Skip to main content Accessibility help
×
Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-20T02:44:58.037Z Has data issue: false hasContentIssue false

3 - Sperm Ultrastructure in Fertile Men and Male Sterility

Revisiting Teratozoospermia

Published online by Cambridge University Press:  25 May 2017

Christopher J. De Jonge
Affiliation:
University of Minnesota
Christopher L. R. Barratt
Affiliation:
University of Dundee
Ryuzo Yanagimachi
Affiliation:
University of Hawaii, Manoa
Get access

Summary

Image of the first page of this content. For PDF version, please use the ‘Save PDF’ preceeding this image.'
Type
Chapter
Information
The Sperm Cell
Production, Maturation, Fertilization, Regeneration
, pp. 36 - 58
Publisher: Cambridge University Press
Print publication year: 2017

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Holstein, AF. Ultrastructural observations on the differentiation of spermatids in man. Andrologia 1976; 8: 157–65.Google ScholarPubMed
Holstein, AF, Roosen Runge, EC. Atlas of Human Spermatogenesis. Berlin: Grosse Verlag, 1981.Google Scholar
Fawcett, DW. The mammalian spermatozoon. Dev Biol 1975; 44: 394436.Google Scholar
Chemes, HE. Sperm centrioles and their dual role in flagellogenesis and cell cycle of the zygote: Structure, function and pathology. In: Schatten, H (Ed.), The Centrosome. New York: Humana Press, 2012: 3348.Google Scholar
Balhorn, R. A model for the structure of chromatin in mammalian sperm. J Cell Biol 1982; 93: 298305.Google Scholar
Oliva, R. Protamines and male infertility. Hum Reprod Update 2006; 12: 417–35.CrossRefGoogle ScholarPubMed
Haraguchi, CM, Mabuchi, T, Hirata, S, Shoda, T, Tokumoto, T, Hoshi, K et al. Possible function of caudal nuclear pocket: Degradation of nucleoproteins by ubiquitin-proteasome system in rat spermatids and human sperm. J Histochem Cytochem 2007; 55: 585–95.Google Scholar
Barone, JG, De Lara, J, Cummings, KB, Ward, WS. DNA organization in human spermatozoa. J Androl 1994; 15: 139–44.Google Scholar
Ward, WS. Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod 2010; 16: 30–6.CrossRefGoogle ScholarPubMed
Zamboni, L. The ultrastructural pathology of the spermatozoon as a cause of infertility: The role of electron microscopy in the evaluation of semen quality. Fertil. Steril. 1987; 48: 711–34.Google Scholar
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; 9: 405–28.CrossRefGoogle Scholar
Francavilla, S, Bianco, MA, Cordeschi, G, D'Abrizio, P, De Stefano, C, Properzi, G et al. Ultrastructural analysis of chromatin defects in testicular spermatids in azoospermic men submitted to TESE-ICSI. Hum Reprod 2001; 16: 1,440–8.Google Scholar
Baccetti, C, Collodel, G, Piomboni, P. Apoptosis in human ejaculated sperm cells. J Submicrosc Cytol Pathol 1996; 28: 587–96.Google ScholarPubMed
Muratori, M, Piomboni, P, Baldi, E, Filimberti, E, Pecchioli, P, Moretti, E et al. Functional and structural features of DNA-fragmented human sperm. J Androl 2000; 21: 903–12.Google Scholar
Alvarez Sedó, C, Lavolpe, M, Uriondo, H, Papier, S, Nodar, F et al. Nuclear vacuoles and apoptosis markers after Annexin V columns in patients with severe teratozoospermia. Fertil Steril 2011; 96: S159–60.Google Scholar
Chemes, HE, Alvarez Sedo, C. Tales of the tail and sperm head aches. Changing concepts on the prognostic significance of sperm pathologies affecting the head, neck/mid piece and tail. Asian J Androl 2012; 14: 1423.Google Scholar
Chemes, H. Phenotypes of sperm pathology: Genetic and acquired forms in infertile men. J Androl 2000; 21: 799808.CrossRefGoogle ScholarPubMed
Bartoov, B, Berkovitz, A, Eltes, F. Selection of spermatozoa with normal nuclei to improve the pregnancy rate with intracytoplasmic sperm injection. N Engl J Med 2001; 345: 1067–8.Google Scholar
Bartoov, B, Berkovitz, A, Eltes, F, Kogosovsky, A, Menezo, Y, Barak, Y. Real-time fine morphology of motile human sperm cells is associated with IVF–ICSI outcome. J Androl 2002; 23: 18.Google Scholar
Bartoov, B, Berkovitz, A, Eltes, F, Kogosovsky, A, Yagoda, A, Lederman, H. Pregnancy rates are higher with intracytoplasmic morphologically selected sperm injection than with conventional intracytoplasmic injection. Fertil Steril 2003; 80: 1413–9.CrossRefGoogle ScholarPubMed
Wu, JY, Ribar, TJ, Cummings, DE, Burton, KA, McKnight, GS, Means, AR. Spermiogenesis and exchange of basic nuclear proteins are impaired in male germ cells lacking Camk4. Nat Genet 2000; 25: 448–52.Google Scholar
Yu, YE, Zhang, Y, Unni, E, Shirley, CR, Deng, JM, Russell, LD et al. Abnormal spermatogenesis and reduced fertility in transition nuclear protein 1-deficient mice. Proc Natl Acad Sci U S A 2000; 97: 4683–8.Google Scholar
Balhorn, R, Reed, S, Tanphaichitr, N. Aberrant protamine 1/protamine 2 ratios in sperm of infertile human males. Experientia 1988; 44: 52–5.CrossRefGoogle ScholarPubMed
Blanchard, Y, Lescoat, D, Le Lannou, D. Anomalous distribution of nuclear basic proteins in round-headed human spermatozoa. Andrologia 1990; 22: 549–55.Google ScholarPubMed
deYebra, L, Ballesca, JL, Vanrell, JA, Corzett, M, Balhorn, R, Oliva, R. Detection of P2 precursors in the sperm cells of infertile patients who have reduced protamine P2 levels. Fertil Steril 1998; 69: 755–9.Google Scholar
Bench, G, Corzett, MH, De Yebra, L, Oliva, R, Balhorn, R. Protein and DNA contents in sperm from an infertile human male possessing protamine defects that vary over time. Mol Reprod Dev 1998; 50: 345–53.Google Scholar
Cho, C, Willis, WD, Goulding, EH, Jung-Ha, H, Choi, YC, Hecht, NB et al. Haploinsufficiency of protamine-1 or -2 genes causes infertility in mice. Nat Genet 2001; 28: 82–6.Google Scholar
Emery, BR, Carrell, DT. The effect of epigenetic sperm abnormalities on early embryogenesis. Asian J Androl 2006; 8: 131–42.Google Scholar
Ravel, C, Chantot-Bastaraud, S, El Houate, B, Berthaut, I, Verstraete, L, De Larouziere, V et al. Mutations in the protamine 1 gene associated with male infertility. Mol Hum Reprod 2007; 13: 461–4.Google Scholar
Gázquez, C, Oriola, J, de Mateo, S, Vidal-Taboada, JM, Ballescà, JL, Oliva, R. A common protamine 1 promoter polymorphism [-190 C->A] correlates with abnormal sperm morphology and increased protamine P1/P2 ratio in infertile patients. J Androl 2008; 29: 540–8.Google Scholar
Imken, L, Rouba, H, El Houate, B, Louanjli, N, Barakat, A, Chafik, A et al. Mutations in the protamine locus: Association with spermatogenic failure? Mol Hum Reprod 2009; 15: 733–8.Google Scholar
Venkatesh, S, Kumar, R, Deka, D, Deecaraman, M, Dada, R. Analysis of sperm nuclear protein gene polymorphisms and DNA integrity in infertile men. Syst Biol Reprod Med 2011; 57: 124–32.CrossRefGoogle ScholarPubMed
Jodar, M, Oliva, R. Protamine alterations in human spermatozoa. Adv Exp Med Biol 2014; 791: 83102.Google Scholar
Kierszenbaum, AL, Tres, LL. The acrosome–acroplaxome–manchette complex and the shaping of the spermatid head. Arch Histol Cytol 2004; 67: 271–84.Google Scholar
Holstein, AF, Schirren, C, Schirren, CG. Human spermatids and spermatozoa lacking acrosomes. J Reprod Fertil 1973; 35: 489–91.Google Scholar
Bisson, JP, David, G, Magnin, C. Etude ultrastructurale des anomalies de l´acrosome dans le spermatozoide a tete irregulière. Bull Assoc Anat [Nancy] 1975; 59: 345–6.Google Scholar
Baccetti, B, Renieri, T, Rosati, F, Selmi, MG, Casanova, S. Further observations on the morphogenesis of the round headed human spermatozoa. Andrologia 1977; 9: 255–64.Google ScholarPubMed
Nistal, M, Herruzo, A, Sanchez Corral, F. Teratozoospermia absoluta de presentación familiar: Spermatozoides microcéfalos irregulares sin acrosoma. Andrologia 1978; 10: 234–40.Google Scholar
Florke-Gerloff, S, Topfer-Petersen, E, Muller-Esterl, W, Mansouri, A, Schatz, R, Schirren, C. Biochemical and genetic investigation of round-headed spermatozoa in infertile men including two brothers and their father. Andrologia 1984; 16: 187202.Google Scholar
Alvarez Sedo, C, Rawe, VY, Chemes, HE. Acrosomal biogenesis in human globozoospermia: Immunocytochemical, ultrastructural and proteomic studies. Hum Reprod 2012; 27: 1912–21.Google Scholar
Holstein, AF. Morphologische Studien an abnormen Spermatiden und Spermatozoon des Menschen. Virchows Arch 1975; 367: 93112.Google Scholar
Anton-Lampretch, I, Kotsur, B, Schopf, E. On round headed human spermatozoa. Fertil Steril 1976; 27: 685–93.Google Scholar
Parrington, J, Swann, K, Shevchenko, VI, Sesay, AK, Lai, FA. Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature 1996; 379: 364–8.Google Scholar
Sutovsky, P, Manandhar, G, Wu, A, Oko, R. Interactions of sperm perinuclear theca with the oocyte: Implications for oocyte activation, anti-polyspermy defense and assisted reproduction. Microsc Res Tech 2003; 61: 362–78.Google Scholar
Ito, C, Yamatoya, K, Yoshida, K, Kyono, K, Yao, R, Noda, T et al. Appearance of an oocyte activation-related substance during spermatogenesis in mice and humans. Hum Reprod 2010; 25: 2734–44.Google Scholar
Bos-Mikich, A, Whittingham, DG, Jones, KT. Meiotic and mitotic Ca21 oscillations affect cell composition in resulting blastocysts. Dev Biol 1997; 182: 172–9.CrossRefGoogle Scholar
Yanagida, K, Katayose, H, Hayashi, S, Sato, A. Successful pregnancy after ICSI with strontium oocyte activation in low rates of fertilization. Reprod Biomed Online 2006; 13: 801–6.Google Scholar
Escalier, D. Failure of differentiation of the nuclear–perinuclear skeletal complex in the round-headed human spermatozoa. Int J Dev Biol 1990; 34: 287–97.Google ScholarPubMed
Oko, R, Aul, RB, Wu, A, Sutovsky, P. The sperm head cytoskeleton. In: Robaire, B, Chemes, HE, Morales, C (Eds.), Andrology in the 21st Century. Medimond Publishing Company, 2001: 3751.Google Scholar
Alvarez Sedó, C, Sutovsky, P, Oko, R, Rawe, VY, Chemes, HE. Biogenesis of the sperm perinuclear theca during human spermiogenesis. Fertil Steril 2009; 92: 1472–3.CrossRefGoogle ScholarPubMed
Nomikos, M, Sanders, JR, Parthimos, D, Buntwal, L, Calver, BL, Stamatiadis, P, et al. Essential role of the EF-hand domain in targeting sperm phospholipase Cζ to membrane PIP2. J Biol Chem 2015 Oct 1. pii: jbc.M115.658443. [Epub ahead of print]Google Scholar
Yeste, M, Jones, C, Amdani, SN, Patel, S, Coward, K. Oocyte activation deficiency: A role for an oocyte contribution? Hum Reprod Update 2015 Sep 7. pii: dmv040. [Epub ahead of print].Google Scholar
Baccetti, B, Capitani, S, Collodel, G, Di Cairano, G, Gambera, L, Moretti, E et al. Genetic sperm defects and consanguinity. Hum Reprod 2001; 16: 1365–71.Google Scholar
Koscinski, I, Elinati, E, Fossard, C, Redin, C, Muller, J, Velez de la Calle, J et al. DPY19L2 deletion as a major cause of globozoospermia. Am J Hum Genet 2011; 88: 344–50.Google Scholar
Harbuz, R, Zouari, R, Pierre, V, Ben Khelifa, M, Kharouf, M, Coutton, C et al. A recurrent deletion of DPY19L2 causes infertility in man by blocking sperm head elongation and acrosome formation. Am J Hum Genet 2011; 88: 351–61.Google Scholar
Escoffier, J, Yassine, S, Lee, HC, Martinez, G, Delaroche, J, Coutton, C et al. Subcellular localization of phospholipase Cζ in human sperm and its absence in DPY19L2-deficient sperm are consistent with its role in oocyte activation. Mol Hum Reprod 2015; 21: 157–68.Google Scholar
Yassine, S, Escoffier, J, Martinez, G, Coutton, C, Karaouzène, T, Zouari, R et al. Dpy19l2-deficient globozoospermic sperm display altered genome packaging and DNA damage that compromises the initiation of embryo development. Mol Hum Reprod 2015; 21: 169–85.CrossRefGoogle ScholarPubMed
Fawcett, DW, Phillips, DM. The fine structure and development of the neck region of the mammalian spermatozoon. Anat Rec 1969; 165: 153–84.CrossRefGoogle ScholarPubMed
Liska, F, Gosele, C, Rivkin, E, Tres, L, Cardoso, MC, Domaing, P et al. Rat hd mutation reveals an essential role of centrobin in spermatid head shaping and assembly of the head-tail coupling apparatus. Biol Reprod 2009; 81: 1196205.Google Scholar
Zaneveld, LJD, Polakoski, KL. Collection and physical examination of the ejaculate. In Hafez, ESE (Ed.), Techniques of Human Andrology. Elsevier North Holland Biomedical Press, 1977: 147–72.Google Scholar
LeLannou, D. Teratozoospermie consistant en l'absence de tete spermatique par defaut de conexion. J Gynecol Obstet Biol Reprod [Paris] 1979; 8: 43–5.Google Scholar
Perotti, ME, Giarola, A, Gioria, M. Ultrastructural study of the decapitated sperm defect in an infertile man. J Reprod Fertil 1981; 63: 543–49.Google Scholar
Perotti, ME, Gioria, M. Fine structure and morphogenesis of “headless” human spermatozoa associated with infertility. Cell Biol Int Rep 1981; 5: 113.Google Scholar
Baccetti, B, Selmi, MG, Soldani, P. Morphogenesis of “decapitated spermatozoa” in a man. J Reprod Fertil 1984; 70: 395–7.Google Scholar
Chemes, HE, Carizza, C, Scarinci, F, Brugo Olmedo, S, Neuspiller, N, Schwarsztein, L. Lack of a head in human spermatozoa from sterile patients: a syndrome associated with impaired fertilization. Fertil Steril 1987; 47: 310–6.CrossRefGoogle ScholarPubMed
Baccetti, B, Burrini, A.G, Collodel, G, Magnano, AR, Piomboni, P, Renieri, T et al. Morphogenesis of the decapitated and decaudated sperm defect in two brothers. Gamete Res 1989; 23: 181–8.Google Scholar
Holstein, A.F., Schill, W.B., Breucker, H. Dissociated centriole development as a cause of spermatid malformation in a man. J Reprod Fert 1986; 78: 719–25.Google Scholar
Chemes, HE, Puigdomenech, ET, Carizza, C, Brugo Olmedo, S, 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.Google Scholar
Rawe, VY, Terada, Y, Nakamura, S, Chillik, C, Brugo Olmedo, S, Chemes, HE. A pathology of the sperm centriole responsible for defective sperm aster formation, syngamy and cleavage. Hum Reprod 2002; 17: 2344–9.Google Scholar
Porcu, G, Mercier, G, Boyer, P, Achard, V, Banet, J, Vasserot, M et al. Pregnancies after ICSI using sperm with abnormal head-tail junction from two brothers: Case report. Hum Reprod 2003; 18: 562–7.Google Scholar
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.Google ScholarPubMed
Mendoza-Lujambio, I., Burfeind, P., Dixkens, C., Meinhardt, A., Hoyer-Fender, S., Engel, W et al. The Hook1 gene is non-functional in the abnormal spermatozoon head shape [azh] mutant mouse. Hum Mol Genet 2002; 11: 1647–58.Google Scholar
Yang, K, Grzmil, P, Meinhardt, A, Hoyer-Fender, S. Haplo-deficiency of ODF1/HSPB10 in mouse sperm causes relaxation of head-to-tail linkage. Reproduction 2014; 148: 499506.Google Scholar
Yuan, S, Stratton, CJ, Bao, J, Zheng, H, Bhetwal, BP, Yanagimachi, R et al. Spata6 is required for normal assembly of the sperm connecting piece and tight head-tail conjunction. Proc Natl Acad Sci USA 2015; 112: E430–9.Google Scholar
Saias-Magnan, J, Metzler-Guillemain, C, Mercier, G, Carles-Marcorelles, F, Grillo, JM, Guichaoua, MR. Failure of pregnancy after intracytoplasmic sperm injection with decapitated spermatozoa: Case report. Hum Reprod 1999; 14: 1989–92.Google Scholar
Rawe, VY, Díaz, ES, Abdelmassih, R, Wójcik, C, Morales, P, Sutovsky, P et al. The role of sperm proteasomes during sperm aster formation and early zygote development: Implications for fertilization failure in humans. Hum Reprod 2008; 23: 573–80.Google Scholar
Terada, Y, Schatten, G, Hasegawa, H, Yaegashi, N. Essential roles of the sperm centrosome in human fertilization: Developing the therapy for fertilization failure due to sperm centrosomal dysfunction. Tohoku J Exp Med 2010; 220: 247–58.CrossRefGoogle ScholarPubMed
Wójcik, C, Benchaib, M, Lornage, J, Czyba, JC, Guerin, JF. Proteasomes in human spermatozoa. Int J Androl 2000; 23: 169–77.Google Scholar
Morales, P, Diaz, ES, Pizarro, E, Rawe, VY, Chemes, HE. Decreased proteasome enzymatic activity in sperm from patients with genetic abnormalities of the head–tail junction and acephalic spermatozoa. J Androl March–April 2004 [suppl], 41.Google Scholar
Emery, BR, Thorp, C, Malo, JW, Carrell, DT. Pregnancy from intracytoplasmic sperm injection of a sperm head and detached tail. Fertil Steril 2004; 81: 686–8.Google Scholar
Gambera, L, Falcone, P, Mencaglia, L, Collodel, G, Serafini, F, De Leo, V et al. Intracytoplasmic sperm injection and pregnancy with decapitated sperm. Fertil Steril 2010; 93: e712.Google Scholar
Oko, R, Clermont, Y. Light microscopic immunocytochemical study of fibrous sheath and outer dense fiber formation in the rat spermatid. Anat Rec 1989; 225: 4655.Google Scholar
Sauvalle, A, Le Bris, C, Izard, J. Supernumerary microtubules and prolongation of the middle piece in two infertile patients. Int J Fertil 1983; 28: 173–6.Google ScholarPubMed
Wilton, LJ, Temple-Smith, PD, de Kretser, DM. Quantitative ultrastructural analysis of sperm tails reveals flagellar defects associated with persistent asthenozoospermia. Hum Reprod 1992; 7: 510–6.CrossRefGoogle ScholarPubMed
Folgero, T, Bertheussen, K, Lindal, S, Torbergsen, T, Oian, P. Mitochondrial disease and reduced sperm motility. Hum Reprod 1993; 11: 1863–8.Google Scholar
Mundy, AJ, Ryder, TA, Edmonds, DK. Asthenozoospermia and the human sperm mid piece. Hum Reprod 1995; 10: 116–9.Google Scholar
Rawe, VY, Hermes, R, Nodar, FN, Fiszbajn, G, Chemes, HE. Results of intracytoplasmic sperm injection in two infertile patients with abnormal organization of sperm mitochondrial sheaths and severe astheno-teratozoospermia. Fertil Steril 2007; 88: 649–53.Google Scholar
Holyoake, AJ, McHugh, P, Wu, M, O'Carroll, S, Benny, P, Sin, IL, et al. High incidence of single nucleotide substitutions in the mitochondrial genome is associated with poor semen parameters in men. Int J Androl 2001; 243: 175–82.Google Scholar
Thangaraj, K, Joshi, MB, Reddy, AG, Rasalkar, AA, Singh, L. Sperm mitochondrial mutations as a cause of low sperm motility. J Androl 2003; 24: 388–92.Google Scholar
Chemes, H, Brugo Olmedo, S, Zanchetti, F, Carrere, C, Lavieri, JC. Dysplasia of the fibrous sheath. An ultrastructural defect of human spermatozoa associated with sperm immotility and primary sterility. Fertil Steril 1987; 48: 664–9.Google Scholar
Chemes, H, Brugo Olmedo, SB, Carrere, C, Oses, R, Carizza, C. Ultrastructural pathologyof the sperm flagellum. Association between flagellar pathology and fertility prognosisin severely asthenozoospermic men. Hum Reprod 1998; 13: 2521–6.Google Scholar
Escalier, D, David, G. Pathology of the cytoskeleton of the human sperm flagellum: axonemal and peri-axonemal anomalies. Biol Cell 1984; 50: 3752.Google Scholar
Ben Khelifa, M, Coutton, C, Zouari, R, Karaouzène, T, Rendu, J, Bidart, M et al. Mutations in DNAH1, which encodes an inner arm heavy chain dynein, lead to male infertility from multiple morphological abnormalities of the sperm flagella. Am J Hum Genet 2014; 94: 95104.Google Scholar
Coutton, C, Escoffier, J, Martinez, G, Arnoult, C, Ray, PF. Teratozoospermia: Spotlight on the main genetic actors in the human. Hum Reprod Update 2015; 21: 455–85.Google Scholar
Chemes, HE. The significance of flagellar pathology in the evaluation of abnormal sperm motility. In: Baccetti, B (Ed.), Comparative Spermatology 20 Years After (Serono Symposia Publications from Raven Press), Vol. 75. Raven Press, 1991: 815–9.Google Scholar
Ross, A, Christie, S, Edmond, P. Ultrastructural tail defects in the spermatozoa from two men attending a subfertility clinic. J Reprod Fertil 1973; 32: 243–51.Google Scholar
Afzelius, BA, Eliasson, R, Johnsen, O, Lindholmer, C. Lack of dynein arms in immotile human spermatozoa. J Cell Biol 1975; 66: 225–32.Google Scholar
Pedersen, H, Rebbe, H. Absence of arms in the axoneme of immotile human spermatozoa. Biol Reprod 1975; 12: 541–4.Google Scholar
Rossman, CM, Forrest, JB, Less, RM, Newhouse, AF, Newhouse, MT. The dyskinetic cilia syndrome: Abnormal ciliary motility in association with abnormal ciliary ultrastructure. Chest 1981; 80: 860–5.Google Scholar
Pennarun, G, Escudier, E, Chapelin, C, Bridoux, AM, Cacheux, V, Roger, G et al. Loss-of-function mutations in a human gene related to Chlamydomonas reinhardtii dynein IC78 result in primary ciliary dyskinesia. Am J Hum Genet 1999; 65: 1508–19.Google Scholar
Blouin, JL, Meeks, M, Radhakrishna, U, Sainsbury, A, Gehring, C, Sail, GD et al. Primary ciliary dyskinesia: A genome-wide linkage analysis reveals extensive locus heterogeneity. Eur J Hum Genet 2000; 8: 109–18.Google Scholar
Bartoloni, L, Blouin, JL, Pan, Y, Gehrig, C, Maiti, AK, Scamuffa, N et al. Mutations in the DNAH11 (axonemal heavy chain dynein type 11) gene cause one form of situs inversus totalis and most likely primary ciliary dyskinesia. Proc Natl Acad Sci USA 2002; 99: 10282–6.Google Scholar
Olbrich, H, Haffner, K, Kispert, A, Volkel, A, Volz, A, Sasmaz, G et al. Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left–right asymmetry. Nat Genet 2002; 30: 143–4.Google Scholar
Ibanez-Tallon, I, Gorokhova, S, Heintz, N. Loss of function of axonemal dynein Mdnah5 causes primary ciliary dyskinesia and hydrocephalus. Hum Mol Genet 2002; 11: 715–21.Google Scholar
Sapiro, R, Kostetskii, I, Olds-Clarke, P, Gerton, GL, Radice, GL, Strauss, JF. Male infertility, impaired sperm motility, and hydrocephalus in mice deficient in sperm-associated antigen 6. Mol Cell Biol 2002; 22: 6298305.Google Scholar
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.Google Scholar
Turner, RM, Musse, MP, Mandal, A, Klotz, K, Javes, FC, Herr, JC et al. Molecular genetic analysis of two human sperm fibrous sheath proteins, AKAP4 and AKAP3, in men with dysplasia of the fibrous sheath. J Androl 2001; 22: 302–15.Google Scholar
Baccetti, B, Collodel, G, Estenoz, M, Manca, D, Moretti, E, Piomboni, P. Gene deletions in an infertile man with sperm fibrous sheath dysplasia. Hum Reprod 2005; 20: 2790–4.Google Scholar
Duriez, B, Duquesnoy, P, Escudier, E, Bridoux, AM, Escalier, D, Rayet, I et al. A common variant in combination with a nonsense mutation in a member of the thioredoxin family causes primary ciliary dyskinesia. Proc Natl Acad Sci USA 2007; 27: 3336–41.Google Scholar
Neugebauer, DC, Neuwinger, J, Jockenhövel, F, Nieschlag, E. ‘9 + 0' axoneme in spermatozoa and some nasal cilia of a patient with totally immotile spermatozoa associated with thickened sheath and short midpiece. Hum Reprod 1990; 5: 981–6.CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×