Human sperm devoid of germinal angiotensin-converting enzyme is responsible for total fertilization failure and lower fertilization rates by conventional in vitro fertilization

Biology of Reproduction

Volumn 90, Issue 6, 2014, Pages

  Li, Le Jun ^a   Zhang, Feng Bin ^a   Liu, Shu Yuan ^a   Tian, Yong Hong ^a   Le, Fang ^a   Wang, Li Ya ^a   Lou, Hang Ying ^a   Xu, Xiang Rong ^a   Huang, He Feng ^a   Jin, Fan ^a,b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Conventional in vitro fertilization; Germinal angiotensin converting enzyme; Lower fertilization rates; Sperm; Total fertilization failure

Indexed keywords

DIPEPTIDYL CARBOXYPEPTIDASE;

ADULT; ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; CORRELATIONAL STUDY; FEMALE; FERTILIZATION IN VITRO; GENOTYPE; HUMAN; IMMUNOFLUORESCENCE; INTRACYTOPLASMIC SPERM INJECTION; LOWER FERTILIZATION RATE; MAJOR CLINICAL STUDY; MALE; MALE GENITAL TRACT PARAMETERS; MALE INFERTILITY; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM; SPERM; TOTAL FERTILIZATION FAILURE; WESTERN BLOTTING; CHEMISTRY; CYTOLOGY; ENZYME ACTIVE SITE; ENZYMOLOGY; FERTILIZATION; GENETIC SCREENING; GENETICS; INFERTILITY, MALE; METABOLISM; OOCYTE RETRIEVAL; PHYSIOLOGY; PROMOTER REGION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SPERMATOZOON; TESTIS; TREATMENT FAILURE;

ADULT; CATALYTIC DOMAIN; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; GENETIC TESTING; GENOTYPE; HUMANS; INFERTILITY, MALE; MALE; OOCYTE RETRIEVAL; PEPTIDYL-DIPEPTIDASE A; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; PROMOTER REGIONS, GENETIC; SPERM INJECTIONS, INTRACYTOPLASMIC; SPERMATOZOA; TESTIS; TREATMENT FAILURE;

EID: 84903795668     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.114827     Document Type: Article

References (40)

1. Molloy D, Harrison K, Breen T, Hennessey J. The predictive value of idiopathic failure to fertilize on the first in vitro fertilization attempt. Fertil Steril 1991; 56:285-289.
2. Mahutte NG, Arici A. Failed fertilization: is it predictable? Curr Opin Obstet Gynecol 2003; 15:211-218.
3. Roest J, Van Heusden AM, Zeilmaker GH, Verhoeff A. Treatment policy after poor fertilization in the first IVF cycle. J Assist Reprod Genet 1998; 15:18-21.
4. Benadiva CA, Nulsen J, Siano L, Jennings J, Givargis HB, Maier D. Intracytoplasmic sperm injection overcomes previous fertilization failure with conventional in vitro fertilization. Fertil Steril 1999; 72:1041-1044.
5. van der Westerlaken L, Helmerhorst F, Dieben S, Naaktgeboren N. Intracytoplasmic sperm injection as a treatment for unexplained total fertilization failure or low fertilization after conventional in vitro fertilization. Fertil Steril 2005; 83:612-617.
6. Liu DY, Baker HW. Defective sperm-zona pellucida interaction: a major cause of failure of fertilization in clinical in-vitro fertilization. Hum Reprod 2000; 15:702-708.
7. Baba D, Kashiwabara S, Honda A, Yamagata K, Wu Q, Ikawa M, Okabe M, Baba T. Mouse sperm lacking cell surface hyaluronidase PH-20 can pass through the layer of cumulus cells and fertilize the egg. J Biol Chem 2002; 277:30310-30314.
8. Inoue N, Ikawa M, Nakanishi T, Matsumoto M, Nomura M, Seya T, Okabe M. Disruption of mouse CD46 causes an accelerated spontaneous acrosome reaction in sperm. Mol Cell Biol 2003; 23:2614-2622.
9. Baba T, Niida Y, Michikawa Y, Kashiwabara S, Kodaira K, Takenaka M, Kohno N, Gerton GL, Arai Y. An acrosomal protein, sp32, in mammalian sperm is a binding protein specific for two proacrosins and an acrosin intermediate. J Biol Chem 1994; 269:10133-10140.
10. Muro Y, Okabe M. Mechanisms of fertilization: a view from the study of gene-manipulated mice. J Androl 2011; 32:218-225.
11. Cho C, Bunch DO, Faure JE, Goulding EH, Eddy EM, Primakoff P, Myles DG. Fertilization defects in sperm from mice lacking fertilin beta. Science 1998; 281:1857-1859.
12. Cushman D, Cheung H. Studies in vitro of angiotensin-converting enzyme of lung and other tissues. In: Genest J, Koiw E (eds.), Hypertension. Berlin: Springer-Verlag Press; 1972:532-541.
13. Hubert C, Houot AM, Corvol P, Soubrier F. Structure of the angiotensin Iconverting enzyme gene: two alternate promoters correspond to evolutionary steps of a duplicated gene. J Biol Chem 1991; 266: 15377-15383.
14. Howard T, Balogh R, Overbeek P, Bernstein KE. Sperm-specific expression of angiotensin-converting enzyme (ACE) is mediated by a 91-base-pair promoter containing a CRE-like element. Mol Cell Biol 1993; 13:18-27.
15. Hagaman JR, Moyer JS, Bachman ES, Sibony M, Magyar PL, Welch JE, Smithies O, Krege JH, O'Brien DA. Angiotensin-converting enzyme and male fertility. Proc Natl Acad Sci U S A 1998; 95:2552-2557.
16. Yoon SY, Jellerette T, Salicioni AM, Lee HC, Yoo MS, Coward K, Parrington J, Grow D, Cibelli JB, Visconti PE, Mager J, Fissore RA. Human sperm devoid of PLC, zeta 1 fail to induce Ca(2+) release and are unable to initiate the first step of embryo development. J Clin Invest 2008; 118:3671-3681.
17. Goodrich R, Johnson G, Krawetz SA. The preparation of human spermatozoal RNA for clinical analysis. Arch Androl 2007; 53:161-167.
18. World Health Organization. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction, 4th ed. New York: Cambridge University Press; 1999.
19. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-685.
20. Gazquez C, Oriola J, de Mateo S, Vidal-Taboada JM, Ballesca JL, Oliva R. A common protamine 1 promoter polymorphism (_190 C-. >A) correlates with abnormal sperm morphology and increased protamine P1/ P2 ratio in infertile patients. J Androl 2008; 29:540-548.
21. Persu A, Lambert M, Deinum J, Cossu M, de Visscher N, Irenge L, Ambroise J, Minon JM, Nesterovitch AB, Churbanov A, Popova IA, Danilov SM, et al. A novel splice-site mutation in angiotensin I-converting enzyme (ACE) gene, c.3691+1G>A (IVS25+1G>A), causes a dramatic increase in circulating ACE through deletion of the transmembrane anchor. PLoS One 2013; 8:e59537.
22. Nikolaeva MA, Balyasnikova IV, Alexinskaya MA, Metzger R, Franke FE, Albrecht RF II, Kulakov VI, Sukhikh GT, Danilov SM. Testicular isoform of angiotensin I-converting enzyme (ACE, CD143) on the surface of human spermatozoa: revelation and quantification using monoclonal antibodies. Am J Reprod Immunol 2006; 55:54-68.
23. Database of Single Nucleotide Polymorphisms (dbSNP), National Center for Biotechnology Information. Bethesda, MD: National Library of Medicine Build 139. http://www.ncbi.nlm.nih.gov/projects/SNP. Accessed 17 November 2013.
24. Verheyen G, Tournaye H, Staessen C, De Vos A, Vandervorst M, Van Steirteghem A. Controlled comparison of conventional in-vitro fertilization and intracytoplasmic sperm injection in patients with asthenozoospermia. Hum Reprod 1999; 14:2313-2319.
25. Repping S, van Weert JM, Mol BW, de Vries JW, van der Veen F. Use of the total motile sperm count to predict total fertilization failure in in vitro fertilization. Fertil Steril 2002; 78:22-28.
26. Krege JH, John SW, Langenbach LL, Hodgin JB, Hagaman JR, Bachman ES, Jennette JC, O'Brien DA, Smithies O. Male-female differences in fertility and blood pressure in ACE-deficient mice. Nature 1995; 375: 146-148.
27. Ramaraj P, Kessler SP, Colmenares C, Sen GC. Selective restoration of male fertility in mice lacking angiotensin-converting enzymes by spermspecific expression of the testicular isozyme. J Clin Invest 1998; 102: 371-378.
28. Foresta C, Mioni R, Rossato M, Varotto A, Zorzi M. Evidence for the involvement of sperm angiotensin converting enzyme in fertilization. Int J Androl 1991; 14:333-339.
29. Shibahara H, Kamata M, Hu J, Nakagawa H, Obara H, Kondoh N, Shima H, Sato I. Activity of testis angiotensin converting enzyme (ACE) in ejaculated human spermatozoa. Int J Androl 2001; 24:295-299.
30. Balyasnikova IV, Metzger R, Franke FE, Conrad N, Towbin H, Schwartz DE, Sturrock ED, Danilov SM. Epitope mapping of mAbs to denatured human testicular ACE (CD143). Tissue Antigens 2008; 72:354-368.
31. Tanahatoe SJ, McDonnell J, Goverde AJ, Hompes PG, Lambalk CB. Total fertilization failure and idiopathic subfertility. Reprod Biol Endocrinol 2009; 7:3.
32. Howard TE, Shai SY, Langford KG, Martin BM, Bernstein KE. Transcription of testicular angiotensin-converting enzyme (ACE) is initiated within the 12th intron of the somatic ACE gene. Mol Cell Biol 1990; 10:4294-4302.
33. Sibony M, Segretain D, Gasc JM. Angiotensin-converting enzyme in murine testis: step-specific expression of the germinal isoform during spermiogenesis. Biol Reprod 1994; 50:1015-1026.
34. Fuchs S, Frenzel K, Hubert C, Lyng R, Muller L, Michaud A, Xiao HD, Adams JW, Capecchi MR, Corvol P, Shur BD, Bernstein KE. Male fertility is dependent on dipeptidase activity of testis ACE. Nat Med 2005; 11:1140-1142, author reply 1142-1143.
35. Ehlers MR, Fox EA, Strydom DJ, Riordan JF. Molecular cloning of human testicular angiotensin-converting enzyme: the testis isozyme is identical to the C-terminal half of endothelial angiotensin-converting enzyme. Proc Natl Acad Sci U S A 1989; 86:7741-7745.
36. Kumar RS, Kusari J, Roy SN, Soffer RL, Sen GC. Structure of testicular angiotensin-converting enzyme: a segmental mosaic isozyme. J Biol Chem 1989; 264:16754-16758.
37. Lattion AL, Soubrier F, Allegrini J, Hubert C, Corvol P, Alhenc-Gelas F. The testicular transcript of the angiotensin I-converting enzyme encodes for the ancestral, non-duplicated form of the enzyme. FEBS Lett 1989; 252:99-104.
38. Langford KG, Zhou Y, Russell LD, Wilcox JN, Bernstein KE. Regulated expression of testis angiotensin-converting enzyme during spermatogenesis in mice. Biol Reprod 1993; 48:1210-1218.
39. Corvol P. ACE sets up fertilization. Nat Med 2005; 11:118-119.
40. Fujihara Y, Tokuhiro K, Muro Y, Kondoh G, Araki Y, Ikawa M, Okabe M. Expression of TEX101, regulated by ACE, is essential for the production of fertile mouse spermatozoa. Proc Natl Acad Sci U S A 2013; 110:8111-8116.