Isoforms of angiotensin I-converting enzyme in the development and differentiation of human testis and epididymis

Andrologia

Volumn 35, Issue 1, 2003, Pages 32-43

  Pauls, K ^a   Metzger, R ^b   Steger, K ^c   Klonisch, T ^d   Danilov, S ^e   Franke, Folker E ^c  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

ACE; CD143; Epididymis; Germ cells; Immunohistochemistry; in situ hybridization; Testis

Indexed keywords

DIPEPTIDYL CARBOXYPEPTIDASE; MONOCLONAL ANTIBODY; RNA;

CELL DIFFERENTIATION; CELL MATURATION; CELLULAR DISTRIBUTION; CONFERENCE PAPER; CONTROLLED STUDY; ENDOTHELIUM CELL; EPIDIDYMIS; EPITHELIUM CELL; FETUS (ANATOMY); GERM CELL; HUMAN; HUMAN TISSUE; LEYDIG CELL; MALE; MALE FERTILITY; MALE GENITAL SYSTEM; NECK; ONTOGENY; SEMINIFEROUS TUBULE; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOZOON; TESTIS; VAS DEFERENS;

AGING; ANTIBODIES, MONOCLONAL; CELL DIFFERENTIATION; EPIDIDYMIS; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; ISOENZYMES; LEYDIG CELLS; MALE; PEPTIDYL-DIPEPTIDASE A; RNA, MESSENGER; SEMINIFEROUS TUBULES; SPERMATIDS; SPERMATOGENESIS; SPERMATOZOA; TESTIS; TISSUE DISTRIBUTION; VAS DEFERENS;

EID: 0037325195     PISSN: 03034569     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1439-0272.2003.00535.x     Document Type: Conference Paper

References (81)

1. Atanassova N, Kancheva L, Somlev B (1998) Bradykinin stimulates prepubertal germ cell proliferation in vitro. Immunopharmacology 40:173-178.
2. Berg T, Sulner J, Lai CY, Soffer RL (1986) Immunohistochemical localization of two angiotensin I-converting isoenzymes in the reproductive tract of the male rabbit. J Histochem Cytochem 34:753-760.
3. Bergmann M, Kliesch S (1994) The distribution pattern of cytokeratin and vimentin immunoreactivity in testicular biopsies of infertile men. Anat Embryol 190:515-520.
4. Borkowski JA, Ramson RW, Seabrook GR, Trumbauer M, Chen H, Hill RG, Strader CD, Hess JF (1995) Targeted disruption of a B2 bradykinin receptor gene in mice eliminates bradykinin action in smooth muscle and neurons. J Biol Chem 270:13706-13710.
5. Brentjens JR, Matsuo S, Andres GA, Caldwell PR, Zamboni L (1986) Gametes contain angiotensin converting enzyme (kininase II). Experientia 42:399-402.
6. Bruneval P, Hinglais N, Alhenc-Gelas F, Tricottet V, Corvol P, Menard J, Camilleri JP, Bariety J (1986) Angiotensin I converting enzyme in human intestine and kidney: ultrastructural immunohistochemical localization. Histochemistry 85:73-80.
7. Corvol P, Michaud A, Soubrier F, Williams TA (1995) Recent advances in knowledge of the structure and function of the angiotensin I-converting enzyme. J Hypertens 13:S3-S10.
8. Danilov S, Jaspard E, Churakova T, Towbin H, Savoie F, Wei L, Alhenc-Gelas F (1994) Structure-function analysis of angiotensin I-converting enzyme using monoclonal antibodies: selective inhibition of the amino-terminal active site. J Biol Chem 269:26806-26814.
9. Danilov SM, Franke FE, Erdös EG (1997) CD143 (angiotensin-converting enzyme) workshop panel report. In: Leucocyte Typing VI. Kishimoto T et al. (eds). Garland Publishing, New York and London, pp. 746-749.
10. Ehlers MR, Riordan JF (1989) Angiotensin-converting enzyme: new concepts concerning its biological role. Biochemistry 28:5331-5318.
11. Ehlers MR, Chen YN, Riordan JF (1992) The unique N-terminal sequence of testis angiotensin-converting enzyme is heavily O-glycosylated and unessential for activity or stability. Biochem Biophys Res Commun 183:199-205.
12. El-Dorry HA, MacGregor JS, Soffer RL (1983) Dipeptidyl carboxypeptidase from seminal fluid resembles the pulmonary rather than the testicular isoenzyme. Biochem Biophys Res Commun 115:1096-1100.
13. Foresta C, Mioni R, Rossato M, Varotto A, Zorzi M (1991) Evidence for the involvement of sperm angiotensin converting enzyme in fertilization. Int J Androl 14:333-339.
14. Foulkes NS, Schlotter F, Pevet P, Sassone-Corsi P (1993) Pituitary hormone FSH directs the CREM functional switch during spermatogenesis. Nature 362:264-267.
15. Franke FE, Pauls K, Kerkman L, Steger K, Klonisch T, Metzger R, Alhenc-Gelas F, Burkhardt E, Bergrnann M, Danilov SM (2000) Somatic isoform of angiotensin I-converting enzyme in the pathology of testicular germ cell tumors. Hum Pathol 31:1466-1476.
16. Fraser LR, Pondel MD, Vinson GP (2001) Calcitonin, angiotensin II and FPP significantly modulate mouse sperm function. Mol Hum Reprod 7:245-253.
17. Gatti JL, Druart X, Guerin Y, Dacheux F, Dacheux JL (1999) A 105- to 94-kilodalton protein in the epididymal fluids of domestic mammals is angiotensin I-converting enzyme (ACE); evidence that sperm are the source of this ACE. Biol Reprod 60:937-945.
18. Goraya TY, Kessler SP, Kumar RS, Douglas J, Sen GC (1994) Identification of positive and negative transcriptional regulatory elements of the rabbit angiotensin-converting enzyme gene. Nucl Acid Res 22:1194-1201.
19. Goraya TY, Kessler SP, Stanton P, Hanson RW, Sen GC (1995) The cyclic AMP response elements of the genes for angiotensin-converting enzyme and phosphoenolpyruvate carboxykinase (GPT) can mediate transcriptional activation by CREMτ and CREMα. J Biol Chem 270:19078-19085.
20. Hagaman JR, Moyer JS, Bachman ES, Sibony M, Magyar PL, Welch JE, Smithies O, Krege JH, O'Brien DA (1998) Angiotensin-converting enzyme and male fertility. Proc Natl Acad Sci USA 95:2552-2557.
21. Hilscher W (1991) The genetic control and germ cell kinetics of the female and male germ line in mammals including man. Human Reprod 6:1416-1425.
22. Hooper NM, Karran EH, Turner AJ (1997) Membrane protein secretases. Biochem J 321:265-279.
23. Howard TE, Shai SY, Langford KG, Martin BM, Bernstein KE (1990) Transcription of testicular angiotensin-converting enzyme (ACE) is initiated within the 12th intron of the somatic ACE gene. Mol Cell Biol 10:4294-4302.
24. Hubert C, Houot AM, Corvol P, Soubrier F (1991) Structure of the angiotensin I-converting enzyme gene. Two alternative promoters correspond to evolutionary steps of a duplicated gene. J Biol Chem 266:15377-15383.
25. Jaspard E, Alhenc-Gelas F (1995) Catalytic properties of the two active sites of angiotensin I-convertlng enzyme on the cell surface. Biochem Biophys Res Commun 211:528-534.
26. Jorgensen N, Rajpert-De Meyts E, Graem N, Muller J, Giwercman A, Skakkebaek NE (1995) Expression of immunohistochemical markers for testicular carcinoma in situ by normal human fetal germ cells. Lab Invest 72:223-231.
27. Kamata M, Hu J, Shibahara H, Nakagawa H (2001) Assay of testicular angiotensin-converting enzyme activity in human spermatozoa. Int J Androl 24:225-231.
28. Kessler SP, Rowe TM, Blendy JA, Erickson RP, Sen GC (1998) A cyclic AMP response element in the angiotensin-converting enzyme gene and the transcription factor CREM are required for transcription of the mRNA for the testicular isozyme. J Biol Chem 273:9971-9975.
29. Kessler SP, Rowe TM, Gomos JB, Kessler PM, Sen GC (2000) Physiological non-equivalence of the two isoforms of angiotensin-converting enzyme. J Biol Chem 275:26259-26264.
30. Kim HS, Krege JH, Kluckman KD, Hagaman JR, Hodgin JB, Best CF, Jenette JC, Coffman TM, Maeda N, Smithies O (1995) Genetic control of blood pressure and angiotensinogen locus. Proc Natl Acad Sci USA 92:2735-2739.
31. Köhn FM, Miska W, Schill WB (1995) Release of angiotensin-converting enzyme (ACE) from human spermatozoa during capacitation and acrosome reaction. J Androl 16:259-265.
32. Köhn FM, Dammshäuser I, Neukamm C, Renneberg H, Siems WE, Schill WB, Aumüller G (1998) Ultrastructural localization of angiotensin-converting enzyme in ejaculated human spermatozoa. Hum Reprod 13:604-610.
33. Krege JH, John SW, Langenbach LL, Hodgin JB, Hagaman JR, Bachman ES, Jennette JC, O'Brien DA, Smithies O (1995) Male-female differences in fertility and blood pressure in ACE-deficient mice. Nature 375:146-148.
34. Kumar RS, Thekkumkara TJ, Sen GC (1991) The mRNAs encoding the two angiotensin-converting isozymes are transcribed from the same gene by a tissue-specific choice of alternative transcription initiation sites. J Biol Chem 266:3854-3862.
35. Langford KG, Zhou Y, Russell LD, Wilcox JN, Bernstein KE (1993) Regulated expression of testis angiotensin-converting enzyme during spermatogenesis in mice. Biol Reprod 48:1210-1218.
36. Lattion AL, Soubrier F, Allegrini J, Hubert C, Corvol P, Alhenc-Gelas F (1989) The testicular transcript of the angiotensin I-converting enzyme encodes for the ancestral, non-duplicated form of the enzyme. FEBS Lett 252:99-104.
37. Lenfant M, Wdzieczak-Bakala J, Guittet E, Prome JC, Sotty D, Frindel E (1989) Inhibitor of hematopoietic pluripotent stem cell proliferation: purification and determination of its structure. Proc Nat Acad Sci USA 86:779-782.
38. Leung PS, Chan HC, Fu LXM, Leung PY, Chew SBC, Wong PYD (1997) Angiotensin II receptors, localization of type 1 and type II in the rat epididymides of different developmental stages. J Membrane Biol 157:97-103.
39. Leung PS, Wong TP, Sernia C (1999) Angiotensinogen expression by rat epididymis: evidence for an intrinsic angiotensin-generating system. Mol Cell Endocrinol 155:115-122.
40. Metzger R, Bohle RM, Pauls K, Eichner G, Alhenc-Gelas F, Danilov SM, Franke FE (1999) Angiotensin-converting enzyme in non-neoplastic kidney diseases. Kidney Int 56:1442-1454.
41. Metzger R, Bohle RM, Chumachenko P, Danilov SM, Franke FE (2000) CD143 in the development of atherosclerosis. Atherosclerosis 150:21-31.
42. Monsees TK, Miska W, Schill WB (1996) Enzymatic digestion of bradykinin by rat Sertoli cell cultures. J Androl 17:375-381.
43. Monsees TK, Miska W, Blöcher S, Schill WB, Winkler A, Siems WE (1999) Elements of the kallikrein kinin system are present in the rat seminiferous epithelium. Immunopharmacol 45:107-114.
44. Monsees TK, Blöcher S, Heidorn F, Winkler A, Siems WE, Müller-Esterl W, Hayatpour J, Miska W, Schill WB (2002) Expression and location of the bradykinin B2 receptor in rat testis. Biol Reprod 67:1832-1839.
45. O'Mahony OA, Djahanbahkch O, Mahmood T, Puddefoot JR, Vinson GP (2000) Angiotensin II in human seminal fluid. Hum Reprod 15:1345-1349.
46. Pandey KN, Misono KS, Inagami T (1984) Evidence for intracellular formations of angiotensins: coexistence of renin and angiotensin-converting enzyme in Leydig cells of rat testis. Biochem Biophys Res Commun 122:1337-1343.
47. Pauls K, Fink L, Franke FE (1999) Angiotensin-converting enzyme in neoplastic germ cells. Lab Invest 79:1425-1435.
48. Ramaraj P, Kessler SP, Colmenares C, Sen GC (1998) Selective restoration of male fertility in mice lacking angiotensin-converting enzymes by sperm-specific expression of the testicular isozyme. J Clin Invest 102:371-378.
49. Ramchandran R, Sen GC, Misono K, Sen I (1994) Regulated cleavage-secretion of the membrane-bound angiotensin-converting enzyme. J Biol Chem 269:2125-2130.
50. Rousseau A, Michaud A, Chauvet MT, Lenfant M, Corvol P (1995) The hemoregulatory peptide N-Acetyl-Ser-Asp-Lys-Pro is a natural and specific substrate of the N-terminal active site of human angiotensin-converting enzyme. J Biol Chem 270:3656-3661.
51. Ryan US, RyanJW, Whitaker C, Chiu A (1976) Localization of angiotensin converting enzyme (kininase II). II. Immunocytochemistry and immunofluorescence. Tissue Cell 8:125-145.
52. Sabeur K, Vo AT, Ball BA (2000) Effects of angiotensin II on the acrosome reaction in equine spermatozoa. J Reprod Fertil 120:135-142.
53. Sabeur K, Vo AT, Ball BA (2001) Characterization of angiotensin-converting enzyme in canine testis. Reproduction 122:139-146.
54. Schill WB, Miska W (1992) Possible effects of the kallikrein-kinin system on male reproductive functions. Andrologia 24:69-75.
55. Schütz S, Le Moullec JM, Corvol P, Gasc JM (1996) Early expression of all the components of the renin-angiotensin-system in human development. Am J Pathol 149:2067-2079.
56. Sibony M, Gasc JM, Soubrier F, Alhenc-Gelas F, Corvol P (1993) Gene expression and tissue localization of the two isoforms of angiotensin I converting enzyme. Hypertension 21:827-835.
57. Sibony M, Segretain D, Gasc JM (1994) Angiotensin-converting enzyme in murine testis: step-specific expression of the germinal isoform during spermiogenesis. Biol Reprod 50:1015-1026.
58. Skakkebeak NE, Berthelsen JG, Giwercman A, Muller J (1987) Carcinoma-in-situ of the testis: possible origin from gonocytes and precursor of all types of germ cell tumours except spermatocytoma. Int J Androl 10:19-28.
59. Skidgel RA, Erdös EG (1993) Biochemistry of angiotensin I-converting enzyme. In: Renin Angiotensin System. Robertson JIS, Nichols MG (eds). Gower Medical, London, pp. 10.1-10.10.
60. Soubrier F, Alhenc-Gelas F, Hubert C, Allegrini J, John M, Tregear G, Corvol P (1988) Two putative active centers in human angiotensin I-converting enzyme revealed by molecular cloning. Proc Natl Acad Sci USA 85:9386-9390.
61. Steger K (1999) Transcriptional and translational regulation of gene expression in haploid spermatids. Anat Embryol 199:471-487.
62. Steger K, Klonisch T, Gavenis K, Drabent B, Doenecke D, Bergmann M (1998) Expression of mRNA and protein of nucleoproteins during human spermiogenesis. Mol Hum Reprod 4:939-945.
63. Stephan J, Melaine N, Ezan E, Hakovirta H, Maddocks S, Toppari J, Garnier D, Wdzieczak-Bakala J, Jegou B (2000) Sourse, catabolism and role of the tetrapeptide N-acetyl-ser-asp-lys-Pro within the testis. J Cell Sci 113:113-121.
64. Strittmatter SM, Thiele EA, De Souza EB, Snyder SH (1985) Angiotensin-converting enzyme in the testis and epididymis, differential development and pituitary regulation of isozymes. Endocrinology 117:1374-1379.
65. Tanimoto K, Sugiyama F, Goto Y (1994) Angiotensinogen-deficient mice with hypotension. J Biol Chem 269:331-334.
66. Testut P, Soubrier F, Corvol P, Hubert C (1993) Functional analysis of the human somatic angiotensin I-converting enzyme gene promoter. Biochem J 293:843-848.
67. Vanha-Perttula T, Mather JP, Bardin CW, Moss SB, Bellve AR (1985) Localization of the angiotensin-converting enzyme activity in testis and epididymis. Biol Reprod 33:870-877.
68. Velletri PA, Aquilano DR, Bruckwick E, Tsai-Morris CH, Dufau ML, Lovenberg W (1985) Endocrinological control and cellular localization of rat testicular angiotensin-converting enzyme (EC 3.4.15.1). Endocrinology 116:2516-2522.
69. Villard E, Alonso A, Agrapart M, Challah M, Soubrier F (1998) Induction of angiotensin I-converting enzyme transcription by a protein kinase C-dependent mechanism in human endothelial cells. J Biol Chem 272:25191-25197.
70. Vinson GP, Puddefoot JR, Ho MM, Barker S, Mehta J, Saridogan E, Djahanbakhch O (1995) Type 1 angiotensin II receptors in rat and human sperm. J Endocrinol 144:369-378.
71. Vinson GP, Mehta J, Evans S, Matthews S, Puddefoot JR, Saridogan E, Holt WV, Djahanbakhch O (1996) Angiotensin II stimulates sperm motility. Regul Pept 67:131-135.
72. Vivet F, Callard P, Gamoudi A (1987) Immunolocalization of angiotensin 1 converting enzyme in the human male genital tract by the avidin-biotin-complex method. Histochemistry 86:499-502.
73. Wartenberg H (1981) Differentiation and development of the testis. In: The Testis. Burger H, de Kretser D (eds). Raven Press, New York, pp. 39-80.
74. Wei L, Alhenc-Gelas F, Soubrier F, Corvol P, Clausner E (1991a) Expression and characterization of recombinant human angiotensin I-converting enzyme, evidence for a C-terminal transmembrane anchor and for a proteolytic processing of the secreted recombinant and plasma enzymes. J Biol Chem 266:5540-5546.
75. Wei L, Alhenc-Gelas F, Corvol P, Clauser E (1991b) The two homologous domains of human angiotensin I-converting enzyme are both catalytically active. J Biol Chem 266:9002-9008.
76. Wei L, Clauser E, Alhenc-Gelas F, Corvol P (1992) The two homologous domains of human angiotensin I-converting enzyme interact differently with competitor inhibitors. J Biol Chem 267:13398-13405.
77. Williams TA, Barnes K, Kenny AJ, Turner AJ, Hooper NM (1992) A comparison of the zinc contents and substrate specificities of the endothelial and testicular forms of porcine angiotensin converting enzyme and the preparation of isoenzyme-specific antisera. Biochem J 288:875-881.
78. Wong PYD, Uchendu CN (1990) The role of angiotensin-converting enzyme in the rat epididymis. J Endocrinol 125:457-465.
79. Wong PYD, Uchendu CN (1991) Studies on renin-angiotensin system in primary monolayer cell cultures of the rat epididymis. J Endocrinol 131:287-293.
80. Yeung CH, Nashan D, Sorg C, Oberpenning F, Schulze H, Nieschlag E, Cooper TG (1994) Basal cells of the human epididymis - antigenic and ultrastructural similarities to tissue-fixed macrophages. Biol Reprod 50:917-926.
81. Zhou Y, Sun Z, Means AR, Sassone CP, Bernstein KE (1996) cAMP-response element modulator tau is a positive regulator of testis angiotensin converting enzyme transcription. Proc Natl Acad Sci USA 93:12262-12266.