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Myoglobin Chemistry and Modifications that
Influence (Color and) Color Stability
Cameron Faustman
Introduction
Myoglobin is a heme-containing protein that participates
in aerobic metabolism in antemortem muscle by storing
and/or delivering oxygen. Several scholarly reviews have
been devoted to the chemical characterization of myoglobin and its effect on meat color (Faustman and Cassens,
1990; Renerre, 2000; Mancini and Hunt, 2005). This
review will re-confirm the criticality of heme properties
as they relate to meat color and color stability but also
remind the reader that myoglobin’s apoprotein, within
which heme is located, plays an important role in the extent to which heme-related reactions may occur (Wang,
1962).
Relevance of Myoglobin Structure
The primary sequences of myoglobin are known for a variety of animal species including those that are used to
produce meat (Joseph et al., 2010; Yin et al., 2011). As
with all proteins, myoglobin’s constituent amino acids
have chemical similarities but are distinguished from each
other by their reactive side chains. Myoglobin contains
considerable secondary structure and averages approximately 75-80% α-helix (Antonini, 1965). The primary
sequence and chemistry (e.g., polarity) of myoglobin’s
amino acid side chains drives the formation of its tertiary structure which in turn is critical for normal function. Alteration of myoglobin’s tertiary structure through
application of energy including high pressure processing
(Wackerbarth et al., 2009; Ma and Ledward, 2013; Chun
et al., 2014) or irradiation (Brewer, 2004) affects the color of meat. Biological alteration of a protein’s structure
may also be accomplished by substitution of one or more
amino acids to form mutant proteins with compromised
function. The apoprotein pocket within which heme resides in myoglobin is an important part of the protein’s ter-
Cameron Faustman, Ph.D.
Animal Science Department
University of Connecticut
Unit 4040, 3636 Horsebarn Road Extension
Storrs, Connecticut 06269-4040
[email protected]
American Meat Science Association
tiary structure and affects redox stability (Livingston and
Brown, 1981). The relevance of mutations for myoglobin
is that a small structural change would alter the region
around the heme prosthetic group and affect redox stability of the heme and/or the propensity for iron to be lost
from the heme and increase lipid oxidation (Grunwald
and Richards, 2006).
Chemical alteration of the normal protein can also affect macromolecular properties. Reactive side chains of
myoglobin’s amino acids may be accessible to chemical
species that are naturally present in the sarcoplasm or that
are added as a result of processing or experimentation.
The extent of reactivity depends on the protein’s environment (pH, temperature), chemical nature of the amino
acid side chain and the other chemical species present.
Our laboratory has published extensively on the alkylation of myoglobin by α,β-unsaturated aldehydes and the
destabilizing effect these have on oxymyoglobin stability
(Faustman et al, 2010). The evolution of mass spectrometry and tools of proteomics have provided the basis for
advancing studies related to myoglobin primary structure,
and biological and chemical effects on redox stability
(Suman and Joseph, 2011).
Myoglobin and
Meat Color/Color Stability
The heme group of myoglobin contains an iron atom within a protoporphyrin ring. The color that myoglobin imparts to meat is determined by the redox status of its heme
iron and the chemical species bound to heme. Four of the
iron atom’s six coordination sites keep it anchored within
the planar heme structure. One of the coordination sites
binds heme to the apoprotein and the sixth coordination
site is available to bind a variety of ligands; in meat these
include oxygen, water, carbon monoxide and nitric oxide. The conditions for differing colors and their respective common names and their interconversions are presented in Table 1. Deoxymyoglobin (DeOxyMb) is most
commonly observed in freshly cut beef slices. Skeletal
muscles within postmortem, postrigor livestock carcasses
destined for provision of meat are anoxic and DeOxyMb
predominates. This ferrous myoglobin predominates until
meat slice surfaces are exposed to an aerobic atmosphere
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Table 1. Chemical basis for observed myoglobin-related colors in meat.
Redox status
of heme iron
Ferrous, 2+
Ferrous, 2+
Ferric, 3+
Ferrous, 2+
Ferrous, 2+; Ferric, 3+
Ligand at 6th
coordination site
of heme ironNameColor
Nothing
Oxygen
Water
Carbon monoxide
Nitric oxide
where oxygen-binding and formation of oxymyoglobin
(OxyMb) occur. Modified packaging atmospheres which
contain oxygen in a proportion greater than that in the
normal atmosphere have been used to saturate myoglobin and obtain a rich fresh meat color that persists during
retail display (McMillin, 2008; Arvanitoyannis and Stratakos, 2012). Over time, the heme iron in ferrous myoglobins will oxidize to ferric status and this occurs over time
in meat in a fairly predictable muscle-dependent manner
(O’Keeffe and Hood, 1982; McKenna et al., 2005). The
resulting molecule is known as metmyoglobin (MetMb)
and is considered undesirable because of its brownish red
color. The oxidation of ferrous to ferric myoglobin has
been characterized thermodynamically and kinetically
(Shikama, 1985). Under controlled conditions, MetMb
accumulation occurs at different rates in different species
(Chow, 1991; Gutzke et al., 2002; Yin et al., 2012; Nair
DeoxyMb
OxyMb
MetMb
CarboxyMb
Nitric oxide Mb
Purplish red
Cherry red
Brown red
Cherry red
Pink red
et al., 2013) and metmyoglobin accumulates to a point at
which brown coloration predominates and the meat is no
longer considered acceptable. Each of these three redox
forms of myoglobin display distinctive light absorption
characteristics in the visible spectrum (Figure 1) and these
have been used to estimate the relative proportions of the
three redox forms in fresh meat (Tang et al., 2004).
The relative concentration of oxygen to which myoglobin is exposed is critical to the redox form it will assume.
There is an interesting and incompletely understood relationship between the partial pressure of oxygen and the
redox form of myoglobin (Brooks, 1929; Ledward, 1970).
When oxygen is completely absent, or constitutes the
entire atmosphere within which myoglobin resides, the
predominant redox form is DeOxyMb and OxyMb, respectively. When oxygen is present at approximately 4 to
Figure 1. Absorption spectra for OxyMb, MetMb and their combination. Taken from Suman et al.
(2006a) with permission.
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67th Annual Reciprocal Meat Conference
6 mm Hg, the MetMb form will predominate (Ledward,
1970). This is a very important relationship and must be
considered in light of natural oxygen-consumption that
may occur from mitochondrial activity, lipid oxidation
and/or bacterial growth.
The reduction of ferric myoglobin to ferrous myoglobin
has been observed in meat; its occurrence is attributed to
MetMb reductase and/or related enzymes (Bekhit et al.,
2005). It affects perceived color stability because it acts
in opposition to the oxidation process. It is believed the
MetMb reduction counters OxyMb oxidation to the extent
made possible by “reducing equivalents” (e.g., NADH)
present in meat. As these reducing equivalents are consumed and MetMb reduction wanes, MetMb accumulates
and meat discoloration occurs.
Two additional chemical species that readily react with
myoglobin heme iron are carbon monoxide and nitric
oxide. Carbon monoxide binds tightly to heme to form
carboxymyoglobin (CarboxyMb) and yields an absorption
spectrum (Suman et al., 2006a; Smulevich et al., 2007)
and cherry red color that is very similar to that of OxyMb
(Chow et al., 1997; Nam and Ahn, 2002). CarboxyMb
is quite stable compared to OxyMb and can persist for
long periods of time (Jayasingh et al., 2001); it has been
identified as the source of pink color in irradiated poultry
(Nam and Ahn, 2002). The inclusion of carbon monoxide-containing packaging atmospheres for the purpose of
prolonging a desirable red color in fresh meat has been
studied extensively (Luno et al., 1998; Hunt et al., 2004;
Jeong and Claus, 2010).
Nitric oxide myoglobin is typically formed in raw meat
during the preparation of cured products (Moeller and
Skibsted, 2002; Honikel, 2008). Sodium nitrite is chemically reduced through a series of complex chemical reactions to yield the highly reactive nitric oxide which binds
to myoglobin at the 6th coordination site (Sebranek and
Fox, 1985). Connolly et al. (2002) reported that peroxynitrite enhanced the oxidation of OxyMb.
Other Chemical Modifications of
Myoglobin Observed in Meat
Several researchers have reported on the ability of hydrogen sulfide, presumably produced by contaminating
bacteria (Nicol et al., 1970; Egan et al., 1989), to bind
heme and form the green pigment, sulfmyoglobin (Morrell
and Chang, 1967; Berzofsky et al., 1972). Interestingly,
Smolander et al. (2002) reported on the intentional application of this reaction for detecting hydrogen sulfide in
stored poultry meat via agarose-immobilized myoglobin.
Fox et al. (1974) reported that the greenish heme protein,
choleglobin, could be formed by reactions between hydrogen peroxide and heme at acidic pH.
An interesting modification that does not apply to fresh
meat but that is worth noting here is that of the displacement/replacement of iron in heme by zinc to form Znprotoporphyrin IX (Wakamatsu et al., 2004; Adamsen et
American Meat Science Association
al., 2006a). This occurs in dry-cured Italian and Spanish
hams and is responsible for characteristic red colors associated with those traditional products; the addition of
nitrite inhibits formation of the zinc complex (Adamsen
et al., 2006b).
Redox Stability as Affected
by Modifications of the
Myoglobin Apoprotein
In 1989, Faustman et al. (1989ab) published the first
reports of improved beef color stability obtained from vitamin E-supplemented cattle. The effect was subsequently confirmed by many others (Faustman et al., 1998) and
was generally attributed to the fact that vitamin E, i.e.,
α-tocopherol, accumulated in the muscle membranes of
cattle in a dose-dependent manner and acted as an antioxidant. The actual mechanism by which this fat-soluble
antioxidant maintained greater redox stability of watersoluble myoglobin in meat was unclear. It was initially
suggested that α-tocopherol protected unsaturated fatty
acids of membrane phospholipids against oxidation and
that this delayed the production of lipid oxidation breakdown products that were responsible for enhancing myoglobin oxidation. Subsequent investigations provided
support for this hypothesis in vitro (Chan et al., 1997;
Faustman et al., 1999; Lynch and Faustman, 2000). Faustman et al. (1999) demonstrated that α,β- unsaturated aldehydes, known secondary products of lipid oxidation,
formed covalent complexes with myoglobin and that this
was concomitant with enhanced oxidation of untreated
(i.e., no aldehyde addition) controls. Joseph et al. (2009)
reported that HNE can also alkylate CarboxyMb.
The nucleophilic side chains of several of myoglobin’s
constituent amino acids are targets of alkylation by α,βunsaturated aldehydes. Many investigators have used the
α,β- unsaturated aldehyde, 2-hydroxy-4-nonenal (HNE),
as a model secondary product of lipid oxidation (Poli et
al., 2007); HNE has been identified in meat (Sakai et al.,
1998). To date, histidine has been the only amino acid
site confirmed for alkylation by HNE in myoglobin. HNE
appears to decrease myoglobin redox stability and form
more histidine adducts at neutral pH than at meat pH
(Faustman et al., 1999; Alderton et al., 2003; Naveena et
al., 2010). Multiple adducts can be formed depending on
length of incubation and pH (Faustman et al., 1999; Joseph et al., 2009) and species origin (Suman et al., 2006b;
Maheswarappa et al., 2009; Yin et al. 2011; Nair et al.,
2014). Yin et al. (2011) investigated the relative effect of
HNE on myoglobin from seven different meat-producing
species and demonstrated that greater histidine numbers
in the primary sequence predisposed those myoglobins to
greater HNE-enhanced oxidation than those with a lower
number of histidine residues. Suman et al. (2007) reported
that histidine 36 in porcine myoglobin and histidine residues 81 and 88 in bovine myoglobins were preferentially
alkylated by HNE and hypothesized that initial adduct formation might be sufficient to alter tertiary structure such
3
that subsequent alkylation could occur at previously inaccessible amino acid sites. The overall implication of these
reactions would be that myoglobin’s heme pocket might
be altered and expose heme iron to oxidation.
The extent to which secondary products of lipid oxidation actually contribute to redox instability of myoglobin
in meat has not been determined. The model studies noted
previously provide a mechanism that could be a basis for
the long known relationship between lipid oxidation and
myoglobin oxidation. Additionally, the model was used
by Suman et al. (2006b, 2007) to suggest a reason for different responses of pork and beef color stability to dietary
vitamin E supplementation of pigs and cattle, respectively.
That is, while many studies reported that beef color stability was improved, published support for enhanced pork
color stability with vitamin E was considerably less consistent (Suman et al., 2007). This was unexpected because
fatty acids in pork are more unsaturated and if vitamin
E exerted its color-preserving effect by decreasing lipid
oxidation, then pork rather than beef should demonstrate
a greater response to increased muscle concentrations of
α-tocopherol. An examination of the primary sequences
of bovine and porcine myoglobins revealed that the number of histidine residues was 13 and 9, respectively. The
in vitro redox stability of porcine myoglobin was greater
than beef myoglobin when exposed to HNE. Not surprisingly, the extent of adduct formation was less in porcine
myoglobin. Thus, Suman et al. (2007) concluded that
bovine myoglobin’s primary structure predisposed it to
greater HNE alkylation and concomitant myoglobin redox
instability than that of porcine myoglobin.
Subsequent support for the criticality of primary sequence in predicting/describing the bases for myoglobin
susceptibility to HNE and redox instability, particularly
as it related to the observations for porcine and bovine
myoglobins, was provided by Tatiyaborworntham et al.
(2012). Suman et al. (2006b) showed that bovine OxyMb
was alkylated by HNE at 7 sites including histidine 88
and histidine 152, while porcine Mb was not alkylated at
sites 88 (proline; P) or 152 (glutamine; Q). Tatiyaborworntham et al. (2012) hypothesized that the lack of histidine
residues at sites 88 and 152 in porcine Mb contributed
to its slower autoxidation than bovine myoglobin in the
presence of HNE and they used wild type (WT) and mutant sperm whale myoglobins to test the hypothesis. WT
sperm whale and porcine myoglobins contain proline and
glutamine at sites 88 and 152, respectively.
Mutant sperm whale myoglobins were developed in
which histidine (H) was substituted at amino acid residues
88 and 152 (mutant P88H/Q152H). The oxidation of WT
and P88H/Q152H sperm whale OxyMbs were similar,
but the relative oxidation of P88H/Q152H appeared to be
enhanced by HNE more than WT when each was compared to their respective controls (Figure 2). MALDI-TOF
mass spectrometry revealed that each of the myoglobins
contained mono- and di- adducts at 24 hr and 72 hr in-
Figure 2. Effect of 4-hydroxy-2-nonenal (HNE) on relative metmyoglobin formation
in wild type (WT) and mutant (P88H/Q152H) sperm whale myoglobins at pH 5.6 and
4°C. Taken from Tatiyaborworntham et al. (2012) with permission.
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67th Annual Reciprocal Meat Conference
cubation (pH 5.6, 4°C), respectively. Histidine residues
48, 88 and 152 were identified as HNE alkylation sites
by MALDI-TOF-TOF tandem mass spectrometry. It is important to remember that the double mutation not only
increased the number of nucleophilic histidine residues
available for HNE alkylation, but also likely altered the
tertiary structure which would have affected the potential
for HNE adduct formation.
Final Thoughts
The chemistry of myoglobin is critical to understanding
the basis for normal and anomalous color in fresh meat.
Reactions critical to myoglobin redox stability can involve
both the heme and apoprotein components, and future
advancements for improving meat color stability will continue to require attention to the fundamental chemistry of
this protein.
Acknowledgements
I would like to thank all of my colleagues worldwide that
have engaged in meat color research and in particular
those that have focused on the biochemistry of myoglobin. Appreciation is extended to Surendranath Suman
and Joe Sebranek who provided helpful contributions to
this manuscript.
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67th Annual Reciprocal Meat Conference