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Ultrastructural Pathology of the Spermatozoa with Genetic Basis

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Clues in the Diagnosis of Non-tumoral Testicular Pathology

Abstract

Electron microscopy is an important tool to know not only the presence but the nature of spermatozoa defects. The data it provides along with molecular studies, even if taken in isolation, are of higher value than simply mobility or coloring characteristics. An ultrastructural study is indicated in the following situations: (a) in all cases of moderate or severe persistent asthenozoospermia unexplained by sperm infection, varicocele, or the presence of anti-spermatozoa antibodies; (b) in teratozoospermia, provided that the number of spermatozoa showing the same anomaly is very high; and (c) in all patients with lengthy unexplained infertility, before including them in an IVF program. Anomalies considered to have a potential genetic basis are the following: globozoospermia, hypoplasia of the acrosome, macrocephalic spermatozoa syndrome, abnormal head-tail attachment, decapitated spermatozoa syndrome, fibrous sheath dysplasia, and primary ciliary dyskinesia. The different morphological abnormalities and the molecular basis of these anomalies are discussed in this chapter.

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References

  1. Baccetti B, Capitani S, Collodel G, Di Cairano G, Gambera L, Moretti E, Piomboni P. Genetic sperm defects and consanguinity. Hum Reprod. 2001;16:1365–71.

    Article  CAS  PubMed  Google Scholar 

  2. Kalahanis J, Rousso D, Kourtis A, Mavromatidis G, Makedos G, Panidis D. Round-headed spermatozoa in semen specimens from fertile and subfertile men. J Reprod Med. 2002;47:489–93.

    PubMed  Google Scholar 

  3. Seuanez HN, Carothers AD, Martin DE, Short RV. Morphological abnormalities in spermatozoa of man and great apes. Nature. 1977;270:345–7.

    Article  CAS  PubMed  Google Scholar 

  4. Holstein AF, Schirren C, Schirren CG. Human spermatids and spermatozoa lacking acrosomes. J Reprod Fertil. 1973;35:489–91.

    Article  CAS  PubMed  Google Scholar 

  5. Vicari E, Perdichizzi A, De Palma A, Burrello N, D’Agata R, Calogero AE. Globozoospermia is associated with chromatin structure abnormalities: case report. Hum Reprod. 2002;17:2128–33.

    Article  PubMed  Google Scholar 

  6. Ricci G, Andolfi L, Zabucchi G, Luppi S, Boscolo R, Martinelli M, Zweyer M, Trevisan E. Ultrastructural morphology of sperm from human globozoospermia. Biomed Res Int. 2015;2015:798754.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Dam AH, Ramos L, Dijkman HB, Woestenenk R, Robben H, van den Hoven L, Kremer JA. Morphology of partial globozoospermia. J Androl. 2011;32:199–206.

    Article  PubMed  Google Scholar 

  8. Kullander S, Rausing A. On round-headed human spermatozoa. Int J Fertil. 1975;20:33–40.

    CAS  PubMed  Google Scholar 

  9. Nistal M, Paniagua R. Morphogenesis of round-headed human spermatozoa lacking acrosomes in a case of severe teratozoospermia. Andrologia. 1978;10:49–51.

    Article  CAS  PubMed  Google Scholar 

  10. Flörke-Gerloff S, Töpfer-Petersen E, Müller-Esterl W, Mansouri A, Schatz R, Schirren C, Schill W, Engel W. Biochemical and genetic investigation of round-headed spermatozoa in infertile men including two brothers and their father. Andrologia. 1984;16:187–202.

    Article  PubMed  Google Scholar 

  11. Koscinski I, Elinati E, Fossard C, Redin C, Muller J, Velez de la Calle J, Schmitt F, Ben Khelifa M, Ray PF, Kilani Z, Barratt CL, Viville S. DPY19L2 deletion as a major cause of globozoospermia. Am J Hum Genet. 2011;88:344–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Chianese C, Fino MG, Riera Escamilla A, López Rodrigo O, Vinci S, Guarducci E, Daguin F, Muratori M, Tamburrino L, Lo Giacco D, Ars E, Bassas L, Costa M, Pisatauro V, Noci I, Coccia E, Provenzano A, Ruiz-Castañé E, Giglio S, Piomboni P, Krausz C. Comprehensive investigation in patients affected by sperm macrocephaly and globozoospermia. Andrology. 2015;3:203–12.

    Article  CAS  PubMed  Google Scholar 

  13. Flörke-Gerloff S, Töpfer-Petersen E, Müller-Esterl W, Schill WB, Engel W. Acrosin and the acrosome in human spermatogenesis. Hum Genet. 1983;65:61–7.

    Article  PubMed  Google Scholar 

  14. Reichart M, Lederman H, Har-Even D, Kedem P, Bartoov B. Human sperm acrosin activity with relation to semen parameters and acrosomal ultrastructure. Andrologia. 1993;25:59–66.

    Article  CAS  PubMed  Google Scholar 

  15. Lundin K, Sjögren A, Nilsson L, Hamberger L. Fertilization and pregnancy after intracytoplasmic microinjection of acrosomeless spermatozoa. Fertil Steril. 1994;62:1266–7.

    Article  CAS  PubMed  Google Scholar 

  16. Karaca N, Akpak YK, Oral S, Durmus T, Yilmaz R. A successful healthy childbirth in a case of total globozoospermia with oocyte activation by calcium ionophore. J Reprod Infertil. 2015;16:116–20.

    PubMed  PubMed Central  Google Scholar 

  17. Chansel-Debordeaux L, Dandieu S, Bechoua S, Jimenez C. Reproductive outcome in globozoospermic men: update and prospects. Andrology. 2015;3:1022–34.

    Article  CAS  PubMed  Google Scholar 

  18. Anton-Lamprecht I, Kotzur B, Schopf E. Round-headed human spermatozoa. Fertil Steril. 1976;276:685–93.

    Article  Google Scholar 

  19. Meschede D, Rolf C, Neugebauer DC, Horst J, Nieschlag E. Sperm acrosome defects in a patient with Aarskog-Scott syndrome. Am J Med Genet. 1996;66:340–2.

    Article  CAS  PubMed  Google Scholar 

  20. Nistal M, Paniagua R, Herruzo A. Multi-tailed spermatozoa in a case with asthenospermia and teratospermia. Virchows Arch B Cell Pathol. 1977;26:111–8.

    CAS  PubMed  Google Scholar 

  21. Devillard F, Metzler-Guillemain C, Pelletier R, DeRobertis C, Bergues U, Hennebicq S, Guichaoua M, Sele B, Rousseaux S. Polyploidy in large-headed sperm: FISH study of three cases. Hum Reprod. 2002;17:1292–8.

    Article  CAS  PubMed  Google Scholar 

  22. Escalier D. Genetic approach to male meiotic division deficiency: the human macronuclear spermatozoa. Mol Hum Reprod. 2002;8:1–7.

    Article  CAS  PubMed  Google Scholar 

  23. Dieterich K, Soto Rifo R, Faure AK, Hennebicq S, Ben Amar B, Zahi M, Perrin J, Martinez D, Sèle B, Jouk PS, Ohlmann T, Rousseaux S, Lunardi J, Ray PF. Homozygous mutation of AURKC yields large-headed polyploid spermatozoa and causes male infertility. Nat Genet. 2007;39:661–5.

    Article  CAS  PubMed  Google Scholar 

  24. El Kerch F, Lamzouri A, Laarabi FZ, Zahi M, Ben Amar B, Sefiani A. Confirmation of the high prevalence in Morocco of the homozygous mutation c.144delC in the aurora kinase C gene (AURKC) in the teratozoospermia with large-headed spermatozoa. J Gynecol Obstet Biol Reprod (Paris). 2011;40:329–33.

    Article  CAS  Google Scholar 

  25. Ounis L, Zoghmar A, Coutton C, Rouabah L, Hachemi M, Martinez D, Martinez G, Bellil I, Khelifi D, Arnoult C, Fauré J, Benbouhedja S, Rouabah A, Ray PF. Mutations of the aurora kinase C gene causing macrozoospermia are the most frequent genetic cause of male infertility in Algerian men. Asian J Androl. 2015;17:68–73.

    Article  CAS  PubMed  Google Scholar 

  26. Molinari E, Mirabelli M, Raimondo S, Brussino A, Gennarelli G, Bongioanni F, Revelli A. Sperm macrocephaly syndrome in a patient without AURKC mutations and with a history of recurrent miscarriage. Reprod Biomed Online. 2013;26:148–56.

    Article  PubMed  Google Scholar 

  27. Shimizu Y, Kiumura F, Kaku S, Izuno M, Tomita K, Thumkeo D, Murakami T. Successful delivery following ICSI with macrocephalic sperm head syndrome: a case report. Reprod Biomed Online. 2012;24:603–5.

    Article  PubMed  Google Scholar 

  28. Lüders G. A defect of the head-flagellum-connection of human spermatozoa. Andrologia. 1976;8:365–8.

    Article  PubMed  Google Scholar 

  29. Perotti ME, Giarola A, Gioria M. Ultrastructural study of the decapitated sperm defect in an infertile man. J Reprod Fertil. 1981;63:543–9.

    Article  CAS  PubMed  Google Scholar 

  30. Chemes HE, Puigdomenech ET, Carizza C, Olmedo SB, Zanchetti F, Hermes R. Acephalic spermatozoa and abnormal development of the head-neck attachment: a human syndrome of genetic origin. Hum Reprod. 1999;14:1811–8.

    Article  CAS  PubMed  Google Scholar 

  31. Kamal A, Mansour R, Fahmy I, Serour G, Rhodes C, Aboulghar M. Easily decapitated spermatozoa defect: a possible cause of unexplained infertility. Hum Reprod. 1999;14:2791–5.

    Article  CAS  PubMed  Google Scholar 

  32. Baccetti B, Burrini AG, Collodel G, Magnano AR, Piomboni P, Renieri T, Sensini C. Morphogenesis of the decapitated and decaudated sperm defect in two brothers. Gamete Res. 1989;23:181–8.

    Article  CAS  PubMed  Google Scholar 

  33. Aughey E, Orr PS. An unusual abnormality of human spermatozoa. J Reprod Fertil. 1978;53:341–2.

    Article  CAS  PubMed  Google Scholar 

  34. Zamboni L. Sperm structure and its relevance to infertility. An electron microscopic study. Arch Pathol Lab Med. 1992;116:325–44.

    CAS  PubMed  Google Scholar 

  35. Holstein AF, Schill WB, Breucker H. Dissociated centriole development as a cause of spermatid malformation in man. J Reprod Fertil. 1986;78:719–25.

    Article  CAS  PubMed  Google Scholar 

  36. Toyama Y, Iwamoto T, Yajima M, Baba K, Yuasa S. Decapitated and decaudated spermatozoa in man, and pathogenesis based on the ultrastructure. Int J Androl. 2000;23:109–15.

    Article  CAS  PubMed  Google Scholar 

  37. Chemes HE, Rawe VY. The making of abnormal spermatozoa: cellular and molecular mechanisms underlying pathological spermiogenesis. Cell Tissue Res. 2010;341:349–57.

    Article  PubMed  Google Scholar 

  38. Nistal M, Paniagua R, Herruzo A. Lack of the central pair of axial filaments in a case of short-tailed spermatozoa human teratospermia. J Gynecol Obstet Biol Reprod (Paris). 1979;8:47–50.

    CAS  Google Scholar 

  39. Pedersen H, Hammen R. Ultrastructure of human spermatozoa with complete subcellular derangement. Arch Androl. 1982;9:251–9.

    Article  CAS  PubMed  Google Scholar 

  40. Escalier D, David G. Pathology of the cytoskeleton of the human sperm flagellum: axonemal and peri-axonemal anomalies. Biol Cell. 1984;50:37–52.

    Article  CAS  PubMed  Google Scholar 

  41. Baccetti B, Burrini AG, Capitani S, Collodel G, Moretti E, Piomboni P, Renieri T. Notulae seminologicae. 2. The ‘short tail’ and ‘stump’ defect in human spermatozoa. Andrologia. 1993;25:331–5.

    Article  CAS  PubMed  Google Scholar 

  42. Eddy EM, Toshimori K, O’Brien DA. Fibrous sheath of mammalian spermatozoa. Microsc Res Tech. 2003;61:103–15.

    Article  CAS  PubMed  Google Scholar 

  43. Barthelemy C, Tharanne MJ, Lebos C, Lecomte P, Lansac J. Tail stump spermatozoa: morphogenesis of the defect. An ultrastructural study of sperm and testicular biopsy. Andrologia. 1990;22:417–25.

    Article  CAS  PubMed  Google Scholar 

  44. Chemes HE, Morero JL, Lavieri JC. Extreme asthenozoospermia and chronic respiratory disease: a new variant of the immotile cilia syndrome. Int J Androl. 1990;13:216–22.

    Article  CAS  PubMed  Google Scholar 

  45. 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;2:125–30.

    CAS  PubMed  Google Scholar 

  46. Taylor RE. Abnormal mucociliary transport study in a patient with Kartagener syndrome. Clin Nucl Med. 2006;31:240–2.

    Article  PubMed  Google Scholar 

  47. Baccetti B, Burrini AG, Pallini V. Different axoneme patterns in cilia and flagella of the same animal. J Submicrosc Cytol. 1981;13:479–81.

    CAS  PubMed  Google Scholar 

  48. Moryan A, Guay AT, Kurtz S, Nowak PJ. Familial ciliary dyskinesis: a cause of infertility without respiratory disease. Fertil Steril. 1985;44:539–42.

    Article  CAS  PubMed  Google Scholar 

  49. Okada H, Fujioka H, Tatsumi N, Fujisawa M, Gohji K, Arakawa S, Kato H, Kobayashi S, Isojima S, Kamidono S. Assisted reproduction for infertile patients with 9 + 0 immotile spermatozoa associated with autosomal dominant polycystic kidney disease. Hum Reprod. 1999;14:110–3.

    Article  CAS  PubMed  Google Scholar 

  50. Baccetti B, Burrini AG, Pallini V. Spermatozoa and cilia lacking axoneme in an infertile man. Andrologia. 1980;12:525–32.

    Article  CAS  PubMed  Google Scholar 

  51. Afzelius BA, Dallai R, Lanzavecchia S, Bellon PL. Flagellar structure in normal human spermatozoa and in spermatozoa that lack dynein arms. Tissue Cell. 1995;27:241–7.

    Article  CAS  PubMed  Google Scholar 

  52. Jonsson MS, McCormick JR, Gillies CG, Gondos B. Kartagener’s syndrome with motile spermatozoa. N Engl J Med. 1982;307:1131–3.

    Article  CAS  PubMed  Google Scholar 

  53. Schneeberger EE, McCormack J, Issenberg HJ, Schuster SR, Gerald PS. Heterogeneity of ciliary morphology in the immotile-cilia syndrome in man. J Ultrastruct Res. 1980;73:34–43.

    Article  CAS  PubMed  Google Scholar 

  54. Kartagener M. Zur Pathogenese der Bronchiektasien. I. Mitteilung: Bronchiektasien bei Situs viscerum inversus. Beitr Klin Tuberk. 1933;83:489–501.

    Article  Google Scholar 

  55. Carlen B, Stenram U. Primary ciliary dyskinesia: a review. Ultrastruct Pathol. 2005;29:217–20.

    Article  PubMed  Google Scholar 

  56. Douard R, Feldman A, Bargy F, Loric S, Delmas V. Anomalies of lateralization in man: a case of total situs inversus. Surg Radiol Anat. 2000;22:293–7.

    Article  CAS  PubMed  Google Scholar 

  57. Wolf JP, Feneux D, Escalier D, Rodrigues D, Frydman R, Jouannet P. Pregnancy after subzonal insemination with spermatozoa lacking outer dynein arms. J Reprod Fertil. 1993;97:487–92.

    Article  CAS  PubMed  Google Scholar 

  58. Chemes HE, Olmedo SB, Carrere C, Oses R, Carizza C, Leisner M, Blaquier J. Ultrastructural pathology of the sperm flagellum: association between flagellar pathology and fertility prognosis in severely asthenozoospermic men. Hum Reprod. 1998;13:2521–6.

    Article  CAS  PubMed  Google Scholar 

  59. Kay VJ, Irvine DS. Successful in-vitro fertilization with spermatozoa from a patient with Kartagener’s syndrome. Hum Reprod. 2000;15:135–8.

    Article  CAS  PubMed  Google Scholar 

  60. Fedick AM, Jalas C, Treff NR, Knowles MR, Zariwala MA. Carrier frequencies of eleven mutations in eight genes associated with primary ciliary dyskinesia in the Ashkenazi Jewish population. Mol Genet Genomic Med. 2015;3:137–42.

    Article  CAS  PubMed  Google Scholar 

  61. Schwabe GC, Hoffmann K, Loges NT, Birker D, Rossier C, de Santi MM, Olbrich H, Fliegauf M, Failly M, Liebers U, Collura M, Gaedicke G, Mundlos S, Wahn U, Blouin JL, Niggemann B, Omran H, Antonarakis SE, Bartoloni L. Primary ciliary dyskinesia associated with normal axoneme ultrastructure is caused by DNAH11 mutations. Hum Mutat. 2008;29:289–98.

    Article  CAS  PubMed  Google Scholar 

  62. Geremek M, Schoenmaker F, Zietkiewicz E, Pogorzelski A, Diehl S, Wijmenga C, Witt M. Sequence analysis of 21 genes located in the Kartagener syndrome linkage region on chromosome 15q. Eur J Hum Genet. 2008;16:688–95.

    Article  CAS  PubMed  Google Scholar 

  63. Pennarun G, Bridoux AM, Escudier E, Dastot-Le Moal F, Cacheux V, Amselem S, Duriez B. Isolation and expression of the human hPF20 gene orthologous to Chlamydomonas PF20: evaluation as a candidate for axonemal defects of respiratory cilia and sperm flagella. Am J Respir Cell Mol Biol. 2002;26:362–70.

    Article  CAS  PubMed  Google Scholar 

  64. Devuyst O, Arnould VJ. Mutations in RPGRIP1L: extending the clinical spectrum of ciliopathies. Nephrol Dial Transplant. 2008;23:1500–3.

    Article  PubMed  Google Scholar 

  65. Nowiński A, Hawryłkjewicz I, Sulikowska-Rowińska A, Górecka D. Primary ciliary dyskinesia – Kartagener's syndrome and fertile male. Pneumonol Alergol Pol. 2002;70:312–7.

    PubMed  Google Scholar 

  66. 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;76:612–4.

    Article  CAS  PubMed  Google Scholar 

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Nistal, M., González-Peramato, P., Serrano, Á. (2017). Ultrastructural Pathology of the Spermatozoa with Genetic Basis. In: Clues in the Diagnosis of Non-tumoral Testicular Pathology. Springer, Cham. https://doi.org/10.1007/978-3-319-49364-0_20

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