Testicular hyperthermia induces unfolded protein response signaling activation in spermatocyte

Biochemical and Biophysical Research Communications

Volumn 434, Issue 4, 2013, Pages 861-866

  Kim, Jung Hak ^a   Park, Sun Ji ^a   Kim, Tae Shin ^b   Park, Hyo Jin ^a   Park, Junghyung ^a   Kim, Bo Kyung ^a   Kim, Gyeong Ryul ^a   Kim, Jin Man ^c   Huang, Song Mei ^c   Chae, Jung Il ^d   Park, Choon Keun ^e   Lee, Dong Seok ^a  

^a Kyungpook National University   (South Korea)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Chungnam National University   (South Korea)

^d Chonbuk National University   (South Korea)

^e Kangwon National University   (South Korea)

Author keywords

Apoptosis; ER stress; Spermatocyte; Testicular hyperthermia; Unfolded Protein Response signaling pathway

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; CASPASE 3; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; MESSENGER RNA; STRESS ACTIVATED PROTEIN KINASE; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN; ENDOPLASMIC RETICULUM STRESS; ENZYME PHOSPHORYLATION; HYPERTHERMIA; IMMUNOHISTOCHEMISTRY; KIDNEY; LIVER; MALE; MOUSE; NICK END LABELING; NONHUMAN; PANCREAS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN UNFOLDING; SPERMATOCYTE; SPERMATOGENESIS; TESTIS; UNFOLDED PROTEIN RESPONSE; WESTERN BLOTTING;

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; ALTERNATIVE SPLICING; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; EUKARYOTIC INITIATION FACTOR-2; HOT TEMPERATURE; IMMUNOHISTOCHEMISTRY; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MICE; MICE, INBRED C57BL; PROTEIN PHOSPHATASE 1; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPERMATOCYTES; TESTIS; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE;

MAMMALIA;

EID: 84878177278     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.04.032     Document Type: Article

References (30)

1. Danno S., Itoh K., Matsuda T., Fujita J. Decreased expression of mouse Rbm3, a cold-shock protein, in Sertoli cells of cryptorchid testis. Am. J. Pathol. 2000, 156:1685-1692.
2. Mieusset R., Bujan L. Testicular heating and its possible contributions to male infertility: a review. Int. J. Androl. 1995, 18:169-184.
3. Kandeel F.R., Swerdloff R.S. Role of temperature in regulation of spermatogenesis and the use of heating as a method for contraception. Fertil. Steril. 1988, 49:1-23.
4. Kim I., Xu W., Reed J.C. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov. 2008, 7:1013-1030.
5. Liu Y., Sakamoto H., Adachi M., Zhao S., Ukai W., Hashimoto E., Hareyama M., Ishida T., Imai K., Shinomura Y. Heat stress activates ER stress signals which suppress the heat shock response, an effect occurring preferentially in the cortex in rats. Mol. Biol. Rep. 2012, 39:3987-3993.
6. Brewer J.W., Cleveland J.L., Hendershot L.M. A pathway distinct from the mammalian unfolded protein response regulates expression of endoplasmic reticulum chaperones in non-stressed cells. EMBO J. 1997, 16:7207-7216.
7. Schroder M., Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 2005, 74:739-789.
8. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8:519-529.
9. Lai E., Teodoro T., Volchuk A. Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology (Bethesda) 2007, 22:193-201.
10. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403:98-103.
11. Nakagawa T., Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 2000, 150:887-894.
12. Bertolotti A., Zhang Y., Hendershot L.M., Harding H.P., Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2000, 2:326-332.
13. Oyadomari S., Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 2004, 11:381-389.
14. Xu X., Gupta S., Hu W., McGrath B.C., Cavener D.R. Hyperthermia induces the ER stress pathway. PLoS One 2011, 6:e23740.
15. Setchell B.P. The Parkes Lecture. Heat and the testis. J. Reprod. Fertil. 1998, 114:179-194.
16. Szegezdi E., Logue S.E., Gorman A.M., Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006, 7:880-885.
17. Nakagawa T., Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 2000, 150:887-894.
18. Morishima N., Nakanishi K., Takenouchi H., Shibata T., Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J. Biol. Chem. 2002, 277:34287-34294.
19. Hand J.W., Walker H., Hornsey S., Field S.B. Effects of hyperthermia on the mouse testis and its response to X-rays, as assayed by weight loss. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 1979, 35:521-528.
20. Casady R., Myers R., Legates J. The Effect of Exposure to High Ambient Temperature on Spermatogenesis in the Dairy Bull1. J. Dairy Sci. 1953, 36:14-23.
21. Rockett J.C., Mapp F.L., Garges J.B., Luft J.C., Mori C., Dix D.J. Effects of hyperthermia on spermatogenesis, apoptosis, gene expression, and fertility in adult male mice. Biol. Reprod. 2001, 65:229-239.
22. Huo R., Zhu Y.F., Ma X., Lin M., Zhou Z.M., Sha J.H. Differential expression of glucose-regulated protein 78 during spermatogenesis. Cell Tissue Res. 2004, 316:359-367.
23. Lee A.S. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem. Sci. 2001, 26:504-510.
24. Lai E.D., Teodoro T., Volchuk A. Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology 2007, 22:193-201.
25. Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell. 2000, 6:1099-1108.
26. Park S.J., Kim T.S., Park C.K., Lee S.H., Kim J.M., Lee K.S., Lee I.K., Park J.W., Lawson M.A., Lee D.S. HCG-induced endoplasmic reticulum stress triggers apoptosis and reduces steroidogenic enzyme expression through activating transcription factor 6 in Leydig cells of the testis. J. Mol. Endocrinol. 2013, 50:151-166.
27. Yoshida H., Matsui T., Yamamoto A., Okada T., Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001, 107:881-891.
28. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287:664-666.
29. Fonseca S.G., Gromada J., Urano F. Endoplasmic reticulum stress and pancreatic beta-cell death. Trends Endocrinol. Metab. 2011, 22:266-274.
30. Szegezdi E., Logue S.E., Gorman A.M., Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006, 7:880-885.