Involvement of Bicarbonate-Induced Radical Signaling in Oxysterol Formation and Sterol Depletion of Capacitating Mammalian Sperm During In Vitro Fertilization

被引:56
作者
Boerke, Arjan [1 ]
Brouwers, Jos F. [1 ]
Olkkonen, Vesa M. [2 ]
van de Lest, Chris H. A. [1 ]
Sostaric, Edita
Schoevers, Eric J. [3 ,4 ]
Helms, J. Bernd [1 ]
Gadella, Barend M. [1 ,4 ]
机构
[1] Univ Utrecht, Fac Vet Med, Dept Biochem & Cell Biol, Utrecht, Netherlands
[2] Minerva Fdn, Inst Med Res, Biomedicum Helsinki 2U, Helsinki, Finland
[3] Univ Utrecht, Fac Vet Med, Dept Equine Sci, Utrecht, Netherlands
[4] Univ Utrecht, Fac Vet Med, Dept Farm Anim Hlth, Utrecht, Netherlands
关键词
acrosome reaction; in vitro fertilization (IVF); oxidative stress; porcine/pig; sperm capacitation; CHOLESTEROL EFFLUX; LIPID RAFTS; MOUSE SPERM; TYROSINE PHOSPHORYLATION; HYDROGEN-PEROXIDE; ALPHA-TOCOPHEROL; PLASMA-MEMBRANE; BINDING; PROTEINS; REORGANIZATION;
D O I
10.1095/biolreprod.112.101253
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
This study demonstrates for the first time that porcine and mouse sperm incubated in capacitation media supplemented with bicarbonate produce oxysterols. The production is dependent on a reactive oxygen species (ROS) signaling pathway that is activated by bicarbonate and can be inhibited or blocked by addition of vitamin E or vitamin A or induced in absence of bicarbonate with pro-oxidants. The oxysterol formation was required to initiate albumin dependent depletion of 30% of the total free sterol and >50% of the formed oxysterols. Incubation of bicarbonate treated sperm with oxysterol-binding proteins (ORP-1 or ORP-2) caused a reduction of >70% of the formed oxysterols in the sperm pellet but no free sterol depletion. Interestingly, both ORP and albumin treatments led to similar signs of sperm capacitation: hyperactivated motility, tyrosin phosphorylation, and aggregation of flotillin in the apical ridge area of the sperm head. However, only albumin incubations led to high in vitro fertilization rates of the oocytes, whereas the ORP-1 and ORP-2 incubations did not. A pretreatment of sperm with vitamin E or A caused reduced in vitro fertilization rates with 47% and 100%, respectively. Artificial depletion of sterols mediated by methyl-beta cyclodextrin bypasses the bicarbonate ROS oxysterol signaling pathway but resulted only in low in vitro fertilization rates and oocyte degeneration. Thus, bicarbonate-induced ROS formation causes at the sperm surface oxysterol formation and a simultaneous activation of reverse sterol transport from the sperm surface, which appears to be required for efficient oocyte fertilization.
引用
收藏
页数:18
相关论文
共 46 条
[1]   The Capacitation-Apoptosis Highway: Oxysterols and Mammalian Sperm Function [J].
Aitken, R. John .
BIOLOGY OF REPRODUCTION, 2011, 85 (01) :9-12
[2]   Oxidative stress, sperm survival and fertility control [J].
Aitken, RJ ;
Baker, MA .
MOLECULAR AND CELLULAR ENDOCRINOLOGY, 2006, 250 (1-2) :66-69
[3]   GENERATION OF REACTIVE OXYGEN SPECIES, LIPID-PEROXIDATION, AND HUMAN-SPERM FUNCTION [J].
AITKEN, RJ ;
CLARKSON, JS ;
FISHEL, S .
BIOLOGY OF REPRODUCTION, 1989, 41 (01) :183-197
[4]   Effect of tyrosine kinase inhibitors on tyrosine phosphorylation and motility parameters in human sperm [J].
Bajpai, M ;
Asin, S ;
Doncel, GF .
ARCHIVES OF ANDROLOGY, 2003, 49 (03) :229-246
[5]   Cloning of ABCA17, a novel rodent sperm-specific ABC (ATP-binding cassette) transporter that regulates intracellular lipid metabolism [J].
Ban, N ;
Sasaki, M ;
Sakai, H ;
Ueda, K ;
Inagaki, N .
BIOCHEMICAL JOURNAL, 2005, 389 :577-585
[6]   Protein supplementation of human IVF culture media [J].
Blake, D ;
Svalander, P ;
Jin, MS ;
Silversand, C ;
Hamberger, L .
JOURNAL OF ASSISTED REPRODUCTION AND GENETICS, 2002, 19 (03) :137-143
[7]   Capacitation-dependent reorganization of microdomains in the apical sperm head plasma membrane: Functional relationship with zona binding and the zona-induced acrosome reaction [J].
Boerke, A. ;
Tsai, P. S. ;
Garcia-Gil, N. ;
Brewis, I. A. ;
Gadella, B. M. .
THERIOGENOLOGY, 2008, 70 (08) :1188-1196
[8]   Additional value of computer assisted semen analysis (CASA) compared to conventional motility assessments in pig artificial insemination [J].
Broekhuijse, M. L. W. J. ;
Sostaric, E. ;
Feitsma, H. ;
Gadella, B. M. .
THERIOGENOLOGY, 2011, 76 (08) :1473-1486
[9]   Mass Spectrometric Detection of Cholesterol Oxidation in Bovine Sperm [J].
Brouwers, Jos F. ;
Boerke, Arjan ;
Silva, Patricia F. N. ;
Garcia-Gil, Nuria ;
van Gestel, Renske A. ;
Helms, J. Bernd ;
van de Lest, Chris H. A. ;
Gadella, Bart M. .
BIOLOGY OF REPRODUCTION, 2011, 85 (01) :128-136
[10]   Cyclodextrin removes cholesterol from mouse sperm and induces capacitation in a protein-free medium [J].
Choi, YH ;
Toyoda, Y .
BIOLOGY OF REPRODUCTION, 1998, 59 (06) :1328-1333