LCN5蛋白在雄性绵羊生殖器官及精子中的表达定位

doi:10.3864/j.issn.0578-1752.2022.07.015

Abstract

Abstract:

【Objective】The aim of this experiment was to investigate the expression pattern and localization of LCN5 in the testis of ram, the different segments of the epididymis and spermatozoa among them, providing clues to further explore the function of LCN5 in ram reproductive organs. 【Method】All the samples were from 6 healthy 9-month-old rams with similar weight (65.23±1.95 kg). Three rams were used to collect ejaculated sperm via artificial vagina while the others for collecting the testes, epididymis, and vas deferens as well as the regional spermatozoa within these male reproductive ducts using aseptic castration. The right testis, efferent ducts (ED), caput (E1-E2), corpus (E3-E5), cauda (E6-E7) and vas deferens (VS) samples were collected and placed in liquid nitrogen and 4% paraformaldehyde, respectively; the spermatozoa from ejaculated semen, the right testis, various segments of the epididymis and the vas deferens were separated and determined by the CASA system. Western Blot and immunohistochemistry were performed to detect the localization of LCN5 in the testis, the various segments of the epididymis, and vas deferens, respectively. Immunofluorescence was carried out to examine the dynamic localization of LCN5 in the spermatozoa from the testis, different segment of epididymis and vas deferens. 【Result】 (1) The CASA results showed that the proportion of grade A and C spermatozoa and the sperm kinematic parameters were highest, including VAP, VSL, VCL, ALH, BCF, WOB, LIN and STR from the ejaculated sperm and spermatozoa in caudal epididymis, compared with those from the other segments of male reproductive ducts. Except for that, there were the more grade A spermatozoa in VS, which showed better motility than others. However, the spermatozoa from testis were completely immotile. (2)The Western Blot results discovered that the highest expression of LCN5 was found in the E1 segment, next in segment E2 and E7, which were more than in corpus, testis and efferent ducts (P<0.05). The quantitative analysis showed the LCN5 expression levels in these tissues was ordered as E1>E2>E6>E3≈E5≈E4≈E7>VS>ED>T. (3) Immunohistochemistry found that there were slight positive signals of LCN5 in the testicular elongated spermatids, the principal and basal cells of the efferent ducts, while strong positive signals could be detected in the principal and basal cells, stereocilia of epididymal epithelium in the caput, corpus, and cauda. Granular signals of LCN5 were scattered around the sperm in the epididymal lumen. Besides, the weak LCN5 positive signals were found in the smooth muscle cells of the vas deferens. (4) Immunofluorescence results of LCN5 protein on the spermatozoa from different regions showed dynamic changes. Firstly, the local positive signals on the surface of sperm acrosome and midpiece of spermatozoa from testis and ED could be only found. With the spermatozoa transition from the testis to the epididymis, these signals began to expand and spread on the whole surface of sperm acrosome and the intensity of the signals on the sperm acrosome and midpiece reached the peak in the E1 segment. Secondly, the positive signals also existed in cytoplasmic droplets of the sperm flagellum. These signals also showed gradually loss with the removal of cytoplasmic droplets along the epidydimal ducts until E6 or E7. The expression pattern of LCN5 on the cauda and corpus on the sperm surface was similar to that of the caput. 【Conclusion】This research firstly revealed that LCN5 protein was regionally expressed in the ram reproductive system, highly expressed in the epididymal caput and gathered in the E6 segment. In the epididymal cauda, LCN5 was mainly expressed in the surface of acrosome on the spermatozoa from the caput, corpus, caudal of epididymis, as well as the cytoplasmic droplets of the sperm flagellum, which presented a dynamic distribution both on the surface of sperm and midpiece corresponding to the sperm quality and motility along the ram reproductive ducts, highlighting its potential function in sperm maturation. Taken together, LCN5 could play an essential role in spermatogenesis, maturation, storage, which provided the theoretical basis for its functional research and exploitation.

Key words: LCN5, different segments of the epididymis, sperm maturation, storage of sperm, ram

DONG FuCheng,MA ShuLi,SHI JuanJuan,ZHANG JunMei,CUI Yan,REN YouShe,ZHANG ChunXiang. Expression and Localization of LCN5 in Ram Reproductive Organs and Spermatozoa[J].Scientia Agricultura Sinica, 2022, 55(7): 1445-1457.

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References 60

[1]	JOHNSTON D S, JELINSKY S A, BANG H J, DICANDELORO P, WILSON E, KOPF G S, TURNER T T. The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biology of Reproduction, 2005, 73(3):404-413. doi: 10.1095/biolreprod.105.039719. doi: 10.1095/biolreprod.105.039719
[2]	DACHEUX J L, CASTELLA S, GATTI J L, DACHEUX F. Epididymal cell secretory activities and the role of proteins in boar sperm maturation. Theriogenology, 2005, 63(2):319-341. doi: 10.1016/j.theriogenology.2004.09.015. doi: 10.1016/j.theriogenology.2004.09.015
[3]	GONZÁLEZ-CADAVID V, MARTINS J A, MORENO F B, ANDRADE T S, SANTOS A C, MONTEIRO-MOREIRA A C, MOREIRA R A, MOURA A A. Seminal plasma proteins of adult boars and correlations with sperm parameters. Theriogenology, 2014, 82(5):697-707. doi: 10.1016/j.theriogenology.2014.05.024. doi: 10.1016/j.theriogenology.2014.05.024
[4]	WESTFALEWICZ B, DIETRICH M A, MOSTEK A, PARTYKA A, BIELAS W, NIŻAŃSKI W, CIERESZKO A. Identification and functional analysis of bull (Bos taurus) cauda epididymal fluid proteome. Journal of Dairy Science, 2017, 100(8):6707-6719. doi: 10.3168/jds.2016-12526. doi: 10.3168/jds.2016-12526
[5]	FLOWER D R, SKERRA A. The Lipocalin Protein Family. The Biochemical Journal, 1996, 318(Pt1):1-14. doi: 10.1042/bj3180001
[6]	ZHOU W, STANGER S J, ANDERSON A L, BERNSTEIN I R, DE IULIIS G N, MCCLUSKEY A, MCLAUGHLIN E A, DUN M D, NIXON B. Mechanisms of tethering and cargo transfer during epididymosome-sperm interactions. BMC Biology, 2019, 17(1):35. doi: 10.1186/s12915-019-0653-5. doi: 10.1186/s12915-019-0653-5
[7]	JELINSKY S A, TURNER T T, BANG H J, FINGER J N, SOLARZ M K, WILSON E, BROWN E L, KOPF G S, JOHNSTON D S. The rat epididymal transcriptome: comparison of segmental gene expression in the rat and mouse epididymides. Biology of Reproduction, 2007, 76(4):561-570. doi: 10.1095/biolreprod.106.057323. doi: 10.1095/biolreprod.106.057323
[8]	CORNWALL G A. New insights into epididymal biology and function. Human Reproduction Update, 2009, 15(2):213-227. doi: 10.1093/humupd/dmn055. doi: 10.1093/humupd/dmn055
[9]	DACHEUX J L, DACHEUX F. New insights into epididymal function in relation to sperm maturation. Reproduction (Cambridge, England), 2014, 147(2):R27-R42. doi: 10.1530/rep-13-0420. doi: 10.1530/rep-13-0420
[10]	NEWCOMER M E. Structure of the epididymal retinoic acid binding protein at 2.1 A resolution. Journal of Clinical Medicine, 1993, 1(1):7-18. doi: 10.1016/0969-2126(93)90004-z. doi: 10.1016/0969-2126(93)90004-z
[11]	SUZUKI K, YU X, CHAURAND P, ARAKI Y, LAREYRE J J, CAPRIOLI R M, MATUSIK R J, ORGEBIN-CRIST M C. Epididymis-specific promoter-driven gene targeting: A transcription factor which regulates epididymis-specific gene expression. Molecular of Cell Endocrinology, 2006, 250(1/2):184-189. doi: 10.1016/j.mce.2005.12.043
[12]	RANKIN T L, ONG D E, ORGEBIN-CRIST M C. The 18-kDa mouse epididymal protein (MEP 10) binds retinoic acid. Avian Diseases, 1992, 46(5):767-771. doi: 10.1095/biolreprod46.5.767. doi: 10.1095/biolreprod46.5.767
[13]	SUZUKI K, YU X, CHAURAND P, ARAKI Y, LAREYRE J J, CAPRIOLI R M, ORGEBIN-CRIST M C, MATUSIK R J. Epididymis-specific lipocalin promoters. Asian Journal of Andrology, 2007, 9(4):515-521. doi: 10.1111/j.1745-7262.2007.00300.x. doi: 10.1111/j.1745-7262.2007.00300.x
[14]	XIE S, XU J, MA W, LIU Q, HAN J, YAO G, HUANG X, ZHANG Y. Lcn5 promoter directs the region-specific expression of cre recombinase in caput epididymidis of transgenic mice. Biology of Reproduction, 2013, 88(3):71. doi: 10.1095/biolreprod.112.104034. doi: 10.1095/biolreprod.112.104034
[15]	ZWAIN I H, GRIMA J, CHENG C Y. Rat epididymal retinoic acid-binding protein: development of a radioimmunoassay, its tissue distribution, and its changes in selected androgen-dependent organs after orchiectomy. BJOG, 1992, 131(3):1511-1526. doi: 10.1210/endo.131.3.1324164. doi: 10.1210/endo.131.3.1324164
[16]	CHARKOFTAKI G, WANG Y, MCANDREWS M, BRUFORD E A, THOMPSON D C, VASILIOU V, NEBERT D W. Update on the human and mouse lipocalin (LCN) gene family, including evidence the mouse Mup cluster is result of an “evolutionary bloom”. Human Genomics, 2019, 13(1):11. doi: 10.1186/s40246-019-0191-9. doi: 10.1186/s40246-019-0191-9
[17]	ZHANG Y R, ZHAO Y Q, HUANG J F. Retinoid-binding proteins: similar protein architectures bind similar ligands via completely different ways. PLoS ONE, 2012, 7(5):e36772. doi: 10.1371/journal.pone.0036772. doi: 10.1371/journal.pone.0036772
[18]	HALL J C, TUBBS C E. Quantification of epididymal retinoic acid- binding protein (ERABP) mRNA in different anatomical regions of the adult rat epididymis. Biochemistry Molecular Biology Internation, 2010, 42(4):833-841.
[19]	WEBER A, ARGENTI L E, DE SOUZA A P B, SANTI L, BEYS-DA-SILVA W O, YATES J R, BUSTAMANTE-FILHO I C. Ready for the journey: A comparative proteome profiling of porcine cauda epididymal fluid and spermatozoa. Cell and Tissue Research, 2020, 379(2):389-405. doi: 10.1007/s00441-019-03080-0. doi: 10.1007/s00441-019-03080-0
[20]	MARTÍNEZ-FRESNEDA L, SYLVESTER M, SHAKERI F, BUNES A, DEL POZO J C, GARCÍA-VÁZQUEZ F A, NEUHOFF C, TESFAYE D, SCHELLANDER K, SANTIAGO-MORENO J. Differential proteome between ejaculate and epididymal sperm represents a key factor for sperm freezability in wild small ruminants. Cryobiology, 2021, 99:64-77. doi: 10.1016/j.cryobiol.2021.01.012. doi: 10.1016/j.cryobiol.2021.01.012
[21]	VAN TILBURG M, SOUSA S, LOBO M D P, MONTEIRO- AZEVEDO A C O M, AZEVEDO R A, ARAÚJO A A, MOURA A A. Mapping the major proteome of reproductive fluids and sperm membranes of rams: from the cauda epididymis to ejaculation. Theriogenology, 2021, 159:98-107. doi: 10.1016/j.theriogenology.2020.10.003. doi: 10.1016/j.theriogenology.2020.10.003
[22]	张春香, 张国林, 郭丽娜, 赵辉, 任有蛇. 基于高通量转录组测序的山羊睾丸和附睾头差异表达基因分析. 畜牧兽医学报, 2014, 45(3):391-401. doi: 10.11843/j.issn.0366-6964.2014.03.008. doi: 10.11843/j.issn.0366-6964.2014.03.008
	ZHANG C X, ZHANG G L, GUO L N, ZHAO H, REN Y S. Study on differentially expressed genes between caprine testis and epididymis caput based on transcriptomes with high-throughput RNA-seq technology. Acta Veterinaria et Zootechnica Sinica, 2014, 45(3):391-401. doi: 10.11843/j.issn.0366-6964.2014.03.008. (in Chinese) doi: 10.11843/j.issn.0366-6964.2014.03.008
[23]	任有蛇, 郭丽娜, 张春香, 张国林, 夏龙钢, 乔利英, 靳黎, 刘文忠. 山羊Lcn 5的表达特点及其在繁殖器官中定位. 畜牧兽医学报, 2015, 46(5):711-718. doi: 10.11843/j.issn.0366-6964.2015.05.005. doi: 10.11843/j.issn.0366-6964.2015.05.005
	REN Y S, GUO L N, ZHANG C X, ZHANG G L, XIA L G, QIAO L Y, JIN L, LIU W Z. Expression characteristics of Lcn 5 and its localization in reproduction organ of Bucks. Acta Veterinaria et Zootechnica Sinica, 2015, 46(5):711-718. doi: 10.11843/j.issn.0366- 6964.2015.05.005. (in Chinese) doi: 10.11843/j.issn.0366-6964.2015.05.005
[24]	董复成, 崔岩, 任有蛇, 张春香. 太行山羊附睾头细胞Lcn5免疫荧光定位. 中国草食动物科学, 2020(6):1-5.
	DONG F C, CUI Y, REN Y S, ZHANG C X. Localization of Lcn5 in epididymal caput cells in vitro of Taihang goat. China Herbivore Science, 2020(6):1-5. (in Chinese)
[25]	张彩霞. Lcn5对山羊精子获能和运动能力的影响[D]. 太谷:山西农业大学, 2016.
	ZHANG C X. Effects of Lcn5 on sperm capacitation and motility in goats. Taigu: Shanxi Agricultural Aniversity, 2016. (in Chinese)
[26]	MAJUMDER G C. Occurrence of a cyclic AMP-dependent protein kinase on the outer surface of rat epididymal spermatozoa. Journal of Diabetes Science and Technology, 1978, 83(3):829-836. doi: 10.1016/0006-291x(78)91469-9. doi: 10.1016/0006-291x(78)91469-9
[27]	AMANN R P, HAY S R, HAMMERSTEDT R H. Yield, characteristics, motility and cAMP content of sperm isolated from seven regions of ram epididymis. American Journal of Cancer Research, 1982, 27(3):723-733. doi: 10.1095/biolreprod27.3.723. doi: 10.1095/biolreprod27.3.723
[28]	MIRó J, LOBO V, QUINTERO-MORENO A, MEDRANO A, PE A A, RIGAU T. Sperm motility patterns and metabolism in Catalonian donkey semen. Theriogenology, 2005, 63(6):1706-1716. doi: 10.1016/j.theriogenology.2004.07.022
[29]	DORADO J, RODRíGUEZ I, HIDALGO M. Cryopreservation of goat spermatozoa: Comparison of two freezing extenders based on post-thaw sperm quality and fertility rates after artificial insemination. Theriogenology, 2007, 68(2):168-177. doi: 10.1016/j.theriogenology.2007.04.048
[30]	DEMYDA-PEYRáS S, BOTTREL M, ACHA D, ORTIZ I, DORADO J. Effect of cooling rate on sperm quality of cryopreserved Andalusian donkey spermatozoa. Animal Reproduction Science, 2018, 193.
[31]	TOSHIMORI K. Biology of spermatozoa maturation: an overview with an introduction to this issue. Microscopy Research and Technique, 2003, 61(1):1-6. doi: 10.1002/jemt.10311. doi: 10.1002/jemt.10311
[32]	YANAGIMACHI R, NODA Y D, FUJIMOTO M, NICOLSON G L. The distribution of negative surface charges on mammalian spermatozoa. Australian Prescriber, 1972, 135(4):497-519. doi: 10.1002/aja.1001350405. doi: 10.1002/aja.1001350405
[33]	ROBAIRE B, HERMO L. Efferent ducts, epididymis, and Vas deferens: Structure, functions, and their regulation. The Physiology of Reproduction, 1988: 999-1080.
[34]	TOHIDNEZHAD M, VAROGA D, PODSCHUN R, WRUCK C J, SEEKAMP A, BRANDENBURG L O, PUFE T, LIPPROSS S. Thrombocytes are effectors of the innate immune system releasing human beta defensin-3. Injury, 2011, 42(7):682-686. doi: 10.1016/j.injury.2010.12.010. doi: 10.1016/j.injury.2010.12.010
[35]	BELLEANNÉE C, LABAS V, TEIXEIRA-GOMES A P, GATTI J L, DACHEUX J L, DACHEUX F. Identification of luminal and secreted proteins in bull epididymis. Journal of Proteomics, 2011, 74(1):59-78. doi: 10.1016/j.jprot.2010.07.013. doi: 10.1016/j.jprot.2010.07.013
[36]	GUYONNET B, MAROT G, DACHEUX J L, MERCAT M J, SCHWOB S, JAFFRÉZIC F, GATTI J L. The adult boar testicular and epididymal transcriptomes. BMC Genomics, 2009, 10:369. doi: 10.1186/1471-2164-10-369. doi: 10.1186/1471-2164-10-369
[37]	TURNER T T, BOMGARDNER D, JACOBS J P. Sonic hedgehog pathway genes are expressed and transcribed in the adult mouse epididymis. Journal of Andrology, 2004, 25(4):514-522. doi: 10.1002/j.1939-4640.2004.tb02822.x. doi: 10.1002/j.1939-4640.2004.tb02822.x
[38]	JOHNSTON D S, JELINSKY S A, BANG H J, DICANDELORO P, WILSON E, KOPF G S, TURNER T T. The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biology of Reproduction, 2005, 73(3):404-413. doi: 10.1095/biolreprod.105.039719. doi: 10.1095/biolreprod.105.039719
[39]	JELINSKY S A, TURNER T T, BANG H J, FINGER J N, SOLARZ M K, WILSON E, BROWN E L, KOPF G S, JOHNSTON D S. The rat epididymal transcriptome: Comparison of segmental gene expression in the rat and mouse epididymides. Biology of Reproduction, 2007, 76(4):561-570. doi: 10.1095/biolreprod.106.057323. doi: 10.1095/biolreprod.106.057323
[40]	TURNER T T, JOHNSTON D S, FINGER J N, JELINSKY S A. Differential gene expression among the proximal segments of the rat epididymis is lost after efferent duct ligation. Biology of Reproduction, 2007, 77(1):165-171. doi: 10.1095/biolreprod.106.059493. doi: 10.1095/biolreprod.106.059493
[41]	赵翊林, 孟繁荣, 张春香, 任有蛇. 成年公山羊脂质运载蛋白8基因的组织表达谱分析. 中国草食动物科学, 2020, 40(1):1-4.
	ZHAO Y L, MENG F R, ZHANG C X, REN Y S. Expression profiles of Lcn8 in the organs and tissues of adult male goat. China Herbivore Science, 2020, 40(1):1-4. (in Chinese)
[42]	张昱, 孟繁荣, 任有蛇, 张春香. β防御素126在成年公山羊组织中的表达特性. 中国草食动物科学, 2019, 39(6):12-15. doi: 10.3969/j.issn.2095-3887.2019.06.003. doi: 10.3969/j.issn.2095-3887.2019.06.003
	ZHANG Y, MENG F R, REN Y S, ZHANG C X. Expression profile of β-defensin126 mRNA in various tissues of adult male goat. China Herbivore Science, 2019, 39(6):12-15. doi: 10.3969/j.issn.2095-3887.2019.06.003. (in Chinese) doi: 10.3969/j.issn.2095-3887.2019.06.003
[43]	杜海燕. 山羊附睾头β防御素家族表达特点及gBD 124功能分析[D]. 山西农业大学, 2018.
	DU H Y. The expression characteristics of β-defensin family from caprine epididymis and function analysis of gBD124. Taigu: Shanxi Agricultural Aniversity, 2018. (in Chinese)
[44]	MARCHESE S, PES D, SCALONI A, CARBONE V, PELOSI P. Lipocalins of boar salivary glands binding odours and pheromones. European Journal of Biochemistry, 1998, 252(3):563-568. doi: 10.1046/j.1432-1327.1998.2520563.x. doi: 10.1046/j.1432-1327.1998.2520563.x
[45]	CHAURAND P, FOUCHÉCOURT S, DAGUE B B, XU B J, REYZER M L, ORGEBIN-CRIST M C, CAPRIOLI R M. Profiling and imaging proteins in the mouse epididymis by imaging mass spectrometry. Proteomics, 2003, 3(11):2221-2239. doi: 10.1002/pmic.200300474. doi: 10.1002/pmic.200300474
[46]	TOLLNER T L, BEVINS C L, CHERR G N. Multifunctional glycoprotein DEFB126: A curious story of defensin-clad spermatozoa. Nature Reviews Urology, 2012, 9(7):365-375. doi: 10.1038/nrurol.2012.109. doi: 10.1038/nrurol.2012.109
[47]	YUDIN A I, TOLLNER T L, LI M W, TREECE C A, CHERR G N. ESP13.2, a member of the -Defensin family, Is a Macaque sperm surface-coating protein involved in the capacitation process. Biology of Reproduction, 2003, 69(4):1118-1128. doi: 10.1095/biolreprod.103.016105
[48]	PÉREZ-PATIÑO C, PARRILLA I, LI J, BARRANCO I, MARTÍNEZ E A, RODRIGUEZ-MARTÍNEZ H, ROCA J. The proteome of pig spermatozoa is remodeled during ejaculation. Molecular & Cellular Proteomics, 2019, 18(1):41-50. doi: 10.1074/mcp.ra118.000840. doi: 10.1074/mcp.ra118.000840
[49]	HAO S L, NI F D, YANG W X. The dynamics and regulation of chromatin remodeling during spermiogenesis. Gene, 2019, 706:201-210. doi: 10.1016/j.gene.2019.05.027. doi: 10.1016/j.gene.2019.05.027
[50]	MARTÍNEZ-FRESNEDA L, CASTAÑO C, BÓVEDA P, TESFAYE D, SCHELLANDER K, SANTIAGO-MORENO J, GARCÍA-VÁZQUEZ F A. Epididymal and ejaculated sperm differ on their response to the cryopreservation and capacitation processes in mouflon (Ovis musimon). Scientific Reports, 2019, 9(1):15659. doi: 10.1038/s41598-019-52057-0. doi: 10.1038/s41598-019-52057-0
[51]	LAREYRE J J, WINFREY V P, KASPER S, ONG D E, MATUSIK R J, OLSON G E, ORGEBIN-CRIST M C. Gene duplication gives rise to a new 17-kilodalton lipocalin that shows epididymal region-specific expression and testicular factor(s) regulation. Endocrinology, 2001, 142(3):1296-1308. doi: 10.1210/endo.142.3.8045. doi: 10.1210/endo.142.3.8045
[52]	COSTA S L, BOEKELHEIDE K, VANDERHYDEN B C, SETH R, MCBURNEY M W. Male infertility caused by epididymal dysfunction in transgenic mice expressing a dominant negative mutation of retinoic acid receptor alpha 1. Biology of Reproduction, 1997, 56(4):985-990. doi: 10.1095/biolreprod56.4.985. doi: 10.1095/biolreprod56.4.985
[53]	LEE Y C, LIAO C J, LI P T, TZENG W F, CHU S T. Mouse lipocalin as an enhancer of spermatozoa motility. Molecular Biology Reports, 2003, 30(3):165-172. doi: 10.1023/A:1024985024661. doi: 10.1023/A:1024985024661
[54]	BEZERRA M J B, ARRUDA-ALENCAR J M, MARTINS J A M, VIANA A G A, VIANA NETO A M, RÊGO J P A, OLIVEIRA R V, LOBO M, MOREIRA A C O, MOREIRA R A, MOURA A A. Major seminal plasma proteome of rabbits and associations with sperm quality. Theriogenology, 2019, 128:156-166. doi: 10.1016/j.theriogenology.2019.01.013. doi: 10.1016/j.theriogenology.2019.01.013
[55]	NIEDERREITHER K, SUBBARAYAN V, DOLLÉ P, CHAMBON P. Embryonic retinoic acid synthesis is essential for early mouse post- implantation development. Nature Genetics, 1999, 21(4):444-448. doi: 10.1038/7788. doi: 10.1038/7788
[56]	RAMOS A S. Morphologic variations along the length of the monkey vas deferens. Environmental Pollution. Journal of Reproductive Systems, 1979, 3(3):187-196. doi: 10.3109/01485017908988404. doi: 10.3109/01485017908988404
[57]	RIVA A, AüMULLER G. Epithelium of the Distal Portion of the Human Spermatic Pathway: Seminal Vesicle, Ampulla Ductus Deferentis, and Ejaculatory Duct. City: Ultrastructure of the Male Urogenital Glands, 1994.
[58]	ROMAS A S. Ultra-structural variations and phagocytosis of spermatozoa in the epithelium of the monkey vas deferens. Biology of Reproduction, 1979, 20:61A.
[59]	SNYDER E M, SMALL C L, BOMGARDNER D, XU B, EVANOFF R, GRISWOLD M D, HINTON B T. Gene expression in the efferent ducts, epididymis, and vas deferens during embryonic development of the mouse. Developmental Dynamics, 2010, 239(9):2479-2491. doi: 10.1002/dvdy.22378
[60]	SELDIN M M, KOPLEV S, RAJBHANDARI P, VERGNES L, ROSENBERG G M, MENG Y, PAN C, PHUONG T M N, GHARAKHANIAN R, CHE N, MÄKINEN S, SHIH D M, CIVELEK M, PARKS B W, KIM E D, NORHEIM F, CHELLA KRISHNAN K, HASIN-BRUMSHTEIN Y, MEHRABIAN M, LAAKSO M, DREVON C A, KOISTINEN H A, TONTONOZ P, REUE K, CANTOR R M, BJÖRKEGREN J L M, LUSIS A J. A strategy for discovery of endocrine interactions with application to whole-body metabolism. Cell Metabolism, 2018, 27(5):1138-1155. doi: 10.1016/j.cmet.2018.03.015. doi: 10.1016/j.cmet.2018.03.015

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组别 Group	A percent (%)	C percent (%)	D percent (%)	VAP (μm·s^-1)	VSL (μm·s^-1)	VCL (μm·s^-1)	ALH (μm)	BCF (Hz)	WOB (%)	LIN (%)	STR (%)
ED	0.86± 0.27d	8.24± 1.94c	90.91± 5.92a	14.05± 1.18e	5.97± 0.46e	25.27± 3.98c	1.04± 0.23c	0.97± 0.36d	46.71± 9.63e	21.64± 5.52d	40.80± 6.57c
E1	0.97± 0.45d	18.14± 2.78a	79.22± 9.98b	14.19± 2.6e	7.36± 1.04de	29.27± 4.85c	1.09± 0.36c	1.57± 0.59cd	59.07± 9.03bcde	33.25± 5.23bcd	54.14± 7.63b
E2	1.52± 0.63d	11.64± 3.1abc	86.88± 12.92ab	17.64± 2.86de	9.53± 1.27de	33.79± 3.82bc	2.08± 0.70b	2.56± 0.78bcd	57.58± 7.54cde	33.68± 5.95bcd	55.74± 6.86bcd
E3	2.12± 0.44d	10.27± 1.50abc	87.60± 4.69ab	19.33± 2.26de	10.10± 2.64de	40.31± 4.48bc	1.59± 0.46bc	2.32± 0.75bcd	51.61± 9.59d	34.12± 6.13bcd	53.40± 4.88b
E4	1.87± 0.32d	18.34± 3.13a	79.78± 7.06b	18.93± 2.70de	13.19± 2.50de	30.06± 8.9c	1.68± 0.54bc	3.19± 1.25bc	56.30± 7.18de	43.49± 8.54abc	62.53± 9.59ab
E5	6.22± 1.65d	10.01± 2.62abc	83.76± 7.38ab	26.13± 4.75d	15.60± 1.85d	46.89± 3.6b	2.09± 0.29b	4.58± 2.48b	55.27± 9.40de	32.64± 5.20cd	56.41± 5.91b
E6	64.55± 9.39b	17.72± 3.47ab	14.72± 5.98d	60.55± 8.33b	46.13± 6.46b	99.62± 9.86a	3.83± 0.26a	8.48± 1.10a	62.81± 6.18abc	45.65± 5.39a	72.26± 5.42a
E7	67.13± 3.10b	12.38± 1.99abc	20.48± 5.61d	72.18± 4.97a	54.16± 6.63ab	101.8± 9.86a	3.58± 0.19a	8.40± 0.98a	69.65± 7.42ab	52.03± 6.21a	74.28± 5.42a
VS	43.41± 7.99c	13.50± 2.40 abc	43.09± 9.15c	46.27± 3.76c	29.58± 5.20c	89.42± 11.67a	3.76± 0.54a	9.80± 1.65a	51.60± 5.03d	32.52± 5.16cd	62.27± 7.05ab
ES	76.79± 4.88a	8.60± 1.5bc	14.88± 5.35d	74.24± 9.91a	55.27± 7.38a	100.6± 15.37a	3.77± 0.35a	8.83± 1.06a	73.25± 6.07a	54.52± 6.44a	74.29± 4.18a

Expression and Localization of LCN5 in Ram Reproductive Organs and Spermatozoa

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