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- W2024659558 abstract "The effects of cryopreservation on meiotic progression, synapsis, recombination, and structure of synaptonemal complexes (SCs) in testicular tissues were evaluated by comparing the above-mentioned parameters in frozen and fresh testicular tissues from the same men. No differences in meiotic progression, the mean number of MLH1 foci per cell, the mean number of autosomal SCs with different numbers of MLH1 foci, or the fidelity of the synapsis were observed between fresh and frozen testicular tissues. The effects of cryopreservation on meiotic progression, synapsis, recombination, and structure of synaptonemal complexes (SCs) in testicular tissues were evaluated by comparing the above-mentioned parameters in frozen and fresh testicular tissues from the same men. No differences in meiotic progression, the mean number of MLH1 foci per cell, the mean number of autosomal SCs with different numbers of MLH1 foci, or the fidelity of the synapsis were observed between fresh and frozen testicular tissues. Infertility is estimated to affect 10%–15% of couples, and approximately 40% of this infertility is due to male factors (1Hull M.G. Glazener C.M. Kelly N.J. Conway D.I. Foster P.A. Hinton R.A. et al.Population study of causes, treatment, and outcome of infertility.Br Med J (Clin Res Ed). 1985; 291: 1693-1697Crossref PubMed Scopus (918) Google Scholar, 2Dunson D.B. Baird D.D. Colombo B. Increased infertility with age in men and women.Obstet Gynecol. 2004; 103: 51-56Crossref PubMed Scopus (300) Google Scholar). To avoid repetitive biopsies for azoospermic men and to preserve fertile tissues from prepubertal boys and adult men undergoing gonadotoxic treatment such as chemotherapy or radiotherapy for malignant diseases, cryopreservation of testicular tissues is becoming an increasingly urgent clinical requisite (3Brook P.F. Radford J.A. Shalet S.M. Joyce A.D. Gosden R.G. Isolation of germ cells from human testicular tissue for low temperature storage and autotransplantation.Fertil Steril. 2001; 75: 269-274Abstract Full Text Full Text PDF PubMed Scopus (154) Google Scholar, 4Hovatta O. Cryopreservation of testicular tissue in young cancer patients.Hum Reprod Update. 2001; 7: 378-383Crossref PubMed Scopus (73) Google Scholar). Most studies on testicular cryopreservation have been aimed at evaluating the condition of testicular spermatozoa for future use in infertility treatment and for optimization of the cryopreservation protocol (5Tuuri T. Moilanen J. Kaukoranta S. Hovatta O. Testicular biopsy gun needle biopsy in collecting spermatozoa for intracytoplasmic injection, cryopreservation and histology.Hum Reprod. 1999; 14: 1274-1278Crossref PubMed Scopus (50) Google Scholar, 6Keros V. Rosenlund B. Hultenby K. Aghajanova L. Levkov L. Hovatta O. Optimizing cryopreservation of human testicular tissue: comparison of protocols with glycerol, propanediol and dimethylsulphoxide as cryoprotectants.Hum Reprod. 2005; 20: 1676-1687Crossref PubMed Scopus (130) Google Scholar, 7Keros V. Hultenby K. Borgström B. Fridström M. Jahnukainen K. Hovatta O. Methods of cryopreservation of testicular tissue with viable spermatogonia in pre-pubertal boys undergoing gonadotoxic cancer treatment.Hum Reprod. 2007; 22: 1384-1395Crossref PubMed Scopus (227) Google Scholar, 8Wyns C. Curaba M. Martinez-Madrid B. Van Langendonckt A. François-Xavier W. Donnez J. Spermatogonial survival after cryopreservation and short-term orthotopic immature human cryptorchid testicular tissue grafting to immunodeficient mice.Hum Reprod. 2007; 22: 1603-1611Crossref PubMed Scopus (137) Google Scholar). Few attempts have been made to examine the effects of the freezing and thawing procedure itself on spermatogenesis, particularly on homologous synapsis and recombination during prophase I of meiosis. Sun et al. (9Sun F. Trpkov K. Rademaker A. Ko E. Barclay L. Mikhaail-Philips M. et al.The effect of cold storage on recombination frequencies in human male testicular cells.Cytogenet Genome Res. 2004; 106: 39-42Crossref PubMed Scopus (16) Google Scholar) demonstrated that cold storage of testicular tissue on ice at 4°C for 2 days had no effect on the quality of preparations or on chromosome pairing or recombination. Lyrakou et al. (10Lyrakou S. Mantas D. Msaouel P. Baathalah S. Shrivastav P. Chrisostomou M. et al.Crossover analysis using immunofluorescent detection of MLH1 foci in frozen-thawed testicular tissue.Reprod Biomed Online. 2007; 15: 99-105Abstract Full Text PDF PubMed Scopus (7) Google Scholar) reported that long-term cryopreservation had no effect on meiotic recombination and synapsis based on comparisons with the published data from fresh samples from different patients. However, significant inter- and intraindividual variations in the mean frequency of meiotic recombination have been repeatedly reported (11Codina-Pascual M. Oliver-Bonet M. Navarro J. Campillo M. García F. Egozcue S. et al.Synapsis and meiotic recombination analyses: MLH1 focus in the XY pair as an indicator.Hum Reprod. 2005; 20: 2133-2139Crossref PubMed Scopus (48) Google Scholar, 12Sun F. Trpkov K. Rademaker A. Ko E. Martin R.H. Variation in meiotic recombination frequencies among human males.Hum Genet. 2005; 116: 172-178Crossref PubMed Scopus (59) Google Scholar). Thus, the effect of cryopreservation on meiotic recombination and synapsis in testicular tissues remains to be determined. In this study, the effects of cryopreservation on the progression of prophase I of meiosis, homologous recombination, and chromosome pairing during early meiosis were carefully examined using immunocytogenetic methods. Fresh and cryopreserved testicular tissues from the same men were immunolabeled using antibodies against the synaptonemal complex (SC) axial element protein SCP3 (13Schalk J.A. Dietrich A.J. Vink A.C. Offenberg H.H. van Aalderen M. Heyting C. Localization of SCP2 and SCP3 protein molecules within synaptonemal complexes of the rat.Chromosoma. 1998; 107: 540-548Crossref PubMed Scopus (83) Google Scholar) and MLH1 (a DNA mismatch repair protein that marks recombination sites) (14Baker S.M. Plug A.W. Prolla T.A. Bronner C.E. Harris A.C. Yao X. et al.Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over.Nat Genet. 1996; 13: 336-342Crossref PubMed Scopus (676) Google Scholar). Five testicular samples were obtained: one from a man who underwent orchiectomy for testicular cancer (aged 39 years) and one from each of four prostate cancer patients (aged 62–69 years) from the First Affiliated Hospital of Anhui Medical University. All patients had histologically normal spermatogenesis. Informed consent was obtained from the patients, and the study was approved by the Institutional Review Board at the University of Science and Technology of China. Testicular samples were cut into equal-sized pieces of approximately 3 × 3 × 3 mm in phosphate-buffered saline (PBS) after being transported on ice to the laboratory. One fragment was processed immediately for immunofluorescent analysis, and the other fragments were processed for freezing. Washed testicular tissues were placed into sterile 1.8-mL cryotubes (Greiner Bio-One, Selinger, Germany) containing 0.5–1 mL of cryoprotectant medium (80% Dulbecco's modified Eagle's medium, 10% dimethyl sulfoxide, 10% fetal bovine serum, and 100 U/mL penicillin-streptomycin) for 30 minutes at room temperature (RT) before being placed into a freezing container (Nalgene, Rochester, NY). Then the cryotubes were transferred to a −80°C freezer. After gradual cooling, the cryotubes were taken out of the container and stored at −80°C until further use. To thaw the samples, the cryotubes were taken out of the freezer and rapidly dipped into a 37°C water bath and agitated for 5 minutes. The thawed testicular materials were expelled into a Petri dish and washed in PBS 3 times for 10 minutes each at RT. SC spreads of spermatocytes were prepared using the technique described by Judis et al. (15Judis L. Chan E.R. Schwartz S. Seftel A. Hassold T. Meiosis I arrest and azoospermia in an infertile male explained by failure of formation of a component of the synaptonemal complex.Fertil Steril. 2004; 81: 205-209Abstract Full Text Full Text PDF PubMed Scopus (57) Google Scholar). Briefly, the fresh and frozen-thawed testicular samples were gently teased apart into a loose aggregate in hypoextraction buffer (30 mM Tris, pH 8.2; 50 mM sucrose; 17 mM citric acid; 5 mM ethylenediaminetetraacetic acid; 2.5 mM 1,4-dithiothreitol; 1 mM phenylmethylsulfonal fluoride, pH 8.2–8.4) and incubated at RT for 1 hour. After incubation, a portion of loose tubules was shredded into small pieces in 20 μL of 100 mM sucrose on a microscope slide. A 10-μL drop of the germ cell/sucrose mixture was transferred and spread evenly over a second slide covered with 1% paraformaldehyde solution (pH 9.2) containing 0.2% Triton X–100. Slides were placed in a humid chamber overnight and then air-dried. After air-drying, the slides were immersed in a 0.04% solution of PhotoFlo (Kodak 200 solution; Kodak, Rochester, NY) in water for 4 minutes and then incubated in ADB (1% normal donkey serum, [Jackson ImmunoResearch, West Grove, PA]; 0.3% bovine serum albumin, and 0.005% Triton X–100 in tris buffered saline [TBS] in a humid chamber for 30 minutes at RT. After incubation, 40 μL of primary antibody: rabbit anti-SCP3 (1: 3000; gifted from Christa Heyting), human anti-CREST (1: 1000; Immunovision, Springdale, OH), and mouse anti-MLH1 (1: 60; BD Pharmingen Biosciences, San Diego, CA) were added to each slide, a coverslip was sealed in place with rubber cement, and slides were incubated overnight in a humid chamber at 37°C. On the following day, slides were washed in TBS 3 times for 10 minutes each and incubated in ADB at 4°C for at least 6 hours, and 40 μL of the secondary antibody mixture were applied: Alexa 555 donkey anti-rabbit (Molecular Probes, Carlsbad, CA), Alexa 488 goat anti-mouse (Molecular Probes), and 1-amino-4-methylcoumarin-3-acetic acid donkey anti-human (Jackson Immunoresearch). Slides were incubated at 37°C for 1.5 hours and then were washed 3 times in TBS for 10, 20, and 30 minutes, respectively. Finally, 20 μL of vectashield (Vector Laboratories, Burlingame, CA) was applied, and a coverslip was sealed in place. An epifluorescence microscope (Olympus BX61; Olympus, Tokyo, Japan) and Image Pro-Plus version 5.1 software (Median Cybernetics, Bethesda, MD) were used for cell evaluation and image capturing. In each pachytene cell captured and analyzed, the X,Y pair was identifiable, the number of bivalents was correct, and SCs were not obviously stretched, severely twisted, or overlapped with other SCs. The number of crossovers was assessed by counting distinct pachytene MLH1 foci that were localized on an SC. For meiotic recombination analysis, the mean number of MLH1 foci, the mean number of SCs with 0, 1, 2, 3, 4, or 5 foci per cell, and the presence of an MLH1 focus in the X,Y pair were calculated. An assessment of gaps (discontinuities) and of splits (unpaired lateral elements) in the SCs in bivalents was used to evaluate synapsis. Statistical analysis was performed using SPSS 13.0 software (SPSS Inc., Chicago). The χ2-test was used for comparisons between fresh and frozen tissue groups. The Student's t-test and Mann-Whitney U-test were used for comparisons of means between fresh and frozen tissue groups. For other quantitative comparisons, analysis of variance was used. The different stages of meiotic prophase I (leptotene, zygotene, pachytene, and diplotene stages) could be clearly characterized by immunofluorescent techniques. The percentage of prophase substages in fresh and frozen samples from each patient was scored. The freeze-thaw procedure did not result in a significant difference in the frequency of leptotene (20% vs. 15%, 28% vs. 28%, 17% vs. 18%, 24% vs. 22%, 27% vs. 25%), zygotene (1% vs. 2%, 6% vs. 6%, 0 vs. 0, 3% vs. 2%, 4% vs. 3%), and pachytene (80% vs. 85%, 66% vs. 66%, 83% vs. 79%, 73% vs. 76%, 69% vs. 71%) cells compared with fresh samples from the same patients. The overall mean frequencies of leptotene, zygotene, and pachytene cells in frozen samples were 23%, 3%, and 74%, respectively, with no significant difference from those observed in fresh samples (22%, 3%, and 74%, respectively). Diplotene cells were rare and seen with a proportion of 1% in the meiotic prophase substages in the fresh samples of case number 070804. Furthermore, SC morphology was well preserved and did not reveal any injuries at different stages of meiosis I after a freeze-thaw cycle. This is consistent with and extends previous studies, which demonstrated that testicular samples show no detectable morphological or structural changes, with well-preserved seminiferous tubules and interstitial cells present after freezing-thawing when compared with fresh samples (7Keros V. Hultenby K. Borgström B. Fridström M. Jahnukainen K. Hovatta O. Methods of cryopreservation of testicular tissue with viable spermatogonia in pre-pubertal boys undergoing gonadotoxic cancer treatment.Hum Reprod. 2007; 22: 1384-1395Crossref PubMed Scopus (227) Google Scholar, 16Kvist K. Thorup J. Byskov A.G. Høyer P.E. Møllgård K. Yding Andersen C. Cryopreservation of intact testicular tissue from boys with cryptorchidism.Hum Reprod. 2006; 21: 484-491Crossref PubMed Scopus (123) Google Scholar, 17Prabakaran S.A. Agarwal A. Sundaram A. Thomas A.J. Sikka S. Cryosurvival of testicular spermatozoa from obstructive azoospermic patients: the Cleveland Clinic experience.Fertil Steril. 2006; 86: 1789-1791Abstract Full Text Full Text PDF PubMed Scopus (8) Google Scholar). The comparison of recombination frequency between frozen-thawed and fresh testicular samples from five men is shown in Table 1. A total of 833 cells were analyzed. The mean number of MLH1 foci per cell observed in frozen-thawed samples was 46.1 ± 4.1, 47.3 ± 4.6, 52.1 ± 4.9, 47.7 ± 3.7, and 47.3 ± 3.5, ranging from 37 to 61 for the five individuals. In the fresh sample, means of 47.1 ± 3.7, 48.8 ± 4.0, 52.7 ± 4.4, 47.2 ± 3.2, and 47.6 ± 4.2 foci per cell were observed, respectively, and the number of MLH1 foci ranged from 36 to 62. Similarly, there was no significant difference in the recombination frequency between frozen samples and their fresh controls. As described elsewhere, with MLH1 foci in men with normal spermatogenensis (10Lyrakou S. Mantas D. Msaouel P. Baathalah S. Shrivastav P. Chrisostomou M. et al.Crossover analysis using immunofluorescent detection of MLH1 foci in frozen-thawed testicular tissue.Reprod Biomed Online. 2007; 15: 99-105Abstract Full Text PDF PubMed Scopus (7) Google Scholar, 11Codina-Pascual M. Oliver-Bonet M. Navarro J. Campillo M. García F. Egozcue S. et al.Synapsis and meiotic recombination analyses: MLH1 focus in the XY pair as an indicator.Hum Reprod. 2005; 20: 2133-2139Crossref PubMed Scopus (48) Google Scholar), significant interindividual variation was also observed in the present data. After a freeze-thaw cycle, 76.1%, 73%, 79%, 63.8%, and 78.3%, respectively, of each patient's cells had an MLH1 focus in the XY pair, which was not significantly different from fresh samples (80.7%, 68%, 68%, 67.7%, and 73.2%, respectively). There were no significant differences observed between frozen and fresh samples in autosomal SCs with 0–5 foci per cell (Table 1).Table 1Comparisons of the frequency of MLH1 foci per pachytene cell, autosomal bivalents with 0–5 MLH1 foci, percentage of cells with an MLH1 focus in the X,Y pair, and frequency of gaps/splits between fresh and frozen-thawed human testicular samples from the same patients.MLH1 foci per cellMean no. of autosomal SCs on which the no. of foci isSample no. (age in years)No. of days in cryopreservation, fresh, frozenNo. of cells analyzedMean ± SDRange012345Cells with MLH1 foci in XYCells with gaps,aGaps represent discontinuities in the SCs. %Cells with splits,bSplits represent unpaired regions in the SCs. %070615 (39): Fresh08847.1 ± 3.736–550.13.912.84.40.70.180.715.910.2 Frozen148846.1 ± 4.138–550.14.612.34.10.70.176.118.26.8070802 (65): Fresh010048.8 ± 4.038–590.13.511.95.21.20.068.06.03.0 Frozen4610047.3 ± 4.637–580.13.612.15.21.00.073.010.01.0070804 (69): Fresh010052.7 ± 4.439–620.02.810.56.61.80.268.021.00.0 Frozen4110052.1 ± 4.938–610.02.811.16.11.70.279.023.03.0071023 (62): Fresh08947.2 ± 3.240–560.03.812.65.00.60.067.710.11.1 Frozen1675847.7 ± 3.741–560.03.712.35.20.70.163.812.11.7071024 (68): Fresh05447.6 ± 4.238–560.14.211.25.50.90.173.213.40.0 Frozen1685647.3 ± 3.539–550.24.011.65.50.60.178.319.60.0Mean: Fresh43148.8 ± 4.436–620.13.611.85.31.00.171.213.23.0 Frozen40248.6 ± 4.637–610.13.711.85.21.00.174.616.60.2.8a Gaps represent discontinuities in the SCs.b Splits represent unpaired regions in the SCs. Open table in a new tab Gaps were common and splits were rare in these patients' samples (Table 1). After freezing thawing, a mean percentage of 16.6% cells with gaps and 2.8% with splits were seen, which is not significantly different from fresh samples (gaps, 13.2%; splits, 3.0%). Gaps and splits have been observed at much higher frequencies in testicular biopsies from subfertile or infertile males (18Vidal F. Templado C. Navarro J. Brusadin S. Marina S. Egozcue J. Meiotic and synaptonemal complex studies in 45 subfertile males.Hum Genet. 1982; 60: 301-304Crossref PubMed Scopus (32) Google Scholar, 19Lange R. Krause W. Engel W. Analyses of meiotic chromosomes in testicular biopsies of infertile patients.Hum Reprod. 1997; 12: 2154-2158Crossref PubMed Scopus (36) Google Scholar, 20Sun F. Oliver-Bonet M. Liehr T. Starke H. Ko E. Rademaker A. et al.Discontinuities and unsynapsed regions in meiotic chromosomes have a trans effect on meiotic recombination of some chromosomes in human males.Cytogenet Genome Res. 2007; 119: 27-32Crossref PubMed Scopus (6) Google Scholar). Our gap-bearing cells appeared at a significantly lower frequency than previously reported: 13.2% on average in our five fresh samples compared with 35% reported by Sun et al. (12Sun F. Trpkov K. Rademaker A. Ko E. Martin R.H. Variation in meiotic recombination frequencies among human males.Hum Genet. 2005; 116: 172-178Crossref PubMed Scopus (59) Google Scholar), 32.2% by Lyrakou et al. (10Lyrakou S. Mantas D. Msaouel P. Baathalah S. Shrivastav P. Chrisostomou M. et al.Crossover analysis using immunofluorescent detection of MLH1 foci in frozen-thawed testicular tissue.Reprod Biomed Online. 2007; 15: 99-105Abstract Full Text PDF PubMed Scopus (7) Google Scholar), and 50% from Codina-Pascual et al. (11Codina-Pascual M. Oliver-Bonet M. Navarro J. Campillo M. García F. Egozcue S. et al.Synapsis and meiotic recombination analyses: MLH1 focus in the XY pair as an indicator.Hum Reprod. 2005; 20: 2133-2139Crossref PubMed Scopus (48) Google Scholar). However, as reported in the published literature (12Sun F. Trpkov K. Rademaker A. Ko E. Martin R.H. Variation in meiotic recombination frequencies among human males.Hum Genet. 2005; 116: 172-178Crossref PubMed Scopus (59) Google Scholar), the variation in the frequency of gaps does not seem to be related to or affect the mean recombination frequency in our results. This study demonstrates that cryopreservation of testicular tissues did not alter meiotic recombination frequency, synapsis, or SC integrity. Thus, cryopreservation of human testicular tissue may be a suitable procedure for the preservation of fertility in young boys with cryptorchidism, for cancer patients before radiotherapy and chemotherapy, and for other groups of adult patients with infertility. The authors thank Professor Christa Heyting, Wageningen University, for the kind gift of the SCP3 antibody, and Qingling Yang and Liangwen Zhong, University of Science and Technology of China, for preparing and analyzing SC samples. We are grateful for critical comments on this manuscript by Professor Renée H. Martin, University of Calgary, and Professors Fei Sun and Wei Shen, University of Science and Technology of China. Special thanks to Evelyn Ko, University of Calgary, for proofreading the manuscript." @default.
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- W2024659558 cites W2030599485 @default.
- W2024659558 cites W2035668626 @default.
- W2024659558 cites W2038510092 @default.
- W2024659558 cites W2043892040 @default.
- W2024659558 cites W2050057050 @default.
- W2024659558 cites W2051447424 @default.
- W2024659558 cites W2061648581 @default.
- W2024659558 cites W2067974441 @default.
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- W2024659558 cites W2126449843 @default.
- W2024659558 cites W2138261954 @default.
- W2024659558 cites W2140218030 @default.
- W2024659558 cites W2166656985 @default.
- W2024659558 cites W2169633067 @default.
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