Hum. Reprod. Advance Access originally published online on April 29, 2004
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Human Reproduction, Vol. 19, No. 6, 1345-1351,
June 2004
© 2004 European Society of Human Reproduction and Embryology
Sperm FISH studies in seven male carriers of Robertsonian translocation t(13;14)(q10;q10)
Unitat de Biologia Cel lular, Facultat de Ciències, Universitat Autònoma de Barcelona, 08193-Bellaterra, Barcelona, Spain
1 To whom correspondence should be addressed. e-mail: francesca.vidal{at}uab.es
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
BACKGROUND: Robertsonian translocation t(13;14) is one of the most common structural reorganization in humans, but meiotic segregation studies in these carriers are still limited. The segregation pattern of the chromosomes involved, the possible influence of the translocated chromosomes on the synapsis and disjunction of other chromosome pairs [interchromosomal effects (ICE)] and the rates of unbalanced spermatozoa produced still deserve attention, not only to obtain a better characterization of the meiotic behaviour of this reorganization, but also to offer carrier couples accurate genetic counselling. METHODS: Multicolour fluorescence in-situ hybridization was used to analyse the segregation of chromosomes 13 and 14 and the possible occurrence of ICE (on chromosomes 18, 21, 22, X and Y) in seven male carriers of a t(13;14)(q10;q10). RESULTS AND CONCLUSIONS: The individuals analysed showed a homogeneous segregation pattern, with a clear predominance of alternate segregations resulting in the production of normal/balanced spermatozoa (83–88.23%). A significant increase in the disomy rates for the sex chromosomes, which could be considered as a positive ICE, was observed in two of the carriers analysed.
Key words: FISH/interchromosomal effects/meiotic segregation/Robertsonian translocations/spermatozoa
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Constitutional chromosome abnormalities in humans are known to be directly related to human male infertility (Egozcue et al., 2000
). Structural chromosome rearrangements account for 
21% of all chromosome abnormalities (De Braekeleer and Dao, 1991; Pandiyan et al., 1996), and Robertsonian translocations are one of the more common structural reorganizations, with an incidence of 1.23/1000 newborns (Nielsen and Wohlert, 1991), of which 50% are de novo (Shaffer et al., 1992). Among them, the most frequently seen in the general population is t(13;14), with an incidence of 0.97/1000 newborn carriers (Nielsen and Wohlert, 1991), reaching frequencies up to nine times higher in infertile males (De Braekeleer and Dao, 1991).
The cause of the infertility in these individuals has been directly related to the meiotic process. In Robertsonian translocations, pairing of the reorganized chromosomes during prophase I gives rise to a trivalent structure (Vidal et al., 1982; Luciani et al., 1984). It is well known that this meiotic configuration tends to segregate in an alternate way (Sybenga, 1975), resulting in the production of normal or balanced spermatozoa. However, a certain percentage of unbalanced spermatozoa deriving from adjacent segregations are also produced, and could be responsible for the miscarriages or the severely affected aneuploid offspring frequently born to these carriers (Egozcue et al., 2000). Furthermore, the meiotic disturbances (synaptic anomalies) resulting from the behaviour of the reorganized chromosomes and of other bivalents could lead to different degrees of meiotic arrest, resulting in the oligozoospermia or azoospermia frequently observed in these patients.
Since cytogenetic studies of spermatozoa became possible, several groups have tried to analyse the meiotic behaviour of specific reorganizations and to evaluate the final production of balanced or unbalanced sperm, in order to offer patients accurate reproductive advice. Studies of the segregation products in Robertsonian (13;14) translocation carriers have been carried out since the early 1980s (Table I). The first studies used the human–hamster interspecific fertilization system (Pellestor et al., 1987; Martin, 1988), while Owaga et al. (2000) microinjected mouse oocytes with human sperm. In these three cases, the number of metaphases studied was considered low to reach a definitive conclusion (78, 117 and 45, respectively). More recently, using fluorescence in-situ hybridization (FISH), Escudero et al. (2000), Frydman et al. (2001) and Morel et al. (2001) found a percentage of normal or balanced spermatozoa ranging from 73.6% to 91% (Table I) in eight carriers studied.
|
On the other hand, the possible occurrence of interchromosomal effects (ICE), affecting the normal disjunction of other chromosome pairs not involved in any reorganization, has been a classical topic of discussion since it was suggested by Lejeune (1963)
. Several studies, including a wide spectrum of chromosome reorganizations, have been carried out to assess ICE by FISHing decondensed sperm nuclei in inversion carriers (Colls et al., 1997; Blanco et al., 2000; Pellestor et al., 2001; Anton et al., 2002), reciprocal translocations carriers (Van Hummelen et al., 1997; Blanco et al., 1998b; 2000; Martini et al., 1998; Cifuentes et al., 1999; Honda et al., 1999; Estop et al., 2000; Vegetti et al., 2000; Pellestor et al., 2001; Oliver-Bonet et al., 2002), and Robertsonian translocations (Rousseaux et al., 1995; Blanco et al., 2000; Morel et al., 2001; Vegetti et al., 2000; Baccetti et al., 2002). Results supporting or rejecting ICE have been obtained, and arguments about the behaviour of each particular reorganization or even about interindividual differences reported. Although the information obtained by collecting data from this diversity of chromosomal reorganizations is of interest, the selection of a representative number of each reorganization and the performance of the study in a single laboratory should allow one to reach more solid and homogeneous conclusions regarding the specific segregation behaviour of each structural reorganization and any possible ICE.
In this study, we used multicolour FISH on decondensed sperm nuclei to analyse the segregation of a t(13;14)(q10;q10) in seven male carriers, as well as the possible occurrence of ICE on chromosomes 18, 21, 22, X and Y.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Patients
Seven unrelated males, carriers of the Robertsonian translocation 45,XY,der(13;14)(q10;q10), consulting for infertility were studied. The patients’ age range was 30–37 years. In all cases abnormal seminal parameters were observed (World Health Organization, 1999
) (Table II). The patients gave their written informed consent to participate in the study, and the protocol used was approved by our institutional ethics committee.
|
Semen sample processing
Sperm samples were fixed in methanol:acetic acid (3:1) and spread on a slide. Sperm nuclei were decondensed by slide incubation in 5 mmol/l dithiothreitol, as previously detailed by Vidal et al. (1993)
.
FISH
A dual-colour FISH was used to determine the meiotic segregation of the chromosomes involved in the reorganization. A locus-specific probe for the 13q14 region (LSI 13, RB1, Spectrum Green; Vysis Inc., Downers Grove, IL, USA) plus a subtelomeric probe specific for the 14q region (TelVysion 14q, Spectrum Orange; Vysis Inc.) were used to identify all genotypes resulting from the different segregation modes.
In all patients, the occurrence of ICE for chromosomes 18, 21, 22 and for the sex chromosomes was also evaluated. Chromosomes 21 and 22 were assessed by dual-colour FISH using locus-specific probes for both chromosomes (LSI 21, 21q22.13-q22.2, Spectrum Orange/LSI 22, bcr, 22q11.2, Spectrum Green; Vysis Inc.) and a triple-colour FISH approach was used to analyse chromosomes 18, X and Y (CEP18, D18Z1, Spectrum Aqua/CEPX, DXZ1, Spectrum Green/CEPY, DYZ3, Spectrum Orange; Vysis Inc.).
The protocol for probes and sample denaturation, incubation and detection was as standardized in our laboratory in accordance to manufacturer’s instructions (Vysis Inc.), and sperm nuclei were counterstained with DAPI II solution (Vysis Inc.).
Analyses were carried out using an Olympus BX60 epifluorescence microscope equipped with filter sets for FITC, Texas Red, Aqua and DAPI/Texas Red/FITC. Previously described standard assessment criteria were followed for evaluation of the sperm nuclei (Blanco et al., 1996).
Data analysis
Control data for chromosomes 18, 21, 22, X and Y were derived from previously published results from our group (Blanco et al., 1997; 1998a; Soares et al., 2001). Furthermore, data resulting from the analysis of sperm samples from five normozoospermic men (World Health Organization, 1999) with an age range of 21–25 years, integrated in the control population of our laboratory, were used to assess the efficiency of the probes for the 13q14 region and for the 14q subtelomeric region.
Data obtained were analysed statistically using SigmaStat 2.0 (SPSS Inc., Chicago, IL, USA) under the advice of the statistical service of the Universitat Autònoma de Barcelona. Differences were considered to be statistically significant when P < 0.05.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Hybridization efficiency in sperm nuclei for the probes used in the evaluation of segregation was determined from data obtained from the five normozoospermic control donors. Percentages ranging from 97.99 to 99.44% corresponded to spermatozoa with one signal for each probe used (mean 98.66%) (Figure 1A). Disomy values for chromosome 13 ranged from 0 to 0.19% (mean 0.09%) and for chromosome 14 from 0 to 0.49% (mean 0.13%) (Figure 1B). The nullisomy rates for chromosome 13 ranged from 0.1 to 1.45% (mean 0.57%) (Figure 1C) and for chromosome 14 from 0 to 0.24% (mean 0.29%). A small percentage of diploid spermatozoa were also found with a mean average of 0.27%. The hybridization efficiency value obtained using a conservative approach (Blanco et al., 1996
) was 99.35%.
|
In Robertsonian translocation carriers, segregation analysis was ascertained in a total of 14 450 spermatozoa, ranging from 774 to 6128 cells evaluated per patient. Detailed FISH results are given in Table III.
|
In these patients, most spermatozoa resulted from a 2:1 alternate meiotic segregation, and the percentage of normal or balanced spermatozoa ranged from 83 to 88.23%. The proportion of unbalanced spermatozoa resulting from adjacent segregations accounted for 11.11 to 14.53% of the cells analysed. Taken as a group, all cases studied showed that the percentage rate of nullisomies for chromosomes 13 and 14 were statistically higher than the respective complementary disomies resulting from the adjacent segregation process (P < 0.001) (Table III). Individually, this difference was significant (P < 0.05) for chromosome 13 in patients 4, 5 and 6, and for chromosome 14 in patients 3 and 4 (Table III). No statistically significant differences (P > 0.05) were observed when comparing the percentages of disomies for chromosome 13 (2.46%) and for chromosome 14 (2.01%). The methodological approach used did not allow to differentiate between 3:0 segregations and diploid spermatozoa (both cases show two hybridization signals for the probes used). Unbalanced spermatozoa bearing this combination of signals accounted for 0–0.44% of the cells analysed. Spermatozoa with an unexpected combination of signals according to the theoretical segregations were classified as ‘other’, and corresponded to 0.52% of the total (range 0.08–2.27%) (Table III).
A total of 24 993 spermatozoa were analysed to evaluate the occurrence of ICE. Table IV shows the results from the evaluation of chromosomes 21 and 22, and Table V shows those for chromosomes 18, X and Y. No statistical differences were noted in the aneuploidy rates of chromosomes 18, 21 and 22 compared with controls (P > 0.05) (Blanco et al., 1997; 1998a; Soares et al., 2001). Sex chromosome disomies were statistically higher in patients 3 and 6 (0.94 and 1.34%, respectively; P < 0.001) than in controls (0.37%) (Blanco et al., 1997). The global results of the group studied reflected a significant increase (0.68%; P < 0.001) in the frequency of sex chromosome aneuploidies versus controls (Blanco et al., 1997).
|
|
FISH data from ICE studies were also used to evaluate the diploidy frequency. No statistical differences versus controls were noted (P > 0.05) (Blanco et al., 1997
). Furthermore, percentages of diploid sperm determined through the ICE study were equivalent (P > 0.05) to the percentage of spermatozoa scored as 3:0 or 2n (diploid) in the segregation analysis. |
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Despite the high incidence of Robertsonian translocation 13;14 in humans, FISH on decondensed sperm nuclei has previously been carried out in only a low number of patients, and in different laboratories (Table I); therefore, data about the meiotic segregation and rates of unbalanced spermatozoa produced are not totally homogeneous and are still limited. To our knowledge this is the first study in which seven male carriers of the Robertsonian translocation t(13;14)(q10;q10) have been analysed, representing the largest population of patients studied so far in the same laboratory.
The general results obtained in this work with a predominance of normal/balanced spermatozoa are in good agreement with previously reported studies (Table I), and also with the well-known configuration preferentially adopted by the reorganized chromosomes in metaphase I favouring an alternate segregation (Sybenga, 1975).
Our data support the existence of a similar meiotic behaviour of the reorganized chromosomes in the seven males analysed, reflected in the small range of spermatozoa resulting from an alternate segregation (83–88.23%) and spermatozoa deriving from adjacent segregations (11.11–14.53%). The wider range (73.6–91%) reported from other laboratories analysing the same reorganization (Escudero et al., 2000; Frydman et al., 2001; Morel et al., 2001) is probably related to technical aspects, such as the characteristics and the combination of the probes used (locus-specific, subtelomeric or whole-chromosome paints) and/or the particular scoring criteria established according the protocols used, rather than to inter-individual differences.
The expected 1:1 proportion in the percentage of disomic versus their complementary nullisomic spermatozoa deriving from adjacent segregations was not observed, and was even statistically different in patients 3, 4, 5 and 6. This discrepancy, also noted by other authors (Frydman et al., 2001; Morel et al., 2001; Honda et al., 1999), could be related to different and not mutually exclusive causes.
(i) First of all, the unavoidable limitations of the FISH technique itself. Certainly, hybridization failures scored as nullisomies could probably be responsible for the observed unexpected combination of signals classified as ‘others’ (Table III). However, one would expect hybridization failures to randomly affect all combinations of signals evaluated and, taking into consideration that the combination of probes used had a hybridization efficiency of 99.36%, a total of only 0.64% of sperm coming from all groups would be affected by this fact. Thus, it would not be accurate to attribute the discrepancies between the number of disomic versus their complementary nullisomic spermatozoa exclusively to hybridization failures.
(ii) The possible intervention of meiotic checkpoints should therefore also be considered. As is well known, any factor that delays anaphase (erratic chromosomes, lack of tension, etc.) may produce an arrest of the division cycle leading the cell into apoptosis, as described in male mice carriers of Robertsonian translocation (Eaker et al., 2001). This fact could explain the oligozoospermia present in most carriers of chromosome reorganizations. However, if the cell is capable of completing the division process, the result may be the production of aneuploid or diploid spermatozoa. In these situations, as suggested by Honda et al. (1999), cell maturation arrest would be specially stronger against disomic cells, thus resulting in the observed increased proportion of nullisomies versus disomies.
As expected, and taking into consideration the similar size of the chromosomes involved in the reorganization and the theoretical number and location of chiasmata (Laurie and Hultén, 1985), no statistically significant differences were expected in the frequency of disomies for the chromosomes implicated in the reorganization.
As deduced from the data, spermatozoa classified as resulting from 3:0 segregations or as diploid in the segregation analysis must be considered to be 2n, thus confirming that 3:0 segregation rarely occurs, or results in a selective elimination as suggested by our data in Table III.
In the ICE evaluation, the data obtained did not provide any evidence of an ICE for chromosomes 18, 21 or 22. It is well known that some individuals with oligoasthenozoospermia or oligoasthenoteratozoospermia show an increased incidence of sex chromosome disomies. In fact, all seven patients had oligozoospermia, but only patients 3 and 6 showed this effect. It should be noted that in the case of patient 6, the incidence of sex chromosome disomies was higher than that expected in our oligoasthenoteratozoospermic population (P < 0.05) (Aran et al., 1999). This fact could support the existence of an ICE on the sex chromosomes.
Previous to our report, two other papers investigating ICE showed an increased frequency of sex chromosome disomies in the spermatozoa of some of the t(13;14) carriers analysed (Vegetti et al., 2000; Morel et al., 2001). Taken together, these results support the occurrence of an ICE on the sex chromosomes in some cases of Robertsonian translocation. Classical meiotic studies and synaptonemal complex studies in Robertsonian translocation carriers have reported a non-random association at prophase I between the trivalent, via the short arm regions of the non-fused chromosomes (which also carry the nuclear organizer regions), and the sex chromosomes in several males analysed (Luciani et al., 1984; Navarro et al., 1991). These reports have also described the presence of prophases with several partially asynaptic bivalents, an anomaly also detected in male mice carriers of Robertsonian translocations (Grao et al., 1989).
Thus, the possible interference of the heterosynapsis (which are a rescue mechanism when anaphase is arrested; Saadallah and Hultén, 1986) with the normal segregation of the XY bivalent could explain the increase of XY disomies observed. Moreover, asynaptic bivalents could induce the malsegregation of other chromosome pairs, not detected by the probes used. Furthermore, the inter-individual variations observed among the carriers studied could be related to specific characteristics of the rearranged chromosomes, for instance the well-known satellite polymorphisms (
-satellite heteromorphism) common in acrocentric chromosomes.
It is of note that carriers of Robertsonian translocations, while producing a high proportion of normal or balanced sperm, also produce very high proportion of abnormal embryos (ESHRE PGD Consortium Steering Committee, 2002; Sermon, 2002). Furthermore, reduced pregnancy rates have been observed in translocation carriers enrolled in preimplantational genetic diagnosis cycles (ESHRE PGD Consortium Steering Committee, 2002) and have been suggested to be linked to cytogenetic abnormalities affecting chromosome pairs that are not routinely analysed in these patients, as has been recently shown in female carriers of Robertsonian translocation 13;14 (Pujol et al., 2003). Whether this could be related to the abnormal segregation of other chromosome pairs (ICE) or to other factors still deserves further investigation, because it is a crucial factor in the reproductive future of these patients.
In conclusion, our results indicate that t(13;14) carriers have an homogeneous segregation pattern with a clearly preferential alternate segregation. However, it should be taken into consideration that certain variability among patients was observed and that the data presented demonstrate that in some carriers the trivalent could interfere with the normal segregation of the sex chromosomes. It would be interesting to follow-up these studies in an ever larger series of Robertsonian translocation carriers for the same reorganization, focusing on the segregation analysis but also on the occurrence of ICE, to shed more light on the meiotic behaviour in these individuals, and its final outcome in the spermatozoa produced.
|
Acknowledgements |
|---|
We thank the Servei de Medicina de la Reproducció de l’Institut Universitari Dexeus (Barcelona), Instituto de Reproduccion Asistida CEFER (Barcelona), Instituto Valenciano de Infertilidad (Valencia), Clínica Tambre (Madrid) and Hospital Clínic de Barcelona (Barcelona) for providing the semen samples of the patients studied. This work was supported by Ministerio de Educación y Cultura (DGESEIC; project no. PM98-0174), Ministerio de Ciencia y Tecnología (DGI; project no. SAF2003-04312) and by a FI/FIAP grant (2001FI/00457) from Direcció General de Recerca (Generalitat de Catalunya, Spain).
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Anton E, Blanco J, Egozcue J and Vidal F (2002) Risk assessment and segregation analysis in a pericentric inversion inv(6)(p23q25) carrier using FISH on decondensed sperm nuclei. Cytogenet Genome Res 97,149–154.[CrossRef][Web of Science][Medline]
Aran B, Blanco J, Vidal F, Vendrell JM, Egozcue S, Barri PN, Egozcue J and Veiga A (1999) Screening for abnormalities of chromosomes X, Y and 18 and for diploidy in spermatozoa from infertile men participating in an in vitro fertilization-intracytoplasmatic sperm injection program. Fertil Steril 72,696–701.[CrossRef][Web of Science][Medline]
Baccetti B, Capitani S, Collodel G, Estenoz M, Gambera L and Piomboni P (2002) Infertile spermatozoa in a human carrier of Robertsonian translocation 14;22. Fertil Steril 78,1127–1130.[CrossRef][Web of Science][Medline]
Blanco J, Egozcue J and Vidal F (1996) Incidence of chromosome 21 disomy in human spermatozoa as determined by fluorescent in-situ hybridization. Hum Reprod 11,722–726.
Blanco J, Rubio C, Simon C, Egozcue J and Vidal F (1997) Increased incidence of disomic sperm nuclei in a 47,XYY male assessed by fluorescent in situ hybridization (FISH). Hum Genet 99,413–416.[CrossRef][Web of Science][Medline]
Blanco J, Gabau E, Gómez D, Baena N, Guitart M, Egozcue J and Vidal F (1998a) Chromosome 21 disomy in the spermatozoa of the fathers of children with trisomy 21, in population with high prevalence of Down syndrome: increased incidence in cases of paternal origin. Am J Hum Genet 63,1067–1072.[CrossRef][Web of Science][Medline]
Blanco J, Egozcue J, Clusellas N and Vidal F (1998b) FISH on sperm heads allows the analysis of chromosome segregational effects in carriers of structural rearrangements: results in a translocation carrier, t(5;8)(q33;q13). Cytogenet Cell Genet 83,275–280.[CrossRef][Web of Science][Medline]
Blanco J, Egozcue J and Vidal F (2000) Interchromosomal effects for chromosome 21 in carriers of structural chromosome reorganizations determined by fluorescence in situ hybridization on sperm nuclei. Hum Genet 106,500–505.[CrossRef][Web of Science][Medline]
Cifuentes P, Navarro J, Blanco J, Vidal F, Míguez L, Egozcue J and Benet J (1999) Cytogenetic analysis in a male heterozygous for a reciprocal translocation t(5;7)(q21;q32) by in situ hybridisation. Eur J Hum Genet 7,231–238.[CrossRef][Web of Science][Medline]
Colls P, Blanco J, Martínez-Pasarell O, Vidal F, Egozcue J, Márquez C, Guitard M and Templado C (1997) Chromosome segregation in a man heterozygous for a pericentric inversion, inv(9)(p11q13), analyzed by using sperm karyotyping and two-color fluorescence in situ hybridization on sperm nuclei. Hum Genet 99,761–765.[CrossRef][Web of Science][Medline]
DeBraekeleer M and Dao T-N (1991) Cytogenetic studies in male infertility: a review. Hum Reprod 6,245–250.
Eaker S, Pyle A, Cobb J and Handel MA (2001) Evidence of meiotic spindle checkpoint from analysis of spermatocytes from Robertsonian-chromosome heterozygous mice. J Cell Sci 114,2953–2965.
Egozcue S, Blanco J, Vendrell JM, García F, Veiga A, Aran B, Barri PN, Vidal F and Egozcue J (2000) Human male infertility: chromosome anomalies, meiotic disorders, abnormal spermatozoa and recurrent abortion. Hum Reprod Update 6,93–105.
Escudero T, Lee M, Carrel D, Blanco J and Munné S (2000) Analysis of chromosome abnormalities in sperm and embryos from two 45,XY,t(13;14)(q10;q10) carriers. Prenat Diagn 20,599–602.[CrossRef][Web of Science][Medline]
ESHRE PGD Consortium Steering Committee (2002) ESHRE Preimplantation Genetic Diagnosis Consortium: data collection III (May 2001). Hum Reprod 17,233–246.
Estop AM, Cieply K, Munne S, Surti U, Wakin A and Feingold E (2000) Is there an interchromosomal effect in reciprocal translocation carriers? Sperm FISH studies. Hum Genet 106,517–524.[CrossRef][Web of Science][Medline]
Frydman N, Romana S, Le Lorc’h M, Vekemans M, Frydman R and Tachdjian G (2001) Assisting reproduction of infertile men carrying a Robertsonian translocation. Hum Reprod 16,2274–2277.
Grao P, Coll MD, Ponsa M and Egozcue J (1989) Trivalent behavior during prophase I in male mice heterozygous for three Robertsonian translocations: an electron-microscopic study. Cytogenet Cell Genet 52,105–110.[Web of Science][Medline]
Honda H, Miharu N, Ohashi Y, Honda N, Hara T and Ohama K (1999) Analysis of segregation and aneuploidy in two reciprocal translocation carriers, t(3;9)(q26.2;q32) and t(3;9)(p25;q32), by triple-color fluorescence in situ hybridization. Hum Genet 105,428–436.[CrossRef][Web of Science][Medline]
Laurie DA and Hultén MA (1985) Further studies on bivalent chiasma frequency in human males with normal karyotypes. Ann Hum Genet 49,189–201.[Web of Science][Medline]
Lejeune J (1963) Autosomal disorders. Pediatrics 32,326–337.
Luciani JM, Guichaoua MR, Mattei A, Morazzani MR (1984) Pachytene analysis of a man with a 13q;14q translocation and infertility. Cytgenet Cell Genet 38,14–22.
Martin RH (1988) Cytogenetic analysis of sperm from a male heterozygous for a 13;14 Robertsonian translocation. Hum Genet 80,357–361.[CrossRef][Web of Science][Medline]
Martini E, Von Bergh ARM, Coonen E, Die-Smulders CEM, Ramaekers FCS and Geraedts JPM (1998) Detection of structural abnormalities in spermatozoa of a translocation carrier t(3;11)(q27.3;q24.3) by triple FISH. Hum Genet 102,157–165.[CrossRef][Web of Science][Medline]
Morel F, Roux C and Bresson JL (2001) FISH analysis of the chromosomal status of spermatozoa from three men with 45,XY,der(13;14)(q10;q10) karyotype. Mol Hum Reprod 7,483–488.
Navarro J, Vidal F, Benet J, Templado C, Marina S and Egozcue J (1991) XY-trivalent association and synaptic anomalies in a male carrier of a Robertsonian t(13;14) translocation. Hum Reprod 6,376–381.
Nielsen J and Wohlert M (1991) Chromosome abnormalities found among 34910 newborn children: results from 13-year incidence study in Arhus, Denmark. Hum Genet 87,81–83.[CrossRef][Web of Science][Medline]
Oliver-Bonet M, Navarro J, Carrera M, Egozcue J and Benet J (2002) Aneuploid and unbalanced sperm in two translocation carriers: evaluation of the genetic risk. Mol Hum Reprod 8,958–963.
Owaga S, Araki S, Araki Y, Ohono M and Sato I (2000) Chromosome analysis of human spermatozoa from an oligoasthenozoospermic carrier for a 13;14 Robertsonian translocation by their injection into mouse oocytes. Hum Reprod 15,1136–1139.
Pandiyan N and Jequier AM (1996) Mitotic chromosomal anomalies among 1210 infertile men. Hum Reprod 11,2604–2608.
Pellestor F, Sèle B and Jalbert H (1987) Chromosome analysis of spermatozoa from a male heterozygous for a 13;14 Robertsonian translocation. Hum Genet 76,116–120.[CrossRef][Web of Science][Medline]
Pellestor F, Imbert I, Andréo B and Lefort G (2001) Study of the occurrence of interchromosomal effect in spermatozoa of chromosomal rearrangement carriers by fluorescence in-situ hybridization and primed in-situ labelling techniques. Hum Reprod 16,1155–1164.
Pujol A, Durban M, Benet J, Boiso I, Calafell JM, Egozcue J and Navarro J (2003) Multiple aneuploidies in the oocytes of balanced translocation carriers: a preimplantation genetic diagnosis study using first polar body. Reproduction 126,701–711.[Abstract]
Rousseaux S, Chevret E, Monteil M, Cozzi J, Pelletier R, Delafontaine D and Sèle B (1995) Sperm nuclei analysis of a Robertsonian t(14q21q) carrier, by FISH, using three plasmids and two YAC probes. Hum Genet 96,655–660.[CrossRef][Web of Science][Medline]
Saadallah N and Hultén M (1986) EM investigations of surface spread synaptonemal complexes in a human male carrier of a pericentric inversion inv(13)(p12q14): the role of heterosynapsis for spermatocyte survival. Ann Hum Genet 50,369–383.[Web of Science][Medline]
Sermon K (2002) Current concepts in preimplantation genetic diagnosis (PGD): a molecular biologist’s view. Hum Reprod Update 8,11–20.
Shaffer LG, Jackson-Cook CK, Stasiowski BA, Spence JE and Brown JA (1992) Parental origin determination in thirty de novo Robertsonian translocations. Am J Med Genet 43,957–963.[CrossRef][Web of Science][Medline]
Soares SR, Templado C, Blanco J, Egozcue J and Vidal F (2001) Numerical chromosome abnormalities in the spermatozoa of the fathers of children with trisomy 21 of paternal origin: generalised tendency to meiotic non-disjunction. Hum Genet 108,134–139.[CrossRef][Web of Science][Medline]
Sybenga J (1975) Chromosome structural variants. In J.Sybenga (ed) General Cytogenetics. North-Holland Publishing Company, Amsterdam, The Netherlands, pp. 165–212.
VanHummelen P, Manchester D, Lowe X and Wyrobek AJ (1997) Meiotic segregation, recombination, and gamete aneuploidy assessed in a t(1;10)(p22.1;q22.3) reciprocal translocation carrier by three- and four-probe multicolor FISH in sperm. Am J Hum Genet 61,651–659.[Web of Science][Medline]
Vegetti W, Van Assche E, Frias A, Verheyen G, Bianchi MM, Bonduelle M, Liebaers I and Van Steirteghem A (2000) Correlation between semen parameters and sperm aneuploidy rates investigated by fluorescence in-situ hybridization in infertile men. Hum Reprod 15,351–365.
Vidal F, Templado C, Navarro J, Marina S and Egozcue J (1982) Meiotic and synaptonemal complexes studies in a 14/21 translocation carrier. Int J Androl 5,21–26.[Web of Science][Medline]
Vidal F, Moragas M, Català V, Torelló MJ, Santaló J, Calderón G, Giménez C, Barri PN, Egozcue J and Veiga A (1993) Sephadex filtration and human serum albumin gradients do not select spermatozoa by sex chromosome: a fluorescent in-situ hybridization study. Hum Reprod 8,1740–1743.
World Health Organization (1999) WHO Laboratory Mannual for the Examination of Human Semen and Semen–Cervical Mucus Interaction. 4th edn, Cambridge University Press, Cambridge, UK.
Submitted on February 12, 2004; accepted on February 22, 2004.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. Pinton, A. Calgaro, N. Bonnet, S. Ferchaud, S. Billoux, A.M. Dudez, N. Mary, K. Massip, A. Bonnet-Garnier, M. Yerle, et al. Influence of sex on the meiotic segregation of a t(13;17) Robertsonian translocation: a case study in the pig Hum. Reprod., April 29, 2009; (2009) dep118v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Kirkpatrick, K. A. Ferguson, H. Gao, S. Tang, V. Chow, B. H. Yuen, and S. Ma A comparison of sperm aneuploidy rates between infertile men with normal and abnormal karyotypes Hum. Reprod., July 1, 2008; 23(7): 1679 - 1683. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R.H. Martin Cytogenetic determinants of male fertility Hum. Reprod. Update, June 4, 2008; (2008) dmn017v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Anton, F. Vidal, and J. Blanco Role of sperm FISH studies in the genetic reproductive advice of structural reorganization carriers Hum. Reprod., August 1, 2007; 22(8): 2088 - 2092. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Moradkhani, J. Puechberty, S. Bhatt, J. Lespinasse, P. Vago, G. Lefort, P. Sarda, S. Hamamah, and F. Pellestor Rare Robertsonian translocations and meiotic behaviour: sperm FISH analysis of t(13;15) and t(14;15) translocations: A Case Report Hum. Reprod., December 1, 2006; 21(12): 3193 - 3198. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Moradkhani, J. Puechberty, S. Bhatt, P. Vago, L. Janny, G. Lefort, S. Hamamah, P. Sarda, and F. Pellestor Meiotic segregation of rare Robertsonian translocations: sperm analysis of three t(14q;22q) cases Hum. Reprod., May 1, 2006; 21(5): 1166 - 1171. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Ogur, E. Van Assche, W. Vegetti, G. Verheyen, H. Tournaye, M. Bonduelle, A. Van Steirteghem, and I. Liebaers Chromosomal segregation in spermatozoa of 14 Robertsonian translocation carriers Mol. Hum. Reprod., March 1, 2006; 12(3): 209 - 215. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Baccetti, G. Collodel, R. Marzella, E. Moretti, P. Piomboni, G. Scapigliati, and F. Serafini Ultrastructural studies of spermatozoa from infertile males with Robertsonian translocations and 18, X, Y aneuploidies Hum. Reprod., August 1, 2005; 20(8): 2295 - 2300. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Anahory, S. Hamamah, B. Andreo, B. Hedon, M. Claustres, P. Sarda, and F. Pellestor Sperm segregation analysis of a (13;22) Robertsonian translocation carrier by FISH: a comparison of locus-specific probe and whole chromosome painting Hum. Reprod., July 1, 2005; 20(7): 1850 - 1854. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||