen Zusammenhang geben.

Schließlich werden mögliche Gründe für die Schwierigkeit, den Zusammenhang zwischen Muskelfaser- und Fleischproduktionsmerkmalen herzustellen, diskutiert.

Schlüsselwörter: Muskelfasern, intramuskuläres Fett, Erblichkeit, Wachstum, Fleischqualität Introduction To improve efficiency and profitability of meat animal production, genetic selection, nutrition and breeding conditions have led to a dramatic increase in lean tissue content while decreasing fat deposition. However, there have been some concerns that this would have led to a deterioration of meat quality (CAMERON et al., 1999), but the underlying biological mechanisms are not clearly identified. The highly heterogeneous composition of skeletal muscle makes it difficulty to identify the muscle components specifically involved in the variability of meat quality. Skeletal muscle contains about 75% water, 19% protein, 0.5 to about 10% lipid and 1% glycogen, and is mainly composed of different myofibres, along with intramuscular adipocytes and connective, vascular and nervous tissues. It is widely accepted that myofibre type composition is an important source of variation in meat quality. However, such a direct effect has not been clearly demonstrated and an indirect influence through associations with changes in other muscle components, such as intramuscular fat and/or connective tissue may occur. Myofibres can be characterized by their total number, cross-sectional area (CSA), length and contractile and metabolic types. The total number of fibres (TNF) is reported to be definitely fixed before birth in species such as cattle, pig and chicken (ASHTON et al., 2005). In contrast, myofibre CSA remains quite constant during gestation and dramatically increases postnatally, all the more the fibre is becoming glycolytic (REHFELDT, 2005). After a review of recent data underlying myofibre typing (1), the paper will focus on (2) the relationships between fibre typing and intramuscular fat (IMF) content, (3) genetic data on myofibre traits, and implications of myofibre traits for (4) growth performance and (5) meat quality.

1. Myofibre typing Conventionally, differences in the sensitivity of acto-myosin ATPase activity to pH preincubation has been used to distinguish types I, IIA and IIB fibres by histochemistry (BROOKE and KAISER, 1970). The existence of four adult skeletal myosin heavy chains (MyHC), i.e. types I, IIa, IIx and IIb, was first documented in mice, rats, guinea pigs and rabbits (BÄR and PETTE, 1988; SCHIAFFINO et al.,

1989) and led to revise the conventional fibre classification. Each MyHC is encoded by a separate gene (WEISS et al., 1999). Despite the presence of the IIb gene, the type IIb MyHC isoform was initially reported to be unexpressed in skeletal muscles of large mammals such as human, cattle, horse, goat and dog (SMERDU et al., 1994; ENNION et al., 1995; TANABE et al., 1998; RIVERO et al., 1999; ARGUELLO et al., 2001;

SMERDU et al., 2005). However, recent data using immunocytochemistry, in situ hybridization (Figure 1) and real time RT-PCR demonstrated that IIb MyHC was highly expressed in glycolytic pig and llama skeletal muscles (LEFAUCHEUR et al., 1998; GRAZIOTTI et al., 2001; DA COSTA et al., 2002; LEFAUCHEUR et al., 2002). Interestingly, conventional type IIB fibres exhibit either a moderate or weak oxidative metabolism (Figure 1B) which actually correspond to real types IIx and IIb MyHC expressing fibres, respectively (Figure 1C,D). Therefore, the conventional histochemical fibre typing in types I, IIA and IIB (BROOKE and KAISER, 1970) is

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Muscle fibres use a large amount of ATP for contraction through activation of the acto-myosin ATPase, and a harmonious functioning needs a balance between ATP consumption and production. The relative importance of the two main metabolic pathways of energy production, i.e. glycolysis and mitochondrial oxidative phosphorylation, varies between fibre types depending on their contractile patterns.

Thus, the fast type IIb fibres are adapted to brief and intense contractions fuelled by the glycolytic pathway and immediate availability of phosphocreatine. Type IIx fibres are close to IIb ones, except that they are slightly more oxidative. On the opposite, the slow type I fibres can sustain prolonged low power work in association with a welldeveloped oxidative metabolism. Type IIa fibres are oxido-glycolytic and exhibit an intermediate contractile function between types I and IIx fibres. Interestingly, the few mitochondria of glycolytic fibres are homogeneously distributed throughout the fibre, whereas the numerous mitochondria of oxidative fibres exhibit a radial gradient with a concentration under the plasma membrane (SWATLAND, 1984). Beyond the well documented difference in the amount and distribution of mitochondria between fibre types, recent studies carried out on permeabilized fibres showed that mitochondria are also intrinsically different between fibre types (GUEGUEN et al., 2005a; GUEGUEN et al., 2005b). Thus, the stimulation of mitochonrial respiration by ADP was more sensitive to ADP in types IIb and IIx (Km = 8 µM) than IIa (72 µM) and I (212 µM) fibres, suggesting that mitochondrial respiration is strongly regulated by ADP in types IIb and IIx fibres, whereas other mechanisms are involved in type I fibres. Thus, the addition of creatine or AMP strongly stimulated mitochondrial respiration in type I fibres, whereas no effect was observed in types IIb and IIx fibres, showing a strong coupling between mitochondrial kinases (miCK and AK2) and oxidative phosphorylation in type I fibres, type IIa fibres exhibiting intermediate properties between types I and IIx fibres.

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Fig. 1: Fibre typing of M. longissimus of Large White at 62 kg BW (131 d of age). Detection of mATPase after preincubation at pH 4.35 (A) and succino-dehydrogenase activity (B). Fibres types I, IIA and IIB (BROOKE and KAISER, 1970). In situ hybridization with type IIx (C) and IIb (D) MyHC 35S labelled riboprobes. The x letters denote corresponding type IIx fibres on the serial sections. Bar = 100 µm (adapted from LEFAUCHEUR et al., 2002) (Fasertypisierung vom M. longissimus von Large White bei 62 kg KW (131 Tagen). Nachweis von mATPase nach Inkubation bei pH 4.6 (A) und Succinatdehydrogenase (B). Fasertypen I, IIa, IIB (BROOKE and KAISER, 1970). In situ Hybridisierung mit Typ IIx (C) and IIb (D) MyHC 35S markierten Riboproben. Typ IIxFasern sind mit x gekennzeichnet. Balken = 100 µm (modifiziert nach LEFAUCHEUR et al., 2002))

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Fig. 2: In situ hybridization using 35S labelled MyHC IIx and IIb riboprobes in longissimus muscle of Large White (LW) and Meishan (MS) pigs at 62 kg BW (adapted from LEFAUCHEUR et al., 2004) (In situ Hybridisierung mit Typ IIx and IIb MyHC 35S markierten Riboproben bei Large White und Meishan Schweinen bei 62 kg Körpergewicht (modifiziert nach LEFAUCHEUR et al., 2004)) Glucose, glycogen and fatty acids are important fuels for muscle bioenegetics. It is well established that glucose uptake (BONEN et al., 1981), incorporation of 14Cglucose into glycogen (BÄR and BLANCHAER, 1965), turnover of glycogen (VILLA-MORUZZI et al., 1979) and the number of insulin receptors (LEFAUCHEUR et al., 1986) are higher in type I than II fibres, in particular glycolytic type IIb fibres.

Glycogen distribution is highly variable between fibres and highly dependent on environmental factors, such as exercise, stress and fasting. On average, its level is lower in type I and sometimes type IIA than type IIB fibres, the last ones also exhibit a greater variability of glycogen distribution (KARLSSON et al., 1993; FERNANDEZ et al., 1995). Muscle glycogen content is also influenced by genetic factors. Thus, a single nonsense mutation (R225Q) in the RN gene coding for the γ3 subunit of an AMP dependent serine/threonine kinase (AMPK) has been shown to specifically increase glycogen level by 70% in pig glycolytic muscles, specifically in glycolytic type IIb fibres (MONIN et al., 1987; MARINOVA et al., 1992; MILAN et al., 2000).

Intramyocellular triglyceride level is consistently higher in type I fibres than all fast type II fibres (ESSÉN-GUSTAVSSON et al., 1994), with no significant difference between subtype II fibres. Obesity and/or insulin resistance have often been reported to be associated with increased levels of intramyocellular triglycerides (LOON and GOODPASTER, 2005), however, this does not seem to be a functional relationship.

Indeed, two factors known to increase intramyocellular triglyceride levels, i.e. type I fibre and endurance training, also increase sensitivity of glucose uptake to insulin and decrease insulin resistance.

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