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Expression of apoptosis-related factors in muscles infected with Trichinella spiralis

Published online by Cambridge University Press:  03 March 2004

T. BOONMARS ,
Z. WU ,
I. NAGANO  and
Y. TAKAHASHI
T. BOONMARS
Affiliation:
Department of Parasitology, Gifu University School of Medicine, Tsukasa 40, Gifu, 500-8705 Japan
Z. WU
Affiliation:
Department of Parasitology, Gifu University School of Medicine, Tsukasa 40, Gifu, 500-8705 Japan
I. NAGANO
Affiliation:
Department of Parasitology, Gifu University School of Medicine, Tsukasa 40, Gifu, 500-8705 Japan
Y. TAKAHASHI
Affiliation:
Department of Parasitology, Gifu University School of Medicine, Tsukasa 40, Gifu, 500-8705 Japan
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Abstract

We found that the expression of mitochondrial apoptosis related genes (Bcl-2 associated protein X, BAX; apoptotic protease activating factor 1, Apaf-1; Caspase 9 and serine/threonine protein kinase, PKB) is elevated in Trichinella spiralis-infected muscles during encapsulation. Micro-dissection of the capsule and subsequent reverse transcription polymerase chain reaction (RT-PCR) confirmed that the expressions of these genes are restricted to the nurse cell. Immunocytochemistry revealed that pro-apoptosis factor (BAX, Apaf-1 and Caspase 9) are predominantly expressed in the basophilic cytoplasm (infected muscle cell origin) and anti-apoptosis factor (PKB) in the eosinophilic cytoplasm (satellite cell origin) of the nurse cell. Electron microscopy revealed that the pre-existing mitochondria in the muscle cells became swollen and disappeared immediately after newborn larva invasion, but new mitochondria of smaller size appeared in the cytoplasm. Nuclear fragmentation and condensation were observed in basophilic cytoplasm which is known to die. Together, the results suggest that the infected muscle cells transform but die through the process of apoptosis which is triggered by factors from the newly formed mitochondria. The anti-apoptosis factor may help the eosinophilic cytoplasm with its survival to ensure nurse cell function.

Keywords

Trichinella spiralismitochondrial apoptosisBAXApaf-1Caspase 9PKB
Type
Research Article
Information
Parasitology , Volume 128 , Issue 3 , March 2004 , pp. 323 - 332
Copyright
2004 Cambridge University Press

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References

REFERENCES

BOONMARS, T., WU, Z., NAGANO, I., NAKADA, T. & TAKAHASHI, Y. (2004). Differences and similarities of nurse cells in cysts of Trichinella spiralis and T. pseudospiralis. Journal of Helminthology 10, 000–000.Google Scholar
CARDONE, M. H., ROY, N., STENNICKE, H. R., SALVESEN, G. S., FRANKE, T. F., STANBRIDGE, E., FRISCH, S. & REED, J. C. (1998). Regulation of cell death protease caspase-9 by phosphorylation. Science 282, 1318–1321.CrossRefGoogle Scholar
CHUANG, Y. H., CHUANG, W. L., HUANG, S. P. & HUANG, C. H. (2002). Over-expression of apoptosis-related proteins contributes to muscular damage in the obstructed ureter of the rat. British Journal of Urology International 89, 106–112.CrossRefGoogle Scholar
DATTA, S. R., DUDEK, H., TAO, X., MASTERS, S., FU, H., GOTOH, Y. & GREENBERG, M. E. (1997). Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91, 231–241.CrossRefGoogle Scholar
DEL PESO, L., GONZALEZ-GARCIA, M., PAGE, C., HERRERA, R. & NUNEZ, G. (1997). Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278, 687–689.CrossRefGoogle Scholar
DESAGHER, S. & MARTINOU, J. C. (2000). Mitochondria as the central control point of apoptosis. Trends in Cell Biology 10, 369–377.CrossRefGoogle Scholar
GOTTLIEB, R. A. (2000). Role of mitochondria in apoptosis. Critical Reviews in Eukaryotic Gene Expression 10, 231–239.Google Scholar
IKEZOE, K., NAKAGAWA, M., YAN, C., KIRA, J., GOTO, Y. & NONAKA, I. (2002). Apoptosis is suspended in muscle of mitochondrial encephalomyopathies. Acta Neuropathologica 103, 531–540.CrossRefGoogle Scholar
LAWLOR, M. A. & ALESSI, D. R. (2001). PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? Journal of Cell Science 114, 2903–2910.Google Scholar
LEE, M. J., LEE, J. S. & LEE, M. C. (2001). Apoptosis of skeletal muscle on steroid-induced myopathy in rats. Journal of Korean Medical Science 16, 467–474.CrossRefGoogle Scholar
MANCINI, M., ANDERSON, B. O., CALDWELL, E., SEDGHINASAB, M., PATY, P. B. & HOCKENBERY, D. M. (1997). Mitochondrial proliferation and paradoxical membrane depolarization during terminal differentiation and apoptosis in a human colon carcinoma cell line. The Journal of Cell Biology 138, 449–469.CrossRefGoogle Scholar
MATSUO, A., WU, Z., NAGANO, I. & TAKAHASHI, Y. (2000). Five types of nuclei present in the cyst of Trichinella spiralis. Parasitology 121, 203–210.CrossRefGoogle Scholar
MONICI, M. C., TOSCANO, A., GIRLANDA, P., AGUENNOUZ, M., MUSUMECI, O. & VITA, G. (1998). Apoptosis in metabolic myopathies. Neuroreport 9, 2431–2435.CrossRefGoogle Scholar
NICHOLSON, K. M. & ANDERSON, N. G. (2002). The protein kinase B/Akt signalling pathway in human malignancy. Cellular Signalling 14, 381–395.CrossRefGoogle Scholar
PARONE, P. A., JAMES, D. & MARTINOU, J. C. (2002). Mitochondria: regulating the inevitable. Biochimie 84, 105–111.CrossRefGoogle Scholar
SALEH, A., SRINIVASULA, S. M., ACHARYA, S., FISHEL, R. & ALNEMRI, E. S. (1999). Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. The Journal of Biological Chemistry 274, 17941–17945.CrossRefGoogle Scholar
SANDRI, M. & CARRARO, U. (1999). Apoptosis of skeletal muscles during development and disease. The International Journal of Biochemistry and Cell Biology 31, 1373–1390.CrossRefGoogle Scholar
STEEL, J. M. (1982). Trichinosis. In Handbook Series in Zoonoses: Section C: Parasitic Zoonoses (ed. Schultz, M. G.), pp. 293–329. CRC Press, Boca Raton, Florida, USA.
TAKAHASHI, Y., UNO, T., FURUKI, J., YAMADA, S. & ARAKI, T. (1988). The morphology of Trichinella spiralis: ultrastructural study of mid- and hindgut of the muscle larvae. Parasitology Research 75, 19–27.CrossRefGoogle Scholar
TEWS, D. S. (2002). Apoptosis and muscle fibre loss in neuromuscular disorders. Neuromuscular Disorders 12, 613–622.CrossRefGoogle Scholar
TSUJIMOTO, Y. & SHIMIZU, S. (2000). VDAC regulation by the Bcl-2 family of proteins. Cell Death and Differentiation 7, 1174–1181.CrossRefGoogle Scholar
UMAKI, Y., MITSUI, T., ENDO, I., AKAIKE, M. & MATSUMOTO, T. (2002). Apoptosis-related changes in skeletal muscles of patients with mitochondrial diseases. Acta Neuropathologica 103, 163–170.Google Scholar
WANG, S. J., OMORI, N., LI, F., JIN, G., ZHANG, W. R., HAMAKAWA, Y., SATO, K., NAGANO, I., SHOJI, M. & ABE, K. (2002). Potentiation of Akt and suppression of caspase-9 activations by electroacupuncture after transient middle cerebral artery occlusion in rats. Neuroscience Letters 331, 115–118.CrossRefGoogle Scholar
WU, Z., MASUO, A., NAKADA, T., NAGANO, I. & TAKAHASHI, Y. (2001). Different response of satellite cells in the kinetics of myogenic regulatory factors and ultrastructural pathology after Trichinella spiralis and T. pseudospiralis infection. Parasitology 123, 85–94.CrossRefGoogle Scholar
YAMAGUCHI, H. & WANG, H. G. (2001). The protein kinase PKB/Akt regulates cell survival and apoptosis by inhibiting Bax conformational change. Oncogene 20, 7779–7786.CrossRefGoogle Scholar