Annals of RSCB Vol. XV, Issue 2
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1 COMPLEX CYTOGENETIC AND MOLECULAR EVALUATION IN MEN WITH OLIGO/AZOOSPERMIA IN THE WESTERN PART OF ROMANIA Cristina Gug 1, 2, Delia Huţanu 3, L. Tămaş 4, Anda Alexa 4, A. Anghel 4 1 GENETICS DEPARTMENT, UNIVERSITY OF MEDICINE AND PHARMACY VICTOR BABES, TIMISOARA, ROMANIA, 2 GENETIS MEDICAL CENTER DR. CRISTINA GUG, TIMISOARA, ROMANIA, 3 WEST UNIVERSITY, CHEMISTRY-BIOLOGY-GEOGRAPHY ACULTY, DEPARTMENT OF BIOLOGY, TIMISOARA, ROMANIA, 4 BIOCEMISTRY DEPARTMENT, UNIVERSITY OF MEDICINE AND PHARMACY VICTOR BABES, TIMISOARA, ROMANIA Summary The objective of this study was to evaluate the contribution of chromosomal anomalies to decreased fertility in men. In order to investigate the etiology of infertility in our population and to assess the karyotype in a group of infertile couples and individuals with fertility problems, 900 male with different clinical diagnoses of sterility and infertility were cytogenetically analysed. To each patient cytogenetic analisys form lymphocytes was performed using the standard method and GTG banding. Y chromosome microdeletions were identified by multiplex PCR, using a commercial kit and CFTR mutations were detected by ARMS-PCR with Elucigene CF29 kit. The overall frequency of major chromosomal aberrations was 4,77%, (44:900), which suggests that fertility or sterility problems in this population are due to chromosomal aberrations. In one case (from a group of 35 tested patients) Y chromosome microdeletions were identified (2.85%) and CFTR mutations were found in 4 cases with heterozygous genotypes in 30 tested patients. These results could indicate an increased tendency to meiotic sex chromosome non-disjuction in humans. Key words: Chromosomal aberration, Y microdeletions, CFTR mutations. dr.cristina.gug@gmail.com Introduction Infertility is an important health problem which affects 10-15% families. Among male population the chromosomal abnormalities are considered the main genetic factor, affecting 3% from general population with infertility, 7% from male population with oligospermia and 15% from male population with azoospermia. The second cause of male infertility is Y chromosome microdeletions, found in Yq11 region. The Y chromosome encloses genes involved in human spermatogenesis. These genes are located in the AZF (azoospermia factor) zone, in three areas quoted as AZFa, AZFb, AZFc. Another genetic cause of infertility is represented by CFTR gene mutations associated with low sperm count values in patients without a typical cystic fibrosis phenotype. The present study investigated the genetic causes (cytogenetic and molecular) of male infertility, in order to determine the etiology of the problem, provide the couple with the best genetic advise, establish the best assisted reproductive technique for the couple. 48
2 Material and methods The study group has 900 men from the west part of Romania, with different clinical diagnoses of infertility and sterility and abnormal sperm count values. The patients found with deferent ducts obstruction were excluded from this study. The mean age of the study group was 34 years (between 18 and 54 years of age). For each patient genetic counseling was provided, before and after genetic testing. Male patients were analyzed if oligozoospermia (sperm count below 10x10 6 /ml), azoospermia, hypogonadism or unexplained sterility was diagnosed. Some patients were referred with a clinical diagnosis of Klinefelter syndrome or gynecomastia. The karyotype analyses were performed on preparations made from short-term lymphocyte cultures and GTG-banded metaphase chromosomes. Standard methods employing hypotonic treatment before fixation with methanol acetic acid and slide preparation by the air-drying technique were used (Moorhead et al. 1960). 20 metaphases were evaluated and a minimum of 1 karyotpe/cell clone was made. If one aneuploid cell was found, at least an additional 50 mitoses were analyzed. The biological sample was genomic DNA, extracted from whole blood, on EDTA with QIAamp DNA Blood Mini Kit (QIAGEN). For genotyping, we utilized the Y Chromosome Deletion Detection System, Version 2.0 (PROMEGA), which analyses 20 specific sequences of the Y chromosome (SY 14 SRY gene, SY 81 - DYS 271 gene, SY 86 DYS148 gene, SY 84 DYS 273 gene, SY 182- KALY gene, SY 121- DYS 212 gene, SYPR3- SMCY gene, SY 124- DYS 215 gene, SY 127- DYS218 gene, SY 128- DYS219 gene, SY 130- DYS 221 gene, SY 133- DYS 223 gene, SY 134- DYS 224 gene, SY 145- DYF51S1 gene, SY 152- DYS 236 gene, SY 242- DAZ gene, SY 208- DAZ gene, SY 254- DAZ gene, SY 255- DAZ gene, SY 157- DYS 240 gene) (fig1). The presence of the 20 sequences was analyzed through agarose gel electrophoresis. Fig. 1. Y Chromosome Map Worksheet The region located on the long arm (q) of the Y Chromosome, that controls spermatogenesis is named Azoospermia factor (AZF). This chromosomal region contains all the genes that play an important role in spermatogenesis (DAZ genes) and includes all that twenty analyzed sequences. CFTR mutations were identified by ARMS-PCR (amplification refractory mutation system) using a commercial kit (Elucigene TM CF29) which can detect 29 CFTR mutations. Results The karyotype was made from periferic blood for each case. Cytogenetic constitutional abnormalities were identified in 44 cases (4.77%) (Table I). Chromosomal changes (aberrations) which were identified in infertile men include: 1. Sex chromosome abnormality in 11 cases (fig 2-3) 2. Balanced chromosomal translocation in12 cases (fig 5) 49
3 3. Robertsonian translocation in 5 cases (fig 4) 4. Chromosome inversion 1s (fig 8) 5. Duplication in 2 cases 6. Y deletion in one case 7. Combined chromosome abnormality in 2 cases (fig 6-7) Carrier of Robertson s translocation creates unbalanced gametes with theoretical risk that offspring can be: 1/3 healthy with normal karyotype, 1/3 healthy carrier of same translocation as parent and 1/3 will suffer unbalanced karyotype, therefore will be affected (spontaneous miscarriages, birth of affected alive or dead child). Fig. 2. Karyotype: 47,XXY Sex chromosome abnormalites include aneuploidies such as XXY (fig 2) and XXYY (fig 3), which are characterized by the production of germ cells that are meiotically incompetent or partially incompetent, and give rise to a more or less severe meiotic arrest (Blanco et al., 2001) or structural rearrangements. Fig. 4. Karyotype: 45,XY,-13,- 14,+der,t rob (13;14) Most common type of Robertson s translocation occurring in human is translocation among chromosomes 13 and 14. Carrier of Robertson s translocation has got 45 chromosomes and there is no physical or mental defect. In our t rob (13;14) (fig 4) lot we found the translocation in 2 patients from the same family (father and son) out of a total of 4. Fig. 3. Karyotype: 48, XXYY 50
4 Table I: Identified chromosomal abnormalities type Constitutional chromosome abnormality Sex chromosome abnormality Robertsonian translocation Balanced chromosomal translocation Chromosome inversion Deletion Duplication Combined chromosome abnormality Karyotype 47,XXY 48, XXYY 46,XX 47,XXY/46,XY 46,XY/45,X t rob (13;14) (fig 4) t rob (13;22) t(1;5)(q23;p12) (fig 5) t(2;21)(q34;p11.2) t(2;17)(p22;q21), t(3;14)(q25.2;q32.2) t(4;16)(q34;q24) t(7;14)(q35;q12) t(7;15)(q14;q27) t(7;18)(p13;q11) t(16;18)(p11;p11) t(15;19)(p11;q12) inv(9) (p11;q13) del(y) dup(16)(q12) dup(8)(p22) t(7;10)(p22;p12.1)+t(9;14)(q12;q 23) t(9;15)(q21.2;p11,2)+inv(9) No. of cases 4 cases 2 cases 3 cases 1s (20,45%) 4 cases in 3 families 5 cases (11,36%) 3 cases in one family in 2 generations 12 cases (27,27%) 1s 1s (20,45%) (2,27%) 2 cases (4,54%) 2 cases (4,54%) Total 44 cases (100%) 51
5 Male carriers of balanced translocation (fig 5-7) are not physically affected, but produce 4 variable types of the gametes. Fertilization of the egg cell of translocation carrier by a gamete of a partner with normal karyotype creates 4 types of embryos. First two types embryos with normal karyotype and embryo with balanced translocation same as parent ensure birth of normal, healthy child and other two types result in embryos with unbalanced karyotype, which can cause implantation failure or a spontaneous miscarriage or child is born affected. Carrier of inversion inv(9) (fig 7-8) is usually not affected in its genotype, situation we have encountered in our study. Fig. 7. Karyotype 46,XY,t(9;15)(q21.2;p11,2),inv(9) Fig. 5. Karyotype: 46,XY,t(1;5)(q23;p12) Fig. 8. Karyotype: 46,XY,inv(9) Fig. 6. Karyotype: 46,XY,t(7;10)(p22;p12.1),(9;14) (q12;q23) The chromosome with an inversion has a sequence of genes altered compared to its previous succession in the original chromosome. Carrier of inversion has got an increased risk of reproductive losses (spontaneous miscarriages, stillborn children, children born with physical and intellectual affect). 35 patients were tested for chromosome Y microdeletions (Fig 9). Males, carriers of balanced translocations, usually have reproductive disorders oligospermia to azoospermia (small number to absence of sperms in ejaculate). 52
6 Fig. 9. Y chromosome microdeletions detection - electrophoregrame - normal aspect Mutations were found in only one case (2,85%). The subject with microdeletions was azoospermic. The cases in which electrophoretic bands were missing (negative signal) were repeated at least two times to confirm the deletion of a given marker. Six microdeletions were identified, two for each of A, B and D multiplexes (Fig. 10): Multiplex A - 2 loci: SY 254 (gene DAZ) and SY 157 (DYS 240 gene), Multiplex B - 2 loci: SY 242 (DAZ gene) and SY 208 (DAZ gene), Multiplex D - 2 loci: SY 255 (DAZ gene) and SY 152 (DYS 236 gene). Fig. 10. The Chromosome Y microdeletions analysis showed 6 microdeletions. The microdeletions are consecutive and fill almost completely the AZFc region from Yq Fig. 11. Heterozygous genotype F508/N CFTR mutations were found in 4 out of 30 patients (13,33%). The following mutations were identified in 4 heterozygous genotypes: F508 (n=2) (Fig. 11), G542X (n=1) and I148T (n=1). Discussions The prevalence of chromosomal aberrations in 900 persons with different clinical diagnoses of sterility and fertility (4,77%) is considerably greater than that in the general population (less than 1%) (Nielsen, Wohlert, 1991) and is comparable to other reports ( %) (Maione et al., 1995). Aberrant karyotypes occured in 18% of the couples undergoing an assisted reproductive (Mau et al., 1997). The overall prevalence of major chromosomal aberration was 4,77%, and this finding suggests that defective reproductive success is a major symptom of the chromosomal aberration. The prevalence of chromosomal abnormalities in infertile men was 5 times higher than expected in the normal population (Nielsen, Wohlert, 1991). The consistency of results seems to justify a diagnostic chromosomal analysis in subfertile men (sperm count below 10x10 6 /ml). The only phenotypic manifestation in some chromosomal aberrations may be disturbed spermatogenesis (which does
7 not occur in oogenesis). Besides major chromosomal aberrations, large blocks of duplicated heterochromatin can be a factor disturbing reproduction (Buretic- Tomljanovic et al., 1997). The most commonly involved chromosomal aberrations in subfertile and sterile males and in females are sex chromosomes (Table I, fig 2, fig 3). There are studies (Templado C., et al., 2005) which showed that chromosome 9 has a high susceptibility to be broken and even more, the breakpoints are located in 9q, between the centromere and the 9qh+ region in 50% of cases. In our study, 11 patients presented chromosome 9 inversions (20,45% of all identified abnormalities). These findings are consistent with the high incidence (~1%) observed in the general population of pericentric inversion inv(9)(p11q13). Carriers of structural reorganizations produce unbalanced spermatozoa, and risk having children with duplications and/or deficiencies. In some cases, this risk is considerably lower or higher than average. These patients also show increased diploidy, and a higher risk of producing diandric triploids. Meiotic disorders are frequent in infertile males, and increase with severe oligoasthenozoospemia (OA) and/or high follicle stimulating hormone (FSH) concentrations. These patients produce spermatozoa (Guraya, 1987) with autosomal and sex chromosome disomies, and diploid spermatozoa. Their contribution to recurrent abortion depends on the production of trisomies, monosomies and of triploids. The most frequent sperm chromosome anomaly in infertile males is diploidy, originated by either meiotic mutations or by a compromised testicular environment (Checiu, 2003, Crăciun, 1999). In karyotyping studies, the mean disomy frequency in human sperm is 0.03% for each of the autosomes, and 0.11% for the sex chromosomes, lower than those reported in sperm nuclei by FISH studies using a similar methodology (0.09% and 0.26%, respectively). Both types of studies coincide in that chromosome 21 and sex chromosomes have a greater tendency to suffer segregation errors than the rest of the autosomes (Templado, et al., 2005). Some males with severe oligospermia have a significant deletion of part or whole long limb of Y chromosome. The most frequent microdeletions are found in the AZFc region. The complete deletion of AZFc region (including DAZ gene) is the most frequent known cause of infertility in men. Genetic abnormalities were determined in 20% of azoospermic cases, which is similar to other reported frequencies for infertility cases (15% - 30%) (Imken et al., 2007; Ferlin et al., 2005). In 6,1% cases of men with sperm concentration less than 1x 10 6 /ml Y chromosome microdeletions were detected, comparing to 8,5% in azoospermic men. The clinical correlation of spermatogenic impairment with different AZF region deletions may provide useful information for genetic counseling of infertile couples. AZFa the deletions in this region appear rarely, and if they occur, they are associated with the most severe phenotype: the complete absence of spermatogenesis AZFb the complete deletion of this region brings to zero the possibility of sperm cells maturation. AZFc this region is the most frequently associated with Y microdeletions. The complete deletion of the AZFc region (including DAZ gene) is the most common cause of male 54
8 infertility. A positive test for AZFc deletion on oligozoospermic patients suggests that sperm counts would be dropping in time, and hence cryopreservation upon early diagnosis has been suggested. AZFd the deletions in this region were associated with mild oligozoospermia or even normospermia. Although the severity of phenotype in patients with this type of deletions is directly correlated with the dimension of the deleted segment, even small deletions may be associated with infertility. The presence of deletions was correlated with patient s sperm concentration and clinical picture (hormonal parameters). Studies of large groups of patients with CFTR mutations and polymorphic variants revealed that congenital bilateral absence of the vas deferens (CBAVD) which is a genital form of cystic fibrosis (CF) is responsible for 2%-6% of male infertility cases (Cuppens and Cassiman, 2004). Conclusions An abnormal sperm count values found is compulsatory followed by genetic investigations (chromosomal and molecular), in order to give a correct diagnosis and to establish an adequate therapeutical conduct. Genetic testing is recommended for the identification of azoospermia etiology and for choosing ART strategies. Also, in selected cases, prenatal diagnosis can be performed. We believe that the majority of infertility cases, especially severe oligospermic and azoospermic cases need a cytogenetic analysis besides molecular techniques to reveal the existence of any genetic abnormalities. Detailed cytogenetic analyses of males with decreased reproductive fitness are essential for predicting the success of assisted reproductive procedures. In conclusion, cytogenetic and molecular studies should be performed in order to obtain reliable genetic information for genetic counseling of primary infertile men. Y chromosome microdeletions diagnosis is useful in decision making for assisted reproductive techniques because the association between some deletions and residual spermatogenesis capacity has been proven. References Blanco, J., Egozcue, J.., Vidal, F., Meiotic behavior of the sex chromosomes in three patients with sex chromosome anomalies assessed by fluorescent in situ hybridization. Hum. Reprod. 16, , Blanco, J., Egozcue, J., Vidal, F., meiotic behaviorof the sex chromosomes in three patients with sex chromosome anomalies assessed by fluorescent in situ hybridization. Hum. Reprod. 16, , Buretic-Tomljanovic, A, Radojcic Badovinac, A., Vlastelic, I., Randic, L.J.: Quantitative analysis of constitutive heterochromatin in couples with fetal wastage. Am. J. Reprod. Immunol.; 38, , Buwe, A., Guttenbach, M., Schmid, M. Effect of paternal age on the frequency of cytogenetic abnormalities in human spermatozoa Cytogenet. Genome Res. 111, , Checiu, I.: Embriologie, Curs, Ed. Mirton, Crăciun, C., Florea, A., Dragoş, N., Ardelean, A.: Introduction to cell and Molecular Biology, Cluj University Press, Cuppens, H., Cassiman, J.J.: CFTR mutations and polymorphisms in male infertility, Int. J. Androl., 27, , Egozcue, S.: Human male infertility: chromosome anomalies, meiotic disorders, abnormal spermatozoa and 55
9 recurrent abortion Hum. Reprod. Update 6, , Egozcue, J., Sarrate, Z., Codina-Pascual, M.: Meiotic abnormalities in infertile males Cytogenet. Genome Res., 3-4, , Ferlin, A., Tessari, A., Ganz, F., Marchina, E., Barlati, S., Garolla, A., Engl, B., Foresta, C.: Association of partial AZFc region deletions with spermatogenic impairment and male infertility, J. Med. Genet., 42, , Guraya, S.S.: Biology of Spermatogenesis and Spermatozoa in Mammals, Springer- Verlag, Berlin, Imken, L., El Houate, B., Chafik, A., Nahili, H., Boulouiz, R., Abidi, O., Chadli, E., Louanjli, N., Elfath, A., Hassar, M., McElreavey, K., Barakat, A., Rouba, H.: AZF microdeletions and partial deletions of AZFc region on the Y chromosome in Moroccan men, Asian J. Andro.l., 9, 674-8, Maione, S., Lamberti, L., Alovisi, C., Armellino, F.: Retrospective study of couples with a history of recurrent spontaneous abortion. Acta Eur. Fertil., 26, , Martin, R.H.: Cytogenetic determinants of male fertility Hum. Reprod. Update, 14, , 2008 Mau, U.A., Backert, I.T., Kaiser, P., Kiesel, L.: Chromosomal findings in 150 couples referred for genetic counseling prior to intracytoplasmic sperm injection. Hum. Reprod.; 12: , Moorhead, P.S., Nowell, P.C., Mellman, W.J., Battips, D.M., Hugerford, D.A.: Chromosome preparation of leukocytes cultured from human peripheral blood. Exper. Res., 20, , Nielsen, J., Wohlert, M.: Chromosome abnormalities among 34,910 newborn children: Results from 13-year incidence study in Arhus, Denmark. Hum. Genet.; 87, 81 83, Radojcic Badovinac, A., Buretic- Tomljanoic, A., Starcevic, N., Kapovic, M., Vlastelic, I., Randic, L.: Chromosome studies in patients with defective reproductive success AJRI; 44, , Templado, C., Bosch, M., Benet J.: Frequency and distribution of chromosome abnormalities in human spermatozoa, Cytogenet. Genome Res. 111, ,
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