Why Do We Have Purkinje Fibers Deep in Our Heart?

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Physiol. Res. 63 (Suppl. 1): S9-S18, 2014
REVIEW
Why Do We Have Purkinje Fibers Deep in Our Heart?
D. SEDMERA1,2, R. G. GOURDIE3,4,5
1
Institute of Anatomy, First Faculty of Medicine, Charles University, Prague, Czech Republic,
Department of Cardiovascular Morphogenesis, Institute of Physiology Academy of Sciences of the
Czech Republic, Prague, Czech Republic, 3Virginia Tech Carilion Research Institute, Center for
Heart and Regenerative Medicine Research, Roanoke, Virginia, USA, 4Virginia Tech School of
Biomedical Engineering and Sciences, Roanoke, Virginia, USA, 5Department of Emergency
Medicine, Virginia Tech Carilion School of Medicine, Roanoke, Virginia, USA
2
Received October 21, 2013
Accepted October 29, 2013
Summary
Purkinje fibers were the first discovered component of the
cardiac conduction system. Originally described in sheep in 1839
as pale subendocardial cells, they were found to be present,
although with different morphology, in all mammalian and avian
hearts. Here we review differences in their appearance and
extent in different species, summarize the current state of
knowledge of their function, and provide an update on markers
for these cells. Special emphasis is given to popular model
species and human anatomy.
Key words
Cardiac conduction system • Specialized tracts • Gap junctions •
Connexin
Corresponding author
D. Sedmera,
Department
of
Cardiovascular
Morphogenesis,
Institute of Physiology, Academy of Sciences of the Czech
internodal tracts, the atrioventricular node, the
atrioventricular (His) bundle, its right and left branches,
and the network of Purkinje fibers. While the functional
equivalent of these components are present in some form
in all vertebrate hearts (Sedmera et al. 2003), all
morphologically distinct parts are present only in the
heart of mammals. While development of the CCS has
been subject to numerous reviews (Gourdie et al.
2003a,b, Christoffels et al. 2010, Burggren et al. 2013),
little was written on the comparative morphology of its
components in different species, with a few notable
exceptions (Davies 1930, Davies et al. 1952, 1994). The
goal of this overview is to put the Purkinje fibers into
context of other CCS components, briefly describe the
history of their discovery, provide functional insight into
equivalent structures in the lower vertebrates, and then to
focus in detail on their structure and function in the most
popular model species of mammals and birds.
Republic, Videnska 1083, 14220 Prague, Czech Republic. E-mail:
[email protected]
Function of individual CCS components
Introduction
The SA node is the principal pacemaker of the
heart. Under normal conditions it is the cardiac tissue that
autonomously sets the rhythm of the heart beat. It is also
subject to neurohumoral regulation, in particular by
autonomous nervous system. This allows the heart to
change its frequency in reaction to the functional status of
the organism. Morphologically, it is organized into a
three dimensionally complex compact structure
The cardiac conduction system (CCS) is defined
as a network of specialized myocardial cells that
generates the cardiac rhythm and assures a coordinated
propagation of the electrical impulse for efficient
contraction of the heart. In the adult mammalian heart,
the CCS comprises the sinoatrial (SA) node, the
PHYSIOLOGICAL RESEARCH • ISSN 0862-8408 (print) • ISSN 1802-9973 (online)
© 2014 Institute of Physiology v.v.i., Academy of Sciences of the Czech Republic, Prague, Czech Republic
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Vol. 63
Sedmera and Gourdie
(Mommersteeg et al. 2007, Fedorov et al. 2010), with
specific connection points to the working atrial
myocardium. In lower vertebrates, its function is
contained in a compartment termed the sinus venosus
(Koprla 1987, Jensen et al. 2012). New data on the
cellular origin of the SA node from outside the traditional
heart fields and role of Wnt signaling in recruitment of
mesodermal cells into pacemaker lineage were recently
reported by the Mikawa lab (Bressan et al. 2013).
(Mommersteeg et al. 2007, Aanhaanen et al. 2009, 2010).
Electrophysiologically, this region shows a typical action
potential shape (Arguello et al. 1986) and has a level of
automaticity, which can manifest even in the embryo
when the sinoatrial node is perturbed (Raddatz 1997).
Interfaces between atria and node and node and His are
marked by distinct transitions in connexin expression
(Coppen et al. 1999, Gourdie and Sedmera 2008). Such
abrupt changes in cellular coupling can play a role in AV
delay generation in adult heart (Choi and Salama 1998).
Atrial special conduction pathways
The His bundle
The morphological distinction of specialized
intra-atrial and internodal conduction pathways is a
controversial topic. Some claim that there are tracts of
Purkinje-like cells connecting the sinoatrial and
atrioventricular node (James and Sherf 1971), while other
agree that the conduction through the atria is anisotropic,
see the main reason in holes caused by the entrance
vessels (Betts et al. 2002, Ho et al. 2002). Our view is
that these preferential conduction pathways, the best
example of which is the interatrial bundle of Bachmann
(Sedmera et al. 2006) can be explained by tissue
geometry (pectinate muscles), in agreement with previous
experimental data (Komuro et al. 1986), but are open to a
marker that would distinguish cells within those tracts
from the remaining atrial myocytes.
The AV node
The main function of the atrioventricular node is
generation of a delay between activation (and ensuing
contraction) of the atria and the ventricles. Due to its
prolonged refractory period, it also serves as a filter
against propagation of atrial tachyarrhythmias to the
ventricles. In mammals, it shows a distinct morphological
organization with specific cell phenotypes (Efimov et al.
1997, Aanhaanen et al. 2010). On the other hand, its
morphological localization in birds is still obscure
(Vicente-Steijn et al. 2011). In lower vertebrates, and
during embryonic development, the function of delay
generator is located in the atrioventricular canal region, a
slowly proliferating, conducting and contracting portion
of the cardiac tube that apparently retains its “primitive”
phenotype – not following the pathway of chamber
myocardium
differentiation
(Kirby 2007).
The
transcriptional regulation of these events has been
recently uncovered, and Tbx2, BMP and Tbx3 are
implicated in maintaining this transcription programme
Also known as the atrioventricular, or nonbranching bundle, it forms under normal conditions the
only conductive pathway between the atria and the
ventricles. It is a rapidly conducting tissue, with
propagation velocity an order of magnitude faster than
the working myocardium. As it traverses the
atrioventricular fibrous plane, the bundle is insulated
from the rest of the myocardium except of its proximal
connection with the AV node and distal bifurcation into
the left and right bundle branch.
The bundle branches
These form continuation of the His bundle,
sharing many of its characteristics – rapid conduction
speed, expression of gap junction protein connexin40
(without co-expression of connexin43) and fibrous
insulation from the working myocardium. This makes
these bundles well suited to act as electrical cables,
assuring rapid spread of the impulse through the
ventricles. There is a notable asymmetry between the left
and right bundle branch, the left being broad, in the
mouse composed of multiple parallel isolated strands,
while the right bundle being a narrow structure (Miquerol
et al. 2004). It is likely due to optimization of source:sink
ratio due to a marked asymmetry of the myocardial mass
between the left and right ventricle.
The Purkinje fibers
The Purkinje fibers are the terminal part of the
cardiac conduction system. They form a threedimensional subendocardial network originating from the
bundle branches and their main function is to distribute
the depolarization signal rapidly to the working
myocardium.
2014
Discovery of CCS
The historical sequence, in which various CCS
components were discovered, is in reverse order to the
functional sequence of activation. In 1839 the Czech
scientist Jan Evangeliste Purkinje described a pale
network of cells in the sheep heart, and noted their
microscopic characteristics, including the presence of one
or two nuclei and cross striations, which made him, after
some discussion, consider them a special form muscular
tissue (Eliska 2006). It took more than fifty years before a
Swiss physiologist His found the elusive connection
between the atrial and ventricular myocardium, first by a
series of cuts in the beating heart, then by detailed
histological examination of the region, where such cuts
led to atrioventricular block (Suma 2001). Over a decade
later, Tawara (1906) connected this bundle by describing
the atrioventricular node proximally and the bundle
branches distally. The last component discovered was the
sinoatrial node, described by Keith and Flack (1907) only
a year later.
Original description by Purkinje
The original 1839 description by Purkinje was a
part of a larger volume dealing with innervation of various
organs and published in Polish. He followed up six years
later in 1845 with a more detailed account in German, then
the universal language of morphologists (Eliska 2006).
There are few interesting points in this description that
pertain to the present review. First, while the original
species was sheep, he noted similar structures in the cow,
pig, and horse. On the other hand, he was unable to see his
cells in the human, dog, rabbit, or hare heart. This is an
important reminder of the dangers of expecting that a
functionally similar structure will look the same in
different species (Robb 1965). Second, already by then he
stated with certainty that these structures are not nervous
fibers, especially significant in the context of general focus
of his 1839 text on nervous tissue. Third, although he did
seriously consider (due to their appearance) that these
fibers could be cartilage, the presence of striations made
him to decide that most likely these tissues were muscular.
Nevertheless, later studies using various neuronal markers
re-ignited the issue (Gorza et al. 1988, 1994), and the final
word on myogenic nature of the CCS was provided using
genetic lineage tracing techniques – showing its common
origin with working cardiomyocytes (Gourdie 1995,
Cheng et al. 1999).
Purkinje Fibers in Vertebrates
S11
Differentiation of Purkinje fibers during
development
It has been shown in experimental studies in the
chick heart, that ventricular Purkinje fibers share
common origin with the surrounding ventricular
myocytes and terminally differentiate during fetal period
(Gourdie et al. 1995). In the avian model, it was
convincingly demonstrated that the differentiation
towards the conduction phenotype is time-sensitive, and
locally produced endothelin-1 was demonstrated to be a
key signaling molecule (Gourdie et al. 1998, Hyer et al.
1999, Takebayashi-Suzuki et al. 2000). The clonal
relationship between the working ventricular myocytes
and Purkinje myocytes observed in birds was confirmed
recently in the mammalian (mouse) model (Meilhac et al.
2003, Miquerol et al. 2010). However, transcription or
any other regulation governing this process in mammals
is still elusive. While it was long speculated that
ventricular trabeculae, forming during chamber
differentiation as a means to increase myocardial mass
prior to presence of coronary perfusion, form the
precursors of the Purkinje network (de Jong et al. 1992,
Sedmera et al. 2004), it is clear that not all the trabeculae
will turn into Purkinje fibers – in fact, the majority will
form trabeculae carneae, or “meaty” trabeculations
composed largely of working myocardium, that we find
on the inside of the ventricles. As noted above, our
knowledge of mechanisms governing these decisions is
woefully incomplete.
Subendocardial and intramural network
The Purkinje network is composed of two
components: the subendocardial fibers, which have
connection to the bundle branches and assure the apex-tobase activation of the ventricle, and a variably present
intramural component. While the first is invariably
reported, although with different morphology, from all
mammalian and avian hearts, the latter, presumably
accelerating
transmural
conduction,
is
only
morphologically distinguishable in some species –
in particular sheep (Ryu et al. 2009) (Fig. 1), cow
(Oosthoek et al. 1993), or pig (Fig. 2). In these animals,
connection between the subendocardial and intramural
network can be found at regular intervals (Fig. 6 in
Oosthoek et al. 1993), and the extent in cow is about
80 % of left ventricular wall thickness. On the other hand,
despite quite extensive searches, no intramural fibers
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Sedmera and Gourdie
have been located in the mouse or human heart (Fig. 3).
The presence of absence of the intramural component
does not seem to be related to heart size, as some small
animals – such as rats (Fazel et al. 1989, Thompson et al.
1990, Gourdie et al. 1992, 1993, Vuillemin et al. 1992)
or chicken (Gourdie et al. 1993) (Fig. 4) do have
intramural fibers – in the case of chicken clearly
associated with the coronary arteries.
Vol. 63
Functionally,
the
Purkinje
fibers
are
characterized by a unique ion channel expression and
faster conductivity in comparison to the working
ventricular myocardium. This creates a local
heterogeneity in conduction velocity and coupling, which
can lead to re-entry. Their role as foci of arrhythmias was
recently and extensively reviewed in (Boyden et al.
2010).
Fig. 1. Purkinje fibers in the sheep
heart. A. Actinin staining shows that
both the subendocardially located
Purkinje fibers and the working
cardiomyocytes have well organized
contractile
apparatus.
B.
Hematoxylin and Eosin staining
shows clearly that they are larger
than
the
working
ventricular
myocytes and their spatial and
fibrous isolation. C. Staining for
connexin43 shows very high density
of these gap junction proteins on
the entire cell membrane (compare
to neighboring working myocardium
where it is localized mostly at cell
ends). Wheat germ agglutinin
(WGA) staining highlights cell
boundaries and fibrous tissue. Scale
bars 25 µm.
2014
Purkinje Fibers in Vertebrates
S13
Fig. 2. Purkinje fibers in the pig heart. Connexin40 staining labels specifically both subendocardial (A) and intramural (B) Purkinje
fibers. C and D: similar morphology with Connxin40 staining preferentially localized to cell ends and distribution of Purkinje cells is
found also in the right ventricle. E and F: in contrast, Connexin43 staining is distributed in the entire cell surface.
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Sedmera and Gourdie
Vol. 63
Fig. 3. Purkinje fibers in the murine heart. Panels A and B show the transition of Connexin43-negative left bundle branches into
Purkinje fibers, which co-express both Connexin40 and 43. The tracts are spatially separated from the working myocardium and show a
thin fibrous sheath. Scale bars 10 µm. Panels C and D visualize the Purkinje network using Connexin40:GFP transgenic mouse. The
Purkinje network is formed by 1-3 cells thick strands of myocytes that are thinner but longer than the working myocytes. Panels
E and F compare the arrangement of the entire left ventricular network in mouse (from Miquerol et al. 2004, withe permission) and
human (Tawara 1906). In neither species were described any intramural Purkinje fibers.
2014
Purkinje Fibers in Vertebrates
S15
Fig. 4. Purkinje fibers in the
ED17 chick embryonic heart.
Similar to ungulates, there are
both subendocardial (A, B) as
well as intramural (C) Purkinje
cells; the later are located
periarterially. Coronary arteries
are labeled with asterisks.
Current state of the art future perspectives
As a closing paragraph, we would like to provide
some insight into some potentially fruitful areas of active
reseach of Purkinje fibers. First, new morphological
markers such as contactin (Pallante et al. 2010) allow us
better delineation of the entire network across species
(Ryu et al. 2009), and help to uncover signaling pathways
directing their differentiation from the working myocytes
in mammals such as notch signaling (Rentschler et al.
2012). This would be important to resolve the issue why
some closely related species do or do not possess the
intramural component (e.g. rat vs. mouse). Second little
explored question is the morphological and functional
imaging of contacts and conduction at the Purkinjemyocyte junction, that should be enabled by coupling of
these markers with high-speed, high-resolution mapping
techniques. Is there a gradual transition of phenotype
from clear PF to working myocyte, or is the boundary
sharply defined? The third question worthy of attention is
the origin and differentiation of Purkinje myocytes. Is the
commitment to the conduction lineage irreversible, and if
yes, at which point of development? What is the default
program of ventricular myocytes – conduction, or
working phenotype? Resolution of this particular
question would be important piece of information
necessary to production of larger pieces of implantable
tissue-engineered myocardium.
Conflict of Interest
There is no conflict of interest.
Acknowledgements
Author’s primary research is supported by the Ministry of
Education of the Czech Republic PRVOUK-P35/LF1/5,
and institutional RVO: 67985823 from the Academy of
Sciences of the Czech Republic. Current support from the
Grant Agency of the Czech Republic P302/11/1308 and
13-12412S is also gratefully acknowledged. RGG is
supported by NIH RO1 HL56728.
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