Elena Moretti, Ph.D., Nicola Antonio Pascarelli, Ph.D., Maria Grazia Federico, Ph.D., Tommaso Renieri, Ph.D., and Giulia Collodel, Ph.D.
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1 CASE REPORT Abnormal elongation of midpiece, absence of axoneme and outer dense fibers at principal piece level, supernumerary microtubules: a sperm defect of possible genetic origin? Elena Moretti, Ph.D., Nicola Antonio Pascarelli, Ph.D., Maria Grazia Federico, Ph.D., Tommaso Renieri, Ph.D., and Giulia Collodel, Ph.D. Department of Surgery, Biology Section, University of Siena, Interdepartmental Centre for Research and Therapy of Male Infertility, Siena, Italy Objective: To characterize a flagellar defect involving 95% of the sperm population from an infertile man. Design: Case report. Setting: Interdepartmental Centre for Research and Therapy of Male Infertility, Siena, Italy. Patient(s): A 42-year-old infertile man with severe asthenozoospermia. Intervention(s): Family history, physical examination, hormonal analysis, microbial assays, semen analysis, transmission electron microscopy (TEM) and scanning electron microscopy (SEM), tubulin distribution investigated by immunocytochemistry, fluorescence in situ hybridization for chromosomes 18, X, and Y. Main Outcome Measure(s): Ultrastructural abnormalities of the flagellum detected by methods listed. Result(s): Ultrastructural analysis revealed, in 95% of sperm cells, the total absence of the axoneme and outer dense fibers at the principal piece level, whereas the midpiece appeared abnormally long. Tubulin localization showed a total disorganization of the axoneme with a network of microtubular structures emerging randomly at any level of the flagellum. Fluorescence in situ hybridization analysis was normal. Conclusion(s): We report a rare sperm tail defect, characterized by abnormal elongation of the midpiece and absence of the axoneme and the outer dense fibers at the principal piece level in 95% of flagella. This defect occurs in the vast majority of the sperm population from a sterile man, and therefore a genetic origin could be hypothesized. (Fertil Steril Ò 2008;90:1201.e3 e8. Ó2008 by American Society for Reproductive Medicine.) Key Words: Asthenozoospermia, fluorescence in situ hybridization, mitochondria, principal piece, sperm axoneme, TEM Severely reduced or completely absent motility in subfertile or infertile men is associated with submicroscopic alterations in the cytoskeletal structure of sperm flagellum regarding the axonemal pattern and periaxonemal accessory structures, as well as the outer dense fibers and fibrous sheath. Ultrastructural sperm anomalies can be classified as phenotypic, nonspecific, or nonsystematic sperm defects, or as genotypic or systematic sperm defects (1, 2). The first and most frequent type is comprised of a heterogeneous combination of randomly distributed alterations affecting the head and the tail organelles in a varied percentage of sperm ejaculate. These alterations might be related to andrological pathologies Received September 20, 2007; revised October 30, 2007; accepted November 16, Supported by 2005 P.A.R. grant from the University of Siena, Italy. Reprint requests: Giulia Collodel, Ph.D., Department of Surgery, Biology Section, University of Siena, Policlinico Santa Maria alle Scotte, Viale Bracci, Siena, Italy (FAX: ; collodel@ unisi.it). (i.e., infections, varicocele) or to other endogenous or exogenous factors (2). These defects are potentially responsive to different treatments. The systematic or genetic sperm defects are characterized by an identical and specific alteration affecting the vast majority of the sperm population in sterile patients. They tend to show family clustering (2) and are significantly more frequent in individuals with a history of consanguinity (1). It has been well demonstrated that ultrastructural evaluation of teratozoospermia associated with immunocytochemical investigations and molecular techniques allows for a precise characterization of sperm anomalies. Genetic sperm defects affecting the tail include dysplasia of fibrous sheath, primary ciliary dyskinesia, detached tail, 9þ0 axoneme, and absent axoneme, as extensively reviewed by Chemes and Rawe (2). In addition a very rare alteration (absence of fibrous sheath) characterized by three major defects the absence /08/$34.00 Fertility and Sterility â Vol. 90, No. 4, October e3 doi: /j.fertnstert Copyright ª2008 American Society for Reproductive Medicine, Published by Elsevier Inc.
2 of the fibrous sheath, the presence of supplementary axonemes, and an abnormally elongated midpiece (3) has been characterized and its testicular origin was recently established (4). Before the intracytoplasmic sperm injection (ICSI) era, patients with these disorders were considered sterile; however, some successful pregnancies have been reported since the introduction of this technique (5 7). For this reason, the study of the chromosomal complements of sperm in cases of genetic sperm defects has become particularly important, as ICSI is the only tool available for resolving the infertility of these individuals. Only a few articles have reported the aneuploidy data of sperm showing genetic defects of the tail, as reviewed by Collodel and Moretti (8), particularly concerning the dysplasia of fibrous sheath defect (9, 10) in which diploidy and sex chromosome disomy appear to be higher than normal values. The same kind of aneuploidy was reported in two cases of primary ciliary dyskinesia by Rives et al. (10) and Moretti and Collodel (11). On the contrary, no meiotic alteration was detected in a case of detached tail or in one case of the absence of the fibrous sheath. In the present study we describe a rare flagellar sperm defect affecting the vast majority of a sperm population. MATERIALS AND METHODS Patient A 42-year-old man came to our center for semen analysis after 5 years of sexual intercourse without conception. The lymphocyte karyotype of the patient was 46, XY. The patient did not present a history of consanguinity. Sexual development, medical history, physical examination, and hormonal levels were normal. Tests for microbial infection did not reveal any genitourinary infection. His current partner, aged 34 years, did not have any fertility problems and she reported that she had had an abortion. Semen Analysis Light and electron microscopy Semen samples were collected by masturbation after 4 days of sexual abstinence and examined after liquefaction for 30 minutes at 37 C. Volume, ph, concentration, and motility were evaluated according to World Health Organization (WHO) guidelines (12). The analysis was repeated three times at 3-month intervals. Semen samples were stained with 0.5% eosin Y (CI 45380) in 0.9% aqueous sodium chloride solution. A few minutes after staining the samples were observed at light microscope and stained (dead) cells and unstained (lived) cells were scored. For electron microscopy, sperm samples were fixed in cold Karnovsky fixative and maintained at 4 C for 2 hours, postfixed in 1% buffered osmium tetroxide, then dehydrated in a graded ethanol series and embedded in Epon Araldite. Ultra-thin sections, stained with uranyl acetate and lead citrate, were observed and photographed with a Philips CM10 transmission electron microscope (TEM; Philips Scientifics, Eindhoven, The Netherlands). An aliquot from the same sperm samples was also processed for scanning electron microscopy (SEM), fixing the spermatozoa as described and smearing them on poly-lysine (1%)-coated cover slides. After dehydration, specimens were dried by the critical point technique, coated in gold and observed with a Philips CM 515 scanning electron microscope (Philips Scientifics). Mitochondria staining Semen samples from the patient and sperm from an individual with proven fertility were washed in phosphate-buffered saline (PBS) and incubated with fluorescent stain (Mito-Tracker Green FM; Molecular Probes, Eugene, OR) to a final concentration of 10 nmol/l for 30 minutes at 37 C. After washing in PBS, the staining was examined by a Leitz Aristoplan fluorescence microscope (Leica, Wetzlar, Germany). The images were taken using Leica Q Fluoro Standard, Leica Chantal software. Three hundred sperm from each sample were examined. Immunocytochemistry Sperm samples from the patient and those from a man with proven fertility, after careful wash in PBS, were smeared on glass slides, air dried, rinsed in PBS, and fixed for 15 minutes in methanol at 20 C. Samples were then treated with blocking solution (PBS, 1% bovine serum albumin [BSA], 5% normal goat serum) for 20 minutes at room temperature and incubated overnight at 4 C with mouse monoclonal anti-b-tubulin antibody (Sigma Chemical, St. Louis, MO) diluted 1:100 in PBS, 0.1% BSA, and 1% normal goat serum. After three washes in PBS, the samples were treated with goat antimouse IgG Texas Red conjugated antibody (Southern Biotechnology, Birmingham, AL). Finally, the samples were washed three times in PBS and mounted with Vectashield (Vector Labs, Burlingame, CA). Incubation in primary antibodies was omitted in control samples. Observations were made with a Leitz Aristoplan fluorescence microscope. Five hundred sperm from each sample were examined. Fluorescence in Situ Hybridization Analysis Fluorescence in situ hybridization was performed in two semen samples according to Baccetti et al. (13) on the sperm nuclei using a mix of a-satellite DNA probes (CEP, Chromosome Enumeration Probes, Vysis, IL) for chromosomes 18, X, and Y, directly labeled with different fluorochromes. A total of 8,592 sperm nuclei were scored according to published criteria. Semen samples from seven fertile men (aged years) were analyzed and used as controls. RESULTS Analysis of three subsequent semen samples from the patient revealed a normal volume, ph, and sperm concentration 1201.e4 Moretti et al. Rare sperm defect of possible genetic origin Vol. 90, No. 4, October 2008
3 FIGURE 1 (A) Transmission electron microscopy (TEM) micrograph of a longitudinal section of a sperm head showing a wellshaped acrosome (A) and nucleus (N) with condensed chromatin. Disorganized microtubules (Mt), part of incomplete axonemes were observed at the base of the head. Bar ¼ 1.9 mm. (B) The TEM micrograph of a longitudinal section of a spermatozoon showing a well-shaped nucleus (N) with condensed chromatin, but an abnormal length of midpiece (Mp) is evident. A thin tail emerges from the annulus. The axoneme continues up to the base of the head, cytoplasmic residue (CR). Bar ¼ 1.1 mm. (C) Longitudinal section of a sperm tail coiled and embedded in a cytoplasmic residue (CR). The sections at the principal piece level show the total absence of axoneme and outer dense fibers (arrows), mitochondria (M). Bar ¼ 1.3 mm. (D) The TEM micrograph of cross sections at midpiece level. The mitochondria (M), the axonemes (AX), and the outer dense fibers are well assembled; however, supernumerary microtubules (Mt) arranged as part of the axoneme are visible, embedded in the cytoplasmic residue. Bar ¼ 0.6 mm. (E) The TEM micrograph of a cross section of a coiled sperm tail. The midpiece is normal, but at the principal piece level, despite the presence of a fibrous sheath, the axoneme and outer dense fibers are totally absent (arrows). Bar ¼ 1.04 mm. Moretti. Rare sperm defect of possible genetic origin. Fertil Steril (ranging from to ). All analyzed samples were severely asthenozoospermic: rapid and slow progressive motility ranged between 2% and 3% and 2% and 5%, respectively. Examination at the light microscopy level showed a majority of apparently short tails. Eosin staining revealed that 75% of sperm cells were viable but not motile. The TEM analysis was also performed three times and highlighted regularly shaped acrosomes and nuclei with condensed chromatin in more than 50% of examined sections (Fig. 1A). Axonemes showed a regular pattern in the majority of midpiece cross sections, where cytoplasmic residue was often detected (Fig. 1B,C,D). However, in 40% of these sections supernumerary doublets were observed (Fig. 1D). Dynein arms and outer dense fibers (ODF) were generally normal at the midpiece level. In the longitudinal section of the midpiece region we observed abnormal extension (to 15 mm) of the mitochondrial helix (Fig. 1B), also Fertility and Sterility â 1201.e5
4 FIGURE 1 CONTINUED (F) The TEM micrograph of cross sections of coiled sperm tails at the principal piece level. The absence of axonemes and outer dense fibers is evident. Bar ¼ 0.7 mm. (G) Scanning electron microscopy micrograph of spermatozoa showing normal head, abnormally elongated midpieces, and short thin tails. Bar ¼ 0.2 mm. (H) Scanning electron microscopy micrograph of spermatozoa with coiled tails. Bar ¼ 0.3 mm. (I) Ultraviolet micrograph of sperm treated with MitoTracker green showing an increased length of the mitochondrial helix. The inset shows a normal length of mitochondrial helix in a spermatozoa from a man of proven fertility. Bar ¼ 0.2 mm. (L O) Staining with monoclonal antitubulin antibody highlights a highly disorganized microtubular network emerging at any level of the flagellum (L, N). Phase contrast light microscopy pictures (O, M) are also shown. (L) Bar ¼ 3.6 mm; (M) bar ¼ 3.5 mm; (N) bar ¼ 3.1 mm; (O) bar ¼ 5.2 mm. Moretti. Rare sperm defect of possible genetic origin. Fertil Steril e6 Moretti et al. Rare sperm defect of possible genetic origin Vol. 90, No. 4, October 2008
5 demonstrated by fluorescence staining with MitoTracker Green FM (Fig. 1I), compared to the midpiece (normal length about 5 mm) of sperm from a man with proven fertility (Fig. I inset). Surprisingly, at the principal piece level the axonemal pattern and the ODF were absent in 95% of examined sections (Fig. 1E,F). The principal piece, empty of content, appears very thin, not well visible with a light microscope, and it showed a tendency to be coiled (Fig. 1E,F). For instance, the axoneme seems to reach the annulus region and then continue up to the base of the head (Fig. 1B) where disorganized microtubules and part of incomplete axonemes (Fig. 1A) were observed. Consequently, a straight thin tail, only made up of fibrous sheath, emerges from the annulus region. The SEM analysis showed an elongated midpiece associated with 60% of short thin tails (Fig. 1G) and 10% of tails of normal length but extremely thin, and 25% of tails were rolled up (Fig. 1H). In addition, an apparently normal tail was observed in 5% of sperm cells. The tubulin label showed that the vast majority of cells had a disorganized network of microtubular structures emerging randomly at any level of the flagellum (Fig. 1L O). Fluorescence in situ hybridization analysis performed in two semen samples highlighted a normal incidence of diploidy and disomy for 18, X, and Y chromosomes (Table 1). DISCUSSION In this study we describe the ultrastructural and molecular characteristics of ejaculated spermatozoa from a severe asthenozoospermic patient. The sperm head appeared normally structured, but we observed a total absence of axoneme and ODF in the principal piece at the tail level, justifying the severely reduced motility. The mitochondrial sheath was abnormally extended and supernumerary microtubules, organized in more or less complete axonemes, were observed at the midpiece level. Immunostaining of tubulin demonstrated the total disorganization of microtubules, which were not arranged in the typical axonemal 9þ2 structure at the principal piece level. A similar case was described by Sauvalle et al. (14) in two infertile patients, and Rawe et al. (15) recently reported a case of a patient whose sperm showed a midpiece four times longer than normal, continuing with a short and stiff principal piece, without disorganized supernumerary microtubules. The absence of axonemes has already been reported by Baccetti et al. (16), but in that patient the axoneme was absent for the entire tail length, whereas ODF were regularly present, sometimes showing an abnormal profile. Recently our group described a rare sperm tail defect, originating during spermiogenesis (4), which shares with the present case an abnormally elongated midpiece and the presence of supplementary axonemes, although a total absence of the fibrous sheath was observed in the previous study. The present case shows the presence of fibrous sheath, but the axoneme and ODF at the principal piece level were absent in 95% of flagella. The axoneme seemed to reach the annulus and to continue up to the base of the head, where disorganized microtubules were found. A testicular origin of this defect could be postulated. In both cases, the anomalous length of the mitochondrial helix was associated with severe anomalies at the principal piece level, leading to severe asthenozoospermia. As pointed out by Rawe et al. (15), it is difficult to understand why sperm with an elongated midpiece would have motility problems. One hypothesis contemplates the possibility of an alteration of the normal transmission of the cyclic AMP-dependent signaling cascade through anchor kinase A proteins located at the sperm midpiece, or that the abnormal extension that occupies most of the principal piece, gives rise to short and rigid flagella. TABLE 1 Fluorescence in situ hybridization analysis for chromosomes 18, X, and Y. Normal sperm Disomy frequency Diploidy frequency Samples X/Y-bearing 18,18 X,X Y,Y X,Y 18,18,X,X 18,18,Y,Y 18,18,X,Y Sample %/ 49.5% 0.09% 0.03% 0.03% 0.12% 0.06% 0.09% 0.09% Sample 2 a 49.69%/49.56% 0.08% 0.08% 0.03% 0.11% 0.054% 0.027% 0.082% Controls b mean% SD 0.11% % % a The total number of cells scored by triple fluorescence in situ hybridization analysis was 8,592. b The control group was made up of seven fertile men. Mean percentages (SD) of disomies and diploidies are reported for the chromosomes examined. The mean number of sperm scored by triple fluorescence in situ hybridization analysis was 5, Moretti. Rare sperm defect of possible genetic origin. Fertil Steril Fertility and Sterility â 1201.e7
6 Because individuals with genetic sperm defects are ICSI candidates, the study of the chromosomal constitution of their spermatozoa is of great interest. In dysplasia of fibrous sheath sperm, the most frequently studied genetic sperm tail defect, the alterations in sex chromosome disomy and diploidy have been recorded by different groups (9, 10). Regarding primary ciliary dyskinesia defects, elevated frequencies of disomy of sex chromosomes and diploidy have been observed (10, 11), whereas the absence of the fibrous sheath and the detached tail did not show any meiotic disturbance (11), but it was possible to examine only one case for each defect. For this reason, to complete the study described in this article, we decided to carry out fluorescence in situ hybridization, which revealed normal chromosomal segregation, at least for the analyzed chromosomes 18, X, Y in both examined samples. In conclusion we suggest a possible genetic origin of the described composed defect, as the observed sperm alterations remained stable during the 4 months in which sperm analysis was repeated three times, and particularly because we observed a common sperm phenotype that was predominant in the examined patient. REFERENCES 1. Baccetti B, Capitani S, Collodel G, Di Cairano G, Gambera L, Moretti E, et al. Genetic sperm defects and consanguinity. Hum Reprod 2001;16: Chemes HE, Rawe VY. Sperm pathology: a step beyond descriptive morphology. Origin, characterization and fertility potential of abnormal sperm phenotypes in infertile men. Hum Reprod Update 2003;5: Ross A, Christie S, Kerr MG. An electron microscope study of a tail abnormality in spermatozoa from a subfertile man. J Reprod Fertil 1971;24: Baccetti B, Bruni E, Gambera L, Moretti E, Piomboni P. An ultrastructural and immunocytochemical study of a rare genetic sperm tail defect that causes infertility in humans. Fertil Steril 2004;82: Nijs M, Vanderzwalmen P, Vandamme B, Segal-Bertin G, Lejeune B, Segal L, van Roosendaal E, et al. Fertilizing ability of immotile spermatozoa after intracytoplasmic sperm injection. Hum Reprod 1996;11: Olmedo SB, Rawe VY, Nodar FN, Galaverna GD, Acosta AA, Chemes HE. Pregnancies established through intracytoplasmic sperm injection (ICSI) using spermatozoa with dysplasia of fibrous sheath. Asian J Androl 2000;2: Cayan S, Conaghan J, Schriock ED, Ryan IP, Black LD, Turek PJ. Birth after intracytoplasmic sperm injection with use of testicular sperm from men with Kartagener/immotile cilia syndrome. Fertil Steril 2001;76: Collodel G, Moretti E. Sperm morphology and aneuploidies: defects of supposed genetic origin [Review]. Andrologia 2006;38: Baccetti B, Collodel G, Gambera L, Moretti E, Serafini F, Piomboni P. Fluorescence in situ hybridization and molecular studies in infertile men with dysplasia of the fibrous sheath. Fertil Steril 2005;84: Rives N, Mousset-Simeon N, Mazurier S, Mace B. Primary flagellar abnormality is associated with an increased rate of spermatozoa aneuploidy. J Androl 2005;26: Moretti E, Collodel G. Three cases of genetic defects affecting sperm tail: a FISH study. J Submicrosc Cytol Pathol 2006;38: World Health Organization. WHO laboratory manual for the examination of human semen and semen-cervical mucus interaction. 4th ed. Cambridge: Cambridge University Press, Baccetti B, Bruni E, Collodel G, Gambera L, Moretti E, Marzella R, et al. 10, 15 reciprocal translocation in an infertile man: ultrastructural and fluorescence in-situ hybridization sperm study: case report. Hum Reprod 2003;18: Sauvalle A, Le Bris C, Izard J. Supernumerary microtubules and prolongation of the middle piece in two infertile patients. Int J Fertil 1983;28: Rawe VY, Hermes R, Nodar FN, Fiszbajn G, Chemes H. Results of intracytoplasmic sperm injection in two infertile patients with abnormal organization of sperm mitochondrial sheaths and severe asthenoteratozoospermia. Fertil Steril 2007;88: Baccetti B, Burrini AG, Pallini V. Spermatozoa and cilia lacking axoneme in an infertile man. Andrologia 1980;12: e8 Moretti et al. Rare sperm defect of possible genetic origin Vol. 90, No. 4, October 2008
An ultrastructural and immunocytochemical study of a rare genetic sperm tail defect that causes infertility in humans
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