Sains Malaysiana 48(10)(2019):
2249–2256
http://dx.doi.org/10.17576/jsm-2019-4810-21
Role of Different Salmonella enterica Serotypes in THP-1 Macrophage-Derived Foam Cell
Autophagy and Inflammatory Response
(Peranan Serotip Berbeza Salmonella enterica pada Tindak Balas Sel
Buih THP-1 Makrofaj Terbitan Autofagi dan Inflamasi)
MIN YI WONG1,
YUAN-HSI
TSENG1,
TSUNG-YU
HUANG2,
CHENG-HSUN
CHIU3,4,
CHYI-LIANG
CHEN3
& YAO-KUANG HUANG1*
1Division of Thoracic
and Cardiovascular Surgery, Chiayi Chang Gung Memorial Hospital,
Puzi City, Chiayi County 613, and College of Medicine, Chang
Gung University, Taoyuan City 333, Taiwan (R.O.C.)
2Division of Infectious
Diseases, Department of Internal Medicine, Chang Gung Memorial Hospital,
Chang Gung University College of Medicine, Taoyuan City 333, Taiwan
(R.O.C.)
3Molecular Infectious
Disease Research Center, Chang Gung Memorial Hospital, Taoyuan City
333, Taiwan (R.O.C.)
4Division of Pediatric
Infectious Diseases, Department of Pediatrics, Chang Gung Children’s
Hospital and Chang Gung University, Taoyuan City 333, Taiwan (R.O.C.)
Received: 22 January 2019/Accepted:
12 September 2019
ABSTRACT
Infected
aortic aneurysm is a rare but life-threatening condition. Intimal
injury, especially in arteries with atherosclerotic plaques, is
vulnerable to Salmonella
species. In this study, THP-1 macrophage-derived foam cells were
used to mimic the atherosclerotic plaques. We investigated the role
of different Salmonella serotype infections in foam cell
autophagy and inflammatory response. Three different serotypes of
Salmonella enterica-Typhimurium, Enteritidis,
and Choleraesuis - with or without
a virulence plasmid were used in this study. The foam cell model
was established and observed under confocal microscopy. The expression
of autophagy and inflammasome-related proteins after Salmonella infection
was detected by Western blotting, and the secretion of the proinflammatory
cytokines interleukin-1β and IL-18 was detected using ELISA.
The plasmid-bearing S. enteritidis
OU7130-
and plasmid-less S. choleraesuis OU7266-infected
foam cells both showed a lower expression of beclin-1 at 0.5 h post-infection
(hpi) and p62 at 2 hpi as well as
a higher expression of caspase-1 at 2 hpi
than other infected cells. Moreover, infection of OU7266 induced the highest IL-1β
and IL-18 production among the tested strains. In conclusion,
the virulence plasmid of S. enteritidis
OU7130
induced foam cell inflammatory responses, whereas that of S.
choleraesuis played an opposite role. The different serotype
of Salmonella may impact the infected aortic aneurysms through
regulating inflammatory balance of the macrophage and foam cells
in the atherosclerotic plaque.
Keywords:
Autophagy; foam cells; Salmonella serotypes; virulence
plasmid
ABSTRAK
Aneurisma aortik
yang terjangkit adalah
keadaan yang jarang berlaku namun boleh
mengancam nyawa.
Kecederaan intimal, terutamanya
dalam arteri dengan
plak atherosklerosis,
terdedah kepada spesies Salmonella. Dalam kajian ini,
sel buih yang
berasal daripada makrofaj THP-1 digunakan
untuk meniru
plak aterosklerotik. Kami mengkaji peranan jangkitan serotip Salmonella
yang berbeza dalam
autophagia sel buih dan tindak
balas keradangan.
Tiga serotip Salmonella enterica - Typhimurium, Enteritidis dan Choleraesuis-dengan atau
tanpa kevirulenan
plasmid digunakan dalam kajian ini. Model sel buih telah
ditubuhkan dan
diperhatikan di bawah mikroskopi konflik. Ekspresi protein yang berkaitan
dengan autofagia dan inflamasom selepas jangkitan Salmonella
dikesan oleh blot Western,
dan rembesan
sitokin proinflamasi interleukin-1β
dan IL-18
dikesan menggunakan
ELISA.
Pembekuan plasmid S. enteritidis
OU7130-
dan sel-sel
buih yang dioksida S. choleraesuis OU7266 kedua-duanya
menunjukkan ungkapan
beclin-1 yang lebih rendah
pada 0.5 jam selepas jangkitan (hpi) dan p62 pada 2 hpi serta ungkapan
kaspase-1 yang lebih tinggi
pada 2 hpi daripada sel yang dijangkiti yang lain. Tambahan pula,
jangkitan OU7266
mendorong kepada
pengeluaran tertinggi IL-1β
dan IL-18 dalam
kalangan strain yang diuji.
Sebagai kesimpulan,
plasmid virulensi S. enteritidis
OU7130
bertindak balas
dengan keradangan sel busa, sedangkan
S. choleraesuis memainkan
peranan yang bertentangan.
Serotip Salmonella yang berlainan
boleh memberi
kesan kepada aneurisma
aortik yang dijangkiti
melalui mengawal keseimbangan radang makrofaj dan buih
di plak aterosklerotik.
Kata kunci: Autofagi; kevirulenan
plasmid; sel buih; serotip
Salmonella
REFERENCES
Bobryshev, Y.V.
2006. Monocyte recruitment and foam cell formation in atherosclerosis.
Micron 37(3): 208-222.
Cohen, P.S., O’brien, T.F., Schoenbaum, S.C. & Medeiros, A.A. 1978. The risk of endothelial
infection in adults with Salmonella bacteremia. Annals
of Internal Medicine 89(6): 931-932.
De Meyer, G.R., Grootaert, M.O., Michiels, C.F., Kurdi, A., Schrijvers, D.M. & Martinet, W. 2015. Autophagy in vascular
disease. Circulation Research 116(3): 468-479.
Duewell, P.,
Kono, H., Rayner, K.J., Sirois,
C.M., Vladimer, G., Bauernfeind,
F.G., Abela, G. S., Franchi,
L., Nunez, G., Schnurr, M., Espevik,
T., Lien, E., Fitzgerald, K.A., Rock, K.L., Moore, K.J., Wright,
S.D., Hornung, V. & Latz, E. 2010.
NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature
464(7293): 1357-1361.
Fernández-Guerrero,
M.L., Aguado, J.M., Arribas,
A., Lumbreras, C. & de Gorgolas,
M. 2004. The spectrum of cardiovascular infections due to Salmonella
enterica. Medicine 83(2): 123-138.
Grimont, P.A.
& Weill, F.X. 2007. Antigenic formulae of the Salmonella
serovars. WHO Collaborating Centre for Reference and Research
on Salmonella 9: 1-166.
Guo, H.,
Callaway, J.B. & Ting, J.P. 2015. Inflammasomes:
Mechanism of action, role in disease, and therapeutics. Nature
Medicine 21(7): 677-687.
Huang, Y.K., Ko, P.J., Chen, C.L., Tsai,
F.C., Wu, C.H., Lin, P.J. & Chiu, C.H. 2014. Therapeutic opinion
on endovascular repair for mycotic aortic
aneurysm. Annals of Vascular Surgery 28(3): 579-589.
Jajere, S.M.
2019. A review of Salmonella enterica
with particular focus on the pathogenicity and virulence factors,
host specificity and antimicrobial resistance including multidrug
resistance. Veterinary World 12(4): 504-521.
Kuballa, P.,
Nolte, W.M., Castoreno, A.B. & Xavier,
R.J. 2012. Autophagy and the immune system. Annual Review of
Immunology 30: 611-646.
Liu, W., Yin, Y., Zhou, Z., He, M. & Dai, Y. 2014. OxLDL-induced IL-1 beta secretion promoting foam cells formation
was mainly via CD36 mediated ROS production leading to NLRP3
inflammasome activation. Inflammation Research 63(1):
33-43.
Liu, W.J., Ye, L., Huang, W.F., Guo, L.J.,
Xu, Z.G., Wu, H.L., Yang, C. & Liu, H.F. 2016. p62 links the
autophagy pathway and the ubiqutin-proteasome
system upon ubiquitinated protein degradation.
Cellular & Molecular Biology Letters 21: 29.
Meerkin, D.,
Yinnon, A.M., Munter, R.G., Shemesh, O., Hiller, N. & Abraham, A.S.J.C. 1995. Salmonella
mycotic aneurysm of the aortic arch:
Case report and review. Clinical Infectious Diseases 21(3):
523-528.
Mezal, E.H.,
Sabol, A., Khan, M.A., Ali, N., Stefanova,
R. & Khan, A.A. 2014. Isolation and molecular characterization
of Salmonella enterica serovar
Enteritidis from poultry house and clinical samples during
2010. Food Microbiology 38: 67-74.
Mizushima, N.
& Yoshimori, T. 2014. How to interpret
LC3 immunoblotting. Autophagy 3(6): 542-545.
Moore, K.J. & Tabas, I. 2011. Macrophages
in the pathogenesis of atherosclerosis. Cell 145(3): 341-355.
Oskoui, R.,
Davis, W.A. & Gomes, M.N.J.A. 1993. Salmonella aortitis:
A report of a successfully treated case with a comprehensive review
of the literature. Archives of Internal Medicine 153(4):
517-525.
Salzberger, L.A.,
Cavuoti, D. & Barnard, J. 2002. Fatal
Salmonella aortitis with mycotic
aneurysm rupture. The American Journal of Forensic Medicine and
Pathology 23(4): 382-385.
Schroder, K. & Tschopp, J. 2010. The
inflammasomes. Cell 140(6): 821-832.
Shao, B.Z., Han, B.Z., Zeng, Y.X., Su, D.F. & Liu, C. 2016. The
roles of macrophage autophagy in atherosclerosis. Acta
Pharmacologica Sinica
37(2): 150-156.
Silva, C., Puente, J.L. & Calva, E. 2017. Salmonella virulence
plasmid: Pathogenesis and ecology. Pathogens and Disease.
https://doi.org/10.1093/femspd/ftx070.
Usui, F.,
Shirasuna, K., Kimura, H., Tatsumi,
K., Kawashima, A., Karasawa, T., Hida,
S., Sagara, J., Taniguchi, S. & Takahashi,
M. 2012. Critical role of caspase-1 in vascular inflammation and
development of atherosclerosis in Western diet-fed apolipoprotein
E-deficient mice. Biochemical and Biophysical Research Communications
425(2): 162-168.
Wang, L., Yan, J., Niu, H., Huang, R. &
Wu, S. 2018. Autophagy and ubiquitination in Salmonella infection
and the related inflammatory responses. Frontiers in Cellular
and Infection Microbiology 8: 78.
Watanabe, Y. & Tanaka, M. 2011. p62/SQSTM1 in autophagic clearance of a non-ubiquitylated
substrate. Journal of Cell Science 124(16): 2692-2701.
Yu, X.H., Fu, Y.C., Zhang, D.W., Yin, K. & Tang, C.K. 2013. Foam
cells in atherosclerosis. Clinica
Chimica Acta 424: 245-252.
*Corresponding author; email: yaokuang@gmail.com
|