Region-specific gene expression in the epididymis

Cell and Tissue Research

Volumn 349, Issue 3, 2012, Pages 717-731

  Belleannée, Clémence ^a   Thimon, Véronique ^b   Sullivan, Robert ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ DES ANTILLES   (France)

Author keywords

Epididymis; Gene expression; Lumicrine factors; Small RNAs; Sperm maturation

Indexed keywords

ADAM PROTEIN; ANDROGEN; ANDROGEN RECEPTOR; AQUAPORIN; BETA DEFENSIN; CYSTATIN; DIPEPTIDYL CARBOXYPEPTIDASE; EPIDERMAL GROWTH FACTOR; ESTROGEN; FIBROBLAST GROWTH FACTOR 2; GAMMA GLUTAMYLTRANSFERASE; LIPOCALIN; PROENKEPHALIN; RAF PROTEIN; RETINOIC ACID BINDING PROTEIN; RNA; STEROID HORMONE; TRANSCRIPTION FACTOR PEA3;

EPIDIDYMIS; FERTILIZATION; GENE CONTROL; GENE EXPRESSION; HUMAN; MALE; MALE FERTILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SPERMATOZOON MATURATION; SPERMATOZOON MOTILITY; TEMPERATURE;

ANIMALS; EPIDIDYMIS; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMANS; MALE; SPERM MATURATION;

EID: 84866349599     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-012-1381-0     Document Type: Review

References (169)

1. Abe K, Takano H (1989) Early degeneration of the epithelial cells in the initial segment of the epididymal duct in mice after efferent duct cutting. Arch Histol Cytol 52:299-310
2. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215-233
3. Beaulieu V, Da Silva N, Pastor-Soler N, Brown CR, Smith PJ, Brown D, Breton S (2005) Modulation of the actin cytoskeleton via gelsolin regulates vacuolar H+-ATPase recycling. J Biol Chem 280:8452-8463
4. Bedford JM (1978) Influence of abdominal temperature on epididymal function in the rat and rabbit. Am J Anat 152:509-521
5. Bedford JM (1991) Effects of elevated temperature on the epididymis and testis: experimental studies. Adv Exp Med Biol 286:19-32
6. Bedford JM, Yanagimachi R (1991) Epididymal storage at abdominal temperature reduces the time required for capacitation of hamster spermatozoa. J Reprod Fertil 91:403-410
7. Belleannée C, Da Silva N, Shum WW, Marsolais M, Laprade R, Brown D, Breton S (2009) Segmental expression of the bradykinin type 2 receptor in rat efferent ducts and epididymis and its role in the regulation of aquaporin 9. Biol Reprod 80:134-143
8. Belleannée C, Da Silva N, Shum WW, Brown D, Breton S (2010) Role of purinergic signaling pathways in V-ATPase recruitment to apical membrane of acidifying epididymal clear cells. Am J Physiol Cell Physiol 298:C817-C830
9. Belleannée C, Labas V, Teixeira-Gomes AP, Gatti JL, Dacheux JL, Dacheux F (2011a) Identification of luminal and secreted proteins in bull epididymis. J Proteomics 74:59-78
10. Belleannée C, Belghazi M, Labas V, Teixeira-Gomes AP, Gatti JL, Dacheux JL, Dacheux F (2011b) Purification and identification of sperm surface proteins and changes during epididymal maturation. Proteomics 11:1952-1964
11. Bilinska B, Wiszniewska B, Kosiniak-Kamysz K, Kotula-Balak M, Gancarczyk M, Hejmej A, Sadowska J, Marchlewicz M, Kolasa A, Wenda-Rozewicka L (2006) Hormonal status of male reproductive system: androgens and estrogens in the testis and epididymis. In vivo and in vitro approaches. Reprod Biol 6(Suppl 1):43-58
12. Breton S, Smith PJ, Lui B, Brown D (1996) Acidification of the male reproductive tract by a proton pumping (H+)-ATPase. Nat Med 2:470-472
13. Brooks DE (1976) Activity and androgenic control of glycolytic enzymes in the epididymis and epididymal spermatozoa of the rat. Biochem J 156:527-537
14. Brooks DE (1987) Androgen-regulated epididymal secretory proteins associated with post-testicular sperm development. Ann N YAcad Sci 513:179-194
15. Caballero J, Frenette G, Sullivan R (2010) Post testicular sperm maturational changes in the bull: important role of the epididymosomes and prostasomes. Vet Med Int 2011:757194
16. Chauvin TR, Griswold MD (2004) Androgen-regulated genes in the murine epididymis. Biol Reprod 71:560-569
17. Cheuk BL, Leung PS, Lo AC, Wong PY (2000) Androgen control of cyclooxygenase expression in the rat epididymis. Biol Reprod 63:775-780
18. Cheung KH, Leung GP, Leung MC, Shum WW, Zhou WL, Wong PY (2005) Cell-cell interaction underlies formation of fluid in the male reproductive tract of the rat. J Gen Physiol 125:443-454
19. Cornwall GA (2009) New insights into epididymal biology and function. Hum Reprod Update 15:213-227
20. Cornwall GA, Hsia N (1997) ADAM7, a member of the ADAM (a disintegrin and metalloprotease) gene family is specifically expressed in the mouse anterior pituitary and epididymis. Endocrinology 138:4262-4272
21. Cornwall GA, Orgebin-Crist MC, Hann SR (1992) The CRES gene: a unique testis-regulated gene related to the cystatin family is highly restricted in its expression to the proximal region of the mouse epididymis. Mol Endocrinol 6:1653-1664
22. Cornwall GA, Vreeburg JT, Holland MK, Orgebin-Crist MC (1990) Interactions of labeled epididymal secretory proteins with spermatozoa after injection of 35S-methionine in the mouse. Biol Reprod 43:121-129
23. Cotton LM, O'Bryan MK, Hinton BT (2008) Cellular signaling by fibroblast growth factors (FGFs) and their receptors (FGFRs) in male reproduction. Endocr Rev 29:193-216
24. Cyr DG, Robaire B, Hermo L (1995) Structure and turnover of junctional complexes between principal cells of the rat epididymis. Microsc Res Tech 30:54-66
25. Cyr DG, Gregory M, Dube E, Dufresne J, Chan PT, Hermo L (2007) Orchestration of occludins, claudins, catenins and cadherins as players involved in maintenance of the blood-epididymal barrier in animals and humans. Asian J Androl 9:463-475
26. Da Silva N, Pietrement C, Brown D, Breton S (2006) Segmental and cellular expression of aquaporins in the male excurrent duct. Biochim Biophys Acta 1758:1025-1033
27. Da Silva N, Cortez-Retamozo V, Reinecker HC, Wildgruber M, Hill E, Brown D, Swirski FK, Pittet MJ, Breton S (2011) A dense network of dendritic cells populates the murine epididymis. Reproduction 141:653-663
28. Dacheux JL, Paquignon M (1980) Relations between the fertilizing ability, motility and metabolism of epididymal spermatozoa. Reprod Nutr Dev 20:1085-1099
29. Dacheux JL, Gatti JL, Dacheux F (2003) Contribution of epididymal secretory proteins for spermatozoa maturation. Microsc Res Tech 61:7-17
30. Dacheux JL, Belghazi M, Lanson Y, Dacheux F (2006) Human epididymal secretome and proteome. Mol Cell Endocrinol 250:36-42
31. Dacheux JL, Belleannee C, Jones R, Labas V, Belghazi M, Guyonnet B, Druart X, Gatti JL, Dacheux F (2009) Mammalian epididymal proteome. Mol Cell Endocrinol 306:45-50
32. Danzo BJ (1995) The effects of a gonadotropin-releasing hormone antagonist on androgen-binding protein distribution and other parameters in the adult male rat. Endocrinology 136:4004-4011
33. Danzo BJ, Cooper TG, Orgebin-Crist MC (1977) Androgen binding protein (ABP) in fluids collected from the rete testis and cauda epididymidis of sexually mature and immature rabbits and observations on morphological changes in the epididymis following ligation of the ductuli efferentes. Biol Reprod 17:64-77
34. Desai KV, Kondaiah P (2000) Androgen ablation results in differential regulation of transforming growth factor-beta isoforms in rat male accessory sex organs and epididymis. J Mol Endocrinol 24:253-260
35. Dhar JD, Srivastava SR, Setty BS (1982) Flutamide as an androgen antagonist on epididymal function in the rat. Andrologia 14:55-61
36. Dubé E, Chan PT, Hermo L, Cyr DG (2007) Gene expression profiling and its relevance to the blood-epididymal barrier in the human epididymis. Biol Reprod 76:1034-1044
37. Eddy EM, Washburn TF, Bunch DO, Goulding EH, Gladen BC, Lubahn DB, Korach KS (1996) Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology 137:4796-4805
38. Ellerman DA, Cohen DJ, Da Ros VG, Morgenfeld MM, Busso D, Cuasnicu PS (2006) Sperm protein "DE" mediates gamete fusion through an evolutionarily conserved site of the CRISP family. Dev Biol 297:228-237
39. Esponda P, Bedford JM (1986) The influence of body temperature and castration on the protein composition of fluid in the rat cauda epididymidis. J Reprod Fertil 78:505-514
40. Ezer N, Robaire B (2003) Gene expression is differentially regulated in the epididymis after orchidectomy Endocrinology 144:975-988
41. Fan X, Robaire B (1998) Orchidectomy induces a wave of apoptotic cell death in the epididymis. Endocrinology 139:2128-2136
42. Fawcett DW, Hoffer AP (1979) Failure of exogenous androgen to prevent regression of the initial segments of the rat epididymis after efferent duct ligation or orchidectomy. Biol Reprod 20:162-181
43. Flickinger CJ, Bush LA, Howards SS, Herr JC (1997) Distribution of leukocytes in the epithelium and interstitium of four regions of the Lewis rat epididymis. Anat Rec 248:380-390
44. Foldesy RG, Bedford JM (1982) Biology of the scrotum. I. Temperature and androgen as determinants of the sperm storage capacity of the rat cauda epididymidis. Biol Reprod 26:673-682
45. Frenette G, Lessard C, Sullivan R (2004) Polyol pathway along the bovine epididymis. Mol Reprod Dev 69:448-456
46. Frenette G, Girouard J, Sullivan R (2006) Comparison between epididymosomes collected in the intraluminal compartment of the bovine caput and cauda epididymidis. Biol Reprod 75:885-890
47. Frenette G, Leclerc P, D'Amours O, Sullivan R (2009) Estrogen sulfotransferase is highly expressed along the bovine epididymis and is secreted into the intraluminal environment. J Androl 30:580-589
48. Garrett JE, Garrett SH, Douglass J (1990) A spermatozoa-associated factor regulates proenkephalin gene expression in the rat epididymis. Mol Endocrinol 4:108-118
49. Gebhardt K, Ellerbrock K, Pera I, Ivell R, Kirchhoff C (1999) Differential expression of novel abundant and highly regionalized mRNAs of the canine epididymis. J Reprod Fertil 116:391-402
50. Guyonnet B, Marot G, Dacheux JL, Mercat MJ, Schwob S, Jaffrezic F, Gatti JL (2009) The adult boar testicular and epididymal transcriptomes. BMC Genomics 10:369
51. Guyonnet B, Dacheux F, Dacheux JL, Gatti JL (2011) The epididymal transcriptome and proteome provide some insights into new epididymal regulations. J Androl 32:651-664
52. Hall SH, Yenugu S, Radhakrishnan Y, Avellar MC, Petrusz P, French FS (2007) Characterization and functions of beta defensins in the epididymis. Asian J Androl 9:453-462
53. Hamzeh M, Robaire B (2010) Identification of early response genes and pathway activated by androgens in the initial segment and caput regions of the regressed rat epididymis. Endocrinology 151:4504-4514
54. Hamzeh M, Robaire B (2011) Androgens activate mitogen-activated protein kinase via epidermal growth factor receptor/insulin-like growth factor 1 receptor in the mouse PC-1 cell line. J Endocrinol 209:55-64
55. He B, Kemppainen JA, Voegel JJ, Gronemeyer H, Wilson EM (1999) Activation function 2 in the human androgen receptor ligand binding domain mediates interdomain communication with the NH(2)-terminal domain. J Biol Chem 274:37219-37225
56. Heinlein CA, Chang C (2002) Androgen receptor (AR) coregulators: an overview. Endocr Rev 23:175-200
57. Henderson NA, Cooke GM, Robaire B (2004) Effects of PNU157706, a dual 5alpha-reductase inhibitor, on gene expression in the rat epididymis. J Endocrinol 181:245-261
58. Hermo L, Robaire B (2002) The epididymis: from molecules to clinical practice. Plenum Press, New York
59. Hermo L, Smith CE (2011) Thirsty business: cell, region, and membrane specificity of aquaporins in the testis, efferent ducts, and epididymis and factors regulating their expression. J Androl 32:565-575
60. Hermo L, Dworkin J, Oko R (1988) Role of epithelial clear cells of the rat epididymis in the disposal of the contents of cytoplasmic droplets detached from spermatozoa. Am J Anat 183:107-124
61. Hermo L, Xiaohong S, Morales CR (2000) Circulating and luminal testicular factors affect LRP-2 and Apo J expression in the epididymis following efferent duct ligation. J Androl 21:122-144
62. Hess RA (2000) Oestrogen in fluid transport in efferent ducts of the male reproductive tract. Rev Reprod 5:84-92
63. Hess RA, Bunick D, Bahr JM (1995) Sperm, a source of estrogen. Environ Health Perspect 103(Suppl 7):59-62
64. Hess RA, Fernandes SA, Gomes GR, Oliveira CA, Lazari MF, Porto CS (2011) Estrogen and its receptors in efferent ductules and epididymis. J Androl 32:600-613
65. Hess RA, Bunick D, Lee KH, Bahr J, Taylor JA, Korach KS, Lubahn DB (1997) A role for oestrogens in the male reproductive system. Nature 390:509-512
66. Hess RA, Zhou Q, Nie R, Oliveira C, Cho H, Nakaia M, Carnes K (2001) Estrogens and epididymal function. Reprod Fertil Dev 13:273-283
67. Hinton BT, Howards SS (1981) Permeability characteristics of the epithelium in the rat caput epididymidis. J Reprod Fertil 63:95-99
68. Hinton BT, Lan ZJ, Rudolph DB, Labus JC, Lye RJ (1998) Testicular regulation of epididymal gene expression. J Reprod Fertil Suppl 53:47-57
69. Holland MK, Vreeburg JT, Orgebin-Crist MC (1992) Testicular regulation of epididymal protein secretion. J Androl 13:266-273
70. Isnard-Bagnis C, Da Silva N, Beaulieu V, Yu AS, Brown D, Breton S (2003) Detection of ClC-3 and ClC-5 in epididymal epithelium: immunofluorescence and RT-PCR after LCM. Am J Physiol Cell Physiol 284:C220-C232
71. Janne OA, Moilanen AM, Poukka H, Rouleau N, Karvonen U, Kotaja N, Hakli M, Palvimo JJ (2000) Androgen-receptor-interacting nuclear proteins. Biochem Soc Trans 28:401-405
72. Jara M, Esponda P, Carballada R (2002) Abdominal temperature induces region-specific p53-independent apoptosis in the cauda epididymidis of the mouse. Biol Reprod 67:1189-1196
73. Jelinsky SA, Turner TT, Bang HJ, Finger JN, Solarz MK, Wilson E, Brown EL, Kopf GS, Johnston DS (2007) The rat epididymal transcriptome: comparison of segmental gene expression in the rat and mouse epididymides. Biol Reprod 76:561-570
74. Johnson AL, Howards SS (1976) Intratubular hydrostatic pressure in testis and epididymis before and after long-term vasectomy in the guinea pig. Biol Reprod 14:371-376
75. Johnston DS, Turner TT, Finger JN, Owtscharuk TL, Kopf GS, Jelinsky SA (2007) Identification of epididymis-specific transcripts in the mouse and rat by transcriptional profiling. Asian J Androl 9:522-527
76. Johnston DS, Jelinsky SA, Bang HJ, DiCandeloro P, Wilson E, Kopf GS, Turner TT (2005) The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol Reprod 73:404-413
77. Jones RC, Murdoch RN (1996) Regulation of the motility and metabolism of spermatozoa for storage in the epididymis of eutherian and marsupial mammals. Reprod Fertil Dev 8:553-568
78. Joseph A, Shur BD, Hess RA (2011) Estrogen, efferent ductules, and the epididymis. Biol Reprod 84:207-217
79. Kaunisto K, Fleming RE, Kneer J, Sly WS, Rajaniemi H (1999) Regional expression and androgen regulation of carbonic anhydrase IV and II in the adult rat epididymis. Biol Reprod 61:1521-1526
80. Kaunisto K, Parkkila S, Parkkila AK, Waheed A, Sly WS, Rajaniemi H (1995) Expression of carbonic anhydrase isoenzymes IV and II in rat epididymal duct. Biol Reprod 52:1350-1357
81. Kaur J, Ramakrishnan PR, Rajalakshmi M (1992) Effect of cyproter-one acetate on structure and function of rhesus monkey reproductive organs. Anat Rec 234:62-72
82. Kirby JL, Yang L, Labus JC, Hinton BT (2003) Characterization of fibroblast growth factor receptors expressed in principal cells in the initial segment of the rat epididymis. Biol Reprod 68:2314-2321
83. Kirchhoff C, Carballada R, Harms B, Kascheike I (2000) CD52 mRNA is modulated by androgens and temperature in epididymal cell cultures. Mol Reprod Dev 56:26-33
84. Kohane AC, Pineiro L, Blaquier JA (1983) Androgen-controlled synthesis of specific proteins in the rat epididymis. Endocrinology 112:1590-1596
85. Krull N, Ivell R, Osterhoff C, Kirchhoff C (1993) Region-specific variation of gene expression in the human epididymis as revealed by in situ hybridization with tissue-specific cDNAs. Mol Reprod Dev 34:16-24
86. Krutskikh A, De Gendt K, Sharp V, Verhoeven G, Poutanen M, Huhtaniemi I (2011) Targeted inactivation of the androgen receptor gene in murine proximal epididymis causes epithelial hypotrophy and obstructive azoospermia. Endocrinology 152:689-696
87. Lamb DJ, Weigel NL, Marcelli M (2001) Androgen receptors and their biology. Vitam Horm 62:199-230
88. Lan ZJ, Labus JC, Hinton BT (1998) Regulation of gamma-glutamyl transpeptidase catalytic activity and protein level in the initial segment of the rat epididymis by testicular factors: role of basic fibroblast growth factor. Biol Reprod 58:197-206
89. Lan ZJ, Palladino MA, Rudolph DB, Labus JC, Hinton BT (1997) Identification, expression, and regulation of the transcriptional factor polyomavirus enhancer activator 3, and its putative role in regulating the expression of gamma-glutamyl transpeptidase mRNA-IV in the rat epididymis. Biol Reprod 57:186-193
90. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, Lin C, Socci ND, Hermida L, Fulci V, Chiaretti S, Foa R, Schliwka J, Fuchs U, Novosel A, Muller RU, Schermer B, Bissels U, Inman J, Phan Q, Chien M, Weir DB, Choksi R, De Vita G, Frezzetti D, Trompeter HI, Hornung V, Teng G, Hartmann G, Palkovits M, Di Lauro R, Wernet P, Macino G, Rogler CE, Nagle JW, Ju J, Papavasiliou FN, Benzing T, Lichter P, Tam W, Brownstein MJ, Bosio A, Borkhardt A, Russo JJ, Sander C, Zavolan M, Tuschl T (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129:1401-1414
91. Legare C, Boudreau L, Thimon V, Thabet M, Sullivan R (2010) Vasectomy affects cysteine-rich secretory protein expression along the human epididymis and its association with ejaculated spermatozoa following vasectomy surgical reversal. J Androl 31:573-583
92. Leung GP, Cheung KH, Leung CT, Tsang MW, Wong PY (2004) Regulation of epididymal principal cell functions by basal cells: role of transient receptor potential (Trp) proteins and cyclooxygenase-1 (COX-1). Mol Cell Endocrinol 216:5-13
93. Leung PS, Wong TP, Lam SY, Chan HC, Wong PY (2000) Testicular hormonal regulation of the renin-angiotensin system in the rat epididymis. Life Sci 66:1317-1324
94. Li J, Al-Azzawi F (2009) Mechanism of androgen receptor action. Maturitas 63:142-148
95. Li J, Liu Y, Dong D, Zhang Z (2010) Evolution of an X-linked primate-specific micro RNA cluster. Mol Biol Evol 27:671-683
96. Liu Q, Hamil KG, Sivashanmugam P, Grossman G, Soundararajan R, Rao AJ, Richardson RT, Zhang YL, O'Rand MG, Petrusz P, French FS, Hall SH (2001) Primate epididymis-specific proteins: characterization of ESC42, a novel protein containing a trefoil-like motif in monkey and human. Endocrinology 142:4529-4539
97. Malovannaya A, Lanz RB, Jung SY, Bulynko Y, Le NT, Chan DW, Ding C, Shi Y, Yucer N, Krenciute G, Kim BJ, Li C, Chen R, Li W, Wang Y, O'Malley BW, Qin J (2011) Analysis of the human endogenous coregulator complexome. Cell 145:787-799
98. Metayer S, Dacheux F, Dacheux JL, Gatti JL (2002) Germinal angiotensin I-converting enzyme is totally shed from the rodent sperm membrane during epididymal maturation. Biol Reprod 67:1763-1767
99. Montfort L, Frenette G, Sullivan R (2002) Sperm-zona pellucida interaction involves a carbonyl reductase activity in the hamster. Mol Reprod Dev 61:113-119
100. Nashan D, Malorny U, Sorg C, Cooper T, Nieschlag E (1989) Immuno-competent cells in the murine epididymis. Int J Androl 12:85-94
101. Nicander L, Osman DI, Ploen L, Bugge HP, Kvisgaard KN (1983) Early effects of efferent ductule ligation on the proximal segment of the rat epididymis. Int J Androl 6:91-102
102. Nonogaki T, Noda Y, Narimoto K, Shiotani M, Mori T, Matsuda T, Yoshida O (1992) Localization of CuZn-superoxide dismutase in the human male genital organs. Hum Reprod 7:81-85
103. O'Hara L, Welsh M, Saunders PT, Smith LB (2011) Androgen receptor expression in the caput epididymal epithelium is essential for development of the initial segment and epididymal spermatozoa transit. Endocrinology 152:718-729
104. Oh J, Lee J, Woo JM, Choi E, Park I, Han C, Baek N, Lee H, do Kim H, Cho C (2006) Systematic identification and integrative analysis of novel genes expressed specifically or predominantly in mouse epididymis. BMC Genomics 7:314
105. Olson GE, Hinton BT (1985) Regional differences in luminal fluid polypeptides of the rat testis and epididymis revealed by two-dimensional gel electrophoresis. J Androl 6:20-34
106. Palladino MA, Hinton BT (1994) Expression of multiple gammaglutamyl transpeptidase messenger ribonucleic acid transcripts in the adult rat epididymis is differentially regulated by androgens and testicular factors in a region-specific manner. Endocrinology 135:1146-1156
107. Papaioannou MD, Nef S (2009) microRNAs in the testis: building up male fertility. J Androl 31:26-33
108. Papaioannou MD, Lagarrigue M, Vejnar CE, Rolland AD, Kuhne F, Aubry F, Schaad O, Fort A, Descombes P, Neerman-Arbez M, Guillou F, Zdobnov EM, Pineau C, Nef S (2010) Loss of Dicer in Sertoli cells has a major impact on the testicular proteome of mice. Mol Cell Proteomics 10:M900587MCP900200
109. Papaioannou MD, Pitetti JL, Ro S, Park C, Aubry F, Schaad O, Vejnar CE, Kuhne F, Descombes P, Zdobnov EM, McManus MT, Guillou F, Harfe BD, Yan W, Jegou B, Nef S (2009) Sertoli cell Dicer is essential for spermatogenesis in mice. Dev Biol 326:250-259
110. Pastor-Soler N, Bagnis C, Sabolic I, Tyszkowski R, McKee M, Van Hoek A, Breton S, Brown D (2001) Aquaporin 9 expression along the male reproductive tract. Biol Reprod 65:384-393
111. Pastor-Soler N, Beaulieu V, Litvin TN, Da Silva N, Chen Y, Brown D, Buck J, Levin LR, Breton S (2003) Bicarbonate-regulated adenylyl cyclase (sAC) is a sensor that regulates pH-dependent V-ATPase recycling. J Biol Chem 278:49523-49529
112. Pastor-Soler NM, Fisher JS, Sharpe R, Hill E, Van Hoek A, Brown D, Breton S (2010) Aquaporin 9 expression in the developing rat epididymis is modulated by steroid hormones. Reproduction 139:613-621
113. Patil AA, Cai Y, Sang Y, Blecha F, Zhang G (2005) Cross-species analysis of the mammalian beta-defensin gene family: presence of syntenic gene clusters and preferential expression in the male reproductive tract. Physiol Genomics 23:5-17
114. Pera I, Ivell R, Kirchhoff C (1994) Regional variation of specific gene expression in the dog epididymis as revealed by in-situ transcript hybridization. Int J Androl 17:324-330
115. Pera I, Ivell R, Kirchhoff C (1996) Body temperature (37C) specifically down-regulates the messenger ribonucleic acid for the major sperm surface antigen CD52 in epididymal cell culture. Endocrinology 137:4451-4459
116. Plasterk RH (2006) Micro RNAs in animal development. Cell 124:877-881
117. Rao J, Herr JC, Reddi PP, Wolkowicz MJ, Bush LA, Sherman NE, Black M, Flickinger CJ (2003) Cloning and characterization of a novel sperm-associated isoantigen (E-3) with defensin- and lectin-like motifs expressed in rat epididymis. Biol Reprod 68:290-301
118. Regalado F, Esponda P, Nieto A (1993) Temperature and androgens regulate the biosynthesis of secretory proteins from rabbit cauda epididymidis. Mol Reprod Dev 36:448-453
119. Reyes-Moreno C, Laflamme J, Frenette G, Sirard MA, Sullivan R (2008) Spermatozoa modulate epididymal cell proliferation and protein secretion in vitro. Mol Reprod Dev 75:512-520
120. Rigaudiere N, Ghyselinck NB, Faure J, Dufaure JP (1992) Regulation of the epididymal glutathione peroxidase-like protein in the mouse: dependence upon androgens and testicular factors. Mol Cell Endocrinol 89:67-77
121. Robaire B, Viger RS (1995) Regulation of epididymal epithelial cell functions. Biol Reprod 52:226-236
122. Roberts KP, Wamstad JA, Ensrud KM, Hamilton DW (2003) Inhibition of capacitation-associated tyrosine phosphorylation signaling in rat sperm by epididymal protein Crisp-1. Biol Reprod 69:572-581
123. Rodriguez CM, Kirby JL, Hinton BT (2001) Regulation of gene transcription in the epididymis. Reproduction 122:41-48
124. Romero Y, Meikar O, Papaioannou MD, Conne B, Grey C, Weier M, Pralong F, De Massy B, Kaessmann H, Vassalli JD, Kotaja N, Nef S (2011) Dicer1 depletion in male germ cells leads to infertility due to cumulative meiotic and spermiogenic defects. PLoS One 6: e25241
125. Rulli SB, Gonzalez-Calvar SI, Calandra RS (1997) Ornithine decarboxylase activity and polyamine levels in the epididymis of prepubertal rat after antiandrogen administration. Arch Androl 38:163-171
126. Ruz R, Andonian S, Hermo L (2004) Immunolocalization and regulation of cystic fibrosis transmembrane conductance regulator in the adult rat epididymis. J Androl 25:265-273
127. Schwaab V, Faure J, Dufaure JP, Drevet JR (1998) GPx3: the plasmatype glutathione peroxidase is expressed under androgenic control in the mouse epididymis and vas deferens. Mol Reprod Dev 51:362-372
128. Seiler P, Cooper TG, Yeung CH, Nieschlag E (1999) Regional variation in macrophage antigen expression by murine epididymal basal cells and their regulation by testicular factors. J Androl 20:738-746
129. Serre V, Robaire B (1999) Distribution of immune cells in the epididymis of the aging Brown Norway rat is segment-specific and related to the luminal content. Biol Reprod 61:705-714
130. Shum WW, Da Silva N, Brown D, Breton S (2009) Regulation of luminal acidification in the male reproductive tract via cell-cell crosstalk. J Exp Biol 212:1753-1761
131. Shum WW, Ruan YC, Da Silva N, Breton S (2011) Establishment of cell-cell cross talk in the epididymis: control of luminal acidification. J Androl 32:576-586
132. Shum WW, Da Silva N, McKee M, Smith PJ, Brown D, Breton S (2008) Transepithelial projections from basal cells are luminal sensors in pseudostratified epithelia. Cell 135:1108-1117
133. Sipila P, Krutskikh A, Pujianto DA, Poutanen M, Huhtaniemi I (2011) Regional expression of androgen receptor coregulators and androgen action in the mouse epididymis. J Androl 32:711-717
134. Sipila P, Pujianto DA, Shariatmadari R, Nikkila J, Lehtoranta M, Huhtaniemi IT, Poutanen M (2006) Differential endocrine regulation of genes enriched in initial segment and distal caput of the mouse epididymis as revealed by genome-wide expression profiling. Biol Reprod 75:240-251
135. Snyder EM, Small CL, Li Y, Griswold MD (2009) Regulation of gene expression by estrogen and testosterone in the proximal mouse reproductive tract. Biol Reprod 81:707-716
136. Sullivan R, Frenette G, Girouard J (2007) Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian J Androl 9:483-491
137. Sullivan R, Legare C, Thabet M, Thimon V (2011) Gene expression in the epididymis of normal and vasectomized men: what can we learn about human sperm maturation? J Androl 32:686-697
138. Sun EL, Flickinger CJ (1979) Development of cell types and of regional differences in the postnatal rat epididymis. Am J Anat 154:27-55
139. Sutovsky P, Moreno R, Ramalho-Santos J, Dominko T, Thompson WE, Schatten G (2001) A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J Cell Sci 114:1665-1675
140. Suzuki K, Yu X, Chaurand P, Araki Y, Lareyre JJ, Caprioli RM, Orgebin-Crist MC, Matusik RJ (2007) Epididymis-specific lipocalin promoters. Asian J Androl 9:515-521
141. Thimon V, Koukoui O, Calvo E, Sullivan R (2007) Region-specific gene expression profiling along the human epididymis. Mol Hum Reprod 13:691-704
142. Thimon V, Calvo E, Koukoui O, Legare C, Sullivan R (2008) Effects of vasectomy on gene expression profiling along the human epididymis. Biol Reprod 79:262-273
143. Tollner TL, Yudin AI, Treece CA, Overstreet JW, Cherr GN (2008) Macaque sperm coating protein DEFB126 facilitates sperm penetration of cervical mucus. Hum Reprod 23:2523-2534
144. Tollner TL, Venners SA, Hollox EJ, Yudin AI, Liu X, Tang G, Xing H, Kays RJ, Lau T, Overstreet JW, Xu X, Bevins CL, Cherr GN (2011) A common mutation in the defensin DEFB126 causes impaired sperm function and subfertility. Sci Transl Med 3:92ra65
145. Turmel P, Dufresne J, Hermo L, Smith CE, Penuela S, Laird DW, Cyr DG (2011) Characterization of pannexin1 and pannexin3 and their regulation by androgens in the male reproductive tract of the adult rat. Mol Reprod Dev 78:124-138
146. Turner TT (1995) On the epididymis and its role in the development of the fertile ejaculate. J Androl 16:292-298
147. Turner TT (2008) De Graaf's thread: the human epididymis. J Androl 29:237-250
148. Turner TT, Gleavy JL, Harris JM (1990) Fluid movement in the lumen of the rat epididymis: effect of vasectomy and subsequent vasovasostomy. J Androl 11:422-428
149. Turner TT, Bomgardner D, Jacobs JP, Nguyen QA (2003) Association of segmentation of the epididymal interstitium with segmented tubule function in rats and mice. Reproduction 125:871-878
150. Turner TT, Johnston DS, Finger JN, Jelinsky SA (2007) Differential gene expression among the proximal segments of the rat epididymis is lost after efferent duct ligation. Biol Reprod 77:165-171
151. Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R (2006) Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 20:515-524
152. Veeramachaneni DN, Amann RP, Palmer JS, Hinton BT (1990) Proteins in luminal fluid of the ram excurrent ducts: changes in composition and evidence for differential endocytosis. J Androl 11:140-154
153. Veri JP, Hermo L, Robaire B (1993) Immunocytochemical localization of the Yf subunit of glutathione S-transferase P shows regional variation in the staining of epithelial cells of the testis, efferent ducts, and epididymis of the male rat. J Androl 14:23-44
154. Vernet P, Aitken RJ, Drevet JR (2004) Antioxidant strategies in the epididymis. Mol Cell Endocrinol 216:31-39
155. Vernet P, Faure J, Dufaure JP, Drevet JR (1997) Tissue and developmental distribution, dependence upon testicular factors and attachment to spermatozoa of GPX5, a murine epididymis-specific glutathione peroxidase. Mol Reprod Dev 47:87-98
156. Vierula ME, Rankin TL, Orgebin-Crist MC (1995) Electron microscopic immunolocalization of the 18 and 29 kilodalton secretory proteins in the mouse epididymis: evidence for differential uptake by clear cells. Microsc Res Tech 30:24-36
157. Viger RS, Robaire B (1996) The mRNAs for the steroid 5 alpha-reductase isozymes, types 1 and 2, are differentially regulated in the rat epididymis. J Androl 17:27-34
158. Vreeburg JT, Holland MK, Cornwall GA, Rankin TL, Orgebin-Crist MC (1991) Secretion of epididymal proteins and their interactions with spermatozoa. Bull Assoc Anat (Nancy) 75:171-173
159. Winer MA, Wolgemuth DJ (1995) The segment-specific pattern of A-raf expression in the mouse epididymis is regulated by testicular factors. Endocrinology 136:2561-2572
160. Yeung CH, Weinbauer GF, Cooper TG (1999) Effect of acute androgen withdrawal by GnRH antagonist on epididymal sperm motility and morphology in the cynomolgus monkey. J Androl 20:72-79
161. Yudin AI, Treece CA, Tollner TL, Overstreet JW, Cherr GN (2005) The carbohydrate structure of DEFB126, the major component of the cynomolgus Macaque sperm plasma membrane glycocalyx. J Membr Biol 207:119-129
162. Zanich A, Pascall JC, Jones R (2003) Secreted epididymal glycoprotein 2D6 that binds to the sperm's plasma membrane is a member of the beta-defensin superfamily of pore-forming glycopeptides. Biol Reprod 69:1831-1842
163. Zhang J, Liu Q, Zhang W, Li J, Li Z, Tang Z, Li Y, Han C, Hall SH, Zhang Y (2010) Comparative profiling of genes and miRNAs expressed in the newborn, young adult, and aged human epididymides. Acta Biochim Biophys Sin (Shanghai) 42:145-153
164. Zhang JS, Liu Q, Li YM, Hall SH, French FS, Zhang YL (2006) Genome-wide profiling of segmental-regulated transcriptomes in human epididymis using oligo microarray. Mol Cell Endocrinol 250:169-177
165. Zhang YL, Zhang JS, Zhou YC, Zhao Y, Ni MJ (2011) Identification of microRNAs and application of RNA interference for gene targeting in vivo in the rat epididymis. J Androl 32:587-591
166. Zhao Y, Diao H, Ni Z, Hu S, Yu H, Zhang Y (2011) The epididymis-specific antimicrobial peptide beta-defensin 15 is required for sperm motility and male fertility in the rat (Rattus norvegicus). Cell Mol Life Sci 68:697-708
167. Zhou CX, Zhang YL, Xiao L, Zheng M, Leung KM, Chan MY, Lo PS, Tsang LL, Wong HY, Ho LS, Chung YW, Chan HC (2004) An epididymis-specific beta-defensin is important for the initiation of sperm maturation. Nat Cell Biol 6:458-464
168. Zhou Q, Clarke L, Nie R, Carnes K, Lai LW, Lien YH, Verkman A, Lubahn D, Fisher JS, Katzenellenbogen BS, Hess RA (2001) Estrogen action and male fertility: roles of the sodium/hydrogen exchanger-3 and fluid reabsorption in reproductive tract function. Proc Natl Acad Sci USA 98:14132-14137
169. Zwain IH, Grima J, Cheng CY (1992) Rat epididymal retinoic acid-binding protein: development of a radioimmunoassay, its tissue distribution, and its changes in selected androgen-dependent organs after orchiectomy. Endocrinology 131:1511-1526