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Reduced Semen Quality in Chronic Prostatitis Patients That Induce the Release of Apoptotic Protein Omi/Htra2 from Spermatozoa

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Reduced Semen Quality in Chronic Prostatitis Patients That Induce the Release of Apoptotic Protein Omi/Htra2 from Spermatozoa Prostate Cancer and Prostatic Diseases (2007) 10, 104–108 & 2007 Nature Publishing Group All rights reserved 1365-7852/07 $30.00 www.nature.com/pcan ORIGINAL ARTICLE Reduced semen quality in chronic prostatitis patients that induce the release of apoptotic protein Omi/HtrA2 from spermatozoa XY Hu, YM Xu, Y Qiao, DL Wu, YL Sa, Q Fu, JJ Yu, XR Zhang, J Zhang, BJ Gu, R Chen and H Xie Department of Urology, Shanghai Jiaotong University Affiliated No. 6 People’s Hospital, Shanghai, China The relationship between chronic prostatitis and fertility has been disputed for many years. Several groups have shown infection and autoimmune response against prostate antigens could have a deleterious effect on semen quality and fertility. This study was conducted to test the hypothesis that Omi/HtrA2-induced apoptosis in chronic prostatitis could be a mechanism underlying the observed clinical benefit. The Omi/HtrA2 serine protease is a nuclear-encoded mitochondrial protein, which can be released from mitochondria into the cytosol after apoptosis stimuli, inducing apoptosis in caspase-dependent and independent manners. Forty-one patients diagnosed as suffering from chronic prostatitis were included. Healthy normal individuals were included as controls. Human spermatozoa in the semen were purified by Percoll-gradient technique to separate the seminal plasma and other round cells. Measurements for sperm concentration, motility, morphology, proinflammatory cytokines, Omi/HtrA2 mRNA and protein levels in spermatozoa of chronic protatitis patients, were performed accordingly. Significantly increased levels of proinflammatory cytokines were detected in seminal plasma from these prostatitis patients. Omi/ HtrA2 mRNA and protein levels were significantly higher in prostatitis men than in normal men. This study shows that chronic prostatitis patients present important alterations in their semen quality parameters, Omi/HtrA2 mRNA and protein levels of spermatozoa. We speculate that the inflammatory process involved may affect male fertility by release of proapoptotic protein Omi/HtrA2. Prostate Cancer and Prostatic Diseases (2007) 10, 104–108. doi:10.1038/sj.pcan.4500919; published online 17 October 2006 Keywords: chronic prostatitis; cytokines; male infertility; Omi/HtrA2; semen quality Introduction and inflammatory process, with abnormalities in semen quality and function,7 then male fertility would Chronic prostatitis is a common diagnosis but very little be impaired by prostate secretion meeting sperm cells is understood about the aetiology and the pathogenesis during ejaculation, or including a direct effect of of the disease.1,2 Men with chronic prostatitis present an inflammation on the testis and epididymis, however, episodic and relapsing condition characterized by pelvic the molecular mechanism of it is not fully understood. pain, irritative voiding symptoms and effects on sexual Omi/HtrA2 is a nuclear-encoded mitochondrial serine function.3 The symptoms of the disease are suggestive of protease, which can released from mitochondria into the an infection in the prostate gland and bacterial infections cytosol after apoptosis stimuli, such as tumour necrosis occur in 5–10% of patients. However, a large body of factor (TNF), growth-factor depletion, inflammation evidence accumulated over many years has failed to factors, DNA damaging agents, irradiation and so on, provide convincing proof that some fastidious organisms inducing apoptosis in caspase-dependent and indepen- are responsible for symptoms in a significant proportion dent manners.8 In this study, we analysed a group of of men who present symptoms of chronic prostatitis. patients with chronic prostatitis in order to investigate Recently, several groups reported that autoimmune whether reduced semen quality, mainly of inflammatory response against prostate antigens and the inflamma- factors, induced release of Omi/HtrA2 would have any tory process involved may play an important role in the effect on male fertility. pathogenesis of chronic prostatitis.4–6 Chronic prostatitis associated, mainly of infectious origin, autoimmunity Materials and methods Correspondence: Professor YM Xu, Department of Urology, Shanghai Jiaotong University Affiliated No. 6 People’s Hospital, 600 Yishan Rd, Patients Shanghai 200233, China. 7 7 E-mail: [email protected] We included 41 patients (mean s.d. age: 38.62 7.65 Received 25 July 2006; revised and accepted 19 September 2006; years, range 18–49) and 15 control volunteers (age: published online 17 October 2006 30.4574.83 years, range 24–45) from Department of Omi/HtrA2 release from spermatozoa XY Hu et al Urology, Shanghai Jiaotong University Affiliated Sixth Sperm samples 105 People’s Hospital in our study. Normal individuals Sperm samples were obtained from A and B groups men. answered a questionnaire and had no history of any Semen was collected by masturbation after 3 days of genitourinary symptoms, instrumentation or surgery. sexual abstinence and allowed to liquefy for 30–60 min at They underwent the same assessment as patients. room temperature. A semen analysis was performed Patients and controls agreed to donate blood samples according to WHO (World Health Organization, 1999) and semen; they had not been taking antibiotics, non- guidelines. Eosin–nigrosin staining was used for asses- steroidal anti-inflammatory drugs or steroids for 4 weeks sing viability of selected sperm and the samples with before, or during the study. Volunteers who had under- more than 5% of dead spermatozoa were excluded gone vasectomy were specifically excluded. A diagnosis from this study. Diff-Quik staining was used to evaluate of chronic symptomatic prostatitis was given in cases of a the sperm morphology. Normozoospermic (sperm con- history of X3 months of pelvic or genital pain, or both, centration X20 Â 106/ml, total of motility grades A and B associated with voiding and/or sexual dysfunction and X50%, normal sperm morphology X30%, n ¼ 12) and painful digital rectal examination of the prostate. All prostatitis semen (sperm concentration X20 Â 106/ml, patients underwent a standard evaluation, including total of motility grades A and B p30%, normal sperm digital rectal examination, microscopic examination and morphology X30%, n ¼ 41) were selected for the study. culture of urine and semen. To discriminate between Spermatozoa were purified by the Percoll-gradient patients with infectious and non-infectious chronic technique (four layers: 47.5, 57, 76 and 95%) to separate prostatitis, conventional and non-conventional bacterial seminal plasma and also remove other round cells. After cultures were performed in their urine and semen. We centrifugation (20 min at 400 g,251C), the spermatozoa could detect infection of known prostatic pathogens were collected from the interface 57–76% and the under (e.g.: Escherichia coli; Staphylococcus aureus; Klebsiella sp; layer of 95%, and then washed twice with phosphate- Chlamydia trachomatis; Candida albicans; Trichomonas sp) in buffered saline buffer. The washed spermatozoa were infectious chronic prostatitis patients in 41 patients, and stored at À801C for RNA analysis. In order to detect the we therefore named this group as group A (patients with purification of selected sperm, the samples were exam- type II NIH prostatitis). Group B age-matched volunteers ined under microscope. No remaining round cells were with no history of genitourinary disease, who were observed. This study was approved by the ethical used as control group, did not show any presence of committee of the hospital and all participants signed an infectious agent either in semen or in urine (group B, the consent form permitting to use their sperm samples n ¼ 12). in the study. Semen analysis RT-PCR assay Semen samples were collected directly into a sterile Total RNA from purified spermatozoa was extracted container by masturbation after 2–7 days of sexual with TRIzol Reagent (Invitrogen, Carlsbad, CA, USA). abstinence. Semen samples and blood were obtained Two micrograms of total RNA was reversed transcribed at the same visit. Standard clinical semen analysis with Reverse Transcription System (Promega, Madison, was performed according to World Health Organiza- WI, USA). Polymerase chain reaction (PCR) was per- tion (1999) criteria. Semen analysis consisted of determi- formed on reverse transcription (RT) products 5 ml, 2.5 IU nation of sample volume, sperm density (concentration), of Taq DNA polymerase, 10 Â PCR buffer 5 ml, 25 mM progressive motility, vitality (eosin exclusion), morpho- MgCl2 4 ml, 10 mM dNTP 1 ml and 50 pmol of the forward logy (World Health Organization (1992)) classification and reverse primers in a final volume of 50 ml. Primer for and Kruger classification, pH, and concentrations of Omi/HtrA2 (sense-50-TCCTTTGCCATCCCTTCT-30,anti- citrate and fructose. Citrate and fructose were sense-50-TCTGTCTCGGTGCCCTCA-30) and glyceral- measured as tests of function of the prostate and seminal dehyde-3-phosphate dehydrogenase (GAPDH, sense-50- vesicles, respectively. Identification of leucocytes and TGGGTGTCGCTGTTGAAGTC-30, antisense-50-GCTGG other cells was carried out by a peroxidase cyto- CGCTGAGTACGTCGT-30) was synthesized by Shanghai chemical technique. Results were expressed as 1 Â106 Shenggong Company (Shanghai, China). The PCR con- leucocytes/ml. To assess the functional integrity of ditions were as follows: initial denaturation at 941C for sperm membrane, hypo-osmotic swelling (HOS) test 5 min, then 30 cycles of 951C for 30 s, 551C for
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