Received: 1 September 2017
|
|
Revised: 19 September 2017
Accepted: 24 September 2017
DOI: 10.1111/jfd.12746
ORIGINAL ARTICLE
Aeromonas caviae inhibits hepatic enzymes of the
phosphotransfer network in experimentally infected silver
catfish: Impairment on bioenergetics
M D Baldissera1
Veiga3
| C F Souza2
| C M Verdi1 | K L M dos Santos3 | M L Da
| M I U M da Rocha3 | R C V Santos1 | B S Vizzotto4 | B Baldisserotto2
1
Department of Microbiology and
Parasitology, Universidade Federal de Santa
Maria, Santa Maria, Brazil
Abstract
Several studies have been demonstrated that phosphotransfer network, through the
2
Department of Physiology and
Pharmacology, Universidade Federal de
Santa Maria, Santa Maria, Brazil
3
adenylate kinase (AK) and pyruvate kinase (PK) activities, allows for new perspectives leading to understanding of disease conditions associated with disturbances in
Department of Morphology, Universidade
Federal de Santa Maria (UFSM), Santa
Maria, Brazil
energy metabolism, metabolic monitoring and signalling. In this sense, the aim of
4
alters hepatic AK and PK activities of silver catfish Rhamdia quelen. Hepatic AK and
Laboratory of Molecular Biology, Centro
Universitario Franciscano, Santa Maria,
Brazil
this study was to evaluate whether experimental infection by Aeromonas caviae
PK activities decreased in infected animals compared to uninfected animals, as well
as the hepatic adenosine triphosphate (ATP) levels. Also, a severe hepatic damage
Correspondence
M D Baldissera, Department of Microbiology
and Parasitology, Universidade Federal de
Santa Maria, Santa Maria, Brazil.
Email: matheusd.biomed@yahoo.com.br
and
B Baldisserotto, Department of Physiology
and Pharmacology, Universidade Federal de
Santa Maria, Santa Maria, Brazil.
Email: bbaldisserotto@hotmail.com
was observed in the infected animals due to the presence of dilation and congestion
of vessels, degeneration of hepatocytes and loss of liver parenchyma architecture
and sinusoidal structure. Therefore, we have demonstrated, for the first time, that
experimental infection by A. caviae inhibits key enzymes linked to the communication between sites of ATP generation and ATP utilization. Moreover, the absence of
a reciprocal compensatory mechanism between these enzymes contributes directly
to hepatic damage and for a severe energetic imbalance, which may contribute to
disease pathophysiology.
KEYWORDS
adenosine triphosphate, adenylate kinase, bacterial disease, energy homeostasis, pyruvate
kinase
1 | INTRODUCTION
Aeromonas caviae is a mesophilic species of the genus Aeromonas
and occurs ubiquitously in aquatic environments (Lim, Ee, Yin, &
Aquaculture plays an important role in food production worldwide,
Chan, 2014), such as wastewater (Figueira, Vaz-Moreira, Silva, &
as the fish and fishery products represent a source of proteins and
Manaia, 2011), natural water such as rivers, lakes and estuaries
essential micronutrients important for human health (Ottinger,
(Pic~ao et al., 2013), aquacultures (Schmidt, Bruun, Dalsgaard, & Lar-
Clauss, & Kuenzer, 2016). However, the intensive rearing in aquacul-
sen, 2001) and urban drinking water (Carvalho, Martınez-Murcia,
ture in order to supply the fish demand causes environmental stress
Esteves, Correia, & Saavedra, 2012), and possesses the capacity to
to fish, which results in increasing susceptibility to bacterial diseases,
infect a vast number of hosts, such as humans and fishes (Janda &
caused by Aeromonas caviae, that are considered the major impedi-
Abbott, 2010). Recently, several studies have demonstrated the
ment to the development of aquaculture and are often the most sig-
increase in incidence of A. caviae infection in fish (Abd-El-Malek,
nificant cause of economic loss (Jiang et al., 2016).
2017; Hoel, Vadstein, & Jakobsen, 2017), which is characterized by
J Fish Dis. 2018;41:469–474.
wileyonlinelibrary.com/journal/jfd
© 2017 John Wiley & Sons Ltd
|
469
470
|
BALDISSERA
ET AL.
haemorrhagic septicaemia, hepatosplenomegaly, eye disease and
rio de Fisiologia de Peixes at the Universidade Federal de
Laborato
ulcerative lesions on the body surface (Thomas et al., 2013). This
Santa Maria, where they were maintained in 250-L fibreglass tanks
results in high mortality and economic losses in species such as rain-
with continuous aeration under controlled water variables: tempera-
bow trout (Oncorhynchus mykiss) (Zepeda-Velazquez et al., 2017),
ture 18–20°C (maintained with air conditioner), pH 7.1–7.3 and dis-
Nile tilapia (Oreochromis niloticus) (Meidong, Doolgindachbaporn,
solved oxygen levels 5.9–7.5 mg/L, in freshwater for 7 days.
Sakai, & Tongpim, 2017), tambaqui (Colossoma macropomum) (Mar-
Dissolved oxygen and temperature were measured with a YSI oxy-
ques et al., 2016), Indian catfish (Clarias batrachus) (Thomas et al.,
gen meter (model Y5512, OH, USA) and the pH with a DMPH-2 pH
nior
2013) and silver catfish (Rhamdia quelen) (Baldissera, Souza, Ju
meter (S~ao Paulo, Brazil). The total ammonia and non-ionized ammo-
et al., 2017). The liver is one of the organs most affected by
nia levels were determined according to Verdouw et al. (1978) and
A. caviae (Igbinosa, Igumbor, Aghdasi, Tom, & Okoh, 2012), but the
Colt (2001), respectively, as recently published in detail by Baldis-
effects of bacterial infection on hepatic tissue remain poorly under-
nior et al. (2017). The animals were fed to apparent
sera, Souza, Ju
stood. Thus, more studies are needed to understand the mechanism
satiation with commercial feed once a day. Any uneaten food, faeces
of disease pathophysiology, such as the involvement of enzymes
and other residues were removed daily 1 hr after feeding.
belonging to phosphotransfer network: adenylate kinase (AK) and
pyruvate kinase (PK), essential enzymes for the maintenance of
bioenergetics homeostasis.
2.2 | Inoculum confirmation and preparation
Delivery of metabolic signals to intracellular compartments plays
The pathogen was confirmed through colony morphology and physi-
a critical role in cellular homeostasis, as an efficient communication
ological characteristics, as well as using polymerase chain reaction
between cellular energetics and membrane metabolic sensors is
(PCR) by the analysis of the 16S rRNA gene of A. caviae using the
required to adequately regulate cell functions (Carrasco et al., 2001).
primers 50 TCG TTG GGT TGG GAT GTG 30 (forward) and 50 TGT
In this sense, cellular phosphotransfer reactions catalyse nucleotide
TAC CGC GGT GAA AGG 30 (reverse), according to the methodology
exchange facilitating communication between sites of adenosine
nior et al. (2017).
described in detail by Baldissera, Souza, Ju
triphosphate (ATP) generation and ATP utilization (Saupe, Spindler,
The bacterial isolate was grown on nutrient agar for use in this
Hopkins, Shen, & Ingwall, 2000). In this way, the AK catalyses the
experimental model. The suspension of A. caviae was washed twice
reversible transfer of the c-phosphate group from a phosphate donor
in sterile saline (NaCl 0.9%), and turbidity (OD600) was adjusted to
(normally ATP) to adenosine monophosphate (AMP), releasing two
0.9–1.1 (equivalent to 106 CFU/ml) and the suspension used for the
molecules of adenosine diphosphate (ADP) (ATP + AMP ↔ 2 ADP),
infection model.
that is, molecules involved in the processing of metabolic signals
associated with cellular energy utilization (Dzeja & Terzic, 1998).
Moreover, the PK is a key enzyme of the glycolysis pathway that
2.3 | Animals and experimental design
catalyses the irreversible phosphotransfer of phosphoenolpyruvate
Twenty adult silver catfish (118 21 g; 30 3 cm) were used as
(PEP) to ADP to form pyruvate and ATP (PEP + ADP ? ATP + Pyr)
the experimental model to assess the hepatic AK and PK activities,
(Wang et al., 2002), the main route that provides energy to proper
as well as the hepatic ATP levels. The animals were divided into two
tissue functioning. In this sense, Baldissera, Souza, Santos et al.
groups with 10 animals each: uninfected animals (negative control
(2017) demonstrated that inhibition of branchial AK and PK activities
group) and experimentally infected animals (positive control group)
in silver catfish experimentally infected with Pseudomonas aeruginosa
inoculated intramuscularly with 100 ll of a bacterial suspension con-
impairs the cellular energy homeostasis, contributing to disease
taining 55 9 106 viable cells of A. caviae, according to the protocol
pathogenesis. Thus, our hypothesis is that impairment of enzymes
nior et al. (2017). The negative
established by Baldissera, Souza, Ju
belonging to phosphotransfer network contributes to disease patho-
control group received the same dose of sterile saline through the
physiology of hepatic tissue.
same route.
Based on the fact that hepatic tissue plays a central role in sus-
The methodology used in the experiment was approved by the
taining energetic homeostasis by maintaining a constant supply of
Ethical and Animal Welfare Committee of the Universidade Federal
energy to fuel body tissues, the aim of this study was to evaluate
de Santa Maria under protocol number 074/2014.
whether experimental infection by A. caviae alters hepatic AK and
PK activities of silver catfish.
2 | MATERIAL AND METHODS
2.4 | Sample collection and tissue preparation
On day 4 post-infection (PI), all animals were anaesthetized with natural anaesthetic (Cymbopogon flexuosus essential oil) followed by
2.1 | Fish harvesting, maintenance of animals and
water quality variables
spinal cord section according to the Ethics Committee recommenda-
Healthy fish were collected for experimental purposes from a fish
ment of AK and PK activities and ATP levels, while the other portion
farm located in southern Brazil. The fish were transported to the
for histopathological analysis.
tions. Thereafter, the liver was removed and dissected in a glass dish
over ice and divided into two portions: one portion for the measure-
BALDISSERA
|
ET AL.
471
For the measurement of the enzymes of phosphoryl transfer
transverse sections of 4 lm thickness and stained with haematoxylin
network, the hepatic tissue was washed in SET buffer (0.32 M
and eosin (HE) for identification of the standard structures. The
sucrose, 1 mM EGTA, 10 mM Tris–HCl, pH 7.4) and homogenized
slides were analysed by two histopathologists in a double-blinded
(1:10 w/v) in the same SET buffer with a Potter-Elvehjem glass
manner using an optical microscope.
homogenizer. The homogenate was centrifuged at 800 g for 10 min
at 4°C, and part of the supernatant was used for the determination
of AK activity. The pellet was discarded and the rest of the super-
2.9 | Statistical analysis
natant was centrifuged at 10,000 g for 15 min at 4°C. The super-
Normality and homoscedasticity were analysed by the Shapiro–Wilk
natant of this second centrifugation, containing cytosol and other
and Levene tests, respectively. Significant differences between
cellular components, was collected for the determination of PK
groups were analysed and detected by two-tailed Student’s t-tests
activity.
for independent samples. The differences were considered to be
statistically significant at p < .05. The effect size (r2) was described
2.5 | Hepatic AK and PK activities
and scored as follows: ≤.1 (small), ≥.1 to ≤.3 (medium) and ≥.5
(large).
Hepatic AK activity was measured with a coupled enzyme assay with
hexokinase (HK) and glucose 6-phosphate dehydrogenase (G6PD),
according to Dzeja, Vitkevicius, Redfield, Burnettm, and Terzic
(1999). The reaction mixture contained 100 mM of KCl, 20 mM of
HEPES, 20 mM of glucose, 4 mM of MgCl2, 2 mM of NADP+, 1 mM
3 | RESULTS
3.1 | Hepatic AK and PK activities
of EDTA, 4.5 U/ml of HK, 2 U/ml of G6PD and 20 ll of hepatic
Adenylate kinase activity decreased by 62% [t(18) = 5.23; p = .0002;
homogenate. The reaction was initiated by the addition of 2 mM of
r2 = .78] (Figure 1) and PK activity decreased by 34% [t(18) = 3.11;
+
ADP and the reduction of NADP
was followed at 340 nm for
3 min in a spectrophotometer. The results were expressed in pmol
p = .001; r2 = .52] in the liver of animals infected with A. caviae
compared to the uninfected control group (Figure 2).
ATP formed/min/mg of protein.
Hepatic PK activity was assayed according to the protocol established by Leong, Lai, Lim, and Clark (1981). The incubation medium
3.2 | Hepatic ATP levels
consisted of 0.1 M Tris–HCl buffer, pH 7.5, 10 mM of MgCl2,
Hepatic ATP levels decreased by 50% [t(18) = 4.16; p = .005;
0.16 mM of NADH, 75 mM of KCl, 5.0 mM of ADP, 7 U of lactate
r2 = .61] in animals infected with A. caviae compared to the unin-
dehydrogenase, 0.1% of Triton X-100 and 10 ll of the mitochon-
fected control group (Figure 3).
dria-free supernatant in a final volume of 500 ll. After 10 min of
preincubation at 37°C, the reaction was started by the addition of
1 mM of PEP. The results were expressed as lmol pyruvate formed/
min/mg of protein.
3.3 | Hepatic histopathology
The uninfected animals did not show pathological alterations in
hepatic tissue (Figure 4a). Infected animals showed dilation and
2.6 | Hepatic ATP levels
The ATP levels in hepatic homogenates were measured by Firefly
congestion of vessels (asterisk), degeneration of hepatocytes and
loss of liver parenchyma architecture and sinusoidal structure (Figure 4b).
Luciferase ATP assay kit (Beyotime, China), according to the manufacturer’s protocol, based on luciferase requirements for ATP to produce light (emission maximum at 560 nm), as recently published in
detail by Wen et al. (2015). ATP levels are reported as pmol/mg of
protein.
2.7 | Protein determination
Hepatic protein content was determined by the method of Lowry,
Rosebrough, Farr, and Randall (1951), using bovine albumin serum as
standard.
2.8 | Hepatic histopathology
After euthanasia, fragments of the liver were fixed in Bouin solution,
processed by the usual routine method, embedded in paraffin for
F I G U R E 1 Hepatic adenylate kinase (AK) activity in silver catfish
experimentally infected with Aeromonas caviae compared to the
uninfected control group on day 4 post-infection (PI). Bars with
different letters are statistically different (p < .05; n = 10 per group)
using the two-tailed Student’s t test for independent samples
472
|
BALDISSERA
ET AL.
bioenergetics of infected animals, compromising the ATP synthesis
and the communication between sites of ATP generation and ATP
utilization.
The liver plays an essential role in the physiological regulation of
whole-body energy homeostasis, and the enzymes belonging to
phosphotransfer network are considered to be mainly involved in
the regulation of hepatic bioenergetics (Yegutkin, Wieringa, Robson,
& Jalkanen, 2012). Moreover, a network and circuit view of the
bioenergetics system allows for new perspectives leading to understanding of disease conditions associated with disturbances in
F I G U R E 2 Hepatic pyruvate kinase (PK) activity in silver catfish
experimentally infected with Aeromonas caviae compared to the
uninfected control group on day 4 post-infection (PI). Bars with
different letters are statistically different (p < .05; n = 10 per group)
using the two-tailed Student’s t test for independent samples
energy metabolism, metabolic monitoring and signalling (Dzeja &
Terzic, 2009). Thus, the evaluation of phosphotransfer network provides new information for understanding the alterations in hepatic
energetic metabolism during A. caviae infection. We observed that
AK and PK activities were inhibited by A. caviae, which results in
decreased availability of hepatic ATP and impairment of communication between sites of ATP generation and ATP utilization, in accordance with the results observed in the liver of experimentally
infected rats with the parasite Trypanosoma evansi (Baldissera et al.,
2015). Of particular interest, a recent study conducted by Baldissera,
Souza, Santos et al. (2017) demonstrated that inhibition of branchial
AK and PK activities by P. aeruginosa decreases the ATP availability,
impairs the energy supply of experimentally infected silver catfish
and contributes to disease pathogenesis, in accordance with the
results observed in the present study. In summary, the inhibition of
hepatic AK and PK activities leads to an impairment of energy metabolism during A. caviae infection, contributing to disease pathophysi-
F I G U R E 3 Hepatic adenosine triphosphate (ATP) levels in silver
catfish experimentally infected with Aeromonas caviae compared to
the uninfected control group on day 4 post-infection (PI). Bars with
different letters are statistically different (p < .05; n = 10 per group)
using the two-tailed Student’s t test for independent samples
ology.
It is important to emphasize that a reciprocal compensatory relationship exists between these enzymes in order to safeguard cellular
energy economy, which in turn contributes to an efficient intracellular energetic communication to maintain the balance between cellu-
4 | DISCUSSION
lar ATP consumption and production in an attempt to preserve the
energetic homeostasis (Janssen et al., 2000). Studies also revealed a
The present study is novel as it evaluates important alterations in
remarkable plasticity of the cellular phosphotransfer network system,
the hepatic phosphoryl transfer network of animals experimentally
where a deficiency in an individual enzyme is compensated through
infected by A. caviae. Our findings clearly show the inhibition of the
the remodelling of the whole energetics at enzymatic, architectural
hepatic AK and PK activities, indicating an imbalance of hepatic
and genomic levels (Dzeja, Terzic, & Wieringa, 2004); that is, a
(a)
(b)
F I G U R E 4 Hepatic histopathology of Rhamdia quelen experimentally infected by Aeromonas caviae. (a) Uninfected fish showed normal
hepatic architecture. (b) Fish infected by A. caviae showed dilation and congestion of vessels (asterisk), degeneration of hepatocytes and loss of
liver parenchyma architecture and sinusoidal structure. Bars = 100 lm
BALDISSERA
|
ET AL.
decrease in one enzyme may lead to an increase in the other.
Recently, a study conducted by Baldissera, Souza, Santos et al.
(2017) demonstrated a compensatory mechanism between the
cytosolic and mitochondrial creatine kinase (another important
enzyme belonging to phosphotransfer network) activities in kidney
tissue of experimentally infected silver catfish with A. caviae. However, this compensatory mechanism between AK and PK activities
was not observed in hepatic tissue of experimentally infected silver
catfish, which directly contributes to impairment of hepatic homeostasis. In this sense, the absence of energetic compensation
through the enzymes of phosphotransfer network may contribute to
the appearance of clinical signs of disease and hepatic lesions, as
evaluated in the histopathological analyses due to the presence of
dilation and congestion of vessels, degeneration of hepatocytes and
loss of liver parenchyma architecture and sinusoidal structure.
Based on these evidences, the inhibition of hepatic AK and PK
activities by A. caviae caused an impairment in hepatic energy homeostasis, decreasing the hepatic ATP availability. Moreover, the
absence of a reciprocal compensatory mechanism between these
enzymes directly contributes to hepatic damage and a severe energetic imbalance, which may contribute to disease pathophysiology.
ORCID
M D Baldissera
C F Souza
http://orcid.org/0000-0002-3280-8528
http://orcid.org/0000-0001-9978-0454
M L Da Veiga
B Baldisserotto
http://orcid.org/0000-0002-9303-3324
http://orcid.org/0000-0002-8770-0100
REFERENCES
Abd-El-Malek, A. M. (2017). Incidence and virulence characteristics of
Aeromonas spp. in fish. Veterinary World, 10, 34–37.
Baldissera, M. D., Rech, V. C., Grings, M., Kolling, J., Da Silva, A. S.,
Gressler, L. T., . . . Monteiro, S. G. (2015). Relationship between
pathological findings and enzymes of the energy metabolism in liver
of rats infected by Trypanosoma evansi. Parasitology International, 64,
547–552.
Baldissera, M. D., Souza, C. F., J
unior, G. B., Verdi, C. M., Moreira, K. L.
S., da Rocha, M. I. U. M., . . . Baldisserotto, B. (2017). Aeromonas
caviae alters the cytosolic and mitochondrial creatine kinase activities
in experimentally infected silver catfish: Impairment on renal bioenergetics. Microbial Pathogenesis, 110, 439–443.
Baldissera, M. D., Souza, C. F., Santos, R. C. V., Stefani, L. M., Moreira,
K. L. S., da Veiga, M. L., . . . Baldisserotto, B. (2017). Pseudomonas
aeruginosa strain PAO1 impairs enzymes of the phosphotransfer
network in the gills of Rhamdia quelen. Veterinary Microbiology,
201, 121–125.
Carrasco, A. J., Dzeja, P. P., Alekssev, A. E., Pucar, D., Zingman, L. V.,
Abraham, M. R., . . . Terzic, A. (2001). Adenylate kinase phosphotransfer communicates cellular energetic signals to ATP-sensitive potassium channels. Proceedings of the National Academy of Sciences, 98,
7623–7628.
Carvalho, M. J., Martınez-Murcia, A., Esteves, A. C., Correia, A., & Saavedra,
M. J. (2012). Phylogenetic diversity, antibiotic resistance and virulence
traits of Aeromonas spp. from untreated water for human consumption.
International Journal of Food Microbiology, 159, 230–239.
473
Colt, J. (2001). List of spreadsheets prepared as a complement. In G. A.
Wedemeyer (Ed.), Fish hatchery management, 2nd ed. Bethesda:
American Fisheries Society.
Dzeja, P. P., & Terzic, A. (1998). Phosphotransfer reactions in the regulation of ATP-sensitive K+ channels. FASEB Journal, 12, 523–529.
Dzeja, P., & Terzic, A. (2009). Adenylate kinase and AMP signaling networks: Metabolic monitoring, signal communication and body energy
sensing. International Journal of Molecular Sciences, 10, 1729–1772.
Dzeja, P. P., Terzic, A., & Wieringa, B. (2004). Phosphotransfer dynamics
in skeletal muscle from creatine kinase gene-deleted mice. Molecular
and Cellular Biochemistry, 256–257, 13–27.
Dzeja, P. P., Vitkevicius, K. T., Redfield, M. M., Burnettm, J. C., & Terzic,
A. (1999). Adenylate kinase-catalyzed phosphotransfer in the myocardium: Increased contribution in heart failure. Circulation Research, 84,
1137–1143.
Figueira, V., Vaz-Moreira, I., Silva, M., & Manaia, C. M. (2011). Diversity
and antibiotic resistance of Aeromonas spp. in drinking as waste treatment plants. Water Research, 45, 5599–5611.
Hoel, S., Vadstein, O., & Jakobsen, A. N. (2017). Species distribution and
prevalence of putative virulence factors in mesophilic Aeromonas spp.
isolated from fresh retail sushi. Frontiers in Microbiology, 8, e544234.
Igbinosa, I. H., Igumbor, E. U., Aghdasi, F., Tom, M., & Okoh, A. I. (2012).
Emerging Aeromonas species infections and their significance in public health. Scientific World Journal, 2012, e625023.
Janda, J. M., & Abbott, S. L. (2010). The genus Aeromonas: Taxonomy,
pathogenicity, and infection. Clinical Microbiology Reviews, 23, 35–73.
Janssen, E., Dzeja, P. P., Oerlemans, F., Simonetti, A. W., Heerschap, A.,
de Haan, A., . . . Terzic, A. (2000). Adenylate kinase 1 gene deletion
disrupts muscle energetic economy despite metabolic rearrangement.
EMBO Journal, 19, 6371–6381.
Jiang, Y., Feng, S., Zhang, S., Liu, H., Feng, J., Mu, X., . . . Xu, P. (2016).
Transcriptome signatures in common carp spleen in response to Aeromonas hydrophila infection. Fish and Shellfish Immunology, 57, 41–48.
Leong, S. F., Lai, J. K. F., Lim, L., & Clark, J. B. (1981). Energy-metabolism
in brain regions of adult and aging rats. Journal of Neurochemistry, 37,
1548–1556.
Lim, Y. L., Ee, R., Yin, W. F., & Chan, K. G. (2014). Quorum sensing activity of Aeromonas caviae strain YL12, a bacterium isolated from compost. Sensors, 14, 7026–7040.
Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, 193, 265–267.
jo, J.
Marques, D. S., Ferreira, D. A., Paiva, P. M., Napole~ao, T. H., Arau
M., Maciel Carvalho, E. V., & Coelho, L. C. (2016). Impact of stress on
Aeromonas diversity in tambaqui (Colossoma macropomum) and lectin
level change towards a bacterial challenge. Environmental Technology,
37, 3030–3035.
Meidong, R., Doolgindachbaporn, S., Sakai, K., & Tongpim, S. (2017). Isolation and selection of lactic acid bacteria from Thai indigenous fermented foods for use as probiotic in tilapia fish Oreochromis niloticus.
AACL Bioflux, 10, 455–463.
Ottinger, M., Clauss, K., & Kuenzer, C. (2016). Aquaculture: Relevance,
distribution, impacts and spatial assessments – A review. Ocean and
Coastal Management, 119, 244–266.
Pic~
ao, R. C., Cardoso, J. P., Campana, E. H., Nicoletti, A. G., Petrolini, F.
V., Assis, D. M., . . . Gales, A. C. (2013). The route of antimicrobial
resistance from the hospital effluent to the environment: Focus on
the occurrence of KPC-producing Aeromonas spp. and Enterobacteriaceae in sewage. Diagnostic Microbiology and Infectious Diseases, 76,
80–85.
Saupe, K. W., Spindler, M., Hopkins, J. C. A., Shen, W., & Ingwall, J. S.
(2000). Kinetic, thermodynamic, and developmental consequences of
deleting creatine kinase isoenzymes from the heart reaction kinetics
of the creatine kinase isoenzyme in the intact heart. Journal of Biological Chemistry, 275, 19742–19746.
474
|
Schmidt, A. S., Bruun, M. S., Dalsgaard, I., & Larsen, J. L. (2001). Incidence, distribution, and spread of tetracycline resistance determinants and integron-associated antibiotic resistance genes among
motile aeromonads from a fish farming environment. Applied and
Environmental Microbiology, 67, 5675–5682.
Thomas, J., Madan, N., Nambi, K. S. N., Majeed, S. A., Basha, A. N., &
Hameed, A. S. S. (2013). Studies on ulcerative disease caused by
Aeromonas caviae-like bacterium in Indian catfish, Clarias batrachus
(Linn). Aquaculture, 376–379, 146–150.
Verdouw H., Vanechteld C. J. A., & Deckkers E. M. J. (1978). Ammonia
determinations based on indophenol formation with sodium salicylate. Water Res. 12, 399–402.
Wang, H., Chu, W., Das, S. K., Ren, Q., Hasstedt, S. J., & Elbein, S. C.
(2002). Liver pyruvate kinase polymorphisms are associated with type
2 diabetes in Northern European Caucasians. Diabetes, 51, 2861–
2865.
Wen, F., Li, B., Huang, C., Wei, Z., Zhou, Y., Liu, J., & Zhang, H. (2015).
MiR-34a is involved in the decrease of ATP levels contents induced
by resistin through target on ATP55 in HepG2 cells. Biochemical
Genetics, 53, 301–309.
BALDISSERA
ET AL.
Yegutkin, G. G., Wieringa, B., Robson, S. C., & Jalkanen, S. (2012). Metabolism of circulating ADP in the bloodstream is mediated via integrated actions of soluble adenylate kinase-1 and NTPDase1/CD39
activities. FASEB Journal, 26, 3875–3883.
Zepeda-Velazquez, A. P., Vega-Sanchez, V., Ortega-Santana, C., RubioGodoy, M., de Oca-Mira, D. M., & Soriano-Vargas, E. (2017).
Pathogenicity of Mexican isolates of Aeromonas sp. in immersion
experimentally-infected rainbow trout (Oncorhynchus mykiss, Walbaum 1792). Acta Tropica, 169, 122–124.
How to cite this article: Baldissera MD, Souza CF, Verdi CM,
et al. Aeromonas caviae inhibits hepatic enzymes of the
phosphotransfer network in experimentally infected silver
catfish: Impairment on bioenergetics. J Fish Dis. 2018;41:469–
474. https://doi.org/10.1111/jfd.12746