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|標題:||A study on the molecular mechanism of acute heat stress response in testes of male Taiwan country chickens
|關鍵字:||台灣土雞;睪丸;熱緊迫;mRNA;蛋白質;Taiwan country chicken;testis, heat stress;mRNA;protein||引用:||Abdul, K. M., K. Terada, T. Gotoh, R. M. Hafizur, and M. Mori. 2002. Characterization and functional analysis of a heart-enriched DnaJ/ Hsp40 homolog dj4/DjA4. Cell Stress Chaperones 7:156-166. Albino, D., N. Longoni, L. Curti, M. Mello-Grand, S. Pinton, G. Civenni, G. Thalmann, G. D'Ambrosio, M. Sarti, F. Sessa, G. Chiorino, C. V. Catapano, and G. M. Carbone. 2012. ESE3/EHF controls epithelial cell differentiation and its loss leads to prostate tumors with mesenchymal and stem-like features. Cancer Res. 72:2889-2900. Alberts, B., A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter. 2002. Cell Junctions, cell adhesion, and the extracellular matrix. Molecular Biology of the Cell 4th edition, Garland Science, New York, USA. Arrigo, A. P. 2001. Hsp27: novel regulator of intracellular redox state. IUMMB 52:303-307. Aumuller, G., and J. Seitz. 1988. 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生精作用是精原細胞行減數分裂與分化並最終形成成熟精子之一連串複雜過程。許多研究已指出急性熱緊迫會影響哺乳動物生精細胞之DNA完整性、改變轉錄與轉譯表現，造成細胞凋亡數增加以及受精後之囊胚發育；此外，急性熱緊迫亦會誘發氧化緊迫以及減弱血睪障壁之完整性，這些負面效應干擾生精作用、精子特性及胚胎發育，導致雄性哺乳動物之繁殖力下降；然而，目前尚缺乏急性熱緊迫對雄性禽類生精作用之分子層面探討，因此，本研究之目的即為闡明台灣土雞公雞睪丸對急性熱緊迫之分子反應。台灣土雞的耐熱性比白肉雞佳，L2品系台灣土雞與B品系台灣土雞有同樣遺傳的背景，然而經過世代選拔後L2品系台灣土雞的產蛋量高於B品系台灣土雞，試驗使用L2品系（蛋用土雞）和B品系（肉用土雞）台灣土雞公雞，試驗雞隻經38℃急性熱緊迫處理4小時後，給予0、2和6小時恢復期，試驗期間記錄雞隻體溫與呼吸速率，並於恢復期間第0、2和6小時採集睪丸進行生精細胞形態觀察、細胞凋亡分析、mRNA和蛋白質分析。試驗結果顯示，台灣土雞公雞處於38℃急性熱緊迫1小時後，其呼吸速率和體溫皆顯著上升，而熱緊迫結束後2小時則恢復至正常狀態。L2品系台灣土雞公雞於急性熱緊迫後並恢復2小時可發現其睪丸內形態異常精母細胞、Sertoli細胞與Leydig細胞（細胞核濃染或是多核的情形）顯著增加；熱緊迫後的2小時恢復期亦可觀察到大量的細胞凋亡，多數為精母細胞，精細胞和Sertoli細胞次之。微陣列分析發現L2品系台灣土雞公雞睪丸有309基因於熱緊迫後之mRNA表現量有變化，主要參與代謝、運輸、緊迫或刺激反應、蛋白質代謝、訊息傳遞和細胞聯繫等生物功能；二維差異蛋白質電泳分析結果顯示有119蛋白質點於熱緊迫前後有表現差異，身分鑑定後可確定此等差異表現蛋白質點為92個蛋白質，主要參與代謝、蛋白質折疊和蛋白質水解。B品系台灣土雞公雞於熱緊迫後其精母細胞和Sertoli細胞形態異常的數量顯著增加（P < 0.05）；精原細胞、精母細胞、精細胞與Sertoli細胞之細胞凋亡數量於恢復期2小時顯著增加。經急性熱緊迫後，B品系台灣土雞公雞睪丸有163基因表現受到影響，這些基因主要和代謝、轉錄、細胞結構、刺激反應和訊息傳遞有關；蛋白質方面可偵測到101個蛋白質點於熱緊迫之B品系台灣土雞公雞睪丸有差異表現，分屬於73個蛋白質，此等差異表現蛋白質主要參與代謝、蛋白質代謝、細胞結構、刺激反應、細胞凋亡、運送、恆定以及生精作用有關。蛋用品系土雞與肉用土雞在急性熱緊迫後其睪丸細胞皆有細胞凋亡以及不正常細胞出現，而肉用品系土雞睪丸細胞異常及凋亡的發生比蛋用品系者早，且mRNA和蛋白質表現皆有所差異，這些結果顯示雖然L2品系台灣土雞與B品系台灣土雞源自於同樣遺傳背景的雞種，然而經過世代選拔後L2品系台灣土雞的產蛋量高於B品系台灣土雞，蛋用和肉用品系土雞睪丸基因對於急性熱緊迫之轉錄與轉譯反應有所差異，這些基因表現之差異可能是因長期選拔產蛋量所導致的。由本研究結果可推測蛋用土雞經熱緊迫後其睪丸熱緊迫蛋白質基因與抗凋亡基因大量表現以減緩熱緊迫；與轉譯相關蛋白質表現量顯著減少，以防止未折疊蛋白質生成，同時抗氧化緊迫基因mRNA和蛋白質之表現量增加，以減緩氧化緊迫；然而蛋白質代謝相關蛋白質（例：CCT complex和蛋白酶次單元）的降低造成蛋白質摺疊和降解不足以清除未折疊蛋白質與折疊錯誤蛋白質，最終引起細胞凋亡以清除受損之睪丸細胞。熱緊迫蛋白90、熱緊迫蛋白70和熱緊迫蛋白5的mRNA與蛋白質於熱緊迫後之肉用土雞睪丸大量表現，熱緊迫蛋白5進一步引發不正常蛋白質摺疊反應(unfolded protein response)以清除未折疊蛋白質與折疊錯誤蛋白質，而抗細胞凋亡基因與蛋白質表現量下降則可能與熱緊迫後肉用土雞睪丸之細胞凋亡有關。
Spermatogenesis is a complex process where spermatogonia differentiate into spermatozoa. In mammals, acute heat stress influences DNA integrity, transcription, translation, reactive oxygen species production and thus causes cell death, impairing spermatogenesis, and impairing development of blastocyts. Previous studies have shown that the mechanisms of acute heat stress on male reproduction in mammals; however, there are few studies has been carried out in avian species. Taiwan country chickens (TCCs) show better thermotolerance than commercial broilers. L2 strain TCCs and B strain TCCs have same genetic background, but egg production rate of L2 strain TCCs is greater than B strain TCCs duo to generations of egg selection in L2 strain. The purpose of this study was to explore the molecular response to acute heat stress in the testes of TCCs. The L2 strain (layer-type) and B strain (broiler-type) TCCs were used. Roosters were subjected to acute heat stress of 38℃ and 55% RH for 4 h. The heat-stressed roosters were then allowed to recover at 25℃ for 0, 2, and 6 h. The respiratory rate and body temperature were recorded during the treatment and recovery. The testis samples were collected at 0, 2, and 6 h of recovery for cell morphology, apoptosis, mRNA, and protein analysis. The body temperature and respiratory rate significantly increased in 1 h during heat stress and recovered at 2 h of recovery. In L2 strain TCCs, the numbers of abnormal spermatocytes, Sertoli cells, and Leydig cells (with hyperchromatic nuclei or multinucleated giant nuclei) increased at 2 h after acute heat stress. The TUNEL assay showed that a significant increase of apoptotic cells was observed at 2 h of recovery in the testes of heat-stressed L2 strain TCCs. The TUNEL-positive cells included spermatocytes, spermatids, and Sertoli cells. Microarray analysis showed that the mRNA expression of 309 genes changed in the testes of L2 strain TCCs after acute heat stress. The differentially expressed genes majorly participated in biological processes of metabolism, transport, responses to stimuli/stress, protein metabolism, and signal transduction/cell communication. There were 119 protein spots differentially expressed in the testes of heat-stressed L2 strain TCCs. These protein spots belonged to 92 distinct proteins and most of them involved in metabolism, protein folding, and proteolysis. In B strain TCCs, the numbers of abnormal spermatocytes and Sertoli cells were also increased after acute heat stress. The apoptotic cells in the testes of heat-stressed B strain TCCs, including spermatogonia, spermatocytes, spermatids, and Sertoli cells, increased at 2 h of recovery. Result of microarray analysis showed that the mRNA expression of 163 genes altered in the testes of B strain TCCs after heat stress. The differentially expressed genes were related to metabolism, transcription, cellular organization, response to stimulus, and signal transduction. Furthermore, there were 101 protein spots differentially expressed in the testes of B strain TCCs after acute heat stress. The differentially expressed protein spots represented 73 proteins and mostly involved in metabolism, protein metabolism, cell organization, response to stimulus, apoptosis, transport, homeostasis, and spermatogenesis. The results of this study showed that the apoptotic and abnormal spematogenic cells significantly increased in both layer-type and broiler-type TCCs at recovery time after acute heat stress. However, the abnormality and apoptosis were observed earlier in testes of broiler-type chickens than those in layer-type chickens. Beside, the levels of mRNA and protein showed different expression pattern between the 2 strains of TCCs because generations of egg production selection in L2 strain TCCs. In conclusion, the molecular mechanism of response to acute heat stress in the testes of layer-type TCCs may include the upregulation of HSP family and anti-apoptotic genes to attenuate the heat stress, and the downregulation of proteins related to translation to prevent unfolded protein synthesis. The genes and proteins associated with antioxidant reaction may also be induced to attenuate heat-induced oxidative damage. However, decreased expression of protein metabolism-related proteins, including CCT complex and proteasome subunits, may cause insufficiency of protein folding and degradation and thus trigger apoptosis. In broiler type TCCs, the mRNA and protein expression of HSP90α, HSC70, and HSPA5 were induced in the testes after acute heat stress. The expression of HSPs may thus induce the unfolded protein response to prevent accumulation of unfolded and misfolded protein. Nevertheless, the downregulation of anti-apoptotic genes and proteins may result in apoptosis in the testes of heat-stressed broiler-type TCCs.
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